9

Best Practice & Research Clinical GastroenterologyVol. 20, No. 5, pp. 925e940, 2006

doi:10.1016/j.bpg.2006.03.011available online at http://www.sciencedirect.com

Minimally invasive techniques for oesophageal

cancer surgery

Simon Law* MS, MB, BChir, MA (Cantab), FRCSEd, FACS, FCSHK, FHKAM

Professor of Surgery

Department of Surgery, University of Hong Kong Medical Centre, Queen Mary Hospital, Hong Kong SAR, China

Innovative minimally invasive surgical (MIS) techniques have been explored for the purpose ofoesophagectomy since the early 1990s, including various combinations of thoracoscopy, laparos-copy or laparoscopic-assisted methods, mediastinoscopy and open thoracotomy and laparot-omy. The myriad of surgical approaches implies a lack of consensus on which is superior. Likeopen surgery, it is perhaps more important to have a tailored approach for the individual patient.MIS oesophagectomy has been shown to be feasible, and at least equivalent postoperative mor-bidity and mortality rates to open surgical resection have been demonstrated. Selected serieshave achieved less blood loss, reduction in some postoperative complications, decrease in inten-sive care and hospital stay, and better preservation of pulmonary function. Clear proof ofsuperiority over conventional oesophagectomy methods however is not forthcoming since com-parisons were often made with unmatched patient cohorts, and a well conducted randomizedcontrolled trial has not been carried out. It is expected that with further improvements in in-strumentation and experience, these difficult procedures may become more accessible andwidely practised.

Key words: oesophageal neoplasm; oesophagectomy; minimally invasive surgery; postoperativemorbidity and mortality; survival.

INTRODUCTION

Minimally invasive surgery (MIS) has revolutionized surgical practice, and oesophagealsurgery is no exception. Many minimally invasive procedures dealing with diseases ofthe oesophagus have become well established and accepted by the surgical community,such as laparoscopic fundoplication for gastroesophageal reflux disease,1 thoracoscopic

* Address: Professor Simon Law, Department of Surgery, University of Hong Kong Medical Centre, Queen

Mary Hospital, 102 Pokfulam Road, Hong Kong SAR, China. Tel.: þ852 2855 4774; Fax: þ852 2819 4221.

E-mail address: slaw@hku.hk

1521-6918/$ - see front matter ª 2006 Elsevier Ltd. All rights reserved.

926 S. Law

oesophageal benign tumour resection,2 laparoscopic oesophageal myotomy with hemi-fundoplication for achalasia,3 and laparoscopic or thoracoscopic diverticulectomy for ep-iphrenic diverticulum.4 For these benign diseases, reducing the trauma of surgical accesshas definite advantages; immediate postoperative recovery is enhanced, and equivalentfunctional results can be obtained compared to open procedures.

For oesophageal cancer MIS methods potentially can be used for disease staging,and for oesophagectomy. Progress however has been slow, especially for oesophagec-tomy, primarily because of the technical complexities and uncertain benefits. Cuschieripioneered MIS oesophagectomy in the early 1990s using the thoracoscopicapproach.5e7 Since then many centres have attempted different MIS techniques intreating oesophageal cancer. The indications, the optimum methods, and their benefitsremain controversial. This review serves to summarize the current status of the use ofMIS in treating oesophageal cancer.

MINIMALLY INVASIVE STAGING TECHNIQUES

Thoracoscopy and laparoscopy have their advocates to stage oesophageal cancer.Thoracoscopic staging usually involves a right-sided approach, with opening of themediastinal pleura from below the subclavian vessels to the inferior pulmonary vein;lymph node sampling is then performed. Sometimes left sided-thoracoscopy is alsoperformed to sample lymph nodes at the aorto-pulmonary window. Laparoscopicstaging can include coeliac lymph node biopsy, collection of peritoneal fluid for cyto-logical examination, and the use of laparoscopic ultrasound for detecting liver metas-tases. In a study of 53 patients whose staging included conventional CT scan andendoscopic ultrasound (EUS), minimally invasive staging reassigned a lower stage in10 patients and a more advanced stage in seven patients (32.1%).8 The multi-institutionalstudy (CALGB 9380) investigated the use of combined thoracoscopy and laparoscopystaging in 113 patients, the strategy was feasible in 73% of patients. Thoracoscopy andlaparoscopy identified nodes or metastatic disease missed by CT scan in 50% ofpatients, by magnetic resonance imaging in 40%, and by EUS in 30%. Although no deathsor major complications occurred, staging did involve a general anaesthesia, one-lunganaesthesia, a median operating time of 210 min, and a hospital stay of 3 days.9

The chance of metastases in the abdomen is considerably more with adenocarci-nomas of the lower oesophagus and gastric cardia compared to squamous cell cancersof the oesophagus. Laparoscopy can be of use in diagnosing abdominal metastases likeperitoneal secondaries, or identifying unsuspected cirrhosis, which is a relative contra-indication for surgical resection for some investigators. Its value is much less for moreproximally located tumours.10

One recent study looked at the cost effectiveness of different combinations of stag-ing methods including CT scan, EUS, Positron Emission Tomography (PET) scan, andthoracoscopy and laparoscopy. While PET þ EUS-FNA gave the most accurate stagingcombination, it was more expensive than CT þ EUS-FNA. Although thoracoscopy andlaparoscopy could identify some additional patients with advanced disease, the yieldwas small.11 This study suggests that initial PET staging is indicated, and if no metastaticdisease is identified, EUS þ/� FNA should be performed. Given that PET scan is stillnot widely available, it seems that CT scan and EUS should be the initial stagingmodalities, and PET indicated especially in patients found to have locally advancedtumours with no distant metastases. The invasiveness and cost of thoracoscopy andlaparoscopy, and the constantly improving non-invasive methods like PET scanning,

MIS techniques for oesophageal cancer surgery 927

make the use of minimally invasive staging less attractive. It should be reserved in caseswhere positive confirmation of metastatic disease not otherwise obtained is essentialin deciding on treatment.

MINIMALLY INVASIVE OESOPHAGEAL RESECTION TECHNIQUES

The concept of using a less invasive procedure in oesophagectomy is not new. The de-bate on whether a transthoracic or a transhiatal approach results in less morbidity andbetter outcome has been controversial for a long time.12,13 Two large meta-analysesconcluded that the transthoracic approach probably resulted in higher peri-operativemorbidity and mortality rates, but long-term survival was not different.14,15 The largestrandomized trial published to date compared 106 patients who underwent transhiataloesophagectomy with 114 patients who had the transthoracic approach for mid-lowerthird/cardia adenocarcinomas. This study suggests that transhiatal resection results inlower pulmonary complication rates, shorter ventilation duration, intensive care andhospital stay. There were however no significant differences in in-hospital mortalityat 2% and 4%. Significantly more lymph nodes were dissected in the transthoracicgroup (16 versus 31), and there was a trend towards a survival benefit with the trans-thoracic approach at five years.16 The benefits and drawbacks of a ‘less invasive’ pro-cedure for oesophagectomy are far from conclusive. The advent of MIS surgery simplyadds to this debate.

Since Cuschieri’s early reports,5e7 many different MIS approaches in oesophagec-tomy have been devised, including various combinations of thoracoscopy, laparoscopy,mediastinoscopy, and laparoscopic-assisted (with mini-laparotomy or hand-port de-vices) or thoracoscopic-assisted methods (with mini-thoracotomy). The myriad of sur-gical methods implies a lack of consensus on which is superior.17 The most popular isperhaps thoracoscopic oesophagectomy with gastric mobilization via a laparotomy andcervical oesophago-gastrostomy.7,18e27 Combining laparoscopic and thoracoscopic ap-proaches has its advocates,28e30 so does a totally laparoscopic approach.31e33 Hybridprocedures with MIS-assisted techniques such as the use of hand-ports are also prac-tised by many.34,35 The results of selected published series are shown in Tables 1 and 2.

Thoracoscopic oesophagectomy is usually performed with the patient in the left lat-eral position as for a posterolateral thoracotomy, four to five thoracoports are usedand one-lung anaesthesia is used. A laparotomy for gastric mobilization and pull-upfollows.18,19,22,23,36,37 Two groups in Japan have substantial experience with this tech-nique and reported their results in 80 and 112 patients, respectively,19,37 in whom theyperform extensive three-field lymphadenectomy. Osugi and colleagues utilize an addi-tional 5 cm mini-thoracotomy at the fifth intercostal space on the anterior axillary line.This enhances mediastinal exposure; a rigid retractor can be introduced through thisincision for retraction thus enabling safe dissection, especially when dissecting in theleft paratracheal area.37 Kawahara and associates use a five- to six-port technique,with a 6-cm mini-thoracotomy selectively in difficult cases.19,36 Both groups have re-ported excellent results (Table 1).

The prone position is advocated by some surgeons.7,25,27 The advantage of thisposition is that the lung naturally falls away from the mediastinum, thus improving sur-gical field exposure without the need for additional retractions. Similarly blood will notpool within the surgical field. However, the drawback is cumbersome positioning, andis awkward in the event of an emergent thoracotomy. An Australian group has utilizedthis approach in the largest single centre series of 160 patients. The mean

r without a laparoscopic phase.

opy Blood

loss (mls)

Lymph

nodes

dissected

Mortality Survival

e e 0 e

200 e 1 e767 19.7

(mediastinum)

0 e

e 13 (6e28) 3 e

450 7 1 2-yr:

62% (TS)

63% (TT)

112

(thorax)

27

(mediastinal)

1 (30-day) 5-yr 52%

3 (hospital

death)

Stage I 87.2%

Stage II 70.2%

Stage III 27%

700 e 4 Median

34 mth (TS)

16 mth (TT)

165 (TS) 11 8 Median 29 mth

1-yr 70%

2-yr 57%

5-yr 40%

55%

428 29 0

161 36 0

e e 3 (1.4%)

(30-day)

e

279 10.3 4.3% 3-yr 57%

200 e 5.5% 4-yr: 44%

928

S.Law

Table 1. Selected series using primarily thoracoscopic esophagectomy, with o

N Conversion Hoarseness Respiratory

complication

Anastomotic

leakage

Operating

time (min)

Thoracosc

time (min)

Cuschieri 1994c 26 1 2 3 1 e e

Gossot 1995 29 0 3 5 5 e 135

Akaishi 1996 39 0 7 6 2 448 200

Dexter 1996c 24 2 8 13 2 e 183

Law 1997 22 4 4 4 0 e 110

Yamamoto 2005 112 1 10 (8.9%) 7 (6.3%) 9 (8%) e 112

Law 2000a 30 2 e 12 1 392 90

Smithers 2001c 160 20 e 39 (27%) 6 e 104

Osugi 2003 80 10

early n¼ 34 14% 29% 3% e 278

late n¼ 46 15% 6.5% 0% e 183

Luketich 2003d 222 16 (7.2%) 3.6% 9.5% 11.7% e e

Nguyen 2000/2003d 46 2.2% 1 e 8.7% 350 116

Martin 2005b,c 36 2 e e 19% 240 e

16.7% 16.7% e 550 e 550 20.1

(mediastinum)

e e

11.1

(abdomen)

4 e 1 476 e 343 e e e

ts unless otherwise stated.

sthoracic resection.

tomy only, four patients also had intra-thoracic oesophageal tumours.

open laparotomy (n¼ 15).

mbined.

ort with hand introduced into chest for retraction in thoracoscopy phase.

MIS

techniq

ues

for

oeso

phageal

cancer

surgery

929

Okushiba 2003e 18 e

Suzuki 2005e 19 0

Numbers represent number of patien

TS: thoracoscopic resection, TT: trana For pharyngo-laryngo-oesophagecb Laparoscopic-assisted (n¼ 21) orc Prone position for thoracoscopy.d Thoracoscopy and laparoscopy coe Laparoscopic-assisted with handp

opic-assisted approach without a thoracoscopic phase.

motic

e

Operating

time (min)

Blood

loss (mls)

Lymph

nodes

dissected

Mortality Survival

Swans 390 290 6 (3e12) 0 e

DePau 256 e 11 4 e

Avital 380 220 14.3 1 e

Van de 300 600 7 0 e

Bernab 336 331 8.7 0 eBonavi

260 28 0 e

270 13 0 e

Del G 160 400 8 13.6% 23.7 mths

(DFS)

Espat 274 53 0

Figure val.a Pub Lapc (a) ic with mediastinoscopic dissection n¼ 16.d Ro

930

S.Law

Table 2. Selected series using primarily a laparoscopic or laparosc

N Conversion Hoarseness Respiratory

complication

Anasto

leakag

trom 1997a 9 0 6 5 0

la 1996a 24 2 2 pneumonia 2 6

effusion 16

2005a 22 1 (4.5%) 1 2 1

n Broek 2004b 25 36% 2 2 (pneumonia) 5

e 2005b 17 0 e e ena 2004c 43

(a) 2 e 1

(b) 3 1 1

enio 2004a 35 4.5% 4.5%

2005d 15

s represent number of patients unless otherwise stated. DFS¼ disease free survi

rely laparoscopic oesophagectomy.

-assisted with mini-laparotomy.

Laparoscopic gastric mobilization with right thoracotomy n¼ 27, (b) laparoscop

bot-assisted (Da Vinci system) laparoscopic transhiatal oesophagectomy.

MIS techniques for oesophageal cancer surgery 931

thoracoscopy time was 104 min, blood loss was minimal. Respiratory complicationrate was 27%, and mortality rate was 5%.27

The above methods are modifications of a ‘three-phase’ oesophagectomy withthoracoscopic oesophageal mobilization, followed by laparotomy and cervical oeso-phago-gastrostomy. Some investigators also explored the technique of laparotomyfor gastric mobilization, thoracoscopic oesophagectomy and intrathoracic anastomo-sis.38e41 Performing an intrathoracic anastomosis using thoracoscopy is difficult. Inone report of 17 patients, four out of the five conversions were related to technicaldifficulty with the anastomosis. The leakage rate was high at 18%.38,39 One group ini-tially did intrathoracic anastomosis, but switched to cervical anastomosis after decidingit was unsatisfactory.42,43 It makes better sense for a much easier cervical anastomosis.

Combining thoracoscopic oesophagectomy with laparoscopic gastric mobilizationand pull-up is also a commonly employed approach, with the group in Pittsburg report-ing on the largest experience in 222 patients.28 To facilitate the abdominal procedure,some groups have elected to use a laparoscopic-assisted hand-port system, which mayprovide more tactile control and also potentially can shorten the laparoscopic time.34

A useful modification of using a hand-assisted system is for the assistant’s hand to in-sert via the mini-laparotomy and the retrosternal space into the right thoracic cavity tohelp retraction in the thoracoscopic phase of the procedure.44,45

A laparoscopic or laparoscopic-assisted transhiatal oesophagectomy is preferred bysome investigators.32,35,46e49 This allows gastric mobilization and eliminates at leastpartly the ‘blind’ area of mediastinal dissection by the introduction of laparoscopic in-struments through the diaphragmatic hiatus. To a certain extent lower mediastinallymphadenectomy can also be performed. It is claimed that adequate dissection canbe carried out to the tracheal bifurcation. The superior mediastinum remains thearea out of reach by the laparoscopic instruments.

A mediastinoscopic method is employed by some surgeons to aid superior medias-tinal dissection. Two groups in Germany have reported on the use of a specially de-signed mediastinoscope in oesophageal dissection.50,51 The mediastinoscope, whichis introduced from the neck, has a tissue dilator and several openings for the fibreopticbundle, working channel, as well as flushing and suction devices. A shaped groove in thedilating cone tip allows the mediastinoscope to be guided around the circumference ofthe oesophagus. Thermocautery, biopsy forceps and microscissors can be appliedthrough the working channels, allowing mediastinoscopic dissection to be performedunder magnification. The disadvantage of the technique concerns tumours that areabove the tracheal bifurcation; only small tumours are suitable for the procedure. Inaddition, only a limited mediastinal lymph node dissection is possible. This techniquewas used initially combined with laparotomy for transhiatal resection,50,51 later modi-fied for laparoscopic-assisted resection.33,52,53 There are other endoscopic techniquesfrom the neck. One group describes a method of first making a 10-cm left cervical collarincision, after the left recurrent laryngeal nerve is identified and the oesophagusdissected circumferentially; one 5-mm trocar is placed in the suprasternal notch andone other laterally. Then the cervical incision is closed to prevent gas leakage, andanother 5-mm port is introduced through the centre of this incision. Carbon dioxideinsufflation is used up to a pressure of 4 mm Hg and a conventional 30 �, 5-mm endo-scope is inserted through this central trocar. This method enables better visualizationof the upper mediastinum, and the gentle CO2 insufflation also helps create the dissec-tion plane.54 In another report, a 5-mm mirror scope attached to a retractor witha transparent flat tip (Scuba-dissector, Endopath Saphenous Vein Harvest Tray, EthiconEndosurgery, Cincinnati, OH, USA) is used to aid upper mediastinal dissection.55

932 S. Law

In general, if a transhiatal oesophagectomy is not preferred, most surgeons wouldincorporate a thoracoscopic phase for oesophagectomy to replace the thoracotomy.However, some have combined laparoscopic gastric mobilization with an open thora-cotomy for oesophageal extirpation, theorizing that a thoracotomy allows morethorough mediastinal lymphadenectomy and easier intrathoracic anastomosis.33,56

However, this method is not popular as most would regard avoidance of a thoracot-omy as more important than replacing the laparotomy.

Robotic-assisted oesophagectomy was reported by two groups,57e59 the first in 15patients who underwent laparoscopic transhiatal oesophagectomy.58 Conventionallaparoscopic gastric mobilization was first carried out, then using the Da Vinci system(Intuitive Surgical, Inc., Sunnyvale, CA, USA), mediastinal dissection was performed.This was combined with conventional transhiatal dissection from the cervical incision.The mean operating time was 274 min, with the time decreasing to 216 min for thelast seven cases. Blood loss was minimal. No postoperative death occurred. The sec-ond group reported on only one patient.59 A thoracoscopic oesophageal resectionwith mediastinal nodal dissection was first performed with the robotic system; the pa-tient was then turned supine for the abdominal dissection using the same system. Thetotal time in the operating room was 11 h, and the total surgical console time was 4 h20 min. The estimated blood loss was 900 ml. Hospital length of stay was 8 days.

MINIMALLY INVASIVE OESOPHAGECTOMY AND MORBIDITY

Patient selection

From a technical standpoint, appropriate selection for MIS methods is essential toavoid intra-operative difficulties and complications. Contra-indications for a thoraco-scopic procedure may include extensive pleural adhesions and bulky or locally infiltra-tive tumours, especially those in close proximity with the tracheo-bronchial tree.Some surgeons do not recommend the procedure to patients with prior irradiation,because tissue planes may be obscured,60 while others do not find this prohibitive.19,48

In many series, early-stage cancers or patients with high-grade dysplasia were prefer-entially selected, partly because of the technical ease with which these tumours can beresected.30,47,58,61 In the Pittsburg report, two-thirds of patients had cancer of stage IIand below, 21% had high-grade dysplasia.28

Another technical consideration for patient selection for MIS is the location of theprimary tumour. The changing epidemiology in western countries has led to a predom-inance of lower third and gastro-oesophageal junction adenocarcinomas,62 while pa-tients in the East still suffer mostly from squamous cell cancers of the middleoesophagus.63 It is evident that for most reported series from Asia, thoracoscopicoesophageal mobilization is an integral part of MIS oesophagectomy,18e20,23,44,45,54,64

while a purely laparoscopic or laparoscopic-assisted transhiatal approach withouta thoracic phase is utilized mostly in the West.32,35,46e49,53 This is obviously in partrelated to the perceived ease of oesophageal mobilization in relation to the positionof the primary tumour, and the need for lymphadenectomy. Thorough superior medi-astinal lymph node dissection is only performed in the East, this is not possible withouta thoracoscopic phase.

Adequate pulmonary function may be required in order to withstand the length-ened one-lung anaesthesia for thoracoscopic oesophageal mobilization.64 In the lapa-roscopic technique, the mediastinal pleura is often breached and carbon dioxide

MIS techniques for oesophageal cancer surgery 933

pneumothorax may occur. In one study of 25 patients with laparoscopically assistedtranshiatal oesophageal resections, entry of the pleura occurred in 93% of patients.The CO2 pneumothorax resulted in increased end-tidal CO2 and airway pressurelevels and decreased lung compliance, with significantly higher airway pressure com-pared to a control group of patients who underwent open transhiatal resections.65

The anaesthesiologist should be well aware of this complication and it may be animportant consideration in patients with compromised pulmonary reserve.

Intra-operative complications

Serious intra-operative complications can occur with MIS techniques, such as bleedingfrom the azygous vein;21 aorta;7,66 or intercostal vessel;24 injury to the tracheo-bronchial tree;22,36 recurrent laryngeal nerve;25 and liver and splenic tears.39,43,67

The lack of tactile control is probably a contributory factor. On the contrary, the in-creased magnification and excellent visualization offered by thoracoscopy might in facthelp lessen complications. Technical complications are obviously operator-, technique-and instrument-dependent. More recurrent laryngeal nerve injury with thoracoscopyhas been reported with MIS, which was attributed to increased use of diathermy.25 Onthe contrary, others also claimed that the use of MIS techniques could reduce thiscomplication. In one study, transient hoarseness was reduced from 80% to 18%,23

and in the another, transmediastinal endodissection reduced hoarseness from 13%to 8%.50,68 The increased magnification and excellent visualization offered by thoraco-scopy or mediastinoscopy were given as reasons for these successes. Judicious use ofother energy sources like harmonic scalpel or bipolar scissors may also help reducethis complication. As surgical techniques mature and instrumentation improves, thechance of intra-operative mishaps will likely reduce.

Surgeons must be prepared for conversion to open surgery should difficulties beencountered and modify their technique accordingly. The need to convert to open sur-gery is required in approximately 10% of patients in various series. The reasons re-ported for conversion included lung adhesions,18 intra-operative injury to adjacentstructures or bleeding, advanced tumours,18 loss of one-lung ventilation,24 and equip-ment failure.69 Difficult intrathoracic anastomosis also warrants conversion becausethis procedure is technically demanding using MIS methods.39 Although an innovativetechnique has been devised to circumvent this difficulty,70 most surgeons prefer acervical anastomosis. This point has been discussed.

It seems that serious intra-operative complications can occur with a variety of tech-niques, but it is difficult to compare these data properly and draw firm conclusions be-cause of the large variation in methods used by each group. The surgical teams alsohad very different levels of experience with open oesophagectomy, which could affecttheir success rates.

Postoperative morbidities

Patients who undergo oesophagectomy are often elderly, may have co-morbid dis-eases, and are malnourished from malignant dysphagia. Aside from gross technicalcomplications, cardiopulmonary problems are the main causes of death.71e74 Obviat-ing the need of a thoracotomy or laparotomy may potentially reduce postoperativepain, ventilator dependence, cardiopulmonary complications, shorten intensive careand hospital stay, and result in lower mortality rates.

934 S. Law

Many published studies simply document the results of MIS oesophagectomy, andoften satisfactory outcomes are reported. Few studies have directly compared postop-erative outcome in patients who had MIS with those who underwent conventionaloesophagectomy. One study, comparing the outcome of 22 patients who had thoraco-scopic oesophagectomy with 63 patients who underwent open thoracotomy resectionsduring the same time period (but with different selection criteria), did not find significantdifferences in morbidity and mortality rates. It was noted, however, that blood loss wasslightly less in the thoracoscopy group,18 and that the group selected for thoracoscopyhad poorer Eastern Cooperative Oncology Group (ECOG) performance status. Inanother comparison of patients who underwent pharyngo-laryngo-oesophagectomy(most of whom had cervical oesophageal, hypopharyngeal or laryngeal cancers), anda historical cohort of patients, there were also no significant differences.20 The ‘extra-thoracic’ trauma in this group of patients was substantial, and this may in part explainthe lack of benefit thoracoscopic mobilization was expected to show.

In another study 18 patients who had combined thoracoscopic and laparoscopicoesophagectomy were compared with two historical cohorts of patients who had un-dergone either transthoracic or transhiatal oesophagectomy.29 Patients who had thecombined approach had shorter operative time; less blood loss; fewer transfusions;and shortened intensive care unit and hospital stay compared with the historical con-trols, while anastomotic leakage rates and respiratory complication rates were similar.Because the study had the inherent bias of using historical controls it is difficult todraw firm conclusions.

Osugi and colleagues showed that thoracoscopic oesophagectomy took longer, butblood loss and morbidity rates were similar compared to open three-field oesopha-gectomy.26,75 One recent study looked at 17 patients who underwent laparoscopic-assisted transhiatal resection (with a 8-cm mini-laparotomy) and compared with ahistorical group of 14 matched patients who had open transhiatal oesophagectomy.47

Less blood loss, shorter operating time, and a shorter hospital stay were demon-strated. The 14 control patients however were identified in a 12-year period priorto MIS oesophagectomy and operative techniques and peri-operative care couldhave changed. In addition, the MIS part of the oesophagectomy only involved10e12 cm of oesophageal dissection in the lower mediastinum using laparoscopy,the rest of the transhiatal mobilization was completed in the conventional mannervia the laparotomy wound. It is unlikely such an approach will result in superioroutcome.

Another study compared laparoscopic-assisted transhiatal resections in 25 patientswith a historical cohort of 20 patients who had undergone conventional transhiatal re-section. Operating time in the former group was longer, blood loss was less, andshorter intensive care unit stay was found. No differences in morbidity, mortalityand hospital stay were documented.35 Again use of a historical control group is unsat-isfactory. More importantly there was a 36% conversion rate mainly because of tech-nical difficulties encountered. Appropriate comparisons between the two groups werethus unreliable.

The use of endodissection with the mediastinoscope lessened cardiac complica-tions in one study, from 19.3% using conventional transhiatal resection, to 4.2%with endodissection.50,68 Other complications were not reduced, and only distal oe-sophageal tumours were studied. Akaishi and colleagues found that the incidence ofrecurrent laryngeal nerve injury was less, and that patients were less ventilator-dependent after thoracoscopic resection compared with a historical cohort. Theoverall incidence of pulmonary complications was reduced from 33% to 20%.23

MIS techniques for oesophageal cancer surgery 935

Conventional thoracotomy reduces chest wall compliance, vital capacity and totallung capacity. Restrictive pulmonary damage was less following thoracoscopic sur-gery,26 and spirometric and exercise tolerance was also better in MIS treated pa-tients.75 Quality-of-life measured by Zubrod score was well maintained in patientswho underwent thoracoscopic oesophagectomy.64 Short- to medium-term quality-of-life scores, however, could not be shown to be better than after conventionalopen surgery in another study.76

Studies with well-matched control groups are lacking in reported series, and de-spite most studies showing reasonably good results with MIS techniques, clear advan-tages over conventional open surgery are not seen. This may be partly because of thenumber of patients studied generally was too small to have enough statistical power todemonstrate a difference. There are also other reasons why benefits are difficult toconfirm. With modern analgesic methods such as epidural analgesia, postoperativepain control is a less critical problem.77 The genesis of cardiopulmonary complicationsis multi-factorial and does not depend solely on the size of the incision. Surgical traumaof mediastinal dissection, more likely the major determinant of ‘surgical invasiveness’,is also independent of the incision size. The benefit of smaller port sites comparedwith open thoracotomy may be offset by the lengthened time of single-lung anaesthe-sia. It is well recognized that during one-lung ventilation, hypoxaemia can occur. Duringan open approach, the collapsed lung can be episodically re-inflated. This does not taketoo much time because the lung can be deflated again with manual compression. Ina thoracoscopic approach, deflation and re-inflation requires more time and surgicaldissection has to be halted because of inadequate exposure. The addition of a low con-tinuous positive airway pressure (CPAP) to the non-dependent lung could improve ox-ygenation, but surgical exposure is also compromised.78 The use of a prone positionimproves surgical exposure, and at the same time CPAP can be applied. In the largeseries reported using the prone position, however, respiratory complications were stillsubstantial.27 A learning curve obviously exists for such complicated procedures.37,23

The duration of the thoracoscopic procedure, blood loss, the incidences of postoper-ative pulmonary infection were all less, and the number of mediastinal nodes retrievedwas more, in the later half of a group of 80 patients who had thoracoscopic oesopha-gectomy.37 It was claimed by one investigator that the first 17 cases were necessary toacquire the basic skills, with the most remarkable difference seen between the first 36cases and the others.37,64 Thus for most series the full technical potential may not havebeen realized.

ONCOLOGICAL CONSIDERATIONS IN MIS OESOPHAGECTOMY

Perhaps the most important consideration for MIS oesophagectomy is whether MISoesophagectomy offers comparable oncological clearance to open surgery. Whateverthe technique used, the extent of lymphadenectomy should not be adjusted because oflimitation of the surgical technique.

The importance of patient selection for MIS oesophagectomy has already been dis-cussed from a technical standpoint. Concerns with regards to adequacy of lymphade-nectomy also influence the choice of procedure. Thus high-grade dysplasia in Barrett’soesophagus, or intramucosal, superficial cancers are preferred by many investigators,since the chance of lymphatic spread is minimal,28,47,55,58,61 and a laparoscopic orlaparoscopic-assisted approach is often used. However, for the same reason, onemight prefer an endoscopic, organ preserving resection. If more extensive

936 S. Law

lymphadenectomy is deemed necessary for more advanced tumour or for more prox-imally located tumours, laparoscopy alone offers inferior exposure without additionalthoracoscopic dissection.28,61 Some surgeons include patients with increased medicalrisk, even if they have more advanced tumours. In these patients, postoperative recov-ery and survival are perhaps more important than performing a radical resection.18,55

Palliative resections using MIS methods have also been advocated; again in these pa-tients faster postoperative recovery and quality-of-life issues such as less post-thora-cotomy pain, are more important.32

A surrogate of the extent of dissection is the number of lymph nodes removed atsurgery. Radical lymph node dissection is certainly possible, even in difficult areas likethe left paratracheal region along the left recurrent laryngeal nerve.23,36,64 In fact, thehigher magnification under thoracoscopy by keeping the camera close to the oper-ating field, may allow finer dissection and improve the dissection along the recurrentlaryngeal nerve.23,26 The quality of lymphadenectomy is difficult to evaluate in theliterature. Many do not report on the number of nodes retrieved, and in thosewho do the number of mediastinal, abdominal or cervical nodes are not separatelystated. The problem of using the number of lymph nodes as a surrogate is that thenumber examined in part depends on the conscientiousness of the pathologist ex-amining the surgical specimen, and unless comparisons are made with a concurrentcohort of patients undergoing open surgery, additional bias may be present whenhistorical records are used.

The ultimate test of minimally invasive oesophagectomy is whether long-term sur-vival is similar to that of conventional open oesophagectomy. Thus far in series thatreport their medium to long-term results, or in those where comparative data withopen surgery are presented, this seems to hold true.18,20,64 Only in one report onthe use of endodissection, the investigators showed that for patients with lower oe-sophageal adenocarcinomas, and positive lymph nodes, endodissection resulted in lon-ger survival compared with conventional transhiatal technique.50

Port-site recurrence as a specific problem with MIS has also been reported foroesophageal cancer.18,19,34,79,80 Direct parietal seeding by repeated passing ofdissecting instruments through the ports seemed to be the mechanism. Withimprovement in surgical technique and care taken to protect the port sites, thishas become rare.

SUMMARY

Since the early 1990s, many innovative MIS techniques have evolved for oesophagec-tomy. Larger series have started to appear in the literature and certainly with im-provement in instrumentation and experience, encouraging results are nowshown. In appropriately selected patients, MIS oesophagectomy is certainly feasibleand at least equivalent postoperative morbidity and mortality rates, and so farsurvival data, can be demonstrated. It is unlikely that MIS methods will significantlyreduce mortality rates, since in experienced centres death from oesophagectomyhas become very uncommon. In selected series, postoperative respiratory complica-tion rates can be very low. Without a well conducted randomized trial, however, thispotential benefit is difficult to prove. Softer end-points, such as less blood loss, re-duction in intensive care or hospital stay, analgesic requirement, spirometric and pul-monary function derangements, biochemical changes,81 and short- and medium-termquality of life parameters, are more commonly demonstrated. Because of the

MIS techniques for oesophageal cancer surgery 937

technical complexities of these procedures, they should not be attempted withouttraining and mentorship, and should be investigated further in centres with adequateexperience with the resections. Further evaluation of the role of minimally invasivetechniques in oesophageal cancer would require larger-scale studies, preferably ran-domized controlled trials.

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