Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines

Kimberly M. Fornace, Lou S. Herman, Tommy R. Abidin, Tock Hing Chua, Sylvia Daim, Pauline J. Lorenzo, Lynn Grignard, Nor Afizah Nuin, Lau Tiek Ying, Matthew J. Grigg, Timothy William, Fe Espino, Jonathan Cox, Kevin K.A. Tetteh, Chris J. Drakeley

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    Abstract

    Background: Primarily impacting poor, rural populations, the zoonotic malaria Plasmodium knowlesi is now the main cause of human malaria within Malaysian Borneo. While data is increasingly available on symptomatic cases, little is known about community-level patterns of exposure and infection. Understanding the true burden of disease and associated risk factors within endemic communities is critical for informing evidence-based control measures. 

    Methodology/Principal findings: We conducted comprehensive surveys in three areas where P. knowlesi transmission is reported: Limbuak, Pulau Banggi and Matunggung, Kudat, Sabah, Malaysia and Bacungan, Palawan, the Philippines. Infection prevalence was low with parasites detected by PCR in only 0.2% (4/2503) of the population. P. knowlesi PkSERA3 ag1 antibody responses were detected in 7.1% (95% CI: 6.2–8.2%) of the population, compared with 16.1% (14.6–17.7%) and 12.6% (11.2–14.1%) for P. falciparum and P. vivax. Sero-prevalence was low in individuals <10 years old for P. falciparum and P. vivax consistent with decreased transmission of non-zoonotic malaria species. Results indicated marked heterogeneity in transmission intensity between sites and P. knowlesi exposure was associated with agricultural work (OR 1.63; 95% CI 1.07–2.48) and higher levels of forest cover (OR 2.40; 95% CI 1.29–4.46) and clearing (OR 2.14; 95% CI 1.35–3.40) around houses. Spatial patterns of P. knowlesi exposure differed from exposure to non-zoonotic malaria and P. knowlesi exposed individuals were younger on average than individuals exposed to non-zoonotic malaria. 

    Conclusions/Significance: This is the first study to describe serological exposure to P. knowlesi and associated risk factors within endemic communities. Results indicate community–level patterns of infection and exposure differ markedly from demographics of reported cases, with higher levels of exposure among women and children. Further work is needed to understand these variations in risk across a wider population and spatial scale.

    Original languageEnglish
    Article numbere0006432
    Pages (from-to)1-16
    Number of pages16
    JournalPLoS Neglected Tropical Diseases
    Volume12
    Issue number6
    DOIs
    Publication statusPublished - 1 Jun 2018

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    Plasmodium knowlesi
    Philippines
    Malaysia
    Malaria
    Infection
    Borneo
    Population
    Zoonoses
    Rural Population
    Antibody Formation
    Parasites
    Demography
    Polymerase Chain Reaction

    Cite this

    Fornace, K. M., Herman, L. S., Abidin, T. R., Chua, T. H., Daim, S., Lorenzo, P. J., ... Drakeley, C. J. (2018). Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines. PLoS Neglected Tropical Diseases, 12(6), 1-16. [e0006432]. https://doi.org/10.1371/journal.pntd.0006432
    Fornace, Kimberly M. ; Herman, Lou S. ; Abidin, Tommy R. ; Chua, Tock Hing ; Daim, Sylvia ; Lorenzo, Pauline J. ; Grignard, Lynn ; Nuin, Nor Afizah ; Ying, Lau Tiek ; Grigg, Matthew J. ; William, Timothy ; Espino, Fe ; Cox, Jonathan ; Tetteh, Kevin K.A. ; Drakeley, Chris J. / Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines. In: PLoS Neglected Tropical Diseases. 2018 ; Vol. 12, No. 6. pp. 1-16.
    @article{c1e7bacc93e0445db0ea467437e98b3e,
    title = "Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines",
    abstract = "Background: Primarily impacting poor, rural populations, the zoonotic malaria Plasmodium knowlesi is now the main cause of human malaria within Malaysian Borneo. While data is increasingly available on symptomatic cases, little is known about community-level patterns of exposure and infection. Understanding the true burden of disease and associated risk factors within endemic communities is critical for informing evidence-based control measures. Methodology/Principal findings: We conducted comprehensive surveys in three areas where P. knowlesi transmission is reported: Limbuak, Pulau Banggi and Matunggung, Kudat, Sabah, Malaysia and Bacungan, Palawan, the Philippines. Infection prevalence was low with parasites detected by PCR in only 0.2{\%} (4/2503) of the population. P. knowlesi PkSERA3 ag1 antibody responses were detected in 7.1{\%} (95{\%} CI: 6.2–8.2{\%}) of the population, compared with 16.1{\%} (14.6–17.7{\%}) and 12.6{\%} (11.2–14.1{\%}) for P. falciparum and P. vivax. Sero-prevalence was low in individuals <10 years old for P. falciparum and P. vivax consistent with decreased transmission of non-zoonotic malaria species. Results indicated marked heterogeneity in transmission intensity between sites and P. knowlesi exposure was associated with agricultural work (OR 1.63; 95{\%} CI 1.07–2.48) and higher levels of forest cover (OR 2.40; 95{\%} CI 1.29–4.46) and clearing (OR 2.14; 95{\%} CI 1.35–3.40) around houses. Spatial patterns of P. knowlesi exposure differed from exposure to non-zoonotic malaria and P. knowlesi exposed individuals were younger on average than individuals exposed to non-zoonotic malaria. Conclusions/Significance: This is the first study to describe serological exposure to P. knowlesi and associated risk factors within endemic communities. Results indicate community–level patterns of infection and exposure differ markedly from demographics of reported cases, with higher levels of exposure among women and children. Further work is needed to understand these variations in risk across a wider population and spatial scale.",
    author = "Fornace, {Kimberly M.} and Herman, {Lou S.} and Abidin, {Tommy R.} and Chua, {Tock Hing} and Sylvia Daim and Lorenzo, {Pauline J.} and Lynn Grignard and Nuin, {Nor Afizah} and Ying, {Lau Tiek} and Grigg, {Matthew J.} and Timothy William and Fe Espino and Jonathan Cox and Tetteh, {Kevin K.A.} and Drakeley, {Chris J.}",
    year = "2018",
    month = "6",
    day = "1",
    doi = "10.1371/journal.pntd.0006432",
    language = "English",
    volume = "12",
    pages = "1--16",
    journal = "PLoS Neglected Tropical Diseases",
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    Fornace, KM, Herman, LS, Abidin, TR, Chua, TH, Daim, S, Lorenzo, PJ, Grignard, L, Nuin, NA, Ying, LT, Grigg, MJ, William, T, Espino, F, Cox, J, Tetteh, KKA & Drakeley, CJ 2018, 'Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines', PLoS Neglected Tropical Diseases, vol. 12, no. 6, e0006432, pp. 1-16. https://doi.org/10.1371/journal.pntd.0006432

    Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines. / Fornace, Kimberly M.; Herman, Lou S.; Abidin, Tommy R.; Chua, Tock Hing; Daim, Sylvia; Lorenzo, Pauline J.; Grignard, Lynn; Nuin, Nor Afizah; Ying, Lau Tiek; Grigg, Matthew J.; William, Timothy; Espino, Fe; Cox, Jonathan; Tetteh, Kevin K.A.; Drakeley, Chris J.

    In: PLoS Neglected Tropical Diseases, Vol. 12, No. 6, e0006432, 01.06.2018, p. 1-16.

    Research output: Contribution to journalArticleResearchpeer-review

    TY - JOUR

    T1 - Exposure and infection to Plasmodium knowlesi in case study communities in Northern Sabah, Malaysia and Palawan, The Philippines

    AU - Fornace, Kimberly M.

    AU - Herman, Lou S.

    AU - Abidin, Tommy R.

    AU - Chua, Tock Hing

    AU - Daim, Sylvia

    AU - Lorenzo, Pauline J.

    AU - Grignard, Lynn

    AU - Nuin, Nor Afizah

    AU - Ying, Lau Tiek

    AU - Grigg, Matthew J.

    AU - William, Timothy

    AU - Espino, Fe

    AU - Cox, Jonathan

    AU - Tetteh, Kevin K.A.

    AU - Drakeley, Chris J.

    PY - 2018/6/1

    Y1 - 2018/6/1

    N2 - Background: Primarily impacting poor, rural populations, the zoonotic malaria Plasmodium knowlesi is now the main cause of human malaria within Malaysian Borneo. While data is increasingly available on symptomatic cases, little is known about community-level patterns of exposure and infection. Understanding the true burden of disease and associated risk factors within endemic communities is critical for informing evidence-based control measures. Methodology/Principal findings: We conducted comprehensive surveys in three areas where P. knowlesi transmission is reported: Limbuak, Pulau Banggi and Matunggung, Kudat, Sabah, Malaysia and Bacungan, Palawan, the Philippines. Infection prevalence was low with parasites detected by PCR in only 0.2% (4/2503) of the population. P. knowlesi PkSERA3 ag1 antibody responses were detected in 7.1% (95% CI: 6.2–8.2%) of the population, compared with 16.1% (14.6–17.7%) and 12.6% (11.2–14.1%) for P. falciparum and P. vivax. Sero-prevalence was low in individuals <10 years old for P. falciparum and P. vivax consistent with decreased transmission of non-zoonotic malaria species. Results indicated marked heterogeneity in transmission intensity between sites and P. knowlesi exposure was associated with agricultural work (OR 1.63; 95% CI 1.07–2.48) and higher levels of forest cover (OR 2.40; 95% CI 1.29–4.46) and clearing (OR 2.14; 95% CI 1.35–3.40) around houses. Spatial patterns of P. knowlesi exposure differed from exposure to non-zoonotic malaria and P. knowlesi exposed individuals were younger on average than individuals exposed to non-zoonotic malaria. Conclusions/Significance: This is the first study to describe serological exposure to P. knowlesi and associated risk factors within endemic communities. Results indicate community–level patterns of infection and exposure differ markedly from demographics of reported cases, with higher levels of exposure among women and children. Further work is needed to understand these variations in risk across a wider population and spatial scale.

    AB - Background: Primarily impacting poor, rural populations, the zoonotic malaria Plasmodium knowlesi is now the main cause of human malaria within Malaysian Borneo. While data is increasingly available on symptomatic cases, little is known about community-level patterns of exposure and infection. Understanding the true burden of disease and associated risk factors within endemic communities is critical for informing evidence-based control measures. Methodology/Principal findings: We conducted comprehensive surveys in three areas where P. knowlesi transmission is reported: Limbuak, Pulau Banggi and Matunggung, Kudat, Sabah, Malaysia and Bacungan, Palawan, the Philippines. Infection prevalence was low with parasites detected by PCR in only 0.2% (4/2503) of the population. P. knowlesi PkSERA3 ag1 antibody responses were detected in 7.1% (95% CI: 6.2–8.2%) of the population, compared with 16.1% (14.6–17.7%) and 12.6% (11.2–14.1%) for P. falciparum and P. vivax. Sero-prevalence was low in individuals <10 years old for P. falciparum and P. vivax consistent with decreased transmission of non-zoonotic malaria species. Results indicated marked heterogeneity in transmission intensity between sites and P. knowlesi exposure was associated with agricultural work (OR 1.63; 95% CI 1.07–2.48) and higher levels of forest cover (OR 2.40; 95% CI 1.29–4.46) and clearing (OR 2.14; 95% CI 1.35–3.40) around houses. Spatial patterns of P. knowlesi exposure differed from exposure to non-zoonotic malaria and P. knowlesi exposed individuals were younger on average than individuals exposed to non-zoonotic malaria. Conclusions/Significance: This is the first study to describe serological exposure to P. knowlesi and associated risk factors within endemic communities. Results indicate community–level patterns of infection and exposure differ markedly from demographics of reported cases, with higher levels of exposure among women and children. Further work is needed to understand these variations in risk across a wider population and spatial scale.

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