Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Glucose-6-phosphate dehydrogenase deficiency in people living in malaria endemic districts of Nepal

Authors: Prakash Ghimire, Nihal Singh, Leonard Ortega, Komal Raj Rijal, Bipin Adhikari, Garib Das Thakur, Baburam Marasini

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

Glucose-6-phosphate dehydrogenase (G6PD) is a rate limiting enzyme of the pentose phosphate pathway and is closely associated with the haemolytic disorders among patients receiving anti-malarial drugs, such as primaquine. G6PD deficiency (G6PDd) is an impending factor for radical treatment of malaria which affects the clearance of gametocytes from the blood and subsequent delay in the achievement of malaria elimination. The main objective of this study was to assess the prevalence of G6PD deficiency in six malaria endemic districts in Southern Nepal.

Methods

A cross-sectional population based prevalence survey was conducted in six malaria endemic districts of Nepal, during April–Dec 2013. A total of 1341 blood samples were tested for G6PDd using two different rapid diagnostic test kits (Binax-Now® and Care Start™). Equal proportions of participants from each district (n ≥ 200) were enrolled considering ethnic and demographic representation of the population groups.

Results

Out of total 1341 blood specimens collected from six districts, the overall prevalence of G6PDd was 97/1341; 7.23% on Binax Now and 81/1341; 6.0% on Care Start test. Higher prevalence was observed in male than females [Binax Now: male 10.2%; 53/521 versus female 5.4%; 44/820 (p = 0.003) and Care Start: male 8.4%; 44/521 versus female 4.5%; 37/820 (p = 0.003)]. G6PDd was higher in ethnic groups Rajbanshi (11.7%; 19/162) and Tharu (5.6%; 56/1005) (p = 0.006), major inhabitant of the endemic districts. Higher prevalence of G6PDd was found in Jhapa (22/224; 9.8%) and Morang districts (18/225; 8%) (p = 0.031). In a multivariate analysis, male were found at more risk for G6PDd than females, on Binax test (aOR = 1.97; CI 1.28–3.03; p = 0.002) and Care Start test (aOR = 1.86; CI 1.16–2.97; p = 0.009).

Conclusions

The higher prevalence of G6PDd in certain ethnic group, gender and geographical region clearly demonstrates clustering of the cases and ascertained the risk groups within the population. This is the first study in Nepal which identified the vulnerable population groups for G6PDd in malaria endemic districts. The finding of this study warrants the need for G6PDd testing in vulnerable population groups in endemic districts, and also facilitates use of primaquine in mass supporting timely progress for malaria elimination.
Literature
1.
go back to reference Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis. 2012;6:e1814.CrossRefPubMedPubMedCentral Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis. 2012;6:e1814.CrossRefPubMedPubMedCentral
3.
go back to reference Anstey NM, Douglas NM, Poespoprodjo JR, Price RN. Plasmodium vivax: clinical spectrum, risk factors and pathogenesis. Adv Parasitol. 2012;80:151–201.CrossRefPubMed Anstey NM, Douglas NM, Poespoprodjo JR, Price RN. Plasmodium vivax: clinical spectrum, risk factors and pathogenesis. Adv Parasitol. 2012;80:151–201.CrossRefPubMed
4.
5.
go back to reference Beutler E, Dern RJ, Alving AS. The hemolytic effect of primaquine. III. A study of primaquine-sensitive erythrocytes. J Lab Clin Med. 1954;44:177–84.PubMed Beutler E, Dern RJ, Alving AS. The hemolytic effect of primaquine. III. A study of primaquine-sensitive erythrocytes. J Lab Clin Med. 1954;44:177–84.PubMed
6.
go back to reference Beutler E, Duparc S, G6PD Deficiency Working Group. Glucose-6-phosphate dehydrogenase deficiency and antimalarial drug development. Am J Trop Med Hyg. 2007;77:779–89.PubMed Beutler E, Duparc S, G6PD Deficiency Working Group. Glucose-6-phosphate dehydrogenase deficiency and antimalarial drug development. Am J Trop Med Hyg. 2007;77:779–89.PubMed
7.
go back to reference Howes R, Piel F, Patil A, Nyangiri O, Gething PW, Dewi M, et al. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries, a geostatistical model based map. PLoS Med. 2012;9:e1001339.CrossRefPubMedPubMedCentral Howes R, Piel F, Patil A, Nyangiri O, Gething PW, Dewi M, et al. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries, a geostatistical model based map. PLoS Med. 2012;9:e1001339.CrossRefPubMedPubMedCentral
8.
go back to reference Alving A, Carson P, Flanagan C, Ickes C. Enzymatic deficiency in primaquine-sensitive erythrocytes. Science. 1956;124:484–5.PubMed Alving A, Carson P, Flanagan C, Ickes C. Enzymatic deficiency in primaquine-sensitive erythrocytes. Science. 1956;124:484–5.PubMed
9.
go back to reference Clyde DF. Clinical problems associated with the use of primaquine as a tissue schizontocidal and gametocytocidal drug. Bull World Health Organ. 1981;59:391–5.PubMedPubMedCentral Clyde DF. Clinical problems associated with the use of primaquine as a tissue schizontocidal and gametocytocidal drug. Bull World Health Organ. 1981;59:391–5.PubMedPubMedCentral
11.
go back to reference Frank J. Diagnosis and management of G6PD deficiency. Am Fam Physician. 2005;72:1277–82.PubMed Frank J. Diagnosis and management of G6PD deficiency. Am Fam Physician. 2005;72:1277–82.PubMed
12.
go back to reference Ganczakowski M, Town M, Bowden D, Vulliamy T, Kaneko A, Clegg J, et al. Multiple glucose 6-phosphate dehydrogenase deficient variants correlate with malaria endemicity in the Vanuatu archipelago (Southwestern Pacific). Am J Hum Genet. 1995;56:294–301.PubMedPubMedCentral Ganczakowski M, Town M, Bowden D, Vulliamy T, Kaneko A, Clegg J, et al. Multiple glucose 6-phosphate dehydrogenase deficient variants correlate with malaria endemicity in the Vanuatu archipelago (Southwestern Pacific). Am J Hum Genet. 1995;56:294–301.PubMedPubMedCentral
13.
go back to reference Louicharoen C, Patin E, Paul R, Nuchprayoon I, Witoonpanich B, Peerapittayamongkol C, et al. Positively selected G6PD-Mahidol mutation reduces Plasmodium vivax density in Southeast Asians. Science. 2009;326:1546–9.CrossRefPubMed Louicharoen C, Patin E, Paul R, Nuchprayoon I, Witoonpanich B, Peerapittayamongkol C, et al. Positively selected G6PD-Mahidol mutation reduces Plasmodium vivax density in Southeast Asians. Science. 2009;326:1546–9.CrossRefPubMed
19.
go back to reference Kim S, Nguon C, Guillard B, Duong S, Chy S, Sum S, et al. Performance of the CareStart G6PD deficiency screening test, a point-of-care diagnostic for primaquine therapy screening. PLoS ONE. 2011;6:e28357.CrossRefPubMedPubMedCentral Kim S, Nguon C, Guillard B, Duong S, Chy S, Sum S, et al. Performance of the CareStart G6PD deficiency screening test, a point-of-care diagnostic for primaquine therapy screening. PLoS ONE. 2011;6:e28357.CrossRefPubMedPubMedCentral
20.
go back to reference Tinley K, Loughlin A, Jepson A, Barnett E. Evaluation of a rapid qualitative enzyme chromatographic test for glucose-6-phosphate dehydrogenase deficiency. Am J Trop Med Hyg. 2010;82:210–4.CrossRefPubMedPubMedCentral Tinley K, Loughlin A, Jepson A, Barnett E. Evaluation of a rapid qualitative enzyme chromatographic test for glucose-6-phosphate dehydrogenase deficiency. Am J Trop Med Hyg. 2010;82:210–4.CrossRefPubMedPubMedCentral
21.
go back to reference White N, Qiao L, Qi G, Luzzatto L. Rationale for recommending a lower dose of primaquine as a Plasmodium falciparum gametocytocide in populations where G6PD deficiency is common. Malar J. 2012;11:418.CrossRefPubMedPubMedCentral White N, Qiao L, Qi G, Luzzatto L. Rationale for recommending a lower dose of primaquine as a Plasmodium falciparum gametocytocide in populations where G6PD deficiency is common. Malar J. 2012;11:418.CrossRefPubMedPubMedCentral
22.
go back to reference Hay S, Guerra C, Tatem AJ, Noor A, Snow R. The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis. 2004;4:327–36.CrossRefPubMedPubMedCentral Hay S, Guerra C, Tatem AJ, Noor A, Snow R. The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis. 2004;4:327–36.CrossRefPubMedPubMedCentral
23.
go back to reference Mahgoub H, Gasim G, Musa IR, Adam I. Severe Plasmodium vivax malaria among Sudanese children at New Halfa Hospital, Eastern Sudan. Parasites Vectors. 2012;5:154.CrossRefPubMedPubMedCentral Mahgoub H, Gasim G, Musa IR, Adam I. Severe Plasmodium vivax malaria among Sudanese children at New Halfa Hospital, Eastern Sudan. Parasites Vectors. 2012;5:154.CrossRefPubMedPubMedCentral
24.
go back to reference Harris I, Sharrock WW, Bain L, Gray K, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.CrossRefPubMedPubMedCentral Harris I, Sharrock WW, Bain L, Gray K, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.CrossRefPubMedPubMedCentral
25.
go back to reference Baird J, Surjadjaja C. Consideration of ethics in primaquine therapy against malaria transmission. Trends Parasitol. 2011;27:11–6.CrossRefPubMed Baird J, Surjadjaja C. Consideration of ethics in primaquine therapy against malaria transmission. Trends Parasitol. 2011;27:11–6.CrossRefPubMed
26.
go back to reference Arain YH, Bhutani VK. Prevention of Kernicterus in South Asia: role of neonatal G6PD deficiency and its identification. Indian J Pediatr. 2014;81:599–607.CrossRefPubMed Arain YH, Bhutani VK. Prevention of Kernicterus in South Asia: role of neonatal G6PD deficiency and its identification. Indian J Pediatr. 2014;81:599–607.CrossRefPubMed
27.
go back to reference Adu-Gyasi D, Asante KP, Newton S, Dosoo D, Amoako S, Adjei G, et al. Evaluation of the diagnostic accuracy of CareStart G6PD deficiency rapid diagnostic test (RDT) in a malaria endemic area in Ghana, Africa. PLoS One. 2015;10:e0125796.CrossRefPubMedPubMedCentral Adu-Gyasi D, Asante KP, Newton S, Dosoo D, Amoako S, Adjei G, et al. Evaluation of the diagnostic accuracy of CareStart G6PD deficiency rapid diagnostic test (RDT) in a malaria endemic area in Ghana, Africa. PLoS One. 2015;10:e0125796.CrossRefPubMedPubMedCentral
28.
go back to reference Osorio L, Carter N, Arthur P, Bancone G, Gopalan S, Gupta SK, et al. Performance of BinaxNOW G6PD deficiency point-of-care diagnostic in P. vivax-infected subjects. Am J Trop Med Hyg. 2015;92:22–7.CrossRefPubMedPubMedCentral Osorio L, Carter N, Arthur P, Bancone G, Gopalan S, Gupta SK, et al. Performance of BinaxNOW G6PD deficiency point-of-care diagnostic in P. vivax-infected subjects. Am J Trop Med Hyg. 2015;92:22–7.CrossRefPubMedPubMedCentral
29.
go back to reference Cappellini M, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet Infect Dis. 2008;371:64–74. Cappellini M, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet Infect Dis. 2008;371:64–74.
30.
go back to reference Leslie T, Moiz B, Mohammad N, Amanzai O, Ur Rasheed H, Jan S, et al. Prevalence and molecular basis of G6PD deficiency in Afghan populations: implications for treatment policy in the region. Malar J. 2013;12:230.CrossRefPubMedPubMedCentral Leslie T, Moiz B, Mohammad N, Amanzai O, Ur Rasheed H, Jan S, et al. Prevalence and molecular basis of G6PD deficiency in Afghan populations: implications for treatment policy in the region. Malar J. 2013;12:230.CrossRefPubMedPubMedCentral
31.
go back to reference Kuwahata M, Wijesinghe R, Ho M, Pelecanos A, Bobogare A, Landry L, et al. Population screening for G6PD deficiencies in Isabel Province, Solomon Islands, using a modified enzyme assay on filter paper dried bloodspots. Malar J. 2010;9:223.CrossRefPubMedPubMedCentral Kuwahata M, Wijesinghe R, Ho M, Pelecanos A, Bobogare A, Landry L, et al. Population screening for G6PD deficiencies in Isabel Province, Solomon Islands, using a modified enzyme assay on filter paper dried bloodspots. Malar J. 2010;9:223.CrossRefPubMedPubMedCentral
32.
go back to reference Baxi A, Balakrishanan V, Undevi J, Sanghvi L. Glucose-6-phosphate dehydrogenase deficiency in the Parsee community, Bombay. Indian J Med Sci. 1963;17:493–500.PubMed Baxi A, Balakrishanan V, Undevi J, Sanghvi L. Glucose-6-phosphate dehydrogenase deficiency in the Parsee community, Bombay. Indian J Med Sci. 1963;17:493–500.PubMed
33.
go back to reference Terrenato L, Shrestha S, Dixit K, Luzzatto L, Modiano G, Morpurgo G, et al. Decreased malaria morbidity in the Tharu people compared to sympatric populations in Nepal. Ann Trop Med Parasitol. 1988;82:1–11.CrossRefPubMed Terrenato L, Shrestha S, Dixit K, Luzzatto L, Modiano G, Morpurgo G, et al. Decreased malaria morbidity in the Tharu people compared to sympatric populations in Nepal. Ann Trop Med Parasitol. 1988;82:1–11.CrossRefPubMed
34.
go back to reference Sakai Y, Kobayashi S, Shibata H, Furuumi H, Endo T, Fucharoen S, et al. Molecular analysis of alpha-thalassemia in Nepal: correlation with malaria endemicity. J Human Genet. 2000;45:127–32.CrossRef Sakai Y, Kobayashi S, Shibata H, Furuumi H, Endo T, Fucharoen S, et al. Molecular analysis of alpha-thalassemia in Nepal: correlation with malaria endemicity. J Human Genet. 2000;45:127–32.CrossRef
35.
go back to reference Shigeru K. Cultural and biological adaptations to malaria in Nepal. Bull Grad Sch Soc Cult Stud Kyushu Univ. 1996;2:59–73. Shigeru K. Cultural and biological adaptations to malaria in Nepal. Bull Grad Sch Soc Cult Stud Kyushu Univ. 1996;2:59–73.
36.
go back to reference Mukherjee MB, Colah RB, Martin S, Ghosh K. Glucose-6-phosphate dehydrogenase (G6PD) deficiency among tribal populations of India-Country scenario. Indian J Med Res. 2015;141:516–20.PubMedPubMedCentral Mukherjee MB, Colah RB, Martin S, Ghosh K. Glucose-6-phosphate dehydrogenase (G6PD) deficiency among tribal populations of India-Country scenario. Indian J Med Res. 2015;141:516–20.PubMedPubMedCentral
37.
go back to reference Rai V, Kumar P. Epidemiological study of glucose-6-phosphate dehydrogenase deficiency in scheduled caste population of India. J Anthropol. 2012;2012:984180.CrossRef Rai V, Kumar P. Epidemiological study of glucose-6-phosphate dehydrogenase deficiency in scheduled caste population of India. J Anthropol. 2012;2012:984180.CrossRef
38.
go back to reference Matsuoka H, Jichun W, Hirai M, Yoshida S, Arai M, Ishii A, et al. Two cases of glucose-6-phosphate dehydrogenase-deficient Nepalese belonging to the G6PD Mediterranean-type, not India–Pakistan subtype but Mediterranean-Middle East sub-type. J Hum Genet. 2003;48:275–7.CrossRefPubMed Matsuoka H, Jichun W, Hirai M, Yoshida S, Arai M, Ishii A, et al. Two cases of glucose-6-phosphate dehydrogenase-deficient Nepalese belonging to the G6PD Mediterranean-type, not India–Pakistan subtype but Mediterranean-Middle East sub-type. J Hum Genet. 2003;48:275–7.CrossRefPubMed
40.
go back to reference Peters AL, Van Noorden CJ. Glucose-6-phosphate dehydrogenase deficiency and malaria: cytochemical detection of heterozygous G6PD deficiency in women. J Histochem Cytochem. 2009;57:1003–11.CrossRefPubMedPubMedCentral Peters AL, Van Noorden CJ. Glucose-6-phosphate dehydrogenase deficiency and malaria: cytochemical detection of heterozygous G6PD deficiency in women. J Histochem Cytochem. 2009;57:1003–11.CrossRefPubMedPubMedCentral
41.
go back to reference Domingo GJ, Satyagraha AW, Anvikar A, Baird K, Bancone G, Bansil P, et al. G6PD testing in support of treatment and elimination of malaria: recommendations for evaluation of G6PD tests. Malar J. 2013;12:391.CrossRefPubMedPubMedCentral Domingo GJ, Satyagraha AW, Anvikar A, Baird K, Bancone G, Bansil P, et al. G6PD testing in support of treatment and elimination of malaria: recommendations for evaluation of G6PD tests. Malar J. 2013;12:391.CrossRefPubMedPubMedCentral
Metadata
Title
Glucose-6-phosphate dehydrogenase deficiency in people living in malaria endemic districts of Nepal
Authors
Prakash Ghimire
Nihal Singh
Leonard Ortega
Komal Raj Rijal
Bipin Adhikari
Garib Das Thakur
Baburam Marasini
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1864-2

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.