• 1.

    Herwaldt BL, 1999. Leishmaniasis. Lancet 354: 11911199.

  • 2.

    Efstratiadis G, Boura E, Giamalis P, Mandala E, Leontsini M, Tsiaousis G, Memmos D, 2006. Renal involvement in a patient with visceral leishmaniasis. Nephrol Dial Transplant 21: 235236.

    • Search Google Scholar
    • Export Citation
  • 3.

    Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, Wasunna MK, Bryceson AD, 2002. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis 2: 494501.

    • Search Google Scholar
    • Export Citation
  • 4.

    Camargo LB, Langoni H, 2006. Impact of leishmaniasis on public health. Trop Dis 12: 527548.

  • 5.

    Dantas-Torres F, Brandão-Filho SP, 2006. Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo 48: 151156.

    • Search Google Scholar
    • Export Citation
  • 6.

    Boakye DA, Wilson MD, Kweku M, 2005. A review of leishmaniasis in west Africa. Ghana Med J 39: 9497.

  • 7.

    Salgado Filho N, Ferreira TMAF, Costa JML, 2003. Involvement of the renal function in patients with visceral leishmaniasis (kala-azar). Rev Soc Bras Med Trop 36: 217221.

    • Search Google Scholar
    • Export Citation
  • 8.

    Oliveira AL, Brustoloni YM, Fernandes TD, Dorval ME, Cunha RV, Bóia MN, 2009. Severe adverse reactions to meglumine antimoniate in the treatment of visceral leishmaniasis: a report of 13 cases in the southwestern region of Brazil. Trop Doct 39: 180182.

    • Search Google Scholar
    • Export Citation
  • 9.

    Daher EF, Evangelista LF, Silva Júnior GB, Lima RS, Aragão EB, Arruda GA, Galeano NM, Mota RM, Oliveira RA, Silva SL, 2008. Clinical presentation and renal evaluation of human visceral leishmaniasis (kala-azar): a retrospective study of 57 patients in Brazil. Braz J Infect Dis 12: 329332.

    • Search Google Scholar
    • Export Citation
  • 10.

    Beltrame A, Arzese A, Camporese A, Rorato G, Crapis M, Tarabini-Castellani G, Boscutti G, Pizzolitto S, Calianno G, Matteelli A, Di Muccio T, Gramiccia M, Viale P, 2008. Acute renal failure due to visceral leishmaniasis by Leishmania infantum successfully treated with a single high dose of liposomal amphotericin B. J Travel Med 15: 358360.

    • Search Google Scholar
    • Export Citation
  • 11.

    Navarro M, Bonet J, Bonal J, Romero R, 2006. Secondary amyloidosis with irreversible acute renal failure caused by visceral leishmaniasis in a patient with AIDS. Nefrologia 26: 745746.

    • Search Google Scholar
    • Export Citation
  • 12.

    Rollino C, Bellis D, Beltrame G, Basolo B, Montemagno A, Bucolo S, Ferro M, Quattrocchio G, Coverlizza S, Quarello F, 2003. Acute renal failure in leishmaniasis. Nephrol Dial Transplant 18: 19501951.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ricci Z, Cruz D, Ronco C, 2008. The RIFLE criteria and mortality in acute kidney injury: a systematic review. Kidney Int 73: 538546.

  • 14.

    Lima Verde FA, Lima Verde IA, Silva Junior GB, Daher EF, Lima Verde EM, 2007. Evaluation of renal function in human visceral leishmaniasis (kala-azar): a prospective study of 50 patients from Brazil. J Nephrol 20: 430436.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pisoni R, Wille KM, Tolwani AJ, 2008. The epidemiology of severe acute kidney injury. From BEST to PICARD, in acute kidney injury: new concepts. Nephron Clin Pract 109: c188c191.

    • Search Google Scholar
    • Export Citation
  • 16.

    Lima Verde FAA, Lima Verde FA, Daher EF, Santos GM, Sabóia Neto A, Lima Verde EM, 2009. Renal tubular dysfunction in human visceral leishmaniasis (kala-azar). Clin Nephrol 71: 492500.

    • Search Google Scholar
    • Export Citation
  • 17.

    Weisinger JR, Pinto A, Velasquez GA, Bronstein I, Dessene JJ, Duque JF, Montenegro J, Tapanes F, de Rousse AR, 1978. Clinical and histological kidney involvement in human kala-azar. Am J Trop Med Hyg 2: 357359.

    • Search Google Scholar
    • Export Citation
  • 18.

    Martinelli R, Lourenzo R, Rocha H, 1986. Absence of clinical abnormalities suggesting renal involvement during long-term course of visceral leishmaniasis. Rev Soc Bras Med Trop 19: 209212.

    • Search Google Scholar
    • Export Citation
  • 19.

    Tafuri WL, Michalik MSM, Dias M, Genaro O, Leite VHR, Barbosa AJA, Bambirra EA, Costa CA, Melo MN, Mayrink W, 1989. Estudo ao microscópio óptico e eletrônico do rim de cães natural e experimentalmente infectados com Leishmania chagasi. Rev Inst Med Trop Sao Paulo 31: 139145.

    • Search Google Scholar
    • Export Citation
  • 20.

    Prasad LS, Sen S, Ganguly SK, 1992. Renal involvement in kala-azar. Indian J Med Res 95: 4346.

  • 21.

    Polli A, Abramo F, Mancianti F, Nigro M, Pieri S, Bionda A, 1991. Renal involvement in canine leishmaniasis. A light microscopic, immunohistochemical and electron microscopic study. Nephron 57: 444452.

    • Search Google Scholar
    • Export Citation
  • 22.

    Dutra M, Martinelli M, Carvalho EM, Rodrigues LE, Brito E, Rocha H, 1985. Renal involvement in visceral leishmaniasis. Am J Kidney Dis 6: 2227.

  • 23.

    Duvic C, Nedelec G, Debord T, Herody M, Didelot F, 1999. Important parasitic nephropathies: update from the recent literature. Nephrologie 20: 6574.

    • Search Google Scholar
    • Export Citation
  • 24.

    Chaigne V, Knefati Y, Lafarge R, Bronner J, McGregor B, Fouque D, Sabatier JC, 2004. A patient with visceral leishmaniasis and acute renal failure in necrotizing glomerulonephritis. Nephrologie 25: 179183.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ben Salem L, Khiari K, Turki S, Cherif L, Ali IH, Maazoun I, Ben Moussa F, el Younsi F, Ben Abdallah N, Ben Maïz H, 2003. Obstructive acute renal failure revealing visceral leishmaniasis in a diabetic patient. Nephrologie 24: 9599.

    • Search Google Scholar
    • Export Citation
  • 26.

    Clevenberg P, Okome MN, Benoit S, Bendini JC, De Salvador F, Elbeze M, Cassuto E, Marty P, Dellamonica P, 2002. Acute renal failure as initial presentation of visceral leishmaniasis in an HIV-1 infected patient. Scand J Infect Dis 34: 546547.

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    Berdichevski RH, Luis LB, Crestana L, Manero RC, 2006. Amphotericin B-related nephrotoxicity in low-risk patients. Braz J Infect Dis 10: 9499.

  • 28.

    Bagnis CI, Deray G, 2002. Amphotericin B nephrotoxicity. Saudi J Kidney Dis Transpl 13: 481491.

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    Olliaro PL, Guerin PJ, Gerstl S, Haaskjold AA, Rottingen JA, Sundar S, 2005. Treatment options for visceral leishmaniasis: a systematic review of clinical studies done in India, 1980–2004. Lancet Infect Dis 5: 763774.

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    Werneck GL, Batista MS, Gomes JR, Costa CH, 2003. Prognostic factors from visceral leishmaniasis in Teresina, Brazil. Infection 31: 174177.

 
 
 
 

 

 
 
 

 

 

 

 

 

 

Risk Factors for Acute Kidney Injury in Visceral Leishmaniasis (Kala-Azar)

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  • 1 Post-Graduation Program in Medical Sciences, Department of Internal Medicine, School of Medicine, Federal University of Ceará; Division of Nephrology, Department of Internal Medicine, School of Medicine, Walter Cantídio University Hospital, Federal University of Ceará; Department of Statistics, Science Center, Federal University of Ceará; Discipline of Nephrology, School of Medicine, University of Fortaleza, Fortaleza, Ceará, Brazil

The aim of this study was to investigate the factors associated with acute kidney injury (AKI) in patients with visceral leishmaniasis (VL). The study patients had a diagnosis of VL and were admitted to a tertiary hospital. A multivariate analysis was performed to analyze the risk factors for AKI. A total of 224 patients were included. The mean age was 36 ± 15 years. AKI was observed in 33.9% of cases. Risk factors associated with AKI were male gender (odds ratio [OR] = 2.2; P = 0.03), advanced age (OR = 1.05; P < 0.001), and jaundice (OR = 2.9; P = 0.002). There was an association between amphotericin B use and AKI (OR = 18.4; P < 0.0001), whereas glucantime use was associated with lower incidence of AKI compared with amphotericin B use (OR = 0.05; P < 0.0001). Mortality was 13.3%, and it was higher in AKI patients (30.2%). Therefore, factors associated with AKI were male gender, advanced age, and jaundice. Amphotericin B was an important cause of AKI in VL.

Introduction

Visceral leishmaniasis (VL) is an endemic disease in tropical and subtropicals countries, as well as in southern Europe, affecting 1–2 million individuals and causing ~500,000 new cases and 5,000 deaths each year.14 It is a vector-borne disease caused by different species of Leishmania parasites.1,5,6 As a consequence of the intense parasitism of the reticular endothelial system, kala-azar patients present with marked anemia, leukopenia, and thrombocytopenia, as well as increased plasmatic levels of gamma globulins.7

Renal abnormalities caused by Leishmania have been well-documented in experimental animal studies and are comprised of interstitial and glomerular abnormalities.7 There have been few human studies on renal function in VL. The main pathophysiological mechanism by which VL affects the kidneys probably includes immune-complex disease, which is similar to other parasitic infections such as malaria and schistosomiasis. Most patients present proliferative glomerulonephritis and interstitial nephritis.7 Studies on acute kidney injury (AKI) in VL are rare. Possible causes for AKI in VL include drug toxicity, associated infections, hemodynamic abnormalities, and VL itself.812

The aim of this study was to investigate the prevalence, clinical manifestations, and risk factors associated with AKI in patients with VL.

Patients and Methods

The study was carried out from December 2002 to December 2008 and included patients with a clinical and laboratory diagnosis of VL admitted to São José Hospital of Infectious Diseases in the city of Fortaleza, state of Ceara, Brazil. All patients had the diagnosis of VL based on the identification of amastigotes in smears obtained from sternal bone-marrow aspirate, and some patients underwent rK39 antigen tests during active infection. A standardized case-investigation form was used to complete demographical, epidemiological, clinical, and laboratory data. Patients with age ≤ 14 years, previous renal insufficiency, arterial hypertension, diabetes mellitus, and co-morbidities that could affect renal function during the study were excluded.

Definitions.

Oliguria was considered to be present when the urinary volume was < 400 mL/day despite appropriate fluid replacement. Hypotension was defined as mean arterial blood pressure (MAP) < 60 mmHg, and therapy with vasoactive drugs was initiated when MAP was lower than 60 mmHg. Systolic blood pressure (SBP) and diastolic blood pressure (DBP) at admission were also analyzed. Metabolic acidosis was defined as pH < 7.35 and arterial bicarbonate < 20 mEq/L; coagulation abnormalities were defined as platelet count < 100 × 103/mm3 and prothrombin time lower than 65%. Hypoalbuminemia was defined as serum albumin < 3.5 g/dL, anemia was defined as Hb ≤ 12 g/dL, and leukopenia was defined as white blood cells (WBC) < 3,500 mm3.

Group definition.

The population was divided in two groups: patients with normal renal function (non-AKI) and patients with AKI; these groups were defined according to creatinine levels by applying the RIFLE (risk, injury, failure, loss, end-stage renal disease) criteria13 and were established during hospital stay. We compared these two groups to investigate the differences in clinical manifestations, laboratory features, and risk factors for AKI.

Protocol of treatment.

Patients with VL were treated with intravenous injections of pentavalent antimonials (Glucantime; Sanofi-Aventis, São Paulo, Brazil) 20 mg/kg daily for 20–40 consecutive days, and in severe cases, amphotericin B was given at a 7–20 mg/kg total dose for up to 20 days. None of the patients included in the study received the lipid formulation of amphotericin B. Patients with secondary bacterial infections received antibiotic therapy.

Ethics.

The study was approved by the Ethics Committee of São José Hospital of Infectious Diseases.

Statistical analyses.

The results and means ± standard deviations for quantitative variables are presented in Tables 14. The univariate and multivariate analyses of the clinical and laboratory data were performed using the SPSS package version 10.0 (SPSS Inc., Chicago, IL) and Epi Info version 6.04b (Centers for Disease Control and Prevention, Atlanta, GA) software. Comparison of parameters of the two groups (AKI and non-AKI) was carried out through Student's t test and Fisher's exact test. A logistic regression model was used for the quantitative variables. Adjusted odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. A multivariate logistic regression analysis was performed to assess the possible risk factors for AKI. The factors included in the multivariate model were those that showed a significance level < 20% at the univariate analysis (Mann–Whitney test and χ2 test). P values < 0.05 were considered statistically significant.

Results

A total of 224 patients were included in the study. Mean age was 36 ± 15 years (range = 15–84 years), and 76.8% of the patients were males. Mean hospital stay was 18 ± 11 days (range = 1–69 days). The main signs and symptoms at admission were fever (90.6%), splenomegaly (87.1%), hepatomegaly (77.2%), asthenia (61.6%), anorexia (58.5%), coughing (41.5%), headache (34.8%), abdominal pain (34.8%), diarrhea (28.6%), dyspnea (21.4%), jaundice (19.6%), and edema (18.8%).

AKI was observed in 76 patients (33.9%), and 85.5% of these patients were males. Of the 76 patients who developed AKI, 26 (34.2%) had serum creatinine > 1.4 mg/dL at admission, 39 patients (51.3%) developed AKI within a mean time period of 10 days after the start of treatment with amphotericin B, 7 (9.2%) developed AKI after the start of treatment with glucantime and 4 (5.3%) developed AKI because of co-morbidities as summarized in Figure 1. Oliguria was observed in 6.5% of patients with AKI. The comparison between AKI and non-AKI patients is summarized in Tables 1 and 2. AKI patients presented higher levels of urea, creatinine, potassium, direct bilirubins, and indirect bilirubins, as well as a higher number of WBCs. Sodium, HCO3, pCO2, albumin levels, platelets count, and prothrombin time were lower in AKI compared with non-AKI patients. The factors associated with AKI were male gender, advanced age, jaundice, and use of amphotericin B, and these results are summarized in Table 3.

Figure 1.
Figure 1.

AKI in patients with VL (kala-azar).

Citation: The American Society of Tropical Medicine and Hygiene 82, 3; 10.4269/ajtmh.2010.09-0571

The second choice of treatment for severe VL is amphotericin B, a nephrotoxic drug. We observed a significant association between the use of amphotericin B and AKI (P < 0.0001) in patients with the severe form of VL that did not respond to glucantime. AKI was observed in 39 patients using amphotericin B (82.9% of the patients receiving the drug, which corresponds to 17.4% of all studied patients). The percentage of patients that received glucantime and had AKI was 20.9%. All patients in the AKI group treated with amphotericin B had normal serum creatinine levels at admission. The use of glucantime was associated with a lower incidence of AKI (P < 0.0001) as shown in Table 4.

Overall mortality was 30 (13.3%). Mortality was significantly higher in AKI patients with 23 deaths (30.2%) compared with 7 deaths in the non-AKI group (3.1%; P < 0.0001). The causes of death were respiratory failure in 13 cases (43.4%), septic shock in 10 (33.3%), hepatic failure in 4 (13.3%), and kidney failure in 3 (10%). The risk factors for death were amphotericin B use (OR = 3.1; 95% CI = 1.36–7.0; P = 0.01), oliguria (OR = 9.94; 95% CI = 1.59–62.3; P = 0.02), jaundice (OR = 5.7; 95% CI = 2.5–13.0; P = 0.001), and dyspnea (OR = 17.9; 95% CI = 3.3–97.2; P = 0.001). Mortality was also higher among patients using amphotericin B (25.6% versus 9.7%; P = 0.003) as illustrated in Figure 2.

Figure 2.
Figure 2.

Use of amphotericin B and outcome in patients with VL.

Citation: The American Society of Tropical Medicine and Hygiene 82, 3; 10.4269/ajtmh.2010.09-0571

Discussion

Human VL is an endemic parasitic infection in Brazil that has reemerged, especially in peri-urban areas. Renal involvement is considered rare, presenting as hematuria, proteinuria, or renal-function impairment.2 There is little information on AKI in VL. A prospective study showed renal impairment in only 1 of 11 patients (11%) when considering serum creatinine (Scr) levels > 1.4 mg/dL.7 The present study found a higher incidence of AKI (33.9%) in patients with a confirmed diagnosis of VL.

In a recent study carried out by our group, AKI (considered as serum creatinine levels higher than 1.3 mg/dL) was found in 26.2% of 57 patients with VL.9 Lima Verde and others14 in a cross-sectional study of 50 consecutive patients with visceral leishmaniasis, also carried out in our region, found a decreased glomerular filtration rate in 28% of the cases; this rate was attributed to fluid loss, volume contraction, and immunologic glomerular disease.

In the present study, AKI was more frequent in male patients, and this is in accordance with previous studies.15 The analysis of signs and symptoms showed that dyspnea, edema, jaundice, and oliguria were more frequent in patients with AKI. The laboratory evaluation showed higher levels of urea, creatinine, potassium, direct bilirubins, and indirect bilirubins, as well as a higher WBC count in AKI patients. Sodium and albumin levels, platelet count, and prothrombin time were lower in AKI patients, showing higher disease severity in patients with AKI. HCO3 and pCO2 levels were also lower in patients with AKI, suggesting a high incidence of metabolic acidosis, which could be secondary to renal dysfunction. Decreased titratable acidity was observed in 64% of patients with VL in a recent study in our region, as well as decreased ammonia urinary excretion in 30% of cases. Complete distal renal-tubular acidosis was observed in 30% of patients, and an incomplete form was found in 34%.14 In a recent prospective study including 55 patients with VL, hypoalbuminemia, hypergammaglobulinemia, and increased serum levels of IgG and β2-microglobulins were found in all patients.16 Increased albumin excretion was found in 44% of cases, and β2-microglobulin excretion was elevated in all cases. Other important abnormalities observed were hyponatremia (94.6%), hypomagnesemia (41.8%), hypocalcemia (32%), hypokalemia (26%), hypochloremia (27.2%), and hypouricemia (14.3%).16

Hematuria was seen in 4.5% of cases, even in patients without AKI, suggesting a possible glomerular involvement. Urinary-sediment alterations and decreased renal function have been described in patients with VL.17,18 In a prospective study of 50 patients with VL, urinary-sediment alterations with hematuria and leukocyturia were found in 51% of the studied cases. Slightly increased urinary-protein excretion was observed in 24-hour urine samples from 57.1% of these patients. A high percentage of urinary abnormalities, including macroscopic hematuria (45.4%), proteinuria (90.9%), and leukocyturia (54.5%), were observed in a prospective study of 11 patients with VL from Brazil.7 Mesangial deposits, mesangial cell hyperplasia, and glomerular endothelial cell tumefaction have been found in histopathological studies of patients with VL and in dogs that were naturally infected.19,20 All patients submitted to autopsy presented mononuclear interstitial nephritis, edema, and focal tubular degeneration.21 Acute glomerulonephritis, nephrotic syndrome, acute interstitial nephritis, and renal failure have also been described in VL.2226

In the present study, the use of amphotericin B was an important risk factor for AKI in VL, and it was associated with an 18-fold increased risk of developing AKI. In a recent study with 48 patients receiving amphotericin B, AKI (defined as an increase of > 50% in basal creatinine levels) occurred in 31% of cases.27 Higher incidences of AKI secondary to the use of amphotericin B have been reported, with percentages as high as 80% of patients receiving this drug.28 In the present study, AKI developed in a high number of patients receiving amphotericin B (82.9%). Moreover, amphotericin B was also associated with a higher mortality rate, with 3-fold increased risk of death. AKI was significantly less frequent among patients using glucantime. Since 1940, the pentavalent antimony compounds sodium stibogluconate and meglumine antimoniate (glucantime) have been the mainstays of antileishmanial therapy.1,4,29 In the present study, meglumine antimoniate was the first-choice treatment used in > 88% of cases. New therapeutic options, including oral drugs such as miltefosine, are being considered, as shown in recent studies.3,29

In the present study, overall mortality was 13.3%, and it was significantly higher in AKI patients (30.2% versus 4.7%). There have been few studies on mortality in VL. In a previous study by our study group, the mortality rate was lower (5.2% of 57 study patients), and all deaths were associated with AKI.9 A study of prognostic factors conducted in Northeastern Brazil verified that severe anemia, fever lasting > 60 days, diarrhea, and jaundice were risk factors for death in VL.30 In the present study, the risk factors for mortality were amphotericin B use, oliguria, jaundice, and dyspnea. Mortality was also higher among patients using amphotericin B (25.6% versus 9.7%), and this could be caused by the higher severity of the disease in patients who required the use of amphotericin B (VL-associated resistant infection or VL-associated severe leukopenia and sepsis).

In conclusion, AKI is an important complication in VL that seems to increase mortality. The predictive factors associated with AKI were male gender, advanced age, and jaundice. Amphotericin B is an important cause of AKI in VL, showing that nephrotoxicity plays an important role in the pathogenesis of AKI in this disease. Mortality was higher in AKI patients.

Acknowledgments:

We are very grateful to the team of physicians, residents, medical students, and nurses from the São José Infection Disease Hospital for providing technical support to the development of this research and for the exceptional assistance provided to the patients. CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico; Brazilian National Scientific and Technological Development Council) provided grants for this research.

  • 1.

    Herwaldt BL, 1999. Leishmaniasis. Lancet 354: 11911199.

  • 2.

    Efstratiadis G, Boura E, Giamalis P, Mandala E, Leontsini M, Tsiaousis G, Memmos D, 2006. Renal involvement in a patient with visceral leishmaniasis. Nephrol Dial Transplant 21: 235236.

    • Search Google Scholar
    • Export Citation
  • 3.

    Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, Wasunna MK, Bryceson AD, 2002. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis 2: 494501.

    • Search Google Scholar
    • Export Citation
  • 4.

    Camargo LB, Langoni H, 2006. Impact of leishmaniasis on public health. Trop Dis 12: 527548.

  • 5.

    Dantas-Torres F, Brandão-Filho SP, 2006. Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo 48: 151156.

    • Search Google Scholar
    • Export Citation
  • 6.

    Boakye DA, Wilson MD, Kweku M, 2005. A review of leishmaniasis in west Africa. Ghana Med J 39: 9497.

  • 7.

    Salgado Filho N, Ferreira TMAF, Costa JML, 2003. Involvement of the renal function in patients with visceral leishmaniasis (kala-azar). Rev Soc Bras Med Trop 36: 217221.

    • Search Google Scholar
    • Export Citation
  • 8.

    Oliveira AL, Brustoloni YM, Fernandes TD, Dorval ME, Cunha RV, Bóia MN, 2009. Severe adverse reactions to meglumine antimoniate in the treatment of visceral leishmaniasis: a report of 13 cases in the southwestern region of Brazil. Trop Doct 39: 180182.

    • Search Google Scholar
    • Export Citation
  • 9.

    Daher EF, Evangelista LF, Silva Júnior GB, Lima RS, Aragão EB, Arruda GA, Galeano NM, Mota RM, Oliveira RA, Silva SL, 2008. Clinical presentation and renal evaluation of human visceral leishmaniasis (kala-azar): a retrospective study of 57 patients in Brazil. Braz J Infect Dis 12: 329332.

    • Search Google Scholar
    • Export Citation
  • 10.

    Beltrame A, Arzese A, Camporese A, Rorato G, Crapis M, Tarabini-Castellani G, Boscutti G, Pizzolitto S, Calianno G, Matteelli A, Di Muccio T, Gramiccia M, Viale P, 2008. Acute renal failure due to visceral leishmaniasis by Leishmania infantum successfully treated with a single high dose of liposomal amphotericin B. J Travel Med 15: 358360.

    • Search Google Scholar
    • Export Citation
  • 11.

    Navarro M, Bonet J, Bonal J, Romero R, 2006. Secondary amyloidosis with irreversible acute renal failure caused by visceral leishmaniasis in a patient with AIDS. Nefrologia 26: 745746.

    • Search Google Scholar
    • Export Citation
  • 12.

    Rollino C, Bellis D, Beltrame G, Basolo B, Montemagno A, Bucolo S, Ferro M, Quattrocchio G, Coverlizza S, Quarello F, 2003. Acute renal failure in leishmaniasis. Nephrol Dial Transplant 18: 19501951.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ricci Z, Cruz D, Ronco C, 2008. The RIFLE criteria and mortality in acute kidney injury: a systematic review. Kidney Int 73: 538546.

  • 14.

    Lima Verde FA, Lima Verde IA, Silva Junior GB, Daher EF, Lima Verde EM, 2007. Evaluation of renal function in human visceral leishmaniasis (kala-azar): a prospective study of 50 patients from Brazil. J Nephrol 20: 430436.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pisoni R, Wille KM, Tolwani AJ, 2008. The epidemiology of severe acute kidney injury. From BEST to PICARD, in acute kidney injury: new concepts. Nephron Clin Pract 109: c188c191.

    • Search Google Scholar
    • Export Citation
  • 16.

    Lima Verde FAA, Lima Verde FA, Daher EF, Santos GM, Sabóia Neto A, Lima Verde EM, 2009. Renal tubular dysfunction in human visceral leishmaniasis (kala-azar). Clin Nephrol 71: 492500.

    • Search Google Scholar
    • Export Citation
  • 17.

    Weisinger JR, Pinto A, Velasquez GA, Bronstein I, Dessene JJ, Duque JF, Montenegro J, Tapanes F, de Rousse AR, 1978. Clinical and histological kidney involvement in human kala-azar. Am J Trop Med Hyg 2: 357359.

    • Search Google Scholar
    • Export Citation
  • 18.

    Martinelli R, Lourenzo R, Rocha H, 1986. Absence of clinical abnormalities suggesting renal involvement during long-term course of visceral leishmaniasis. Rev Soc Bras Med Trop 19: 209212.

    • Search Google Scholar
    • Export Citation
  • 19.

    Tafuri WL, Michalik MSM, Dias M, Genaro O, Leite VHR, Barbosa AJA, Bambirra EA, Costa CA, Melo MN, Mayrink W, 1989. Estudo ao microscópio óptico e eletrônico do rim de cães natural e experimentalmente infectados com Leishmania chagasi. Rev Inst Med Trop Sao Paulo 31: 139145.

    • Search Google Scholar
    • Export Citation
  • 20.

    Prasad LS, Sen S, Ganguly SK, 1992. Renal involvement in kala-azar. Indian J Med Res 95: 4346.

  • 21.

    Polli A, Abramo F, Mancianti F, Nigro M, Pieri S, Bionda A, 1991. Renal involvement in canine leishmaniasis. A light microscopic, immunohistochemical and electron microscopic study. Nephron 57: 444452.

    • Search Google Scholar
    • Export Citation
  • 22.

    Dutra M, Martinelli M, Carvalho EM, Rodrigues LE, Brito E, Rocha H, 1985. Renal involvement in visceral leishmaniasis. Am J Kidney Dis 6: 2227.

  • 23.

    Duvic C, Nedelec G, Debord T, Herody M, Didelot F, 1999. Important parasitic nephropathies: update from the recent literature. Nephrologie 20: 6574.

    • Search Google Scholar
    • Export Citation
  • 24.

    Chaigne V, Knefati Y, Lafarge R, Bronner J, McGregor B, Fouque D, Sabatier JC, 2004. A patient with visceral leishmaniasis and acute renal failure in necrotizing glomerulonephritis. Nephrologie 25: 179183.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ben Salem L, Khiari K, Turki S, Cherif L, Ali IH, Maazoun I, Ben Moussa F, el Younsi F, Ben Abdallah N, Ben Maïz H, 2003. Obstructive acute renal failure revealing visceral leishmaniasis in a diabetic patient. Nephrologie 24: 9599.

    • Search Google Scholar
    • Export Citation
  • 26.

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Author Notes

*Address correspondence to Elizabeth De Francesco Daher, Rua Vicente Linhares, 1198, CEP 60270-135, Fortaleza, Ceara, Brazil. E-mails: ef.daher@uol.com.br or geraldobezerrajr@yahoo.com.br

Authors' addresses: Michelle J. C. Oliveira and Elizabeth F. Daher, Post-Graduation Program in Medical Sciences, Department of Internal Medicine, School of Medicine, Federal University of Ceará, Fortaleza, Rua Prof. Costa Mendes, 1608, 4 andar, CEP 60430-140, Ceará, Brazil, E-mails: mi_cavalcante@hotmail.com and ef.daher@uol.com.br. Geraldo B. Silva Júnior, Krasnalhia Lívia S. Abreu, Natália A. Rocha, Ana Valeska V. Garcia, Luiz F. L. G. Franco, and Elizabeth F. Daher, Division of Nephrology, Department of Internal Medicine, School of Medicine, Walter Cantídio University Hospital, Federal University of Ceará, Rua Cap. Francisco Pedro, 1290, CEP 60430-370, Fortaleza, Ceará, Brazil, E-mails: geraldobezerrajr@yahoo.com.br, kras_livinha@yahoo.com.br, natalia.a.rocha@gmail.com, and liganefroufc@yahoogrupos.com.br. Rosa M. S. Mota, Department of Statistics, Science Center, Federal University of Ceará, Campus do Pici, bloco 910, CEP 60455-760, Fortaleza, Ceará, Brazil, E-mail: rosa@ufc.br. Alexandre B. Libório, Discipline of Nephrology, School of Medicine, University of Fortaleza, Rua Desembargador Floriano Benevides Magalhães, 221, 3 andar, CEP 60811-690, Fortaleza, Ceará, Brazil, E-mail: alexandreliborio@yahoo.com.br.

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