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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2010  |  Volume : 21  |  Issue : 2  |  Page : 372-378
Pulse cyclophospamide in severe lupus nephritis: Southern Indian experience

1 Department of Nephrology, Nizam's Institute of Medical Sciences, Punjagutta, Hyderabad, India
2 Department of Pathology, Nizam's Institute of Medical Sciences, Punjagutta, Hyderabad, India

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Date of Web Publication9-Mar-2010


To evaluate the efficacy and safety of the monthly pulse IV cyclophosphamide (IVC) therapy in patients with severe lupus nephritis, we studied 39 patients of lupus nephritis on IVC therapy between 1998 to 2002. Single monthly cyclophosphamide (0.75-1 g/m²) was infused intravenously with oral prednisolone (0.5 mg/kg per day) and appropriate hydration. Of the 39 pa­tients 25 (86.2%) patients were females and 4 (13.8%) were males. Six (2%) cases had irregular follow-up and 3 patients had expired during the initial cycles and were excluded from the study. The mean age was 25.6 + 6.72 years (range 10-40 years). The mean duration of the disease from the onset to renal biopsy was 24.2 + 18.5 months. The clinical presentations included nephrotic syndrome (34.5%), acute glomerulonephritis (31.0%), Pyrexia of unknown origin (PUO) (10.3%), and rapidly progressive renal failure (6.7%). Renal insufficiency was present in 47.2% cases. Twenty-two (75.9%) patients had diffuse proliferative glomerulonephritis (class IV), 6 (20.7%) focal proliferative glomerulonephritis (class III), and one (3.4%) class Vd. After a mean follow-up of 15.8 months, out of 29 patients, 13 (44.8%) had achieved complete remission, 7 (24.1%) partial remission and 9 (31.0%) cases did not respond to the therapy. Side effects of the therapy included vomiting and nausea (100%) and hair loss during the first few doses of IVC. In addition, one case had dysfunctional uterine bleeding and two patients had avascular necrosis of femoral head. We conclude that our data indicate that IVC in severe lupus nephritis is effective in Indian patients though longer follow-up is required.

How to cite this article:
Das U, Dakshina Murty K V, Prasad N, Prayag A. Pulse cyclophospamide in severe lupus nephritis: Southern Indian experience. Saudi J Kidney Dis Transpl 2010;21:372-8

How to cite this URL:
Das U, Dakshina Murty K V, Prasad N, Prayag A. Pulse cyclophospamide in severe lupus nephritis: Southern Indian experience. Saudi J Kidney Dis Transpl [serial online] 2010 [cited 2022 Sep 27];21:372-8. Available from: https://www.sjkdt.org/text.asp?2010/21/2/372/60218

   Introduction Top

Systemic lupus nephritis (SLE) is a multisys­temic disease with a wide array of immuno­logical abnormalities. [1] Survival of patients with SLE have improved greatly, but lupus nephri­tis (LN) remains an important cause of morbi­dity and mortality. [2] The aims of treating lupus nephritis are to induce and maintain remission thereby reducing the risk of progression to re­nal failure. Immunosuppressive drugs are more efficacious than prednisolone alone in contro­lling clinical signs of active nephritis, preven­ting renal scarring, and reducing the risk of end-stage renal disease (ESRD). [3] The most popular therapeutic regimen consists of long-term pul­ses IVC in combination with corticosteroid. [4] However, some investigators have drawn at­tention to the limitation of IVC, including toxi­city during long-term use and possibility of re­lapse. [5] Despite skepticism, cyclophosphamide remains the most effective therapy for initial treatment for aggressive lupus nephritis. [6] Se­veral studies showed that neither pulse methyl prednisolone (MP) nor short course of pulse IVC are as efficacious as extended course of pulse cyclophosphamide in reducing the risk of renal progression or in achieving sustained remission of lupus nephritis [7]

We aimed in this study to analyze our expe­riences and outcome of severe lupus nephritis treated with pulse cyclophosphamide and to evaluate risk factors for poor renal outcome.

   Methods and Patients Top

The study was performed in the Department of Nephrology in Nizam's institute of medical sciences, Hyderabad, India, from January 1998 to December 2002. Inclusion criteria were pa­tients who had fulfilled the revised American Rheumatological Association (ARA) criteria for diagnosis of SLE and revealed renal biopsy evi­denced severe (proliforetive) lupus nephritis, urinary protein excretion of > 500 mg/24h, and serum creatinine (s. Cr) :5 3.4 mg/dL. Informed consent was obtained from all the patients.

The patients who achieved complete remis­sion and those who did not respond to the treat­ment were identified and the predictors of poor outcome were evaluated.

Each renal biopsy specimen was evaluated by light and immunofluroscence microscopy by the renal pathologist of the institute. Specimen were required to have minimum 10 glomeruli for light microscopy and findings were categorized based on the recommendations of the World Health Organization (WHO) [8] and only subjects with severe lupus nephritis (LN) eg; class III/IV and Vc/Vd were included in this study.


Defined as a value for urinary protein excretion of > 250 mg/24h.

Nephrotic syndrome (NS): Defined as a value for urinary protein excretion of > 3 g/24h, se­rum albumin (s. alb) < 3g/dL, serum choles­terol (s. chol) > 300 mg/dL.

Nephritic syndrome: Defined as a value for protienuria > 0.5 g/d and active urinary sedi­ments (> 5 erythrocyte/HPF or casts). [9]

Complete remission (CR): Defined as a value for urinary protein excretion of < 0.3 g/24h, normal urinary sediment, s. alb, and value of Cr. was 15% or < from the baseline value.

Partial remission (PR): Defined as a value of urinary protein excretion between 0.3 and 2.9 g/24h, s. alb ≥ 3 g/dL, and stable renal function.

Treatment failure: Defined as a value for uri­nary protein excretion that remained at or above ≥ 0.3 g/24h and s. alb ≤ 3g/dL, and an increase in s. Cr > 0.6 mg/dL or 15% above the base­ line value. [10]

Renal biopsy was repeated if there was an in­crease in s. Cr or persistent proteinuria

Severe lupus nephritis: Diagnosis of severe nephritis was based on the presence of pro­liferation and/or necrosis in greater than 50% of glomeruli with or without concominent mem­branous glomerulonephritis. [11]

Renal flare: Defined using criteria of Moroni et al [27] which include:

  1. Nephritic flare: an increase in s. Cr. of at least 30% above the basal value with a nephritic urinary sediment.
  2. Protienuric flare: defined as an increase in proteinuria by at least 2 g /day or doubling if basal proteinuria is above 3.5 g/d with­ out modification of s. Cr.
Poor renal outcome: defined as doubling in s. Cr. values for a period of at least 6 months. [12]

Lupus duration: Defined as the time from a patient's first documented lupus diagnosis to the renal biopsy diagnosis of SLE. [13]

Activity and chronicity index (AI/CI): The ac­tivity index consisted of the total 4 features each evaluated on zero to 4 + semiquatitive scale: glomerular leucocyte infiltration, inters­titial inflammation, glomerular karyorrhexis and fibrinoid necrosis, and cellular crescent. The la­tter two features were each weighed by a fac­tor of two, for a maximum activity index score of 24. The chronicity index was determined by the score of glomerular sclerosis, interstitial fibrosis, and tubular atrophy each quantitated on a zero to 4 + scale for a maximum chro­nicity index of 12. [14]

Database: The data collected on the patients included age at time of onset of SLE, age at time of nephritis, sex, hypertension (HTN), com­pliments (C3,C4), anti-dsDNA antibody (anti­DNAab), proteinuria, s. Cr, creatinine clearance at diagnosis, activity index and chronicity in­dex in renal biopsy, prior to the therapy etc.

Follow up: Patients were followed up monthly for 6 months then quarterly for two years or more, and more frequently if needed. Hemog­lobin, total leukocyte count (TLC), blood urea, s. Cr, total serum protein (TSP), serum albumin (s. alb), 24h urinary protein excretion in gram per day (g/d) and creatinine clearance every month, liver function test (LFT) and lipid pro­file at baseline and every 3rd month and C3, C4 and ds DNA antibody at baseline and every 6 th month interval.

Outcome measures

The primary study outcome was the response to the treatment defined by:

  1. Percentage of patients who achieved renal remission.
  2. The number of non-reponders (> 10 RBC/HPF, cellular cast, proteinuria > 1 g/d, doub­ling of creatinine)
  3. Percentage of adverse events.
Secondary outcome:

  1. Progress to ESRD.
  2. Doubling of s. Cr.
  3. Renal relapse.
Adverse effects noted included major Infec­tions, herpes Zoster, neutropenic fever, prema­ture ovarian failure, avascular necrosis, malig­nancy, hemorrhagic cystitis, cataracts, and death.

Ovarian failure: Defined as sustained ame­norrhea occurring before 45 years of age. [26]

Serious infection: Defined as any infection needed intravenous antibiotics or hospitalization.

Treatment protocol

The patients received 6 monthly pulses of cyclophosphamide for induction followed by quarterly pulses for at least one additional year. The standard initial dose of pulse cyclophos­phamide was 0.75-1 g/m 2 BSA in patients with normal renal function. The initial dose was re­duced to 0.50 g/m 2 if the estimated creatinine clearance was less than 40 mL/min, or in obese patient (BMI > 35) to diminish the risk of toxi­city. The patients receive one liter of intrave­nous fluid (0.45 percent or 0.9 percent saline) over a 2 to 4- hour period. Cyclophosphamide was then reconstituted and diluted in 150 mL of saline and infused over one hour. All the pa­tients were instructed to drink at least one liter of fluid every 6 to 8 hours and void as frequently as possible for 24 hours. Nausea was nearly uni­versal in the treated patients; those with rela­tively mild nausea were received prochlorpe­razine 25 mg orally every four hours as nee­ded. For severe vomiting, the patients were treated as per the current NIH protocol that re­commends prophylactic dexamethasone (10 mg, four hours after infusion) and ondansetron (4 to 8 mg; four, eight and 12 hours after infu­sion). The dose of cyclophosphamide was re­duced to 0.5 gm/m 2 if a higher dose was not tolerated. The patients had WBC count before every injection of cyclophosphamide and cy­clophosphamide continued if WBC count was 4500/cumm or more. If the WBC count was less than 4000/cumm, the injection was de­ferred for a week and the test was repeated. Repeated injections were administered when the count was above 4000/cum. Mesna (2-Mer­captoethane sulphonate) at 20% of the cyclo­phosphomide dose was infused i.v. before cy­clophosphomide administration and every 3h thereafter for a total of 4 doses.

Oral prednisolone (0.5 mg/kg/day) was pres­cribed for 3 months or till remission was ac­hieved. Then, the dose of prednisolone was gra­dually reduced to 0.5 mg/kg on alternate days over 6-9 months. After 1 year, the dose was further tapered to a maintenance dose of 0.3 mg/kg/alternate day.

   Statistical Analysis Top

Statistical analysis was done using microsoft excel software Student t' test and P value < 0.05 was considered as significant

   Results Top

A total of 38 patients were included in this study from January 1998 to December 2002. Six patients were excluded from the analysis due to loss of follow-up and 3 patients expired during the initial cycles of therapy. Twenty-­nine cases were included in the final analysis.

[Table 1] shows the clinical, biochemical and pathological characteristics of these patients. The mean age group at the time of renal biopsy was 25.6 + 6.70 (range: 10-40) years, and there were 25 females and 4 males. The mean interval between the diagnosis of SLE and lupus nephritis was 24.2 ± 18.5 (range: 1­60) months. Out of 29 patients, 22 (75.8%) had class IV lupus nephritis, 6 (20.7%) patients had class III, and one (3.4%) had class Vd lupus nephritis. The mean interval of follow-up was 16.6 (8-50) months. Ten patients (34.5%) pre­sented as nephrotic syndrome, 9 (31.0%) as nephritis, 1 (3.40%) as rapidly progressive renal failure (RPRF), and 3 (10.34%) patients pre­sented as pyrexia of unknown origin (PUO). There were 18 (47.1%) patients who had renal insufficiency at presentation and dyslipidemia was present in 27 (71.02%) patients.

The baseline data for non-responding patients to treatment did not differ from the data of res­ponders except hypertension and renal insuffi­ciency, which were more common in the non­responders group.

[Table 2] shows the parameters of the patients who responded and non-responders at the end of the study. After a mean follow up of 15.75 months, out of 29 patients 13 (44.8%) had achieved CR, 7 (24.2%) PR and 9 (31.0%) were NR.

[Table 3] shows the outcome of the 3 subgroups of the study patients. All the patients in the CR group maintained stable s. Cr throughout the follow-up period, while doubling of s. Cr was observed in 77.8% of the patients in the NR group and 14.3% of those in the PR group. None of the patients in the NR group pro­gressed to ESRD till the end of the follow-up period.

The number of renal flares was the highest in the NR (55.5%) group. There were no diffe­rences in the cumulative doses of cyclophos­phamide among the 3 groups (mean 0.9 g). The average time to achieve CR was 6 months. The NR group had a mean baseline s. Cr > 2 mg/dL, whereas the mean of s. Cr was normal in the responder group. We observed a persis­tent reduction of proteinuria and improvement of s. Alb in the responders group from the 3 rd cycle onward.

On histopathological analysis, there were no differences of frequencies of the histological classes of SLE among the responders and the NR except chronicity index was > 3 in the latter group. Out of 9 the NR patients, 8 had a diffuse progressive glomerulonephritis (DPGN). Repeated renal biopsies were performed in 7 cases. Five patients underwent histopathologic transformation; 3 converted from class IV to class V, and all of them achieved complete response subsequently on ponticelli regimen. Two patients converted to class IV and later received pre ESRD management.

There were some complications related to the­rapy; 2 patient had major infections, 2 herpes Zoster, 2 avascular necrosis of the hip (AVN), 1 cataract, and one amenorrhea. No cases expe­rienced hemorrhagic cystitis till the end of the follow-up period. Most of the patients had vo­miting and nauseas during treatment. Alopacia was the most common side effect we ob­served. One patient became pregnant two times during the treatment period and MTP (medical termination of pregnancy) was done at 11 weeks in both times. This patient achieved par­tial remission at the end of follow-up period.

   Discussion Top

In this study, we analyzed prospectively the response of severe lupus nephritis treated with IV cyclophosphomide and predictors of poor outcomes.

The optimum treatment for severe lupus ne­phritis is unclear because large prospective ran­domized trials are lacking. [15] Boumpus et al observed that an extended course of pulse cy­clophosphomide is more effective than 6 mo­nths of pulse methyl prednisolone in preser­ving renal function and addition of a quarterly maintenance regimen to monthly pulse cyclo­phosphomide reduces the rate of exacerbations. [3]

Gourley et al observed CR in 48% of patients, while 29% failed to respond to treatment; doub­ling of s. Cr occurred in only 5% and only 3% progressed to ESRD. Our data is comparable to this study. [16] Ioannidis et al found CR in 78% of patients, but the duration of treatment in this study was 3 years. [17] Korbet et al observed CR in 43% cases treated with high dose predniso­lone and oral CYC. [18] In G.G. Illei study of DPGN patients, CR was achieved in 70% and PR in 11%. [19]

We observed that HTN, renal insufficiency, and higher chronicity index at baseline were the predictors of poor outcome though statis­tically insignificant. G.G. Illei et al [19] found s. Cr > 2 mg/dL, a severe nephritic flare, and a high chronicity index at baselinet,but not acti­vity index, were associated progression to ES­RD. We also observed similar results in our study as well as others. [9],[12],[13],[17],[20]

Mosca et al [12] did not find patient's sex, age or any other serological/clinical variables to be correlating with occurrence of flare. In our stu­dy, no significant differences observed in sex, age, serological data among responders and non­responders. Similarly, in the study of Korbet et al, serological markers failed to predict clinical outcome. [18]

Korbet et al [18] and Appel et al [14] showed that the induction of clinical remission of renal dys­function is predictive of improved long-term prognosis, even in with most severe form of lupus nephritis. Moreover, Baldwin et al [21] ob­served that remission of renal disease achieved in only 17% of patients with severe LN in whom s. Cr levels > 2 mg/dL and 47% of similar patients with s. Cr levels < 2 attained remission. We also found comparable observations in our study patients.

On repeat renal biopsy in the NR group (bio­psy was done in 7out of 9 cases of DPGN), we observed transformation of histology in 5 ca­ses; 2 cases showed progressive renal dysfunc­tion with high activity index. Out of 5 trans­formations, 3 cases transformed to membra­nous lupus nephritis (class V) and 2 cases trans­formed to Class VI. A number of studies have evaluated repeated renal biopsy in SLE; although transition from one form of lupus to another occurred, they were not the role. [21],[22],[23]

In the study of Chang Woo et al [24] out of 21 repeat biopsy cases of DPGN, only 3 cases (14%) underwent histopathologic transforma­tion. Seven cases showed progression to more severe lesion with an increase in s. Cr and blood pressure. These results are comparable to ours. In addition, our study suggests that glomerular activity and interstitial volume density at the initial biopsy are useful histological indices for predicting the renal out-come in patients with DPGN.

Cumulative dose and advancing age have been identified as risk factors for cyclophos­phamide induced ovarian failure. [25] A prolonged course of IVC is associated with more side effects. The profile of side effects was com­parable in our study with that most studies. [3],[15],[16],[19],[20],[13],[26]

In summary, our study showed that long courses of pulse cyclophosphomide are effec­tive in achieving remission in severe lupus nephritis with minimal side effects. High chro­nicity index and renal insufficiency at presen­tation are considered as bad prognostic factors. However, a long follow-up study of these pa­tients is required.

   Acknowledgment Top

Authors thanks all staff, residents and faculty of the Department of Nephrology for their help during the study period.

   References Top

1.Bakke AC, Kirkland PA, Kitridou RC, et al. T lymphocyte sub-sets in systemic lupus erythe­matosus. Arthritis Rheum 1983;26(6):745-50.  Back to cited text no. 1      
2.Cameron JS. The treatment of lupus nephritis. Pediatr Nephrol 1989;3:350-62.  Back to cited text no. 2  [PUBMED]    
3.Boumpas DT, Austin HA 3rd, Vaughn EM et al. Controlled trial of pulse methylprednisolone versus two regimens of pulse cyclophospha­mide in severe lupus nephritis. Lancet 1992; 340:741-5.  Back to cited text no. 3      
4.Austin HA, Klippel JH, Balow JE, le Riche NG. Therapy of lupus nephritis. Controlled trial of prednisone and cytotoxic drugs. N Engl J Med 1986;314:614-9  Back to cited text no. 4      
5.Chan TM, Li FK, Tang CS, et al. Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis. N Engl J Med 2000;343:1156-62.  Back to cited text no. 5  [PUBMED]    
6.Balow JE. Choosing treatment for proliferative lupus nephritis. Arthritis Rheum 2002;46:1981-3.  Back to cited text no. 6  [PUBMED]    
7.Balow JE, Boumpus DT, Austin HA 3 rd , Lupus Nephritis; Therapy in Nephrology& HTN com­panion to Brenner, 5th edition, page-131  Back to cited text no. 7      
8.Vivette D. D'Agathi VD. Renal Disease in SLE. Heptinstall's pathology 5th edn (Vol.1) p. 571.  Back to cited text no. 8      
9.Ciruelo E, de la Cruz J, Lopez I, Gomez-Reino JJ. Cumulative rate of relapse of lupus neph­ritis after successful treatment with cyclo­phosphamide. Arthritis Rheum 1996;39(12): 2028-34.  Back to cited text no. 9      
10.Chan M, Li KF, Colin SO, et al. Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis. N Engl J Med 2000;343:1156-62.  Back to cited text no. 10      
11.Lewis EJ, Hunsicker LG, Lan SP, Rohde RD. A controlled trial of plasmapheresis therapy in severe lupus nephritis. The Lupus Nephritis Collaborative Study Group. N Engl J Med 1992;326:1373.  Back to cited text no. 11      
12.Mosca M, Bencivelli W, Neri R. Renal flares in 91 SLE patients with diffuse proliferative glo­merulonephritis. Kidney int 2002;61:11502-9.  Back to cited text no. 12      
13.Cyclophosphamide therapy for lupus nephritis: Poor renal survival in black American. Kidney Int 1997;51:1188-95.  Back to cited text no. 13      
14.Appel GB, Cohen DJ, Pirani CL, Meltzer JI, Estes D. Long-term follow-up of lupus nephritis: A study based on the WHO classification. Am J Med 1987;83:877-85.  Back to cited text no. 14  [PUBMED]    
15.Mok CC, Ho CT, Chan KW, Lau CS, Wong RW. Outcome and prognostic indicators of diffuse proliferative lupus glomerulonephritis treated with sequential oral cyclophosphamide and azathioprine. Arthritis Rheum 2002;46(4): 1003-13.  Back to cited text no. 15      
16.Gourley MF, Austin HA 3rd, Scott D, et al. Methylprednisolone and cyclophosphamide, alone or in combination, in patients with lupus nephritis, A randomized, controlled trial. Ann Intern Med 1996;125(7):549-57.  Back to cited text no. 16      
17.Ioannidis JP, Boki KA, Katsorida ME. Remi­sion, relapse, and re-remission of proliferative lupus nephritis treated with cyclophosphamide. Kidney Int 2000;57(1):258-64.  Back to cited text no. 17      
18.Korbet SM, Lewis EJ, Schwartz MM, et al. Factors predictive of outcome in severe lupus nephritis. Lupus Nephritis Collaborative Study Group. Am J Kidney Dis 2000;35:904-14.  Back to cited text no. 18      
19.Illei GG, Takada K, Parkin D, et al. Renal flares are common in patients with severe prolife­rative lupus nephritis treated with pulse immu­nosuppressive therapy. Arthritis Rheumat 2002; 46(4):995-1002.  Back to cited text no. 19      
20.Illei GG, Austin HA 3rd, Crane M, Collins L, Gourley MF. Combination therapy with pulse cyclophosphamide plus pulse methylpredniso­lone improves long-term renal outcome with­out adding toxicity in patients with lupus neph­ritis. Ann Intern Med 2001;135:248-57.  Back to cited text no. 20      
21.Baldwin DS, Gluck MC, Lowenstein J. Lupus nephritis. Clinical course as related to morpho­logic forms and their transitions. Am J Med 1977;62(1):12-30.  Back to cited text no. 21      
22.Baldwin DS. Clinical usefulness of the mor­phological classification of lupus nephritis. Am J Kidney Dis 1982;2(Suppl 1):142-9.  Back to cited text no. 22      
23.McCluskey RT. The value of the renal biopsy in lupus nephritis. Arthritis Rheum 1982;25: 867-75.  Back to cited text no. 23  [PUBMED]    
24.Yoo CW, Kim MK, Lee HS. Predictors of renal outcome in diffuse proliferative lupus nephropathy: Data from repeat renal biopsy. Nephrol Dial Transplant 2000;15:1604-8.  Back to cited text no. 24  [PUBMED]    
25.Boumpas DT, Austin HA, Vaughn EM. Risk of sustained amenorrehea in patients with sys­temic lupus eythematosus receiving pulse cyclo­phosphamide. Ann Intern Med 1993;119:366­-9.  Back to cited text no. 25      
26.Malaviya AN, Singh RR, Sindhwai R, et al. Intermittent intravenous pulse cyclophospha­mide treatment in systemic lupus erythema­tosus. Indian J Med Res Br 1992;96:101-8.  Back to cited text no. 26      
27.Moroni G, Quaglini S, Maccario M, et al. Nephritic flares are predictors of bad long-term renal outcome in lupus nephritis. Kidney Int 1996;50:2047-53.  Back to cited text no. 27  [PUBMED]    

Correspondence Address:
Uttara Das
Assistant Professor of Nephrology, Nizam's Institute of Medical Sciences, Panjagutta, Hyderabad 500082, Andhra Pradesh
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Source of Support: None, Conflict of Interest: None

PMID: 20228536

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