Preoperative Administration of Recombinant Human Erythropoietin in Patients Undergoing Gynecologic Surgery
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1 Original Paper Gynecol Obstet Invest 2002;54:1 5 Received: July 11, 2001 Accepted after revision: May 3, 2002 Preoperative Administration of Recombinant Human Erythropoietin in Patients Undergoing Francesco Sesti Carlo Ticconi Simone Bonifacio Emilio Piccione Division of Obstetrics and Gynecology, University of Rome Tor Vergata, S. Eugenio Hospital, Rome, Italy Key Words Erythropoietin W Gynecological surgery W Anemia Abstract The effect of preoperative recombinant human erythropoietin (r-huepo) in anemic women undergoing gynecologic surgery for benign diseases was evaluated in this prospective, not randomized study. One hundred and twenty women were included in the study. Sixty women were treated preoperatively with r-huepo at three different cumulative doses: 80,000, 120,000 and 160,000 IU. Sixty nonanemic women were not treated. Baseline hemoglobin (Hb) levels were measured. Hb levels were also measured on the day of the surgery before starting the procedure, on postoperative day 1 and on the day of discharge from the hospital. Treatment with r-huepo significantly increased both preoperative Hb levels and Hb levels at discharge. Conversely, Hb levels at discharge were lower than baseline levels in untreated women. The effect of r-huepo on Hb levels was exerted in a dose-dependent fashion. No adverse and/or side effects of treatment were observed. Preoperative treatment with r-huepo in selected anemic patients undergoing gynecologic surgery for benign diseases seems to be a safe and useful tool to reduce the need for red blood cell transfusions. Introduction Copyright 2002 S. Karger AG, Basel The decrease in hemoglobin concentrations commonly observed after major surgery is usually corrected by red cell transfusions or oral iron and folate supplementation. The increased awareness of blood-transmissible diseases has led to a restrictive use of homologous blood and to interest in alternatives for correcting anemia. Abdominal or vaginal hysterectomy is often associated with postoperative anemia which can request blood transfusions. The incidence of transfusions following abdominal hysterectomy has been reported to range between 2.2 and 7.5%, and following vaginal hysterectomy between 0.7 and 13% [1]. Critical clinical situations, difficult to be managed without red blood cell transfusion, may occur: (a) in women with preoperative anemia scheduled for an operation in which a considerable blood loss is anticipated; (b) in women with a significant postoperative ane- ABC Fax karger@karger.ch S. Karger AG, Basel /02/ $18.50/0 Accessible online at: Francesco Sesti Division of Obstetrics and Gynecology University of Rome Tor Vergata, S. Eugenio Hospital Piazzale Umanesimo, I Rome (Italy) Tel , Fax , sestifrancesco@tiscalinet.it
2 mia due to unexpected high blood loss during surgery or to inflammation; (c) in patients with considerable transfusion risk due to multiple anti-red-cell antibodies, and (d) in patients who refuse to accept blood transfusion for religious or other reasons [2, 3]. Several surgical centers have reported the preoperative [4 6] or postoperative [7 9] use of recombinant human erythropoietin (r-huepo). In the surgical setting, r- HuEPO can be used either to accelerate the preoperative collection of autologous blood or to stimulate preoperative erythropoiesis in order to increase red cell mass. This should enhance postoperative recovery and reduce the possibility of administering red cell transfusions. Preoperative r-huepo therapy without autologous blood donation is a new concept to avoid blood transfusions [10, 11]. Very recently, r-huepo has been used to correct iron deficiency anemia in pregnancy [12]. To our knowledge, there are no reports on the use of r-huepo in gynecological surgery for benign diseases. The purpose of this clinical, not randomized study was to investigate whether preoperative use of r-huepo in patients undergoing abdominal or vaginal hysterectomy can improve perioperative hemoglobin (Hb) levels. Materials and Methods Study Subjects One hundred and twenty patients scheduled for elective abdominal or vaginal hysterectomy for benign gynecologic diseases were investigated. The indication to perform abdominal surgery was symptomatic uterine fibroids with uterine size 116 gestational weeks, whereas for vaginal hysterectomy, it was uterovaginal prolapse in 8 cases; uterovaginal prolapse associated with leiomyomas in 11 cases, and symptomatic uterine fibroids with uterine size! 16 gestational weeks in 7 cases. Sixty women with preoperative Hb levels!12 g/dl were included in the treatment arm of the study. Sixty women with preoperative Hb levels 1 12 mg/dl did not receive r-huepo. All surgeries were performed between November 1999 and December 2001 at the University of Rome Tor Vergata, Division of Gynecology and Obstetrics, S. Eugenio Hospital, Rome, Italy. Exclusion criteria were: (a) the presence of any primary hematological disease, infectious or neoplastic disease or any condition which might potentially impair a response to r-huepo; (b) administration of drugs known to suppress erythropoiesis 1 month before the entry into the study; (c) clinical suspicion of autoimmune hemolysis; (d) recent blood transfusion (1 month or less before the recruitment into the study); (e) presence of active inflammatory disease; (f) history of drug or alcohol abuse 2 years or less before entry into the study; (g) uncontrolled hypertension, or (h) any significant ongoing blood loss. Informed written consent was obtained from all patients after full explanation of the aim of the study. Treatments Women included in the study were divided into four groups according to their preoperative baseline Hb levels: (1) group I: Hb levels 611 and! 12 g/dl. These women (n = 24) received a total dose of 80,000 IU of r-huepo (Epoxitin, Janssen- Cilag S.A., Issy Le Moulineaux, France) preoperatively (10,000 IU daily self-administered subcutaneously for 8 days); (2) group II: Hb levels 610 and!11 g/dl. These women (n = 17) received a total dose of 120,000 IU of r-huepo preoperatively (10,000 IU daily for 12 days); (3) group III: Hb levels 66 and!10 g/dl. These women (n = 19) received a total dose of 160,000 IU of r-huepo preoperatively (10,000 IU daily for 16 days). (4) group IV: women (n = 60) who did not receive r-huepo because their preoperative Hb levels were 1 12 mg/dl. Administration of r-huepo was started as close as possible to the scheduled time of surgery. It was adjusted according to the dose and was completed 5 days before surgery. All women treated with r- HuEPO were also administered ferrous sulfate (525 mg orally twice a day). Baseline Hb levels were measured in all patients. Hb levels were also measured in all patients on the day of the surgery before starting the procedure, on postoperative day 1 and on the day of discharge from the hospital. Patients undergoing preoperative treatment with r-huepo were instructed to communicate the research staff all the adverse and/or side effects observed during therapy until surgery. Statistical Analysis Data are expressed as means B SD or as percent of control as appropriate. Statistical analysis was performed by using ANOVA with repeated measures. The Student-Newman-Keuls test was used for post hoc multiple comparisons among groups. Significance was set at p! Results No significant differences in age, BMI, operating time, and length of postoperative hospitalization were found between the four study groups (table 1). All the operations were performed by the same surgical staff (E.P., F.S.). The distribution of operative procedures is shown in table 2. No intraoperative complication occurred. Intraoperative blood loss was in the normal range in all cases. The changes in Hb concentrations in the women studied are shown in figure 1. Baseline Hb levels (g/dl) were B 0.26 (group I), B 0.27 (group II), 8.51 B 1.2 (group III) and B 0.72 (group IV). Preoperative administration of r-huepo significantly increased Hb levels: Hb B 0.69 (group I), 13.2 B 0.47 (group II) and B 1.48 (group III). Hb values obtained on postoperative day 1 (PD+1) were significantly reduced in all women compared with preoperative values. However, in the r-huepo-treated women, Hb levels were higher than 2 Gynecol Obstet Invest 2002;54:1 5 Sesti/Ticconi/Bonifacio/Piccione
3 Table 1. Patient characteristics Epoetin alpha (n = 60) group I (n = 24) group II (n = 17) group III (n = 19) Group IV (n = 60) Age, years 45.04B B B B5.42 BMI 24B5.1 24B4.8 24B4.2 24B3.9 Operating time, min B B B B9.30 Postoperative hospital stay, days 4.52B B B B0.90 Table 2. Distribution of operative procedures Epoetin alpha group I group II group III Group IV Abdominal hysterectomy Vaginal hysterectomy Total baseline levels: Hb 12.4 B 0.93 (group I), B 0.39 (group II), B 1.16 (group III) and B 0.99 (group IV). Similar results were observed at discharge from the hospital: Hb B 0.91 (group I), B 0.42 (group II), B 1.17 (group III) and 9.91 B 0.77 (group IV). The mean percent increase in Hb values compared with baseline levels in treated women progressively rose according to the increase in the doses of r-huepo administered: % (group I), % (group II) and % (group III). No adverse and/or side effects were reported by treated women. Discussion The results of this study show that preoperative administration of r-huepo, combined with an oral iron supplement, significantly increases Hb concentration at and after surgery in patients with a preoperative Hb concentration lower than 12 g/dl who underwent elective abdominal or vaginal hysterectomy for benign diseases. Similar results have been reported in patients undergoing orthopedic [13], cardiac [14] and colorectal surgery [15]; however, to our knowledge, there are no data available presently on the use of r-huepo in benign gynecologic surgery. The most appropriate regimen of perioperative erythropoietin administration is yet unknown. In a consensus statement, the administration of 6 doses of 150 IU/kg before surgery plus 6 doses of 200 mg iron has been recommended [16]. In the study by Braga et al. [17], r- HuEPO at a dose of 100 IU/kg was administered three times with an interval of 4 days prior to surgery. Heiss et al. [18] administered 150 IU/kg of r-huepo every second day for 10 days before surgery and 150 IU/kg on the second postoperative day. With the regimen used in our study, individualized according to baseline preoperative Hb levels, significant stimulation of erythropoiesis was achieved in all groups of treated patients. r-huepo administration resulted in a dose-dependent increase in Hb concentration. Postoperative anemia can be explained not only by blood loss occurring during and after surgery. Indeed, there is evidence that the characteristics of postoperative anemia are more similar to those of the anemia from chronic disease than from iron deficiency [19, 20]. This kind of anemia is observed in patients with inflammatory disorders and malignancies: it is characterized by a decrease in the serum levels of iron and transferrin, by transferrin saturation despite adequate iron stores, and by a reduction in erythropoiesis [21, 22]. In fact, in the first week after surgery, endogenous erythropoiesis can be inhibited by acute postoperative inflammatory reactions. Iron supplementation in the presence of normal iron Preoperative Erythropoietin in Benign Gynecol Obstet Invest 2002;54:1 5 3
4 Fig. 1. Hb concentration in the four groups of patients at different times in relation to surgery. C = baseline (control) Hb concentration at the entry into the study; r-huepo = Hb concentration after therapy with erythropoietin; PD+1 = Hb concentration at postoperative day 1; D = Hb concentration at discharge from the hospital. * p! 0.01 (ANOVA); p! 0.05 (Student-Newman-Keuls test) versus baseline (control) Hb levels. stores is ineffective at this time [23]. Another study has demonstrated that the Hb concentration must be below 6.3 mmol/l to induce a significant release of erythropoietin [24]. Only 4 weeks after major surgery, there is an increase in the soluble transferrin receptor concentration, indicating increased erythropoiesis, while iron becomes more available. Therefore, the normal acute inflammatory reaction during the postoperative period may cause inhibition of the erythropoietic response of the bone marrow to endogenous stimuli, which might be overcome by exogenous administration of erythropoietin. This might explain the higher Hb levels at discharge found in treated women compared with untreated ones. Higher postoperative Hb levels can give the advantage of a more rapid postoperative recuperative power, thus shortening the length of recovery and improving shortterm and long-term physical function, all of which can have a substantial impact on the patient s emotional and psychosocial well-being. Treatment with r-huepo can alter the hemostatic variables, leading to an increased risk of either thromboembolic complications or perioperative bleeding due to changes in fibrinolytic activity or platelet count. It has been reported that treatment with r-huepo of patients with renal failure for 6 months resulted in a marked increase in fibrinolytic activity [25]. However, in other studies in which r-huepo was used preoperatively or perioperatively, no changes in hemostatic and fibrinolytic activities have been reported [26, 27]. In the present study, preoperative treatment with r-huepo did not sig- 4 Gynecol Obstet Invest 2002;54:1 5 Sesti/Ticconi/Bonifacio/Piccione
5 nificantly influence intraoperative and postoperative bleeding. No patient developed a deep venous thrombosis. No patient reported adverse reactions or side effects related to the treatment. A cost-effectiveness analysis of the use of r-huepo in a benign gynecologic surgical population may be difficult to be performed because the costs of the potential risks from blood transfusions are difficult to be stated. In conclusion, Hb concentration at the time of surgery and in the week following surgery was significantly increased in patients receiving r-huepo. It may, therefore, be justifiable to carry out larger prospective controlled clinical trials to further define the subgroups of women who might have the maximal benefit from the erythropoietin treatment at optimal cost-effectiveness. References 1 Hill DJ: Complications of hysterectomy. Ballières Clin Obstet Gynaecol 1997;11: Benson KT: The Jehovah s Witness patient: Consideration for the anesthesiologist. Anesth Analg 1989;69: Thompson FL, Powers JS, Graber SE, Krantz SB: Use of recombinant human erythropoietin to enhance autologous blood donation in a patient with multiple red cell allo-antibodies and the anemia of chronic disease. Am J Med 1990;90: Rothstein P, Roye D, Verdisco L, Stern L: Preoperative use of erythropoietin in an adolescent Jehovah s Witness. Anesthesiology 1990; 73: Johnson PW, King R, Slevin ML, White H: The use of erythropoietin in a Jehovah s Witness undergoing major surgery and chemotherapy. Br J Cancer 1991;63: Fullerton DA, Campbell DN, Whitman GJ: Use of human recombinant erythropoietin to correct severe preoperative anemia. Ann Thorac Surg 1991;51: Kraus P, Lipman J: Erythropoietin in a patient following multiple trauma. Anesthesia 1992; 47: Collins SL, Timberlake GA: Severe anemia in the Jehovah s Witness: Case report and discussion. Am J Crit Care 1993;2: Akingbola OA, Custer JR, Bunchman TE, Sedman AB: Management of severe anemia without transfusion in a pediatric Jehovah s Witness patient. Crit Care Med 1994;22: Sowade O, Warnke H, Shigalla P, Sowade B, Francke W, Messinger D: Avoidance of allogeneic blood transfusion by treatment with epoetin beta (recombinant human erythropoietin) in patients undergoing open-heart surgery. Blood 1997;89: Sowade O, Gross J, Sowade B, Franke W, Messinger D, Ziebell E, Scigalla P, Warnke H: Evaluation of oxygen availability with oxygen status algorithm in patients undergoing open-heart surgery treated with epoetin beta. J Lab Clin Med 1997;129: Sifakis S, Angelakis E, Vardaki E, Koumantaki Y, Matalliotakis I: Erythropoietin in the treatment of iron deficiency anemia during pregnancy. Gynecol Obstet Invest 2001;51: Faris PM, Ritter MA, Abels RI: The effects of recombinant human erythropoietin on perioperative transfusion requirements in patients having a major orthopaedic operation. The American Erythropoietin Group. J Bone Joint Surg Am 1996;78: D Ambra M: Perioperative epoietin alpha reduced transfusion requirements in coronary artery bypass graft surgery. Semin Hematol 1996; (suppl 2): Qvist N, Boesby S, Wolff B, Hansen CP: Recombinant human erythropoietin and hemoglobin concentration at operation and during the postoperative period: Reduced need for blood transfusions in patients undergoing colorectal surgery prospective double-blind placebo-controlled study. World J Surg 1999;23: Messmer K: Consensus statement: Using epoietin alpha to decrease the risk of allogenic blood transfusion in the surgical setting. Roundtable of Experts in Surgery Blood Management. Semin Hematol 1996;(2 Suppl 2): Braga M, Gianotti A, Vignali A, Gentilini O, Servida P, Bordignon C, Di Carlo V: Evaluation of recombinant erythropoietin to facilitate autologous blood donation before surgery in anemic patients with cancer of the gastrointestinal tract. Br J Surg 1995;82: Heiss MH, Tarabichi A, Delanoff C, Allgayer H, Jauch KW, Hernandez-Richter T, Mempel W, Beck KG, Schildberg FW, Messmer K: Perisurgical erythropoietin application in anemic patients with colorectal cancer: A double-blind randomized study. Surgery 1996;119: Biesma DH, Van de Wiel A, Beguin Y, Kraayenhagen R, Marx JM: Postoperative erythropoiesis is limited by the inflammatory effect of surgery on iron metabolism. Eur J Clin Invest 1995;25: Zauber NP, Zauber AG, Gordon FJ, Tillis AC, Leeds HC, Berman E: Iron supplementation after femoral head replacement for patients with normal iron stores. JAMA 1992;267: Lee GR: The anemia of chronic disease. Semin Hematol 1983;20: Means RT Jr, Krantz SB: Progress in understanding the pathogenesis of the anemia of chronic disease. Blood 1992;80: Van Iperen CE, Kraaijenhagen RJ, Biesma DH, Beguin Y, Marx JJ, Van de Wiel A: Iron metabolism and erythropoiesis after surgery. Br J Surg 1998;85: Kickler TS, Spivak JL: Effect of whole blood donations on serum immunoreactive erythropoietin levels in autologous donors. JAMA 1998;260: Stenver D, Jeppesen LL, Nielsen B: The effect of erythropoietin on platelet function and fibrinolysis in chronic renal failure. Int J Artif Organs 1994;17: Biesma DH, Bronkhorst PJH, de Groot PG, et al: The effect of recombinant human erythropoietin on haemostasis, fibrinolysis and blood rheology in autologous blood donors. J Lab Clin Med 1994;124: Poulsen KA, Qvist N, Winther K, Boesby S: Haemostatic aspects of recombinant human erythropoietin in colorectal surgery. Eur J Surg 1998;164: Preoperative Erythropoietin in Benign Gynecol Obstet Invest 2002;54:1 5 5
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