Embed Size (px)
Citation preview
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 17
Clinical Study The Morbidity of Reoperative Surgery for RecurrentBenign Nodular Goitre Impact of Previous UnilateralThyroid Lobectomy versus Subtotal Thyroidectomy
Navin Rudolph Claudia Dominguez Anthony Beaulieu
Pierre De Wailly and Jean-Louis Kraimps
Department of Endocrine Surgery University Hospital of Poitiers 983096983094983088983090983089 Poitiers France
Correspondence should be addressed to Navin Rudolph navinrudolphgmailcom
Received 983096 June 983090983088983089983091 Revised 983090983090 September 983090983088983089983091 Accepted 983090983088 October 983090983088983089983091 Published 983089983097 January 983090983088983089983092
Academic Editor Tomas J Fahey
Copyright copy 983090983088983089983092 Navin Rudolph et al Tis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
Background Subtotal thyroidectomy (S) was previously considered the gold standard in the surgical management o multinodular goitre despite its propensity or recurrence Our aim was to assess whether prior S or unilateral lobectomy was associated with increased reoperative morbidity Methods A retrospective analysis was conducted extracting data rom ourendocrine surgical database or the period rom January 983089983097983097983089 to June 983090983088983088983094 wo patient groups were de1047297ned Group 983089 consistedo patients with previous unilateral thyroid lobectomy Group 983090 had undergone previous S Speci1047297c outcomes investigated were
transient and permanent recurrent laryngeal nerve (RLN) injury and hypoparathyroidism Results 983092983097983092 reoperative cases wereperormed which consisted o 983090983093983097 patients with previous unilateral lobectomy (Group 983089) and 983090983091983093 patients with previous subtotalthyroidectomy (Group 983090) A statistically signi1047297cant increase relating to previous S was demonstrated in both permanent RLNinjury (983088983095983095 versus983091983092 RR 983092983091983096 = 0038) and permanenthypoparathyroidism(983089983093 versus 983093983089RR 983091983089983092 = 0041) ransientnerve injury and hypocalcaemia incidence was comparable Conclusions Reoperative surgery ollowing subtotal thyroidectomy is associated with a signi1047297cantly increased risk o permanent recurrent laryngeal nerve injury and hypoparathyroidism whencompared with previous unilateral thyroidectomy Subtotal thyroidectomy should thereore no longer be recommended in themanagement o multinodular goitre
1 Background
Subtotal thyroidectomy (S) was or many years theaccepted standard o management or benign multinodular
goitre Although its role has signi1047297cantly diminished with therecognition o the saety o total thyroidectomy it continuesto be practised in several centres worldwide both in locationsendemic and nonendemic or this disease Te purportedbene1047297ts o the subtotal approach include a reduced morbidity pro1047297le with respect to recurrent laryngeal (RLN) injury andhypoparathyroidism as well as a reduced need or thyroidhormone replacement therapy Te exact deployment o the surgical technique has varied amongst institutions withregard to the size and location o the thyroid remnant andwhether it has been perormed unilaterally or bilaterally Tismarked potential or heterogeneity has hampered reliablescienti1047297c appraisal o the techniquersquos efficacy
Despite these methodological encumbrances severalconcerns regarding S have emerged that challenge itslegitimacy within the surgical armamentarium o the thyroid
surgeon First recurrent disease ofen maniesting many years ollowing the initial surgery is identi1047297ed in a signi1047297cantnumber o patients [983089] Moreover thyroid insufficiency andconsequent need or thyroid hormone replacement therapy are only inrequently eradicated [983090] Te presence o athyroid remnant is problematic i an incidental malignancy is discovered Finally the identi1047297cation o recurrent diseaseheralds technically demanding reoperative surgery raughtwith potential or signi1047297cant morbidity
Alongside this total thyroidectomy () has beendemonstrated to be a sae and efficacious procedure ech-nological advancements in haemostatic vessel sealing deviceshave hastened the operative technique signi1047297cantly and more
Hindawi Publishing CorporationJournal of yroid ResearchVolume 2014 Article ID 231857 6 pageshttpdxdoiorg1011552014231857
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 27
983090 Journal o Tyroid Research
recently nerve monitoring has been widely adopted to urthercombat the low rates o RLN paralysis already demonstratedOther bene1047297ts relate to its superiority in cases o malignancy by removing all gross thyroid and potentially malignanttissue acilitating radioactive iodine (RAI) ablation therapy and acilitating surveillance with ultrasound imaging o the
thyroid bed and thyroglobulin (g) monitoringOur unit is a high volume tertiary endocrine surgery centre perorming over 983093983088983088 thyroid procedures per yearHaving previously practiced S or many years we have a
vast experience with recurrent benign thyroid goitre ollow-ing this procedure In addition a large number o patientswho underwent unilateral thyroid lobectomy or unilateralbenign nodular disease have subsequently required comple-tion totalization thyroidectomy or contralateral recurrentdisease Our unique study approach endeavoured to assesswhether reoperative surgery in these two settings conerredany difference in morbidity speci1047297cally with regard to RLNinjury and hypoparathyroidism
2 Materials and Methods
A retrospective analysis was conducted utilizing our endo-crine surgical database or the period rom January 983089983097983097983089 toJune 983090983088983088983094 Tere were 983092983097983092 patients that required reoperationor recurrent benign goitre and were thus selected or thisstudy Te indications or the reoperative surgery includedenlarging neck lump pressure symptoms and imaging sus-picious or malignancy Te patients were divided into twogroups on the basis o the previous surgery group 983089 consistedo patients who had previous unilateral thyroid lobectomygroup 983090 included patients who had undergone prior subtotalthyroidectomy In all cases both the initial and reoperativeprocedure had been perormed at our own institution
Te technique o unilateral extracapsular thyroidectomy at our institution has been well documented previously [983091]Our subtotal thyroidectomy procedure perormed duringthis period is detailed here to avoid potential ambiguityCareul preoperative study o the thyroid ultrasound wasparamount in order to appreciate the location o the noduleswithin each thyroid lobe A small (less than 983093 grams)homogeneous remnant was lef unilaterally at either thesuperior pole or posteriorly depending on the location o the sonographically or intraoperatively detected nodulesTis combination o unilateral lobectomy and unilateral
subtotal resection has been labelled elsewhere as the Dunhillprocedure [983092] Te operations were all perormed by orunder the direct supervision o a senior endocrine surgeon(JLK) ollowing a highly standardized procedure Postop-erative nonsuppressive thyroxine therapy was employed orrestoration o euthyroidism as dictated by thyroid unctiontests (thyroid-stimulating hormone (SH) ree 983092 and 983091)
Prior to reoperative surgery all patients underwent imag-ing by ultrasound computed tomography scans and tech-netium thyroid uptake scans were perormed on an individu-alized basis depending on the extent o the recurrence Intra-operative nerve monitoring was used in all reoperative casesFibreoptic 1047298exible laryngoscopy was routinely perormed in
983137983138983148983141 983089 Group demographics and timingand indication or reoper-ation
Group 9830891038389 = 259
Group 9830901038389 = 235
Sex
Male 983090983089 (983096) 983090983088 (983097)
Female 983090983091983096 (983097983090) 983090983089983093 (983097983089)
Age
Age at 1047297rst operation 983091983096983088 years 983092983088983088 years
Age at reoperation 983093983091983090 years 983093983091983097 years
Interval between initial andreoperative surgery
983089983093983090 years 983089983091983097 years
Indication or reoperation
Isolated nodule 983091983096 (983089983092983095) 983091983094 (983089983093983091)
Multinodular goitre 983090983090983089 (983096983093983091) 983089983097983097 (983096983092983095)
all patients both preoperatively and on the 1047297rst postoperativeday permitting an accurate calculation o our temporary RLN injury rate Patients with any detected abnormalitiesat this examination underwent a urther laryngoscopy at 983094months postoperatively vocal cord dysunction at this stagewas de1047297ned as permanent RLN injury Calcium levels wereobtained on the 1047297rst and second postoperative days andat a 983094-month ollowup appointment Hypocalcaemia wasde1047297ned as less than 983090983088983088 mmolL and permanent i requiringongoing oral calcium supplementation beyond 983091 monthsMorbidity arising rom the initial operation was not theintended ocus o this study and was excluded rom theanalysisonly new morbidity events speci1047297cally relating to the
reoperative surgery were included Descriptive statistics wereobtained and data subjected to analysis by Fisherrsquos exact testand chi-square test to examine the relative risk o reoperativemorbidity or group 983089 and group 983090 Statistical signi1047297cance wasaccepted at lt 005
3 Results
During the study period our unit perormed thyroid surgery on 983094983095983096983088 patients Tere were 983092983097983092 patients that required reop-eration or recurrent benign goitre which constituted 983095983091 o the unitrsquos thyroid surgery throughput during this period
Group 983089 comprised 983090983093983097 patients with previous thyroid
lobectomy and group 983090 comprised 983090983091983093 patients with previoussubtotal thyroidectomy (able 983089) Te groups displayed dem-ographic parity with respect to mean age (group 983089 983091983096 yearsgroup 983090 983092983088 years) and emale predominance (983097983090 and 983097983089resp)
Te mean interval between initial surgery and reoper-ation was 983089983093983090 years in group 983089 and 983089983091983097 years in group 983090Te indication or reoperation in groups 983089 and 983090 was alsocomparable isolated nodules in 983089983092983095 and 983089983093983091 and multi-nodular goitre in 983096983093983091 and 983096983092983095 respectively
Te impact o the initial surgery on the morbidity relatedto the reoperative case was statistically signi1047297cant or bothpermanent RLN injury and permanent hypocalcaemia
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 37
Journal o Tyroid Research 983091
983137983138983148983141 983090 Incidence o RLN injury ollowing reoperative surgery
Group 983089 (lobectomy)1038389 = 259
Group 983090 (subtotal)1038389 = 235
value Relative risk
Normal laryngoscopy 983090983092983089 (983096983091983097) 983090983089983092 (983096983091983092)
ransient RLN paralysis 983089983094 (983094983089983096) 983089983091 (983093983093983091) 983088983096983093 983088983097983090
Permanent RLN paralysis 983090 (983088983095983095) 983096 (983091983092) 983088983088983091983096 983092983091983096
983137983138983148983141 983091 Incidence o hypocalcaemia ollowing reoperative surgery
Group 983089 (lobectomy)1038389 = 259
Group 983090 (subtotal)1038389 = 235
value Relative risk
Normocalcaemia 983090983090983088 (983096983092983097) 983090983088983090 (983096983093983097)
emporary hypocalcaemia 983091983093 (983089983091983093) 983090983089 (983096983097983091) 983088983089983093 983088983094983097
Permanent hypocalcaemia 983092 (983089983093983092) 983089983090 (983093983089) 983088983088983092983089 983091983089983092
Permanent RLN palsy was observed in only 983090 romgroup 983089 and 983096 rom group 983090 (able 983090) Tis correlates with
a statistically signi1047297cant detrimental effect o initial subtotalthyroidectomy on long-term RLN unction ( lt 0038)Tis indicates a relative risk increase o 983092983091983096 in patients whounderwent initial subtotal thyroidectomy (CI
95 983088983097983092ndash983090983088983092)
ransient paralysis was observed in both groups (group 983089983094983089983096 group 983090 983093983093983091) Te majority o patients in bothgroups however have no disturbance in postoperative RLNunction (group 983089 983096983091983097 group 983090 983096983091983092)
Permanent hypocalcaemia was observed in 983089983093983092 o group 983089 patients and 983093983089983089 o group 983090 patients (able 983091)Again this re1047298ected a statistically signi1047297cant detrimentaleffect o initial subtotal thyroidectomy on the developmento permanent hypocalcaemia ollowing reoperative surgery
( lt 0041
) and correlates with an relative risk increase o 983091983089983092 (CI95
983089983088983097ndash983097983093983097) No association was determined or tem-porary hypocalcaemia and the nature o prior surgery (RR 983088983094983097 CI
95 983088983092983089ndash983089983089983092) O note postoperative normocalcaemia
was evident in 983096983092983097 and 983096983093983097 o patients rom group 983089 andgroup 983090 respectively
Incidental malignancy within the reoperative specimenwasdetermined in 983090983089 patients (983092983090983090) Tere wasan equitabledistribution within the two groups with 983089983089 cases in group 983089and 983089983088 cases in group 983090
4 Discussion
Te optimum extent o initial surgery in the managemento benign thyroid goitre continues to generate considerablecontroversy Te debate between the saety and efficacy o a total versus a less than total thyroidectomy has suc-cessully accomplished the widespread adoption o totalthyroidectomy although not ully extinguishing the practiceo subtotal thyroidectomy in several centres worldwide Ourstudy drawing on a vast experience with reoperative surgery in benign thyroid disease approaches the debate rom adifferent angle Rather than ocussing on the morbidity o aninitial subtotal thyroidectomy versus an extracapsular tech-nique our study represents the 1047297rst direct comparison on themorbidity relating to the reoperative surgery in the setting o
previous subtotal and unilateral thyroid resections Althoughthe results may appear intuitive the study did expose some
interesting and important acets o reoperative surgery inthese circumstances
Reoperative thyroid surgery is inherently difficult onaccount o the distortion o central neck area anatomy and1047297brotic encasement o important structures such as therecurrent laryngeal nerve [983093] Tis has led to the recommen-dation by several authors to avoidreoperations by perormingde1047297nitive initial treatment [983094] Despite these difficultiesLevin et al demonstrated that reoperations could still beperormed with minimal morbidity [983095] In their series a low permanent RLN injury rate o less than 983089 and permanenthypoparathyroidism rate o 983091983096 was attainedmdashthe authorsconsequently stressed that or patients maniesting with
recurrent disease reoperative surgery should not be withheldor ear o generating the aorementioned complications Ourrates o permanent RLN palsy (983090) and hypoparathyroidism(983091983090) rom the two groups combined likewise demonstratethat satisactory outcomes are achievable within specializedcentres Other authors have published series o reoperativecases with permanent RLN rates o 983088ndash983089983093 and highlightedthat although being hardly an innocuous procedure reop-erative surgery is sae in the hands o experienced surgeonshowever a complete initial procedure should obviate theexposure to this unnecessary additional risk [983096 983097]
A different scenario exists when a patient requires sec-ondary thyroid surgery or recurrent benign disease with a
background o unilateral hemithyroidectomy In this situa-tion where the contralateral side is completely untouchedno increased risk is conerred as shown by Chao et aland con1047297rmed in our study with rates o permanent RLNinjury and permanent hypoparathyroidism rates o 983088983095983095and983089983093983092 respectively [983089983088] However previous S in whichboth sides have been dissected is associated with an up to1047297veold increase in complications with reoperative surgery [983089983089 983089983090] Despite the scar tissue and degenerative changescited by Katz and Bronson as the principle culprit actorsrelating to reoperative morbidity [983089983091] Bron and OrsquoBrienound no signi1047297cant correlation between complication rateandprevioussurgery [983089983092] ransient hypoparathyroidism was
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 47
983092 Journal o Tyroid Research
seen in 983089983091983093 o group 983089 patients in our study representing anonstatistically signi1047297cant difference rom the previous Sgroup Germane to this 1047297nding Barczynski et al remark that transient hypoparathyroidism ollowing in an erawhere parathyroid autotransplantation is common should be
viewed as a sequel rather than a complication [983089983093]
Te technique o reoperative thyroid surgery is clearly important when analysing complications Farrag and col-leagues have recently promulgated an algorithm or sae andeffective thyroid bed surgery or malignancy although many aspects can be readily extrapolated to the benign sphereas well [983093] Te principle tenets o the algorithm includepreoperative high-resolution ultrasound examination pre-operative vocal old examination by 1047297breoptic laryngoscopyand routine nerve identi1047297cation that should be acilitatedby the use o intraoperative nerve monitoring (IONM)Several o these attributes are endorsed by internationalthyroid surgery guidelines [983089983094] Additionally Menegaux etal recommend a lateral approach to the thyroid bed withdivision o the inrahyoid musculature in an effort to avoid1047297brous tissue surrounding the thyroid remnant [983089983095]
emerged as an alternativeto S initially in the malig-nant domain Clark embraced the technique or managemento well-differentiated thyroid cancer and demonstrated thesaety o the technique and low complication rate [983089983096] It isrecommended as the operation o choice in all current treat-ment guidelines or thyroid cancer [983089983097] Te purported ben-e1047297ts o a total gland resection in thyroid cancer include theremoval o the primary tumour elimination o any potentialcontralateral disease and acilitation o postoperative RAIablation g surveillance and ultrasound scanning o thethyroid bed [983090983088] Tese bene1047297ts are not present when dealingwith benign disease Proponents o a subtotal resection claima reduced rate o RLN injury and hypoparathyroidism andassert that the majority o thyroid malignancies detectedortuitously on 1047297nal histopathology are o limited clinicalsigni1047297cance Furthermore i recurrences do occur they canbe managed surgically when indicated with less morbidity than i total thyroidectomy was perormed on all cases o thyroid malignancy at the outset [983090983088]
Numerous publications have since established the low morbidity o the extracapsular procedure Mishra et aldemonstrated an 983088983096 permanent RLN rate and 983089983094 per-manent hypoparathyroidism rate whilst Muller et al ounda 983088983097 rate or both morbidities [983090983089 983090983090] Many other studiescon1047297rmed similar 1047297ndings [983090983091ndash983090983093] Serpell and Phan ound a
permanent RLN palsy rate o 983088983091 and hypoparathyroidismrate o 983089983096 and concluded that can be perormed saely in a standard endocrine surgical unit with low complicationrates matching world centres o excellence [983090983094] Documentedhigh rates o incidental thyroid malignancy orti1047297ed thegrowing argument in avour o total thyroidectomy Ourpresent study revealed an incidental papillary microcarci-noma rate o 983092983090983090 that was equally distributed within thetwo groups We have previously published a 983091 rate o occult carcinoma somewhat lower than other subsequently published series rom Bron and OrsquoBrien (983092983094) [983089983092] Colak et al (983095983092) [983090983095] and Levin et al (983090983090) [983095] Menegauxet al determined that thyroid cancer might be ound in
approximately 983089983088 o reoperative cases or recurrent goitreeven though the preceding operation was perormed orbenign disease [983090983096] By the same token ezelman et al oundthat within a cohort o patients diagnosed with thyroid cancerollowing a subtotal thyroidectomy completion resection o the thyroid remnants yielded papillary microcarcinoma in
983093983090983094 [983089]Recurrence o goitre and ailure to prevent hypothy-
roidism have urther weakened the validity o subtotal thy-roidectomy as a surgical strategy or benign thyroid diseaseGoitre recurrence rates associated with S range rom983095983089 to 983092983091 [983089 983089983090] Te incidence o recurrence appearsdirectly related to the length o surveillance [983090983097 983091983088]mdashalthough our study and others have ound that a peak incidence o recurrence occurs at approximately 983089983091 to 983089983093 yearsrom the primary operation [983091983089] a 983092983091 recurrence rate may be observed with up to 983091983088 years o ollowup [ 983089983090] Many have noted the ailure o thyroxine suppression to preventrecurrence with a 983089983092983093 recurrence rate demonstrated in
the study by Pappalardo et al in spite o drug prophylaxis[983090983092] Conversely thyroxine replacement is not obviated in983091983094983094ndash983092983095983096 o subtotal thyroidectomy procedures and henceshould not be used to justiy practice o the procedure [983091983090]
Te undamental difficulty with S is allotting a tissueremnant unaffected by the nodular process Colak et alhighlighted the predicament o leaving healthy tissue intactin patients with huge goitres where the nodular diseaseofen reaches the dorsal capsule [983090983095] Tere is generally anincreasing recognition that the nodular transormations inmultinodular goitre inherently encompass the entire glandhence although S permits a reduction in the bulk o dis-ease it is not an optimal treatment [983091983091] Moreover the rem-
nant posterolateral tissue ofen extends into the retrotrachealand retrooesophageal areas where recurrence portends early pressure symptoms that may require technically demandingreoperative surgery [983091983092] We have previously shown thatmultinodular goitre is a highly signi1047297cant risk actor orrecurrence in benign thyroid disease where a less than totalthyroidectomy has been perormed [983091983093] Recently a novelstudy by ekin et al demonstrated that Ki-983094983095 prolierationmarker levels in remnant S thyroid tissue were signi1047297-cantly higher than in normal thyroid tissue [983091983094] Tey oundthat despite the relatively small size o remnant micronodulesthe high Ki-983094983095 levels re1047298ect high cellular mitotic activity and ensuing signi1047297cant goitrogenic potential o remnant
tissue Furthermore the existence o micronodules in theremnant specimens harbouring similar prolieration index
values as the main thyroid specimen establishes the homoge-neous nature o the parenchymal alteration in multinodulargoitre Gerard et al postulate that recurrent goitres resistantto thyroxine suppression may arise due to the polyclonalnature o nodule ormation involving goitrogenic insulin-likegrowth actors and their binding proteins Tese may occurseparate to iodine de1047297ciency related mechanisms o goitredevelopment based on SH and vascular-endothelial growthactor (VEGF) angiogenesis [983091983095]
Finally the ofen-overlooked denominator and perhapsmost crucial determinant o morbidity is surgical technique
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 57
Journal o Tyroid Research 983093
Tomusch et al commented on the importance o ldquowell-trained surgeons using an appropriate intraoperative tech-niquerdquo in the perormance o total thyroidectomy [983091983096] Teability to perorm a sae total thyroidectomy is clearly adirect derivative o onersquos surgical training and experience[983091983097] Te evolution o more dedicated endocrine surgery
training programmes and specialized units combined withtechnological re1047297nements such as IONM is likely to urtherenhance the sae implementation o or both malignantand benign thyroid disease alike [983092983088]
5 Conclusion
Reoperative surgery or recurrent benign thyroid disease isassociated with increased morbidity when preceded by initialsubtotal thyroidectomy Associated high levels o recurrenceand increased permanent RLN injury and hypoparathy-roidism rates seen in this setting call or the abandonmento this procedure in avour o total thyroidectomy It should
be noted however that successul reoperative thyroid surgery perormed by experienced well-trained surgeons may beaccomplished with low overall rates o morbidity
Conflict of Interests
Te authors disclose no real or potential con1047298ict o interests
References
[983089] S ezelman I Borucu Y Senyurek F unca and erziogluldquoTe change in surgical practice rom subtotal to near-total ortotal thyroidectomy in the treatment o patients with benign
multinodular goiterrdquo World Journal of Surgery vol983091983091no 983091pp983092983088983088ndash983092983088983093 983090983088983088983097
[983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091] ldquoechnique o thyroidectomyrdquo in Endocrine Surgery Principlesand Practice H Gibelin Desurmont J L Kraimps and J GH Hubbard Eds Springer SpecialistSurgery Series chapter 983089983090pp 983089983094983091ndash983089983095983089 Springer London UK 983089st edition 983090983088983088983097
[983092] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092
no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983093] Y Farrag N Agrawal S Sheth et al ldquoAlgorithm or saeand effective reoperative thyroid bed surgery or recurrentpersistent papillary thyroid carcinomardquo Head and Neck vol 983090983097no 983089983090 pp 983089983088983094983097ndash983089983088983095983092 983090983088983088983095
[983094] D B Wilson E D Staren and R A Prinz ldquoTyroid reopera-tions indications and risksrdquo Te American Surgeon vol 983094983092 no983095 pp 983094983095983092ndash983094983095983097 983089983097983097983096
[983095] K E Levin A H Clark Q Duh M Demeure A E Sipersteinand O H Clark ldquoReoperative thyroid surgeryrdquo Surgery vol 983089983089983089no 983094 pp 983094983088983092ndash983094983088983097 983089983097983097983090
[983096] D J erris S S Khichi S K Anderson and M W SeybtldquoReoperative thyroidectomy or benignthyroiddisease the case
or phasing out subtotal thyroidectomyrdquo Laryngoscope vol 983089983089983097no 983089 p S983096983097 983090983088983088983097
[983097] J H Leevre C resallet L Leenhardt C Jublanc J Chigotand F Menegaux ldquoReoperative surgery or thyroid diseaserdquoLangenbeckrsquos Archives of Surgery vol 983091983097983090 no 983094 pp 983094983096983093ndash983094983097983089983090983088983088983095
[983089983088] Chao L Jeng J Lin and M Chen ldquoReoperative thyroid sur-geryrdquo World Journal of Surgery vol 983090983089 no 983094 pp 983094983092983092ndash983094983092983095 983089983097983097983095
[983089983089] S Reeve L Delbridge P Brady P Crummer and C SmythldquoSecondary thyroidectomy a twenty-year experiencerdquo World Journal of Surgery vol 983089983090 no 983092 pp 983092983092983097ndash983092983093983091 983089983097983096983096
[983089983090] J Rojdmark andJ Jarhult ldquoHigh long term recurrence rate afersubtotal thyroidectomy or nodular goitrerdquo European Journal of Surgery vol 983089983094983089 no 983089983088 pp 983095983090983093ndash983095983090983095 983089983097983097983093
[983089983091] A D Katz and D Bronson ldquootal thyroidectomy Te indica-tions and results o 983094983091983088 casesrdquo Te American Journal of Surgery vol 983089983091983094 no 983092 pp 983092983093983088ndash983092983093983092 983089983097983095983096
[983089983092] L P Bron and C J OrsquoBrien ldquootal thyroidectomy or clinically benign disease o the thyroid glandrdquo Te British Journal of Surgery vol 983097983089 no 983093 pp 983093983094983097ndash983093983095983092 983090983088983088983092
[983089983093] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983089983094] ldquoBritish Tyroid Association Guidelines or the managemento thyroid cancer in adultsrdquo 983090983088983089983090 httpwwwbritish-thyroid-associationorgGuidelines
[983089983095] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983089983096] O H Clark ldquo otal thyroidectomy Te treatment o choice orpatients with differentiated thyroid cancerrdquo Annals of Surgery vol 983089983097983094 no 983091 pp 983091983094983089ndash983091983095983088 983089983097983096983090
[983089983097] DS Cooper G M Doherty BR Haugen etal ldquoRevised Amer-ican thyroid association management guidelines or patientswith thyroid nodules and differentiated thyroid cancerrdquo Ty-roid vol 983089983097 no 983089983089 pp 983089983089983094983095ndash983089983090983089983092 983090983088983088983097
[983090983088] M Friedman and H Ibrahim ldquootal versus subtotal thy-roidectomy arguments approaches and recommendationsrdquoOperative echniques in Otolaryngology vol 983089983091 no 983091 pp 983089983097983094ndash983090983088983090 983090983088983088983090
[983090983089] P Muller S Kabus E Robens and F Spelsberg ldquoIndicationsrisks and acceptance o total thyroidectomy or multinodularbenign goiterrdquo Surgery oday vol 983091983089 no 983089983089 pp 983097983093983096ndash983097983094983090 983090983088983088983089
[983090983090] A Mishra A Agarwal G Agarwal and S K Mishra ldquootalthyroidectomy or benign thyroid disorders in an endemicregionrdquo World Journal of Surgery vol 983090983093 no 983091 pp 983091983088983095ndash983091983089983088983090983088983088983089
[983090983091] N Korun C Asci Yilmazlar et al ldquootal thyroidectomy orlobectomy in benign nodular disease o the thyroid changingtrends in surgeryrdquo International Surgery vol 983096983090 no 983092 pp 983092983089983095ndash983092983089983097 983089983097983097983095
[983090983092] G Pappalardo A Guadalaxara F M Frattaroli G Illomei andP Falaschi ldquootal compared with subtotal thyroidectomy inbenign nodular disease personal series and review o publishedreportsrdquo European Journalof Surgery vol 983089983094983092 no 983095 pp 983093983088983089ndash983093983088983094983089983097983097983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 67
983094 Journal o Tyroid Research
[983090983093] D B de Roy van Zuidewijn I Songun J Kievit and C J vande Velde ldquoComplications o thyroid surgeryrdquo Annals of Surgical Oncology vol 983090 no 983089 pp 983093983094ndash983094983088 983089983097983097983093
[983090983094] J W Serpell and D Phan ldquoSaety o total thyroidectomyrdquo Australian and New Zealand Journal of Surgery vol 983095983095 no 983089-983090pp 983089983093ndash983089983097 983090983088983088983095
[983090983095] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and NewZealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983090983096] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983090983097] P E Anderson P R Hurley and P Rosswick ldquoConservativetreatment and long term prophylactic thyroxine in the preven-tion o recurrence o multinodular goiterrdquo Surgery Gynecology and Obstetrics vol 983089983095983089 no 983092 pp 983091983088983097ndash983091983089983092 983089983097983097983088
[983091983088] J L Kraimps R MarechaudD Gineste et al ldquoAnalysisand pre- vention o recurrent goiterrdquo Surgery Gynecology and Obstetrics
vol 983089983095983094 no 983092 pp 983091983089983097ndash983091983090983090 983089983097983097983091[983091983089] L Delbridge A I Guinea and S Reeveldquootal thyroidectomy
or bilateral benign multinodular goiter effect o changingpracticerdquo Archives of Surgery vol 983089983091983092 no 983089983090 pp 983089983091983096983097ndash983089983091983097983091983089983097983097983097
[983091983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091983091] S Reeve L Delbridge A Cohen and P Crummer ldquootalthyroidectomy Te preerred option or multinodular goiterrdquo Annals of Surgery vol 983090983088983094 no 983094 pp 983095983096983090ndash983095983096983094 983089983097983096983095
[983091983092] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and New
Zealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983091983093] H Gibelin M Sierra D Mothes et al ldquoRisk actors or recur-rentnodulargoiterafer thyroidectomy or benigndisease case-control study o 983090983092983092 patientsrdquo World Journal of Surgery vol 983090983096no 983089983089 pp 983089983088983095983097ndash983089983088983096983090 983090983088983088983092
[983091983094] K ekin S Yilmaz N Yalcin et al ldquoWhat would be lef behindi subtotal thyroidectomy were preerred instead o total thy-roidectomyrdquo Te American Journal of Surgery vol 983089983097983097 no 983094pp 983095983094983093ndash983095983094983097 983090983088983089983088
[983091983095] A Gerard S Poncin B Caetano et al ldquoIodine de1047297ciency indu-ces a thyroid stimulating hormone-independent early phase o microvascular reshaping in the thyroidrdquo Te American Journal of Pathology vol 983089983095983090 no 983091 pp 983095983092983096ndash983095983094983088 983090983088983088983096
[983091983096] O Tomusch C Sekulla and H Dralle ldquoIs primary totalthyroidectomy justi1047297ed in benign multinodular goiter Resultso a prospective quality assurance study o 983092983093 hospitals offeringdifferent levels o carerdquo Chirurg vol 983095983092 no 983093 pp 983092983091983095ndash983092983092983091 983090983088983088983091
[983091983097] J K Harness C H Organ Jr and N W Tompson ldquoOperativeexperience o US general surgery residents in thyroid andparathyroid diseaserdquo Surgery vol 983089983089983096 no 983094 pp 983089983088983094983091ndash983089983088983095983088983089983097983097983093
[983092983088] H Dralle C Sekulla K Lorenz M Brauckhoff and AMachens ldquoIntraoperative monitoring o the recurrent laryngealnerve in thyroid surgeryrdquo World Journal of Surgery vol 983091983090 no983095 pp 983089983091983093983096ndash983089983091983094983094 983090983088983088983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 27
983090 Journal o Tyroid Research
recently nerve monitoring has been widely adopted to urthercombat the low rates o RLN paralysis already demonstratedOther bene1047297ts relate to its superiority in cases o malignancy by removing all gross thyroid and potentially malignanttissue acilitating radioactive iodine (RAI) ablation therapy and acilitating surveillance with ultrasound imaging o the
thyroid bed and thyroglobulin (g) monitoringOur unit is a high volume tertiary endocrine surgery centre perorming over 983093983088983088 thyroid procedures per yearHaving previously practiced S or many years we have a
vast experience with recurrent benign thyroid goitre ollow-ing this procedure In addition a large number o patientswho underwent unilateral thyroid lobectomy or unilateralbenign nodular disease have subsequently required comple-tion totalization thyroidectomy or contralateral recurrentdisease Our unique study approach endeavoured to assesswhether reoperative surgery in these two settings conerredany difference in morbidity speci1047297cally with regard to RLNinjury and hypoparathyroidism
2 Materials and Methods
A retrospective analysis was conducted utilizing our endo-crine surgical database or the period rom January 983089983097983097983089 toJune 983090983088983088983094 Tere were 983092983097983092 patients that required reoperationor recurrent benign goitre and were thus selected or thisstudy Te indications or the reoperative surgery includedenlarging neck lump pressure symptoms and imaging sus-picious or malignancy Te patients were divided into twogroups on the basis o the previous surgery group 983089 consistedo patients who had previous unilateral thyroid lobectomygroup 983090 included patients who had undergone prior subtotalthyroidectomy In all cases both the initial and reoperativeprocedure had been perormed at our own institution
Te technique o unilateral extracapsular thyroidectomy at our institution has been well documented previously [983091]Our subtotal thyroidectomy procedure perormed duringthis period is detailed here to avoid potential ambiguityCareul preoperative study o the thyroid ultrasound wasparamount in order to appreciate the location o the noduleswithin each thyroid lobe A small (less than 983093 grams)homogeneous remnant was lef unilaterally at either thesuperior pole or posteriorly depending on the location o the sonographically or intraoperatively detected nodulesTis combination o unilateral lobectomy and unilateral
subtotal resection has been labelled elsewhere as the Dunhillprocedure [983092] Te operations were all perormed by orunder the direct supervision o a senior endocrine surgeon(JLK) ollowing a highly standardized procedure Postop-erative nonsuppressive thyroxine therapy was employed orrestoration o euthyroidism as dictated by thyroid unctiontests (thyroid-stimulating hormone (SH) ree 983092 and 983091)
Prior to reoperative surgery all patients underwent imag-ing by ultrasound computed tomography scans and tech-netium thyroid uptake scans were perormed on an individu-alized basis depending on the extent o the recurrence Intra-operative nerve monitoring was used in all reoperative casesFibreoptic 1047298exible laryngoscopy was routinely perormed in
983137983138983148983141 983089 Group demographics and timingand indication or reoper-ation
Group 9830891038389 = 259
Group 9830901038389 = 235
Sex
Male 983090983089 (983096) 983090983088 (983097)
Female 983090983091983096 (983097983090) 983090983089983093 (983097983089)
Age
Age at 1047297rst operation 983091983096983088 years 983092983088983088 years
Age at reoperation 983093983091983090 years 983093983091983097 years
Interval between initial andreoperative surgery
983089983093983090 years 983089983091983097 years
Indication or reoperation
Isolated nodule 983091983096 (983089983092983095) 983091983094 (983089983093983091)
Multinodular goitre 983090983090983089 (983096983093983091) 983089983097983097 (983096983092983095)
all patients both preoperatively and on the 1047297rst postoperativeday permitting an accurate calculation o our temporary RLN injury rate Patients with any detected abnormalitiesat this examination underwent a urther laryngoscopy at 983094months postoperatively vocal cord dysunction at this stagewas de1047297ned as permanent RLN injury Calcium levels wereobtained on the 1047297rst and second postoperative days andat a 983094-month ollowup appointment Hypocalcaemia wasde1047297ned as less than 983090983088983088 mmolL and permanent i requiringongoing oral calcium supplementation beyond 983091 monthsMorbidity arising rom the initial operation was not theintended ocus o this study and was excluded rom theanalysisonly new morbidity events speci1047297cally relating to the
reoperative surgery were included Descriptive statistics wereobtained and data subjected to analysis by Fisherrsquos exact testand chi-square test to examine the relative risk o reoperativemorbidity or group 983089 and group 983090 Statistical signi1047297cance wasaccepted at lt 005
3 Results
During the study period our unit perormed thyroid surgery on 983094983095983096983088 patients Tere were 983092983097983092 patients that required reop-eration or recurrent benign goitre which constituted 983095983091 o the unitrsquos thyroid surgery throughput during this period
Group 983089 comprised 983090983093983097 patients with previous thyroid
lobectomy and group 983090 comprised 983090983091983093 patients with previoussubtotal thyroidectomy (able 983089) Te groups displayed dem-ographic parity with respect to mean age (group 983089 983091983096 yearsgroup 983090 983092983088 years) and emale predominance (983097983090 and 983097983089resp)
Te mean interval between initial surgery and reoper-ation was 983089983093983090 years in group 983089 and 983089983091983097 years in group 983090Te indication or reoperation in groups 983089 and 983090 was alsocomparable isolated nodules in 983089983092983095 and 983089983093983091 and multi-nodular goitre in 983096983093983091 and 983096983092983095 respectively
Te impact o the initial surgery on the morbidity relatedto the reoperative case was statistically signi1047297cant or bothpermanent RLN injury and permanent hypocalcaemia
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 37
Journal o Tyroid Research 983091
983137983138983148983141 983090 Incidence o RLN injury ollowing reoperative surgery
Group 983089 (lobectomy)1038389 = 259
Group 983090 (subtotal)1038389 = 235
value Relative risk
Normal laryngoscopy 983090983092983089 (983096983091983097) 983090983089983092 (983096983091983092)
ransient RLN paralysis 983089983094 (983094983089983096) 983089983091 (983093983093983091) 983088983096983093 983088983097983090
Permanent RLN paralysis 983090 (983088983095983095) 983096 (983091983092) 983088983088983091983096 983092983091983096
983137983138983148983141 983091 Incidence o hypocalcaemia ollowing reoperative surgery
Group 983089 (lobectomy)1038389 = 259
Group 983090 (subtotal)1038389 = 235
value Relative risk
Normocalcaemia 983090983090983088 (983096983092983097) 983090983088983090 (983096983093983097)
emporary hypocalcaemia 983091983093 (983089983091983093) 983090983089 (983096983097983091) 983088983089983093 983088983094983097
Permanent hypocalcaemia 983092 (983089983093983092) 983089983090 (983093983089) 983088983088983092983089 983091983089983092
Permanent RLN palsy was observed in only 983090 romgroup 983089 and 983096 rom group 983090 (able 983090) Tis correlates with
a statistically signi1047297cant detrimental effect o initial subtotalthyroidectomy on long-term RLN unction ( lt 0038)Tis indicates a relative risk increase o 983092983091983096 in patients whounderwent initial subtotal thyroidectomy (CI
95 983088983097983092ndash983090983088983092)
ransient paralysis was observed in both groups (group 983089983094983089983096 group 983090 983093983093983091) Te majority o patients in bothgroups however have no disturbance in postoperative RLNunction (group 983089 983096983091983097 group 983090 983096983091983092)
Permanent hypocalcaemia was observed in 983089983093983092 o group 983089 patients and 983093983089983089 o group 983090 patients (able 983091)Again this re1047298ected a statistically signi1047297cant detrimentaleffect o initial subtotal thyroidectomy on the developmento permanent hypocalcaemia ollowing reoperative surgery
( lt 0041
) and correlates with an relative risk increase o 983091983089983092 (CI95
983089983088983097ndash983097983093983097) No association was determined or tem-porary hypocalcaemia and the nature o prior surgery (RR 983088983094983097 CI
95 983088983092983089ndash983089983089983092) O note postoperative normocalcaemia
was evident in 983096983092983097 and 983096983093983097 o patients rom group 983089 andgroup 983090 respectively
Incidental malignancy within the reoperative specimenwasdetermined in 983090983089 patients (983092983090983090) Tere wasan equitabledistribution within the two groups with 983089983089 cases in group 983089and 983089983088 cases in group 983090
4 Discussion
Te optimum extent o initial surgery in the managemento benign thyroid goitre continues to generate considerablecontroversy Te debate between the saety and efficacy o a total versus a less than total thyroidectomy has suc-cessully accomplished the widespread adoption o totalthyroidectomy although not ully extinguishing the practiceo subtotal thyroidectomy in several centres worldwide Ourstudy drawing on a vast experience with reoperative surgery in benign thyroid disease approaches the debate rom adifferent angle Rather than ocussing on the morbidity o aninitial subtotal thyroidectomy versus an extracapsular tech-nique our study represents the 1047297rst direct comparison on themorbidity relating to the reoperative surgery in the setting o
previous subtotal and unilateral thyroid resections Althoughthe results may appear intuitive the study did expose some
interesting and important acets o reoperative surgery inthese circumstances
Reoperative thyroid surgery is inherently difficult onaccount o the distortion o central neck area anatomy and1047297brotic encasement o important structures such as therecurrent laryngeal nerve [983093] Tis has led to the recommen-dation by several authors to avoidreoperations by perormingde1047297nitive initial treatment [983094] Despite these difficultiesLevin et al demonstrated that reoperations could still beperormed with minimal morbidity [983095] In their series a low permanent RLN injury rate o less than 983089 and permanenthypoparathyroidism rate o 983091983096 was attainedmdashthe authorsconsequently stressed that or patients maniesting with
recurrent disease reoperative surgery should not be withheldor ear o generating the aorementioned complications Ourrates o permanent RLN palsy (983090) and hypoparathyroidism(983091983090) rom the two groups combined likewise demonstratethat satisactory outcomes are achievable within specializedcentres Other authors have published series o reoperativecases with permanent RLN rates o 983088ndash983089983093 and highlightedthat although being hardly an innocuous procedure reop-erative surgery is sae in the hands o experienced surgeonshowever a complete initial procedure should obviate theexposure to this unnecessary additional risk [983096 983097]
A different scenario exists when a patient requires sec-ondary thyroid surgery or recurrent benign disease with a
background o unilateral hemithyroidectomy In this situa-tion where the contralateral side is completely untouchedno increased risk is conerred as shown by Chao et aland con1047297rmed in our study with rates o permanent RLNinjury and permanent hypoparathyroidism rates o 983088983095983095and983089983093983092 respectively [983089983088] However previous S in whichboth sides have been dissected is associated with an up to1047297veold increase in complications with reoperative surgery [983089983089 983089983090] Despite the scar tissue and degenerative changescited by Katz and Bronson as the principle culprit actorsrelating to reoperative morbidity [983089983091] Bron and OrsquoBrienound no signi1047297cant correlation between complication rateandprevioussurgery [983089983092] ransient hypoparathyroidism was
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 47
983092 Journal o Tyroid Research
seen in 983089983091983093 o group 983089 patients in our study representing anonstatistically signi1047297cant difference rom the previous Sgroup Germane to this 1047297nding Barczynski et al remark that transient hypoparathyroidism ollowing in an erawhere parathyroid autotransplantation is common should be
viewed as a sequel rather than a complication [983089983093]
Te technique o reoperative thyroid surgery is clearly important when analysing complications Farrag and col-leagues have recently promulgated an algorithm or sae andeffective thyroid bed surgery or malignancy although many aspects can be readily extrapolated to the benign sphereas well [983093] Te principle tenets o the algorithm includepreoperative high-resolution ultrasound examination pre-operative vocal old examination by 1047297breoptic laryngoscopyand routine nerve identi1047297cation that should be acilitatedby the use o intraoperative nerve monitoring (IONM)Several o these attributes are endorsed by internationalthyroid surgery guidelines [983089983094] Additionally Menegaux etal recommend a lateral approach to the thyroid bed withdivision o the inrahyoid musculature in an effort to avoid1047297brous tissue surrounding the thyroid remnant [983089983095]
emerged as an alternativeto S initially in the malig-nant domain Clark embraced the technique or managemento well-differentiated thyroid cancer and demonstrated thesaety o the technique and low complication rate [983089983096] It isrecommended as the operation o choice in all current treat-ment guidelines or thyroid cancer [983089983097] Te purported ben-e1047297ts o a total gland resection in thyroid cancer include theremoval o the primary tumour elimination o any potentialcontralateral disease and acilitation o postoperative RAIablation g surveillance and ultrasound scanning o thethyroid bed [983090983088] Tese bene1047297ts are not present when dealingwith benign disease Proponents o a subtotal resection claima reduced rate o RLN injury and hypoparathyroidism andassert that the majority o thyroid malignancies detectedortuitously on 1047297nal histopathology are o limited clinicalsigni1047297cance Furthermore i recurrences do occur they canbe managed surgically when indicated with less morbidity than i total thyroidectomy was perormed on all cases o thyroid malignancy at the outset [983090983088]
Numerous publications have since established the low morbidity o the extracapsular procedure Mishra et aldemonstrated an 983088983096 permanent RLN rate and 983089983094 per-manent hypoparathyroidism rate whilst Muller et al ounda 983088983097 rate or both morbidities [983090983089 983090983090] Many other studiescon1047297rmed similar 1047297ndings [983090983091ndash983090983093] Serpell and Phan ound a
permanent RLN palsy rate o 983088983091 and hypoparathyroidismrate o 983089983096 and concluded that can be perormed saely in a standard endocrine surgical unit with low complicationrates matching world centres o excellence [983090983094] Documentedhigh rates o incidental thyroid malignancy orti1047297ed thegrowing argument in avour o total thyroidectomy Ourpresent study revealed an incidental papillary microcarci-noma rate o 983092983090983090 that was equally distributed within thetwo groups We have previously published a 983091 rate o occult carcinoma somewhat lower than other subsequently published series rom Bron and OrsquoBrien (983092983094) [983089983092] Colak et al (983095983092) [983090983095] and Levin et al (983090983090) [983095] Menegauxet al determined that thyroid cancer might be ound in
approximately 983089983088 o reoperative cases or recurrent goitreeven though the preceding operation was perormed orbenign disease [983090983096] By the same token ezelman et al oundthat within a cohort o patients diagnosed with thyroid cancerollowing a subtotal thyroidectomy completion resection o the thyroid remnants yielded papillary microcarcinoma in
983093983090983094 [983089]Recurrence o goitre and ailure to prevent hypothy-
roidism have urther weakened the validity o subtotal thy-roidectomy as a surgical strategy or benign thyroid diseaseGoitre recurrence rates associated with S range rom983095983089 to 983092983091 [983089 983089983090] Te incidence o recurrence appearsdirectly related to the length o surveillance [983090983097 983091983088]mdashalthough our study and others have ound that a peak incidence o recurrence occurs at approximately 983089983091 to 983089983093 yearsrom the primary operation [983091983089] a 983092983091 recurrence rate may be observed with up to 983091983088 years o ollowup [ 983089983090] Many have noted the ailure o thyroxine suppression to preventrecurrence with a 983089983092983093 recurrence rate demonstrated in
the study by Pappalardo et al in spite o drug prophylaxis[983090983092] Conversely thyroxine replacement is not obviated in983091983094983094ndash983092983095983096 o subtotal thyroidectomy procedures and henceshould not be used to justiy practice o the procedure [983091983090]
Te undamental difficulty with S is allotting a tissueremnant unaffected by the nodular process Colak et alhighlighted the predicament o leaving healthy tissue intactin patients with huge goitres where the nodular diseaseofen reaches the dorsal capsule [983090983095] Tere is generally anincreasing recognition that the nodular transormations inmultinodular goitre inherently encompass the entire glandhence although S permits a reduction in the bulk o dis-ease it is not an optimal treatment [983091983091] Moreover the rem-
nant posterolateral tissue ofen extends into the retrotrachealand retrooesophageal areas where recurrence portends early pressure symptoms that may require technically demandingreoperative surgery [983091983092] We have previously shown thatmultinodular goitre is a highly signi1047297cant risk actor orrecurrence in benign thyroid disease where a less than totalthyroidectomy has been perormed [983091983093] Recently a novelstudy by ekin et al demonstrated that Ki-983094983095 prolierationmarker levels in remnant S thyroid tissue were signi1047297-cantly higher than in normal thyroid tissue [983091983094] Tey oundthat despite the relatively small size o remnant micronodulesthe high Ki-983094983095 levels re1047298ect high cellular mitotic activity and ensuing signi1047297cant goitrogenic potential o remnant
tissue Furthermore the existence o micronodules in theremnant specimens harbouring similar prolieration index
values as the main thyroid specimen establishes the homoge-neous nature o the parenchymal alteration in multinodulargoitre Gerard et al postulate that recurrent goitres resistantto thyroxine suppression may arise due to the polyclonalnature o nodule ormation involving goitrogenic insulin-likegrowth actors and their binding proteins Tese may occurseparate to iodine de1047297ciency related mechanisms o goitredevelopment based on SH and vascular-endothelial growthactor (VEGF) angiogenesis [983091983095]
Finally the ofen-overlooked denominator and perhapsmost crucial determinant o morbidity is surgical technique
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 57
Journal o Tyroid Research 983093
Tomusch et al commented on the importance o ldquowell-trained surgeons using an appropriate intraoperative tech-niquerdquo in the perormance o total thyroidectomy [983091983096] Teability to perorm a sae total thyroidectomy is clearly adirect derivative o onersquos surgical training and experience[983091983097] Te evolution o more dedicated endocrine surgery
training programmes and specialized units combined withtechnological re1047297nements such as IONM is likely to urtherenhance the sae implementation o or both malignantand benign thyroid disease alike [983092983088]
5 Conclusion
Reoperative surgery or recurrent benign thyroid disease isassociated with increased morbidity when preceded by initialsubtotal thyroidectomy Associated high levels o recurrenceand increased permanent RLN injury and hypoparathy-roidism rates seen in this setting call or the abandonmento this procedure in avour o total thyroidectomy It should
be noted however that successul reoperative thyroid surgery perormed by experienced well-trained surgeons may beaccomplished with low overall rates o morbidity
Conflict of Interests
Te authors disclose no real or potential con1047298ict o interests
References
[983089] S ezelman I Borucu Y Senyurek F unca and erziogluldquoTe change in surgical practice rom subtotal to near-total ortotal thyroidectomy in the treatment o patients with benign
multinodular goiterrdquo World Journal of Surgery vol983091983091no 983091pp983092983088983088ndash983092983088983093 983090983088983088983097
[983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091] ldquoechnique o thyroidectomyrdquo in Endocrine Surgery Principlesand Practice H Gibelin Desurmont J L Kraimps and J GH Hubbard Eds Springer SpecialistSurgery Series chapter 983089983090pp 983089983094983091ndash983089983095983089 Springer London UK 983089st edition 983090983088983088983097
[983092] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092
no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983093] Y Farrag N Agrawal S Sheth et al ldquoAlgorithm or saeand effective reoperative thyroid bed surgery or recurrentpersistent papillary thyroid carcinomardquo Head and Neck vol 983090983097no 983089983090 pp 983089983088983094983097ndash983089983088983095983092 983090983088983088983095
[983094] D B Wilson E D Staren and R A Prinz ldquoTyroid reopera-tions indications and risksrdquo Te American Surgeon vol 983094983092 no983095 pp 983094983095983092ndash983094983095983097 983089983097983097983096
[983095] K E Levin A H Clark Q Duh M Demeure A E Sipersteinand O H Clark ldquoReoperative thyroid surgeryrdquo Surgery vol 983089983089983089no 983094 pp 983094983088983092ndash983094983088983097 983089983097983097983090
[983096] D J erris S S Khichi S K Anderson and M W SeybtldquoReoperative thyroidectomy or benignthyroiddisease the case
or phasing out subtotal thyroidectomyrdquo Laryngoscope vol 983089983089983097no 983089 p S983096983097 983090983088983088983097
[983097] J H Leevre C resallet L Leenhardt C Jublanc J Chigotand F Menegaux ldquoReoperative surgery or thyroid diseaserdquoLangenbeckrsquos Archives of Surgery vol 983091983097983090 no 983094 pp 983094983096983093ndash983094983097983089983090983088983088983095
[983089983088] Chao L Jeng J Lin and M Chen ldquoReoperative thyroid sur-geryrdquo World Journal of Surgery vol 983090983089 no 983094 pp 983094983092983092ndash983094983092983095 983089983097983097983095
[983089983089] S Reeve L Delbridge P Brady P Crummer and C SmythldquoSecondary thyroidectomy a twenty-year experiencerdquo World Journal of Surgery vol 983089983090 no 983092 pp 983092983092983097ndash983092983093983091 983089983097983096983096
[983089983090] J Rojdmark andJ Jarhult ldquoHigh long term recurrence rate afersubtotal thyroidectomy or nodular goitrerdquo European Journal of Surgery vol 983089983094983089 no 983089983088 pp 983095983090983093ndash983095983090983095 983089983097983097983093
[983089983091] A D Katz and D Bronson ldquootal thyroidectomy Te indica-tions and results o 983094983091983088 casesrdquo Te American Journal of Surgery vol 983089983091983094 no 983092 pp 983092983093983088ndash983092983093983092 983089983097983095983096
[983089983092] L P Bron and C J OrsquoBrien ldquootal thyroidectomy or clinically benign disease o the thyroid glandrdquo Te British Journal of Surgery vol 983097983089 no 983093 pp 983093983094983097ndash983093983095983092 983090983088983088983092
[983089983093] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983089983094] ldquoBritish Tyroid Association Guidelines or the managemento thyroid cancer in adultsrdquo 983090983088983089983090 httpwwwbritish-thyroid-associationorgGuidelines
[983089983095] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983089983096] O H Clark ldquo otal thyroidectomy Te treatment o choice orpatients with differentiated thyroid cancerrdquo Annals of Surgery vol 983089983097983094 no 983091 pp 983091983094983089ndash983091983095983088 983089983097983096983090
[983089983097] DS Cooper G M Doherty BR Haugen etal ldquoRevised Amer-ican thyroid association management guidelines or patientswith thyroid nodules and differentiated thyroid cancerrdquo Ty-roid vol 983089983097 no 983089983089 pp 983089983089983094983095ndash983089983090983089983092 983090983088983088983097
[983090983088] M Friedman and H Ibrahim ldquootal versus subtotal thy-roidectomy arguments approaches and recommendationsrdquoOperative echniques in Otolaryngology vol 983089983091 no 983091 pp 983089983097983094ndash983090983088983090 983090983088983088983090
[983090983089] P Muller S Kabus E Robens and F Spelsberg ldquoIndicationsrisks and acceptance o total thyroidectomy or multinodularbenign goiterrdquo Surgery oday vol 983091983089 no 983089983089 pp 983097983093983096ndash983097983094983090 983090983088983088983089
[983090983090] A Mishra A Agarwal G Agarwal and S K Mishra ldquootalthyroidectomy or benign thyroid disorders in an endemicregionrdquo World Journal of Surgery vol 983090983093 no 983091 pp 983091983088983095ndash983091983089983088983090983088983088983089
[983090983091] N Korun C Asci Yilmazlar et al ldquootal thyroidectomy orlobectomy in benign nodular disease o the thyroid changingtrends in surgeryrdquo International Surgery vol 983096983090 no 983092 pp 983092983089983095ndash983092983089983097 983089983097983097983095
[983090983092] G Pappalardo A Guadalaxara F M Frattaroli G Illomei andP Falaschi ldquootal compared with subtotal thyroidectomy inbenign nodular disease personal series and review o publishedreportsrdquo European Journalof Surgery vol 983089983094983092 no 983095 pp 983093983088983089ndash983093983088983094983089983097983097983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 67
983094 Journal o Tyroid Research
[983090983093] D B de Roy van Zuidewijn I Songun J Kievit and C J vande Velde ldquoComplications o thyroid surgeryrdquo Annals of Surgical Oncology vol 983090 no 983089 pp 983093983094ndash983094983088 983089983097983097983093
[983090983094] J W Serpell and D Phan ldquoSaety o total thyroidectomyrdquo Australian and New Zealand Journal of Surgery vol 983095983095 no 983089-983090pp 983089983093ndash983089983097 983090983088983088983095
[983090983095] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and NewZealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983090983096] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983090983097] P E Anderson P R Hurley and P Rosswick ldquoConservativetreatment and long term prophylactic thyroxine in the preven-tion o recurrence o multinodular goiterrdquo Surgery Gynecology and Obstetrics vol 983089983095983089 no 983092 pp 983091983088983097ndash983091983089983092 983089983097983097983088
[983091983088] J L Kraimps R MarechaudD Gineste et al ldquoAnalysisand pre- vention o recurrent goiterrdquo Surgery Gynecology and Obstetrics
vol 983089983095983094 no 983092 pp 983091983089983097ndash983091983090983090 983089983097983097983091[983091983089] L Delbridge A I Guinea and S Reeveldquootal thyroidectomy
or bilateral benign multinodular goiter effect o changingpracticerdquo Archives of Surgery vol 983089983091983092 no 983089983090 pp 983089983091983096983097ndash983089983091983097983091983089983097983097983097
[983091983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091983091] S Reeve L Delbridge A Cohen and P Crummer ldquootalthyroidectomy Te preerred option or multinodular goiterrdquo Annals of Surgery vol 983090983088983094 no 983094 pp 983095983096983090ndash983095983096983094 983089983097983096983095
[983091983092] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and New
Zealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983091983093] H Gibelin M Sierra D Mothes et al ldquoRisk actors or recur-rentnodulargoiterafer thyroidectomy or benigndisease case-control study o 983090983092983092 patientsrdquo World Journal of Surgery vol 983090983096no 983089983089 pp 983089983088983095983097ndash983089983088983096983090 983090983088983088983092
[983091983094] K ekin S Yilmaz N Yalcin et al ldquoWhat would be lef behindi subtotal thyroidectomy were preerred instead o total thy-roidectomyrdquo Te American Journal of Surgery vol 983089983097983097 no 983094pp 983095983094983093ndash983095983094983097 983090983088983089983088
[983091983095] A Gerard S Poncin B Caetano et al ldquoIodine de1047297ciency indu-ces a thyroid stimulating hormone-independent early phase o microvascular reshaping in the thyroidrdquo Te American Journal of Pathology vol 983089983095983090 no 983091 pp 983095983092983096ndash983095983094983088 983090983088983088983096
[983091983096] O Tomusch C Sekulla and H Dralle ldquoIs primary totalthyroidectomy justi1047297ed in benign multinodular goiter Resultso a prospective quality assurance study o 983092983093 hospitals offeringdifferent levels o carerdquo Chirurg vol 983095983092 no 983093 pp 983092983091983095ndash983092983092983091 983090983088983088983091
[983091983097] J K Harness C H Organ Jr and N W Tompson ldquoOperativeexperience o US general surgery residents in thyroid andparathyroid diseaserdquo Surgery vol 983089983089983096 no 983094 pp 983089983088983094983091ndash983089983088983095983088983089983097983097983093
[983092983088] H Dralle C Sekulla K Lorenz M Brauckhoff and AMachens ldquoIntraoperative monitoring o the recurrent laryngealnerve in thyroid surgeryrdquo World Journal of Surgery vol 983091983090 no983095 pp 983089983091983093983096ndash983089983091983094983094 983090983088983088983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 37
Journal o Tyroid Research 983091
983137983138983148983141 983090 Incidence o RLN injury ollowing reoperative surgery
Group 983089 (lobectomy)1038389 = 259
Group 983090 (subtotal)1038389 = 235
value Relative risk
Normal laryngoscopy 983090983092983089 (983096983091983097) 983090983089983092 (983096983091983092)
ransient RLN paralysis 983089983094 (983094983089983096) 983089983091 (983093983093983091) 983088983096983093 983088983097983090
Permanent RLN paralysis 983090 (983088983095983095) 983096 (983091983092) 983088983088983091983096 983092983091983096
983137983138983148983141 983091 Incidence o hypocalcaemia ollowing reoperative surgery
Group 983089 (lobectomy)1038389 = 259
Group 983090 (subtotal)1038389 = 235
value Relative risk
Normocalcaemia 983090983090983088 (983096983092983097) 983090983088983090 (983096983093983097)
emporary hypocalcaemia 983091983093 (983089983091983093) 983090983089 (983096983097983091) 983088983089983093 983088983094983097
Permanent hypocalcaemia 983092 (983089983093983092) 983089983090 (983093983089) 983088983088983092983089 983091983089983092
Permanent RLN palsy was observed in only 983090 romgroup 983089 and 983096 rom group 983090 (able 983090) Tis correlates with
a statistically signi1047297cant detrimental effect o initial subtotalthyroidectomy on long-term RLN unction ( lt 0038)Tis indicates a relative risk increase o 983092983091983096 in patients whounderwent initial subtotal thyroidectomy (CI
95 983088983097983092ndash983090983088983092)
ransient paralysis was observed in both groups (group 983089983094983089983096 group 983090 983093983093983091) Te majority o patients in bothgroups however have no disturbance in postoperative RLNunction (group 983089 983096983091983097 group 983090 983096983091983092)
Permanent hypocalcaemia was observed in 983089983093983092 o group 983089 patients and 983093983089983089 o group 983090 patients (able 983091)Again this re1047298ected a statistically signi1047297cant detrimentaleffect o initial subtotal thyroidectomy on the developmento permanent hypocalcaemia ollowing reoperative surgery
( lt 0041
) and correlates with an relative risk increase o 983091983089983092 (CI95
983089983088983097ndash983097983093983097) No association was determined or tem-porary hypocalcaemia and the nature o prior surgery (RR 983088983094983097 CI
95 983088983092983089ndash983089983089983092) O note postoperative normocalcaemia
was evident in 983096983092983097 and 983096983093983097 o patients rom group 983089 andgroup 983090 respectively
Incidental malignancy within the reoperative specimenwasdetermined in 983090983089 patients (983092983090983090) Tere wasan equitabledistribution within the two groups with 983089983089 cases in group 983089and 983089983088 cases in group 983090
4 Discussion
Te optimum extent o initial surgery in the managemento benign thyroid goitre continues to generate considerablecontroversy Te debate between the saety and efficacy o a total versus a less than total thyroidectomy has suc-cessully accomplished the widespread adoption o totalthyroidectomy although not ully extinguishing the practiceo subtotal thyroidectomy in several centres worldwide Ourstudy drawing on a vast experience with reoperative surgery in benign thyroid disease approaches the debate rom adifferent angle Rather than ocussing on the morbidity o aninitial subtotal thyroidectomy versus an extracapsular tech-nique our study represents the 1047297rst direct comparison on themorbidity relating to the reoperative surgery in the setting o
previous subtotal and unilateral thyroid resections Althoughthe results may appear intuitive the study did expose some
interesting and important acets o reoperative surgery inthese circumstances
Reoperative thyroid surgery is inherently difficult onaccount o the distortion o central neck area anatomy and1047297brotic encasement o important structures such as therecurrent laryngeal nerve [983093] Tis has led to the recommen-dation by several authors to avoidreoperations by perormingde1047297nitive initial treatment [983094] Despite these difficultiesLevin et al demonstrated that reoperations could still beperormed with minimal morbidity [983095] In their series a low permanent RLN injury rate o less than 983089 and permanenthypoparathyroidism rate o 983091983096 was attainedmdashthe authorsconsequently stressed that or patients maniesting with
recurrent disease reoperative surgery should not be withheldor ear o generating the aorementioned complications Ourrates o permanent RLN palsy (983090) and hypoparathyroidism(983091983090) rom the two groups combined likewise demonstratethat satisactory outcomes are achievable within specializedcentres Other authors have published series o reoperativecases with permanent RLN rates o 983088ndash983089983093 and highlightedthat although being hardly an innocuous procedure reop-erative surgery is sae in the hands o experienced surgeonshowever a complete initial procedure should obviate theexposure to this unnecessary additional risk [983096 983097]
A different scenario exists when a patient requires sec-ondary thyroid surgery or recurrent benign disease with a
background o unilateral hemithyroidectomy In this situa-tion where the contralateral side is completely untouchedno increased risk is conerred as shown by Chao et aland con1047297rmed in our study with rates o permanent RLNinjury and permanent hypoparathyroidism rates o 983088983095983095and983089983093983092 respectively [983089983088] However previous S in whichboth sides have been dissected is associated with an up to1047297veold increase in complications with reoperative surgery [983089983089 983089983090] Despite the scar tissue and degenerative changescited by Katz and Bronson as the principle culprit actorsrelating to reoperative morbidity [983089983091] Bron and OrsquoBrienound no signi1047297cant correlation between complication rateandprevioussurgery [983089983092] ransient hypoparathyroidism was
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 47
983092 Journal o Tyroid Research
seen in 983089983091983093 o group 983089 patients in our study representing anonstatistically signi1047297cant difference rom the previous Sgroup Germane to this 1047297nding Barczynski et al remark that transient hypoparathyroidism ollowing in an erawhere parathyroid autotransplantation is common should be
viewed as a sequel rather than a complication [983089983093]
Te technique o reoperative thyroid surgery is clearly important when analysing complications Farrag and col-leagues have recently promulgated an algorithm or sae andeffective thyroid bed surgery or malignancy although many aspects can be readily extrapolated to the benign sphereas well [983093] Te principle tenets o the algorithm includepreoperative high-resolution ultrasound examination pre-operative vocal old examination by 1047297breoptic laryngoscopyand routine nerve identi1047297cation that should be acilitatedby the use o intraoperative nerve monitoring (IONM)Several o these attributes are endorsed by internationalthyroid surgery guidelines [983089983094] Additionally Menegaux etal recommend a lateral approach to the thyroid bed withdivision o the inrahyoid musculature in an effort to avoid1047297brous tissue surrounding the thyroid remnant [983089983095]
emerged as an alternativeto S initially in the malig-nant domain Clark embraced the technique or managemento well-differentiated thyroid cancer and demonstrated thesaety o the technique and low complication rate [983089983096] It isrecommended as the operation o choice in all current treat-ment guidelines or thyroid cancer [983089983097] Te purported ben-e1047297ts o a total gland resection in thyroid cancer include theremoval o the primary tumour elimination o any potentialcontralateral disease and acilitation o postoperative RAIablation g surveillance and ultrasound scanning o thethyroid bed [983090983088] Tese bene1047297ts are not present when dealingwith benign disease Proponents o a subtotal resection claima reduced rate o RLN injury and hypoparathyroidism andassert that the majority o thyroid malignancies detectedortuitously on 1047297nal histopathology are o limited clinicalsigni1047297cance Furthermore i recurrences do occur they canbe managed surgically when indicated with less morbidity than i total thyroidectomy was perormed on all cases o thyroid malignancy at the outset [983090983088]
Numerous publications have since established the low morbidity o the extracapsular procedure Mishra et aldemonstrated an 983088983096 permanent RLN rate and 983089983094 per-manent hypoparathyroidism rate whilst Muller et al ounda 983088983097 rate or both morbidities [983090983089 983090983090] Many other studiescon1047297rmed similar 1047297ndings [983090983091ndash983090983093] Serpell and Phan ound a
permanent RLN palsy rate o 983088983091 and hypoparathyroidismrate o 983089983096 and concluded that can be perormed saely in a standard endocrine surgical unit with low complicationrates matching world centres o excellence [983090983094] Documentedhigh rates o incidental thyroid malignancy orti1047297ed thegrowing argument in avour o total thyroidectomy Ourpresent study revealed an incidental papillary microcarci-noma rate o 983092983090983090 that was equally distributed within thetwo groups We have previously published a 983091 rate o occult carcinoma somewhat lower than other subsequently published series rom Bron and OrsquoBrien (983092983094) [983089983092] Colak et al (983095983092) [983090983095] and Levin et al (983090983090) [983095] Menegauxet al determined that thyroid cancer might be ound in
approximately 983089983088 o reoperative cases or recurrent goitreeven though the preceding operation was perormed orbenign disease [983090983096] By the same token ezelman et al oundthat within a cohort o patients diagnosed with thyroid cancerollowing a subtotal thyroidectomy completion resection o the thyroid remnants yielded papillary microcarcinoma in
983093983090983094 [983089]Recurrence o goitre and ailure to prevent hypothy-
roidism have urther weakened the validity o subtotal thy-roidectomy as a surgical strategy or benign thyroid diseaseGoitre recurrence rates associated with S range rom983095983089 to 983092983091 [983089 983089983090] Te incidence o recurrence appearsdirectly related to the length o surveillance [983090983097 983091983088]mdashalthough our study and others have ound that a peak incidence o recurrence occurs at approximately 983089983091 to 983089983093 yearsrom the primary operation [983091983089] a 983092983091 recurrence rate may be observed with up to 983091983088 years o ollowup [ 983089983090] Many have noted the ailure o thyroxine suppression to preventrecurrence with a 983089983092983093 recurrence rate demonstrated in
the study by Pappalardo et al in spite o drug prophylaxis[983090983092] Conversely thyroxine replacement is not obviated in983091983094983094ndash983092983095983096 o subtotal thyroidectomy procedures and henceshould not be used to justiy practice o the procedure [983091983090]
Te undamental difficulty with S is allotting a tissueremnant unaffected by the nodular process Colak et alhighlighted the predicament o leaving healthy tissue intactin patients with huge goitres where the nodular diseaseofen reaches the dorsal capsule [983090983095] Tere is generally anincreasing recognition that the nodular transormations inmultinodular goitre inherently encompass the entire glandhence although S permits a reduction in the bulk o dis-ease it is not an optimal treatment [983091983091] Moreover the rem-
nant posterolateral tissue ofen extends into the retrotrachealand retrooesophageal areas where recurrence portends early pressure symptoms that may require technically demandingreoperative surgery [983091983092] We have previously shown thatmultinodular goitre is a highly signi1047297cant risk actor orrecurrence in benign thyroid disease where a less than totalthyroidectomy has been perormed [983091983093] Recently a novelstudy by ekin et al demonstrated that Ki-983094983095 prolierationmarker levels in remnant S thyroid tissue were signi1047297-cantly higher than in normal thyroid tissue [983091983094] Tey oundthat despite the relatively small size o remnant micronodulesthe high Ki-983094983095 levels re1047298ect high cellular mitotic activity and ensuing signi1047297cant goitrogenic potential o remnant
tissue Furthermore the existence o micronodules in theremnant specimens harbouring similar prolieration index
values as the main thyroid specimen establishes the homoge-neous nature o the parenchymal alteration in multinodulargoitre Gerard et al postulate that recurrent goitres resistantto thyroxine suppression may arise due to the polyclonalnature o nodule ormation involving goitrogenic insulin-likegrowth actors and their binding proteins Tese may occurseparate to iodine de1047297ciency related mechanisms o goitredevelopment based on SH and vascular-endothelial growthactor (VEGF) angiogenesis [983091983095]
Finally the ofen-overlooked denominator and perhapsmost crucial determinant o morbidity is surgical technique
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 57
Journal o Tyroid Research 983093
Tomusch et al commented on the importance o ldquowell-trained surgeons using an appropriate intraoperative tech-niquerdquo in the perormance o total thyroidectomy [983091983096] Teability to perorm a sae total thyroidectomy is clearly adirect derivative o onersquos surgical training and experience[983091983097] Te evolution o more dedicated endocrine surgery
training programmes and specialized units combined withtechnological re1047297nements such as IONM is likely to urtherenhance the sae implementation o or both malignantand benign thyroid disease alike [983092983088]
5 Conclusion
Reoperative surgery or recurrent benign thyroid disease isassociated with increased morbidity when preceded by initialsubtotal thyroidectomy Associated high levels o recurrenceand increased permanent RLN injury and hypoparathy-roidism rates seen in this setting call or the abandonmento this procedure in avour o total thyroidectomy It should
be noted however that successul reoperative thyroid surgery perormed by experienced well-trained surgeons may beaccomplished with low overall rates o morbidity
Conflict of Interests
Te authors disclose no real or potential con1047298ict o interests
References
[983089] S ezelman I Borucu Y Senyurek F unca and erziogluldquoTe change in surgical practice rom subtotal to near-total ortotal thyroidectomy in the treatment o patients with benign
multinodular goiterrdquo World Journal of Surgery vol983091983091no 983091pp983092983088983088ndash983092983088983093 983090983088983088983097
[983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091] ldquoechnique o thyroidectomyrdquo in Endocrine Surgery Principlesand Practice H Gibelin Desurmont J L Kraimps and J GH Hubbard Eds Springer SpecialistSurgery Series chapter 983089983090pp 983089983094983091ndash983089983095983089 Springer London UK 983089st edition 983090983088983088983097
[983092] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092
no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983093] Y Farrag N Agrawal S Sheth et al ldquoAlgorithm or saeand effective reoperative thyroid bed surgery or recurrentpersistent papillary thyroid carcinomardquo Head and Neck vol 983090983097no 983089983090 pp 983089983088983094983097ndash983089983088983095983092 983090983088983088983095
[983094] D B Wilson E D Staren and R A Prinz ldquoTyroid reopera-tions indications and risksrdquo Te American Surgeon vol 983094983092 no983095 pp 983094983095983092ndash983094983095983097 983089983097983097983096
[983095] K E Levin A H Clark Q Duh M Demeure A E Sipersteinand O H Clark ldquoReoperative thyroid surgeryrdquo Surgery vol 983089983089983089no 983094 pp 983094983088983092ndash983094983088983097 983089983097983097983090
[983096] D J erris S S Khichi S K Anderson and M W SeybtldquoReoperative thyroidectomy or benignthyroiddisease the case
or phasing out subtotal thyroidectomyrdquo Laryngoscope vol 983089983089983097no 983089 p S983096983097 983090983088983088983097
[983097] J H Leevre C resallet L Leenhardt C Jublanc J Chigotand F Menegaux ldquoReoperative surgery or thyroid diseaserdquoLangenbeckrsquos Archives of Surgery vol 983091983097983090 no 983094 pp 983094983096983093ndash983094983097983089983090983088983088983095
[983089983088] Chao L Jeng J Lin and M Chen ldquoReoperative thyroid sur-geryrdquo World Journal of Surgery vol 983090983089 no 983094 pp 983094983092983092ndash983094983092983095 983089983097983097983095
[983089983089] S Reeve L Delbridge P Brady P Crummer and C SmythldquoSecondary thyroidectomy a twenty-year experiencerdquo World Journal of Surgery vol 983089983090 no 983092 pp 983092983092983097ndash983092983093983091 983089983097983096983096
[983089983090] J Rojdmark andJ Jarhult ldquoHigh long term recurrence rate afersubtotal thyroidectomy or nodular goitrerdquo European Journal of Surgery vol 983089983094983089 no 983089983088 pp 983095983090983093ndash983095983090983095 983089983097983097983093
[983089983091] A D Katz and D Bronson ldquootal thyroidectomy Te indica-tions and results o 983094983091983088 casesrdquo Te American Journal of Surgery vol 983089983091983094 no 983092 pp 983092983093983088ndash983092983093983092 983089983097983095983096
[983089983092] L P Bron and C J OrsquoBrien ldquootal thyroidectomy or clinically benign disease o the thyroid glandrdquo Te British Journal of Surgery vol 983097983089 no 983093 pp 983093983094983097ndash983093983095983092 983090983088983088983092
[983089983093] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983089983094] ldquoBritish Tyroid Association Guidelines or the managemento thyroid cancer in adultsrdquo 983090983088983089983090 httpwwwbritish-thyroid-associationorgGuidelines
[983089983095] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983089983096] O H Clark ldquo otal thyroidectomy Te treatment o choice orpatients with differentiated thyroid cancerrdquo Annals of Surgery vol 983089983097983094 no 983091 pp 983091983094983089ndash983091983095983088 983089983097983096983090
[983089983097] DS Cooper G M Doherty BR Haugen etal ldquoRevised Amer-ican thyroid association management guidelines or patientswith thyroid nodules and differentiated thyroid cancerrdquo Ty-roid vol 983089983097 no 983089983089 pp 983089983089983094983095ndash983089983090983089983092 983090983088983088983097
[983090983088] M Friedman and H Ibrahim ldquootal versus subtotal thy-roidectomy arguments approaches and recommendationsrdquoOperative echniques in Otolaryngology vol 983089983091 no 983091 pp 983089983097983094ndash983090983088983090 983090983088983088983090
[983090983089] P Muller S Kabus E Robens and F Spelsberg ldquoIndicationsrisks and acceptance o total thyroidectomy or multinodularbenign goiterrdquo Surgery oday vol 983091983089 no 983089983089 pp 983097983093983096ndash983097983094983090 983090983088983088983089
[983090983090] A Mishra A Agarwal G Agarwal and S K Mishra ldquootalthyroidectomy or benign thyroid disorders in an endemicregionrdquo World Journal of Surgery vol 983090983093 no 983091 pp 983091983088983095ndash983091983089983088983090983088983088983089
[983090983091] N Korun C Asci Yilmazlar et al ldquootal thyroidectomy orlobectomy in benign nodular disease o the thyroid changingtrends in surgeryrdquo International Surgery vol 983096983090 no 983092 pp 983092983089983095ndash983092983089983097 983089983097983097983095
[983090983092] G Pappalardo A Guadalaxara F M Frattaroli G Illomei andP Falaschi ldquootal compared with subtotal thyroidectomy inbenign nodular disease personal series and review o publishedreportsrdquo European Journalof Surgery vol 983089983094983092 no 983095 pp 983093983088983089ndash983093983088983094983089983097983097983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 67
983094 Journal o Tyroid Research
[983090983093] D B de Roy van Zuidewijn I Songun J Kievit and C J vande Velde ldquoComplications o thyroid surgeryrdquo Annals of Surgical Oncology vol 983090 no 983089 pp 983093983094ndash983094983088 983089983097983097983093
[983090983094] J W Serpell and D Phan ldquoSaety o total thyroidectomyrdquo Australian and New Zealand Journal of Surgery vol 983095983095 no 983089-983090pp 983089983093ndash983089983097 983090983088983088983095
[983090983095] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and NewZealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983090983096] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983090983097] P E Anderson P R Hurley and P Rosswick ldquoConservativetreatment and long term prophylactic thyroxine in the preven-tion o recurrence o multinodular goiterrdquo Surgery Gynecology and Obstetrics vol 983089983095983089 no 983092 pp 983091983088983097ndash983091983089983092 983089983097983097983088
[983091983088] J L Kraimps R MarechaudD Gineste et al ldquoAnalysisand pre- vention o recurrent goiterrdquo Surgery Gynecology and Obstetrics
vol 983089983095983094 no 983092 pp 983091983089983097ndash983091983090983090 983089983097983097983091[983091983089] L Delbridge A I Guinea and S Reeveldquootal thyroidectomy
or bilateral benign multinodular goiter effect o changingpracticerdquo Archives of Surgery vol 983089983091983092 no 983089983090 pp 983089983091983096983097ndash983089983091983097983091983089983097983097983097
[983091983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091983091] S Reeve L Delbridge A Cohen and P Crummer ldquootalthyroidectomy Te preerred option or multinodular goiterrdquo Annals of Surgery vol 983090983088983094 no 983094 pp 983095983096983090ndash983095983096983094 983089983097983096983095
[983091983092] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and New
Zealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983091983093] H Gibelin M Sierra D Mothes et al ldquoRisk actors or recur-rentnodulargoiterafer thyroidectomy or benigndisease case-control study o 983090983092983092 patientsrdquo World Journal of Surgery vol 983090983096no 983089983089 pp 983089983088983095983097ndash983089983088983096983090 983090983088983088983092
[983091983094] K ekin S Yilmaz N Yalcin et al ldquoWhat would be lef behindi subtotal thyroidectomy were preerred instead o total thy-roidectomyrdquo Te American Journal of Surgery vol 983089983097983097 no 983094pp 983095983094983093ndash983095983094983097 983090983088983089983088
[983091983095] A Gerard S Poncin B Caetano et al ldquoIodine de1047297ciency indu-ces a thyroid stimulating hormone-independent early phase o microvascular reshaping in the thyroidrdquo Te American Journal of Pathology vol 983089983095983090 no 983091 pp 983095983092983096ndash983095983094983088 983090983088983088983096
[983091983096] O Tomusch C Sekulla and H Dralle ldquoIs primary totalthyroidectomy justi1047297ed in benign multinodular goiter Resultso a prospective quality assurance study o 983092983093 hospitals offeringdifferent levels o carerdquo Chirurg vol 983095983092 no 983093 pp 983092983091983095ndash983092983092983091 983090983088983088983091
[983091983097] J K Harness C H Organ Jr and N W Tompson ldquoOperativeexperience o US general surgery residents in thyroid andparathyroid diseaserdquo Surgery vol 983089983089983096 no 983094 pp 983089983088983094983091ndash983089983088983095983088983089983097983097983093
[983092983088] H Dralle C Sekulla K Lorenz M Brauckhoff and AMachens ldquoIntraoperative monitoring o the recurrent laryngealnerve in thyroid surgeryrdquo World Journal of Surgery vol 983091983090 no983095 pp 983089983091983093983096ndash983089983091983094983094 983090983088983088983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 47
983092 Journal o Tyroid Research
seen in 983089983091983093 o group 983089 patients in our study representing anonstatistically signi1047297cant difference rom the previous Sgroup Germane to this 1047297nding Barczynski et al remark that transient hypoparathyroidism ollowing in an erawhere parathyroid autotransplantation is common should be
viewed as a sequel rather than a complication [983089983093]
Te technique o reoperative thyroid surgery is clearly important when analysing complications Farrag and col-leagues have recently promulgated an algorithm or sae andeffective thyroid bed surgery or malignancy although many aspects can be readily extrapolated to the benign sphereas well [983093] Te principle tenets o the algorithm includepreoperative high-resolution ultrasound examination pre-operative vocal old examination by 1047297breoptic laryngoscopyand routine nerve identi1047297cation that should be acilitatedby the use o intraoperative nerve monitoring (IONM)Several o these attributes are endorsed by internationalthyroid surgery guidelines [983089983094] Additionally Menegaux etal recommend a lateral approach to the thyroid bed withdivision o the inrahyoid musculature in an effort to avoid1047297brous tissue surrounding the thyroid remnant [983089983095]
emerged as an alternativeto S initially in the malig-nant domain Clark embraced the technique or managemento well-differentiated thyroid cancer and demonstrated thesaety o the technique and low complication rate [983089983096] It isrecommended as the operation o choice in all current treat-ment guidelines or thyroid cancer [983089983097] Te purported ben-e1047297ts o a total gland resection in thyroid cancer include theremoval o the primary tumour elimination o any potentialcontralateral disease and acilitation o postoperative RAIablation g surveillance and ultrasound scanning o thethyroid bed [983090983088] Tese bene1047297ts are not present when dealingwith benign disease Proponents o a subtotal resection claima reduced rate o RLN injury and hypoparathyroidism andassert that the majority o thyroid malignancies detectedortuitously on 1047297nal histopathology are o limited clinicalsigni1047297cance Furthermore i recurrences do occur they canbe managed surgically when indicated with less morbidity than i total thyroidectomy was perormed on all cases o thyroid malignancy at the outset [983090983088]
Numerous publications have since established the low morbidity o the extracapsular procedure Mishra et aldemonstrated an 983088983096 permanent RLN rate and 983089983094 per-manent hypoparathyroidism rate whilst Muller et al ounda 983088983097 rate or both morbidities [983090983089 983090983090] Many other studiescon1047297rmed similar 1047297ndings [983090983091ndash983090983093] Serpell and Phan ound a
permanent RLN palsy rate o 983088983091 and hypoparathyroidismrate o 983089983096 and concluded that can be perormed saely in a standard endocrine surgical unit with low complicationrates matching world centres o excellence [983090983094] Documentedhigh rates o incidental thyroid malignancy orti1047297ed thegrowing argument in avour o total thyroidectomy Ourpresent study revealed an incidental papillary microcarci-noma rate o 983092983090983090 that was equally distributed within thetwo groups We have previously published a 983091 rate o occult carcinoma somewhat lower than other subsequently published series rom Bron and OrsquoBrien (983092983094) [983089983092] Colak et al (983095983092) [983090983095] and Levin et al (983090983090) [983095] Menegauxet al determined that thyroid cancer might be ound in
approximately 983089983088 o reoperative cases or recurrent goitreeven though the preceding operation was perormed orbenign disease [983090983096] By the same token ezelman et al oundthat within a cohort o patients diagnosed with thyroid cancerollowing a subtotal thyroidectomy completion resection o the thyroid remnants yielded papillary microcarcinoma in
983093983090983094 [983089]Recurrence o goitre and ailure to prevent hypothy-
roidism have urther weakened the validity o subtotal thy-roidectomy as a surgical strategy or benign thyroid diseaseGoitre recurrence rates associated with S range rom983095983089 to 983092983091 [983089 983089983090] Te incidence o recurrence appearsdirectly related to the length o surveillance [983090983097 983091983088]mdashalthough our study and others have ound that a peak incidence o recurrence occurs at approximately 983089983091 to 983089983093 yearsrom the primary operation [983091983089] a 983092983091 recurrence rate may be observed with up to 983091983088 years o ollowup [ 983089983090] Many have noted the ailure o thyroxine suppression to preventrecurrence with a 983089983092983093 recurrence rate demonstrated in
the study by Pappalardo et al in spite o drug prophylaxis[983090983092] Conversely thyroxine replacement is not obviated in983091983094983094ndash983092983095983096 o subtotal thyroidectomy procedures and henceshould not be used to justiy practice o the procedure [983091983090]
Te undamental difficulty with S is allotting a tissueremnant unaffected by the nodular process Colak et alhighlighted the predicament o leaving healthy tissue intactin patients with huge goitres where the nodular diseaseofen reaches the dorsal capsule [983090983095] Tere is generally anincreasing recognition that the nodular transormations inmultinodular goitre inherently encompass the entire glandhence although S permits a reduction in the bulk o dis-ease it is not an optimal treatment [983091983091] Moreover the rem-
nant posterolateral tissue ofen extends into the retrotrachealand retrooesophageal areas where recurrence portends early pressure symptoms that may require technically demandingreoperative surgery [983091983092] We have previously shown thatmultinodular goitre is a highly signi1047297cant risk actor orrecurrence in benign thyroid disease where a less than totalthyroidectomy has been perormed [983091983093] Recently a novelstudy by ekin et al demonstrated that Ki-983094983095 prolierationmarker levels in remnant S thyroid tissue were signi1047297-cantly higher than in normal thyroid tissue [983091983094] Tey oundthat despite the relatively small size o remnant micronodulesthe high Ki-983094983095 levels re1047298ect high cellular mitotic activity and ensuing signi1047297cant goitrogenic potential o remnant
tissue Furthermore the existence o micronodules in theremnant specimens harbouring similar prolieration index
values as the main thyroid specimen establishes the homoge-neous nature o the parenchymal alteration in multinodulargoitre Gerard et al postulate that recurrent goitres resistantto thyroxine suppression may arise due to the polyclonalnature o nodule ormation involving goitrogenic insulin-likegrowth actors and their binding proteins Tese may occurseparate to iodine de1047297ciency related mechanisms o goitredevelopment based on SH and vascular-endothelial growthactor (VEGF) angiogenesis [983091983095]
Finally the ofen-overlooked denominator and perhapsmost crucial determinant o morbidity is surgical technique
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 57
Journal o Tyroid Research 983093
Tomusch et al commented on the importance o ldquowell-trained surgeons using an appropriate intraoperative tech-niquerdquo in the perormance o total thyroidectomy [983091983096] Teability to perorm a sae total thyroidectomy is clearly adirect derivative o onersquos surgical training and experience[983091983097] Te evolution o more dedicated endocrine surgery
training programmes and specialized units combined withtechnological re1047297nements such as IONM is likely to urtherenhance the sae implementation o or both malignantand benign thyroid disease alike [983092983088]
5 Conclusion
Reoperative surgery or recurrent benign thyroid disease isassociated with increased morbidity when preceded by initialsubtotal thyroidectomy Associated high levels o recurrenceand increased permanent RLN injury and hypoparathy-roidism rates seen in this setting call or the abandonmento this procedure in avour o total thyroidectomy It should
be noted however that successul reoperative thyroid surgery perormed by experienced well-trained surgeons may beaccomplished with low overall rates o morbidity
Conflict of Interests
Te authors disclose no real or potential con1047298ict o interests
References
[983089] S ezelman I Borucu Y Senyurek F unca and erziogluldquoTe change in surgical practice rom subtotal to near-total ortotal thyroidectomy in the treatment o patients with benign
multinodular goiterrdquo World Journal of Surgery vol983091983091no 983091pp983092983088983088ndash983092983088983093 983090983088983088983097
[983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091] ldquoechnique o thyroidectomyrdquo in Endocrine Surgery Principlesand Practice H Gibelin Desurmont J L Kraimps and J GH Hubbard Eds Springer SpecialistSurgery Series chapter 983089983090pp 983089983094983091ndash983089983095983089 Springer London UK 983089st edition 983090983088983088983097
[983092] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092
no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983093] Y Farrag N Agrawal S Sheth et al ldquoAlgorithm or saeand effective reoperative thyroid bed surgery or recurrentpersistent papillary thyroid carcinomardquo Head and Neck vol 983090983097no 983089983090 pp 983089983088983094983097ndash983089983088983095983092 983090983088983088983095
[983094] D B Wilson E D Staren and R A Prinz ldquoTyroid reopera-tions indications and risksrdquo Te American Surgeon vol 983094983092 no983095 pp 983094983095983092ndash983094983095983097 983089983097983097983096
[983095] K E Levin A H Clark Q Duh M Demeure A E Sipersteinand O H Clark ldquoReoperative thyroid surgeryrdquo Surgery vol 983089983089983089no 983094 pp 983094983088983092ndash983094983088983097 983089983097983097983090
[983096] D J erris S S Khichi S K Anderson and M W SeybtldquoReoperative thyroidectomy or benignthyroiddisease the case
or phasing out subtotal thyroidectomyrdquo Laryngoscope vol 983089983089983097no 983089 p S983096983097 983090983088983088983097
[983097] J H Leevre C resallet L Leenhardt C Jublanc J Chigotand F Menegaux ldquoReoperative surgery or thyroid diseaserdquoLangenbeckrsquos Archives of Surgery vol 983091983097983090 no 983094 pp 983094983096983093ndash983094983097983089983090983088983088983095
[983089983088] Chao L Jeng J Lin and M Chen ldquoReoperative thyroid sur-geryrdquo World Journal of Surgery vol 983090983089 no 983094 pp 983094983092983092ndash983094983092983095 983089983097983097983095
[983089983089] S Reeve L Delbridge P Brady P Crummer and C SmythldquoSecondary thyroidectomy a twenty-year experiencerdquo World Journal of Surgery vol 983089983090 no 983092 pp 983092983092983097ndash983092983093983091 983089983097983096983096
[983089983090] J Rojdmark andJ Jarhult ldquoHigh long term recurrence rate afersubtotal thyroidectomy or nodular goitrerdquo European Journal of Surgery vol 983089983094983089 no 983089983088 pp 983095983090983093ndash983095983090983095 983089983097983097983093
[983089983091] A D Katz and D Bronson ldquootal thyroidectomy Te indica-tions and results o 983094983091983088 casesrdquo Te American Journal of Surgery vol 983089983091983094 no 983092 pp 983092983093983088ndash983092983093983092 983089983097983095983096
[983089983092] L P Bron and C J OrsquoBrien ldquootal thyroidectomy or clinically benign disease o the thyroid glandrdquo Te British Journal of Surgery vol 983097983089 no 983093 pp 983093983094983097ndash983093983095983092 983090983088983088983092
[983089983093] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983089983094] ldquoBritish Tyroid Association Guidelines or the managemento thyroid cancer in adultsrdquo 983090983088983089983090 httpwwwbritish-thyroid-associationorgGuidelines
[983089983095] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983089983096] O H Clark ldquo otal thyroidectomy Te treatment o choice orpatients with differentiated thyroid cancerrdquo Annals of Surgery vol 983089983097983094 no 983091 pp 983091983094983089ndash983091983095983088 983089983097983096983090
[983089983097] DS Cooper G M Doherty BR Haugen etal ldquoRevised Amer-ican thyroid association management guidelines or patientswith thyroid nodules and differentiated thyroid cancerrdquo Ty-roid vol 983089983097 no 983089983089 pp 983089983089983094983095ndash983089983090983089983092 983090983088983088983097
[983090983088] M Friedman and H Ibrahim ldquootal versus subtotal thy-roidectomy arguments approaches and recommendationsrdquoOperative echniques in Otolaryngology vol 983089983091 no 983091 pp 983089983097983094ndash983090983088983090 983090983088983088983090
[983090983089] P Muller S Kabus E Robens and F Spelsberg ldquoIndicationsrisks and acceptance o total thyroidectomy or multinodularbenign goiterrdquo Surgery oday vol 983091983089 no 983089983089 pp 983097983093983096ndash983097983094983090 983090983088983088983089
[983090983090] A Mishra A Agarwal G Agarwal and S K Mishra ldquootalthyroidectomy or benign thyroid disorders in an endemicregionrdquo World Journal of Surgery vol 983090983093 no 983091 pp 983091983088983095ndash983091983089983088983090983088983088983089
[983090983091] N Korun C Asci Yilmazlar et al ldquootal thyroidectomy orlobectomy in benign nodular disease o the thyroid changingtrends in surgeryrdquo International Surgery vol 983096983090 no 983092 pp 983092983089983095ndash983092983089983097 983089983097983097983095
[983090983092] G Pappalardo A Guadalaxara F M Frattaroli G Illomei andP Falaschi ldquootal compared with subtotal thyroidectomy inbenign nodular disease personal series and review o publishedreportsrdquo European Journalof Surgery vol 983089983094983092 no 983095 pp 983093983088983089ndash983093983088983094983089983097983097983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 67
983094 Journal o Tyroid Research
[983090983093] D B de Roy van Zuidewijn I Songun J Kievit and C J vande Velde ldquoComplications o thyroid surgeryrdquo Annals of Surgical Oncology vol 983090 no 983089 pp 983093983094ndash983094983088 983089983097983097983093
[983090983094] J W Serpell and D Phan ldquoSaety o total thyroidectomyrdquo Australian and New Zealand Journal of Surgery vol 983095983095 no 983089-983090pp 983089983093ndash983089983097 983090983088983088983095
[983090983095] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and NewZealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983090983096] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983090983097] P E Anderson P R Hurley and P Rosswick ldquoConservativetreatment and long term prophylactic thyroxine in the preven-tion o recurrence o multinodular goiterrdquo Surgery Gynecology and Obstetrics vol 983089983095983089 no 983092 pp 983091983088983097ndash983091983089983092 983089983097983097983088
[983091983088] J L Kraimps R MarechaudD Gineste et al ldquoAnalysisand pre- vention o recurrent goiterrdquo Surgery Gynecology and Obstetrics
vol 983089983095983094 no 983092 pp 983091983089983097ndash983091983090983090 983089983097983097983091[983091983089] L Delbridge A I Guinea and S Reeveldquootal thyroidectomy
or bilateral benign multinodular goiter effect o changingpracticerdquo Archives of Surgery vol 983089983091983092 no 983089983090 pp 983089983091983096983097ndash983089983091983097983091983089983097983097983097
[983091983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091983091] S Reeve L Delbridge A Cohen and P Crummer ldquootalthyroidectomy Te preerred option or multinodular goiterrdquo Annals of Surgery vol 983090983088983094 no 983094 pp 983095983096983090ndash983095983096983094 983089983097983096983095
[983091983092] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and New
Zealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983091983093] H Gibelin M Sierra D Mothes et al ldquoRisk actors or recur-rentnodulargoiterafer thyroidectomy or benigndisease case-control study o 983090983092983092 patientsrdquo World Journal of Surgery vol 983090983096no 983089983089 pp 983089983088983095983097ndash983089983088983096983090 983090983088983088983092
[983091983094] K ekin S Yilmaz N Yalcin et al ldquoWhat would be lef behindi subtotal thyroidectomy were preerred instead o total thy-roidectomyrdquo Te American Journal of Surgery vol 983089983097983097 no 983094pp 983095983094983093ndash983095983094983097 983090983088983089983088
[983091983095] A Gerard S Poncin B Caetano et al ldquoIodine de1047297ciency indu-ces a thyroid stimulating hormone-independent early phase o microvascular reshaping in the thyroidrdquo Te American Journal of Pathology vol 983089983095983090 no 983091 pp 983095983092983096ndash983095983094983088 983090983088983088983096
[983091983096] O Tomusch C Sekulla and H Dralle ldquoIs primary totalthyroidectomy justi1047297ed in benign multinodular goiter Resultso a prospective quality assurance study o 983092983093 hospitals offeringdifferent levels o carerdquo Chirurg vol 983095983092 no 983093 pp 983092983091983095ndash983092983092983091 983090983088983088983091
[983091983097] J K Harness C H Organ Jr and N W Tompson ldquoOperativeexperience o US general surgery residents in thyroid andparathyroid diseaserdquo Surgery vol 983089983089983096 no 983094 pp 983089983088983094983091ndash983089983088983095983088983089983097983097983093
[983092983088] H Dralle C Sekulla K Lorenz M Brauckhoff and AMachens ldquoIntraoperative monitoring o the recurrent laryngealnerve in thyroid surgeryrdquo World Journal of Surgery vol 983091983090 no983095 pp 983089983091983093983096ndash983089983091983094983094 983090983088983088983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 57
Journal o Tyroid Research 983093
Tomusch et al commented on the importance o ldquowell-trained surgeons using an appropriate intraoperative tech-niquerdquo in the perormance o total thyroidectomy [983091983096] Teability to perorm a sae total thyroidectomy is clearly adirect derivative o onersquos surgical training and experience[983091983097] Te evolution o more dedicated endocrine surgery
training programmes and specialized units combined withtechnological re1047297nements such as IONM is likely to urtherenhance the sae implementation o or both malignantand benign thyroid disease alike [983092983088]
5 Conclusion
Reoperative surgery or recurrent benign thyroid disease isassociated with increased morbidity when preceded by initialsubtotal thyroidectomy Associated high levels o recurrenceand increased permanent RLN injury and hypoparathy-roidism rates seen in this setting call or the abandonmento this procedure in avour o total thyroidectomy It should
be noted however that successul reoperative thyroid surgery perormed by experienced well-trained surgeons may beaccomplished with low overall rates o morbidity
Conflict of Interests
Te authors disclose no real or potential con1047298ict o interests
References
[983089] S ezelman I Borucu Y Senyurek F unca and erziogluldquoTe change in surgical practice rom subtotal to near-total ortotal thyroidectomy in the treatment o patients with benign
multinodular goiterrdquo World Journal of Surgery vol983091983091no 983091pp983092983088983088ndash983092983088983093 983090983088983088983097
[983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091] ldquoechnique o thyroidectomyrdquo in Endocrine Surgery Principlesand Practice H Gibelin Desurmont J L Kraimps and J GH Hubbard Eds Springer SpecialistSurgery Series chapter 983089983090pp 983089983094983091ndash983089983095983089 Springer London UK 983089st edition 983090983088983088983097
[983092] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092
no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983093] Y Farrag N Agrawal S Sheth et al ldquoAlgorithm or saeand effective reoperative thyroid bed surgery or recurrentpersistent papillary thyroid carcinomardquo Head and Neck vol 983090983097no 983089983090 pp 983089983088983094983097ndash983089983088983095983092 983090983088983088983095
[983094] D B Wilson E D Staren and R A Prinz ldquoTyroid reopera-tions indications and risksrdquo Te American Surgeon vol 983094983092 no983095 pp 983094983095983092ndash983094983095983097 983089983097983097983096
[983095] K E Levin A H Clark Q Duh M Demeure A E Sipersteinand O H Clark ldquoReoperative thyroid surgeryrdquo Surgery vol 983089983089983089no 983094 pp 983094983088983092ndash983094983088983097 983089983097983097983090
[983096] D J erris S S Khichi S K Anderson and M W SeybtldquoReoperative thyroidectomy or benignthyroiddisease the case
or phasing out subtotal thyroidectomyrdquo Laryngoscope vol 983089983089983097no 983089 p S983096983097 983090983088983088983097
[983097] J H Leevre C resallet L Leenhardt C Jublanc J Chigotand F Menegaux ldquoReoperative surgery or thyroid diseaserdquoLangenbeckrsquos Archives of Surgery vol 983091983097983090 no 983094 pp 983094983096983093ndash983094983097983089983090983088983088983095
[983089983088] Chao L Jeng J Lin and M Chen ldquoReoperative thyroid sur-geryrdquo World Journal of Surgery vol 983090983089 no 983094 pp 983094983092983092ndash983094983092983095 983089983097983097983095
[983089983089] S Reeve L Delbridge P Brady P Crummer and C SmythldquoSecondary thyroidectomy a twenty-year experiencerdquo World Journal of Surgery vol 983089983090 no 983092 pp 983092983092983097ndash983092983093983091 983089983097983096983096
[983089983090] J Rojdmark andJ Jarhult ldquoHigh long term recurrence rate afersubtotal thyroidectomy or nodular goitrerdquo European Journal of Surgery vol 983089983094983089 no 983089983088 pp 983095983090983093ndash983095983090983095 983089983097983097983093
[983089983091] A D Katz and D Bronson ldquootal thyroidectomy Te indica-tions and results o 983094983091983088 casesrdquo Te American Journal of Surgery vol 983089983091983094 no 983092 pp 983092983093983088ndash983092983093983092 983089983097983095983096
[983089983092] L P Bron and C J OrsquoBrien ldquootal thyroidectomy or clinically benign disease o the thyroid glandrdquo Te British Journal of Surgery vol 983097983089 no 983093 pp 983093983094983097ndash983093983095983092 983090983088983088983092
[983089983093] M Barczy nski A Konturek A Hubalewska-Dydejczyk FGolkowski S Cichon and W Nowak ldquoFive-year ollow-upo a randomized clinical trial o total thyroidectomy versusdunhill operation versus bilateral subtotal thyroidectomy ormultinodular nontoxic goiterrdquo World Journal of Surgery vol 983091983092no 983094 pp 983089983090983088983091ndash983089983090983089983091 983090983088983089983088
[983089983094] ldquoBritish Tyroid Association Guidelines or the managemento thyroid cancer in adultsrdquo 983090983088983089983090 httpwwwbritish-thyroid-associationorgGuidelines
[983089983095] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983089983096] O H Clark ldquo otal thyroidectomy Te treatment o choice orpatients with differentiated thyroid cancerrdquo Annals of Surgery vol 983089983097983094 no 983091 pp 983091983094983089ndash983091983095983088 983089983097983096983090
[983089983097] DS Cooper G M Doherty BR Haugen etal ldquoRevised Amer-ican thyroid association management guidelines or patientswith thyroid nodules and differentiated thyroid cancerrdquo Ty-roid vol 983089983097 no 983089983089 pp 983089983089983094983095ndash983089983090983089983092 983090983088983088983097
[983090983088] M Friedman and H Ibrahim ldquootal versus subtotal thy-roidectomy arguments approaches and recommendationsrdquoOperative echniques in Otolaryngology vol 983089983091 no 983091 pp 983089983097983094ndash983090983088983090 983090983088983088983090
[983090983089] P Muller S Kabus E Robens and F Spelsberg ldquoIndicationsrisks and acceptance o total thyroidectomy or multinodularbenign goiterrdquo Surgery oday vol 983091983089 no 983089983089 pp 983097983093983096ndash983097983094983090 983090983088983088983089
[983090983090] A Mishra A Agarwal G Agarwal and S K Mishra ldquootalthyroidectomy or benign thyroid disorders in an endemicregionrdquo World Journal of Surgery vol 983090983093 no 983091 pp 983091983088983095ndash983091983089983088983090983088983088983089
[983090983091] N Korun C Asci Yilmazlar et al ldquootal thyroidectomy orlobectomy in benign nodular disease o the thyroid changingtrends in surgeryrdquo International Surgery vol 983096983090 no 983092 pp 983092983089983095ndash983092983089983097 983089983097983097983095
[983090983092] G Pappalardo A Guadalaxara F M Frattaroli G Illomei andP Falaschi ldquootal compared with subtotal thyroidectomy inbenign nodular disease personal series and review o publishedreportsrdquo European Journalof Surgery vol 983089983094983092 no 983095 pp 983093983088983089ndash983093983088983094983089983097983097983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 67
983094 Journal o Tyroid Research
[983090983093] D B de Roy van Zuidewijn I Songun J Kievit and C J vande Velde ldquoComplications o thyroid surgeryrdquo Annals of Surgical Oncology vol 983090 no 983089 pp 983093983094ndash983094983088 983089983097983097983093
[983090983094] J W Serpell and D Phan ldquoSaety o total thyroidectomyrdquo Australian and New Zealand Journal of Surgery vol 983095983095 no 983089-983090pp 983089983093ndash983089983097 983090983088983088983095
[983090983095] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and NewZealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983090983096] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983090983097] P E Anderson P R Hurley and P Rosswick ldquoConservativetreatment and long term prophylactic thyroxine in the preven-tion o recurrence o multinodular goiterrdquo Surgery Gynecology and Obstetrics vol 983089983095983089 no 983092 pp 983091983088983097ndash983091983089983092 983089983097983097983088
[983091983088] J L Kraimps R MarechaudD Gineste et al ldquoAnalysisand pre- vention o recurrent goiterrdquo Surgery Gynecology and Obstetrics
vol 983089983095983094 no 983092 pp 983091983089983097ndash983091983090983090 983089983097983097983091[983091983089] L Delbridge A I Guinea and S Reeveldquootal thyroidectomy
or bilateral benign multinodular goiter effect o changingpracticerdquo Archives of Surgery vol 983089983091983092 no 983089983090 pp 983089983091983096983097ndash983089983091983097983091983089983097983097983097
[983091983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091983091] S Reeve L Delbridge A Cohen and P Crummer ldquootalthyroidectomy Te preerred option or multinodular goiterrdquo Annals of Surgery vol 983090983088983094 no 983094 pp 983095983096983090ndash983095983096983094 983089983097983096983095
[983091983092] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and New
Zealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983091983093] H Gibelin M Sierra D Mothes et al ldquoRisk actors or recur-rentnodulargoiterafer thyroidectomy or benigndisease case-control study o 983090983092983092 patientsrdquo World Journal of Surgery vol 983090983096no 983089983089 pp 983089983088983095983097ndash983089983088983096983090 983090983088983088983092
[983091983094] K ekin S Yilmaz N Yalcin et al ldquoWhat would be lef behindi subtotal thyroidectomy were preerred instead o total thy-roidectomyrdquo Te American Journal of Surgery vol 983089983097983097 no 983094pp 983095983094983093ndash983095983094983097 983090983088983089983088
[983091983095] A Gerard S Poncin B Caetano et al ldquoIodine de1047297ciency indu-ces a thyroid stimulating hormone-independent early phase o microvascular reshaping in the thyroidrdquo Te American Journal of Pathology vol 983089983095983090 no 983091 pp 983095983092983096ndash983095983094983088 983090983088983088983096
[983091983096] O Tomusch C Sekulla and H Dralle ldquoIs primary totalthyroidectomy justi1047297ed in benign multinodular goiter Resultso a prospective quality assurance study o 983092983093 hospitals offeringdifferent levels o carerdquo Chirurg vol 983095983092 no 983093 pp 983092983091983095ndash983092983092983091 983090983088983088983091
[983091983097] J K Harness C H Organ Jr and N W Tompson ldquoOperativeexperience o US general surgery residents in thyroid andparathyroid diseaserdquo Surgery vol 983089983089983096 no 983094 pp 983089983088983094983091ndash983089983088983095983088983089983097983097983093
[983092983088] H Dralle C Sekulla K Lorenz M Brauckhoff and AMachens ldquoIntraoperative monitoring o the recurrent laryngealnerve in thyroid surgeryrdquo World Journal of Surgery vol 983091983090 no983095 pp 983089983091983093983096ndash983089983091983094983094 983090983088983088983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 67
983094 Journal o Tyroid Research
[983090983093] D B de Roy van Zuidewijn I Songun J Kievit and C J vande Velde ldquoComplications o thyroid surgeryrdquo Annals of Surgical Oncology vol 983090 no 983089 pp 983093983094ndash983094983088 983089983097983097983093
[983090983094] J W Serpell and D Phan ldquoSaety o total thyroidectomyrdquo Australian and New Zealand Journal of Surgery vol 983095983095 no 983089-983090pp 983089983093ndash983089983097 983090983088983088983095
[983090983095] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and NewZealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983090983096] F Menegaux G urpin M Dahman et al ldquoSecondary thy-roidectomy in patients with prior thyroid surgery or benigndisease a study o 983090983088983091 casesrdquo Surgery vol 983089983090983094 no 983091 pp 983092983095983097ndash983092983096983091 983089983097983097983097
[983090983097] P E Anderson P R Hurley and P Rosswick ldquoConservativetreatment and long term prophylactic thyroxine in the preven-tion o recurrence o multinodular goiterrdquo Surgery Gynecology and Obstetrics vol 983089983095983089 no 983092 pp 983091983088983097ndash983091983089983092 983089983097983097983088
[983091983088] J L Kraimps R MarechaudD Gineste et al ldquoAnalysisand pre- vention o recurrent goiterrdquo Surgery Gynecology and Obstetrics
vol 983089983095983094 no 983092 pp 983091983089983097ndash983091983090983090 983089983097983097983091[983091983089] L Delbridge A I Guinea and S Reeveldquootal thyroidectomy
or bilateral benign multinodular goiter effect o changingpracticerdquo Archives of Surgery vol 983089983091983092 no 983089983090 pp 983089983091983096983097ndash983089983091983097983091983089983097983097983097
[983091983090] A Koyuncu H S Dokmetas M uran et al ldquoComparison o different thyroidectomy techniques or benign thyroid diseaserdquoEndocrine Journal vol 983093983088 no 983094 pp 983095983090983091ndash983095983090983095 983090983088983088983091
[983091983091] S Reeve L Delbridge A Cohen and P Crummer ldquootalthyroidectomy Te preerred option or multinodular goiterrdquo Annals of Surgery vol 983090983088983094 no 983094 pp 983095983096983090ndash983095983096983094 983089983097983096983095
[983091983092] Colak Akca A Kanik D Yapici and S Aydin ldquootal versus subtotal thyroidectomy or the management o benignmultinodular goiter in an endemic regionrdquo Australian and New
Zealand Journal of Surgery vol 983095983092 no 983089983089 pp 983097983095983092ndash983097983095983096 983090983088983088983092
[983091983093] H Gibelin M Sierra D Mothes et al ldquoRisk actors or recur-rentnodulargoiterafer thyroidectomy or benigndisease case-control study o 983090983092983092 patientsrdquo World Journal of Surgery vol 983090983096no 983089983089 pp 983089983088983095983097ndash983089983088983096983090 983090983088983088983092
[983091983094] K ekin S Yilmaz N Yalcin et al ldquoWhat would be lef behindi subtotal thyroidectomy were preerred instead o total thy-roidectomyrdquo Te American Journal of Surgery vol 983089983097983097 no 983094pp 983095983094983093ndash983095983094983097 983090983088983089983088
[983091983095] A Gerard S Poncin B Caetano et al ldquoIodine de1047297ciency indu-ces a thyroid stimulating hormone-independent early phase o microvascular reshaping in the thyroidrdquo Te American Journal of Pathology vol 983089983095983090 no 983091 pp 983095983092983096ndash983095983094983088 983090983088983088983096
[983091983096] O Tomusch C Sekulla and H Dralle ldquoIs primary totalthyroidectomy justi1047297ed in benign multinodular goiter Resultso a prospective quality assurance study o 983092983093 hospitals offeringdifferent levels o carerdquo Chirurg vol 983095983092 no 983093 pp 983092983091983095ndash983092983092983091 983090983088983088983091
[983091983097] J K Harness C H Organ Jr and N W Tompson ldquoOperativeexperience o US general surgery residents in thyroid andparathyroid diseaserdquo Surgery vol 983089983089983096 no 983094 pp 983089983088983094983091ndash983089983088983095983088983089983097983097983093
[983092983088] H Dralle C Sekulla K Lorenz M Brauckhoff and AMachens ldquoIntraoperative monitoring o the recurrent laryngealnerve in thyroid surgeryrdquo World Journal of Surgery vol 983091983090 no983095 pp 983089983091983093983096ndash983089983091983094983094 983090983088983088983096
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
8202019 2318jkj57
httpslidepdfcomreaderfull2318jkj57 77
Submit your manuscripts at
httpwwwhindawicom
