Cystic Fibrosis and Endoscopic Sinus Surgery

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ORIGINAL ARTICLE

Cystic Fibrosis and Endoscopic Sinus Surgery

Relationship Between Nasal Polyposis and Likelihood of Revision Endoscopic SinusSurgery in Patients With Cystic Fibrosis

Scott Rickert, MD; Victoria E. Banuchi, MD; Joan D. Germana, MD; Michael G. Stewart, MD, MPH; Max M. April, MD

Objectives: To observe the extent of nasal polyposis en-doscopically in a cystic fibrosis population before the firstsurgicalintervention andto grade theextent usinga modi-fied Malm scale, to observe patients prospectively andrecord the need for revision endoscopic sinus surgery(ESS), and to compare this among the individual polypgrading groupings.

Design: Retrospective medical record review of datacol-lected prospectively.

Setting: Tertiary care hospital.

Patients: Forty-nine consecutive patients with a clini-cal preoperative diagnosis of cystic fibrosis and sinus-itis.

Main Outcome Measures: Using a modified Malmscale, the extent of polyps was prospectively graded into3 groups before the first surgical intervention. The num-ber of patients needing revision ESS and the mean time

to revision ESS were compared among the 3 groups.

Results: Forty-nine consecutive patients underwent ESSbetween 1992 and 2007. We used a 3-stage system for ex-tent of polyposis: 16 patients were noted to have no pol-yps (grade A), 14 hadmildpolyposis (grade B), and 19 hadextensive polyposis (grade C). During the study, 14 pa-tientsrequired revision surgery: 3 with mild polyps and11with extensive polyps. Mean time to revision surgery was

39.7 months for those with grade B and 23.8 months forthose with grade C. In the overall statistical analysis, therate of revision ESS was significantly different among the3 groups (P.001). In pairwise comparisons, there weresignificant differences between those with grades A and C(P.001) and between those with grades B and C (P=.04)anda trend towardsignificance between those with gradesAandB(P=.052). There were no complications from ESS.

Conclusion: Preoperative grading of nasal polyposis inpatients with cysticfibrosis canhelp assessthe future like-lihood of revision ESS.

Arch Otolaryngol Head Neck Surg. 2010;136(10):988-992

CYSTIC FIBROSIS (CF) IScaused by a mutation inthe CF transmembraneconductance regulatorgene on the long arm of

chromosome7. Thisdefect alters the trans-membrane passage of the chloride ionacross cell membranes, resulting in mul-tisystemic dysfunction that can lead to

chronic respiratory tract infections, pan-creatic insufficiency, andmalnutrition.1 Na-sal obstruction and chronic rhinosinusitisareotolaryngologicmanifestations of thedis-ease.2 Alteredviscoelasticpropertiesof mu-custhat resultin bacterialcolonization, par-ticularly of Pseudomonas aeruginosa, are

thought to contribute to the impaired cili-aryclearanceseen in patients with CF.2 Thisciliary clearance dysfunction can result inobstruction of the sinus ostia, leading tochronic sinusitis and mucosaledema, lead-ing to sinonasal polyposis and nasal ob-struction. However,notallpatientswith CFdevelop nasal polyposis.

There are several reasons to considerendoscopic sinus surgery (ESS) in pa-tientswith CF. Theprevalenceof sinusdis-

ease in this population approaches 100%accordingto a combination of signs, symp-toms, and radiologic findings3: more than90% of patients with CF show radiologicevidence of sinus mucosal disease.4 Sino-nasal disease can lead to significant mor-bidity in these patients, placing them at anincreased risk for pneumonia, acute ex-acerbations, and frequent hospitaliza-tions.5 Approximately 20% to 25% of pa-tients with CF require sinus surgical

CME available online atwww.jamaarchivescme.comand questions on page 944

Author Affiliations: Departmentof OtorhinolaryngologyHeadand Neck Surgery, Weill CornellMedical College,New YorkPresbyterian Hospital,New York, New York(Drs Rickert, Banuchi, Stewart,and April); and Cystic FibrosisCenter at Schneider ChildrensHospital, New Hyde Park,New York (Dr Germana).

(REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/VOL 136 (NO. 10), OCT 2010 WWW.ARCHOTO.COM988

2010 American Medical Association. All rights reserved.wnloaded From: http://archotol.jamanetwork.com/ on 06/21/2012


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intervention at some point.6 In addition, surgical treat-ment of the paranasal sinuses is often recommended asa preventive and preparatory measure for lung trans-plant candidates because a major cause of death after lungtransplantation is pneumonia resulting from P aerugi-nosa, whose origin is likely to be the paranasal sinuses.3

Endoscopicsinus surgery has been shown to besafe andeffectivefor the treatment of paranasal sinus disease in pa-tients with CF.7-12 As treatments for CF continue to im-prove, patients are living longer and quality-of-life issuesare coming more to the forefront. Life expectancy hasdra-matically improved during the past 40 years. In 1969, theaverage age of survival was 14 years. By 1987, the meanage of survival was 23 years, and by 2006, the mean sur-vival age had increased further to 37 years.

Although several studies3,9-11,13-18 haveaddressedsymp-tom outcomes after sinus surgery in CF, it is a chronic dis-ease of mucociliary transport, andeven after successful sur-gery, infection, obstruction, and polyposis can recur.Furthermore, the number of study participants and thelengthof follow-upin previousstudies of sinus surgery forCF are limited. These facts lead some surgeons to ques-tion whether ESS has long-term benefits based on the un-derlying disease and the perception of eventual failure.

It is known that computed tomographic (CT) sever-ity (ie, extent of mucosal disease) does not correlate withsymptom severity in patients with chronic rhinosinusi-tis.19,20 Almost all patients with CF show CT abnormali-ties,21 but not all have symptoms of sinusitis or requireESS. Medical and surgical treatment of sinusitis in pa-tients with CF is based on symptoms and overall status,including pulmonary status andinfection frequency. Find-ings from CT may remain abnormal after sinus surgery,even when symptoms, pulmonary status, and infectionfrequency are all improved.22 Although CT severity, and,therefore, the extent of mucosal disease, is not associ-ated with symptom severity at any point in time, we setout to determine whether anatomical severityin thiscase, the presence and extent of nasal polyposismightpredict future outcomes after sinus surgery. If so, thatprognostic information could be helpful to physicians inthe management of this challenging disease.

METHODS

A retrospective medical record review was performed of con-secutive patients with CF and chronic sinusitis requiring sur-

gery seen between 1992 and 2007. The inclusion criteria werea confirmed clinical preoperative diagnosis of CF and chronicsinusitis requiring surgery.

All surgical procedures in this series were performed by asingle experienced surgeon (M.M.A.). The same indications forsurgery were used throughout the study and were based onsymptoms and overallstatus, including pulmonary status, ratherthan on endoscopic or CT findings. Surgical intervention wasperformed after conservative medical measures were ex-hausted. Conservative medical measures included long-termnasal corticosteroid treatment, nasal saline use, and multiplecourses of oral antibiotics, as individually determined by oneof us (M.M.A.), frequently in a culture-directed manner. Mostof these patients had symptoms of nasal obstruction, nasal dis-charge, and postnasal drip. Less common symptoms includedheadache and facial pain. Nasal obstruction and the extent ofmucosal nasal disease were evaluated by CT. There were nonoted significant discrepancies between CT/endoscopic find-ings and symptoms because many patients with CF presentedwith similar symptoms of nasal discharge, nasal obstruction,and postnasal drip. Although there was a range in the severityof the symptoms, each patient underwent surgical interven-tion only after maximal medical intervention failed to im-prove his or her individual symptoms. Given the young age atpresentation of this patient population, none of the patientshad

truly adapted to their symptoms. The same surgical technique(including the use of powered instrumentation) was usedthroughout this series. Most patients received a 2- to 3-weekcourse of culture-directed oral antibiotics postoperatively. Nopatients had catheters placed in the maxillary sinus for irriga-tion.23 Indications for revision surgery were similar to initialindicationsfor surgical intervention. Those who underwent pre-vious surgical intervention and either continued to have symp-toms or their preoperative symptoms recurred during postop-erative follow-up were treated with conservative medicalmanagement as stated previously herein. These patients pro-ceeded to revision surgery only after medical measures failedto improve their symptoms.

Rigid endoscopic nasal examination was performed beforethe first surgery, and the degree of nasal polyposis was graded

accordingto a modified Malm scale24

: grade A, no polyps; gradeB, mild polypsnot causing nasal obstruction or a solitary polypfrom the antrum; or grade C, extensive nasal polyposis caus-ing nasal obstruction (Figure). All office visits were also per-formed by the same physician (M.M.A.), with consistent medi-cal record documentation. Clinical data were extracted fromthe medical record, specifically, demographic data, initial stageof polyposis, and dates of surgery.

Statistical analysis comparing the need for revision surgeryby polyp stage was performed using the 2 test for trend, andthen individual pairwise comparisons were performed using astandard2 test. Means were compared usingthe t test or 1-way

A B C

Figure. Computed tomographic images of the modified Malm scale: grade A, minimal polyps and medialization of the lateral nasal wall (A); grade B, moderatepolyps but no nasal obstruction (B); and grade C, extensive nasal polyps with nasal obstruction (C).




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analysisof variance.Statistical significant was set at P .05. TheWeill Cornell Medical College institutional review board ap-proved this study.

RESULTS

We identified 49 patients with CF who underwent ESSbetween 1992 and 2007. These patients underwent 77ESS procedures. There were 22 males (45%) and 27 fe-males (55%), and mean age at first surgical interventionwas 10.8 years (range, 2-39 years). Four of the 49 pa-tients had had a single previous surgical intervention ata different institution and subsequently had further sur-gical interventions as part of this series. Of these 4 pa-tients, 1 was noted to have a limited polypectomy withrevision surgery within 1 year. The other 3 patients hadrevision surgery 2, 4, and 6 years after their initial sur-gery at an outside institution. Two of these patients hadextensive polyposis, and 1 had moderate polyposis. Noneof these patientshad multiple operations before thisstudy.

Mean total follow-up was 7.3 years (range, 1.3-15.0years). Seventy-seven separate ESS procedures were per-formed, and there were no major complications, such asorbital injury or cerebrospinal fluid leak. During follow-up, 3 patients died of complications associated with CF,and 1 patient received a lung transplant. The 3 deathswere patients who did not have any revision sinus sur-gery and were observed for 5, 7, and 9 years. The lungtransplant patient (grade B) had 1 revision surgery be-fore transplantation and had none for 4 years after.

Regarding polyp stage just before surgical interven-tion, 16 patients (33%) hadgrade A (nopolyps), 14 (29%)had grade B (moderate nonobstructing polyps), and 19(39%) had grade C (extensive polyposis). Mean age at

first surgical intervention was as follows: grade A pa-tients, 11.4 years; grade B patients, 11.5 years; and gradeC patients, 9.7 years. These differences were not signifi-cant (P =.64)

Fourteen patients (29%) required revision ESS dur-ing follow-up; 9 (64%) were male and 5 (36%) were fe-male. We compared the rate of revision surgery by ini-tialpolypstage. None of the patients without polyps(gradeA) required revision surgery (mean follow-up, 6.0 years).Three of 14 patients (21%) with grade B polyps re-quired revision surgery (mean follow-up, 8.7 years), and

11 of 19 patients (58%) with grade C polyp disease re-quired revision surgery (mean follow-up, 7.8 years). Thecomparison between all groups wassignificant (2=14.48,P .001). In pairwise comparisons between groups, therewere significant differences between those with gradesA and C (2=13.508, P .001) and between those withgradesB andC (2=4.388, P =.04). There was a trend to-ward significance between those with grades A and B(2=3.81, P =.052).

Revision surgery details are summarized in theTable.Fourteen patients underwent 28 revision ESS proce-dures, for a mean of 2 revision procedures per patient.Theonlypatients requiring more than 1 revision hadgradeC polyps at initial surgery. Mean time to revision sur-gery for all the patients was 27.1 months. Patients withgrade B polyps hadrevision surgery a mean of 39.7 monthsafter initial surgery, and those with grade C polyps hadrevision surgery at a mean of 23.8 months. This differ-ence was not significant (P =.25).

COMMENT

Previous studies7-12 have shown that ESS is safe and ef-fective for the treatment of paranasal sinus disease in pa-tients with CF. Many studies addressing symptom out-comes after sinus surgery haveshown good results.3,9-11,13-18

In fact, one study7 advocated aggressive sinus surgery inpatients with complete nasal obstruction caused by na-sal polyposis. Another study17 showed a reduced need forhospital stays in the 6 months after ESS.

The only outcome addressed in the present study wasthe need for revision surgery. In CF, this is an impor-tant outcome because mucosal problems are long-term,and minimizing the number of procedures and associ-ated risk is an important consideration. Note that al-

though this is technically a retrospective review, the datawerecollected prospectively and treatmentprotocols wereconsistent throughout, with the same experienced sur-geon. We also report a long fo3llow-up period.

We used a modified polyp grading system during thestudy, so it is difficult to comparepolyp severity with thatof other studies. However, the overall prevalence of pol-yps in patients with CF has been reported to vary from36% to 57%.1,25We report a higher overall prevalence ofendoscopically diagnosed polyps (67%), but this samplecomprised patients who underwent sinus surgery, not anentirepopulation of patientswith CF.So thehigher preva-lence in the present series is not surprising.

The overall rate of revisionsurgery in the present study

was lower than anticipated(30%).In patientswith mod-erate or severe polyposis, the rate of revision surgery was42%, which is slightly below the reported rates of 50%by Rowe-Jones and Mackay18 and 58% by Yung et al.25

Some researchers have reported overall rates of revisionsurgery as high as 72%.23 We also found that polyp se-verity at initial surgery wasstrongly predictive of the needfor revision surgery, with patients with more extensivepolyps requiring revision surgery more frequently. How-ever, even in the group with the most extensive polyp-osis, the revision rate, with follow-up of almost 8 years,

Table. Modified Malm Polyp Scale Comparing RevisionESS Among Grades, Total Revision ESS Procedures,and Time Between Procedures

PolypGradea

Patients, No.

Total RevisionESS Procedures,

No.

Time BetweenProcedures,

Mean (SD), moAll

(n=49)

RevisionESS

(n=14)

A 16 0 0 NA

B 14 3 3 39.7 (22.3)C 19 11 25 23.8 (19.4)

Abbreviations: ESS, endoscopic sinus surgery; NA, not applicable.a Classifications of the modified Malm scale: grade A, minimal polyps and

medialization of the lateral nasal wall; grade B, moderate polyps but no nasalobstruction; and grade C, extensive nasal polyps with nasal obstruction.




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was 58%. This compares favorably with the 75% revisionrateof severe nasal polyposisby Rowe-Jones andMackay.18

As expected,in this group the time to revision surgery wasalso shortest. Overall, these rates and frequencies of revi-sion surgery are probably lower than mighthave been pre-dicted because some authors have discussed the possibil-ity of yearly sinus surgery in patients with CF and aneventual revision rate of almost 100%.

In the present series, patients with minimal polyp dis-

ease who underwent ESS did not require revision sinussurgery during mean follow-up of 6 years. The differ-ences between groups of polyp severity were signifi-cant, which is consistent with other studies. One study26

found that CT findings are a significant predictor of theneed for revision sinus surgery, with more significant dis-ease on CT (ie, higher Lund-McKay scores) being asso-ciated with a higher rate of revision surgery. However,CT shows paranasal sinus abnormalities in most pa-tients with CF,21 and one study22 comparing CT per-formed preoperatively and postoperatively showed no sig-nificant difference, making CT a poor measureof outcome.Other studies have shown that endoscopic examinationseverity is correlated with CT severity measured using

the Lund-McKay or other CT staging systems,19

whichmakes clinical sense because endoscopic examination andCT assess mucosal disease.

Two major studies of ESS in patients with CF, one byRowe-Jones and Mackay18 and one by Yung et al,25 haveexamined similar issues. Rowe-Jones andMackay noted 46patientswith a mean follow-up of 26 months. Most of theirpatients were adults, with a mean age of 23 years at firstsurgical intervention. They noted a 50% chance of need-ing revision ESS during follow-up. The present study hassimilarnumbersof patientsbut differsin patientage at sur-gical intervention(10.8vs23 years)andfollow-up(7.3 yearsvs 28 months). Yung et al had fewer patients at presenta-tion (n=23) and surgical intervention (n=12). Their age

at first surgical intervention was8 years, similar to the pres-ent study, with a mean follow-up of 4 years.The present study, therefore, yields 3 major advan-

tages over previous studies. First, the larger population(49 surgical patients) compared favorably with the 46 pa-tients of Rowe-Jones and Mackay18 and the 23 patientsof Yung et al.25 Second, the present study has a muchyounger initial age at intervention than does the studyby Rowe-Jones and Mackay (10.8 vs 23 years) but is simi-lar to that in the study by Yung et al (10.8 vs 8 years),making it the largest study of its kind in the pediatric CFpopulation. Third, the extended follow-up of 7.3 yearsis significantly longer than the 28 months in the studyby Rowe-Jones and Mackay and 4 years in the study by

Yung et al. These 3 separate points strengthen the con-clusions of this study and make it a unique contributionto the literature.

We report no complications after ESS in the presentseries, which is lower than in some other studies12 butconsistent with series of ESS for patients without CF. Asin this series, ESS in patients with CF is usually per-formed in children, and there are no reports of adverseeffects of ESS on facial growth.27

In summary, we found that the extent of polyposis atthe time of initial surgery predicted the need for future

revision surgery. This might seem obvious or expected,but in fact, it is an important finding and not necessarilyintuitive. There is a range of severity of sinus involve-ment in patients with CF and, in all cases, patients haveabnormal mucosa before and after surgery. So, it is notnecessarily expected that the severity of mucosal dis-ease would indicate the need for more frequent surgery.And, in this series, as in many others, patients under-went surgery based on symptom severity only. Al-

though CT severity might not accurately predict symp-toms at the time, other series (in patients without CF)19,20

have found that CT severity can predict future out-comes. A plausible explanation for that finding is thatthe extent of mucosal disease or number of sinuses in-volved might be a manifestation of the underlying bur-den of disease or the patients intrinsic inflammatory re-sponse, and, therefore, greater CT severity and mucosaldisease burden would predict future outcomes, such asthe need for revision surgery.

The present study also found that with several years offollow-up, the overall revision rate was not as high as ex-pected per previous studies.18,25 This implies that thor-ough ESS does not always result in prompt disease recur-

rence and the need for revision surgery. Furthermore,because revision surgery was performed when symptoms(and overall status) worsened, that meansthat ESS was ef-fective at improving sinonasal symptoms and overall sta-tus for long periods. These periods between surgical pro-cedures were shorter in many patients with extensivepolyposis but not in all patients, and this ability to prog-nosticate could be helpful to patients and physicians.

One weakness of this study is its retrospective na-ture, although the treatments were standardized through-out. In addition, the nature of the data collection meansthat many variables that would be of interest for furtheranalysis, such as pulmonary function data, presence ofcomorbid conditions (such as laryngopharyngeal re-

flux), microbiology of sinusitis, and possibly genotype,were unavailable. The strengths of the study include thestandardized treatment protocol, with only 1 surgeon;the large sample (49 patients) undergoing ESS, one ofthe largest studies of sinus surgery in the CF literature(and in the pediatric CF literature); and consistent, goodfollow-up.

In conclusion, in patients with CF, preoperative grad-ing of nasal polyposis at the initial surgical interventioncan help predict the future need for revision ESS and theinterval between revision surgical procedures.

Submitted for Publication: May 28, 2009; final revisionreceived March 26, 2010; accepted June 1, 2010.

Correspondence: Max M. April, MD, Department of Oto-rhinolaryngologyHead and Neck Surgery, Weill Cor-nell Medical College, New YorkPresbyterian Hospital,1305 York Ave, Fifth Floor, New York, NY 10021([email protected]).Author Contributions: Drs Rickert, Banuchi, Germana,and April had full access to all the data in the study andtake responsibility for the integrity of the data and theaccuracy of the data analysis. Study concept and design:Rickert, Banuchi, and April. Acquisition of data: Rickert,Banuchi, Germana, and April. Analysis and interpreta-




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tion of data: Rickert, Germana, Stewart, and April. Draft-ing of the manuscript: Rickert, Banuchi, and Stewart. Criti-cal revision of the manuscript for important intellectualcontent: Rickert, Germana, Stewart, and April. Statisti-cal analysis: Rickert and Stewart. Administrative, techni-cal, and material support: Banuchi, Germana, and Stew-art. Study supervision: Germana, Stewart, and April.Financial Disclosure: None reported.Previous Presentation: This study was presented at the

American Society of Pediatric Otolaryngology meeting;May 4, 2008; Orlando, Florida.

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Cystic Fibrosis and Endoscopic Sinus Surgery