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Research ArticleAccepted Article

A single APOL1 nephropathy variant increases risk of advanced lupus nephritis in Brazilians

Gisele Vajgel, Suelen Cristina Lima, Diego Jeronimo S. Santana, Camila B. L. Oliveira, Denise Maria N. Costa, Pamela J. Hicks, Maria Alina G. M. Cavalcante, Carl D. Langefeld, Lucila Maria Valente, Sergio Crovella, Gianna Mastroianni Kirsztajn, Barry I. Freedman and Paula Sandrin-Garcia
The Journal of Rheumatology November 2019, jrheum.190684; DOI: https://doi.org/10.3899/jrheum.190684
Gisele Vajgel
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Suelen Cristina Lima
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Diego Jeronimo S. Santana
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Camila B. L. Oliveira
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Denise Maria N. Costa
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Pamela J. Hicks
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Maria Alina G. M. Cavalcante
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Carl D. Langefeld
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Lucila Maria Valente
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Sergio Crovella
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Gianna Mastroianni Kirsztajn
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Barry I. Freedman
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Paula Sandrin-Garcia
From the Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Molecular Biology Laboratory, Keizo Asami Immunopathology Laboratory (LIKA), Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil; Division of Nephrology, Instituto de Medicina Integral Prof Fernando Figueira (IMIP), Recife, Pernambuco, Brazil; Division of Public Health Sciences, Department of Biostatistical Sciences; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA; Division of Nephrology, Department of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil; Center for Diabetes Research; Wake Forest School of Medicine, Winston- Salem, North Carolina, USA; Department of Internal Medicine, Section on Nephrology; Wake Forest School of Medicine, Winston-Salem, North Carolina, USA. Wake Forest University Health Sciences and BIF have rights to an issued US patent related to APOL1 genetic testing (www.apol1genetest.com). Dr. Freedman is a consultant for AstraZeneca Pharmaceuticals and Renalytix AI. Address correspondence to Dr. Gisele Vajgel (@gvajgel) Division of Nephrology, Hospital das Clinicas, Federal University of Pernambuco (UFPE), Recife, Pernambuco, Brazil Av. Prof Moraes Rego, 1235. Cidade Universitaria Recife PE – Brazil ZIP: 50670-901. E-mail: giselevajgel@hotmail.com
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Abstract

Objective Apolipoprotein L1 gene (APOL1) G1 and G2 renal-risk alleles (RRAs) are associated with end-stage renal disease (ESRD) in blacks with lupus nephritis (LN). The present study determined frequencies of APOL1 RRAs in non-white Brazilian patients with LN and controls to assess association with renal outcomes.

Methods APOL1 RRAs were genotyped in 222 healthy blood donors (controls) and 201 cases with LN from three outpatient clinics. Two single nucleotide polymorphisms in the G1 (rs73885319; rs60910145) and an indel for the G2 (rs71785313) variant were genotyped.

Results The frequency of APOL1 RRAs in non-white Brazilian LN cases did not differ significantly from healthy controls, few participants had 2 RRAs. In the sample, 84.6% of LN cases and 82.9% of controls had 0 RRAs, 13.4% and 15.3% had 1 RRA, and 2.0% and 0.4% had 2 RRAs, respectively. LN cases with >1 APOL1 RRAs had similar baseline characteristics and renal responses to treatment, yet faced higher risk for progressive chronic kidney disease (CKD) to an eGFR <30 ml/min/1.732 compared to those with 0 RRAs (11.1% with 0, 29.6% with 1; 50% with 2 RRAs, p=0.005). Although glomerular lesions and activity scores on initial kidney biopsy did not differ significantly between individuals based on APOL1 genotype, chronicity scores, tubular atrophy and interstitial fibrosis were more severe in those with >1 RRA.

Conclusion Although initial kidney lesions and treatment responses were similar, a single APOL1 RRA in non-white Brazilians with LN was associated with increased risk of advanced CKD and possibly more tubulo-interstitial damage.

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Vol. 46, Issue 12
1 Dec 2019
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Accepted manuscript
A single APOL1 nephropathy variant increases risk of advanced lupus nephritis in Brazilians
Gisele Vajgel, Suelen Cristina Lima, Diego Jeronimo S. Santana, Camila B. L. Oliveira, Denise Maria N. Costa, Pamela J. Hicks, Maria Alina G. M. Cavalcante, Carl D. Langefeld, Lucila Maria Valente, Sergio Crovella, Gianna Mastroianni Kirsztajn, Barry I. Freedman, Paula Sandrin-Garcia
The Journal of Rheumatology Nov 2019, jrheum.190684; DOI: 10.3899/jrheum.190684

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Accepted manuscript
A single APOL1 nephropathy variant increases risk of advanced lupus nephritis in Brazilians
Gisele Vajgel, Suelen Cristina Lima, Diego Jeronimo S. Santana, Camila B. L. Oliveira, Denise Maria N. Costa, Pamela J. Hicks, Maria Alina G. M. Cavalcante, Carl D. Langefeld, Lucila Maria Valente, Sergio Crovella, Gianna Mastroianni Kirsztajn, Barry I. Freedman, Paula Sandrin-Garcia
The Journal of Rheumatology Nov 2019, jrheum.190684; DOI: 10.3899/jrheum.190684
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