Comparaison entre la biopsie rénale transpéritonéale laparoscopique et la biopsie rénale percutanée guidée par l’imagerie : une étude cas-témoin

25 février 2019

Auteurs : F. Aoun, R. Mansour, C. Chalouhy, J.M. Ruck, S. Albisinni, S. Finianos, H. Azar, D. Chelala, C. Ghorra, T. Roumeguere, M. Moukarzel
Référence : Prog Urol, 2019, 2, 29, 95-100




 




Introduction


Renal biopsy is a well-established diagnostic procedure in patients with underlying medical renal disease [1]. It is mainly indicated in unexplained renal failure, isolated glomerular hematuria, isolated non-nephrotic proteinuria, acute nephritic syndrome, nephrotic syndrome, renal transplant rejection or dysfunction and in some cases of connective tissue diseases [2]. To date, image-guided percutaneous renal biopsy remains the standard approach in all patients without contraindications [3]. The procedure is well tolerated under local anesthesia with minimal post-procedural morbidity. The most common complication following percutaneous renal biopsy is bleeding, while the most worrisome is arteriovenous fistula formation [4]. Percutaneous renal biopsy typically yields an adequate specimen for accurate interpretation in contemporary series, and the diagnostic yield is as high as 80% of cases [5]. However, obtaining a specimen that is sub-optimal or inadequate can result in delays in diagnosis and treatment, increased health-care costs, and additional risks to the patient due to the need for a repeated biopsy procedure.


Absolute contraindications to renal biopsy include uncorrectable bleeding diathesis, chronic anticoagulation therapy, skin infection at biopsy site, uncooperative patient, and uncontrollable severe hypertension [6]. Relative contraindications to the procedure include morbid obesity or patients with anatomic abnormalities such as small kidney, solitary kidney, retro-renal colon, or high localized retroperitoneal kidneys. These patients are best managed by trans-peritoneal laparoscopic approach with direct visualization of the biopsy site and good hemostatic control [7]. The laparoscopic approach can also be preferred in cases where the initial biopsy by image-guided percutaneous approach was inconclusive.


Authors from the John Hopkins Hospital were the first to report their experience with the trans-peritoneal laparoscopic renal biopsy. They demonstrated adequate tissue sampling in 96% of patients with a mean operative time of 123min and a mean estimated blood loss of 67ml [8]. The laparoscopic technique was feasible but serious complications were encountered in initial cases using this approach. As their expertise increased, complication rates and operative duration decreased, as demonstrated recently. Therefore, while the feasibility of the trans-peritoneal laparoscopic renal biopsy has been demonstrated, its efficacy and safety have not been directly compared to those of the standard percutaneous approach. We sought to compare the adequacy of the biopsy material, the diagnostic yield, and the complication rates of the trans-peritoneal laparoscopic approach and the image-guided percutaneous approach to renal biopsy in the diagnosis of native kidney disease.


Patients and methods


Study population


After institutional review board approval, a retrospective chart review of all renal biopsies performed at our center was undertaken between January 2000 and December 2013 (n =806). Age was determined at the time of the biopsy. We excluded patients younger than 16 years old (n =256), biopsies of renal masses (n =41), and renal biopsies of transplanted grafts (n =82). We also excluded patients with incomplete data in their medical records (n =56). Our sample population consisted of 371 adult patients who underwent a native renal biopsy for a medical kidney disease during the study time period.


Renal biopsy procedure


Renal biopsies were performed percutaneously under CT scan guidance in 331 cases and laparoscopically in 40 cases. Percutaneous CT scan-guided biopsies were performed by 3 expert nephrologists under local anesthesia in all cases. Written informed consent, a thorough history, a complete blood count and a coagulation profile were obtained from all patients. The CT scan was performed with the patient prone and landmarks were taken. A 16G or an 18G co-axial-needle were used to obtain one or two biopsy cores from the lower pole that were sent immediately to the histopathology department. We recommended that all patients have bed rest and observation (i.e. pulse and blood pressure monitoring) over the first 24hours following the procedure, and we ensured regular inquiries about pain and hematuria.


All trans-peritoneal laparoscopic renal biopsies were performed in the operating room under general anesthesia by a single expert operator with a large experience with laparoscopic living donor nephrectomy. Trocar insertion and configuration were similar to trans-peritoneal laparoscopic nephrectomy. A surgical specimen was obtained from the lower pole using cold scissors and the defect was closed by suturing the edges of the wound with a multifilament absorbable suture. A drain was inserted for 24hours following the procedure and then removed.


Matching


Patients with a trans-peritoneal laparoscopic renal biopsy were matched 1:3 with patients who underwent percutaneous renal biopsy in the same years. Patients and controls were matched on year of procedure and biopsy indication. Of note, patients and controls were not matched on outcome. To confirm the appropriateness of matching, clinical and pathologic characteristics were compared between patients and controls using the Wilcoxon Rank-sum test for continuous variables and the &khgr; 2 test for categorical variables. Univariate logistic regression was performed to analyze the association between the biopsy approach and risk of complications. Complications were retrospectively collected based on the charts. We performed Wilcoxon Rank-sum or &khgr; 2 test, as appropriate, to test differences in adequacy of biopsy material (i.e. number of glomeruli, continuous) and diagnostic yield (categorical). A specimen was considered adequate if it contained at least ten glomeruli for light microscopy. The diagnostic yield was considered clinically relevant if the information obtained from the specimen helped the nephrologists in their diagnostic work-up. Statistical significance was considered for P <0.05. Analyses were performed using Stata version 11 (College Station, Texas).


Results


Study population


Patients undergoing biopsy via the percutaneous and laparoscopic approaches were of similar age, sex and body mass index (all P >0.05) (Table 1, Table 2). The indications for renal biopsies in each group are summarized in Table 3. The indications for trans-peritoneal approach to renal biopsy rather than a percutaneous renal biopsy were: obesity (n =4), patient intolerance of percutaneous procedure (n =2), severe hypertension (n =3), chronic use of antiplatelet or anticoagulation (n =5), coagulopathy (n =4), inconclusive prior percutaneous biopsy (n =9) and unknown (n =13).


Biopsy results


Laparoscopic biopsy was associated with a higher number of harbored glomeruli (median 50, IQR 20-77) compared to the percutaneous approach (median 10, IQR 7-15), P <0.001. Adequate biopsies containing at least ten glomeruli were obtained in a significantly higher percentage of patients in the laparoscopic group versus the percutaneous group (92.5% vs. 57.1%, P <0.001). The laparoscopic approach was also associated with a significantly higher diagnostic yield than the percutaneous approach (82.5% vs. 63.5%, P =0.027). Patients who underwent laparoscopic biopsy had no perioperative or postoperative complications, resulting in a significantly lower complication rate than percutaneous biopsy (0% vs. 4%, P <0.001), particularly in the need for transfusion for post-procedure bleeding (0% vs. 1.8%, P <0.001). One patient in the percutaneous group developed an arteriovenous fistula, which was well-managed with embolization. No patients in the laparoscopic group developed a fistula. No cases of death were recorded in either group (Table 4).


Discussion


In this single-center retrospective matched pair analysis of percutaneous versus laparoscopic renal biopsy approaches, we found that trans-peritoneal laparoscopic renal biopsy had a significantly higher frequency of adequate sampling and diagnostic yield and a significantly lower frequency of complications, including post-procedure bleeding. An adequate sample of glomeruli (≥10 glomeruli) was obtained in nearly all patients who underwent laparoscopic biopsy, versus only about half of those patients undergoing percutaneous biopsy (92.5% vs. 57.1%, P <0.001). In summary, we found that laparoscopic renal biopsy is a safe and effective method of obtaining renal tissue, with superior diagnostic yield and lower rates of complications than the standard percutaneous approach. However, it is noteworthy to mention that patients who received the laparoscopic approach were contraindicated for percutaneous renal biopsy in our series. Consequently, laparoscopic approach can't be the first choice in all patients due to the more invasive nature of the procedure, the fact that it is performed under general anesthesia and its cost. Our study demonstrated that laparoscopic approach is a safe alternative to percutaneous biopsy when uncorrectable contraindications are present.


The diagnostic yield of 63.5% obtained in percutaneous biopsies in this series is low compared to what was reported in recent studies, where diagnostic yield was reported to be 69-100% [9, 10]. However, those studies include biopsies of renal masses, which likely increased diagnostic yield. Additionally, percutaneous biopsies in this study were performed using an 18-gauge needle, versus the more commonly used 14-gauge needle. The use of the smaller-bore needle is standard at our center and is intended to decrease complication rates. Despite the use of risk-mitigating strategies in percutaneous biopsy at our center, we found that the laparoscopic approach still had significantly lower rates of complications than the percutaneous biopsy approach.


Pneumoperitoneum during and following laparoscopy has been found to have renal side effects. This has primarily been demonstrated in animal models, where prolonged pneumoperitoneum resulted in increased apoptosis of renal tubular cells [11] decreased renal blood flow, oliguria, and impaired creatinine clearance [12, 13, 14]; and increased xanthine oxidase activity and decreased glutathione consistent with renal oxidative stress [15]. However, studies of the effect of pneumoperitoneum on renal function in humans, largely following laparoscopic renal transplantation, have shown no significant detrimental effects [16]. Similarly, we did not observe any renal side effects of pneumoperitoneum; no patients in our study who underwent laparoscopic renal biopsy had any complications.


We acknowledge several limitations to our study. One of the limitations is the single-center retrospective design of the study and the lack of long-term follow-up. However, we anticipated that patients undergoing laparoscopic biopsy would be a higher-risk cohort, as they were contraindicated for percutaneous biopsy. Instead, we found that patients undergoing laparoscopic biopsy had fewer complications, including fewer of the most common (e.g. bleeding) and severe complications (e.g. arteriovenous fistula formation). Additionally, most complications of renal biopsy would have been evident during the follow-up time period available for analysis. Finally, the number of glomeruli required in a sample to consider it an adequate biopsy differs between studies. In this study, we a priori selected 10 glomeruli as the definition of an adequate sample after consultation with pathologists and nephrologists at our center. However, we recognize that the number of glomeruli required for diagnosis varies by disease and the sample; one glomerulus could be sufficient to diagnose crescentic glomerulonephritis, whereas more than 20 glomeruli are required to diagnose focal segmental glomerulonephritis. As a result, we presented both the frequency of adequate glomerular yield and diagnostic yield in this study.


Conclusion


In this retrospective matched-pair analysis, trans-peritoneal laparoscopic renal biopsy was safer and more effective for the diagnosis of medical renal diseases compared to percutaneous renal biopsy. Prospective trials with a good follow-up are needed to define the best candidate for each approach.


Disclosure of interest


The authors declare that they have no competing interest.




Table 1 - Patient characteristics after matching.
  Laparoscopic trans-peritoneal kidney biopsy  Percutaneous kidney biopsy  P -value 
Number of patients  40  120   
Age  43±17  43±16  0.830 
Sex (F/M)  16/24  161/170  0.319 
BMI (mean±SD)  25.2± 24.4±2.6  0.460 





Table 2 - The indications for renal biopsies in each group.
Reason for biopsy  Laparoscopic trans-peritoneal kidney biopsy  Percutaneous kidney biopsy 
Isolated non-nephrotic proteinuria  10  24 
Connective tissue diseases 
Nephrotic syndrome  12  38 
Acute nephritic syndrome  10 
Isolated glomerular hematuria  16 
Unexplained renal failure  25 





Table 3 - The indications to trans-peritoneal approach to renal biopsy.
Reason  Number of patients 
Obesity 
Uncooperative patient 
Severe hypertension 
Chronic use of antiplatelet 
Chronic use of anticoagulation 
Coagulopathy 
Inconclusive prior percutaneous biopsy 
Unknown  13 





Table 4 - Comparison between the two approaches.
  Laparoscopic transperitoneal biopsy  Percutaneous renal biopsy  P -value 
Median number of harbored glomeruli (IQR)  50 (20-77)  10 (7-15)  <0.001 
Adequate biopsies containing at least ten glomeruli  92.5%  57.1%  <0.001 
Diagnostic yield  82.5%  63.5%  0.027 
Perioperative complications  0%  4%  <0.001 
Need for transfusion for post-procedure bleeding  0%  1.8%  <0.001 
Arteriovenous fistula  0%  0.3%  <0.019 




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