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10.1245/ASO.2004.03.048
Annals of Surgical Oncology 11:682-689 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Association of Splenectomy With Postoperative Complications in Patients With Proximal Gastric and Gastroesophageal Junction Cancer

Jürgen Weitz, MD, PhD, David P. Jaques, MD, FACS, Murray Brennan, MD, FACS and Martin Karpeh, MD, FACS

From the Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: David P. Jaques, MD, FACS, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021; Fax: 212-717-3645; E-mail: jaquesd{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Splenectomy has been associated with increased morbidity after gastrectomy for gastric cancer. Resection of proximal versus distal tumors is associated with a higher morbidity. Because splenectomy is more commonly performed in resection of proximal tumors, these analyses may be biased. The aim of this study was to describe the association of splenectomy with complications in patients undergoing resection of proximal gastric and gastroesophageal junction (GEJ) cancers.

Methods: From July 1985 to August 2001, 335 patients underwent resection of proximal gastric or GEJ (type II and III) cancers. Clinical and pathologic factors were retrieved from a prospective database.

Results: Overall morbidity was 59% (infectious complications, 41%; noninfectious complications, 36%), and mortality was 4.5%. Splenectomy was associated with a higher rate of infectious complications (57% vs. 33%; P < .01) but not of noninfectious complications (39% vs. 34%; not significant) or mortality (4% vs. 5%; not significant). Splenectomy was also associated with a higher rate of infectious complications on multivariate analysis (hazard ratio, 2.4; P < .01).

Conclusions: Morbidity after resection of proximal gastric and GEJ cancer is significant; splenectomy is associated with increased morbidity, but not mortality, in these patients. Because these complications can be managed without an increase in mortality, splenectomy should be performed when indicated by the extent of the tumor.

Key Words: Gastric cancer • Gastrectomy • Splenectomy • Complications


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Gastric adenocarcinoma remains one of the most frequent solid-organ cancers in the world, with an estimated 21,600 new diagnoses and 12,400 deaths from disease in the United States in the year 2002.1 The only potentially curative treatment for gastric adenocarcinoma remains surgical resection with complete removal of the primary tumor and regional lymph nodes. Despite advances in perioperative management, gastric resections are still associated with significant morbidity ranging from 19% to 75% and with mortality ranging from 1.7% to 11.4%.2

Splenectomy, which is performed in an effort to increase tumor clearance or because of accidental injury, is associated with an increased incidence of postoperative infectious complications.3–6 Prospective, randomized trials, however, have not demonstrated an improved outcome for patients who undergo extended lymphadenectomy, splenectomy, or both.5–7 An increased incidence of complications and a lack of an improved outcome in patients who undergo splenectomy has led most authors to recommend splenic preservation in the surgical treatment of gastric cancer. In proximal gastric and gastroesophageal junction (GEJ) cancers, however, lymph node metastases are found more frequently in the splenic hilum. Therefore, some surgeons still consider splenectomy for these tumors.8–10

Several studies have investigated the association of splenectomy with postoperative complications in patients who undergo gastrectomy for gastric cancer. Because resection of proximal compared with distal gastric tumors is associated with higher morbidity and because splenectomy is more often performed in proximal tumors, these analyses may be biased. The aim of this study was to describe the association of splenectomy with complications in patients who undergo resection of proximal gastric and GEJ cancers.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patients and Treatment
The prospective gastric cancer database at Memorial Sloan-Kettering Cancer Center comprises 1598 patients who underwent resection of gastric adenocarcinoma between July 1, 1985, and July 30, 2001. From this database, we identified 335 patients with proximal gastric or GEJ cancer type II or III who underwent resection through a transabdominal or left thoracoabdominal approach. A tumor in the proximal third of the stomach was classified as a proximal gastric cancer; previously published guidelines were used to classify tumors at the GEJ.11

Patient demographics; tumor characteristics; treatment-related factors, including postoperative complications; and hospital course were analyzed. Perioperative transfusion was defined as allogeneic blood transfusion during surgery or the first two postoperative days. We did not include all transfusions the patients received during the hospital stay in this analysis, because some patients who developed complications received blood transfusions after the complication had developed. Inclusion of all transfusions would therefore bias the analysis of risk factors for complications.

Infectious complications included sepsis, anastomotic leak, intra-abdominal abscess, pancreatic fistula, infectious diarrhea, pneumonia, catheter sepsis, and wound and urinary tract infections. Noninfectious complications consisted of renal failure, postoperative hemorrhage, pulmonary embolism, atelectasis, cardiac complications, pneumothorax, pleural effusion, deep vein thrombosis, stroke, and urinary retention. The specific definitions of these complications have been published previously.2

The severity of complications was determined by using a grading system implemented at Memorial Sloan-Kettering Cancer Center. This system scores complications by severity from 1 to 5 (1, oral medication/bedside management; 2, intravenous treatment; 3, operative or radiological reintervention; 4, chronic disability; 5, death). Tumor stage and grade were classified according to the 5th edition of the tumor-node-metastasis classification by the International Union Against Cancer and the American Joint Committee on Cancer.12

Statistical Analysis
Statistical computations were performed with JMP (SAS Institute, Cary, NC) and SPSS (SPSS Inc., Chicago, IL). Continuous variables were expressed as medians and were compared by using the Wilcoxon test, whereas categorical variables were compared by using the Fisher’s exact or {chi}2 test. Multivariate logistic regression was performed by incorporating factors with a P value ≤.1 on univariate analysis. Statistical significance was defined as P ≤ .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patient Characteristics and Hospital Course
The median age of the 335 patients included in the study was 65 years (range, 21–89 years). The median operative time was 270 minutes (range, 100–625 minutes), the median blood loss was 650 mL (range, 50–6300 mL), and the median number of lymph nodes removed was 19 (range, 0–70). A complete macroscopic and microscopic resection (R0) was performed in 77% of patients (257 of 335), an R1 resection was performed in 10% of patients (35 of 335), and an R2 resection was performed in 13% of patients (43 of 335). The median hospital stay was 14 days (range, 6–93 days). Overall morbidity was 59% (197 of 335 patients): infectious complications occurred in 41% of patients (137 of 335), and noninfectious complications occurred in 36% of patients (120 of 335). Surgical revision was required in 10% of patients (34 of 335). Thirty-day mortality was 4.5% (15 of 335 patients). The main infectious complications were pneumonia (18%; 61 of 335 patients), anastomotic leakage (13%; 45 of 335 patients), wound infection (11%; 36 of 335 patients), and intra-abdominal abscesses (8%; 26 of 335 patients). The patient characteristics and incidences of complications are listed in Tables 1 and 2Go.


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  		TABLE 1. Patient characteristics
 

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  		TABLE 2. Postoperative course
 
Factors Associated With Splenectomy
In 31% of the patients (105 of 335), a splenectomy was performed. Reasons for splenectomy were as follows: extent of tumor in 23% of patients (77 of 335), bleeding in 5% of patients (18 of 335), and ischemia of the spleen in .3% of patients (1 of 335). The basis for splenectomy was unknown in 3% of patients (9 of 335).

Table 3 lists the patient and tumor characteristics associated with splenectomy. From this analysis, it is apparent that splenectomy was more commonly performed for larger, more advanced tumors.


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  		TABLE 3. Association of splenectomy with patient and tumor characteristics
 
The association of splenectomy with treatment-related factors and postoperative course is shown in Table 4. Splenectomy did not show an association with the number of removed lymph nodes (P = .06), but patients who underwent a splenectomy were more likely to have ≥14 lymph nodes removed (73% vs. 62%; P = .04). Splenectomy was associated with greater blood loss (1000 vs. 575 mL; P < .01), a higher transfusion rate (60% vs. 34%; P < .01), a longer hospital stay (15 vs. 14 days; P < .01), a higher reintervention rate (15% vs. 8%; P = .04), and a higher rate of infectious (57% vs. 33%; P < .01) but not of noninfectious (39% vs. 34%; not significant) complications. Splenectomy was specifically associated with a higher rate of grade 2 (26% vs. 16%; P = .03) and grade 3 (20% vs. 9%; P < .01) infectious complications, but mortality was not increased (4% vs. 5%; not significant). Pneumonia (34% vs. 11%; P < .01) and intra-abdominal abscesses (13% vs. 5%; P = .01) showed the strongest correlation with splenectomy.


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  		TABLE 4. Association of splenectomy with treatment-related factors and postoperative course
 
Univariate Analysis of Factors Associated With Complications
Table 5 depicts the univariate analysis of factors associated with postoperative infectious complications. Splenectomy, high American Society of Anesthesiologists (ASA) score, perioperative blood transfusion, longer operating room time, and blood loss ≥750 mL were associated with an increased incidence of such complications. No tumor-related factor—such as tumor-node-metastasis stage, tumor size, vascular or perineural invasion, or differentiation—was associated with infectious complications. The incidence of infectious complications in patients who underwent an unplanned splenectomy (for example, because of bleeding) was 47% (9 of 19), compared with 56% (43 of 77) in patients with a splenectomy due to the extent of the tumor (P = not significant). The rate of infectious complications in patients who underwent splenectomy and pancreatectomy was 58% (14 of 25), compared with 56% (46 of 80) in patients who underwent splenectomy alone (P = not significant).


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  		TABLE 5. Univariate analysis of factors associated with postoperative infectious complications
 
Factors associated with postoperative noninfectious complications on univariate analysis are listed in Table 6. Age >65 years, esophagogastrectomy, and an intrathoracic anastomosis were associated with such complications. No tumor-related factors showed an association with postoperative complications.


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  		TABLE 6. Univariate analysis of factors associated with postoperative noninfectious complications
 
Multivariate Analysis of Factors Associated With Complications
Multivariate analysis revealed that splenectomy had the strongest association with infectious complications (Table 7). High ASA score, blood loss >750 mL, prolonged operating room time, and preoperative weight loss were also associated with such complications. The only factors associated with noninfectious complications were age ≥65 years and an intrathoracic anastomosis (Table 7).


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  		TABLE 7. Multivariate analysis of factors associated with postoperative complications
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
This study investigated the association of splenectomy and other factors with postoperative complications in patients undergoing resection of proximal gastric or GEJ cancer. There is a considerable body of literature regarding the association of splenectomy with postoperative complications in patients with gastric cancer. Because resection of proximal gastric cancer is associated with a higher postoperative morbidity than resection of distal gastric cancer and because splenectomy is more often performed for proximal gastric cancers, the published studies might be biased.13,14 A comparison of the postoperative complications of patients undergoing resection of proximal versus distal gastric cancers without the need for splenectomy would be one way to address this bias. A second approach, which was chosen in this study, is to analyze the effect of splenectomy on morbidity in a homogenous patient group with proximal gastric and GEJ (type II and III) cancers.

The objective of splenectomy in the surgical treatment of gastric cancer is to facilitate a more complete lymphadenectomy by thorough clearance of the lymph nodes in the splenic hilum. This might be especially important in proximal gastric or GEJ cancers, which are known to have a higher incidence of lymph node metastases in the splenic hilum.8,9 Numerous retrospective, as well as prospective, randomized trials, however, have not demonstrated a prognostic benefit for splenectomy or extended lymphadenectomy.3,5–7,15 It is also well documented that a sufficient lymphadenectomy in the splenic hilum can be achieved without splenectomy and that a D2 lymphadenectomy can be performed without added morbidity, thereby demonstrating a differential effect of D2 lymphadenectomy and splenectomy on morbidity.16,17

Splenectomy has long been associated with postoperative infectious complications, as has been demonstrated in patients with benign diseases and incidental splenectomy.18,19 Three prior randomized trials drew conclusions regarding the effect of splenectomy on morbidity in patients undergoing resection of gastric cancer:3–6,20

In the randomized trial performed by Csendes et al.,6 splenectomy was associated with an increased risk of postoperative fever (50% vs. 39%; P < .04), pulmonary complications (35% vs. 24%; P < .08), and subphrenic abscess formation (11% vs. 4%; P < .05), but not of wound infections (18% vs. 11%; not significant). The incidence of reoperations (11.1% vs. 9.3%; not significant) and postoperative mortality (4.4% vs. 3.1%; not significant) did not differ between groups.

In the Dutch Gastric Cancer Trial, splenectomy was the most significant risk factor for overall complications, with a risk ratio of 2.13.20 In this trial, patients were randomized to a D1 versus D2 lymphadenectomy. In the D1 group, 11% of patients underwent a splenectomy and 3% underwent a pancreatectomy, compared with 37% and 30%, respectively, in the D2 group. Patients in the D2 group had a higher rate of complications (43% vs. 25%; P < .001) and postoperative death (10% vs. 4%; P = .004).5 In the Medical Research Council trial, patients randomized to the D2 group experienced higher rates of postoperative morbidity (46% vs. 28%; P < .001) and mortality (13% vs. 6.5%; P = .04), likely because of an increased incidence of pancreaticosplenectomy and splenectomy in the D2 group.4

Other factors also have to be considered when postoperative complications of gastric cancer are discussed. A large retrospective study, for example, identified male sex, age, type of procedure, lack of perioperative antibiotic prophylaxis, and splenectomy as independent risk factors.14 A recent study from our institution, which considered all patients with gastric cancer, identified resection of two or more organs as a significant risk factor for postoperative complications, and the spleen was the most frequent organ resected.15

This study is unique in that it studied several patient-, tumor-, and treatment-related factors in their association with postoperative complications in a homogenous patient group and in that it used a grading system for postoperative complications. The overall morbidity was 59% (infectious complications, 41%; noninfectious complications, 36%), reflecting the high efficiency of the reporting system for complications in our institution. The breakdown according to grade of complication demonstrates that 35% of all patients had a grade 1 or 2 complication (treated without reintervention). Seventeen percent of all patients had a grade 3 complication that led to surgery or another form of invasive reintervention. Chronic disability (grade 4 complication) occurred in 2.5% of patients, and perioperative mortality was 4.5%.

As expected, splenectomy was performed more often in advanced tumors, commensurate with our policy to perform a selective splenectomy. Splenectomy was associated with a higher rate of infectious complications (57% vs. 33%; P < .01), but not of noninfectious complications (39% vs. 34%; not significant) or mortality (4% vs. 5%; not significant). Splenectomy was specifically associated with a higher rate of grade 2 (26% vs. 16%; P = .03) and grade 3 (20% vs. 9%; P < .01) infectious complications. This analysis demonstrates that a substantial proportion of the complications associated with splenectomy led to a reintervention but that mortality was not increased. Pneumonia (34% vs. 11%; P < .01) and intra-abdominal abscesses (13% vs. 5%; P = .01) showed the strongest association with splenectomy, which is in accordance with the randomized trial performed by Csendes et al.6

On univariate analysis, splenectomy was also associated with more intraoperative blood loss, a higher rate of perioperative blood transfusions, and a longer hospital stay. On multivariate analysis, splenectomy was the strongest risk factor for infectious complications, with a hazard ratio of 2.4 (95% confidence interval, 1.3–4.4).

The increased incidence of infectious complications after splenectomy could be explained by impaired immunological function after splenectomy, because splenectomy is thought to be associated with impaired phagocytic activity, decreased antibody response, and altered levels of immunoglobulins and T-cell function.21 This concept is supported by clinical reports demonstrating a suppression of immune function after splenectomy in gastric cancer patients.22

Nonimmunological reasons for the increase in infectious complications should also be considered. Splenectomy, for example, increases the risk of pancreatic fistulas, which can cause subphrenic abscesses; in addition, splenectomy results in a relative dead space underneath the left diaphragm, and this potentially increases the risk of fluid accumulation and abscess formation.

We were able to identify factors other than splenectomy that were associated with infectious complications, such as an ASA score of III or IV or preoperative weight loss. High intraoperative blood loss and longer operative time, but not D2 lymphadenectomy, were also identified as independent risk factors. This analysis demonstrates the importance of considering not only splenectomy, but also other relevant factors, when infectious complications after gastric resection are discussed. Our study also demonstrates the importance of stratifying complications into infectious and noninfectious groups, because different risk factors can be identified for both groups. Grading the complications allows an assessment of the actual effect of the complications on the postoperative management of patients with gastric cancer.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Splenectomy is associated with an increased risk of infectious complications in patients who undergo resection of proximal gastric and GEJ (type II and III) cancers. Other patient- and treatment-related factors also have to be considered when the morbidity of these procedures is discussed. Our grading system for complications helps to assess the severity of complications associated with splenectomy. The complications after splenectomy can be managed without an increase in perioperative mortality. Our study further substantiates that a D2 lymphadenectomy can be performed without an increased risk of complications and that splenectomy and its influence on complications should be discussed independently of lymphadenectomy. Morbidity after resection of proximal gastric and GEJ cancer is significant. Avoidance of splenectomy, minimizing operating room time, and reducing blood loss might decrease postoperative infectious complications. Because most of the complications associated with splenectomy can be managed without increasing mortality, splenectomy should be performed when indicated by the extent of the tumor.


   ACKNOWLEDGMENTS
 
Supported by a grant from the Gelb foundation.


   FOOTNOTES
 
Splenectomy is the main risk factor for infectious complications after resection of proximal gastric and gastroesophageal junction cancers. However, other patient- and treatment-related factors also have to be considered when the morbidity of these procedures is discussed.

Received for publication March 8, 2003. Accepted for publication March 24, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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