10.1245/ASO.2005.02.017
Annals of Surgical Oncology 12:960-970 (2005)
© 2005 Society of Surgical Oncology
Minimally Invasive Surgery for Colorectal Carcinoma
Luca Stocchi, MD and
Heidi Nelson, MD, FACS
Division of Colon and Rectal Surgery, Gonda 9S, Mayo Clinic and Mayo Foundation, 200 First Street S.W., Rochester, Minnesota 55905
Correspondence: Address correspondence and reprint requests to: Heidi Nelson, MD, FACS; E-mail: nelson.heidi{at}mayo.edu
Key Words: Laparoscopy • Colorectal neoplasm • Quality of life • Minimally invasive surgery • Colon carcinoma • Colon surgery
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INTRODUCTION
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Laparoscopic-assisted colectomy (LAC) has gradually gained acceptance in the treatment of several benign conditions. Several advantages of LAC when compared with traditional open colectomy (OC) have been reported, including cosmesis, preserved immune function, lesser analgesic requirements, a faster time to recovery from surgery, and, ultimately, a reduction of hospital stay. Despite these benefits, there has been reluctance to accept LAC in the treatment of colorectal carcinoma. In fact, several oncological concerns have been raised that are based on the suspicion that the laparoscopic technique might alter tumor spread and cause increased recurrence rates. Only recently has a multicenter, randomized trial conducted in the United States effectively addressed this issue. The purpose of this review article is to outline the early concerns regarding LAC for carcinoma, to present results from the most current series, and to discuss the main issues regarding the applicability of LAC and the possible future developments of laparoscopic techniques in colorectal carcinoma.
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EARLY ONCOLOGICAL CONCERNS
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One of the early concerns regarding LAC for carcinoma was that laparoscopy would not allow adequate tactile sensation and might impair proper intraoperative tumor staging, especially with respect to the evaluation of the liver. In addition, there was some trepidation regarding the ability of laparoscopic resection to provide a satisfactory surgical specimen with sufficient resection margins and adequate lymph node collection. In the early experiences with LAC for carcinoma, these parameters were also of particular importance as oncological surrogates of survival and tumor recurrence rates in the absence of meaningful follow-up. Laparoscopic ultrasonography has been developed, both experimentally1 and clinically,2 to improve accuracy in the intraoperative evaluation of the liver for metastatic disease. More recently, hand-assisted laparoscopic surgery has been proposed as a variant of LAC which would allow resumption of a complete tactile sensation. With regard to the adequacy of the resected specimen, several series have shown similar lymph node collection between OC and LAC (Table 1
). Studies on specimen length and resection margins have also confirmed equivalence between LAC and OC.3–6 Although data on margins and lymph node collection could provide reassurance regarding the adequacy of LAC for carcinoma during the early clinical experience, subsequent data on survival and tumor recurrence have more strongly corroborated the evidence that LAC and OC are comparable in providing effective tumor staging.
Concerns were also raised that tumor spread might be altered because of the different intra-abdominal environment related to the use of trocars to gain access to the abdominal cavity and the establishment of pneumoperitoneum to provide adequate exposure. Several case reports, mainly in the early 1990s, had become cautionary notes against the widespread use of LAC for cancer.7–9 This culminated in 1994, when a small series presented an alarming 21% incidence of port-site recurrences.10 However, further clinical experience with LAC eventually reduced the anxiety over port-site recurrences. In fact, several series published in the last decade have generally confirmed the incidence of this phenomenon at 
1%, which is comparable to the wound recurrence rate after open surgery (Table 2).11–13 In a consensus report from the European Association of Endoscopic Surgeons, Veldkamp et al.14 collected all reported cases of port-site recurrences from a total of 28 different studies from Europe, Asia, Australia, and North America. There were 38 overall port-site recurrences on a denominator of 5225 combined patients, corresponding to an overall incidence of .72%.
It is now accepted that port-site recurrence is a technical complication of LAC and not an inevitable consequence of the laparoscopic approach. Therefore, most surgeons performing LAC either use a wound protector or irrigate the port site with a variety of tumoricidal solutions to minimize the chance of a port-site or extraction-site recurrence. The US multicenter prospective randomized trial on LAC versus OC for colon carcinoma has confirmed a similar incidence of abdominal wall recurrence and port-site recurrences, well below 1%.15 Sound evidence from this multicenter randomized trial should help put the issue of port-site recurrences to rest.
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EQUIVALENCE IN SURVIVAL: THE CLINICAL OUTCOME OF SURGICAL THERAPY TRIAL
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A surgical consortium referred to as the Clinical Outcome of Surgical Therapy (COST) study group conducted a noninferiority trial comparing LAC and OC for colonic carcinoma. The results at 3 years from their phase III prospective multicenter randomized trial, sponsored by the National Cancer Institute and National Cancer Institute cooperative groups, have been recently reported.15
The end points of the study were time to tumor recurrence, disease-free and overall survival, morbidity, recovery parameters, and quality of life (QOL). Conversions were included in the LAC group on the basis of an intent-to-treat analysis.
A total of 872 patients were randomized over 7 years. The conversion rate was 21%. There was no difference in conversion rates among participating surgeons based on the number of patients each of them contributed to the trial. Operating times were longer after LAC (150 vs. 90 minutes; P < .001). The extent of resection and median number of lymph nodes harvested (n = 12) were comparable in the two groups. Morbidity and mortality were similar between groups. The durations of use of parenteral and oral analgesics were significantly shorter after LAC than after OC (median: 3 vs. 4 days [P < .001] and 1 vs. 2 days [P = .02], respectively). Hospital stay was also shorter after LAC (median: 5 vs. 6 days; P < .001). After a median follow-up of 4.4 years, the tumor recurrence rate and disease-free and overall survival were similar for OC and LAC. This was confirmed after stage-adjusted analysis. Although the design of the trial did not allow for true statistical equivalence to be tested, the COST study was the first large multicenter randomized trial to demonstrate no inferiority for LAC compared with OC for overall or disease-free survival. It therefore provides sound data to justify the use of LAC for colon carcinoma.
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POSSIBLE ONCOLOGICAL BENEFITS OF LAC
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During the last decade and along with the controversy regarding a possible increase in tumor spread related to the laparoscopic technique, several experimental studies were conducted that showed that laparoscopy could actually decrease tumor spread.16 Although overall survival after LAC versus OC is comparable in most series (Table 3), some series of LAC have actually shown higher survival rates than in historical controls.17 Under these circumstances, it is important to consider that several of these patients are admittedly a select group and that often limited data are available on other relevant variables, such as chemotherapy regimens, that likely influence survival rates.
However, the results from a recent prospective randomized trial showing decreased recurrence rates in stage III patients generated great interest and enthusiasm because they seemed to confirm clinically the experimental data showing decreased tumor spread after laparoscopy.18 That these data come from a single center and these positive results are based on a subset analysis of 37 patients may explain why they have not been reproduced in larger multi-institutional studies. Furthermore, 79 patients were considered for enrollment but ended up refusing to participate, which raises the possibility of a selection bias. Although intriguing, these results should therefore be viewed with caution. Most studies, including the US prospective randomized trial, have not found significant survival differences even in stage-by-stage comparisons. In a study specifically focused on long-term follow-up after LAC for stage III colorectal carcinoma, the survival was comparable to reported stage-adjusted survival from large national databases19 (Table 4).
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QUALITY OF LIFE
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How best to measure QOL in patients undergoing LAC remains a topic of debate. Initially, improved QOL was assumed from assessments of pain, such as the measurement of duration or dosage of parenteral and/or oral analgesics. This is obviously a very limited tool both in time (usually the immediate postoperative course) and in scope, because many factors besides physical pain contribute to what is considered QOL. Reports on LAC almost uniformly report a decreased use of postoperative narcotics, either measured as days of use4,15,18 or, more rarely, as the amount of narcotic medication required.20,21
Other studies have measured QOL as patient-reported return to full social activity, physical activity, return to work, or a combination thereof. At least two studies have found that return to full activities occurred between 2 and 5 weeks faster after LAC than after OC.22,23 More complex measurement scales have been developed, mostly in the United States and in Europe, in the form of questionnaires covering the various aspects of what should constitute as a whole the QOL. These are currently accepted as the most accurate tools to measure QOL, although there is evidence that scores from two different questionnaires can result in up to 30% difference in the measured QOL.24 Questionnaires completed by select series of patients undergoing LAC versus OC for a variety of indications have shown mainly cosmetic benefits and otherwise minimal differences in perceived QOL between the two techniques.25,26
In the largest study reported to date, QOL was analyzed in 428 patients randomly assigned to LAC versus OC for colonic carcinoma as part of the multicenter randomized National Cancer Institute–sponsored trial.27 The conversion rate in this group was 25%. QOL was measured by using several standardized instruments. They included the Symptoms Distress Scale, based on patient self-reported symptoms; the QOL index, based on measurements of QOL in five domains (activity, daily living, health, support, and outlook); and the Global QOL, which was a patient-reported score ranging from 0 to 100, where 0 corresponded to death and 100 to excellent health. Patient data on all scales were obtained before surgery and 2 days, 2 weeks, and 2 months after surgery. The only statistical difference noted was in the global rating scale score measured 2 weeks after surgery, which corresponded to a modest clinical benefit in favor of LAC. Preliminary results from the COlon carcinoma Laparoscopic or Open Resection (COLOR) trial confirm these results28 (also see the section on international trials).
It remains unclear why LAC has not demonstrated QOL benefits as significant as other parameters of postoperative recovery. One possible explanation is that relatively high conversion rates within an intent-to-treat analysis might mask the favorable effect on QOL of cases that were completed laparoscopically. Several surgeons participating in the COST trial had variable experience in LAC. It is therefore conceivable that a more efficient patient selection could decrease conversion rates and allow greater QOL benefits. For example, in a recent series on 1253 patients undergoing laparoscopic intestinal surgery, a score to measure the risk of conversion was developed that was based on the most important predictive factors. These included increased body mass index, American Society of Anesthesiologists classification, complexity of resection (especially laparoscopic rectal resection), intra-abdominal abscess or fistula, and prior experience in LAC of the operating surgeon. The total conversion rate was 10%.29 Future studies will need to examine whether the reduction in conversion rates can improve QOL.
Another possible explanation for the modest QOL benefits might derive from the inability of the currently available tools to appropriately measure QOL after LAC for carcinoma. In fact, the evaluation of short-term QOL benefits in these randomized trials should be performed in the context of cancer surgery, where survival and possible cure are the most important aspects of patient care. This means that a patient who has undergone operation for carcinoma might evaluate his or her QOL differently from a patient who underwent an analogous operation for benign disease, for which cosmesis, postoperative pain, and limitations of social activities might play a more relevant role. In addition, some of the tools used to measure QOL have not been specifically tailored for patients undergoing surgery for colorectal carcinoma, but rather for patients undergoing chemotherapy and radiotherapy for carcinoma. In other cases, QOL measurements have been based on patients undergoing surgery, but not necessarily for carcinoma. It is therefore apparent that more precise instruments should be designed in the future to capture the aspects of QOL after LAC which are specific for this subgroup of cancer patients.
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MORBIDITY AND POSTOPERATIVE MORTALITY
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Morbidity and mortality after LAC have been generally comparable to those after OC, with a few studies showing a significant difference in favor of LAC (Table 5). In particular, prospective randomized trials from the United States and Asia have shown comparable rates,15,20,21 whereas one study from Europe showed lower morbidity rates after LAC (12% vs. 31%; P = .001).18 It has been suggested that the minimally invasive approach might be particularly beneficial in reducing postoperative complications in patients who are more likely to have significant comorbidity at the time of their colectomy. In this regard, at least four studies have shown that LAC might be particularly beneficial in reducing morbidity in elderly patients.30–33 Delgado et al.31 used the threshold of 70 years to divide their patients who underwent LAC and OC. Whereas the morbidity after LAC was 11.4% and 10.2% in younger and elderly patients, respectively, postoperative morbidity after OC increased from 20.3% in younger to 31.3% in elderly patients (P = .004). In a US case-matched study analyzing patients 75 years and older, 42 LAC patients were compared with 42 counterparts undergoing OC. Morbidity was 14.3% after LAC versus 33.3% after OC (P = .04).30 It also seems logical to expect that LAC, with its shorter incision, would result in reduced wound-infection rates. Some studies have indeed reported a decreased wound infection rate after LAC.18,34–36 In addition, LAC might be associated with a decreased rate of small-bowel obstruction due to less adhesion formation and reduced rates of incisional hernia related to the smaller incisions used. However, definitive long-term data on these issues are still limited.
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TABLE 5. Morbidity and mortality rates for LAC versus OC for carcinoma (converted cases are considered as LAC; noncontrolled studies)
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In a retrospective cohort study comparing 211 patients undergoing laparoscopic-assisted bowel resection with 505 open counterparts, Duepree et al.37 found that laparoscopic procedures resulted in significantly fewer incisional hernias (2.4% vs. 12.9%; P = .00002) and small-bowel obstructions requiring nonoperative treatment (1.9% vs. 6.1%; P = .016). Overall reoperation rates were lower for laparoscopic procedures (3.8% vs. 7.7%; P = .03). The rate of small-bowel obstruction requiring surgery was similar (1.4% for laparoscopic procedures vs. 1.6% for open procedures; P = .87). Contrasting data regarding incisional hernia rates come from Winslow et al.,38 who also evaluated the incidence of wound infections in 83 patients prospectively randomized to LAC versus OC as part of the COST multicenter trial. After a mean follow-up of 30 months, the wound-infection and incisional hernia rates in 37 patients undergoing LAC were 13.5% and 24.3%, respectively. When compared with the 10.9% wound-infection rate and 17.4% incisional hernia rate experienced by 46 patients undergoing OC, there was no statistically significant difference. When a meta-analysis was conducted on a total of 2512 procedures from 12 different randomized trials comparing LAC and OC for carcinoma, overall morbidity was significantly lower after LAC, with reduced wound-infection rates as a determining factor.39 In the presence of conflicting or unclear results, further data from large prospective randomized studies with longer follow-up will be needed to further clarify the extent of morbidity benefits after LAC. However, current data support at least equivalence in postoperative morbidity after LAC or OC.
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COSTS
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It is difficult for several reasons to estimate the costs associated with an operation. First of all, there are differences between hospital expenses and hospital charges and differences among various hospitals. In addition, there are scarce data on the indirect costs generated by lost revenues due to illness-related absence from work, which continues after hospital discharge. This issue is complicated by the difficulties in comparing costs among different countries, where the health care and reimbursement systems are often dramatically dissimilar. In general, it is widely accepted that LAC requires longer operative times and greater instrumentation costs. However, a reduced hospital stay should offset the increased intraoperative costs. Costs derived from laparoscopic instrumentation might be reduced in the future by more widespread acceptance of reusable instruments.
Rarely have studies been conducted on patients with colorectal carcinoma exclusively; rather, a mixed population of benign and malignant disease has been considered. In some studies, only operative costs have been considered, whereas other authors have attempted the analysis of indirect costs. Results on cost analyses have not been uniformly in favor of LAC,40,41 but several reports from centers with an interest in laparoscopic techniques have suggested reduced overall costs after LAC.42,43 In one such study, 33 consecutive patients undergoing ileocolic resection for Crohn’s disease were compared with those undergoing OC after computer matching based on age, sex, diagnosis, type of resection, and date of operation. Both direct and indirect costs were measured, including adjusted-billed charges and physician services. There was an overall reduction of more than $3000 in favor of LAC, with demonstrable savings even when direct and indirect costs were considered separately.44
In the largest study to date focused on the issue of cost of LAC versus OC, Delaney et al.45 matched 150 LAC cases performed in 2000 and 2001 with 150 OC counterparts. The two groups were matched for age (within 10 years), sex, surgical procedure, and presence of comorbidity according to disease-related grouping. Both groups included benign and malignant disease. Patients with previous abdominal procedures whose extent could result in a possible contraindication to LAC were excluded as the corresponding OC. Direct costs were calculated as hospital expenses, and professional and billed costs were not calculated. Complications including readmissions within 30 days from discharge, American Society of Anesthesiologists status, and body mass index were not significantly different. Not surprisingly, operating room time was longer and costs were higher in the LAC group, whereas hospital stay was longer and related costs were higher after OC. Overall, LAC resulted in significantly reduced costs when compared with OC ($3208 vs. $3654; P = .003). The economic benefits of LAC mainly came from pharmacy, laboratory, and nursing care costs. The authors contend that such a reduction in direct costs might correspond to an even greater difference when billed costs are considered.
Although this article provides important data on the potential economic implications of LAC, it comes from a single center where, reportedly, only two experienced laparoscopic surgeons performed LAC. A cost analysis is currently under way for at least three large multicenter prospective randomized trials comparing LAC and OC for carcinoma, including the COST, the COLOR, and the Conventional versus Laparoscopic-Assisted Surgery in Colorectal Cancer (CLASSICC) studies. Although these trials are mainly focused on oncological outcomes and QOL, cost analyses from these studies will also provide important data to clarify the economic potential of LAC.
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CREDENTIALING
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Although the COST trial provides data demonstrating feasibility and safety of LAC for carcinoma, the acceptance of LAC for carcinoma poses concerns regarding adequate training to perform this procedure. Experience with at least 20 LAC cases was required to be eligible as a surgeon to enroll patients onto the trial. With regard to specific parameters that are representative of a learning curve for LAC, a few studies have reported that 30 to 50 cases of LAC are necessary to significantly reduce operative times, conversion rates, and morbidity.4,46–49 However, this learning curve is not specific for carcinoma, and these reports come from surgeons with a specific interest in LAC. It is therefore not easily applicable to the general surgeon, who performs an average of 11 colonic resections annually, according to data from the recertifying examination of the American College of Surgeons.50 Animal and cadaver courses, as well as other industry-sponsored initiatives, are useful adjuncts but cannot replace appropriate surgical experience. Although 15 to 20 cases could be sufficient in a training program, strategies should be developed to implement an appropriate credentialing system for surgeons with no experience in LAC. It has been suggested51 that guidelines on LAC for carcinoma should be developed that are similar to those for OC for carcinoma published in 2000.52 The American Society of Colon and Rectal Surgeons has released a statement approving LAC for carcinoma, but only if the technical steps of the procedure are performed appropriately and if the operating surgeon has performed at least 20 laparoscopic colonic resections (Appendix 1).
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INTERNATIONAL TRIALS
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A number of international trials are in progress to evaluate the efficacy of LAC for cancer. Results from these studies in different socioeconomic conditions might validate the COST study results.
The COLOR trial is a major European multicenter randomized study that started in 1997; it compares LAC with OC for colon carcinoma. Patients with a single tumor located above the peritoneal reflection were eligible to participate. Patients with concurrent malignancies, metastases, or previous colonic resection were excluded. Short-term results have recently been presented in abstract form on 1005 patients. The conversion rate approached 18%. There were no significant differences between the two approaches with regard to postoperative morbidity and mortality, reintervention, or readmission rates. In contrast, there were significant advantages in favor of LAC concerning faster recovery of bowel function and reduced hospital stay.53 Oncological outcomes at 3- and 5-year follow-up are not yet available.
Data on QOL from the COLOR trial have been presented in abstract form on 186 patients. Patients were evenly divided between LAC and OC. Validated questionnaires were used, including the EuroQol, Short Form-36, European Organization for Research and Treatment of Cancer-CR 38, and visual analogue scale. Pain and nausea measured by visual analogue scale were less after LAC. There was also an advantage for LAC regarding the performance of usual activities at 3 and 14 days. Detailed analyses of health profiles by EuroQol and measurements from the disease-specific questionnaire European Organization for Research and Treatment of Cancer-CR 38 did not show significant differences. Overall, there was what was described as a "very modest improvement in QOL" from LAC, which also mirrors the currently available QOL outcomes from the COST trial.
Another prospective randomized study is the Medical Research Council–funded CLASSICC trial, which opened to recruitment in 1996 and involves 15 hospitals throughout the United Kingdom. The design is largely modeled after the COST trial, with some adaptation to the UK medical system. Rectal carcinoma patients are included. Economic evaluations include a cost analysis of the resources necessary for patient treatment but also account for possible differences in patient benefits measured by the so-called Q-TWIST analysis (quality-adjusted time without symptoms of disease and toxicity of treatment).54 Similar trials are also being developed in Brazil and in Australia. To the best of our knowledge, results from these trials have not yet been published.
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FUTURE DEVELOPMENTS
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Hand-Assisted Laparoscopic Surgery
Several groups are studying the extent of the benefit of hand-assisted laparoscopic colorectal surgery as compared with traditional LAC.15,55–58 Proponents of this technical variation of more conventional LAC contend that hand assistance restores the tactile feeling, which would be otherwise limited, and reduces operative times while retaining the recovery benefits of a laparoscopic procedure. Chang et al.59 recently presented data on 85 patients treated with traditional laparoscopic sigmoidectomy compared with 66 patients treated with hand-assisted sigmoid resection. Staff with limited prior experience in LAC as well as surgical residents performed a significant portion of hand-assisted cases. Even so, operative times were shorter after hand-assisted sigmoidectomy when compared with conventional laparoscopic-assisted resection. There were no significant differences in regard to flatus and hospital stay, which was approximately 5 days for either technique. Morbidity was similar between the two groups, and there were no conversions for the hand-assisted technique. The conversion rate was 13% for traditional laparoscopic sigmoidectomy.
If favorable results were confirmed by larger series, hand-assisted laparoscopic surgery could help reduce the operative costs related to longer operative times and provide an alternative to traditional laparoscopic procedures, especially for more complex procedures such as rectal dissection.60 It also has the important potential for a faster learning curve, which would be of particular benefit for surgeons with no previous training in laparoscopic colectomy. Studies on the applicability of hand-assisted techniques for the specific indication of carcinoma are still limited,57 but early results would suggest no oncological drawbacks when compared with conventional LAC.
Rectal Carcinoma
The demonstrated safety of LAC for carcinoma corroborates the impetus to develop laparoscopic resection for rectal carcinoma. Several series have been published in the last 5 years, and most of them suggest feasibility of the laparoscopic approach for both abdominoperineal and anterior resection.60–72 In one of the largest series reported to date, Lacy et al.73 analyzed 220 patients. A total of 36% of them had undergone previous abdominal operations, and 50% received neoadjuvant chemoradiation treatment. Conversion was necessary in 44 patients (20%). The overall postoperative morbidity was 25.4%, including anastomotic leakage in 7.6% of patients treated with anterior resections. Postoperative mortality was .9%, and the mean hospital stay was 6.8 days. It is important to point out that most of the feasibility studies on the laparoscopic approach for rectal carcinoma come from specialized centers. Even so, the data confirm that laparoscopic rectal resection remains technically challenging. Although the magnification offered by the laparoscope makes it attractive and might reduce rates of postoperative sexual dysfunction,74 exposure can be problematic, especially for the anterior dissection, and laparoscopic staplers can be cumbersome in the lower rectum. Several series62,63,69,72 have reported anastomotic leak rates ranging from 17% to 21.2%.
In addition, oncological concerns have been raised,75 with at least two series61,69 reporting local recurrence rates of approximately 20%. Therefore, whether the laparoscopic approach for rectal carcinoma can become widely applicable remains to be determined.
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CONCLUSIONS
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LAC for colon carcinoma benefits patients when it is performed by experienced surgeons. It is associated with similar morbidity and faster postoperative recovery when compared with OC. Early concerns regarding the oncological effectiveness of laparoscopic colonic resection have been addressed by numerous studies and especially by the multicenter prospective randomized COST trial. Reported QOL benefits seem to be clinically modest and might require a refinement of our measuring tools to detect meaningful differences as well as a more careful patient selection to reduce conversion rates. Although there is already increasing evidence that LAC is economically advantageous when compared with OC, evolutions in laparoscopic instrumentation might further reduce intraoperative costs. As LAC becomes part of the standard training for colon and rectal surgeons, the issue of widespread credentialing for LAC remains essential for surgeons who were not exposed to LAC as part of their training. Hand-assisted techniques and laparoscopic rectal resection are generally accepted, and their applicability is currently under investigation.
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APPENDIX 1: APPROVED STATEMENT BY THE AMERICAN SOCIETY OF COLON AND RECTAL SURGEONS ENDORSED BY THE SOCIETY OF AMERICAN GASTROINTESTINAL ENDOSCOPIC SURGEONS
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Laparoscopic colectomy for curable cancer results in cancer-related survival equivalent to that with OC when it is performed by experienced surgeons. Adherence to standard cancer resection techniques, including but not limited to complete exploration of the abdomen, adequate proximal and distal margins, ligation of the major vessels at their respective origins, containment and careful tissue handling, and en-bloc resection with negative tumor margins using the laparoscopic approach, will result in acceptable outcomes. On the basis of the COST trial, prerequisite experience should include at least 20 laparoscopic colorectal resections with anastomosis for benign disease or metastatic colon cancer before the technique is used to treat curable cancer. Hospitals may base credentialing for laparoscopic colectomy for cancer on experience gained by formal graduate medical educational training or advanced laparoscopic experience, participation in hands-on training courses, and outcomes.
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FOOTNOTES
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Luca Stocchi, MD is now at Department of Colorectal Surgery, Desk A30, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195.
Received for publication February 15, 2005.
Accepted for publication July 17, 2005.
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TOP
INTRODUCTION
EARLY ONCOLOGICAL CONCERNS
