Plasmodium interspecies interactions during a period of increasing prevalence of Plasmodium ovale in symptomatic individuals seeking treatment: an observational study

Akala, Hoseah M.; Watson, Oliver; Mitei, Kenneth K.; Juma, Dennis W.; Verity, Robert; Ingasia, Luicer A.; Opot, Benjamin; Okoth, Raphael; Chemwor, Gladys; Juma, Jackline A.; Mwakio, Edwin W.; Brazeau, Nicholas F.; Cheruiyot, Agnes C.; Yeda, Redemptah; Maraka, Maureen N.; Okello, Charles O.; Kateete, David Patrick; Managbanag, Jim Ray; Andagalu, Ben; Ogutu, Bernhards; Kamau, Edwin

doi:10.1016/s2666-5247(21)00009-4

Cited by 40 publications

(57 citation statements)

References 32 publications

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“…Sensitivity of light microscopy was estimated to be considerably lower for P. knowlesi, P. malariae , and P. ovale than for P. falciparum and P. vivax . This suggests that the burden of P. knowlesi, P. malariae , and P. ovale in a clinical setting may be appreciably underestimated, consistent with a recent study of P. ovale in health clinics in Kenya 4 .…”

Section: Discussionsupporting

confidence: 86%

“…Given their contribution to the global burden of malaria, P. falciparum and P. vivax remain the primary focus of public health efforts aimed at achieving malaria elimination and eradication 3 . However, three additional Plasmodium species— P. knowlesi, P. malariae , and P. ovale —also cause clinical episodes of malaria, though their overall burden remains uncertain due in part to routine misdiagnosis in a clinical setting 4 .…”

Section: Introductionmentioning

confidence: 99%

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The impact of emerging Plasmodium knowlesi on accurate diagnosis by light microscopy: a systematic review and modelling analysis

Huber

Elliott

Koepfli

et al. 2021

Preprint

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Background The five Plasmodium spp. that cause human malaria appear similar under light microscopy, which raises the possibility that misdiagnosis could routinely occur in clinical settings. Assessing the extent of misdiagnosis is of particular importance for monitoring P. knowlesi, which co-circulates with the other Plasmodium spp. Methods We performed a systematic review and meta-analysis of studies comparing the performance of microscopy and PCR for diagnosing malaria in settings with co-circulation of the five Plasmodium spp. We assessed the extent to which co-circulation of Plasmodium parasites affects diagnostic outcomes. We fit a Bayesian hierarchical latent class model to estimate variation in microscopy sensitivity and specificity. Results Mean sensitivity of microscopy was low, yet highly variable across Plasmodium spp., ranging from 41.7% (95% CI: 22.8 - 64.1%) for P. falciparum and 40.3% (22.0 - 61.5%) for P. vivax to 0.119% (0.0121 - 0.640%) for P. knowlesi, 7.57% (2.66 - 22.0%) for P. malariae, and 0.180% (0.00491 - 1.21%) for P. ovale. Observed PCR prevalence was positively correlated with estimated microscopic sensitivity and negatively correlated with estimated microscopic specificity, though the strength of the associations varied by species. Conclusions Our analysis suggests that co-circulation of Plasmodium spp. undermines the accuracy of microscopy. Sensitivity was considerably lower for P. knowlesi, P. malariae, and P. ovale. The negative association between specificity and PCR prevalence imply that less frequently encountered species may be misdiagnosed as more frequently encountered species. Together, these results suggest that the burden of P. knowlesi, P. malariae, and P. ovale may be underappreciated in a clinical setting.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

The impact of emerging Plasmodium knowlesi on accurate diagnosis by light microscopy: a systematic review and modelling analysis

Huber

Elliott

Koepfli

et al. 2021

Preprint

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“…These observations, along with the relatively high proportion of P. falciparum/P. ovale co-infections in October–November and reported in other studies [ 2 , 5 , 6 ], suggest that the two parasite species are frequently co-transmitted in the same mosquitoes, a phenomenon we also observed in two DFA participants.…”

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confidence: 88%

Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania

et al. 2022

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Background Plasmodium ovale is a neglected malarial parasite that can form latent hypnozoites in the human liver. Over the last decade, molecular surveillance studies of non-falciparum malaria in Africa have highlighted that P. ovale is circulating below the radar, including areas where Plasmodium falciparum is in decline. To eliminate malaria where P. ovale is endemic, a better understanding of its epidemiology, asymptomatic carriage, and transmission biology is needed. Methods We performed a pilot study on P. ovale transmission as part of an ongoing study of human-to-mosquito transmission of P. falciparum from asymptomatic carriers. To characterize the malaria asymptomatic reservoir, cross-sectional qPCR surveys were conducted in Bagamoyo, Tanzania, over three transmission seasons. Positive individuals were enrolled in transmission studies of P. falciparum using direct skin feeding assays (DFAs) with Anopheles gambiae s.s. (IFAKARA strain) mosquitoes. For a subset of participants who screened positive for P. ovale on the day of DFA, we incubated blood-fed mosquitoes for 14 days to assess sporozoite development. Results Molecular surveillance of asymptomatic individuals revealed a P. ovale prevalence of 11% (300/2718), compared to 29% (780/2718) for P. falciparum. Prevalence for P. ovale was highest at the beginning of the long rainy season (15.5%, 128/826) in contrast to P. falciparum, which peaked later in both the long and short rainy seasons. Considering that these early-season P. ovale infections were low-density mono-infections (127/128), we speculate many were due to hypnozoite-induced relapse. Six of eight P. ovale-infected asymptomatic individuals who underwent DFAs successfully transmitted P. ovale parasites to A. gambiae. Conclusions Plasmodium ovale is circulating at 4–15% prevalence among asymptomatic individuals in coastal Tanzania, largely invisible to field diagnostics. A different seasonal peak from co-endemic P. falciparum, the capacity to relapse, and efficient transmission to Anopheles vectors likely contribute to its persistence amid control efforts focused on P. falciparum. Graphical Abstract

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“…Recent findings suggest declining P. falciparum prevalence in East Africa may be associated with increases in non-falciparum infections [17][18][19][20] . However, comprehensive surveys of non-falciparum malaria in sub-Saharan Africa are infrequent because detection of these species remains challenging 11,17 . Existing field diagnostic methods such as microscopy and pan-Plasmodium spp.…”

Section: Introductionmentioning

confidence: 99%

Non-falciparum malaria infections are as prevalent as P. falciparum among Tanzanian schoolchildren

Sendor

Mitchell

Chacky

et al. 2022

Preprint

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Efforts to achieve malaria elimination need to consider both falciparum and non-falciparum infections. The prevalence and geographic distribution of four Plasmodium species were determined by real-time PCR using dried blood spots collected during the 2017 School Malaria Parasitological Survey of eight regions of Tanzania. Among 3,456 schoolchildren, 22% had P. falciparum, 24% P. ovale spp., 4% P. malariae, and 0.3% P. vivax. Ninety-one percent of P. ovale infections had very low parasite densities, based on amplification at later cycle thresholds. Sixty-four percent of P. ovale infections were single-species, and 35% of these were detected in low malaria endemicity regions. P. malariae infections were predominantly co-infections with P. falciparum (73%). P. vivax was largely detected in northern and eastern regions. Overall, 43% of children with P. falciparum were co-infected with at least one non-falciparum species. A large, previously under-appreciated burden of P. ovale spp. infection exists among Tanzanian schoolchildren.Article SummaryA previously unrecognized burden of non-falciparum malaria infections was detected among Tanzanian schoolchildren in a 2017 cross-sectional study, with P. ovale spp. prevalence comparable to P. falciparum, and low-level prevalences of P. malariae and P. vivax detected.

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Plasmodium interspecies interactions during a period of increasing prevalence of Plasmodium ovale in symptomatic individuals seeking treatment: an observational study

Cited by 40 publications

References 32 publications

The impact of emerging Plasmodium knowlesi on accurate diagnosis by light microscopy: a systematic review and modelling analysis

The impact of emerging Plasmodium knowlesi on accurate diagnosis by light microscopy: a systematic review and modelling analysis

Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania

Non-falciparum malaria infections are as prevalent as P. falciparum among Tanzanian schoolchildren

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