J Clin Ultrasound 20:545-552, October 1992 0 1992 by John Wiley & Sons, Inc. CCC 0091-2751/92/080545-08

Complications of Renal Transplantation and the Role of Interventional Radiology Henry C. Irving, FRCR, a n d S. Habib Kashi, FRCS Ed

Abstract: As rejection therapy has improved, the interventional complications of renal transplantation have increased in relative importance as potentially reversible causes of graft malfunction and failure. Ultrasonically guided aspiration and drainage techniques are essential for the characterization and subsequent management of perinephric fluid collections that occur in as many as 51% of cases, of which up to 18% may be clinically significant. In a series of 507 consecutive renal transplants, urological complications were seen in 9%of patients, consisting of ureteric obstruction in 6% and urinary leaks in 3%. Detection via ultrasound scanning, evaluation via antegrade pyelography and pressure-flow tests, and management via percutaneous nephrostomy and ureteric stenting all contribute to rapid diagnosis and subsequent treatment. Serial ultrasound scanning of renal transplants and the aggressive use of interventional radiological techniques are vital to the early detection and management of complications, and can lead to preservation of graft function and continued improvement in graft survival figures. 0 John Wiley & Sons, Inc. Indexing Words: Kidney transplant . Renal transplant complications

In the field of renal transplantation, advances in the management of graft rejection have led to improved graft and patient survival rates. Thus, although surgical complications of renal transplantation remain rare, their relative importance as a group of potentially reversible causes of patient morbidity and mortality has increased significantly. Early diagnosis of surgical complications revolves around close and careful clinical monitoring combined with noninvasive imaging. Ultrasound scanning now has an established role in the detection and management of peri-nephric fluid collections and the urological complications of renal transplantation. Interventional radiological techniques, which are also heavily dependent on ultrasound for puncture guidance, can then be utilized as effective treatment options offering the potential for cure via minimally invasive methods. From the Departments of Radiology and Surgery, St. James’s University Hospital, Leeds, United Kingdom. For reprints contact Dr. H.C. Irving, Department of Radiology, St. James’s University Hospital, Beckett Street, Leeds, LS9 7TF, UK.

PERI-NEPHRIC COLLECTIONS

Serial ultrasound scans in the early postoperative period will detect peri-nephric fluid collections in as many as 51% of cases,’ but the majority of these collections are small, clinically insignificant, and can be safely ignored.2 However, up to 18%of collections are ~ignificantl-~ and will become symptomatic, causing pain, tenderness, and swelling, and may eventually embarrass renal function with decreased urine output and rising serum creatinine. The nature of the fluid within the collection is not usually apparent from the ultrasound scan, although the interfaces caused by the fibrin strands within hematomas and by the clumps of debris and necrotic leukocytes within abscesses give rise to a disorganised internal echo-content. Urine and lymph collections may contain septa but are otherwise echo-free (Figure 1). Ultrasound-guided aspiration is thus essential for characterization of the peri-nephric fluid, and percutaneous external drains can then be inserted if necessary.

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Lymphocoele

Hematoma

Accumulations of lymph may originate from either the host or donor tissues. Careful dissection and meticulous attention to detail is necessary in the preparation of the recipient renal bed, as is the avoidance of too vigorous a dissection of the donor renal hilar structures and ureter. Transection of both host and donor lymphatic vessels can then be kept to a minimum, and the incidence of lymphocoeles will be correspondingly low. A recent review of 13 publications revealed an overall incidence of lymphocoeles of 4.1%, but there was a range from as low as 0.5% t o as high as 20%. Lymphocoeles are seen on ultrasound as echofree collections with internal septa; they may occur at any site in relation to the transplanted kidney and ureter. Aspiration will produce clear amber fluid that is macroscopically indistinguishable from urine, but on biochemical analysis the fluid is seen to be high in protein content with creatinine and electrolyte levels similar to those in the serum. Simple aspiration may be adequate in up to a third of c a s q 4 but reaccumulation is often rapid. External catheter drainage increases the chances of successful treatment,5’6and percutaneous sclerotherapy via the instillation of povidone-iodine has been de~ c r i b e d . ~However, ” drainage needs to be long term, and the risks of secondary infection in an immunosuppressed patient are such that most surgeons currently opt for internal marsupialization of the lymphocoele.

Small hematomas are common in the postoperative period, rarely give rise to problems, and usually resolve spontaneously. Occasionally it becomes important to exclude secondary infection; this is accomplished by diagnostic aspiration. Both subcapsular and extracapsular hematomas may develop after percutaneous renal biopsy, but the incidence of this complication may be minimized by accurate ultrasound guidanceg and the use of smaller gauge (18G) needles in a springloaded biopsy device.”

Abscess Infected peri-renal collections may be insidious: their clinical effects being masked by the immunosuppressive therapy, the fever and raised white-cell count being erroneously attributed to rejection. It is, therefore, imperative that fluid collections be further investigated whenever renal function or patient well-being are less than optimal. Ultrasound-guided aspiration can be performed using fine (22G) needles, although, if the fluid is thick and viscous, larger (18G) needles may be required. Samples are sent for microscopy, culture, and determination of antibiotic sensitivity. Most abscesses can be drained via percutaneous insertion of 8F catheters, although larger bore (12F or 14F) catheters may be required occasionally. Successful resolution of peritransplant abscesses is usually accomplished by a combination of such percutaneous drainage with appropriate antibiotic therapy.

Urinoma Accumulations of urine may occur due to leaks from the surgical anastomosis, or from ischemic necrosis of the ureter or intra-renal collecting system. Diagnostic aspiration is needed because the ultrasound appearance of echo-free fluid collections with or without internal septations is nonspecific, and the increased concentration of urea and creatinine over that in serum is the clue to the true nature of the fluid. Although external drainage via percutaneous catheter insertion may serve either to control any urinary fistula or to achieve decompression of a collection that is causing problems by mass effects, the definitive treatment is restoration of the continuity of the urinary tract and depends upon the exact site and cause of the leak (see below and Figure 5 ) .

UROLOGICAL COMPLICATIONS

Urological complications of renal transplantation comprise urinary leaks and ureteric obstruction and represent the most important subgroup of nonvascular problems. These complications must be diagnosed early and differentiated from rejection, for delays in accurate diagnosis and inappropriate antirejection therapy may result in loss of the transplanted kidney as well as increased patient morbidity and mortality. At our institution, analysis of a series of 507 consecutive renal transplants, carried out in a 6 year period since the introduction of cyclosporin A as an immunosuppressive agent, revealed urological complications in 45 patients (9%),consisting of ureteric obstruction in 30 (6%) and urinary leaks in 15 (3%).” These results compare favorably with those from other large series from the pre-cyclosporin and help to dispel speculation that this drug might be implicated in JOURNAL OF CLINICAL ULTRASOUND

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FIGURE 1. Peri-renal fluid collections. (A) Hematoma (between cursors) with echoes within the fluid posterior to the kidney. (B) Lymphocoele with internal septations extending up into the right iliac fossa.

the increased incidence of ureteric stenosis seen at certain centers.14

Obstruction The key to the early diagnosis of ureteric obstruction is serial ultrasound scanning. The use of ultrasound for the detection of collecting system dilatation has long been e~tablished'~ (Figure 21, but the significance of this finding in the early postoperative period has been subject to some uncertainty. In a recent study16 we evaluated varying deVOL. 20, NO. 8, OCTOBER 1992

grees of pelvicalyceal dilatation in the presence of good or poor renal function and estimated the long-term sequelae of early collecting system dilatation. In the absence of ultrasonically detected pelvicalyceal dilatation and in the presence of good or improving renal function, the chances of obstruction were nil. Furthermore, even in the presence of poor or deteriorating renal function, a normal ultrasound scan provides a sensitivity of 93% and specificity of 99%, because only one patient of 135 was ultimately shown to be obstructed on subsequent investigations.

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FIGURE 2. Collecting system dilatation. (A) Longitudinal scan. (B) Transverse scan.

Dilatation of the collecting system may occur in the absence of obstruction, which was present in only 9.5% of cases with mild dilatation, but in 65% of those with moderate to severe dilatation. While the cause of the dilatation in the nonobstructed cases is not known, possibilities include preexisting dilatation in the donor system or dilatation due to a resolving rejection process. Most grafts with mechanical obstruction of the ureter can be rescued by appropriate management. In a group of 135 consecutive renal transplants, we showed16 that the 14 grafts with ureteric obstruction had a similar 2-year graft survival rate to the nonobstructed grafts. How-

ever, the renal function at 2 years was significantly impaired with a median serum creatinine of 178 pmol/L in those that had been obstructed compared with 132 pmol/L in those without obstruction. This irrevocable loss of renal function was despite an aggressive approach using both surgery and interventional radiology, and serves to emphasize the importance of early diagnosis and rapid relief of obstruction. Obstruction is suspected clinically when there is tenderness over the kidney and there is elevation of serum creatinine and/or decreasing urine output. An ultrasound scan is performed and, if dilatation of the collecting system has developed or increased in severity since the baseline or previJOURNAL OF CLINICAL ULTRASOUND

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but antibiotic cover is advisable to minimize the hazards of inducing a bacteremia if the punctured system contains infected urine. Percutaneous nephrostomy. When obstruction is suspected from the antegrade pyelogram, a percutaneous nephrostomy should be performed to relieve the obstruction, restore renal function, and gain time during which the options for the most appropriate form of therapy can be discussed by the surgeon and radiologist. The collecting system is punctured using an 18G sheathed needle under either ultrasound or fluoroscopic guidance, or using a combination of both. As with native kidneys, a posterior calyx should preferably be punctured via a lateral approach, maximizing the thickness of renal parenchyma traversed and facilitating the passage of guide-wires and catheters into the renal pelvis FIGURE 3. Antegrade pyelogram during pressureiflow study. Two fine needles (22G)have been introduced into the pelvicalyceal sysand upper ~ r e t e r . ’ ~ , ~ ~ tem under untrasound guidance. The narrowing at the lower end of When the collecting system has been puncthe ureter was shown to be functionally insignificant. tured, a guide-wire can be passed through the sheath-a stiff bodied wire with a fixed J-tip is ous scan, antegrade pyelography should be perfavored because straight-tipped wires might formed. damage or puncture the delicate uroepithelium. Antegrade pyelography. Under ultrasound The track is then dilated and a pigtail nephguidance, a 22G needle is passed through the rerostomy catheter (6F or 8F) passed over the wire nal parenchyma to enter the collecting system. A into the renal pelvis; free drainage of urine via point of entry as lateral as possible should be sethe nephrostomy catheter is thus established lected to ensure a retroperitoneal needle track. A (Figure 4). Renal function recovers rapidly; in a transperitoneal approach is considerably more series of 2 1 consecutive renal transplants with painful for the patient and runs the risk of inureteric obstruction,” median serum creatinine traperitoneal leakage. fell from 485 pmol/L to 396 pmol/L at 48 hours, When the needle tip is within the collecting and to 229 pmol/L at 2 weeks postintervention. system, urine can be aspirated and contrast meFurther management of these patients dedium infused (Figure 3). Antegrade pyelograms pends upon the exact cause of the obstruction. provide anatomical information and also permit Early postoperative obstruction may be due to an assessment of the rate of flow of contrast down edema at the uretero-vesicostomy and may rethe ureter into the bladder. The presence or absolve spontaneously after a few days of external sence of partial or complete ureteric obstruction is drainage. In these patients, repeat nephrostousually obvious, but the addition of pressure-flow grams to confirm the patency of the urinary tract studies (Whittaker test) provides a more objecare followed by a period of “catheter clamping” tive assessment of impedance to urine flow. before eventual withdrawal of the catheter. If Pressure-flow studies. The pressure within the obstruction at the uretero-vesicostomy perthe collecting system is measured by connecting sists, insertion of a double pigtail ureteric stent, the 22G needle to a pressure transducer, and diwith or without balloon dilatation of the striclute contrast medium is then infused at a conture, is the treatment of choice. Balloon dilatastant rate (10 mL/min) for 5 minutes through a tion using high pressure angioplasty balloons second 22G needle (Figures 3 and 4).Intravesical 4mm t o 6mm in diameter is performed when pressure must be maintained at zero by inserting there has been any difficulty in passing an 8F catheter through the stricture. This should ala catheter into the bladder. The resting pressure ways be followed by denting. Stents are left in within the collecting system and its response to the infusion can then be recorded- increasing place for at least 3 months and up to 6 months, the specificity of the diagnosis of ob~truction.’~ when close monitoring of both serum creatinine Fine-needle puncture of the renal transplant is a levels and the ultrasound appearance are mandatory to detect whether the ureteric structure remarkably safe procedure” especially when recurs. performed under direct ultrasound visualization, VOL. 20, NO. 8, OCTOBER 1992

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FIGURE 4. Functionally significant narrowing of the distal ureter. (A) Placement of nephrostomy catheter through lower pole calyx. (B) A catheter has been passed down the ureter and into the bladder to permit internal drainage while preserving external access t o the system.

Other causes of ureteric obstruction that may be managed percutaneously include obstruction due to stone when percutaneous ureterolithotomy can be performed,21postsurgical obstruction at a pyelo-ureterostomy, and compression of the ureter by a fluid collection, with success rates for percutaneous therapy alone of more than 70%.'',23 However, not all causes of obstruction are amenable to interventional radiology, and long ureteric strictures due to ischemia, obstruction due to tumors, such as immunosuppression-induced lymphoma, and recurrent uretero-vesicostomy strictures are likely to necessitate a surgical approach.

Urinary Leakage In our series of 507 consecutive renal transplants performed between the years 1984 and 1990, there were 15 patients with urinary leaks, 9 of whom were found to have developed uretric necrosis; the other 6 leaks could be traced to the cystotomy, (4),and to pyeloureterostomy (1) and ureteroureterostomy (1)closures." Indications of urinary leak include low urine output, a rise in serum creatinine, detection of a peri-renal fluid collection, or a leak from the wound. A micturating cystogram may demonstrate a leak from the bladder at the site of cystotomy when treatment is by continuing drainage via the urethral catheter, with surgical repair if the leak fails to resolve. If a leak at the ureteroneocystostomy is demonstrated, or if no

leak is detected at cystography, an antegrade pyelogram is performed. Needle puncture of a nondilated collecting system is not easy, but using ultrasound guidance it can usually be accomplished by a radiologist experienced in such manoeuvers. If antegrade pyelography confirms a leak, a percutaneous nephrostomy catheter is inserted. A subsequent nephrostogram will show whether there is total ureterovesical discontinuity, in which case surgical repair is indicated, or whether some communication exists. In the latter case, an attempt can be made to pass a guidewire into the bladder so that antegrade stent insertion can be performed (Figure 5 ) . Using the above guidelines, of our 9 cases of lower ureteric or vesico-ureteric junction urinary leak, 5 underwent surgical repair, 2 cases resolved on continued bladder drainage, and 2 transplants were successfully managed with the placement of double pigtail stents across the site of leakage (Figure 5). In the 6 patients with other sources of urinary leakage, 3 cases of cystotomy leakage resolved on urethral catheter drainage and 2 went for surgical repair. The uretero-ureterostomy was converted to pyeloureterostomy which again leaked and was then successfully managed by a period of nephrostomy catheter drainage. Two kidneys from the 15 patients with urinary leaks were lost due to overwhelming sepsis. Other groups report similar res u l t ~ , but ~ ~all - ~the ~ series are relatively small and each case should be managed on its merits by the surgeon and radiologist working together JOURNAL OF CLINICAL ULTRASOUND

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FIGURE 5. (A) An antegrade pyelogram reveals a nondilated collecting system with a leak at the ureterocystostomy leading t o a fluid collection that has been drained via percutaneous insertion of a pigtail catheter. ( 6 )A catheter has been passed down the ureter into the bladder, and the leaking anastomosis has thus been stented. (C) Following a period of stenting via the external-internal catheter, the leak had diminished and a double pigtail catheter was inserted. The leak completely healed, and the stent was removed after 3 months.

to determine the least invasive and most effective line of management.

DISCUSSION

The cause of ureteric stenosis or necrosis remains open to speculation, although vascular insufficiency seems highly likely. The blood supply to the terminal ureter in renal allografts is clearly vulnerable to surgical trauma as it is entirely derived from the main renal artery, but vasculitis due to preservation injury, rejection, or even cyclosporin toxicity have all been suggested as alternative pathogenic mechanisms. Analysis of the data in our series" failed to indicate any association between ureteric stricture or leak with an increased number of rejection episodes, with patients having produced cytotoxic antibodies, or with the degree of matching on the HLA loci. The incidence of these complications VOL. 20. NO. 8, OCTOBER 1992

showed no increase in the era since the introduction of cyclosporin. But the group with ureteric complications, had a significant increase in the incidence of delayed primary function suggesting that damage during organ harvesting or the preservation period were causative factors.

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CONCLUSION

An active policy of investigation using serial ultrasound scans is an essential prerequisite to the early detection of complications of renal transplantation. Such complications must be managed aggressively with a minimum of delay if graft function is to be preserved. Antegrade pyelography , pressure flow tests, percutaneous nephrostomy, and antegrade insertion of ureteric stents are all dependent upon ultrasound-guided puncture procedures, and offer minimally invasive methods for effective evaluation and treatment of the problems of peri-renal collections, ureteric obstruction, and urinary leakage. Successful use of these techniques depends upon close cooperation with the transplant surgeon, and, as in so many areas of modern radiology, a team approach is vital. REFERENCES 1. Silver TM, Campbell D, Wicks JD, et al: Peritransplant fluid collections. Radiology 138:145151,1981. 2. Pollak R, Vermis SA, Maddux MS, et al: The natural history of and therapy for perirenal fluid collections following renal transplant. J Urol 140:716-720,1988. 3. Kumar R, Silson DD, Santa-Cruz FR: Postoperative urological complications of renal transplant. Radiographics 4:531-547, 1984. 4. Smith TP, Cragg AH: Nonvascular interventional radiologic procedures after renal transplantation, in Letourneau JG, Daty DL, Ascher NL (eds): Radiology of Organ Transplantation, St. Louis, Mosby Year Book, 1991. 5. Cohan RH, Saeed M, Sussman SK, et al: Percutaneous drainage of pelvic lymphatic fluid collections in the renal transplant patient. Invest Radiol 22:864-867, 1987. 6. White M, Mueller PR, Ferucci JT, et al: Percutaneous drainage of postoperative abdominal and pelvic lymphocoeles. A J R 151507-510, 1985. 7. Burgos FJ, Teruel JL, Mayayo T, et al: Diagnosis and management of lymphocoeles after renal transplantation. Br J Urol61:289-293, 1988. 8. Gilliland JD, Spies JB, Brown SB, et al: Lymphocoeles: Percutaneous treatment with povidoneiodine sclerosis. Radiology 171:227-229, 1989. 9. Ubhi CS, Irving HC, Guillou, et al: A new technique for renal allograft biopsy. Br J Radiol 60~599-600, 1987.

10. Worth DP, Khanna SK, Ubhi CS, et al: The Biopty cut procedure for renal biopsies. Br Med J 296:1603, 1988. 11. Kashi SH, Lodge JPA, Giles GR, et al: Urological complications of renal transplantation: role of aggressive management. Br J Urol, in press, 12. Munday AR, Podesta ML, Bewick M, et al: The urological complications of 1000 renal transplants. B r J Urol 53:397-402, 1981. 13. Loughlin KR, Tilney NL, Richie JP: Urological complications in 718 renal transplant patients. Surgery 95:297-302, 1984. 14. Rigg KM, Lennard TWJ, Proud G, et al: Urological complications following renal transplantation. Paper presented to British Transplantation Society, Cambridge, 1991. 15. Bartrum FLJ J r , Smith EH, D’Orsi CJ, et al: Evaluation of renal transplants with ultrasound. Radiology 118:405, 1976. 16. Kashi SH, Lodge JPA, Giles GR, et al: Ultrasonography of renal allografts: Collecting system dilatation and its clinical significance. Nephrol Dial Transplant 6:358-362, 1991. 17. Kashi SH, Giles GR, Irving HC: Pressure-flow studies in the evaluation of ureteric obstruction in renal allografts. Paper presented to British Transplantation Society, October 1991. 18. Lieberman RP, Crummy AB, Glass NR, et al: Fine needle antegrade pyelography in the renal transplant. J Urol 126:155-158, 1982. 19. Pfister RC, Newhouse JH: Interventional percutaneous pyeloureteral techniques: 11. Percutaneous nephrostomy and other techniques. Radiol Clin North A m 17:351-363, 1979. 20. Irving HC, Arthur RJ, Thomas DFM: Percutaneous nephrostomy in paediatrics. Clin Radiol 38:245-249, 1987. 21. Gedroyc WMW, MacIver D, Joyce MRL, et al: Percutaneous stone and stent removal from renal transplants. Clin Radiol 40:174- 177, 1989. 22. Bennett LN, Voegeli DR, Crummy AB, et al: Urologic complications following renal transplantation: Role of interventional radiologic procedures. Radiology 160:531-536, 1986. 23. Lieberman RP, Glass NR, Crummy AB, et al: Nonoperative percutaneous management of urinary fistulas and strictures in renal transplantation. Surg Gynecol Obstet 155:l-6, 1982. 24. Smith TP, Hunter DW, Letorneau JG, et al: Urine leaks after renal transplantation: Value of percutaneous pyelography and drainage for diagnosis and treatment. AJR 151:511-513, 1988.

JOURNAL OF CLINICAL ULTRASOUND

Complications of renal transplantation and the role of interventional radiology.

As rejection therapy has improved, the interventional complications of renal transplantation have increased in relative importance as potentially reve...
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