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Annals of Surgical Oncology 10:363-368 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Body Mass Index Does Not Affect Systematic D2 Lymph Node Dissection and Postoperative Morbidity in Gastric Cancer Patients

Stephan Gretschel, MD, Frank Christoph, MD, Andreas Bembenek, MD, Lope Estevez-Schwarz, MD, Ulrike Schneider, MD and Peter M. Schlag, MD, PhD

From the Department of Surgery and Surgical Oncology (SG, FC, AB, LE-S, PMS) and the Pathology Unit (US), Humboldt University, Charité, Campus Berlin Buch, Robert-Rössle Hospital, HELIOS Klinikum, Berlin, Germany.

Correspondence: Address correspondence and reprint requests to: Peter M. Schlag, MD, PhD, Department of Surgery and Surgical Oncology, University Hospital Charité, Campus Buch, Humboldt University to Berlin, Robert-Rössle Klinik at the HELIOS Klinikum Berlin, Lindenberger Weg 80, 13125 Berlin, Germany; Fax: 49-30-9417-1404; E-mail: schlag{at}rrk-berlin.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The extent of standard lymph node dissection (D1, D2, or D3) in gastric cancer patients is still controversial. Several prospective European trials attained contradictory results. A generally increased body mass index (BMI) of the European patients was assumed to be one of the major causes for postoperative morbidity.

Methods: We evaluated the effect of BMI on the quality of routine D2 lymph node dissection and on postoperative morbidity in patients with gastric cancer who underwent a potentially curative total gastrectomy. A total of 199 consecutive gastric cancer patients who underwent a total gastrectomy and a routine D2 lymph node dissection between 1992 and 2001 were included in the study. According to BMI, they were assigned to three groups: group A, with BMI <25 kg/m2 (normal body weight); group B, with BMI of 25 to 30 kg/m2 (overweight); and group C, with BMI >30 kg/m2 (obesity). Parameters such as complete histopathological staging, intraoperative blood loss, length of operation, and surgical and nonsurgical morbidity were recorded and correlated within the different groups.

Results: No significant differences were found with regard to the number of examined lymph nodes, blood loss, length of operation, surgical complications, or length of stay in the intensive care unit.

Conclusions: In contrast to comparable Japanese studies, our analysis reveals that even for overweight patients, a standard D2 lymph node dissection is justified without significantly increased morbidity.

Key Words: Gastric cancer • D2 lymph node dissection • Body mass index • Morbidity


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The issue about the extent of lymph node dissection has been a matter of controversial discussion for years. The results of the Japanese Research Group for Gastric Cancer (JRSGC), routinely performing D2 lymph node dissection since 1963, show a consecutive increase in 5-year survival rates from 41.2% to 63.8%.1,2 One of the reasons could be a decrease in local recurrence rates from 38% (1967–1971) to 12% (1982–1986).3–5 However, several prospective randomized European studies revealed no unequivocal survival benefit after D2 lymph node dissection.6–9 The problems of these studies, describing high incidences of pancreatic resections and splenectomies and low annual rates of operations per year at each participating center, were widely discussed. The main argument against D2 lymph node dissection was the increased postoperative morbidity and mortality rate compared with D1 resection. An increased body mass index (BMI) causing technical difficulties in D2 lymphadenectomy (LD) may be assumed as one of the reasons. More than 50% of the adults in Europe are overweight (BMI between 25 and 30 kg/m2) or obese (BMI >30 kg/m2).10 Compared with the Japanese population, the Western European patients have a higher body weight, are older at time of first tumor diagnosis, show a higher incidence of concomitant disease, and, in general, reveal more proximally located tumor sites.11–13 Compared with the US population, Europeans have a lower average BMI (24.7 to 27.8 kg/m2).14–16 The technical difficulties in D2 lymph node dissection of obese patients are based on the assumption that more fat, blood, and lymph vessels, as well as parts of the sympathic and parasympathetic nerve system, have to be removed, potentially inducing an increased rate of postoperative complications.6–9,17,18 Only two publications have investigated the influence of an increased body weight in selected patients after D2 lymph node dissection.23,24 Therefore, we investigated the effect of BMI in patients who underwent total gastrectomy with D2 lymph node dissection on the length of surgical intervention, intraoperative blood loss, postoperative morbidity, and the average length of stay in the intensive care unit (ICU). A histopathologic staging, with its implications for the oncological cure, and the postoperative treatment were taken into consideration as well.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All patients with gastric adenocarcinoma who underwent total gastrectomy and D2 LD from 1992 to 2001 at the Robert-Rössle Hospital were included in this study. Patients with subtotal gastrectomy, including patients with resection of the cardia/fundus, were excluded from the study. We performed D2 LD according to the criteria of the Japanese Research Society for Gastric Cancer.1,2 It included all first-level perigastric lymph nodes and left gastric artery, hepatic artery, proximal splenic artery, and celiac artery lymph nodes of the second level. All specimens were sectioned and investigated for lymph node metastasis at the Department of Pathology of the Robert-Rössle Hospital. The patients were assigned to three groups according to their BMI: group A, BMI <25 kg/m2 (normal weight); group B, BMI 25 to 30 kg/m2 (overweight); and group C, BMI >30 kg/m2 (obesity). We registered and compared sex, concomitant diseases, tumor infiltration (pT), lymph node status (pN; 1997 International Union Against Cancer classification), number of examined lymph nodes, number of infiltrated lymph nodes, lymph node ratio, operation time, blood loss, length of stay at the ICU, postoperative surgical and nonsurgical complications, and hospital mortality in each of the BMI groups. The patient data were analyzed on a personal computer by using SPSS for Windows (version 10.0; SPSSTM, Inc., Chicago, IL). All values were presented as median with minimum and maximum. Statistical analysis was performed with the Kruskal-Wallis test, Mann-Whitney U-test, and {chi}2 test. The level of significance was assumed at P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A total of 199 patients, who underwent total gastrectomy and D2 lymph node dissection, were included in the study. Eighty-two patients were selected in BMI group A, 81 in group B, and 36 in group C. Gender and age were evenly distributed between these groups. Depth of tumor infiltration and metastatic lymph node infiltration were significantly increased in group A compared with groups B and C (Table 1). Groups B and C showed a higher rate of comorbidity, such as diabetes and hypertonia, compared with group A. The prevalence of additional concomitant diseases was not statistically significant different in the three groups (Table 2). The average time of surgery was 300 minutes (range, 93–540 minutes) in group A, 300 minutes (range, 90–480 minutes) in group B, and 312 minutes (range, 200–450 minutes) in group C, and it did not reveal any statistically significant difference (Fig. 1). A median blood loss was registered as 511 mL (range, 100–3100 mL) in group A, 512 mL (range, 100–2000 mL) in group B, and 536 mL (range, 100–1300 mL) in group C, not differing significantly (Fig. 2). The average time in the ICU was 7 days (range, 0–68 days) in group A, 6 days (range, 0–47 days) in group B, and 7.5 days (range, 0–58 days) in group C, and there was no significant difference (P = .3). The median number of examined lymph nodes was 33 (range, 10–101), with a median number of tumor-infiltrated nodes of 2 (range, 0–67) (Fig. 3). The distribution within each BMI group is listed in Table 3. The postoperative morbidity for surgical and nonsurgical complications is listed in Table 4. The postoperative lethality was 3.5% overall and did not vary significantly in all three groups investigated (3.7%, 3.7%, and 2.8%). The postoperative surgical complications were not significantly different (P = .27). However, whereas the most important nonsurgical complications (pulmonary, cardiac, cerebral, and renal) were not significantly different, the total nonsurgical complications showed a significant increase in group C (BMI >30 kg/m2) because of further complications such as catheter infections, polyneuropathy, postoperative hypertension, and ear-nose-throat infections.


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  		TABLE 1. Data of the patients and tumors
 

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  		TABLE 2. Concomitant disease, n (%)
 


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  		FIG. 1. Median operation time (minutes) of patients with D2 lymph node dissection according to three body mass index (BMI) groups (P = .16).

 


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  		FIG. 2. Median blood loss (mL) of patients with D2 lymph node dissection according to body mass index (BMI) groups (P = .86).

 


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  		FIG. 3. Median number of examined lymph nodes according to three body mass index (BMI) groups of patients with D2 lymph node dissection (P = .107).

 

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  		TABLE 3. Median number of examined and diseased lymph nodes and lymph node ratio of BMI groups (minimum/maximum)
 

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  		TABLE 4. Postoperative complication rates, n (%)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
At present, the preoperative visualization of the individual extent of metastatic lymph node disease in gastric cancer patients is not yet possible with satisfying accuracy. Efforts with lymphatic mapping and the detection of sentinel lymph nodes in gastric cancer intend to individualize the lymph node dissection in patients with early gastric cancer but still lack clinical evidence.19–22,25,26 Thus, preoperative shortcomings in the nodal status urge the surgeon to perform a standardized lymph node dissection guided by anatomical compartments. The extent of this dissection is still a matter of discussion, but the high incidence of advanced carcinomas with an increased probability of positive D2 lymph nodes in Europe, the obviously high incidence of occult micrometastasis, and the prevalence of skip metastasis in up to 20% of the cases may favor a routine D2 lymph node dissection, at least for European patients.27–36 However, the outcome of D2 lymph node dissection may be influenced by increased body weight and, therefore, may imply a (relative) contraindication for the subgroup of obese patients. Our results failed to support this conclusion. We could not find any significant correlation between the BMI and the number of resected and examined lymph nodes. Bias due to low rates of resected lymph nodes can be excluded because for D2 LD, a median of 33 (range, 10–101) lymph nodes per patient was removed, including >25 lymph nodes per patient in 77% of the patients. According to the International Union Against Cancer staging criteria, 15 removed lymph nodes are necessary to obtain valid information about lymph node status; according to the experience of the German Gastric Cancer Study Group and the Japanese Gastric Cancer Association, 25 lymph nodes are necessary.1,37 In the different BMI groups, the number of lymph nodes examined was 36 in group A, 32 in group B, and 27 in group C (Table 3). The difference was not statistically significant (P = .107). However, the numbers may represent a tendency toward fewer lymph nodes being examined in more obese patients. This would be in accordance with the results by Dhar et al., who examined 21 nodes in the higher-BMI group and 28 nodes in the lower-BMI group.23 The underlying reason may be that it is considerably more difficult for pathologists to prepare the lymph nodes in surgical specimens of obese patients.

The inverse correlation between BMI and involved lymph nodes or a lymph node ratio can be explained by slightly deeper tumor infiltration in slim patients. Obviously, the advanced tumor stages of group A patients not only result in a higher rate of metastases, but also cause a net loss of body weight, which is reflected by the lower BMI of this group.

Moreover, the study failed to show any correlations between BMI and operation time, intraoperative blood loss, surgical complications, and important nonsurgical complications. The overall rate of other nonsurgical complications of patients with increased BMI is not due to D2 LD, but to other general risk factors that cause catheter infections, polyneuropathy, postoperative hypertension, or ear-nose-throat infections.

The apparent contradiction of our results compared with those reported from Japanese studies may be explained by the general composition of the gastric cancer population.23,24 The Japanese studies included 13% to 23% of obese or overweight patients, whereas 60% of our patients had BMI >25 kg/m2. Because of a high volume of diverse patients and population-based differences in their characteristics, it can be assumed that in general, our center benefits from its extensive experience in treating overweight patients. This experience concerns not only surgical expertise, but also early postoperative management, including aggressive approaches for the prevention of respiratory complications or early mobilization. We conclude that an increased BMI is not a contraindication for D2 LD in gastric cancer patients if it is performed in an experienced center. Concern about comorbidity is important for a preventive perioperative strategy to avoid perioperative complications.


   Acknowledgments
 
The authors thank Ch. Kettelhack, MD, PhD, for critical reading the manuscript. They also thank Tania Schink and Ingo Hoffmann for statistical evaluation.

The acknowledgments are available online at www.annalssurgicaloncology.org.


   Footnotes
 
The influence of the body mass index (BMI) on the quality of routine D2 lymph node dissection and on the postoperative outcome of patients with gastric cancer was evaluated. No significant differences were found among three BMI groups (A, <25 kg/m2; B, 25–30 kg/m2; and C, >30 kg/m2).

Received for publication July 8, 2002. Accepted for publication December 6, 2002.


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 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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