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Early Vascular Thrombosis After Kidney Transplantation: Can We Predict Patients at Risk?
Early Vascular Thrombosis After Kidney Transplantation: Can We Predict Patients at Risk? R.A.P. de Freitasa,b, M.L. de Limaa,b, and M. Mazzalia,c,* a Renal Transplant Unit, Clinics Hospital, State University of Campinas, Campinas, São Paulo, Brazil; bDivision of Urology, Department of Surgery, State University of Campinas, Campinas, São Paulo, Brazil; and cDivision of Nephrology, Department of Medicine, State University of Campinas, Campinas, São Paulo, Brazil
ABSTRACT Background. Renal transplant is the therapy of choice for patients with chronic renal disease. In recent years, improvement in immunosuppressive drugs reduced early graft loss associated with acute rejection. However, vascular thrombosis, accounting for 5% of early graft loss, can sensitize the recipient for human leukocyte antibodies, reducing the chance for a second transplant. The aim of this study was to identify risk factors for vascular thrombosis in a single transplant center, to design specific prevention protocol. Methods. This was a retrospective, case-control study. From the Renal Transplant Unit database, we identified 21 cases of vascular thrombosis in recipients of kidneys from deceased donors. Recipients from the contralateral kidney from the same donor, without vascular complications, were assigned to the control group. Data analyzed included donor, recipient, transplant surgery, and post-operative follow-up. The local ethics committee approved the protocol. Results. Thrombosis and control groups were comparable for recipient characteristics, cold ischemia time, organ side (right or left), and site of arterial anastomosis. We observed an increased risk for vascular thrombosis in kidneys with multiple veins (odds ratio, 11.32; P ¼ .03). Organ retrieval surgery complications, such as vascular lesions or heterogeneous perfusion, despite normal pre-implantation biopsy, were considered risk factors for vascular thrombosis within the first post-operative day (odds ratio, 7.1; P ¼ .03). Conclusions. In this series, multiple renal vein and organ retrieval surgery complications were risk factors for early vascular thrombosis.
R
ENAL transplant is considered the best therapy for patients with chronic renal disease, with a better survival and quality of life [1]. In past decades, a better graft survival has been associated with the development of new and more potent immunosuppressive agents. As a consequence, vascular thrombosis became the main cause of early graft loss, accounting for a third of early graft loss [2]. Risk factors for vascular thrombosis can be associated with recipient, graft, donor, and surgical procedure. However, because the majority of reports are retrospective and descriptive, results are controversial and dependent of center specificities, such as pre-transplant donor and recipient approach, surgical technique, anesthesia and post-operative management, as well as recipient age and body mass index [2e14]. In the present series, we analyzed a group of patients ª 2017 Elsevier Inc. All rights reserved. 230 Park Avenue, New York, NY 10169
Transplantation Proceedings, 49, 817e820 (2017)
with early vascular thrombosis and compared them with recipients of contralateral kidney from the same donor to identify possible risk factors for vascular graft thrombosis. METHODS This was a retrospective, case-control study. From the Renal Transplant Unit Database, we selected the cases of early graft loss
*Address correspondence to Marilda Mazzali, Division of Nephology, Department of Medicine, School of Medical Sciences, State University of Campinas-Unicamp, Rua Tessalia Vieira de Camargo, 126, Cidade Universitária Zeferino Vaz, 13083-970 Campinas, São Paulo, Brasil. E-mail: [email protected] 0041-1345/17 http://dx.doi.org/10.1016/j.transproceed.2017.03.004
817
818 caused by vascular thrombosis. Recipients from the contralateral kidney from the same donor were considered as control subjects. Inclusion criteria included recipients of renal transplant from August 2005 to August 2015, age 16 years at transplant surgery. Exclusion criteria included pediatric renal transplant recipients and recipients from an isolated kidney (when contralateral kidney was discarded or transplanted in a different center). Vascular thrombosis was defined as the absence of vascular flow at Doppler ultrasound within the first post-operative day. In cases of doubt, a renal dynamic renal scintigraphy with TC99m-DTPA was performed, according to center protocol [15]. Graft nephrectomy and histologic analysis were indicated if thrombosis was confirmed. Data were collected from medical records and included donor and recipient data, surgical and anesthesia controls, immunosuppression, and anatomic description. The local ethics committee approved the protocol. Statistical analysis was performed with the use of Prism 6.0 Software. Significance was considered at a value of P < .05.
RESULTS
From August 2005 to August 2015, 1016 renal transplants were performed at our transplant center. The majority of the recipients (n ¼ 944, 92.9%) were 16 years old at transplant and received a kidney from a deceased donor (n ¼ 786, 83.2%). In a 10-year period, early vascular thrombosis within the first month after transplant was diagnosed in 26 patients, resulting in a 3.3% incidence. According to our criteria, we analyzed only the cases in which the data of the recipients of contralateral kidneys were available. The final study group excluded 5 cases: 2 for the contralateral kidney implanted in a pediatric recipient, 2 for kidney implanted in a different transplant center, and 1 case of unavailable data. The study group comprised 21 renal transplants with thrombosis and 21 contralateral kidney controls. Twenty-one donors were 39.7 15.7 years old, with a similar sex distribution (10 male) and body surface of 1.78 0.22 m2. Donor serum creatinine was normal (1.25 0.74 mg/dL), and the main cause of brain death was stroke (57%), followed by head trauma (38%). Recipients from thrombosis and control groups were comparable in age, sex, length of pre-transplant dialysis, previous blood transfusions, history of systemic hypertension or diabetes, use of acetyl salicylic acid, and pretransplant hemoglobin levels (Table 1). Groups also had a similar estimated post-transplant survival score of 34.1% for the thrombosis group and 36.1% for the control group (P ¼ NS). Kidney side (left or right) did not differ between groups. However, we observed a higher incidence of multiple veins in the thrombosis group compared with the control Group (Table 2). There was no correlation between thrombosis and surgical or anesthesia procedures, nor in the immediate post-operative treatment. Diagnosis of vascular thrombosis was done by means of a routine Doppler ultrasound within the first post-operative day. Vascular thrombosis was identified at the first exam in 53% of the cases, whereas in the 47% remaining cases,
DE FREITAS, DE LIMA, AND MAZZALI Table 1. Recipient Characteristics According to Groups Thrombosis
Control
Age (years) 45.2 11.3 49.9 10.4 Sex (male:female) 12:9 15:6 Body surface area (m2) 1.80 0.22 1.78 0.24 Length of dialysis pre 46.6 32.8 45.3 31.9 transplant (mos) Urine output before transplant (mL) 377.8 426.4 549.0 693.4 Blood transfusion before transplant 7 (33.3%) 10 (47.6%) (% patients) Previous femoral catheter for 2 (9.5%) 0 dialysis (% patients) Pre-transplant hypertension (%) 19 (90.4%) 21 (100%) Pre-transplant diabetes (%) 6 (28.6%) 4 (19%) Pre-transplant acetyl salicylic acid 8 (38.1%) 7 (33.3%) Pre-transplant hemoglobin (g/dL) 11.9 2.5 12.3 1.8
diagnosis was made in sequential Doppler ultrasound. When patients were analyzed according to time of thrombosis diagnosis, in the early (first) or late (sequential) exams, we observed that complications associated with organ retrieval, such as multiple vessels, vascular lesion, or heterogeneous perfusion, were more frequent in the early thrombosis group (Table 3). However, pre-implantation biopsies from these kidneys showed normal renal parenchyma histology.
DISCUSSION
Vascular thrombosis, although rare, is an important cause of early graft loss, with a negative impact on patient survival associated with a risk for development of anti-HLA antibodies [11e13]. In the present series, the incidence of vascular thrombosis was 3.3%, similar to previous reports [8,11]. The overall incidence of vascular thrombosis in a series of 2300 renal transplants from January 1984 to August 2015 was of 3.7%, corresponding to 84 episodes. Identification of patients at risk for thrombosis remains a problem. Previous reports suggest different factors, such as Table 2. Risk Factors for Early Vascular Thrombosis, Organ- and Surgery-Related Thrombosis
Right kidney Cold ischemia (min) Multiple arteries Multiple veins Renal artery anastomosis (min) Renal vein anastomosis (min) Internal iliac artery anastomosis (%) Total bleeding (mL) Heterogeneous reperfusion (%) Mean blood pressure at reperfusion (mm Hg) Intra-operative vasoactive drugs (%) Anesthesia length (min) Post-operative vasoactive drugs (%) Immediate diuresis
11 (52.4%) 20.15 6.14 2 (9.5%) 4 (19%) 26.1 12.1 19.6 5.2 9 (42.8%) 552.3 411.5 10 (47%) 99.8 12.0
Control
10 (47.6%) 20.2 4.7 0 0 24.4 7.5 17.6 3.8 8 (38%) 800 592.1 5 (23.8%) 95.5 18.2
16 (76.1%) 14 (66.6%) 294.5 64.4 293.3 48.2 9 7 616.8 863.9 977.4 951.0
EARLY VASCULAR THROMBOSIS AFTER KT Table 3. Relative Risk for Vascular Thrombosis RR (Confidence Interval)
Risk factor for thrombosis Female recipient Right kidney Multiple vein Heterogeneous perfusion Risk factor for early thrombosis Organ retrieval associated*
0.83 (0.45e1.55), P ¼ NS 1.32 (0.81e2.15), P ¼ NS 2.23 (1.5e3.18), P ¼ .08 1.63 (0.91e2.9), P ¼ NS 2.66 (1.08e7.46), P ¼ .03
*Organ retrievaleassociated complications include multiple veins and heterogeneous perfusion.
older age, female donor, number of arteries, kidney side, previous use of acetyl salicylic acid, prolonged cold ischemia, and previous history of recipient’s hypertension and/or diabetes [2e13]. These discrepancies can be a consequence of the characteristics of these reports, mainly retrospective studies and small series of cases, and can be influenced by population characteristics, donor source, surgical technique, and surgical team experience. To exclude donor-associated factors, we compared renal transplant patients with vascular thrombosis and their control subjects, recipients from the contralateral kidney from the same donor. There was no difference in sex, age, primary renal disease, and incidence of diabetes or hypertension in recipients from both groups. Also, the estimated post-transplant survival score was comparable between the 2 groups, excluding recipients’ selection bias. Surgery-associated risk factors were also considered. The choice of vascular site anastomosis usually occurs during the transplant surgery, considering the artery width, presence of atherosclerotic plaques, and technical conditions. Renal artery anastomosis to the internal iliac is more delicate, with an increased risk for late stenosis. In the present series, there was no difference in internal or external iliac anastomosis that could be attributed to the experience of the surgical team using the internal iliac as a preferred anastomosis site [14]. One can argue that vascular thrombosis was associated with prolonged anastomosis time or technical problems during anastomosis, such as bleeding or heterogeneous reperfusion. However, anesthesia and pre-operative data were similar in both groups. The use of the right kidney can increase the risk because the shorter renal vein can prolong anastomosis time. Amézquita et al [5] observed that 80% of early thrombosis occurred in the right kidney. In our series, there was no difference in thrombosis for the right or left kidney. We should consider that at our center during organ retrieval from deceased donors, it is routine to keep part of the cava vein with the right kidney vein to permit the surgical enlargement of the renal vein during back-table surgery. In the present series, data about vein surgery of specific backtable procedures were not available and the risk could not be analyzed. However, we observed an increased risk for early thrombosis for kidneys with multiple veins. In these cases, the usual procedure is the closure of the smallercaliber vein [4,5] or small ramifications of the main vein
819
to reduce risks associated with anastomosis of small-caliber veins and to prevent endothelial lesions associated with prolonged vascular manipulation. These procedures consider that venous drainage is not compromised by smallvein or small-ramification closure, because intra-renal ramifications can compensate the kidney perfusion. There is a lack of reports of renal transplants associated with multiple veins and risk for thrombosis. Considering our results, we decided to design a specific protocol to analyze the effects of venous manipulation and back-table surgery on vascular resistance and incidence of vascular complications. Vascular thrombosis can occur within the first postoperative day. Anuria could be considered an early marker of thrombosis. However, in this series, we observed kidneys with thrombosis with urine output within the first day, suggesting partial function. On the other hand, we observed kidneys from the control group with anuria that could be attributed to delayed graft function and acute tubular necrosis, a frequent finding in renal transplants from deceased donors [15]. To identify factors associated with early or late vascular thrombosis, cases were divided according to the time for diagnosis. Early thrombosis was diagnosed within 24 hours from surgery, whereas late thrombosis considered cases with an initial Doppler ultrasound with kidney perfusion and loss of perfusion in a sequential ultrasound. In the early thrombosis group, we observed a higher incidence of organ retrievaleassociated complications, such as heterogeneous perfusion. In the late group, however, we found no retrievalassociated complications, and both groups were comparable in all data analyzed. CONCLUSIONS
The incidence of vascular thrombosis in the present series is similar to that in previous reports. Use of the right or left kidney did not influence the incidence of thrombosis or the use of the internal or external iliac artery. The only risk factor was the presence of multiple veins in the thrombosis group. However, the impact of small-caliber vein closure and back-table vein surgery remains to be investigated. For early thrombosis, organ retrieval surgery complication can be a risk factor, and careful evaluation, preservation, and reperfusion could reduce the thrombosis risk. REFERENCES [1] Yildirim A. The importance of patient satisfaction and health-related quality of life after renal transplantation. Transplant Proc 2006;38:2831e4. [2] Penny MJ, Nankivell BP, Disney AP, et al. Renal graft thrombosis: a survey of 134 consecutive cases. Transplantation 1994;58:565e9. [3] Keller AK, Jorgensen TM, Jespersen B. Identification of risk factors for vascular thrombosis may reduce early renal graft loss: a review of recent literature. J Transplant 2012;2012:793461. [4] Vaccarisi S, Bonaiuto E, Spadafora N, et al. Complications and graft survival in kidney transplants with vascular variants: our experience and literature review. Transplant Proc 2013;45:2663e5.
820 [5] Amézquita Y, Méndez C, Fernández A, et al. Risk factors for early renal graft thrombosis: a case-controlled study in grafts from the same donor. Transplant Proc 2008;40:2891e3. [6] Bakir N, Sluiter WJ, Ploeg RJ, et al. Primary renal graft thrombosis. Nephrol Dial Transplant 1996;11:140e7. [7] Ojo AO, Hanson JA, Wolfe RA, et al. Dialysis modality and the risk of allograft thrombosis in adult renal transplant recipients. Kidney Int 1999;55:1952e60. [8] Englesbe MJ, Punch JD, Armstrong DR, et al. Single-center study of technical graft loss in 714 consecutive renal transplants. Transplantation 2004;78:623e6. [9] Benedetti E, Troppmann C, Gillingham K, et al. Short and long-term outcomes of kidney transplants with multiple renal arteries. Ann Surg 1995;221:406e14. [10] Hernández D, Rufino M, Armas S, et al. Retrospective analysis of surgical complications following cadaveric kidney
DE FREITAS, DE LIMA, AND MAZZALI transplantation in the modern transplant era. Nephrol Dial Transplant 2006;21:2908e15. [11] Cruzado JM, Manonelles A, Vila H, et al. Residual urinary volume is a risk factor for primary non-function in kidney transplantation. Transpl Int 2015;28:1276e82. [12] Phelan PJ, O’Kelly P, Tarazi M, et al. Renal allograft loss in the first post-operative month: causes and consequences. Clin Transplant 2012;26:544e9. [13] Hamed MO, Chen Y, Pasea L, et al. Early graft loss after kidney transplantation: risk factors and consequences. Am J Transplant 2015;15:1632e43. [14] Matheus WE, Reis LO, Ferreira U, et al. Kidney transplant anastomosis: internal or external iliac artery? Urol J 2009;6:260e6. [15] Sanches A, Etchebehere EC, Mazzali M, et al. The accuracy of (99m)tc-DTPA scintigraphy in the evaluation of acute graft complications. Int Braz J Urol 2003;29:507e16.
ABSTRACT Background. Renal transplant is the therapy of choice for patients with chronic renal disease. In recent years, improvement in immunosuppressive drugs reduced early graft loss associated with acute rejection. However, vascular thrombosis, accounting for 5% of early graft loss, can sensitize the recipient for human leukocyte antibodies, reducing the chance for a second transplant. The aim of this study was to identify risk factors for vascular thrombosis in a single transplant center, to design specific prevention protocol. Methods. This was a retrospective, case-control study. From the Renal Transplant Unit database, we identified 21 cases of vascular thrombosis in recipients of kidneys from deceased donors. Recipients from the contralateral kidney from the same donor, without vascular complications, were assigned to the control group. Data analyzed included donor, recipient, transplant surgery, and post-operative follow-up. The local ethics committee approved the protocol. Results. Thrombosis and control groups were comparable for recipient characteristics, cold ischemia time, organ side (right or left), and site of arterial anastomosis. We observed an increased risk for vascular thrombosis in kidneys with multiple veins (odds ratio, 11.32; P ¼ .03). Organ retrieval surgery complications, such as vascular lesions or heterogeneous perfusion, despite normal pre-implantation biopsy, were considered risk factors for vascular thrombosis within the first post-operative day (odds ratio, 7.1; P ¼ .03). Conclusions. In this series, multiple renal vein and organ retrieval surgery complications were risk factors for early vascular thrombosis.
R
ENAL transplant is considered the best therapy for patients with chronic renal disease, with a better survival and quality of life [1]. In past decades, a better graft survival has been associated with the development of new and more potent immunosuppressive agents. As a consequence, vascular thrombosis became the main cause of early graft loss, accounting for a third of early graft loss [2]. Risk factors for vascular thrombosis can be associated with recipient, graft, donor, and surgical procedure. However, because the majority of reports are retrospective and descriptive, results are controversial and dependent of center specificities, such as pre-transplant donor and recipient approach, surgical technique, anesthesia and post-operative management, as well as recipient age and body mass index [2e14]. In the present series, we analyzed a group of patients ª 2017 Elsevier Inc. All rights reserved. 230 Park Avenue, New York, NY 10169
Transplantation Proceedings, 49, 817e820 (2017)
with early vascular thrombosis and compared them with recipients of contralateral kidney from the same donor to identify possible risk factors for vascular graft thrombosis. METHODS This was a retrospective, case-control study. From the Renal Transplant Unit Database, we selected the cases of early graft loss
*Address correspondence to Marilda Mazzali, Division of Nephology, Department of Medicine, School of Medical Sciences, State University of Campinas-Unicamp, Rua Tessalia Vieira de Camargo, 126, Cidade Universitária Zeferino Vaz, 13083-970 Campinas, São Paulo, Brasil. E-mail: [email protected] 0041-1345/17 http://dx.doi.org/10.1016/j.transproceed.2017.03.004
817
818 caused by vascular thrombosis. Recipients from the contralateral kidney from the same donor were considered as control subjects. Inclusion criteria included recipients of renal transplant from August 2005 to August 2015, age 16 years at transplant surgery. Exclusion criteria included pediatric renal transplant recipients and recipients from an isolated kidney (when contralateral kidney was discarded or transplanted in a different center). Vascular thrombosis was defined as the absence of vascular flow at Doppler ultrasound within the first post-operative day. In cases of doubt, a renal dynamic renal scintigraphy with TC99m-DTPA was performed, according to center protocol [15]. Graft nephrectomy and histologic analysis were indicated if thrombosis was confirmed. Data were collected from medical records and included donor and recipient data, surgical and anesthesia controls, immunosuppression, and anatomic description. The local ethics committee approved the protocol. Statistical analysis was performed with the use of Prism 6.0 Software. Significance was considered at a value of P < .05.
RESULTS
From August 2005 to August 2015, 1016 renal transplants were performed at our transplant center. The majority of the recipients (n ¼ 944, 92.9%) were 16 years old at transplant and received a kidney from a deceased donor (n ¼ 786, 83.2%). In a 10-year period, early vascular thrombosis within the first month after transplant was diagnosed in 26 patients, resulting in a 3.3% incidence. According to our criteria, we analyzed only the cases in which the data of the recipients of contralateral kidneys were available. The final study group excluded 5 cases: 2 for the contralateral kidney implanted in a pediatric recipient, 2 for kidney implanted in a different transplant center, and 1 case of unavailable data. The study group comprised 21 renal transplants with thrombosis and 21 contralateral kidney controls. Twenty-one donors were 39.7 15.7 years old, with a similar sex distribution (10 male) and body surface of 1.78 0.22 m2. Donor serum creatinine was normal (1.25 0.74 mg/dL), and the main cause of brain death was stroke (57%), followed by head trauma (38%). Recipients from thrombosis and control groups were comparable in age, sex, length of pre-transplant dialysis, previous blood transfusions, history of systemic hypertension or diabetes, use of acetyl salicylic acid, and pretransplant hemoglobin levels (Table 1). Groups also had a similar estimated post-transplant survival score of 34.1% for the thrombosis group and 36.1% for the control group (P ¼ NS). Kidney side (left or right) did not differ between groups. However, we observed a higher incidence of multiple veins in the thrombosis group compared with the control Group (Table 2). There was no correlation between thrombosis and surgical or anesthesia procedures, nor in the immediate post-operative treatment. Diagnosis of vascular thrombosis was done by means of a routine Doppler ultrasound within the first post-operative day. Vascular thrombosis was identified at the first exam in 53% of the cases, whereas in the 47% remaining cases,
DE FREITAS, DE LIMA, AND MAZZALI Table 1. Recipient Characteristics According to Groups Thrombosis
Control
Age (years) 45.2 11.3 49.9 10.4 Sex (male:female) 12:9 15:6 Body surface area (m2) 1.80 0.22 1.78 0.24 Length of dialysis pre 46.6 32.8 45.3 31.9 transplant (mos) Urine output before transplant (mL) 377.8 426.4 549.0 693.4 Blood transfusion before transplant 7 (33.3%) 10 (47.6%) (% patients) Previous femoral catheter for 2 (9.5%) 0 dialysis (% patients) Pre-transplant hypertension (%) 19 (90.4%) 21 (100%) Pre-transplant diabetes (%) 6 (28.6%) 4 (19%) Pre-transplant acetyl salicylic acid 8 (38.1%) 7 (33.3%) Pre-transplant hemoglobin (g/dL) 11.9 2.5 12.3 1.8
diagnosis was made in sequential Doppler ultrasound. When patients were analyzed according to time of thrombosis diagnosis, in the early (first) or late (sequential) exams, we observed that complications associated with organ retrieval, such as multiple vessels, vascular lesion, or heterogeneous perfusion, were more frequent in the early thrombosis group (Table 3). However, pre-implantation biopsies from these kidneys showed normal renal parenchyma histology.
DISCUSSION
Vascular thrombosis, although rare, is an important cause of early graft loss, with a negative impact on patient survival associated with a risk for development of anti-HLA antibodies [11e13]. In the present series, the incidence of vascular thrombosis was 3.3%, similar to previous reports [8,11]. The overall incidence of vascular thrombosis in a series of 2300 renal transplants from January 1984 to August 2015 was of 3.7%, corresponding to 84 episodes. Identification of patients at risk for thrombosis remains a problem. Previous reports suggest different factors, such as Table 2. Risk Factors for Early Vascular Thrombosis, Organ- and Surgery-Related Thrombosis
Right kidney Cold ischemia (min) Multiple arteries Multiple veins Renal artery anastomosis (min) Renal vein anastomosis (min) Internal iliac artery anastomosis (%) Total bleeding (mL) Heterogeneous reperfusion (%) Mean blood pressure at reperfusion (mm Hg) Intra-operative vasoactive drugs (%) Anesthesia length (min) Post-operative vasoactive drugs (%) Immediate diuresis
11 (52.4%) 20.15 6.14 2 (9.5%) 4 (19%) 26.1 12.1 19.6 5.2 9 (42.8%) 552.3 411.5 10 (47%) 99.8 12.0
Control
10 (47.6%) 20.2 4.7 0 0 24.4 7.5 17.6 3.8 8 (38%) 800 592.1 5 (23.8%) 95.5 18.2
16 (76.1%) 14 (66.6%) 294.5 64.4 293.3 48.2 9 7 616.8 863.9 977.4 951.0
EARLY VASCULAR THROMBOSIS AFTER KT Table 3. Relative Risk for Vascular Thrombosis RR (Confidence Interval)
Risk factor for thrombosis Female recipient Right kidney Multiple vein Heterogeneous perfusion Risk factor for early thrombosis Organ retrieval associated*
0.83 (0.45e1.55), P ¼ NS 1.32 (0.81e2.15), P ¼ NS 2.23 (1.5e3.18), P ¼ .08 1.63 (0.91e2.9), P ¼ NS 2.66 (1.08e7.46), P ¼ .03
*Organ retrievaleassociated complications include multiple veins and heterogeneous perfusion.
older age, female donor, number of arteries, kidney side, previous use of acetyl salicylic acid, prolonged cold ischemia, and previous history of recipient’s hypertension and/or diabetes [2e13]. These discrepancies can be a consequence of the characteristics of these reports, mainly retrospective studies and small series of cases, and can be influenced by population characteristics, donor source, surgical technique, and surgical team experience. To exclude donor-associated factors, we compared renal transplant patients with vascular thrombosis and their control subjects, recipients from the contralateral kidney from the same donor. There was no difference in sex, age, primary renal disease, and incidence of diabetes or hypertension in recipients from both groups. Also, the estimated post-transplant survival score was comparable between the 2 groups, excluding recipients’ selection bias. Surgery-associated risk factors were also considered. The choice of vascular site anastomosis usually occurs during the transplant surgery, considering the artery width, presence of atherosclerotic plaques, and technical conditions. Renal artery anastomosis to the internal iliac is more delicate, with an increased risk for late stenosis. In the present series, there was no difference in internal or external iliac anastomosis that could be attributed to the experience of the surgical team using the internal iliac as a preferred anastomosis site [14]. One can argue that vascular thrombosis was associated with prolonged anastomosis time or technical problems during anastomosis, such as bleeding or heterogeneous reperfusion. However, anesthesia and pre-operative data were similar in both groups. The use of the right kidney can increase the risk because the shorter renal vein can prolong anastomosis time. Amézquita et al [5] observed that 80% of early thrombosis occurred in the right kidney. In our series, there was no difference in thrombosis for the right or left kidney. We should consider that at our center during organ retrieval from deceased donors, it is routine to keep part of the cava vein with the right kidney vein to permit the surgical enlargement of the renal vein during back-table surgery. In the present series, data about vein surgery of specific backtable procedures were not available and the risk could not be analyzed. However, we observed an increased risk for early thrombosis for kidneys with multiple veins. In these cases, the usual procedure is the closure of the smallercaliber vein [4,5] or small ramifications of the main vein
819
to reduce risks associated with anastomosis of small-caliber veins and to prevent endothelial lesions associated with prolonged vascular manipulation. These procedures consider that venous drainage is not compromised by smallvein or small-ramification closure, because intra-renal ramifications can compensate the kidney perfusion. There is a lack of reports of renal transplants associated with multiple veins and risk for thrombosis. Considering our results, we decided to design a specific protocol to analyze the effects of venous manipulation and back-table surgery on vascular resistance and incidence of vascular complications. Vascular thrombosis can occur within the first postoperative day. Anuria could be considered an early marker of thrombosis. However, in this series, we observed kidneys with thrombosis with urine output within the first day, suggesting partial function. On the other hand, we observed kidneys from the control group with anuria that could be attributed to delayed graft function and acute tubular necrosis, a frequent finding in renal transplants from deceased donors [15]. To identify factors associated with early or late vascular thrombosis, cases were divided according to the time for diagnosis. Early thrombosis was diagnosed within 24 hours from surgery, whereas late thrombosis considered cases with an initial Doppler ultrasound with kidney perfusion and loss of perfusion in a sequential ultrasound. In the early thrombosis group, we observed a higher incidence of organ retrievaleassociated complications, such as heterogeneous perfusion. In the late group, however, we found no retrievalassociated complications, and both groups were comparable in all data analyzed. CONCLUSIONS
The incidence of vascular thrombosis in the present series is similar to that in previous reports. Use of the right or left kidney did not influence the incidence of thrombosis or the use of the internal or external iliac artery. The only risk factor was the presence of multiple veins in the thrombosis group. However, the impact of small-caliber vein closure and back-table vein surgery remains to be investigated. For early thrombosis, organ retrieval surgery complication can be a risk factor, and careful evaluation, preservation, and reperfusion could reduce the thrombosis risk. REFERENCES [1] Yildirim A. The importance of patient satisfaction and health-related quality of life after renal transplantation. Transplant Proc 2006;38:2831e4. [2] Penny MJ, Nankivell BP, Disney AP, et al. Renal graft thrombosis: a survey of 134 consecutive cases. Transplantation 1994;58:565e9. [3] Keller AK, Jorgensen TM, Jespersen B. Identification of risk factors for vascular thrombosis may reduce early renal graft loss: a review of recent literature. J Transplant 2012;2012:793461. [4] Vaccarisi S, Bonaiuto E, Spadafora N, et al. Complications and graft survival in kidney transplants with vascular variants: our experience and literature review. Transplant Proc 2013;45:2663e5.
820 [5] Amézquita Y, Méndez C, Fernández A, et al. Risk factors for early renal graft thrombosis: a case-controlled study in grafts from the same donor. Transplant Proc 2008;40:2891e3. [6] Bakir N, Sluiter WJ, Ploeg RJ, et al. Primary renal graft thrombosis. Nephrol Dial Transplant 1996;11:140e7. [7] Ojo AO, Hanson JA, Wolfe RA, et al. Dialysis modality and the risk of allograft thrombosis in adult renal transplant recipients. Kidney Int 1999;55:1952e60. [8] Englesbe MJ, Punch JD, Armstrong DR, et al. Single-center study of technical graft loss in 714 consecutive renal transplants. Transplantation 2004;78:623e6. [9] Benedetti E, Troppmann C, Gillingham K, et al. Short and long-term outcomes of kidney transplants with multiple renal arteries. Ann Surg 1995;221:406e14. [10] Hernández D, Rufino M, Armas S, et al. Retrospective analysis of surgical complications following cadaveric kidney
DE FREITAS, DE LIMA, AND MAZZALI transplantation in the modern transplant era. Nephrol Dial Transplant 2006;21:2908e15. [11] Cruzado JM, Manonelles A, Vila H, et al. Residual urinary volume is a risk factor for primary non-function in kidney transplantation. Transpl Int 2015;28:1276e82. [12] Phelan PJ, O’Kelly P, Tarazi M, et al. Renal allograft loss in the first post-operative month: causes and consequences. Clin Transplant 2012;26:544e9. [13] Hamed MO, Chen Y, Pasea L, et al. Early graft loss after kidney transplantation: risk factors and consequences. Am J Transplant 2015;15:1632e43. [14] Matheus WE, Reis LO, Ferreira U, et al. Kidney transplant anastomosis: internal or external iliac artery? Urol J 2009;6:260e6. [15] Sanches A, Etchebehere EC, Mazzali M, et al. The accuracy of (99m)tc-DTPA scintigraphy in the evaluation of acute graft complications. Int Braz J Urol 2003;29:507e16.