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10.1245/s10434-006-9235-1
Annals of Surgical Oncology 14:1288-1294 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Abdominal Shape of Gastric Cancer Patients Influences Short-Term Surgical Outcomes

Jun Ho Lee1, Yong Hae Paik1, Jong Seok Lee1, Keun Won Ryu1, Chan Gyoo Kim1, Sook Ryeon Park1, Young Woo Kim1, Myeong Cherl Kook1, Byung-ho Nam2 and Jae-Moon Bae1,3

1 Research Institute and Hospital, National Cancer Center, 809 Madu1-dong, Ilsandong-gu, Goyang-si, Gyeonggi-do, 411-769, Korea
2 Cancer Biostatistics Branch, Research Institute for National Cancer Control & evaluation, National Cancer Center, 809 Madu1-dong, Ilsandong-gu, Goyang-si, Gyeonggi-do, 411-769, Korea
3 Center for Gastric Cancer, Research Institute & Hospital National Cancer Center, Madu-dong 806 Dongilsan-gu Goyang-si, Gyeonggi-do, 411-764, Korea

Correspondence: Address correspondence and reprint requests to: Jae-Moon Bae. Center for Gastric Cancer, Research Institute & Hospital National Cancer Center, Madu-dong 806 Dongilsan-gu Goyang-si, Gyeonggi-do, 411-764, Korea; E-mail: jmoonbae{at}ncc.re.kr


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: There is a prevailing belief that both obesity and abdominal shape influence abdominal accessibility, and thus affect short-term surgical outcomes of gastric cancer surgery.

Methods: We measured the thickness of subcutaneous fat (SCF), abdominal anterior-posterior diameter (APD), transverse diameter (TD), and intra-abdominal fat volume (IFV) at the umbilicus level by using the abdominal CT scans of 291 gastric cancer patients who had undergone subtotal gastrectomy and D2 lymph node dissection. Clinicopathological factors including body mass index (BMI), APD, TD, IFV, and SCF and surgical outcomes, i.e., dissected lymph node number, morbidity, and mortality were analyzed.

Results: SCF thickness, APD, TD, IFV, and BMI mean values were 20.0 mm (range 2.0–64.0), 188.4 mm (range 128.0–332.0), 301.4 mm (range 160.0–651.0), 198.3 mm2 (range 123.4–312.1), and 23.9 kg/m2 (range 16.6–34.6), respectively. In male patients, APD was found to correlate with the number of retrieved lymph nodes (P = 0.045). Whereas in female patients, this was not the case (P = 0.093). Twenty-one patients experienced postoperative complications but no postoperative mortality occurred. Female patients who experienced postoperative complications had higher APD (32.9 ± 10.0 mm versus 26.1 ± 7.9 mm, P = 0.044) and BMI (27.3 ± 4.1 kg/m2 versus 24.3 ± 3.5 kg/m2, P = 0.049) values than those who did not.

Conclusions: We conclude that obesity and abdominal shape of gastric cancer patients both influence the short-term surgical outcomes of subtotal gastrectomy with D2 lymph node dissection.

Key Words: Body shape • Gastric cancer • Lymph node • Dissection


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Gastric cancer is the most common form of cancer in Korea,1 and the overall age-standardized incidence rates of gastric cancer in 2002 were 69.6 per 100,000 among males and 26.8 per 100,000 among females.2 D2 lymph node dissection remains a standard treatment method for gastric cancer,35 and although it increases the radical nature of surgical therapy, it also allows adequate lymph node staging.

Obesity is an expanding problem throughout the world,6 and substantially increases the risks of morbidity and mortality in patients who undergo abdominal surgery.710 Moreover, recent data suggests that the survivals of obese patients treated surgically for gastric cancer are compromised.11 Poor accessibility in the obese to lymph nodes deeply embedded in adipose tissues around major abdominal vessels predisposes such patients to unsuccessful lymph node dissection.11,12

However, abdominal shape may also influence accessibility in patients with gastric cancer. For example, a large anterior to posterior abdominal wall diameter may make it difficult to access the abdominal cavity. However, no data is available concerning the effects of abdominal shape on the surgical outcomes of gastric cancer patients.

Thus, we conducted this study to explore the effects of abdominal shape on gastric cancer patient short-term surgical outcomes in both genders, in terms of retrieved lymph node numbers, morbidities, and mortality.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The medical records and the abdominal CT scans of 291 patients who underwent subtotal gastrectomy at the Center for Gastric Cancer, National Cancer Center, Korea between January 1 and June 31, 2004 were reviewed. Subcutaneous fat thickness (SCF), abdominal anterior to posterior diameter (APD), and transverse diameter (TD) were measured and total intra-abdominal fat volume (IFV) at the umbilicus level was calculated using preoperative abdominal CT scans. The potential effects of clinicopathological factors, e.g., age, sex, and body mass index (BMI), on surgical outcome defined in terms of retrieved lymph node numbers, morbidities, and mortalities were investigated.

All the CT scans were performed within 4 weeks before surgery according to gastric cancer CT protocol as follows. CT scans were performed using a four channel multidetector CT (MX-8000, Philips Medical Systems, Highland Heights, OH) using the following parameters; 120 kVp, 250 mAs, 3.2 mm beam collimation, 1.625 pitch, 5 mm slice thickness, prone position with the stomach fully distended with water (a negative contrast medium) 65 s after contrast medium injection (Ultravist, Schering, Berlin, Germany) at a rate of 3 ml/s, and again in the right decubitus position 3 min after contrast medium injection. SCF, APD, and TD were measured using a picture archiving and communication system (Mview, Marotech, Seoul), IFV was measured using a 3D workstation (Rapidia, Infinitt, Seoul) by one person (YHB). SCF, APD, and TD were measured at the umbilicus level. SCF was measured from the anterior abdominal wall to the anterior aspect of the rectus abdominis muscle; APD was defined as the maximum distance between the anterior abdominal skin and the back skin vertically at supine position, and TD was defined as the maximal distance measured at right angles to the APD at supine position. The data used for measuring IFV were transferred using digital imaging and communications in medicine (DICOM) format to a workstation. Fat was defined as any area with Hounsfield intensity of between –250 and –50 HU. Intra-abdominal fat was defined as fat located in muscular abdominal structures (rectus abdominis, oblique muscles, back muscles). The workstation automatically calculated fat area densities inside of abdominal muscles drawn manually.

All patients enrolled in the present study underwent subtotal gastrectomy with D2 lymph node dissection. Four gastric cancer surgeons at our center performed gastric cancer surgery only, and for institutional standardization purposes, each surgeon initially acts as a first assistant during surgery for at least 3 months, regardless of previous fellowship training. Distal subtotal gastrectomy was performed if there was a tumor-free margin of 5 cm in the case of advanced gastric carcinoma or 2 cm in the case of early gastric carcinoma. Lymph node dissection extents are as described by the recommendations of the Japanese Research Society for Gastric Carcinoma.13 Cancers were staged according to the tumor node metastasis (TNM) classification system of the Union Internacional Contra la Cancrum (UICC), and potentially curative resection was defined as R0 resection in accord with the UICC residual tumor classification.14

All the specimens were sent to the department of pathology for pathological examination immediate after resection. Single pathologist (M. Kook) retrieved all the lymph nodes using palpation under gross inspection. All the pathological examinations were performed in a standard manner.

Statistical Analysis
Analysis of covariance was performed to examine the associations between SCF, APD, TD, IFV, and BMI (as independent variables) with outcome variables (the number of retrieved lymph nodes and morbidities). Patients who experienced postoperative complications were compared with those who did not with respect to SCF, APD, TD, IFV, and BMI using the Student’s t test. In addition, we investigated the possibility of an interaction between gender and AP with respect to each outcome variable. SAS ‘PROC GLM’ software was used throughout. P values of <0.05 were considered statistically significant. Bio-statistician (B.H. Nam, Ph.D.) performed all the statistical analysis.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Clinicopathological Characteristics of the Patients
Median patient age was 58 years (range 25–85 years), and there were 189 (64.9%) male patients and 102 (35.1%) female patients (Table 1Go). Fifty-two tumors (19.6%) were located in the middle third of the stomach. One hundred and fifty-two patients (52.2%) had early gastric cancer and 139 advanced gastric cancer (Table 1Go). All patients underwent distal subtotal gastrectomy with D2 lymph node dissection. The mean number of lymph nodes retrieved was 34.7 (range 10–79) and the mean operation time was 169.8 min (range 90–340). No difference was found between male and female patients with respect to age, tumor location, TNM stage, or the number of lymph nodes retrieved.


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TABLE 1. Clinicopathological characteristics of the patients
 
Abdominal Shapes and Body Mass Indexes
Mean SCF, APD, TD, IFV, and BMI were 20.0 mm (range 2.0–64.0), 188.4 mm (range 128.0–332.0), 301.4 mm (range 160.0–651.0), 198.3 mm2 (range 123.4–312.1) and 23.9 kg/m2 (range 16.6–34.6), respectively. Female patients had higher SCF, IFV, and BMI than male patients, as shown in Table 2Go.


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TABLE 2. Body shape and BMI of the patients
 
Abdominal Shape and Body Mass Index, and their relationships with retrieved Lymph Node Numbers and Operating Time
In male patients, the number of retrieved lymph nodes decreased with increasing quartiles of AP diameter of abdomen (F = 3.73, P = 0.012), whereas in female patients, no correlation was found (F = 1.53, P = 0.212) (Table 3aGo; Fig. 1Go). When we compared the top quartile with the bottom quartile, the number of retrieved lymph was different both in male (P = 0.008) and female patients (P = 0.045). An age-adjusted trend analysis showed that there was a significant decrease in the mean number of dissected lymph nodes as the quartile increased in male patients (P = 0.001), while in female patients, there was a borderline significance (P = 0.05). Similar results were demonstrated for the TD and IFV (Table 3aGo). The number of retrieved lymph nodes decreased with increasing quartiles of BMI in both genders (male patients, F = 5.36, P = 0.001; female patients, F = 2.92, P = 0.037, respectively).


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TABLE 3A. Number of retrieved lymph nodes for Categories of Body shape, BMI
 

Figure 1
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FIG. 1. Bar chart showing the mean number of retrieved lymph nodes in each quartile of the anterior to posterior diameter of abdomen. In male patients, the number of retrieved lymph nodes decreased with increasing quartiles of AP diameter of abdomen (F = 3.73, P = 0.012), whereas in female patients, no correlation was found (F = 1.53, P = 0.212).

 
Table 3bGo presents the operating time for each of body shape categories in both genders. The operating times were increased with increasing quartiles of SCF, AP diameters of abdomen, and BMI in male patients while these correlations were not found in female patients. Figure 2Go presents the relationship of the operating times and quartile of AP diameter of abdomen.


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TABLE 3B. Operating time for Categories of Body shape, BMI
 

Figure 2
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FIG. 2. Bar chart showing the mean operating time in each quartile of the anterior to posterior diameter of abdomen. In male patients, the mean operating time increased with increasing quartiles of AP diameter of abdomen (F = 5.13, P = 0.001), whereas in female patients, no correlation was found (F = 0.63, P = 0.598).

 
Abdominal Shape and BMI and their Relationships with Morbidities
Twenty-one patients (7.2%) experienced postoperative complications but there was no postoperative mortality (Table 4Go). The most common complication was wound infection (5 patients, 23.8%) followed by minor anastomotic leakage (4 patients, 19.0%). Leakages were treated conservatively in all but one patient who underwent reoperation. SCF and BMI differed in female patients who experienced a postoperative complication, and in female patients who did not experience a postoperative complication (Table 5Go).


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TABLE 4. Postoperative complications
 

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TABLE 5. Comparison of Body shape and BMI according to complication
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study revealed a significant negative relationship between abdominal shape, as determined by APD and IFV, and the number of lymph nodes retrieved. Age-adjusted trend analysis showed that there was a significant decrease in the mean number of retrieved lymph nodes as the quartile of APD increased in men, while in women, there was borderline significance. In female patients only, the SCFs and BMIs of those who experienced postoperative complications were higher than those who did not.

Obesity is known to increase the risk of morbidity and mortality in those who undergo abdominal surgery.710 Moreover, body mass index has been reported to be a poor prognostic factor in gastric cancer patients, and it has been suggested that poor accessibility to lymph nodes deeply embedded in adipose tissues around major abdominal vessels may predispose a patient to unsuccessful lymph node dissection.11,12

We found that poor abdominal wall accessibility during gastric cancer surgery is also influenced by patient body shape. Moreover, it is possible that abdominal shape may influence lymph node dissection, and thus result in down-staging or inaccurate nodal staging. In addition, a greater anterior to posterior abdominal wall distance and a larger intra-abdominal fat volume may make extra-perigastric lymph nodes difficult to access. In the present study, we found that these relations differed in men and women. Both male and female patients showed decreasing trend of the number of retrieved lymph nodes as increasing APD. This trend was stronger in male patients than in female patients. Differing abdominal wall distensibility in men and women due to muscle mass differences might explain why APD was found to be more strongly associated with the number of lymph nodes retrieved in male patients than in female patients.

Not only for a surgeon but also for a pathologist, obesity make it difficult to retrieve lymph nodes embedded in heavy fat tissue because fat infiltration makes it difficult to differentiate lymph nodes from surrounding fat tissues. However, a single experienced pathologist examined all the resected gastric specimens in a standard manner in this study. Thus, the main reason for fewer lymph nodes in obese patients in this study might be due to not the pathologist’s technique but surgical difficulties.

Although statistically insignificant, intra-abdominal fat volume was found to be better correlated with the number of lymph nodes retrieved in female patients. Abdominal obesity is known to be a characteristic feature of Asians, whereas Caucasians tend to develop generalized obesity.15,16 In terms of the impacts of abdominal obesity and distensibility on Asian patients undergoing gastric cancer surgery, the distensibility of the abdominal wall appears to be a problem in men, whereas abdominal fat volume is more of an issue in women.

No operative mortality occurred in the present study and the morbidity rate was 7.2%. These results are lower than expected, as recent reports quote morbidity rates of about 10%.17,18 Strict internal standardization and specialization may explain our low reported morbidity rates. The reason for the observed association between SCF and morbidities in female patients may be that subcutaneous fat is thicker and linea alba thinner in women. Half of the postoperative complications that occurred were due to wound infections. However, the reason for the association between BMI and postoperative complications in female patients only is unclear.

The reported numbers of lymph nodes retrieved at institutions vary and might be influenced by factors other than obesity and body shape, such as, TNM stage or the extent of gastric resection.19,20 In the present study, to minimize sampling bias, we only enrolled patients who had undergone subtotal gastrectomy; a larger scale exercise will be needed for more detailed subgroup analysis.

The present study suggests that abdominal shape and BMI influence the short-term surgical outcomes of gastric cancer patients who are treated by subtotal gastrectomy with D2 lymph node dissection and emphasizes the need for gastric cancer surgeons to consider abdominal shape, especially AP diameter and intra-abdominal fat volume, to reduce the risks of surgically associated sequelae.


    FOOTNOTES
 
No competing interests declared.

Received for publication November 11, 2005. Accepted for publication February 21, 2006.


    REFERENCES
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 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  12. Adachi W, Kobayashi M, Koike S, et al. The influence of excess body weight on the surgical treatment of patients with gastric cancer. Surg Today 1995; 25:939–945.[CrossRef][Medline]
  13. Japanese Research Society for Gastric Cancer: Japanese classification of gastric carcinoma. Tokyo: Kanehara & Co., LTD. 1995: 1–71.
  14. Sobin LH, Wittenkind C. International Union Against Cancer (UICC) TNM Classification of Malignant Tumours 5th ed. New York: Wiley-Liss; 1997 pp 59–62.
  15. Ferreira SR, Lerario DD, Gimeno SG, et al. Japanese-Brazilian Diabetes Study Group Obesity and central adiposity in Japanese immigrants: role of the Western dietary pattern. J Epidemiol 2002; 12:431–8.[Medline]
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  17. Sano T, Sasako M, Yamamoto S, et al. Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy–Japan Clinical Oncology Group study 9501. J Clin Oncol 2004; 22:2767–2773.[Abstract/Free Full Text]
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