Light chain crystalline kidney disease: diagnostic urine microscopy as the liquid kidney biopsy
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1 Clinical Nephrology, Vol. No. /2014 (1-5) Neph Education 2014 Dustri-Verlag Dr. K. Feistle ISSN DOI /CN e-pub: month day, year Light chain crystalline kidney disease: diagnostic urine microscopy as the liquid kidney biopsy Randy L. Luciano 1, Ekaterina Castano 2, Giovanni B. Fogazzi 3, and Mark A. Perazella 1 1 Section of Nephrology, 2 Department of Pathology, Yale University School of Medicine, New Haven, CT, USA, and 3 Milano State University, Milano, Italy Key words light chain cast nephropathy acute kidney injury crystal casts multiple myeloma Abstract. Multiple myeloma (MM) is a plasma cell disorder, which often causes parenchymal kidney disease. Light chain (LC) cast nephropathy represents the most common renal lesion. In some instances, LC crystals precipitate within renal tubular lumens and deposit within proximal tubular cell cytoplasms. Importantly, urine microscopy in such patients can provide insight into the underlying LC-related lesion. Here we present two patients with MM complicated by acute kidney injury (AKI) where LC crystalline casts were observed on urinary sediment analysis. Kidney biopsy revealed acute tubular injury with LC crystal casts within both tubular lumens and renal tubular epithelial cell cytoplasms. These findings suggest that the urinary sediment may be a non-invasive way to diagnose LC crystalline-induced AKI in patients with MM. MM [5]. The excessive light chain burden leads to increased luminal concentration of free LCs that aggregate with Tamm-Horsfall protein leading to cast formation resulting in obstruction and inflammation [6]. Interestingly, monoclonal LC crystals can be seen on biopsy specimens from MM patients with AKI. However, these crystals have not been described in the urine of patients. Here we present two patients with LC crystalline casts visualized in the urine sediment and confirmed with biopsy. Identification of these crystalline casts in the urine can be a noninvasive way of recognizing LC-associated kidney injury such as cast nephropathy and perhaps light chain proximal tubulopathy. Received July 10, 2014; accepted in revised form September 5, 2014 Correspondence to Mark A. Perazella, MD Professor of Medicine Section of Nephrology, Yale University School of Medicine, 114 BB, 330 Cedar Street, New Haven, CT 06520, USA mark.perazella@yale.edu Introduction Multiple myeloma (MM) is a malignant plasma cell disorder that comprises ~ 1% of all cancers [1]. Malignant plasma cells produce abnormal paraproteins associated with kidney disease in upwards of 40% of patients [2, 3]. Acute kidney injury (AKI) associated with myeloma can be due to a number of parenchymal lesions; however, lightchain (LC) cast nephropathy, LC deposition disease, and AL amyloidosis are the most common [4]. Urine protein-immunoelectrophoresis and automated urinalysis are commonly utilized to assess kidney involvement in patients. However, these tests are unable to provide insight into the specific kidney lesion. In contrast, urine sediment examination may demonstrate findings reflective of the underlying kidney lesion. Myeloma LC cast nephropathy is the most common kidney injury associated with Case 1 A 48-year-old male with IgA-λ myeloma of 3 years duration presented with AKI. His treatment regimen included bortezomib, lenalidomide, and dexamethasone, resulting in remission for 1 year, followed by dexamethasone, cyclophosphamide, and carfilzomib upon recurrence. The patient was seen 3 months earlier at an outside hospital for an increased serum creatinine (2.7 mg/dl). The patient underwent kidney biopsy (described below), received intravenous fluids, and was continued on his chemotherapy regimen. Serum creatinine fluctuated between mg/dl with serum and urine free λ-lcs remaining elevated ( mg/dl; 750 1,000 mg/dl). At the time of consultation at our hospital, the patient was being treated with vancomycin and piperacillin/ tazobactam for pneumonia with bacteremia. His last dose of chemotherapy had been 1 week prior to admission. On review of his
2 Luciano, Castano, Fogazzi, and Perazella 2 creatinine slowly improved to 1.5 mg/dl, serum free LCs decreased, and the crystalline casts decreased in density and subsequently disappeared with subsequent urine sediment evaluations. Evaluation of a renal biopsy performed for an elevated serum creatinine (see above) at another institution from 3 months prior revealed crystalline cast structures in tubular lumens (Figure 2A, B). Proximal tubules showed acute injury with vacuolization, blebbing, and dilatation. In addition, the interstitium demonstrated a dense lymphoplasmacytic infiltrate. Electron microscopy demonstrated occasional hexagonal crystals in tubular epithelial cells (images not shown). Figure 1. A, B: Light microscopy of spun urine sediment for case 1 showing casts containing amorphous crystalline structures (magnification 400); C, D: Light microscopy of spun urine sediment for case 2 showing light chain crystalline casts (magnification 400). hospital course his blood pressure had always been normal ( /50 70 mmhg) and his urine output non-oliguric. Exam was remarkable for rales at his left lung base, but otherwise no signs of volume depletion or overload. Laboratory evaluations showed serum sodium of 136 meq/l, potassium of 5.2 meq/l, chloride of 104 meq/l, bicarbonate of 16.5 meq/l, glucose of 84 mg/dl, serum calcium of 8.5 mg/dl, BUN of 44 mg/ dl, and serum creatinine that had increased from a baseline of 2.2 mg/dl to 3.6 mg/dl, in 1 week. Serum free λ-lcs were 989 mg/ dl and urine free λ-lcs were 1,050 mg/dl, while κ-lcs were suppressed. Urinalysis revealed a specific gravity of 1.009, ph of 7, 2+ protein, negative glucose, 3 WBCs/hpf, and 1 RBC/hpf. Direct microscopic visualization of the sediment demonstrated 1 2 renal tubular epithelial cells/hpf, 3 5 free crystals of varying shape/hpf, and 1 2 crystalline casts/hpf (Figure 1A, B). The casts contained irregularly shaped crystalline structures with 0 25% birefringence under polarized microscopy. The crystalline casts persisted with repeat sediment evaluation. In the setting of rising serum creatinine and serum free LCs, treatment with cyclophosphamide, etoposide, and dexamethasone was started. Serum Case 2 A 56-year-old gentleman with a 2-year history of IgG-κ myeloma presented with AKI. The patient had suffered a bout of AKI that lead to kidney biopsy (see description below). Treatment initially included bortezomib and dexamethasone, which was associated with response and improved kidney function. However, after 12 months, the patient was switched to lenalidomide and dexamethasone when the LC burden started to increase and serum creatinine increased to 2.1 mg/dl. With this regimen, a reduction of serum and urine free κ-lcs was noted and kidney function improved to serum creatinine in the mg/dl range. However, the patient again became refractory to treatment ~ 2 months prior to the current hospitalization, serum free LCs increased and he was subsequently switched to carfilzomib and dexamethasone. In this setting, the patient developed a rise in serum creatinine from a baseline of 1.6 mg/dl to 3.2 mg/ dl over several weeks. Renal consultation was commenced at this time. On evaluation, the patient was mildly hypertensive ( /60 90 mmhg) with no signs of volume depletion. Laboratory evaluations showed serum sodium of 135 meq/l, potassium of 3.8 meq/l, chloride of 106 meq/l, bicarbonate of 19.7 meq/l, glucose of 116 mg/dl, serum calcium of 9.1 mg/dl, BUN of 49 mg/dl and serum creatinine of 3.2 mg/dl. Serum free κ-lcs were elevated at 326 mg/dl and urine κ-lcs elevated at
3 3 AKI from light chain crystalline casts RBCs/hpf. Urine sediment analysis on two separate occasions demonstrated aggregates of crystals and crystalline casts, with 25% birefringence with polarization (Figure 1C, D). On repeat samples, separated by several months LC crystalline casts persisted. Figure 2. A, B: Biopsy specimen from case 1. Refractile crystals are present within tubular lumens surrounding proteinacious material. Examples of crystalline material in periphery of tubule lumen are indicated (black arrows). The tubules show acute tubular injury with nuclear drop-out and flattening of the epithelium (hematoxylin and eosin (H & E), original magnification 1,000); C, D: Biopsy specimen from case 2. Tubular lumens show crystals, fractured light chain casts, and fragments of sloughed-off epithelial cells. Examples of crystal fragments within casts are indicated (black arrows). Acute tubular injury is present. Interstitium shows lymphocytic infiltrate (C: hematoxylin, phloxin, saffronin (HPS) stain; D: H & E, both original magnification 400). Figure 3. Electron microscopy shows numerous crystalline structures within the cytoplasm of the tubular epithelial cells (A: Electron microscopy, direct magnification 5,000) and in the tubular lumen (B: Electron microscopy, direct magnification 4,000). 239 mg/dl, while λ-lcs were suppressed. Urinalysis revealed a specific gravity of 1.010, 1+ protein, negative glucose, and 8 Evaluation of a renal biopsy performed for AKI from 2 years prior confirmed the presence of LC crystalline casts (Figure 2C, D). The proximal tubules demonstrated extensive tubular injury. Tubular lumens were filled with eosinophilic refractile material of varying shapes. Many tubular profiles showed light chain crystals in the cytoplasm of the proximal tubular epithelial cells and LC crystals in distal tubular lumens as well as fractured casts with epithelioid reaction. In addition there was a significant lymphocyte predominant interstitial infiltrate. Electron microscopy revealed multifaceted crystals in the proximal tubular lumens and within the cytoplasm of tubular epithelial cells (Figure 3). Discussion The two cases described are unique in that they demonstrate free LC crystals and LC crystalline casts in the urine sediment of patients with multiple myeloma and LC-related kidney disease. These findings have not been previously reported in the literature. In addition, these findings reinforce that urine microscopy can provide a window into the underlying kidney lesion and that urine sediment findings can at times truly be the liquid kidney biopsy. Monoclonal LC crystal formation has been previously reported in biopsy specimens of the kidneys and other organs. Reported cases of paraprotein-related crystal deposition demonstrated both κ- and λ-lc crystals deposited in kidney, heart, lung, spleen, thyroid, skin, and intestine [7]. Renal deposition of LC crystals has been associated with both AKI and proximal tubular dysfunction [8, 9, 10, 11]. While κ-lc crystal deposition within the kidneys has been more widely reported, λ-lc crystals have also been noted. In some cases, LC crystal deposition leads to rapidly progressive kidney failure [9, 12] Luciano / 23. September 2014, 3:27 PM
4 Luciano, Castano, Fogazzi, and Perazella 4 Fogazzi et al. [13] utilized immunofluorescence (IF) staining (anti-sera to LC immunoglobulins) of the urine sediment to identify monoclonal LCs in patients with kidney disease and various monoclonal gammopathies. They described urinary casts and other various shaped particles in the urine of 20 out of 27 patients with monoclonal disease and none in 25 control patients with non-monoclonal kidney disease. The sensitivity of the urine sediment IF staining was 74%, the specificity was 100%, and the positive predictive value was 100%. Another case of myeloma cast nephropathy described hexagonal crystals in the urine (not photographed) that were similar to those seen in the kidney biopsy light and electron microscopy specimens [14]. While neither of these cases showed images of LC crystalline casts in the urine sediment, these data confirm that urine sediment contains identifiable LC both free and within casts. Our data suggest that urine microscopy can identify LC crystals in the urine sediment, which can provide a window into the process within the renal parenchyma. The major challenge for the urine microscopist is to distinguish these LC crystalline casts from other urinary casts, such as coarsely granular casts. Careful inspection of the crystalline casts reveals the following unique characteristics when compared with granular casts. First, these casts contain crystals that are also seen free in the urine of both cases. In addition, these crystals were up to 25% birefringent under polarization, which is not seen with granular casts. Finally, the crystalline casts have a refractile appearance that is not seen with granular casts. Urine microscopy is a crucial part of the evaluation of kidney disease, including those with AKI, hematuria, and proteinuria [15]. Thorough evaluation of the spun urinary sediment provides data that cannot be otherwise obtained by dipstick urinalysis and automated or laboratory technician-performed urine examination. Expert differentiation of urinary cell morphology, accurate identification of cellular and non-cellular casts, and recognition and diagnosis of various endogenous and drug-related crystals can lead to rapid diagnosis of the kidney-related process. Paraprotein-related diseases such as MM and associated monoclonal LC disorders, which are commonly complicated by kidney injury, lend themselves well to diagnostic evaluation by urine sediment examination. While serum and urine protein immunoelectrophoresis and serum free LCs are routinely utilized to assess for kidney involvement, they cannot distinguish the type of lesion present. Nowadays, clinicians utilize the automated urinalysis report to confirm potential renal disease while rarely viewing the urine sediment. As a result, the renal diagnosis is presumed based on serum and urine immunoglobulin (Ig) or LC testing combined with urinalysis. A percutaneous kidney biopsy is pursued for diagnostic adjudication and confirmation in some cases. In conclusion, we report unique urinary LC crystalline casts and free crystals in two patients with MM. Thorough examination of the urine sediment in patients with monoclonal LCs and evidence of kidney disease will potentially provide the diagnosis. It is logical that patients with monoclonal diseases and evidence for kidney injury should have urine microscopy performed by an appropriately trained nephrologist. In addition, it is possible that urine sediment exam in patients with an underlying monoclonal gammopathy may provide information about kidney injury and serve as a biomarker of early kidney disease. Conflicts of interest None. References [1] Raab MS, Podar K, Breitkreutz I, Richardson PG, Anderson KC. Multiple myeloma. Lancet. 2009; 374: [2] Dimopoulos MA, Terpos E, Chanan-Khan A, Leung N, Ludwig H, Jagannath S, Niesvizky R, Giralt S, Fermand JP, Bladé J, Comenzo RL, Sezer O, Palumbo A, Harousseau JL, Richardson PG, Barlogie B, Anderson KC, Sonneveld P, Tosi P, Cavo M, et al. Renal impairment in patients with multiple myeloma: a consensus statement on behalf of the International Myeloma Working Group. J Clin Oncol. 2010; 28: [3] Bladé J, Fernández-Llama P, Bosch F, Montolíu J, Lens XM, Montoto S, Cases A, Darnell A, Rozman C, Montserrat E. Renal failure in multiple myeloma: presenting features and predictors of outcome in 94 patients from a single institution. Arch Intern Med. 1998; 158:
5 AKI from light chain crystalline casts 5 [4] Leung N, Nasr SH. Myeloma-related kidney disease. Adv Chronic Kidney Dis. 2014; 21: [5] Ying WZ, Allen CE, Curtis LM, Aaron KJ, Sanders PW. Mechanism and prevention of acute kidney injury from cast nephropathy in a rodent model. J Clin Invest. 2012; 122: [6] Huang ZQ, Kirk KA, Connelly KG, Sanders PW. Bence Jones proteins bind to a common peptide segment of Tamm-Horsfall glycoprotein to promote heterotypic aggregation. J Clin Invest. 1993; 92: [7] Usuda H, Emura I, Naito M. Crystalglobulin-induced vasculopathy accompanying ischemic intestinal lesions of a patient with myeloma. Pathol Int. 1996; 46: [8] Orfila C, Lepert JC, Modesto A, Bernadet P, Suc JM. Fanconi s syndrome, kappa light-chain myeloma, non-amyloid fibrils and cytoplasmic crystals in renal tubular epithelium. Am J Nephrol. 1991; 11: [9] Keller LS, Faull RJ, Smith P, Swift J, Bannister KM, Otto S, Peh CA. Crystalloid deposits in the kidney. Nephrology (Carlton). 2005; 10: [10] Toly-Ndour C, Peltier J, Piedagnel R, Coppo P, Sachon E, Ronco P, Rondeau E, Callard P, Aucouturier P. Acute renal failure with lambda light chainderived crystals in a patient with IgD myeloma. Nephrol Dial Transplant. 2011; 26: [11] Larsen CP, Bell JM, Harris AA, Messias NC, Wang YH, Walker PD. The morphologic spectrum and clinical significance of light chain proximal tubulopathy with and without crystal formation. Mod Pathol. 2011; 24: [12] Kanno Y, Okada H, Nemoto H, Sugahara S, Nakamoto H, Suzuki H. Crystal nephropathy: a variant form of myeloma kidney a case report and review of the literature. Clin Nephrol. 2001; 56: [13] Fogazzi GB, Pozzi C, Passerini P, Simonini P, Locatelli F, Ponticelli C. Utility of immunofluorescence of urine sediment for identifying patients with renal disease due to monoclonal gammopathies. Am J Kidney Dis. 1991; 17: [14] Dehmel B, Schneider W, Kettritz R, Luft FC. Not so acute renal failure with crystals in the urine. Nephrol Dial Transplant. 2003; 18: [15] Fogazzi GB, Grignani S, Colucci P. Urinary microscopy as seen by nephrologists. Clin Chem Lab Med. 1998; 36:
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