Skip to main content
Top
Published in: Malaria Journal 1/2014

Open Access 01-12-2014 | Research

Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi

Authors: Timothy William, Jenarun Jelip, Jayaram Menon, Fread Anderios, Rashidah Mohammad, Tajul A Awang Mohammad, Matthew J Grigg, Tsin W Yeo, Nicholas M Anstey, Bridget E Barber

Published in: Malaria Journal | Issue 1/2014

Login to get access

Abstract

Background

While Malaysia has had great success in controlling Plasmodium falciparum and Plasmodium vivax, notifications of Plasmodium malariae and the microscopically near-identical Plasmodium knowlesi increased substantially over the past decade. However, whether this represents microscopic misdiagnosis or increased recognition of P. knowlesi has remained uncertain.

Methods

To describe the changing epidemiology of malaria in Sabah, in particular the increasing incidence of P. knowlesi, a retrospective descriptive study was undertaken involving a review of Department of Health malaria notification data from 2012–2013, extending a previous review of these data from 1992–2011. In addition, malaria PCR and microscopy data from the State Public Health Laboratory were reviewed to estimate the accuracy of the microscopy-based notification data.

Results

Notifications of P. malariae/P. knowlesi increased from 703 in 2011 to 815 in 2012 and 996 in 2013. Notifications of P. vivax and P. falciparum decreased from 605 and 628, respectively, in 2011, to 297 and 263 in 2013. In 2013, P. malariae/P. knowlesi accounted for 62% of all malaria notifications compared to 35% in 2011. Among 1,082 P. malariae/P. knowlesi blood slides referred for PCR testing during 2011–2013, there were 924 (85%) P. knowlesi mono-infections, 30 (2.8%) P. falciparum, 43 (4.0%) P. vivax, seven (0.6%) P. malariae, six (0.6%) mixed infections, 31 (2.9%) positive only for Plasmodium genus, and 41 (3.8%) Plasmodium-negative. Plasmodium knowlesi mono-infection accounted for 32/156 (21%) and 33/87 (38%) blood slides diagnosed by microscopy as P. falciparum and P. vivax, respectively. Twenty-six malaria deaths were reported during 2010–2013, including 12 with ‘P. malariae/P. knowlesi’ (all adults), 12 with P. falciparum (seven adults), and two adults with P. vivax.

Conclusions

Notifications of P. malariae/P. knowlesi in Sabah are increasing, with this trend likely reflecting a true increase in incidence of P. knowlesi and presenting a major threat to malaria control and elimination in Malaysia. With the decline of P. falciparum and P. vivax, control programmes need to incorporate measures to protect against P. knowlesi, with further research required to determine effective interventions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mudin RN: Malaria: battling old disease with new strategies. 5th Perak Health Conference. 2013, Ipoh, Perak, Malaysia Mudin RN: Malaria: battling old disease with new strategies. 5th Perak Health Conference. 2013, Ipoh, Perak, Malaysia
2.
go back to reference World Health Organization: World Malaria Report 2013. 2013, Geneva: World Health Organization World Health Organization: World Malaria Report 2013. 2013, Geneva: World Health Organization
3.
go back to reference William T, Rahman HA, Jelip J, Ibrahim MY, Menon J, Grigg MJ, Yeo TW, Anstey NM, Barber BE: Increasing incidence of Plasmodium knowlesi malaria following control of P. falciparum and P. vivax malaria in Sabah, Malaysia. PLoS Negl Trop Dis. 2013, 7: e2026-10.1371/journal.pntd.0002026.PubMedCentralCrossRefPubMed William T, Rahman HA, Jelip J, Ibrahim MY, Menon J, Grigg MJ, Yeo TW, Anstey NM, Barber BE: Increasing incidence of Plasmodium knowlesi malaria following control of P. falciparum and P. vivax malaria in Sabah, Malaysia. PLoS Negl Trop Dis. 2013, 7: e2026-10.1371/journal.pntd.0002026.PubMedCentralCrossRefPubMed
4.
go back to reference Naing DKS, Anderios F, Lin Z: Geographic and ethnic distribution of P. knowlesi infection in Sabah, Malaysia. Int J Collaborative Res Intern Med Public Health. 2011, 3: 391-400. Naing DKS, Anderios F, Lin Z: Geographic and ethnic distribution of P. knowlesi infection in Sabah, Malaysia. Int J Collaborative Res Intern Med Public Health. 2011, 3: 391-400.
5.
go back to reference Barber BE, William T, Dhararaj P, Anderios F, Grigg MJ, Yeo TW, Anstey NM: Epidemiology of Plasmodium knowlesi malaria in northeast Sabah, Malaysia: family clusters and wide age distribution. Malar J. 2012, 11: 401-10.1186/1475-2875-11-401.PubMedCentralCrossRefPubMed Barber BE, William T, Dhararaj P, Anderios F, Grigg MJ, Yeo TW, Anstey NM: Epidemiology of Plasmodium knowlesi malaria in northeast Sabah, Malaysia: family clusters and wide age distribution. Malar J. 2012, 11: 401-10.1186/1475-2875-11-401.PubMedCentralCrossRefPubMed
6.
go back to reference Joveen-Neoh WF, Chong KL, Wong CM, Lau TY: Incidence of malaria in the Interior Division of Sabah, Malaysian Borneo, based on nested PCR. J Parasitol Res. 2011, 2011: e104284-CrossRef Joveen-Neoh WF, Chong KL, Wong CM, Lau TY: Incidence of malaria in the Interior Division of Sabah, Malaysian Borneo, based on nested PCR. J Parasitol Res. 2011, 2011: e104284-CrossRef
7.
go back to reference Singh B, Sung LK, Matusop A, Radhakrishnan A, Shamsul SSG, Cox-Singh J, Thomas A, Conway DJ: A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004, 363: 1017-1024. 10.1016/S0140-6736(04)15836-4.CrossRefPubMed Singh B, Sung LK, Matusop A, Radhakrishnan A, Shamsul SSG, Cox-Singh J, Thomas A, Conway DJ: A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004, 363: 1017-1024. 10.1016/S0140-6736(04)15836-4.CrossRefPubMed
8.
go back to reference Cox-Singh J, Davis TM, Lee KS, Shamsul SS, Matusop A, Ratnam S, Rahman HA, Conway DJ, Singh B: Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis. 2008, 46: 165-171. 10.1086/524888.PubMedCentralCrossRefPubMed Cox-Singh J, Davis TM, Lee KS, Shamsul SS, Matusop A, Ratnam S, Rahman HA, Conway DJ, Singh B: Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis. 2008, 46: 165-171. 10.1086/524888.PubMedCentralCrossRefPubMed
9.
go back to reference Vythilingam I, NoorAzian Y, Huat T, Jiram A, Yusri Y, Azahari A, NorParina I, NoorRain A, LokmanHakim S: Plasmodium knowlesi in humans, macaques and mosquitoes in peninsular Malaysia. Parasit Vectors. 2008, 1: 26-10.1186/1756-3305-1-26.PubMedCentralCrossRefPubMed Vythilingam I, NoorAzian Y, Huat T, Jiram A, Yusri Y, Azahari A, NorParina I, NoorRain A, LokmanHakim S: Plasmodium knowlesi in humans, macaques and mosquitoes in peninsular Malaysia. Parasit Vectors. 2008, 1: 26-10.1186/1756-3305-1-26.PubMedCentralCrossRefPubMed
10.
go back to reference Barber BE, William T, Grigg MJ, Yeo TW, Anstey NM: Limitations of microscopy to differentiate Plasmodium species in a region co-endemic for Plasmodium falciparum, Plasmodium vivax and Plasmodium knowlesi. Malar J. 2013, 12: 8-10.1186/1475-2875-12-8.PubMedCentralCrossRefPubMed Barber BE, William T, Grigg MJ, Yeo TW, Anstey NM: Limitations of microscopy to differentiate Plasmodium species in a region co-endemic for Plasmodium falciparum, Plasmodium vivax and Plasmodium knowlesi. Malar J. 2013, 12: 8-10.1186/1475-2875-12-8.PubMedCentralCrossRefPubMed
11.
go back to reference Barber BE, William T, Grigg MJ, Menon J, Auburn S, Marfurt J, Anstey NM, Yeo TW: A prospective comparative study of knowlesi, falciparum and vivax malaria in Sabah, Malaysia: high proportion with severe disease from Plasmodium knowlesi and P. vivax but no mortality with early referral and artesunate therapy. Clin Infect Dis. 2013, 56: 383-397. 10.1093/cid/cis902.CrossRefPubMed Barber BE, William T, Grigg MJ, Menon J, Auburn S, Marfurt J, Anstey NM, Yeo TW: A prospective comparative study of knowlesi, falciparum and vivax malaria in Sabah, Malaysia: high proportion with severe disease from Plasmodium knowlesi and P. vivax but no mortality with early referral and artesunate therapy. Clin Infect Dis. 2013, 56: 383-397. 10.1093/cid/cis902.CrossRefPubMed
12.
go back to reference Daneshvar C, Davis TM, Cox-Singh J, Rafa’ee M, Zakaria S, Divis P, Singh B: Clinical and laboratory features of human Plasmodium knowlesi infection. Clin Infect Dis. 2009, 49: 852-860. 10.1086/605439.PubMedCentralCrossRefPubMed Daneshvar C, Davis TM, Cox-Singh J, Rafa’ee M, Zakaria S, Divis P, Singh B: Clinical and laboratory features of human Plasmodium knowlesi infection. Clin Infect Dis. 2009, 49: 852-860. 10.1086/605439.PubMedCentralCrossRefPubMed
13.
go back to reference Cox-Singh J, Hiu J, Lucas SB, Divis PC, Zulkarnaen M, Chandran P, Wong KT, Adem P, Zaki SR, Singh B: Severe malaria-a case of fatal Plasmodium knowlesi infection with post-mortem findings. Malar J. 2010, 9: 10-10.1186/1475-2875-9-10.PubMedCentralCrossRefPubMed Cox-Singh J, Hiu J, Lucas SB, Divis PC, Zulkarnaen M, Chandran P, Wong KT, Adem P, Zaki SR, Singh B: Severe malaria-a case of fatal Plasmodium knowlesi infection with post-mortem findings. Malar J. 2010, 9: 10-10.1186/1475-2875-9-10.PubMedCentralCrossRefPubMed
14.
go back to reference Rajahram G, Barber BE, William T, Menon J, Anstey NM, Yeo TW: Deaths due to Plasmodium knowlesi malaria in Sabah, Malaysia: association with reporting as P. malariae and delayed parenteral artesunate. Malar J. 2012, 11: 284-10.1186/1475-2875-11-284.PubMedCentralCrossRefPubMed Rajahram G, Barber BE, William T, Menon J, Anstey NM, Yeo TW: Deaths due to Plasmodium knowlesi malaria in Sabah, Malaysia: association with reporting as P. malariae and delayed parenteral artesunate. Malar J. 2012, 11: 284-10.1186/1475-2875-11-284.PubMedCentralCrossRefPubMed
15.
go back to reference William T, Menon J, Rajahram G, Chan L, Ma G, Donaldson S, Khoo S, Fredrick C, Jilip J, Anstey NM, Yeo TW: Severe Plasmodium knowlesi malaria in a tertiary hospital, Sabah, Malaysia. Emerg Infect Dis. 2011, 17: 1248-1255. 10.3201/eid1707.101017.PubMedCentralCrossRefPubMed William T, Menon J, Rajahram G, Chan L, Ma G, Donaldson S, Khoo S, Fredrick C, Jilip J, Anstey NM, Yeo TW: Severe Plasmodium knowlesi malaria in a tertiary hospital, Sabah, Malaysia. Emerg Infect Dis. 2011, 17: 1248-1255. 10.3201/eid1707.101017.PubMedCentralCrossRefPubMed
16.
go back to reference Chin W, Contacos P, Collins W, Jeter M, Alpert E: Experimental mosquito-transmission of Plasmodium knowlesi to man and monkey. Am J Trop Med Hyg. 1968, 17: 355-PubMed Chin W, Contacos P, Collins W, Jeter M, Alpert E: Experimental mosquito-transmission of Plasmodium knowlesi to man and monkey. Am J Trop Med Hyg. 1968, 17: 355-PubMed
17.
go back to reference Divis P, Shokoples SE, Singh B, Yanow SK: A TaqMan real-time PCR assay for the detection and quantitation of Plasmodium knowlesi. Malar J. 2010, 9: 344-10.1186/1475-2875-9-344.PubMedCentralCrossRefPubMed Divis P, Shokoples SE, Singh B, Yanow SK: A TaqMan real-time PCR assay for the detection and quantitation of Plasmodium knowlesi. Malar J. 2010, 9: 344-10.1186/1475-2875-9-344.PubMedCentralCrossRefPubMed
18.
go back to reference Imwong M, Tanomsing N, Pukrittayakamee S, Day NPJ, White NJ, Snounou G: Spurious amplification of a Plasmodium vivax small-subunit RNA gene by use of primers currently used to detect P. knowlesi. J Clin Microbiol. 2009, 47: 4173-10.1128/JCM.00811-09.PubMedCentralCrossRefPubMed Imwong M, Tanomsing N, Pukrittayakamee S, Day NPJ, White NJ, Snounou G: Spurious amplification of a Plasmodium vivax small-subunit RNA gene by use of primers currently used to detect P. knowlesi. J Clin Microbiol. 2009, 47: 4173-10.1128/JCM.00811-09.PubMedCentralCrossRefPubMed
19.
go back to reference Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK: Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol. 2009, 47: 975-980. 10.1128/JCM.01858-08.PubMedCentralCrossRefPubMed Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK: Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol. 2009, 47: 975-980. 10.1128/JCM.01858-08.PubMedCentralCrossRefPubMed
20.
go back to reference Department of Statistics, Malaysia: Population Distribution and Basic Demographic Characteristics, Population and Housing Census of Malaysia 2010. 2011, Kuala Lumpur, Malaysia: Department of Statistics Department of Statistics, Malaysia: Population Distribution and Basic Demographic Characteristics, Population and Housing Census of Malaysia 2010. 2011, Kuala Lumpur, Malaysia: Department of Statistics
23.
go back to reference Yusof R, Lau Y, Mahmud R, Fong M, Jelip J, Ngian H, Mustakim S, Mat Hussin H, Marzuki N, Mohd Ali M: High proportion of knowlesi malaria in recent malaria cases in Malaysia. Malar J. 2014, 13: 168-10.1186/1475-2875-13-168.PubMedCentralCrossRefPubMed Yusof R, Lau Y, Mahmud R, Fong M, Jelip J, Ngian H, Mustakim S, Mat Hussin H, Marzuki N, Mohd Ali M: High proportion of knowlesi malaria in recent malaria cases in Malaysia. Malar J. 2014, 13: 168-10.1186/1475-2875-13-168.PubMedCentralCrossRefPubMed
24.
go back to reference Moyes CL, Henry AJ, Golding N, Huang Z, Singh B, Baird JK, Newton PN, Huffman M, Duda KA, Drakeley CJ: Defining the geographical range of the Plasmodium knowlesi reservoir. PLoS Negl Trop Dis. 2014, 8: e2780-10.1371/journal.pntd.0002780.PubMedCentralCrossRefPubMed Moyes CL, Henry AJ, Golding N, Huang Z, Singh B, Baird JK, Newton PN, Huffman M, Duda KA, Drakeley CJ: Defining the geographical range of the Plasmodium knowlesi reservoir. PLoS Negl Trop Dis. 2014, 8: e2780-10.1371/journal.pntd.0002780.PubMedCentralCrossRefPubMed
25.
go back to reference Bouman A, Heineman MJ, Faas MM: Sex hormones and the immune response in humans. Hum Reprod Update. 2005, 11: 411-423. 10.1093/humupd/dmi008.CrossRefPubMed Bouman A, Heineman MJ, Faas MM: Sex hormones and the immune response in humans. Hum Reprod Update. 2005, 11: 411-423. 10.1093/humupd/dmi008.CrossRefPubMed
26.
go back to reference Pennell LM, Galligan CL, Fish EN: Sex affects immunity. J Autoimmun. 2012, 38: J282-J291. 10.1016/j.jaut.2011.11.013.CrossRefPubMed Pennell LM, Galligan CL, Fish EN: Sex affects immunity. J Autoimmun. 2012, 38: J282-J291. 10.1016/j.jaut.2011.11.013.CrossRefPubMed
27.
go back to reference Lim C, Hansen E, DeSimone TM, Moreno Y, Junker K, Bei A, Brugnara C, Buckee CO, Duraisingh MT: Expansion of host cellular niche can drive adaptation of a zoonotic malaria parasite to humans. Nat Commun. 2013, 4: 1638-PubMedCentralCrossRefPubMed Lim C, Hansen E, DeSimone TM, Moreno Y, Junker K, Bei A, Brugnara C, Buckee CO, Duraisingh MT: Expansion of host cellular niche can drive adaptation of a zoonotic malaria parasite to humans. Nat Commun. 2013, 4: 1638-PubMedCentralCrossRefPubMed
28.
go back to reference Ciuca M, Chelarescu M, Sofletea A, Constantenescu P, Teriteanu E, Cortez P, Balanovschi G, Ilies M: Contribution expérimentale à l’étude de l’immunité dans le paludisme. 1955, L’Academia: Bucarest Ciuca M, Chelarescu M, Sofletea A, Constantenescu P, Teriteanu E, Cortez P, Balanovschi G, Ilies M: Contribution expérimentale à l’étude de l’immunité dans le paludisme. 1955, L’Academia: Bucarest
29.
go back to reference Imai N, White MT, Ghani AC, Drakeley CJ: Transmission and control of Plasmodium knowlesi: a mathematical modelling study. PLoS Negl Trop Dis. 2014, 8: e2978-10.1371/journal.pntd.0002978.PubMedCentralCrossRefPubMed Imai N, White MT, Ghani AC, Drakeley CJ: Transmission and control of Plasmodium knowlesi: a mathematical modelling study. PLoS Negl Trop Dis. 2014, 8: e2978-10.1371/journal.pntd.0002978.PubMedCentralCrossRefPubMed
30.
go back to reference Lee K-S, Divis PCS, Zakaria SK, Matusop A, Julin RA, Conway DJ, Cox-Singh J, Singh B: Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathog. 2011, 7: e1002105-10.1371/journal.ppat.1002105.CrossRef Lee K-S, Divis PCS, Zakaria SK, Matusop A, Julin RA, Conway DJ, Cox-Singh J, Singh B: Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathog. 2011, 7: e1002105-10.1371/journal.ppat.1002105.CrossRef
Metadata
Title
Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi
Authors
Timothy William
Jenarun Jelip
Jayaram Menon
Fread Anderios
Rashidah Mohammad
Tajul A Awang Mohammad
Matthew J Grigg
Tsin W Yeo
Nicholas M Anstey
Bridget E Barber
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2014
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-13-390

Other articles of this Issue 1/2014

Malaria Journal 1/2014 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
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.