Introduction
Nephrotic syndrome is one of the best known presentations of kidney disease. This term describes the association of proteinuria greater than 3.5 g/1.73 m2 body surface area/24 hours with hypoalbuminemia, oedema and hyperlipidemia. Glomerular diseases manifesting the nephrotic syndrome are caused by defects in the glomerular filtration barrier. The glomerular filtration barrier comprises cellular and extracellular structural elements including: the glomerular basement membrane (GBM), endothelial cells, visceral epithelial cells (podocytes), and interposed slit diaphragms. Disruption of the glomerular filtration barrier may be due to: immune-complex deposition, circulating permeability factors, T-lymphocyte abnormalities, genetic defects in podocyte proteins, viral infections, stretch injury, toxins, drugs, glomerular inflammation, and physicochemical alterations [1].
It is estimated that cancer occurs in 11% to 13% of patients with the nephrotic syndrome [2, 3]. However, the determination of the real incidence and prevalence of paraneoplastic nephrotic syndrome is very difficult, because most often, associations between nephrotic syndrome and neoplasia are described as case reports and case series making the risk assessment difficult. Criteria for the diagnosis of paraneoplastic glomerulopathy are as follows: a clinical and histological remission after complete surgical removal of the tumour, or chemotherapy-induced complete remission of the disease, renal relapse associated with recurrence of the neoplasia, a pathophysiologic link established between the two diseases, including the detection of tumour antigens and antitumor antibodies within immune deposits [4]. A causal relationship is suggested if nephrotic range proteinuria develops either 6 months before or after the diagnosis of malignancy [5].
The pathogenesis of the paraneoplastic syndrome includes involvement of tumour associated antigens, re-expressed foetal antigens and/or viral antigens, host-antibody response of the shedding of tumour antigen, circulating tumour antigen-antibody complexes which may inhibit or suppress tumour-specific cell-mediated immunity [6]. Numerous attempts have been made to identify tumour antigens or their specific antibodies in kidneys of cancer patients, however antigens/antibodies have been demonstrated in only several cases of paraneoplastic glomerulopathy [7]. Tumour antigens implicated in the formation of immune deposits have been the carcinoembryonic antigen, prostate-specific antigens, the renal tubular epithelial antigen (RTE), and other unidentified tumour products [8-12]. The presence of tumour antigens and their corresponding antibodies in patients with paraneoplastic glomerulopathies does not mean, however, that they are involved in the initial pathogenetic process leading to the formation of immune deposits. These components can become passively deposited because of increased glomerular permeability to proteins as a result of the initial insult [6]. Birkeland and Storm [13] suggested an association between nephrotic syndrome with malignancies and persistent virus infections, which cause glomerulonephritis first and then malignancies.
The concept of paraneoplastic glomerulopathy was introduced in 1922 by Galloway [14]. In 1939, Cornig [15] reported the first case of nephrotic syndrome and Hodgkin’s disease. The first convincing clinicopathologic study was published in 1966 by Lee et al. [2]. Out of their 101 adult patients who presented with the nephrotic syndrome, 11% were found to have carcinoma. In 1977, Eagen and Lewis [16] collected 171 cases of nephrotic syndrome associated with cancers including carcinoma, Hodgkin’s disease, non-Hodgkin’s lymphoma, leukaemia, and plasma cell dyscrasia. The glomerular lesion of paraneoplastic nephrotic syndrome usually presents as membranous nephropathy (MN) in patients with solid tumours, particularly adenocarcinomas of the lung and gastrointestinal tract [2-5, 15-18]. Minimal change disease (MCD) is strongly associated with Hodgkin’s lymphoma (HL), whereas the most common lesions observed in patients with chronic lymphocytic leukaemia (CLL) are membranoproliferative glomerulopathy (MPGN) and membranous nephropathy [2, 4, 5, 15-21]. Extracapillary crescentic glomerulopathy, IgA nephropathy and focal segmental glomerulosclerosis can also be associated with neoplasia [5, 22-25]. Glomerulopathies presented with nephrotic syndrome associated with neoplasm reported in the literature are shown in Table I [26-48] and Table II [49-61]. Nephrotic syndrome is rarely observed in patients with benign tumours (Table III) [62-66].
Case presentation
We present 6 cases of nephrotic syndrome and neoplasia. Clinical data and the types of glomerular injury are shown in Table IV. Age of the patients was 55-65 years, mean age= 59.3, male/female ratio was 3/3. Three patients clinically manifested the nephrotic syndrome prior to the diagnosis of the tumour. Epithelial malignancies (1 case of small cell lung carcinoma, 1 case of gastric adenocarcinoma and 2 cases of colon adenocarcinomas) were associated with membranous nephropathy. In 2 cases of lymphoproliferative malignancies (chronic lymphocytic leukaemia and Hodgkin’s lymphoma), renal biopsy revealed membranoproliferative glomerulonephritis and minimal change disease, respectively. In light microscopy, immunofluorescence study and electron microscopy, the renal lesions did not differ from idiopathic forms of glomerulopathies. In membranous nephropathies, uniform thickening of the glomerular capillary walls was seen (Fig. 1) due to diffuse subepithelial and intramembranous immune deposits (Fig. 2). An increase in mesangial matrix was present in three cases of paraneoplastic membranous nephropathy. Immunofluorescence study in paraneoplastic MN revealed strong granular staining of IgG and C3 along glomerular capillary loops. In the patient with paraneoplastic minimal change disease, diffuse effacement of the podocyte foot processes and microvillous transformation were seen in electron microscopy (Fig. 3). In this case of paraneoplastic MCD, light microscopy did not reveal any abnormalities, and immunofluorescence was completely negative. The renal biopsy in the patient with paraneoplastic membranoproliferative glomerulonephritis showed accentuated lobular configuration in glomeruli and variable thickening of capillary walls. An increase in mesangial matrix and mesangial cells was seen in light microscopy (Fig. 4). Electron microscopy revealed subepithelial, as well as mesangial deposits. Granular staining of IgG, C3 and IgM in the mesangium and along the periphery of capillary loops was present in the immunofluorescence study. The patient with paraneoplastic MN due to small cell lung cancer died within 4 months after the renal biopsy. A transient amelioration of the nephrotic syndrome after excision of the tumour was seen in the patient with gastric adenocarcinoma and paraneoplastic MN. Resolution of the nephrotic syndrome after surgical removal of the tumour was noted in 2 patients with MN and colon adenocarcinoma. In the patient with paraneoplastic MCD and Hodgkin’s lymphoma and in the patient with chronic lymphocytic leukaemia and paraneoplastic MPGN, the resolution of the nephrotic syndrome after chemotherapy was observed.
Discussion
In our study light microscopy, immunofluorescence study and electron microscopy revealed membranous nephropathy in all cases of epithelial malignancies. It is well known that MN is the most common nephropathy associated with neoplasm. This occurs in approximately 70% of patients reported to have a malignancy-associated nephrotic syndrome [5]. The most frequent type of malignancy related to membranous glomerulopathy is carcinoma of the colon, lung, stomach, pancreas, kidney, prostate, and melanoma of the skin [2-6, 16-18]. Out of the patients with carcinoma and membranous glomerulopathy, 40% to 45% clinically manifest the nephrotic syndrome prior to the diagnosis of the tumour [5]. In our study, in 3 patients with malignancies and paraneoplastic MN, nephrotic syndrome preceded the diagnosis of the lung, gastric and colon cancer. In one patient with colon adenocarcinoma, nephrotic syndrome due to paraneoplastic membranous nephropathy was observed after the diagnosis of the tumour. In our study, the clinical remission after surgical removal of the tumour indicates the relationship between malignancy and glomerulopathy. The age of patients with paraneoplastic nephrotic syndrome due to membranous nephropathy was from 55 to 65, and the mean age was almost 60. It must be stressed that the incidence of malignancy-associated MN among patients over the age of 60 is 19.4% [67], whereas cancer rates can reach as high as 24.7% in patients over the age of 64 [68]. The literature data indicate that the renal lesions seen in paraneoplastic membranous nephropathy are similar to those of idiopathic MN, although several authors have noted the presence of numerous polymorphonuclear leukocytes in capillary loops, occasionally associated with intravascular hyaline thrombi in the absence of renal vein thrombosis [69]. Lefaucher et al. [70] showed that the number of inflammatory cells infiltrating glomeruli is significantly higher in patients with cancer-associated MN, and the best cutoff value for distinguishing malignancy-related cases from idiopathic is 8 cells per glomerulus in patients with cancer-associated MN. Ohtani et al. [71] pointed out that in malignancy-associated MN, the staining for IgG1 and IgG2 is of the greatest intensity. In our study, light and electron microscopy did not reveal any differences in comparison to idiopathic forms of membranous nephropathy. Immunofluorescence evaluation showed strong granular staining of IgG and C3 along glomerular capillary walls. We did not study subclasses of IgG, because in the routine practice such evaluation is used very rarely.
In patients with nephrotic syndrome and lymphomas, light microscopy, immunofluorescence and electron microscopy evaluation of the renal tissue revealed minimal change disease and membranoproliferative glomerulonephritis. Hodgkin’s lymphoma was associated with MCD, and chronic lymphocytic leukaemia with MPGN. The association between Hodgkin’s disease and glomerulopathy is probably the best known of the hemopathy-induced paraneoplastic glomerulopathies, although in two large series collecting 1,700 Hodgkin’s disease patients, only 0.4% of them had MCD [72, 73]. Moulin et al. [74] have identified approximately 100 reports of Hodgkin’s-disease-associated glomerulopathy, mainly amyloidosis (37%) and MCD (42%). The development of MCD may precede or be simultaneous with the diagnosis of Hodgkin’s disease. The morphological subtype is predominantly mixed cellularity (MC) form of classical Hodgkin’s lymphoma [75], however in a more recent review, nodular sclerosis (NS) was reported as a predominant morphological subtype associated with paraneoplastic nephrotic syndrome and cHL [19]. Effective treatment of the hemopathy is associated with the disappearance of MCD [18]. In our study, in the patient with Hodgkin’s lymphoma (subtype mixed cellularity) nephrotic syndrome preceded the diagnosis of the lymphoma, and the resolution of the nephrotic syndrome after chemotherapy was observed. In this case of paraneoplastic glomerulopathy, the renal lesions did not differ in comparison to the idiopathic form of MCD.
Paraneoplastic nephrotic syndrome due to MCD may also be associated with solid tumours, especially with thymoma, renal cell carcinoma, colorectal carcinoma, and lung carcinoma. Taniguchi et al. [76] described a patient with rectal adenocarcinoma associated with MCD and elevation of vascular endothelial growth factor (VEGF). What is more, after tumour resection, proteinuria disappeared and VEGF decreased to the normal level. The link between thymoma and MCD is very interesting. In an animal model of paraneoplastic glomerulopathy, the Buffalo/Mna rat (spontaneous thymoma, myasthenia and glomerulopathy due to genetic abnormality) had proteinuria and nephrotic syndrome leading to MCD and FSGS [77].
Nephrotic glomerulopathies rarely occur in association with acute leukaemia, but they have been described in chronic lymphocytic leukaemia. Membranoproliferative glomerulopathy and membranous nephropathy are the most common lesions observed in CLL [78, 79]. In a review by Seney et al. [80], nephrotic syndrome occurred in less than 1-2% of CLL. In the presented case, in the patient with chronic lymphocytic leukaemia, nephrotic syndrome appeared 6 months after the diagnosis of CLL. Complete remission of nephrotic syndrome after chemotherapy was noted. In this case, light microscopy, immunofluorescence and electron microscopy evaluation of the renal biopsy revealed membranoproliferative glomerulonephritis, similar to the idiopathic type of MPGN,
In conclusion, the glomerular lesion of paraneoplastic nephrotic syndrome usually presents as membranous nephropathy, minimal change disease or membranoproliferative glomerulonephritis. The clinical remission after surgical removal of the tumour, or chemotherapy-induced complete remission of the disease indicates the relationship between malignancy and glomerulopathy. The search for malignancy is warranted in patients over the age of 55 presenting with nephrotic syndrome, particularly in the cases of membranous nephropathy.
Acknowledgment
This work was supported by grant of Polish Ministry of Science and Higher Education N N402 088735.
References
1. Stokes MB, Markowitz GS, D’Agati VD. Glomerular diseases associated with nephrotic syndrome and proteinuria. In: Silva’s Diagnostic Renal Pathology. Zhou XJ, Laszik Z, Nadasdy T, et al. (eds). Cambridge University Press, Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sao Paulo, Delhi 2009; 79-81.
2. Lee JR, Yamauchi H, Hopper J Jr. The association of cancer and nephrotic syndrome. Ann Intern Med 1966; 64: 41-51.
3. Zech P, Colon S, Pointet PH, et al. The nephrotic syndrome in adults aged over 60: etiology, evolution, and treatment of 76 cases. Clin Nephrol 1982; 17: 232-236.
4. Burstein DM, Korbet SM, Schwartz MM. Membranous glomerulonephritis and malignancy. Am J Kidney Dis 1993; 22: 5-10.
5. Davison AM. Renal diseases associated with malignancies. Nephrol Dial Transplant 2001; 16 (Suppl 6): 13-14.
6. Bacchetta J, Juillard L, Cochat P, et al. Paraneoplastic glomerular diseases and malignancies Crit Rev Oncol Hematol 2009; 70: 39-58.
7. Lewis MG, Longridge LW, Philps TM. Immunological studies in nephrotic syndrome associated with extrarenal malignant disease. Lancet 1971; 2: 134-135.
8. Constanza ME, Pinny V, Schwartz RS, et al. Carcinoembryonic antigen-antibody complexes in a patient with colonic carcinoma and nephrotic syndrome. N Engl J Med 1973; 289: 520-522.
9. Pascal RR, Slovin SF. Tumor directed antibody and carcinoembryonic antigen in the glomeruli of a patient with gastric carcinoma. Hum Pathol 1980; 11: 679-682.
10. Weksler ME, Cerey T, Day N, et al. Nephrotic syndrome in malignant melanoma.
Demonstration of melanoma antigen-antibody in the kidney. Kidney Int 1974; 6: 112A.
11. Olson JL, Phillips TM, Lewis MG, et al. Malignant melanoma with renal dense deposits containing tumor antigens. Clin Nephrol 1979; 12: 74-82.
12. Ozawa T, Pluss R, Lacher J, et al. Endogenous immune complex nephropathy associated with malignancy. I. Studies on the nature and immunopathogenic significance of glomerular-bound antigen and antibody and circulating immune complexes. Q J Med 1975; 44: 523-541.
13. Birkeland SA, Storn HH. Glomerulonephritis and malignancy: a population based analysis. Kidney Int 2003; 63: 716-721.
14. Galloway J. Remarks of Hodgkin’s disease. BMJ 1922; 2: 1201-1208.
15. Cornig HJ. Une forme nouvelle de la maladie de Hodgkin: Lymphogranulomatose maigne a type de nephrose lipidique. These de Paris 1939; 571.
16. Eagen JW, Lewis EJ. Glomerulopathies of neoplasma. Kidney Int 1977; 11: 297-306.
17. Alpers E, Cotran RS. Neoplasia and glomerular injury. Kidney Int 1986; 30: 465-473.
18. Ronco PM. Paraneoplastic glomerulopathies: new insights into an old entity. Kidney Int 1999; 56: 355-377.
19. Audard V, Larousserie F, Grimbert P, et al. Minimal change nephrotic syndrome and classical Hodgkin’s lymphoma: report of 21 cases and review of the literature. Kidney Int 2006; 69: 2251-2260.
20. Da'as N, Polliack A, Cohen Y, et al. Kidney involvement and renal manifestations in non-Hodgkin's lymphoma and lymphocytic leukemia: a retrospective study in 700 patients. Eur J Haematol 2001; 67: 158-164.
21. Dabs DJ, Striker LM, Mignon F, et al. Glomerular lesions in lymphomas and leukemias. Am J Med 1986; 80: 63-70.
22. Jain S, Kakkar N, Joshi K, et al. Crescentic glomerulonephritis associated with renal cell carcinoma. Ren Fail 2001; 23: 287-290.
23. Mustonen J, Pasternack A, Helin H. IgA mesangial nephropathy in neoplastic disease. Contr Nephrol 1984; 40: 283-291.
24. Yacoub G, Kosseifi SG, Shah LS, et al. IgA nephropathy and small lung carcinoma. Tenn
Med 2008; 101: 35-37.
25. Biava CG, Gonwa TA, Naughton IJ, et al. Crescentic glomerulonephritis associated with non-renal malignancies. Am J Nephrol 1984; 4: 208-214.
26. Yamagata T, Akamatsu K, Kuroda M, et al. Squamous cell lung cancer with minimal-change nephrotic syndrome. Nippon Kokyuki Gakkai Zasshi 1998; 36: 1032-1037.
27. Singer CR, Boulton-Jones MJ. Minimal change nephropathy as-sociated with anaplastic carcinoma of bronchus. Postgrad Med J 1986; 62: 213-217.
28. Arenas MD, Gil MT, Malek T, et al. Nephrotic syndrome as paraneoplastic manifestation of primary pulmonary lymphoepithelioma-like carcinoma. Clin Nephrol 2009; 72: 206-210.
29. Komori S, Nakazawa E, Akimoto T, et al. Nephrotic syndrome associated with lung adenocarcinoma: report of an autopsy case. Nippon Jinzo Gakkai Shi 2009; 51: 138-144.
30. Boon ES, Vrij AA, Nieuwhof C, et al. Small cell lung cancer with paraneoplastic nephrotic syndrome. Eur Respir 1994; 7: 1192-1193.
31. Usalan C, Emri S. Membranoproliferative glomerulonephritis associated with small cell lung carcinoma. Int Urol Nephrol 1998; 30: 209-211.
32. Ohara G, Satoh H, Kurishima K, et al. Paraneoplastic nephrotic syndrome in patients with lung cancer. Inter Med 2009; 48: 1817-1820.
33. Wakashin M, Wakashin Y, Iesato K, et al. Association of gastric cancer and nephrotic syndrome. Immunologic study in three patients. Gastroenterology 1980; 78: 749-756.
34. Waki M, Ishimura E, Morii H, et al. A case of membranous glomerulonephritis associated with gastric cancer. Osaka City Med J 1997; 43: 95-105.
35. Catane R, Kaufman JH, Douglass HO, et al. Nephrotic syndrome associated with gastric cancer. J Surg Oncol 1977; 9: 207-211.
36. Weintroub S, Stavorovsky M, Griffel B. Membranous glomerulonephritis. An initial
symptom of gastric carcinoma? Arch Surg 1975; 110: 833-838.
37. Gandini E, Allaria P, Castiglioni et al. Minimal change nephrotic syndrome with cecum adenocarcinoma. Clin Nephrol 1996; 45: 268-270.
38. Goldstein D, Kelly R, Ralston M, et al. Chemotherapy influencing the course of nephrotic syndrome in colonic carcinoma. Med Oncol Tumor Pharmacother 1987; 4: 101-105.
39. Couser WG, Wagonfeld JB, Spargo BH, et al. Glomerular deposition of tumor antigen in membranous nephropathy associated with colonic carcinoma. Am J Med 1974; 57: 962-970.
40. Stuart K, Fallon BG, Cardi MA. Development of nephrotic syndrome in a patient with prostatic carcinoma. Am J Med 1986; 80: 295-298.
41. Matsuura H, Sakurai M, Arima K. Nephrotic syndrome due to membranous nephropathy associated with metastatic prostate cancer: rapid remission after initial endocrine therapy. Nephron 2000; 84: 75-78.
42. Barton CH, Vaziri ND, Spear GS. Nephrotic syndrome associated with adenocarcinoma of the breast. Am J Med 1980; 68: 308-312.
43. Valcamonico F, Ferrari F, Simoncini E, et al. Paraneoplastic nephrotic syndrome in advanced breast cancer patient. A case report. Tumori 2004; 90: 154-156.
44. Kijima Y, Yoshinaka H, Owaki T, et al. Breast cancer with nephrotic syndrome: report of two cases. Surg Today 2004; 34: 755-759.
45. Bonkain F, Ena G, Depierreux M, et al. Nephrotic syndrome and renal failure as an unusual presentation of solid tumor. NDT Plus 2010; 3: 51-53.
46. Fujita Y, Kashiwagi T, Takei H, et al. Membranous nephropathy complicated by renal cell carcinoma. Clin Exp Nephrol 2004; 8: 59-62.
47. Kuroda I, Ueno M, Okada H, et al. Nephrotic syndrome as a result of membranous nephropathy caused by renal cell carcinoma. Int J Urol 2004; 11: 235-238.
48. Togawa A, Yamamoto T, Suzuki H, et al. Membranous glomerulonephritis associated with renal cell carcinoma: failure to detect a nephritogenic tumor antigen. Nephron 2002; 90: 219-221.
49. Zheng HI, Maruyama T, Matsuda S, et al. Neuroblastoma presenting with nephrotic syndrome. J Pediatr Surg 1979; 14: 414-419.
50. Salazar-Exaire D, Rodríguez A, Galindo-Rujana ME, et al. Membranoproliferative glomerulonephritis associated with a mixed-cell germinal ovary tumor. Am J Nephrol 2001; 21: 51-54.
51. Meydani MM, Erguvan R, Altinok MT, et al. Rare case of neuroendocrine small cell carcinoma of the endometrium with paraneoplastic membranous glomerulonephritis. Tumori 2003; 89: 213-217.
52. Cimic A, Pastan SO, Bijol V. Membranous nephropathy associated with gastrointestinal stromal tumour: a case report. NDT Plus 2009; 2: 306-308.
53. Texier F, Dharancy S, Provot F, et al. Membranous glomerulonephritis complicating hepatocellular carcinoma. Gastroenterol Clin Biol 2004; 28: 605-607.
54. Muramoto T, Kaneko K, Kuroki A, et al. Causal relationships between esophageal squamous cell carcinoma and nephrotic syndrome. Inter Med 2009; 48: 65-69.
55. Lee HC, Cheng YF, Chuang FR, et al. Minimal change nephrotic syndrome associated with malignant thymoma: case report and literature review. Chang Gung Med J 2001; 24: 576-581.
56. Fakuda A, Sato Y, Iwatsubo S, et al. Minimal change nephrotic syndrome complicated with recurrence of malignant thymoma: an interesting case with remission due to steroid therapy of both nephrotic syndrome and thymoma. Nippon Jinzo Gakkai Shi 2009; 51: 130-137.
57. Altiparmak MR, Pamuk ON, Pamuk GE, et al. Membranous glomerulonephritis in a patient with choriocarcinoma: case report. South Med J 2003; 96: 198-200.
58. Uramatsu T, Furusu T, Nishino T, et al. Membranous nephropathy complicated nasopharyngeal carcinoma. Inter Med 2010; 49: 585-588.
59. Ashman N, Steele JP, Sheaff M, et al. Membranous nephropathy resolving with treatment of bronchial carcinoid tumor. Am J Kidney Dis 2000; 36: E15.
60. Startelet H, Melin JP, Wynckel A, et al. Membranoproliferative glomerulonephritis (MPGN) and pulmonary carcinoid tumour. Nephrol Dial Transplant 1997; 12: 2405-2406.
61. Bacccheta J, Ranchere D, Dijoud F, et al. Mesothelioma of the testis and nephrotic syndrome: a case report. J Med Case Reports 2009; 3: 7248-7251.
62. Ng SB, Tan PH, Chuah KL, et al. A case of juxtaglomerular cell tumor associated with membranous glomerulonephritis. Am Diagn Pathol 2003; 7: 314-320.
63. Wadwha NK, Gupta M, Afolabi A, et al. Membranous glomerulonephritis in a patient with an adrenal ganglioneuroma. Am J Kidney Dis 2004; 44: 363-368.
64. Sood AK, Dua A, Mahajan A, et al. Minimal change nephrotic syndrome with extrarenal neurilemmoma. Nephron 1997; 75: 230-232.
65. Alexopoulos E, Kirmizis D, Visvardis G, et al. Focal segmental glomerulosclerosis in a patient with large bilateral asymptomatic adrenal myelolipomas. Ren Fail 2003; 25: 1051-1056.
66. Kon SP, Fan SL, Kwan JT, et al. Membranous nephropathy complicating adenolymphoma of the parotid (Wathin’s tumour). Nephron 1996; 73: 692-694.
67. Glassock RJ. Secondary membranous glomerulonephritis. Nephrol Dial Transplant 1992; 7 Suppl 1: 64-71.
68. Honig C, Mouradian JA, Montoliu J, et al. Mesangial electron-dense deposits in membranous nephropathy. Lab Invest 1980; 42: 427-432.
69. Mignon F, Beaufils H, Morel-Maroger L, et al. Glomerulopathies au cours des affections malignes. Seminaires d’uro-nephrologie Pitie-Salpetriere, Paris, Masson 1982: 171-193.
70. Lefaucheur C, Stengel B, Nochy D, et al. Membranous nephropathy and cancer: epidemiologic evidence and determinants of high-risk cancer association. Kidney Int 2006;
70: 1510-1517.
71. Ohtani H, Wakuj H, Komatsuda A, et al. Distribution of glomerular IgG subclass deposits in malignancy-associated membranous glomerulopathy. Nephrol Dial Transplant 2004; 19: 574-579.
72. Plager J, Stutzman L. Acute nephrotic syndrome as a manifestation of active Hodgkin’s disease. Am J Med 1971; 50: 56-66.
73. Kramer P, Sizoo W, Twiss EE. Nephrotic syndrome in Hodgkin’s disease. Neth J Med 1981; 24: 114-119.
74. Moulin B, Chantrel F, Petitjean P, et al. Chronic lymphoproliferative disorders and glomerular disease: review of the literature and pathophysiologic considerations. J Nephrol 1995; 8: 20-26.
75. Moorthy AV, Zimmerman SW, Burkholder PM. Nephrotic syndrome in Hodgkin’s disease: evidence for pathogenesis alternative to immune complex deposition. Am J Med 1976; 61: 471-477.
76. Taniguchi K, Fujioka H, Torashima Y, et al. Rectal cancer with paraneoplastic nephropathy: association of vascular endothelial growth factor. Dig Surg 2006; 3: 32-37.
77. Karras A, de Montpreville V, Fakhouri F, et al. Renal and thymic pathology in thymoma-associated nephropathy: report of 21 cases and review of the literature. Nephrol Dial Transplant 2005; 20: 1075-1082.
78. Moulin B, Ronco PM, Mougenot B, et al. Glomerulonephritis in chronic lymphocytic leukemia and related B-cell lymphomas. Kidney Int 1992; 42: 127-135.
79. Yahata N, Kawanishi Y, Okabe S, et al. Membranous glomerulonephritis with nephrotic syndrome associated with chronic lymphocytic leukemia. Am J Nephrol 2000; 20: 402-407.
80. Seney TD Jr, Pedergreen WR, Stein H, et al. A review of nephrotic syndrome associated
with chronic lymphocytic leukemia. Arch Intern Med 1986; 148: 137-141.
Address for correspondence
Małgorzata Wągrowska-Danielewicz
Department of Nephropathology
Medical University of Łódź
ul. Pomorska 251
92-216 Łódź
phone/fax +48 42 675 76 33
e-mail: malgorzata.wagrowska-danilewicz@umed.lodz.pl
