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Annals of Surgical Oncology 9:5-12 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Adverse Effects of Perioperative Transfusion on Patients With Stage III and IV Gastric Cancer

Woo Jin Hyung, MD, Sung Hoon Noh, MD, Dong Woo Shin, MD, Ji Hun J. Huh, BA, Bong J. Huh, MD, Seung Ho Choi, MD and Jin Sik Min, MD

From the Department of Surgery (WJH, SHN, DWS, SHC, JSM) and the Cancer Metastasis Research Center (WJH, SHN), Yonsei University College of Medicine, Seoul, Korea; Washington University, School of Medicine (JHJH), St. Louis, Missouri; and Liverpool Hospital Center (BJH), Liverpool, Australia.

Correspondence: Address correspondence and reprint requests to: Sung Hoon Noh, MD, Department of Surgery, Yonsei University College of Medicine, C.P.O. Box 8044, Seoul, Korea; Fax: 82-2-313-8289; E-mail: sunghoonn{at}yumc.yonsei.ac.kr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The degree of immunomodulation by perioperative blood transfusion and its resultant effects on cancer surgery are a subject of controversy. We evaluated the prognostic effects of perioperative blood transfusion on gastric cancer surgery.

Methods: A total of 1710 patients who underwent curative gastrectomy for gastric cancer from 1991 to 1995 were retrospectively reviewed. Uni- and multivariate analyses of the incidence, amount, and timing of perioperative blood transfusions and a comparison of the clinicopathological features were performed.

Results: A higher incidence of blood transfusions was associated with female sex, large tumors, upper-body location, Borrmann type III or IV lesions, longer operations, total gastrectomies, splenectomies, and D3 or more extended lymphadenectomy. The tumors in the transfused group were more advanced in depth of invasion and nodal classification. More frequent tumor recurrences were found in the transfused group. A dose-response relationship between the amount of transfused blood and prognosis was evident. Subgroup analyses of prognosis according to stage showed significant differences in stages III and IV between the transfused and nontransfused groups. On multivariate analysis, transfusion was shown to be an independent risk factor for recurrence and poor prognosis.

Conclusions: These results suggest that perioperative transfusion is an unfavorable prognostic factor. It is thus better to refrain from unnecessary blood transfusion and to give the least amount of blood to patients with gastric cancer when transfusion is inevitable, especially for those with stage III and IV gastric cancers.

Key Words: Transfusion • Immunomodulation • Gastric cancer • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Blood transfusion may result in immunological changes, or immune modulation, which is beneficial to some patients but harmful to others.1,2 Immunomodulating effects associated with homologous blood transfusion were first observed in renal allograft transplantations, and these effects led to better survival rates.3 Many experimental and clinical studies have shown that perioperative blood transfusion, probably because of immunosuppression, has an adverse effect on outcome after surgery for hepatocellular carcinoma, breast cancer, head and neck cancer, lung cancer, soft-tissue sarcoma, osteosarcoma, and prostate cancer.4–10 Moreover, many studies using multivariate or meta-analysis of individual retrospective studies strongly support the concept that allogeneic blood transfusion increases cancer recurrence after a potentially curative surgical resection.11–13 However, studies that have analyzed the influence of perioperative transfusions on recurrence or survival for gastric cancer are contradictory.14–20

We performed a retrospective study to investigate whether perioperative blood transfusions significantly affect recurrence and survival in patients undergoing curative gastric resection for gastric cancer. We also investigated the relationship between the prognosis and the amount of transfused blood.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From January 1991 to December 1995, 1844 patients underwent curative gastrectomy (R0 resection according to the International Union Against Cancer [UICC]21) for gastric adenocarcinoma at the Department of Surgery, Yonsei University College of Medicine, Seoul, Korea. Eighteen patients who had a history of other-organ cancer before operation and 32 patients with gastric remnant cancer were excluded from the study. Also, 84 patients who either had fewer than 15 lymph nodes retrieved or had undergone D1 lymph node dissection were excluded because these cases could possibly have been inadequately staged. As a result, 1710 patients were analyzed and divided into two groups: transfused and nontransfused.

The transfused group consisted of those who received perioperative blood transfusion, defined as either whole blood or packed red blood cells administered within 14 days before surgery, during surgery, or 14 days after surgery. The incidence, amount, and timing of perioperative blood transfusions were analyzed. The clinicopathological features, tumor recurrences, and survival rates between the two groups were also compared. Histological slides and resected specimens were reviewed to confirm the diagnosis and to study the following pathologic features: location, macroscopic type and size of the primary tumor, depth of invasion, and nodal status. Other variables analyzed included age, sex, hemoglobin level on admission, the duration of operation, the type of operation, splenectomy, the extent of lymph node dissection, anticancer chemotherapy, and stage by the new tumor, node, metastasis system of the UICC.21 As for the histological classification, tubular carcinoma and papillary adenocarcinoma were classified as differentiated type, whereas poorly differentiated adenocarcinoma, mucinous adenocarcinoma, and signet-ring cell carcinoma were classified as undifferentiated type.

The following standardized operative procedures were performed: (1) total or distal subtotal gastrectomies were performed, depending on the location and macroscopic type of gastric cancer; and (2) for early gastric cancer, D2 lymphadenectomy was performed, whereas for advanced gastric cancer, D3 lymphadenectomy was usually performed, according to the rules of the Japanese Research Society for Gastric Cancer.22 The definitions as to the extent of the lymphadenectomy are as follows. The regional lymph nodes of the stomach were classified into four compartments. Compartment 1 consisted of the perigastric lymph nodes. Compartment 2 consisted of lymph nodes along the left gastric artery, along the common hepatic artery, around the celiac axis, and along the splenic artery. Compartment 3 consisted of lymph nodes in the hepatoduodenal ligament, at the posterior aspect of the head of the pancreas, and at the root of the mesenterium. When the cancer was located in the lower third of the stomach, lymph nodes along the splenic artery were classified as compartment 3. Compartment 4 consisted of lymph nodes along the middle colic vessels and the para-aortic lymph nodes. The anatomical level of D2 lymphadenectomy included complete dissection of compartments 1 and 2; D3 lymphadenectomy included that of compartments 1, 2, and 3; and D4 lymphadenectomy included dissection of all four compartments.

In our institute, the principles of adjuvant chemotherapy are as follows. For early gastric cancer patients, no adjuvant chemotherapy is performed. For advanced gastric cancer patients, fluorouracil-based adjuvant chemotherapy is given, except for patients with T2N0M0 stage.

All the statistical analyses were performed with the statistical software SPSSTM version 9.0 for Windows (SPSS, Inc., Chicago, IL).23 The intergroup comparisons of clinicopathological variables were made by using Student’s t-test for continuous variables and two-tailed {chi}2 tests for discrete variables.

Follow-up of patients was completed until death or until the date of last follow-up of December 31, 1999. At the time of the last follow-up, 57 patients (3.3%) had been lost to follow-up. The median follow-up interval for patients alive at the incised date was 70 months (range, 48–106 months). Postoperative mortalities, defined as mortalities occurring within 30 days after operation, occurred in nine cases (.5%).

The lost cases and operative mortality cases were treated as censored data for the analysis of survival rates. The Kaplan-Meier method was used for calculating the survival rate, and the difference between the curves was assessed with the log-rank test.24 Risk factors influencing recurrence were determined by logistic regression analysis. A multivariate analysis of the prognostic factors was performed with the Cox proportional hazard model.25 The relative risk in the multivariate analysis was defined as the ratio of the probability that an event (recurrence or death) would occur to the probability that it would not occur. The prognostic power of covariates was expressed by calculation of a relative risk with a 95% confidence interval. The accepted level of significance was P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Incidence and Patterns of Transfusion
Among the 1710 patients, 757 (44.3%) underwent blood transfusions; the remaining 953 (55.7%) received no transfusion. The majority of transfused patients (438 patients, 57.9%) received 2 U of blood or less, whereas 131 patients (17.3%) received more than 4 U (Table 1). Most patients (61.5%) were transfused intraoperatively, postoperatively, or both (Table 1).


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  		TABLE 1. Incidence, timing, and amount of transfusion
 
Comparison of the Clinicopathologic Features
A higher incidence of blood transfusions was associated with female sex, large tumors, upper body location, Borrmann type III or IV lesions, longer operations, total gastrectomies, splenectomies, and D3 or more extended lymphadenectomy (P < .05). The patients in the transfused group underwent adjuvant chemotherapy more frequently than did the nontransfused patients. Because tumors in the transfused group were more advanced in depth of invasion and nodal stage, the tumor, node, metastasis stages of the transfused group were also more advanced (Tables 2–4).


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  		TABLE 2. Demographic and perioperative data between transfused and nontransfused patients
 

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  		TABLE 3. Pathologic data between transfused and nontransfused patients
 

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  		TABLE 4. Tumor, node, metastasis classification, stage, and recurrences between transfused and nontransfused patients
 
Comparison of Recurrence and Prognosis
Cancer recurrences were more frequently detected in the transfused group (33.7%) than in the nontransfused group (21.2%; P < .001; Table 4). The cumulative survival rate was significantly higher in the nontransfused than in the transfused group (P < .0001); the 5-year survival rates were 74.1% for the nontransfused group and 55.6% for the transfused group. A dose-response relationship between the amount of transfused blood and prognosis was evident. A significant difference in the survival rates according to the amount of transfused blood was noted (P < .0001). The 5-year survival rates were 60.7% with 1 to 2 U, 55.4% with 3 to 4 U, and 38.2% with more than 4 U (Fig. 1).



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  		FIG. 1. Cumulative survival curves according to the amount of transfusion (P < .0001, log rank test). The 5-year survival rate was significantly decreased as the amount of transfusion increased: 74.1% for nontransfused, 60.7% for 1 to 2 U, 55.4% for 3 to 4 U, and 38.2% for more than 4 U.

 
In a comparison of survival rates based on tumor, node, metastasis stage between the two groups, a better survival rate in stage I and II was observed in the nontransfused group, although no statistically significant difference was found (Fig. 2). Significant differences in survival rates were found in stage III (P = .0028) and stage IV (P = .0045). The 5-year survival rates were 41.8% for the transfused group and 53.3% for the nontransfused group in stage III; they were 11.7% for the transfused group and 21.5% for the nontransfused group in stage IV (Fig. 3).



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  		FIG. 2. Cumulative survival curves for stage I gastric cancer patients with or without transfusion (P = .1235, log-rank test) and for stage II gastric cancer patients with or without transfusion (P = .2795, log-rank test). The 5-year survival rates were 88.7% for transfused patients and 92.1% for nontransfused patients in stage I; they were 70.1% for transfused patients and 73.5% for nontransfused patients in stage II.

 


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  		FIG. 3. Cumulative survival curves for stage III gastric cancer patients with or without transfusion (P = .0028, log-rank test) and for stage IV gastric cancer patients with or without transfusion (P = .0045, log-rank test). The 5-year survival rates were 41.8% for transfused patients and 53.3% for nontransfused patients in stage III; they were 11.7% for transfused patients and 21.5% for nontransfused patients in stage IV.

 
Logistic regression analysis for tumor recurrence revealed that transfusion was an independent risk factor (relative risk, 1.43; 95% confidence interval, 1.10–1.86; P = .0075; Table 5). In multivariate analysis by Cox’s proportional hazard model, the transfusion was an independent prognostic factor (relative risk, 1.55; 95% confidence interval, 1.24–1.95; P = .0008), as did age, type of operation, macroscopic type, tumor size, depth of tumor invasion, and lymph node involvement (Table 6).


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  		TABLE 5. Logistical regression analysis of risk factors for recurrence
 

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  		TABLE 6. Cox’s proportional hazard model analysis of prognostic factors
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The main findings of this study are that (1) a dose-response relationship between the amount of transfused blood and prognosis exists and that (2) transfusion is an independent risk factor for recurrence and poor prognosis.

Exposure to a foreign antigen can induce both immune activation and immunosuppression. Although there have been several reports on the detrimental effects of perioperative blood transfusions in patients undergoing surgery for cancer, it has been difficult to prove that there is any causal relationship between transfusions and poor survival rates. The most frequently suggested explanation for the adverse effect of transfusion on the survival of cancer patients is the role of nonspecific immunosuppression, probably because of increased activities of suppressor T lymphocytes, decreased natural killer cell activity, stimulated anti-idiotypic antibody production, and impaired lymphocyte blastogenesis.26 However, there are several compounding factors, such as cancer bleeding, anemia caused by long-standing malnutrition, and the extent of lymph node dissection for curative surgery, with which perioperative blood transfusions are inevitably linked. Busch et al.27 have reported in their prospective study that the prognosis of patients with colorectal cancer who received allogeneic or autologous blood transfusions demonstrated a lower survival rate, without any particular difference in survival between the two differently transfused groups. They have also pointed out that it is not the transfusion itself that results in poor prognosis in transfused patients, but rather it is a combination of several other factors, such as more advanced stage of the disease with a greater blood loss during the dissection of tumors, the skills of surgeons, and the nutritional status of patients.

Among the treatment factors, total gastrectomy, splenectomy, D3 or more extended lymphadenectomy, and postoperative adjuvant chemotherapy were the factors that were associated with transfusion in our study. However, the above treatment factors were more frequently performed in the advanced stages. The incidences of these factors were similar in each stage irrespective of transfusion having taken place. Our results suggested that surgery for advanced gastric cancer itself is the most important factor necessitating perioperative blood transfusions, because the majority of patients with advanced stages were transfused intraoperatively, postoperatively, or both. Therefore, early diagnosis remains a prerequisite for avoiding transfusion.

In both retrospective and prospective randomized studies, many attempts to determine the effects of perioperative transfusion have been made, and yet their results have been contradictory and even confusing.14–20 For example, some reports have demonstrated the adverse effect of transfusion on the prognosis of patients with gastric cancer,14–18 whereas others have shown that allogeneic blood transfusions do not seem to have deleterious effects on the 5-year survival rates of patients who undergo curative surgery for gastric carcinoma.19,20 These contradictory results may arise through inadequate study design, inadequate eligibility criteria, small sample sizes, or inadequate statistical analysis. There has been no study confirming the dose-response relationship between the amount of transfused blood and prognosis. This study of 1710 curatively resected patients performed during a relatively short period has advantages in having enough patients to compare prognosis in each stage, in showing a dose-response relationship between the amount of transfused blood and prognosis, and in using adequate eligibility criteria by excluding patients who had a possibility of inaccurate staging. The limitations are that this study was performed retrospectively and included only curatively gastrectomized patients; therefore, evaluation of the various types of treatment modalities or of the patients who could not undergo curative gastric resection was impossible.

This study showed a significantly poor survival rate in the transfused group, and a dose-response relationship was evident. The comparison in stages III and IV revealed significant differences in the 5-year survival rate, whereas that in stages I and II did not. Recurrences were also more frequently observed in the transfused group. Heiss et al.28 have reported that the prognostic effect of transfusion is mediated through its effect on minimal residual disease in resected-cancer patients. They have observed that transfusion-associated immune modulation affects minimal residual disease after curative tumor resection. They have also witnessed that quantitative assessment of tumor cells in bone marrow during follow-up demonstrated a significant quantitative increase of tumor cells in transfused patients only.28 The further the stage advances, the greater the possibility of minimal residual disease, even when curative surgery is performed. In advanced stages, immunosuppression may cause progression of metastatic foci and failure to remove circulating cancer cells and cells in bone marrow. These findings may support our results that there are significantly different recurrence and survival rates between transfused and nontransfused groups, especially in advanced stages.

Until now, there have been no reports concerning the benefits of transfusion on the outcome of oncologic surgery, and the treatment results of gastric cancer recurrence remain dismal.29,30 Therefore, it is crucial to refrain from unnecessary blood transfusion. Presumably, in similar cases when the transfusion need is clinically equivocal, it should be avoided. Considering the dose-response relationship between the amount of received blood and prognosis, transfusing the least amount possible would be helpful when transfusion is inevitable. Therefore, attention should be directed toward minimizing operative blood loss and transfusing only for factors known to be clinically important, such as oxygen delivery and hemodynamics, and not for arbitrary hemoglobin levels.

Recently there have been several reports that the use of recombinant human erythropoietin could reduce the need for blood transfusions in patients undergoing major surgery.31 It has also been reported that red blood cell substitutes, such as cell-free hemoglobin, perfluorocarbon emulsions, or liposome-encapsulated hemoglobin, are solutions that can potentially be used in emergencies or during surgery when the rapid expansion of blood volume with an oxygen carrier is needed.32 Although the clinical implications of red blood cell substitutes and recombinant human erythropoietin have not yet been proven, the use of these materials in addition to other methods for reducing blood loss during the operation (such as anatomical dissection and meticulous bleeding control with electrocoagulation, ultrasonic, and laser devices) may reduce the incidence and the amount of perioperative blood transfusion.33 In this study, most patients were transfused 2 U of blood or less (57.9%) and were transfused intraoperatively, postoperatively, or both (61.9%). Thus, if these alternative methods are used for minimizing blood loss during the operation or reducing the amount to be transfused, it will be feasible to lessen the adverse effects of transfusion.

In conclusion, although the advanced stage of tumor and extended surgery necessitate perioperative transfusion, transfusion itself is an unfavorable prognostic factor, and thus it is better to refrain from unnecessary transfusion and to give the least possible amount of blood to patients with gastric cancer when it is inevitable, especially for those with stage III and IV gastric cancers.


   Acknowledgments
 
The authors thank David Atherton for his editorial comments on the manuscript.

Received for publication March 5, 2001. Accepted for publication August 29, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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