Laparoscopy in renal transplant patients

ELSEVIER

LAPAROSCOPY IN RENAL TRANSPLANT PATIENTS PAOLO FORNARA,

CHRISTIAN

DOEHN,

LUTZ FRICKE,

JOCHEM

HOYER, AND DIETER JOCHAM

ABSTRACT Objectives. To evaluate the use of laparoscopic techniques in patients with a renal transplant. Methods. Since 1992, 358 patients have undergone urologic laparoscopy at our hospital. Among these, 37 procedures (10.4%) were performed in patients with a renal transplant: 14 bilateral nephrectomies for severe drug-resistant hypertension, 9 marsupializations of symptomatic lymphoceles, 6 renal allograft biopsies in patients with clotting abnormalities, 6 unilateral nephrectomies, and 2 nephroureterectomies for recurrent episodes of pyelonephritis and symptomatic vesicoureteral reflux, respectively. Results. Five complications (14%) and three conversions (8%) occurred. Patients who underwent successful laparoscopic operations began mobilization and oral intake on the day after the operation. The hospital stay ranged from 1 to 6 days. In the nephrectomy groups, perioperative urine outputs remained stable and postoperative urine outputs were increased as compared with those in the perioperative period (P ~0.05). Postoperatively, serum creatinine remained stable or improved in patients who underwent nephrectomy or marsupialization of lymphocele. Conclusions. Our results indicate that laparoscopic techniques are safe and effective in the treatment of patients with a renal transplant. Renal allograft function apparently is not affected by laparoscopic procedures. UROLOGY 49: 521-527, 1997. 0 1997, Elsevier Science Inc. All rights reserved.

I

n the last 6 years, laparoscopic surgery has gained increased attention in the field of urology. Laparoscopic operations on the kidney have been performed at multiple centers, with an increasing number of reports. Laparoscopic unilateral nephrectomy, even for malignant diseases, has been reported, with favorable outcome, by several groups of researchers.lm3 Moreover, bilateral nephrectomy has been performed for severe drug-resistant hypertension after renal transplantation.4,5 In addition, laparoscopic nephroureterectomy for transitional cell carcinoma affecting the upper urinary tract or reflux anomaly has been described.6,7 Symptomatic lymphocele subsequent to renal transplantation has been treated effectively by laparoscopic marsupialization.8-‘1 Several groups of investigators have reported decreased urine production in patients undergoing laparoscopic operations or in patients with in-

From the Departments of Urology and Internal Medicine, and the Renal Transplant Unit, Medical University of Liibeck, Liibeck, Germany Reprint requests: Paolo Fomara, M.D., Department of LJrology, Medical University of Liibeck, Ratzeburger Allee 160, Liibeck 23538, Germany Submitted: April 17, 1996, accepted (with revisions): October 14, 1996 COPYRIGHT 1997 BY ELSEVIER SCIENCE INC. ALL RIGHTS RESERVED

creased intra-abdominal pressure resulting from postoperative hemorrhage.12-I4 This phenomenon is probably a multifactorial process. However, similar observations have not been reported for renal transplant patients undergoing laparoscopy. We have been interested in expanding the application of laparoscopic operations to the renal transplant population. We describe our experience with laparoscopic unilateral and bilateral nephrectomy, unilateral nephroureterectomy, renal allograft biopsy, and marsupialization of symptomatic lymphocele in patients with a renal transplant at the Medical University of Liibeck. MATERIAL

AND

METHODS

PATIENT POPULATION Between June 1993 and December 1995, 37 patients (19 women and 18 men aged 22 to 59 years, mean 37) underwent laparoscopic operations after renal transplantation at our hospital. Bilateral nephrectomy was indicated for severe drugresistant hypertension in 14 patients (Table I). One of the 14 had to start hemodialysis before undergoing bilateral nephrectomy. However, his renal allograft still produced about 1500 mL urine each day. In 9 patients, post-transplant lymphoceles caused hydronephrosis, impaired renal allograft function, or pain. After percutaneous drainage with or without sclerotherapy, lymphocele recurred and the patients were selected for laparoscopic marsupialization. Six patients with recurrent episodes of pyelonephritis and 2 patients with symptomatic 0090-4295/97/$17,00 PII SOO90-4295(96)00559-6

521

TABLE Parameter

412 35

717 37

2/o 27

214 40

415 43

7

13

4

3

4

Unilateral Nephrectomy*

Parameter No. of ports Mean operative time [minutes) Mean blood loss (mL) Complication rate (%) Conversion rate (%I Resumption of diet and mobilization (days) Mean hospital stay (days1 patients.

* Includes patientsrequiringlurthermedud

I I.

Operative

Bilateral Nephrectomy

Unilateral Nephroureterectomy

and postoperative Unilateral Nephroureterectomy

415

516

415

100 250 17 17

190 300 21 14

120 220 None None

l-3

l-4 3

4

Renal Allograft Biopsy

Marsupialization of Lymphocele

data Renal Allograft Biopsy+

Marsupialiiation of Lymphocele

1

3

35 40 None None

42 90 11 None

1

1

1

3

5

4

~reatmenf for rejection.

vesicoureteral reflux were considered for unilateral nephrectomy and nephroureterectomy, respectively. Six patients with impaired renal allograft function of an undetermined cause were hospitalized to obtain a transplant biopsy. These patients had severe clotting abnormalities such as thrombocytopenia, von Willebrand’s disease, or phenprocoumon therapy. Under such conditions, percutaneous biopsy under ultrasound guidance was considered difficult. Therefore, the biopsy was planned to be performed laparoscopically. OPERATIVE PROCEDURES Except for the patients undergoing laparoscopic biopsy, all patients were admitted to the hospital on the day before the operation and underwent routine diagnostic investigations and bowel preparation. A single shot of intravenous penicillin or cephalosporin was administered 2 hours preoperatively. Oral immunosuppressive medication was administered continuously during the hospital stay. A preoperative angiogram or cystoscopy with insertion of ureteric stem was not performed. Unilateral and bilateral nephrectomy were completed as previously described by several groups of researchers.1.2.4.5 Laparoscopic nephroureterectomy was performed as reported by McDougall et al,6 and Rassweiler et al.’ Marsupialization of lymphocele was achieved as described by several groups of researchers.8-1’ For renal allograft biopsy, one port was used. The camera was inserted, and the renal allograft was identified bulging into the abdominal cavity. Intraperitoneally, a 14gauge biopsy needle for biopsy gun and a second Zgauge needle were inserted. The biopsy was obtained under direct vision, followed by immediate application of fibrin glue through the second needle to prevent or stop bleeding.

RENAL ALLOGRAFT FUNCTION Special interest was focused on renal allograft function. In all patients, daily serum creatinine levels (PmoVL) were de522

data

Bilateral Nephrectomy

TABLE

converted

Demographic

Unilateral Nephrectomy

No. of women/men Mean age (years) Mean interval to transplantation (months)

* Includes

I.

termined before and after laparoscopy during the hospital stay. In addition, 24-hour urine outputs were obtained before and after the operation in all patients who underwent nephrectomy or nephroureterectomy (n = 22). Perioperative and early postoperative urine outputs were measured by bladder catheter drainage. In all patients, urine output was calculated in milliliters per kilogram of body weight per hour (mlIkg/hr) to provide intraindividual and interindividual comparison. Friedman test and Wilcoxon-Wilcox test were used to compare preoperative, perioperative, and postoperative urine outputs as well as preoperative and postoperative serum creatinine in the nephrectomy groups.

RESULTS

According to the procedure, the mean operative time ranged from 35 to 190 minutes (Table II). Five complications (14%) and three conversions (8%) were noted. Hospital stay ranged from 3 to 5 days in patients who underwent successful laparoscopy. In the nephrectomy groups and the lymphocele group, neither parenteral nutrition nor changes in the oral immunosuppressive treatment were necessary. All patients treated with cyclosporine had stable blood levels. BILATERAL

NEPHRECTOMY

The mean operative time for bilateral nephrectomy was 190 minutes, and the mean blood loss was 300 mL (Table II). In 1 patient, a urinary tract infection developed after nephrectomy. He was UROLOGY

49 (4), 1997

TABLE Unilateral Nephrectomy

Parameter Mean follow-up (months) Successful treatment* Good renal allograft function+

I I I.

Bilateral Nephrectomy

follow-up Unilateral Nephroureterectomy

Renal Allograft Biopsy

Marsupialization of Lymphocele

12 616

13 10/14

13 212

17 616

15 919

616

10/14

212

416

819

infection inunilateral nephrectomy andnephroureterectomy, controlled blood pressure in bilateral nephrectomy, biopsy suitable for histopathologic examination inrenalallograJt biopsy, and freeofwcwwnce inmarsupialization oflymphocele. ’ Defined as suun~ creatinine level lessthan200 umoUL. * Free

of

treated with oral penicillin and had an uneventful recovery. Another patient had fever of undetermined cause which subsided after 2 days of antibiotic treatment. A third patient demonstrated retroperitoneal hematoma and required 2 U blood. In addition, two conversions were noted. One patient needed conversion for bleeding from the right renal artery. He received 3 U blood, and open surgery was completed without further complications. The other patient had multiple intra-abdominal adhesions after long-term continuous ambulatory peritoneal dialysis (CAPD) and therefore was converted to open transperitoneal nephrectomy. For this group, the complication rate was 21% and the conversion rate was 14%. All patients, except those converted, resumed oral intake and mobilization on postoperative day 1 (Table II). Hospital stay after successful laparoscopic operation ranged from 3 to 6 days. In the converted patients, hospital stay lasted 7 and 9 days, respectively. At mean follow-up of 13 months, 10 of 14 patients (71%) showed well-controlled blood pressure, and fewer or no antihypertensive drugs were needed (Table III). The remaining 4 patients showed no improvement in blood pressure, and 3 of the 4 had resumed hemodialysis due to chronic rejection.

UNILATERAL NEPHRECTOMY AND NEPHROLJRETERECTOMY The mean operative time in unilateral nephrectomy and nephroureterectomy was 100 and 120 minutes, respectively (Table II). The mean blood loss was 250 mL in unilateral nephrectomy and 220 mL in nephroureterectomy. One patient had to be converted to open nephrectomy due to bleeding from the renal artery. He received 2 U blood and recovered without further complications. Postoperatively, 1 patient had a retroperitoneal hematoma and received 2 U blood. For this group, the complication and conversion rates were 17%. The mean hospital stay was 3 days except for that of the converted patient. At mean follow-up of 12 and 13 months respectively, no patients had signs of infection (Table III). UROLOGY 49

(41,19%

MARSLJPIALIZATION OF LYMPHOCELE The mean operative time for marsupialization of lymphocele was 42 minutes, and the estimated blood loss was 90 mL (Table II). In 1 patient, fever of undetermined cause developed. He received oral cephalosporin, and his body temperature became normal after 2 days. Patients were discharged between postoperative days 2 and 5. In 3 patients, serum creatinine level had not been affected by preoperative lymphocele. Postoperative renal allograft function remained stable in these patients. In 6 patients, the lymphocele had caused hydronephrosis and impaired allograft function. Postoperative serum creatinine returned to levels observed before occurrence of the lymphocele in all patients (Table III). At mean followup of 15 months, no recurrence of lymphocele was evident and 8 of 9 patients had serum creatinine levels similar to their best preoperative results.

RENALALLOGRAFT BIOPSY In the renal allograft biopsy group, the mean operative time was 35 minutes (Table II). All specimens were suitable for histopathologic examination, and no bleeding or hematoma occurred. With regard to postoperative status, the patients were ready for discharge from the hospital on the day after the operation, but further medical treatment in accordance with the biopsy results was necessary in 4 patients. At mean follow-up of 17 months, 2 patients had resumed hemodialysis due to chronic rejection; the remaining 4 had good renal allograft function with a serum creatinine less than 200 pmol/L (Table III). RENALALLOGRAFT FU~XTIONIN NEPHRECTOMY GROWS Urine outputs were measured in patients who underwent nephrectomy or nephroureterectomy (n = 22). In these groups, the perioperative urine outputs ranged from 0.62 to 4.64 mIfkg/hr (mean 1.64) and had not decreased significantly as compared with preoperative urine outputs (between 0.7 and 3.2 ml/kg/l-u-,mean 1.95). Early postoperative urine outputs were significantly (P <0.05) 523

1

0

n=22 Preoperative FIGURE 1. Preoperative, nephrectomy.

perioperative,

n=22 Perioperative and postoperative

n=22 Postoperative

urine outputs in 22 patients

#I6

#6

*5

*5

who underwent

laparoscopic

#6,9,11

*5

*9

*9

0

n=19

n=19

Preoperative

Postoperative

n=16

Follow -up

and postoperative serum creatinine levels in 22 patients who underwent laparoscopic FIGURE 2. Preoperative nephrectomy. Patients with poor allograt? function (asterisk) and patients on hemodialysis (pound sign) are excluded.

increased (range 0.76 to 3.97, mean 2.41) as compared with perioperative outputs (Fig. 1). Preoperative serum creatinine levels ranged from 99 to 180 pmol/L in 19 patients (mean 142). Of the remaining patients, 2 had poor allograft function 524

with serum creatinine levels of 400 and 518 PmoV L, respectively. One patient had started hemodialysis before undergoing bilateral nephrectomy. Postoperatively, serum creatinine levels were measured daily and remained stable in all patients. On UROLOGY 49 (41, 1997

patients’ discharge from hospital, serum creatinine ranged from 99 to 197 ymol/L (mean 153) in the 19 patients with good preoperative renal allograft function (P = NS). The 2 patients with poor function had serum creatinine levels of 420 and 499 pmol/L, respectively. At mean follow-up of 10 (bilateral nephrectomy group), 12 (unilateral nephrectomy group), and 13 months (unilateral nephroureterectomy group), 18 patients showed good renal allograft function, defined as serum creatinine level less than 200 ~rnol/J_(range 87 to 192, mean 138, P = NS). The 2 patients with preoperative poor renal allograft function and a third patient had to start hemodialysis due to chronic allograft rejection (Fig. 2). COMMENT With increasing experience, the field of indications for laparoscopic operations in urology has expanded. The first successful laparoscopic nephrectomy was performed by Clayman et al. in 1990, and many laparoscopic procedures on the kidney are now being performed at multiple centers wor1dwide.l Recently, Eraky et al. published the results of 106 laparoscopic unilateral nephrectomies and Gill et al. described the morbidity in 185 laparoscopic nephrectomies performed at five centers in the United States.2’3 The rate of complications was 30.2% and 16%, respectively, with a decreasing incidence in accordance with the learning curve. Conversion to open surgery was necessary in 8.5% and 5.4%, respectively. There was no mortality in the reported series, and hospital stay and reconvalescence times were short. A laparoscopic bilateral nephrectomy was reported by Bales et al., who performed this procedure for renin-mediated hypertension in 2 patients after renal transplantation.4 Recently, we described 11 patients with renal transplants who underwent laparoscopic bilateral nephrectomy for severe drug-resistant hypertension.5 Small series of laparoscopic nephroureterectomy for transitional cell carcinoma of the upper urinary tract or vesicoureteral reflux were reported by McDougall et aL6 and Rassweiler et uL7 Based on our clinical experience with laparoscopic nephrectomy in patients who did not undergo transplant, we performed 6 unilateral nephrectomies, 14 bilateral nephrectomies, and 2 nephroureterectomies in patients with renal transplant. The indications were severe drug-resistant hypertension in patients who underwent bilateral nephrectomy and recurrent episodes of pylonephritis without or with vesicoureteral reflux in patients who underwent unilateral nephrectomy or nephroureterectomy. Postoperatively, no patient in the unilateral nephrectomy group had signs of UROLOGY 49 (41, 1997

pyelonephritis. In the bilateral nephrectomy group, 10 patients (71%) needed less or no antihypertensive medication, The conversion rate was 14% in the bilateral nephrectomy group and 17% in the unilateral group. These rates were twice as high as our results in patients who did not undergo transplant (data not shown) and those reported by other researchers.2*3 However, when more experience is gained in patients with a renal transplant, the conversion rate is likely to decrease. The complication rate in the nephrectomy groups was 18%, which is comparable to the rate noted in our performance of laparoscopic unilateral nephrectomy in patients who did not undergo transplant and to the results of Eraky et al.’ and Gill et ~1.~For open bilateral nephrectomy, a morbidity rate of 18% to 45% has been reported for large series.15-r7 These results were achieved in patients undergoing dialysis before a planned renal transplantation. Only two episodes of postoperative infection occurred in our nephrectomy groups. Both were brought under control with antibiotics, and no further complications were observed. Durations of immobilization, hospitalization, and reconvalescence were short in most patients, reflecting the well-known benefits of laparoscopic techniques as compared with open surgery. Several groups of investigators have reported a decreased urine output from native kidneys during laparoscopy. Iwase et al. studied 7 patients who underwent laparoscopic cholecystectomy.‘* After initiation of the pneumoperitoneum, effective renal plasma flow, glomerular filtration rate, and urine output were significantly decreased. These results were not due to hemodynamic alterations. Chang et al. reported 6 patients with significantly decreased urine output during laparoscopic surgery.13 Perioperative hemodynamics in their study also were stable. Preoperative and postoperative serum creatinine concentrations did not differ significantly. Risk factors for the development of oliguria were not identified, but renal ischemia resulting from extravascular compression was recognized as an etiologic factor. Richards et al. investigated 4 patients with acute renal failure and increased abdominal pressure from postoperative hemorrhage.14 They suspected obstruction of the vena cava and renal veins. To our knowledge, there are no reports of investigations of renal allograft function during laparoscopy. In our series, as compared with preoperative results, there were no major changes in urine outputs during laparoscopic nephrectomy or nephroureterectomy. Moreover, there were no significant changes in postoperative serum creatinine level (during hospital stay and at follow-up). These results are in 525

contrast to those observed in patients who did not undergo transplant. In our series, increase in intraabdominal pressure with renal ischemia or compression of the vena cava or renal veins might have been evident but did not result in significant decrease in urine outputs. Major changes in hemodynamics during laparoscopy did not occur (data not shown). Therefore, other factors may play a role in the reduction of urine output during laparoscopy in patients who do not undergo transplant. Denervation of the renal allograft might be a reason for nonaffected allograft function during laparoscopy. However, further studies are needed to explain this phenomenon. Renal allograft biopsies are generally obtained by percutaneous techniques under ultrasound guidance. The complication rate in large series ranged from 4.3% to 10°&18-22 The most common problem was hematuria, and operative treatment was required in a few patients. Rarely, occurrence of arteriovenous fistula or allograft loss has been described.** Apart from the possible complications, approximately 4% of all biopsies were not suitable for histopathologic examination. We performed a laparoscopic renal allograft biopsy in 6 patients with impaired allograft function of an undetermined cause. All patients had severe clotting abnormalities, and percutaneous biopsy was considered dangerous. The biopsies were performed under direct vision, and all were suitable for histopathologic examination. There was no morbidity in this group. Although technically a simple procedure, the laparoscopic approach is more invasive than a percutaneous biopsy and should be reserved for a minority of patients. Perirenal fluid collections including lymphoceles have been reported to develop in almost 50% of patients after renal transplantation.23 Most of the lymphoceles are asymptomatic and treatment is not required. However, once the ureter is compressed and hydronephrosis with impaired renal allograft function is present, the lymphocele must be drained. Complications such as compression of vessels with possible deep vein thrombosis, pain, or infection may also occur. Percutaneous aspiration or temporary drainage with or without sclerotherapy is considered first-line treatment, but recurrence of lymphocele is common. Open and, more recently, laparoscopic marsupialization of lymphoceles has been shown to be effective, with a low rate of recurrence.8-1o Gill et al. investigated laparoscopic and open marsupialization of lymphoceles after renal transplantation or pelvic lymphadenectomy. l1 Patients who underwent open marsupialization had a longer operative time but less blood loss, earlier resumption of oral intake, shorter hospital stay, and shorter convalescence than the laparoscopy group. Lymphocele 526

did not recur and, owing to the favorable results, Gill et al. recommend the laparoscopic approach for treatment of recurrent lymphocele. In our series, the mean operative time was 42 minutes, a shorter time than that required in a previous group of patients who underwent open marsupialization of lymphocele between 1990 and 1993 at our hospital (data not shown). In that group of 8 patients, the mean operative time was 115 minutes. Results for resumption of oral intake, hospital stay, duration of convalescence, or success rate were comparable to those reported by Gill et al. Consecutively, no patient with symptomatic lymphocele has undergone open surgery since the introduction of laparoscopic techniques at our hospital. CONCLUSIONS The results of our series indicate that laparoscopic operations produce similar results in patients undergoing renal transplant and in those who do not undergo renal transplant. Morbidity, including rate of infection, is moderate and not increased as compared with that caused by laparoscopy in patients who do not undergo transplant. Moreover, oral immunosuppressive medication can be administered continuously during the hospital stay. Renal allograft function, represented by serum creatinine level and perioperative and postoperative urine outputs, apparently is not affected by laparoscopy. Therefore, laparoscopic procedures, without threatening the allograft themselves, are feasible for treatment of potentially allograft-threatening disorders that might do so. REFERENCES 1. Clayman RV, Kavoussi LR, Soper NJ, Dierks SM, Meretyk S, Darcy MD, Roemer FD, Pingleton ED, Thompson PG, and Long SR: Laparoscopic nephrectomy: initial case report. J Ural 146: 278-282, 1991. 2. Eraky I, El-Kappany HA, and Ghoneim MA: Laparoscopic nephrectomy: Mansoura experience with 106 cases. Br J Urol75: 271-275,1995. 3. Gill IS, Kavoussi LR, Clayman RV, Ehrlich R, Evans R, Fuchs G, Gersham A, Hulbert JC, McDougall EM, Rosenthal T, et al: Complications of laparoscopic nephrectomy in 185 patients: a multi-institutional review. J Urol 154: 479-483, 1995. 4. Bales GT, Fellner SK, Chodak GW, and Rukstalis DB: Laparoscopic bilateral nephrectomy for renin-mediated hypertension. Urology 43: 874-877, 1994. 5. Fornara P, Doehn C, Fricke L, Durek C, Thyssen G, and Jocham D: Laparoscopic bilateral nephrectomy: results in 11 renal transplant patients. J Urol 157: 445-449, 1997. 6. McDougall EM, Clayman RV, and Elashry 0: Laparoscopic nephroureterectomy for upper tract transitional cell cancer: the Washington University experience. J Urol 154: 975-980, 1995. 7. Rassweiler J, Henkel TO, Stoch C, Greschner M, Becker P, Preminger GM, Schulman CC, Frede T, and Alken P: Retroperitoneal laparoscopic nephrectomy and other procedures

UROLOGY 49 (41, 1997

in the upper retroperitoneum using a ballon dissection technique. Em Urol 25: 229-236, 1994. 8. McCullough CS, Soper NJ, Clayman RV, So SSK, Jendrisak MD, and Hanto DW: Laparoscopic drainage of a posttransplant lymphocele. Transplantation 51: 725-727, 1991. 9. Fahlenkamp D, Raatz D, Schdnberger B, and Loening SA: Laparoscopic lymphocele drainage after renal transplantation. J Urol 150: 316-318, 1993. 10. Lange V, Schardey HM, Meyer G, Illner WD, Petersen P, and Land W: Laparoscopic deroofing of post-transplant lymphoceles. Transplant Int 7: 140- 143, 1994. 11. Gill IS, Hodge EE, Munch LC, Goldfarb DA, Novick AC, and Lucas BA: Transperitoneal marsupialization of lymphoceles: comparison of laparoscopic and open techniques. J Urol 153: 706-711, 1995. 12. Iwase K, Takenaka H, Ishizaka T, Ohata T, Oshima S, and Sakaguchi K: Serial changes in renal function during laparoscopic cholecystectomy. Eur Surg Res 25: 203-212, 1993. 13. Chang DT, Kirsch AJ, and Sawczuk IS: Oliguria during laparoscopic surgery. J Endourol8: 349-352, 1994. 14. Richards WO, Scovill W, Shin B, and Reed W: Acute renal failure associated with increased intra-abdominal pressure. Ann Surg 197: 183-187, 1983. 15. Viner NA, Raw1 JC, Braren V, and Rhamy RK: Bilateral nephrectomy: an analysis of 100 consecutive cases. J Urol 113: 291-294, 1975.

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16. Yarimizu SN, Susan LP, Straffon RA, Stewart BM, Magnusson MO, and Nakamoto SS: Mortality and morbidity in pretransplant bilateral nephrectomy: analysis of 305 cases. Urology 12: 55-58, 1978. 17. Darby CR, Cranston D, Raine AEG, and Morris PJ: Bilateral nephrectomy before transplantation: indications, surgical approach, morbidity and mortality. Br J Surg 78: 305307,199l. 18. Wennberg L, Miyahara S, and Wilczek HE: Percutaneous core-needle biopsy of renal transplant performed safely without radiographic aid: a prospective trial. Transplant Proc 26: 1769-1770, 1994. 19. Cahen R, Trolliet P, Jean G, Megri K, Dijoud F, and Francois B: Automated renal transplant biopsy with real-time ultrasonic guidance. Transplant Proc 27: 1729-1730, 1995. 20. Wilczek HE: Percutaneous needle biopsy of the renal allograft. Transplantation 50: 790-797, 1990. 21. Beckingham IJ, Nicholson ML, and Bell PRF: Analysis of factors associated with complications following renal transplant needle core biopsy. Br J Urol 73: 13-15, 1994. 22. Dixon TK, Bowman JS, Sago AL, and Jaffers G: A safer renal allograft biopsy. Clin Transplant 5: 126- 128, 1991. 23. Pollak R, Veremis SA, Maddux MS, and Mozes MF: The natural history of and therapy for perirenal fluid collections following renal transplantation. J Urol 140: 716720, 1988.

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