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Vascular and Interventional Radiology |
1 From the Diagnostic and Interventional Polyvalent Radiology Service (P.C., M.F.B., Y.M., O.L., P.A.G.) and the Nephrology Service (F.M., G.D.), Université Pierre et Marie Curie, Hôpital Pitié-Salpêtrière, 43-87 boulevard de l'Hôpital, 75651 Paris cedex 13, France; Unité Institut National de la Santé et de la Recherche Médicale (INSERM) 423, Paris, France (H.B., C.J.); and Unité INSERM 494, Paris, France (P.A.G.). Received May 7, 1999; revision requested July 16; revision received August 31; accepted September 24. Address correspondence to P.C. (e-mail: philippe .cluzel@psl.ap-hop-paris.fr).
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Abstract |
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MATERIALS AND METHODS: Results and complications of 400 consecutive transjugular renal biopsies performed between 1993 and 1998 with a modified Colapinto transjugular hepatic biopsy system were compared retrospectively with those of 400 percutaneous renal biopsies performed during the same period. Transjugular renal biopsy was associated with 14 cardiac and 35 hepatic biopsies. Number of glomeruli per tissue core, adequacy of tissue core for histopathologic diagnosis, and rate and severity of complications were analyzed.
RESULTS: Renal tissue was obtained with percutaneous renal biopsy in 382 (95.5%) of 400 patients and with transjugular renal biopsy in 383 (95.8%) of 400 patients. The mean numbers of intact glomeruli per tissue core with optical microscopy were 11.2 ± 7.7 (SD) and 9.8 ± 7.6 for percutaneous renal biopsy and transjugular renal biopsy, respectively. With immunofluorescent microscopy, the mean numbers were 6.4 ± 5.3 and 4.6 ± 4.6 for percutaneous renal biopsy and transjugular renal biopsy, respectively. Tissue cores were adequate for histopathologic diagnosis in 98.2% with both techniques. Major complications occurred with transjugular renal biopsy in four patients and with percutaneous renal biopsy in three patients.
CONCLUSION: Use of transjugular renal biopsy provides diagnostic yield and safety similar to those of percutaneous renal biopsy and allows multiorgan biopsy during the same procedure. It can be recommended in patients with percutaneous renal biopsy contraindication or failure.
Index terms: Biopsies, complications, 81.458 • Biopsies, technology, 81.1261 • Kidney, biopsy, 81.1261, 81.458
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Introduction |
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To obtain renal tissue samples in such patients, the transjugular hepatic biopsy technique was modified and described (11). However, to our knowledge this technique has gained little acceptance; the only large series we know of, comprising 200 patients, came from the same institution as the modified transjugular hepatic biopsy technique (12). A few reports (13,14) also were published and describe the results of transjugular renal biopsy, and some limitations, which include the absence of a right kidney, that prevent its use have been emphasized (12).
The purpose of this study was to compare the effectiveness and safety of transjugular renal biopsy with those of percutaneous renal biopsy for the diagnosis of renal parenchymal disease.
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MATERIALS AND METHODS |
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In the transjugular renal biopsy group, the 273 male and 127 female patients ranged in age from 17 to 80 years (mean, 42 years). The transjugular route was chosen in 303 patients (75.8%) because of bleeding disorders. Bleeding disorders included bleeding time longer than 8 minutes (Ivy bleeding time test), treatment with antiplatelet drugs or anticoagulants, spontaneous prothrombin activity of less than 70%, or a platelet count of less than 80,000/mm3 (80 x 109/L).
Transjugular renal biopsy was performed in 30 patients for one of the following associated morbid conditions: uncontrolled hypertension (n = 14 [3.5%]), morbid obesity (n = 5 [1.3%]), or single kidney (n = 11 [2.8%]).
Last, transjugular renal biopsy was chosen when patients were undergoing biopsy of multiple organs (heart and kidney, n = 14 [3.5%]; liver and kidney, n = 35 [8.8%]) or when the percutaneous renal biopsy approach failed (n = 18 [4.5%]). Twenty-eight patients with hepatic disease also had abnormal clotting parameters.
Procedures
Percutaneous renal biopsy.—Percutaneous renal biopsy was performed by two nephrologists (F.M., G.D.) by using a blinded technique at the patient's bedside after US and CT localization of the kidney. An automated spring-loaded device with a 16-gauge needle (Bard Biopsy Gun; Bard Urologic, Covington, Ga) was used in all patients. A trained pathology technician (C.J.) was present and recorded whether any tissue had been obtained during each pass and, when tissue was present, how many glomeruli it contained (to limit the number of passes, which never exceeded eight). When this blinded approach failed, renal biopsy was rescheduled and performed by using real-time US or CT guidance. Results of percutaneous biopsy performed blinded or under US or CT guidance were used for comparison (blinded [n = 360], under US [n = 33], or under CT [n = 7]).
All patients were kept under close observation with bed rest for at least 24 hours after all procedures. Color Doppler US images in the kidneys in which biopsy was performed were obtained when abnormalities in clinical or hemodynamic status or in diuresis were observed. Patients with no signs of complication and with no reason to prolong hospitalization were discharged the following day.
Transjugular renal biopsy.—All procedures were performed in the angiography suite. The patient was placed in the supine position, with his or her head turned away slightly from the side of puncture. The skin was cleaned with an iodine solution (Betadine; Asta Medica, Merignac, France), and the patient was covered with a surgical drape. All biopsies were performed by two interventional radiologists (P.C., Y.M.) by using the same technique.
Local anesthetic, 5–10 mL of 2% lidocaine hydrochloride (Xylocaine; Astra France, Rueil Malmaison, France), was administered subcutaneously, but no sedative was administered. After a Valsalva maneuver, the internal jugular vein was punctured with an 18-gauge needle (Critikon, Chatenay-Malabry, France), with an anterior approach above the thyroid cartilage, on the inside of the sternal head of the sternocleidomastoid muscle. A 9-F venous sheath (Plastired; St Lieu-La-Foret, France) was inserted over a short 0.035-inch guide wire into the vein. The number of passes for jugular venous puncture and the occurrence of arterial puncture were not recorded. The catheter, filled with a nonionic contrast medium (iohexol [Omnipaque 240; Nycomed, Paris, France]) and attached to a 10-mL syringe (Becton Dickinson, Franklin Lakes, NJ), was advanced into the inferior vena cava under fluoroscopic control. Renal venograms were obtained to choose the best-suited vein. Whenever the navigation was painful, the patient was asked to breathe slowly and shallowly. Renal veins are relatively fragile, and progression in the renal vein should be kept as atraumatic as possible. If the vein was too horizontal or was ascending slightly, a deep inspiration or a guide wire was useful. We preferred to use a curved 0.035-inch Glidewire (Terumo, Tokyo, Japan) rather than a Teflon-coated, metallic guide wire.
The catheter then was advanced into the right renal vein and was advanced gently as distally as possible into a peripheral cortical vein of the lower pole of the kidney. Its position was checked by flushing it with a small amount of contrast medium. The position was judged to be satisfactory when a wedge of cortical parenchyma was enhanced (Fig 2). Then the patient was asked to breathe shallowly and slowly, and the transjugular renal biopsy needle, filled with normal saline solution (Fresenius France Pharma, Louviers, France) and attached to a 20-mL syringe (Becton Dickinson), was advanced down the catheter. The biopsy sample was obtained by using the Menghini "1-second" technique during apnea (15): The needle was plunged into the renal parenchyma and removed in one continuous motion while suction was maintained with the 20-mL syringe. A second pass was possible without retrieving the needle after checking the position of the catheter, which could have advanced over the needle during the first pass. If the catheter had advanced over the needle, the catheter was pulled back a few millimeters, and the orientation of the needle was changed to minimize the risk of perforation. The renal tissue sample, which usually was retained in the syringe, was then expelled onto a sterile compress.
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In eight patients, transjugular renal biopsy was performed with an 18-gauge, 60-cm-long automated biopsy device (Quick-Core; Cook, Bloomington, Ind) that was introduced coaxially through a 90-cm-long, 6-F guide catheter (MP A1, VistaBrite Tip; Cordis, Miami, Fla) cut to 58 cm.
Complications
Complications were considered to be major if embolization, surgery, or blood transfusion was required or if they caused clinical sequelae and minor if minimal or no treatment was required. For transjugular renal biopsy, complications were divided into those associated with jugular venous puncture and those associated with renal biopsy.
Histopathologic Examination
For both approaches, the goal was to obtain two renal samples. The first core was fixed in Bouin fixative for optical microscopy, and the second was frozen for immunofluorescent microscopy. An experienced pathologist (H.B.) evaluated all biopsy specimens. All 800 renal biopsy pathology reports that focused on the adequacy of tissue recovery and on the number of intact glomeruli per tissue core were reviewed (P.C., F.M., and H.B.). The tissue core was considered adequate when sufficient numbers of intact glomeruli to obtain a precise pathologic diagnosis were present.
Statistical Analyses
Means were compared by using the Student t test or by using analysis of variance. Percentage values were compared with the 
2 test. When small numbers invalidated the 2 approximation, the Fisher exact test was used. When SDs were unequal, the nonparametric Mann-Whitney test was applied. P values of less than .05 were considered to indicate a significant difference.
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RESULTS |
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Transjugular renal biopsy.—Venous access was obtained in all patients, with right internal jugular venous access in all but nine patients. The right external jugular vein was punctured in two patients and the left internal jugular vein was punctured in seven patients to perform biopsy in the right kidney. In these latter patients, the progression of the needle through the catheter across the mediastinum sometimes required the use of a metallic guide wire to traverse the course of the left brachiocephalic vein.
Biopsy was feasible in 397 of 400 patients (99.3%) but could not be performed successfully in the remaining three because of anatomic anomalies or because of associated morbid conditions. Two of these latter patients had recurrent courses of both renal veins that precluded the advancement of the rigid modified Colapinto needle, despite the use of deep breathing in the patient and a stiff guide wire. The third patient's renal veins had achieved thrombosis, which prevented the passage of the catheter.
In 13 patients, biopsy was performed without difficulty in the left kidney for one of the following reasons: Only the left kidney was available (n = 5), or there was smoother access to the left than to the right kidney (n = 8) (Fig 3).
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Histopathologic Diagnoses
Percutaneous renal biopsy.—Renal tissue was obtained in 382 (95.5%) of 400 patients. The mean numbers of intact glomeruli per tissue core at optical and immunofluorescent microscopy were 11.2 ± 7.7 (SD) (range, 0–48 glomeruli) and 6.4 ± 5.3 (range, 0–40 glomeruli), respectively. Tissue cores were considered adequate for histopathologic diagnosis in 375 (98.2%) of these 382 patients.
Transjugular renal biopsy.—Renal tissue was obtained in 383 (95.8%) of 400 patients. The mean numbers of intact glomeruli per tissue core at optical and immunofluorescent microscopy were 9.8 ± 7.6 (range, 0–40 glomeruli) and 4.6 ± 4.6 (range, 0–35 glomeruli), respectively. Tissue cores were considered adequate for histopathologic diagnosis in 376 (98.2%) of 383 patients.
The mean numbers of glomeruli obtained with each technique did not differ significantly (P = .361). The mean numbers of glomeruli at immunofluorescent microscopy were significantly different (P < .001). Both groups included a few patients whose histopathologic diagnoses could be made despite suboptimal specimens. Histopathologic diagnoses based on findings in samples obtained with either approach are reported in the Table.
Complications
Four patients (1.00%) in the transjugular renal biopsy group and three patients (0.75%) in the percutaneous renal biopsy group experienced major complications.
Percutaneous renal biopsy.—Three major complications related to renal biopsy occurred in patients with no underlying disease: Two renal arteriovenous fistulas occurred, with abundant and prolonged hematuria, that were embolized successfully with microcoils, and an inadvertent puncture of the spleen occurred that required emergency splenectomy. Four minor complications occurred: a large perirenal hematoma prolonging the hospital stay, an inadvertent puncture of the spleen, and two inadvertent hepatic biopsies.
Transjugular renal biopsy.—Jugular venous puncture was associated with a major complication in a 50-year-old obese man with multiple myeloma: thrombocytopenia (platelet count, 40,000/mm3) that necessitated a blood transfusion. One minor hematoma around the puncture site also was recorded in a 55-year-old woman with multiple myeloma, acute renal insufficiency, and thrombocytopenia (platelet count, 36,000/mm3).
Biopsy itself was associated with three major complications (large perirenal hematomas), two of them in patients with mixed cryoglobulinemia. Two hematomas were embolized successfully with microcoils and without substantial loss of renal parenchyma; the third was in a patient in whom blood transfusion was required. Minor complications also occurred; no treatment was required for a large perirenal hematoma, and several episodes of minor hematuria not necessitating treatment were recorded.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Tissue yields and complications of percutaneous renal biopsy with a biopsy gun have been reported (1,6–8,16–20). Tissue recovery and major complication rates ranged from 92% to 100% and from 0% to 4%, respectively, in studies in which the 14-gauge, automated biopsy needle was evaluated (7,17,19,21–23). These rates improved slightly when an 18-gauge needle was used and ranged from 93% to 100% and from 0% to 3.5% (1,6,8,16,18,23,24). Our control group of 400 patients in whom percutaneous renal biopsy was performed (360 with a blinded technique and 40 with direct US or CT guidance) compared favorably with the control groups in these series. Although we observed no statistically significant differences between the complication rates that resulted from the two methods, it can be argued that the complication rate in the percutaneous renal biopsy group could have been lowered further with US guidance (7,10,21,22,25) and that splenic puncture could have been avoided.
The transjugular renal biopsy technique was described in 1990 by Mal et al (11) in patients with contraindications or with other anomalies precluding percutaneous renal biopsy. This meritorious technique has, surprisingly, been exploited poorly (12–14); perhaps this is because the technical aspects have been described inadequately. Unlike transjugular hepatic biopsy, in which tissue is obtained with the catheter in a free position—not blocked in the parenchyma—within the hepatic vein, renal biopsy requires that the device be wedged as far as possible into the peripheral renal vein to obtain contrast medium enhancement of a wedge of cortical parenchyma before puncture. In such a position, there is little likelihood of damaging a large central vein or artery.
Moreover, more glomeruli were obtained per pass when parenchymal enhancement was obtained. This observation was similar to that reported by Marchetto et al (26), who obtained better specimens after unintentional capsular perforation. Indeed, capsular perforation is not uncommon with this technique and can be detected with the leakage of a small amount of contrast medium into the perirenal space but without causing complications other than those reported.
No attempt at track embolization was made or was required in this study. Two of the three large perirenal hematomas occurred in patients with cryoglobulinemia. In accordance with these results, we think that multiple causes of bleeding disorders (hematocrit level < 30%, anemia, renal insufficiency, low platelet count, monoclonal components, cryoglobulinemia, etc) increase the risk of the procedure; thus, the number of passes should be limited in patients with these disorders. Indeed, it must be emphasized that the complications reported did not occur early in our experience with transjugular renal biopsy. Of course, the close monitoring of patients for 24 hours after the procedure and the possibility of rapid embolization increase the safety of the procedure.
The evaluation of a new technique of transfemoral renal biopsy with a flexible forceps in high-risk patients was reported recently by Bilbao et al (27). In their study, samples adequate for diagnosis were obtained from 13 (81%) of the 16 patients, and the mean number of glomeruli per procedure was 12.6 (range, 0–39 glomeruli). No major complications were reported. The importance of selecting a peripheral subcortical renal vein to obtain adequate samples of cortical parenchyma that contain sufficient numbers of glomeruli also was emphasized.
Two patients could not undergo biopsy because of the recurrent courses of both renal veins that precluded the advancement of the rigid Colapinto needle, despite the use of deep breathing and a stiff guide wire. In theory, congenital anomaly of the left renal vein also could preclude left renal biopsy. Trigaux et al (28) found 38 (3.7%) retrocaval renal veins in a series of 1,014 patients with contrast material-enhanced spiral CT scans. The transfemoral approach reported by Bilbao et al (27), in which a 7-F, 100-cm-long biopsy forceps was used, could be recommended in both situations. We performed biopsy in the left kidney without difficulty in 13 instances. Thus, in our experience, the absence of a right kidney can no longer be considered a limitation for the transjugular route.
To the best of our knowledge, use of the 18-gauge automated biopsy device has never been reported for renal biopsy in humans. Marchetto et al (26) envisioned its use and reported its efficacy in an ex vivo swine kidney model. However, in our opinion, the 14-gauge, thin-walled, stainless steel stiffening cannula that protects the guide catheter from perforation by the sharp biopsy needle is too rigid to perform renal biopsy anywhere other than in the lower pole of the right kidney. It also precludes a left jugular approach, in contrast with the Colapinto needle, which is flexible; this explains why we used a flexible-arm guide catheter to perform biopsy with the 18-gauge automated biopsy device. One major advantage of this system was its thinness, which allowed the catheter to be placed deeper inside the renal parenchyma. Indeed, with the Colapinto needle, we sometimes encountered valves in the renal veins or encountered vessels of small diameter that prevented the rapid good positioning of the catheter.
The paucity of major complications from the puncture of the jugular vein in the 303 patients (75.8%) with bleeding disorders demonstrates the safety of the anterior approach to the jugular vein far away from the pleural dome, mediastinum, and major collateral vessels of the subclavian artery. Investigators in numerous studies have emphasized the superiority of US-guided cannulation of the internal jugular vein over blinded techniques. However, US is reserved for only when the puncture site is 1–2 cm above the clavicle for long-term venous access—for example, in high-risk patients—to avoid pneumothorax or mediastinal hematoma.
Finally, in terms of cost-effectiveness, one should note that, in our institution, percutaneous renal biopsy with a blinded technique or with US guidance costs $93, while transjugular renal biopsy costs $167. Percutaneous renal biopsy with CT guidance costs $217.
In conclusion, transjugular renal biopsy with the modified Colapinto needle can be used to obtain an adequate tissue sample for the specific histopathologic diagnosis of renal dysfunction at a rate comparable to that with percutaneous renal biopsy. However, transjugular renal biopsy usually is performed in high-risk patients in whom percutaneous renal biopsy is not feasible or is contraindicated. In accordance with our results, transjugular renal biopsy can be chosen when multiorgan biopsy is indicated or when a patient with an emergency cannot wait for the biologic effects of an antivitamin K or antiplatelet drugs to disappear.
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Acknowledgments |
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Footnotes |
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References |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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