British Journal of Urology (1992), 70, 135-138 01992 British Journal of Urology
Blood Transfusion and Survival Following Surgery for Renal Carcinoma T.-H. EDNA, K. VADA, F. HESSELBERG and 0. K. MJOLNERIZID Department of Surgery, Innherred Hospital, Levanger; Section of Urology, Department of Surgery, University Hospital, Trondheim,Norway
Summary-The effect of peri-operative blood transfusion on survival after surgery for renal carcinoma was studied in 201 patients. In addition to blood transfusion, several other factors were included in a multivariate analysis. Using Cox's proportional hazards model, transfusion of more than 4 units of blood was found to be an independent prognostic factor in addition to tumour stage, erythrocyte sedimentation rate and macrohaematuria.
Peri-operative blood transfusion has been reported to have a detrimental effect on survival following surgery for cancer. This may be due to the immunosuppressive effect of blood transfusion. Using multivariate analysis, the independent prognostic effect of transfusion has been studied. A negative effect on survival has been reported for prostate cancer (Heal et al. 1988; McClinton et al., 1990), colorectal cancer (Voogt et al., 1987; van Lawick van Pabst et al., 1988),lung cancer (Moores et al., 1989), cervical cancer (Blumberg et al., 1988) and osteosarcoma (Chesi et al., 1989). Others have found no independent effect on survival in colorectal cancer (Nathanson et al., 1985), gastric cancer (Kampschoer et al., 1989), lung cancer (Keller et al., 1988) and breast cancer (Voogt et al., 1987). Few studies have been done on the effect of blood transfusion on survival in renal carcinoma. A possible negative effect was reported by Mikulin et al. (1986) and Moffat and Sunderland (1985) but no such effect was found by Manyonda et al. (1986) and Moffat et al. (1987). We have studied survival in a larger series of patients after surgery for renal carcinoma, to determine the effect of transfusion in relation to other risk factors.
Accepted for publication 29 August 1991
Patients and Methods The records of 68 patients operated on for renal carcinoma at Innherred Hospital between 1969 and 1987 and 133 patients treated at the Regional Hospital of Trondheim between 1974 and 1987 were reviewed. The series included 108 men and 93 women whose median age at operation was 64 years (range 27-82). Information on peri-operative transfusion was gathered, together with data on known and possible risk factors such as age, sex, haemoglobin and erythrocyte sedimentation rate (ESR) on admission, microscopic or macroscopic haematuria, loin pain, pre-operative plugging of the renal artery, duration of operation, tumour stage and tumour size. Retrospective staging was assessed using the Robson classification (Robson et al., 1969). The vital status was known in all cases. Eight patients whose cause of death was uncertain were considered to have died from a disease not related to renal carcinoma. Those who died from causes other than renal carcinoma, or who survived until the end of the study, were treated as censored data. Adjusted survival rates were calculated by using death from renal carcinoma as the terminal event and death from an unrelated cause as a censored event.
135
136 The patients were divided into 3 groups. Group I received no transfusion during their hospital stay. Group I1 were given between 1 and 4 units of blood and group I11 received more than 4 units. Adjusted survival times for the groups were compared using the Kaplan-Meier product-limit method. The survivor functions across the 3 groups were compared using the log-rank (Mantel-Cox) test. An altered trend in survivor function with increasing units of blood transfusion was tested using the trend version of the Mantel-Cox and Breslow tests (Benedetti et al., 1990). To investigate the combined effects of different variables on survival, Cox’s proportional hazards regression model was used (Hopkins, 1990). The event of interest was death from renal carcinoma. At first, all possible prognostic factors (except blood transfusion) were used. The significant factors were selected by a backward stepwise approach. To test whether the variable “transfusion” made a statistically significant improvement, this was added to the model as the last step of the analysis. Results
In the course of the study 120 patients (60%) died; 91 deaths were related to renal carcinoma. Blood transfusions were given to 154 patients (77%). The median amount transfused was 2 units (range 1-21). The median age at operation was 64 years (range 27-82). Survival after operation is shown in the Figure. At 30 months the total number of patients at risk was 108 and at 60 months it was 68. In testing the univariate relationship between transfusion and survival, the difference between groups I and I1 was not significant. Group I11 was different from groups I and I1 (P 4 units of blood.
additional significant effect when more than 4 units of blood were considered (Wald test P=0.005) (Table 1). Table 2 shows the 2-year cumulative survival in relation to stage and transfusion status. Very few patients with tumour stage 4 survived 2 years. The 1-year cumulative survival for these patients was 0.26 when 0 to 4 units of blood had been given and 0.08 when more than 4 units had been given. During the first half of the study period whole blood was transfused. During the latter years packed red cells were used. When analysis was limited to the years when only whole blood was used the effect of blood transfusion on survival was unchanged. Discussion
The major determinant of survival was tumour stage. Macrohaematuria was associated with improved survival rates (Moffat et al., 1987). A causal relationship is unlikely and the explanation may be an association between macrohaematuria and an unmeasured prognostic variable. In patients with macrohaematuria the tumours might have been discovered earlier. The seemingly marked effect of transfusion on survival which was shown in the univariate analysis
BLOOD TRANSFUSION AND SURVIVAL FOLLOWING SURGERY FOR RENAL CARCINOMA
137
Table 1 Survival Analysis using Cox’s Proportional Hazards Model
Variable
No. of patients
No. of cancer-related deaths (%)
79 38 35 8 5 36 1 04 97 118 83 158 43
19 (24) 14 (37) 15 (43) 5 (63) 5 (100) 33 (92) 33 (32) 58 (60) 62 (53) 29 (35) 58 (37) 33 (77)
Relative hazard
95%
confidence limits
~
Stage 1 2 3a 3b 3c 4 ESR 40
Macrohaematuria:No Yes Transfusion: 0-4 units > 4 units
1 (ref7 1.69 1.71 5.30 5.59 9.90 1 ref 2.14 1 (ref) 0.63 1 (ref) 2.01
0.85-3.38 0.84-3.49 1.91-14.75 1.81-17.28 5.28-18.56 1.35-3.40 0.39-1.02 1.23-3.28
A relative hazard value greater than 1 indicates a negative effect on survival time. A value less than 1 has the reverse interpretation.
Table 2 Two-year Cumulative Survival in Relation to Stage and Transfusion Status Transfusion (units)
No. of patients
No. of cancer-related deaths (%)
Cumulative survival at 2 years
1 1
0-4
73 6
16 (22) 3 (50)
0.90 0.83
2 2
0-4
35 3
12 (34) 2 (67)
0.79 0.67
3 3
0-4
27 21
10 (37) 15 (71)
0.70 0.34
4 4
0-4
23 13
20 (87) 13 (100)
0.18 0.08
Stage
>4 >4 >4 24
diminished, but was still significant when viewed in the light of the other prognostic factors selected in Cox’s multivariate analysis. Larger tumours with increasingly difficult operations may have a worse prognosis and increase the need for transfusion. The size and stage of the tumour were tested in the multivariate analysis. Difficult operations would be partly reflected in the longer duration of the procedure, a factor which was taken into account in the analysis. Although unmeasured variables might have confounded the analysis, peri-operative transfusion of more than 4 units appeared to have an independent negative effect on survival. Transfusion of more than 4 units seemed to have an adverse affect on cumulative survival at 2 years for all tumour stages. However, one must be careful not to draw firm conclusions regarding stages 1 and 2, since few of these patients received more than 4 units of blood.
Wobbes et al. (1989) found a relationship between the volume of blood given and survival in colorectal carcinoma. Significant differences were found in the disease-free survival rate if more than 6 units of blood were given. A dose-dependent relationship between transfusion and negative effect on survival has also been reported after resection of colorectal liver metastases (Stephenson et al., 1988). Patients receiving more than 10 units of blood had a significantly decreased overall survival rate than patients who received 3 to 10 units. The immunosuppressive effect of transfusion has been proposed as a reason for the effect on survival in cancer patients. Lieberman et al. (1990) showed that transfusion of washed red cells induced deficits in cellular immunity and resulted in diminished host survival in a murine neuroblastoma model. The effect was present when allogeneic blood was transfused but absent in syngeneic transfusions.
138
BRITISH JOURNAL OF UROLOGY
A deleterious effect of transfusion on tumour MeClinton, S., Moffat, L. E., Scott, S. et d (1990). Blood transfusion and survival following surgery for prostatic recurrence may also be mediated by the increased carcinoma. Br. J . Surg., 77, 14C142. mitogenic activity observed in stored blood (Hoh et Mikulin, T., Powell, C. S., Urwin, G. H. et d (1986). Relation al., 1990). The principal changes occurred from the between blood transfusion and survival in renal adenocarciend of the second week. Increased mitogenic noma. Br. J . Surg., 73,1036-1037. activity was measured in cancer patients following Moffat, L. E.F., Sunderland,G . T. and Lamont, D. (1987).Blood transfusion and survival following nephrectomy for carcinoma the transfusion of stored blood. of kidney. Br. J . Urol., 60,316-319. In conclusion, peri-operative blood transfusion Moffat, L. E.F. and Sunderland, G. T. (1985).Relation between seems to have a moderate, adverse effect on survival recurrence of cancer and blood transfusion. Br. Med. J . , 291, 971. in patients undergoing surgery for renal carcinoma. The practical implication is that peri-operative Moores, D. W., Piantadosi, S. and McKneally, M. F. (1989). Effect of perioperative blood transfusion on outcome in transfusion should be given only when absolutely patients with surgically resected lung cancer. Ann. Thorac. essential. In particular, precautions should be taken Surg., 47,346351. during the operation to avoid major haemorrhage, Nathanson, S. D., Tilley, B. C., Schultz, L. et d (1985). Perioperative allogeneic blood transfusions. Survival in since this could necessitate the transfusion of patients with resected carcinomas of the colon and rectum. multiple units of blood.
References Benedetti, J., Yuen, K. and Young, L. (1990). Life tables and survivor functions. In BMDP Statistical Software Manual, ed. Dixon, W. J., Brown, M. B., Engelman, L. etal. Pp. 739-768. Berkeley, Los Angeles, Oxford : University of California Press. Blumberg, N., Aganval, M. M. and Chuang, C. (1988).A possible association between survival time and transfusion in cervical cancer. Yale J . Biol. Med., 61,493-500. Chesi, R., Cazzola, A., Bacci, G. et d (1989). Effect of perioperative transfusions on survival in osteosarcoma treated by multimodal therapy. Cancer, 64,1727-1737. Heal, J. M., Chuang, C. and Blumberg, N. (1988).Perioperative blood transfusions and prostate cancer recurrence and survival. Am. J . Surg., 156, 374-380. Hoh, H., Umpleby, H. and Taylor, I. (1990). Recurrence of colorectal cancer and perioperative blood transfusion. Is blood storage time important? Dis. Colon Rectum, 33,127-130. Hopkins, A. (1990).Survival analysis with covariates. In BMBP Statistical Software Manual, ed. Dixon, W. J., Brown, M. B., Engelman, L. et al. Pp. 769-806. Berkeley, Los Angeles, Oxford : University of California Press. Kampschoer,G. H.,Maruyama,K.,Sasako,M.etd(1989). The effects of blood transfusion on the prognosis of patients with gastric cancer. World J . Surg., 13,637-643. Keller, S. M., Groshen, S., Martini, N. et d (1988). Blood transfusion and lung cancer recurrence. Cancer, 62,606-610. Lieberman,M. D.,Shou, J.,Sigal, R. K. et al. (1990).Transfusioninduced immunosuppression results in diminished host survival in a murine neuroblastoma model. J . Surg. Res., 8,, 498503. Manyonda, I. T., Shaw, D. E., Foulkes, A. et d (1986). Renal cell carcinoma: blood transfusion and survival. Br. Med. J . , 293, 537-538.
Arch. Surg., 120,734-738. Robson, C., Churchill, B. and Anderson, W. (1969).The results of radical nephrectomy for renal cell carcinoma. J . Urol., 101, 297-301. Stephenson,K. R., Steinberg, S. M., Hughes, K. S. et d (1988). Perioperative blood transfusions are associated with decreased time to recurrence and decreased survival after resection of colorectal liver metastases. Ann. Surg., 208,679487. van Lawick van Pabst, W. P., Langenhorst, B. L., Mulder, P. G. et d (1988).Effect of perioperative blood loss and perioperative blood transfusions on colorectal cancer survival. Eur. J . Cancer Clin. Oncol., 24,741-747. Voogt, P. J., van der Velde, C. J., Brand, A. et d (1987). Perioperative blood transfusion and cancer prognosis. Different effects of blood transfusion on prognosis of colon and breast cancer patients. Cancer, 59,83&843. Wobbes, T.,Joosen, K. H. G., Kuypers, H. H. C. et d (1989). The effect of packed cells and whole blood transfusions on survival after curative resection for colorectal carcinoma. Dis. Colon Rectum, 32,743-748.
The Authors T.-H. Edna, MD, PhD, Consultant Surgeon. K. Vada, MD, Senior Registrar. F. Hesselberg, MD, Chief Consultant, Section of Urology, Department of Surgery, Innherred Hospital. 0. K. Mj~lnererd,MD, Chief Consultant, Section of Urology, Department of Surgery, University Hospital of Trondheim.
Requests for reprints to: T.-H. Edna, Department of Surgery, Innherred Hospital, N-7600Levanger, Norway.
Blood Transfusion and Survival Following Surgery for Renal Carcinoma T.-H. EDNA, K. VADA, F. HESSELBERG and 0. K. MJOLNERIZID Department of Surgery, Innherred Hospital, Levanger; Section of Urology, Department of Surgery, University Hospital, Trondheim,Norway
Summary-The effect of peri-operative blood transfusion on survival after surgery for renal carcinoma was studied in 201 patients. In addition to blood transfusion, several other factors were included in a multivariate analysis. Using Cox's proportional hazards model, transfusion of more than 4 units of blood was found to be an independent prognostic factor in addition to tumour stage, erythrocyte sedimentation rate and macrohaematuria.
Peri-operative blood transfusion has been reported to have a detrimental effect on survival following surgery for cancer. This may be due to the immunosuppressive effect of blood transfusion. Using multivariate analysis, the independent prognostic effect of transfusion has been studied. A negative effect on survival has been reported for prostate cancer (Heal et al. 1988; McClinton et al., 1990), colorectal cancer (Voogt et al., 1987; van Lawick van Pabst et al., 1988),lung cancer (Moores et al., 1989), cervical cancer (Blumberg et al., 1988) and osteosarcoma (Chesi et al., 1989). Others have found no independent effect on survival in colorectal cancer (Nathanson et al., 1985), gastric cancer (Kampschoer et al., 1989), lung cancer (Keller et al., 1988) and breast cancer (Voogt et al., 1987). Few studies have been done on the effect of blood transfusion on survival in renal carcinoma. A possible negative effect was reported by Mikulin et al. (1986) and Moffat and Sunderland (1985) but no such effect was found by Manyonda et al. (1986) and Moffat et al. (1987). We have studied survival in a larger series of patients after surgery for renal carcinoma, to determine the effect of transfusion in relation to other risk factors.
Accepted for publication 29 August 1991
Patients and Methods The records of 68 patients operated on for renal carcinoma at Innherred Hospital between 1969 and 1987 and 133 patients treated at the Regional Hospital of Trondheim between 1974 and 1987 were reviewed. The series included 108 men and 93 women whose median age at operation was 64 years (range 27-82). Information on peri-operative transfusion was gathered, together with data on known and possible risk factors such as age, sex, haemoglobin and erythrocyte sedimentation rate (ESR) on admission, microscopic or macroscopic haematuria, loin pain, pre-operative plugging of the renal artery, duration of operation, tumour stage and tumour size. Retrospective staging was assessed using the Robson classification (Robson et al., 1969). The vital status was known in all cases. Eight patients whose cause of death was uncertain were considered to have died from a disease not related to renal carcinoma. Those who died from causes other than renal carcinoma, or who survived until the end of the study, were treated as censored data. Adjusted survival rates were calculated by using death from renal carcinoma as the terminal event and death from an unrelated cause as a censored event.
135
136 The patients were divided into 3 groups. Group I received no transfusion during their hospital stay. Group I1 were given between 1 and 4 units of blood and group I11 received more than 4 units. Adjusted survival times for the groups were compared using the Kaplan-Meier product-limit method. The survivor functions across the 3 groups were compared using the log-rank (Mantel-Cox) test. An altered trend in survivor function with increasing units of blood transfusion was tested using the trend version of the Mantel-Cox and Breslow tests (Benedetti et al., 1990). To investigate the combined effects of different variables on survival, Cox’s proportional hazards regression model was used (Hopkins, 1990). The event of interest was death from renal carcinoma. At first, all possible prognostic factors (except blood transfusion) were used. The significant factors were selected by a backward stepwise approach. To test whether the variable “transfusion” made a statistically significant improvement, this was added to the model as the last step of the analysis. Results
In the course of the study 120 patients (60%) died; 91 deaths were related to renal carcinoma. Blood transfusions were given to 154 patients (77%). The median amount transfused was 2 units (range 1-21). The median age at operation was 64 years (range 27-82). Survival after operation is shown in the Figure. At 30 months the total number of patients at risk was 108 and at 60 months it was 68. In testing the univariate relationship between transfusion and survival, the difference between groups I and I1 was not significant. Group I11 was different from groups I and I1 (P 4 units of blood.
additional significant effect when more than 4 units of blood were considered (Wald test P=0.005) (Table 1). Table 2 shows the 2-year cumulative survival in relation to stage and transfusion status. Very few patients with tumour stage 4 survived 2 years. The 1-year cumulative survival for these patients was 0.26 when 0 to 4 units of blood had been given and 0.08 when more than 4 units had been given. During the first half of the study period whole blood was transfused. During the latter years packed red cells were used. When analysis was limited to the years when only whole blood was used the effect of blood transfusion on survival was unchanged. Discussion
The major determinant of survival was tumour stage. Macrohaematuria was associated with improved survival rates (Moffat et al., 1987). A causal relationship is unlikely and the explanation may be an association between macrohaematuria and an unmeasured prognostic variable. In patients with macrohaematuria the tumours might have been discovered earlier. The seemingly marked effect of transfusion on survival which was shown in the univariate analysis
BLOOD TRANSFUSION AND SURVIVAL FOLLOWING SURGERY FOR RENAL CARCINOMA
137
Table 1 Survival Analysis using Cox’s Proportional Hazards Model
Variable
No. of patients
No. of cancer-related deaths (%)
79 38 35 8 5 36 1 04 97 118 83 158 43
19 (24) 14 (37) 15 (43) 5 (63) 5 (100) 33 (92) 33 (32) 58 (60) 62 (53) 29 (35) 58 (37) 33 (77)
Relative hazard
95%
confidence limits
~
Stage 1 2 3a 3b 3c 4 ESR 40
Macrohaematuria:No Yes Transfusion: 0-4 units > 4 units
1 (ref7 1.69 1.71 5.30 5.59 9.90 1 ref 2.14 1 (ref) 0.63 1 (ref) 2.01
0.85-3.38 0.84-3.49 1.91-14.75 1.81-17.28 5.28-18.56 1.35-3.40 0.39-1.02 1.23-3.28
A relative hazard value greater than 1 indicates a negative effect on survival time. A value less than 1 has the reverse interpretation.
Table 2 Two-year Cumulative Survival in Relation to Stage and Transfusion Status Transfusion (units)
No. of patients
No. of cancer-related deaths (%)
Cumulative survival at 2 years
1 1
0-4
73 6
16 (22) 3 (50)
0.90 0.83
2 2
0-4
35 3
12 (34) 2 (67)
0.79 0.67
3 3
0-4
27 21
10 (37) 15 (71)
0.70 0.34
4 4
0-4
23 13
20 (87) 13 (100)
0.18 0.08
Stage
>4 >4 >4 24
diminished, but was still significant when viewed in the light of the other prognostic factors selected in Cox’s multivariate analysis. Larger tumours with increasingly difficult operations may have a worse prognosis and increase the need for transfusion. The size and stage of the tumour were tested in the multivariate analysis. Difficult operations would be partly reflected in the longer duration of the procedure, a factor which was taken into account in the analysis. Although unmeasured variables might have confounded the analysis, peri-operative transfusion of more than 4 units appeared to have an independent negative effect on survival. Transfusion of more than 4 units seemed to have an adverse affect on cumulative survival at 2 years for all tumour stages. However, one must be careful not to draw firm conclusions regarding stages 1 and 2, since few of these patients received more than 4 units of blood.
Wobbes et al. (1989) found a relationship between the volume of blood given and survival in colorectal carcinoma. Significant differences were found in the disease-free survival rate if more than 6 units of blood were given. A dose-dependent relationship between transfusion and negative effect on survival has also been reported after resection of colorectal liver metastases (Stephenson et al., 1988). Patients receiving more than 10 units of blood had a significantly decreased overall survival rate than patients who received 3 to 10 units. The immunosuppressive effect of transfusion has been proposed as a reason for the effect on survival in cancer patients. Lieberman et al. (1990) showed that transfusion of washed red cells induced deficits in cellular immunity and resulted in diminished host survival in a murine neuroblastoma model. The effect was present when allogeneic blood was transfused but absent in syngeneic transfusions.
138
BRITISH JOURNAL OF UROLOGY
A deleterious effect of transfusion on tumour MeClinton, S., Moffat, L. E., Scott, S. et d (1990). Blood transfusion and survival following surgery for prostatic recurrence may also be mediated by the increased carcinoma. Br. J . Surg., 77, 14C142. mitogenic activity observed in stored blood (Hoh et Mikulin, T., Powell, C. S., Urwin, G. H. et d (1986). Relation al., 1990). The principal changes occurred from the between blood transfusion and survival in renal adenocarciend of the second week. Increased mitogenic noma. Br. J . Surg., 73,1036-1037. activity was measured in cancer patients following Moffat, L. E.F., Sunderland,G . T. and Lamont, D. (1987).Blood transfusion and survival following nephrectomy for carcinoma the transfusion of stored blood. of kidney. Br. J . Urol., 60,316-319. In conclusion, peri-operative blood transfusion Moffat, L. E.F. and Sunderland, G. T. (1985).Relation between seems to have a moderate, adverse effect on survival recurrence of cancer and blood transfusion. Br. Med. J . , 291, 971. in patients undergoing surgery for renal carcinoma. The practical implication is that peri-operative Moores, D. W., Piantadosi, S. and McKneally, M. F. (1989). Effect of perioperative blood transfusion on outcome in transfusion should be given only when absolutely patients with surgically resected lung cancer. Ann. Thorac. essential. In particular, precautions should be taken Surg., 47,346351. during the operation to avoid major haemorrhage, Nathanson, S. D., Tilley, B. C., Schultz, L. et d (1985). Perioperative allogeneic blood transfusions. Survival in since this could necessitate the transfusion of patients with resected carcinomas of the colon and rectum. multiple units of blood.
References Benedetti, J., Yuen, K. and Young, L. (1990). Life tables and survivor functions. In BMDP Statistical Software Manual, ed. Dixon, W. J., Brown, M. B., Engelman, L. etal. Pp. 739-768. Berkeley, Los Angeles, Oxford : University of California Press. Blumberg, N., Aganval, M. M. and Chuang, C. (1988).A possible association between survival time and transfusion in cervical cancer. Yale J . Biol. Med., 61,493-500. Chesi, R., Cazzola, A., Bacci, G. et d (1989). Effect of perioperative transfusions on survival in osteosarcoma treated by multimodal therapy. Cancer, 64,1727-1737. Heal, J. M., Chuang, C. and Blumberg, N. (1988).Perioperative blood transfusions and prostate cancer recurrence and survival. Am. J . Surg., 156, 374-380. Hoh, H., Umpleby, H. and Taylor, I. (1990). Recurrence of colorectal cancer and perioperative blood transfusion. Is blood storage time important? Dis. Colon Rectum, 33,127-130. Hopkins, A. (1990).Survival analysis with covariates. In BMBP Statistical Software Manual, ed. Dixon, W. J., Brown, M. B., Engelman, L. et al. Pp. 769-806. Berkeley, Los Angeles, Oxford : University of California Press. Kampschoer,G. H.,Maruyama,K.,Sasako,M.etd(1989). The effects of blood transfusion on the prognosis of patients with gastric cancer. World J . Surg., 13,637-643. Keller, S. M., Groshen, S., Martini, N. et d (1988). Blood transfusion and lung cancer recurrence. Cancer, 62,606-610. Lieberman,M. D.,Shou, J.,Sigal, R. K. et al. (1990).Transfusioninduced immunosuppression results in diminished host survival in a murine neuroblastoma model. J . Surg. Res., 8,, 498503. Manyonda, I. T., Shaw, D. E., Foulkes, A. et d (1986). Renal cell carcinoma: blood transfusion and survival. Br. Med. J . , 293, 537-538.
Arch. Surg., 120,734-738. Robson, C., Churchill, B. and Anderson, W. (1969).The results of radical nephrectomy for renal cell carcinoma. J . Urol., 101, 297-301. Stephenson,K. R., Steinberg, S. M., Hughes, K. S. et d (1988). Perioperative blood transfusions are associated with decreased time to recurrence and decreased survival after resection of colorectal liver metastases. Ann. Surg., 208,679487. van Lawick van Pabst, W. P., Langenhorst, B. L., Mulder, P. G. et d (1988).Effect of perioperative blood loss and perioperative blood transfusions on colorectal cancer survival. Eur. J . Cancer Clin. Oncol., 24,741-747. Voogt, P. J., van der Velde, C. J., Brand, A. et d (1987). Perioperative blood transfusion and cancer prognosis. Different effects of blood transfusion on prognosis of colon and breast cancer patients. Cancer, 59,83&843. Wobbes, T.,Joosen, K. H. G., Kuypers, H. H. C. et d (1989). The effect of packed cells and whole blood transfusions on survival after curative resection for colorectal carcinoma. Dis. Colon Rectum, 32,743-748.
The Authors T.-H. Edna, MD, PhD, Consultant Surgeon. K. Vada, MD, Senior Registrar. F. Hesselberg, MD, Chief Consultant, Section of Urology, Department of Surgery, Innherred Hospital. 0. K. Mj~lnererd,MD, Chief Consultant, Section of Urology, Department of Surgery, University Hospital of Trondheim.
Requests for reprints to: T.-H. Edna, Department of Surgery, Innherred Hospital, N-7600Levanger, Norway.
