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Wild Chimpanzees Infected with Five Plasmodium Species
Courtesy Emerging Infectious Diseases: (CDC)
Original Article Here
DOI: 10.3201/eid1612.100424
Suggested citation for this article: Kaiser M, L?wa A, Ulrich M, Ellerbrok, Goffe AS, Blasse A, et al. Wild chimpanzees infected with 5 Plasmodium species. Emerg Infect Dis. 2010 Dec; [Epub ahead of print]
Wild Chimpanzees Infected with 5 Plasmodium Species
Marco Kaiser, Anna L?wa, Markus Ulrich, Heinz Ellerbrok, Adeelia S. Goffe, Anja Blasse, Zinta Zommers, Emmanuel Couacy-Hymann, Fred Babweteera, Klaus Zuberb?hler, Sonja Metzger, Sebastian Geidel, Christophe Boesch, Thomas R. Gillespie, and Fabian H. Leendertz
Author affiliations: Robert Koch-Institute , Berlin, Germany (M. Kaiser, A. L?wa, H. Ellerbrok, A.S. Goffe, A. Blasse, F.H. Leendertz); GenExpress GmbH, Berlin (M. Kaiser, M. Ulrich); University of Oxford, Tubney Abingdon, UK (A.S. Goffe, Z. Zommers); LANADA/LCPA, Bi ngerville, C?te d'Ivoire (E. Couacy-Hymann); Budongo Conservation Field Station, Masindi, Uganda (F. Babweteera, K. Zuberb?hler); Un iversity of St. Andrews, St. Andrews, Scotland, UK (K. Zuberb?hler); Max-Planck-Institute for Evolutionary Anth ropology, Leipzig, Germany (S. Metzger, S. Geidel, C. Boesch, F.H. Leendertz); and Emory University , Atlanta, Georgia, USA (T.R. Gillespie)
Data are missing on the diversity of Plasmodium spp. infecting apes that live in their natural habitat, with limited possibility of human-mosquito-ape exchange. We surveyed Plasmodium spp. diversity in wild chimpanzees living in an undisturbed tropical rainforest habitat and found 5 species: P. malariae , P. vivax, P. ovale , P. reichenowi , and P. gaboni.
Despite ongoing and, in some regions, escalating morbidity and mortality rates associated with malaria-causing parasites, the evolutionary epidemiology of Plasmodium spp. is not well characterized. Classical studies of the blood pathogens of primates have found protozoa resembling human malaria parasites in chimpanzees and gorillas ( 1 ); however, these studies were limited to microscopy, negating conclusions regarding evolutionary relationships between human and ape parasites. Recent studies that used molecular approaches showed that captive and wild chimpanzees ( Pan troglodytes ) and lowland gorillas ( Gorilla gorilla ), as well as captive bonobos ( Pan paniscus ), harbor parasites broadly related to P. falciparum ( 2-5 ); wild and captive gorillas
and captive bonobos and chimpanzees are sometimes infected with P. falciparum itself ( 4-6 ). Further, captive chimpanzees and bonobos have been shown to have malaria parasites related to human P. ovale and P. malariae ( 6 - 8 ); P. vivax has been identified in various monkeys and 1 semiwild chimpanzee ( 5,9 ). Recently, P. knowlesi , a simian malaria species, became the fifth human-infecting species ( 10 ), highlighting the possibility of transmission of new Plasmodium spp. from wild primates to humans.
The Study
To investigate the prevalence of different Plasmodium spp. in wild great apes living in their natural habitat (tropical rainforests), we analyzed tissue samples from 16 wild West African chimpanzees that died primarily of anthrax or respiratory disease in Tai National Park, C?te d'Ivoire. A generic real-time PCR that detects all known Plasmodium spp. was used to test all samples for the parasite. Sequence analysis of the CytB gene and small subunit rRNA genes was conducted for real-time PCR-positive samples to determine the strain present; 1,140 bp of the CytB gene and 765 bp of the 18S gene of the plasmodium genome were amplified by classic PCR. Resulting products were sequenced either directly or after cloning for rRNA gene and when initial sequence information showed the possible presence of 2 different strains (Table). Phylogenetic analyses of sequences obtained confirmed the presence of 5 species: P. reichenowi and P. gaboni , which had been found previously ( 2,3 ); but also P. vivax , P. ovale, and P. malariae -like strains (Figures 1, 2). The most prevalent species was P. reichenowi (6/16), which had representatives in subclusters P. gaboni and P. reichenowi . The other species were rare, seen only 1 ( P. ovale and P. vivax ) or 2 ( P. malariae ) times. Two chimpanzees showed co- infections with multiple Plasmodium spp. (Figures 1, 2), 1 infected with P. reichenowi and a P. malariae -like strain and the other with P. reichenowi and P. gaboni .
Is the observed high prevalence of Plasmodium s pp. typical for wild chimpanzees or related to reduced immune function associated with the severe infection that was the primary cause of death in each case? To investigate this question, we tested DNA extracted from fecal samples of apparently healthy chimpanzees collected over the past 8 years (n = 30) ( 13 ) of the same study population by using the generic real -time PCR followed by amplification of the CytB gene. Of these samples, 21 (70%) were positive for Plasmodium spp. by real-time PCR. Because of low copy numbers in feces, phylogentic analyses were limited to 2 samples in which P. reichenowi of the P. gaboni subcluster was confirmed.
To determine if the observed high prevalence of plasmodia was a site- or chimpanzee subspecies-specific phenomenon, we tested 30 randomly selected fecal samples of individually known apparently healthy wild Eastern chimpanzees from the Budongo Forest in Uganda. Overall prevalence of Plasmodium spp. was lower than in West African chimpanzees but still relatively high (40%); P. reichenowi and P. gaboni were identified in 3 samples. Our results demonstrate that the prevalence of different Plasmodium spp. in wild chimpanzees is similar to that of untreated human populations in sub-Saharan Africa (www.who.int/malaria). Throughout sub-Saharan Africa, P. falciparum is more predominant in humans than other Plasmodium spp. Considering the lack of clinical signs of malaria in chimpanzees from which fecal samples were collected and those that had died of respiratory disease or anthrax, Plasmodium spp. infections appear to be asymptomatic or at least nonlethal in wild chimpanzees. However, signs of illness are rarely observed in wild primates because infected animals often mask weakness to maintain social position and avoi d attack by predators (11). Recently developed technologies for the noninvasive determination of temperature in wild chimpanzees may enable more effective examination of the relationship between the primary clinical feature of malaria (i.e., cyclical fevers) and Plasmodium spp. infection ( 12 ). P. ovale was previously described from captive chimpanzees and P. malariae from captive chimpanzees and captive bonobos have been described ( 5-8 ). Our study results demonstrate that P. malariae and P. ovale occur in wild chimpanzees that inhabit pristine contiguous forest with extremely limited exposure to humans, suggesting the natural existence of these parasites in wild great apes.
Because of a Duffy-negative condition in 95%-99% of the human population in western and central continental Africa, transmission of P. vivax does not seem to occur. However, P. vivax infections are common in travelers returning from these areas ( 13 ). Even though we cannot totally exclude the possibility of introduction of P. vivax in the chimpanzee population through humans, our discovery of P. vivax in wild chimpanzees living exclusively within their natural habitat suggests that wild African apes may be a natural reservoir.
Our study shows the existence of P. reichenowi and related strains in wild chimpanzees as described for chimpanzees and gorilla by others ( 2-4,6 ). Infections with strains of the P. reichenowi group (sometimes referred to as the species P. gaboni , P. billbrayi, and P. billcollinsi ) appear to occur widely in wild and captive great apes in Africa with some variation between chimpanzee subspecies from biogeographically distinct sites. The wild chimpanzees examined demonstrated no inf ections with classic human P. falciparum . This lack of infection is likely caused by low human presence in their habitat and, consequently, few or no infected vectors, low sample size, or a missing receptor in chimpanzees ( 14 ). More investigations are needed because recently P. falciparum infections have been described for 2 captive chimpanzees ( 6 ). The situation is clearer for captive and wild lowland gorillas ( Gorilla gorilla ) for which infections and receptors have recently been described ( 4 ). Infections have also been documented for captive bonobos ( 5 ).
Conclusions
Previous examination of the role of our clos est phylogenetic relatives, the great apes, in the evolution and persistence of human plasmodia has been limited by a lack of data from wild ape populations where opportunities for human-mosquito-ape malaria exchange are minimal. Interpretation of patterns of malaria infection in captive ape populations, such as sanctuaries and zoos, must consider the ample opportunities for human-to-ape transmission of such parasites, negating the opportunity to investigate the evolutionary origins and public health-related risks of these parasites. Conversely, our examination of these parasites in wild chimpanzees with no contact to the periphery of the rainforest habitat (online Technical Appendix Figure, www.cdc.gov/EID/content/ 16/12/pdfs/10-0424-Techapp.pdf ) demonstrates that these apes are most likely naturally infected with P. ovale , P. vivax, and P. malariae , 3 types of plasmodia rarely observed in humans of the region. Whether wild great apes are the origin or reservoirs of these Plasmodium types requires further investigation. These results may have implications for global efforts to eradicate malaria in humans, including vaccine development based on animal variants of human parasites .
Addendum
While this article was in press, Liu et al. published a study showing strong evidence that P. falciparum originated in gorillas ( 15 ). Their study also recovered other plasmodia, complementing our findings. As recommended in our conclusions section, the Liu et al. study was based on a large number of samples from wild great apes.
Acknowledgments
We thank the authorities of C?te d'Ivoire for long-term support, especially the Ministry of the Environment and Forests, the Ministry of Research, the directorship of the Tai National Park, and the Swiss Research Centre in Abidjan. In addition, we thank the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for granting us permission to conduct this research, the assistants and students of the each of the chimpanzee projects for support during field observations, R. Wittig and J. Tesch for technical support, and S. Calvignac for phylogenetic analyses and helpful discussion.
This work was supported by the Robert Koch-Institute, the Max-Planck-Society, and Emory University. The Budongo Conservation Field Station receives core funding from the Royal Zoological Society of Scotland and the European Commission Ultra Sensitive Detection of Emerging Pathogens (USDEP) project; LSHB-CT-2006- 037560).
Mr Kaiser is a PhD candidate at the Robert Koch-Institute. He specializes in the development of PCR- based detection methods for various pathogens.
References
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2. Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF, Aminake MN, et al. The origin of malignant malaria. Proc Natl Acad Sci U S A. 2009;106:14902-7. PubMed DOI: 10.1073/pnas.0907740106 3. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, Nkoghe D, et al. A new malaria agent in African hominids. PLoS Pathog. 2009;5:e1000446. PubMed DOI: 10.1371/journal.ppat.1000446 4. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci U S A. 2010;107:1458-63. PubMed DOI: 10.1073/pnas.0914440107
5. Krief S, Escalante AA, Pacheco MA, Mugisha L, Andr? C, Halwax M, et al. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from bonobos. PLoS Pathog. 2010;6:e1000765. PubMed DOI: 10.1371/journal.ppat.1000765 6. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, Goodman SM, et al. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc Natl Acad Sci U S A. 2010; [Epub ahead of print].
7. Duval L, Nerrienet E, Rousset D, Sadeuh SA, Houze S, Fourment M, et al. Chimpanzee malaria parasites related to Plasmodium ovale in Africa. PLoS ONE. 2009;4:e5520. PubMed DOI: 10.1371/journal.pone.0005520
8. Hayakawa T, Arisue N, Udono T, Hirai H, Sattabongkot J, Toyama T, et al. Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees. PLoS ONE. 2009;4:e7412. PubMed DOI: 10.1371/journal.pone.0007412
9. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, Collins WE, et al. A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci U S A. 2005;102:1980-5. PubMed DOI: 10.1073/pnas.0409652102
10. Galinski MRBarnwell JW . Monkey malaria kills four humans. Trends Parasitol. 2009;25:200-4. DOI: 10.1016/j.pt.2009.02.002PubMed
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12. Jensen SA, Mundry R, Nunn CL, Boesch C, Leendertz FH. Non-invasive body temperature measurement of wild chimpanzees using fecal temperature decline. J Wildl Dis. 2009;45:542-6. PubMed
13. Culleton RL, Mita T, Ndounga M, Unger H, Cravo PV, Paganotti GM, et al. Failure to detect Plasmodium vivax in West and Central Africa by PCR species typing. Malar J. 2008;7:174. PubMed DOI: 10.1186/1475-2875-7-174
14. Martin MJ, Rayner JC, Gagneux P, Barnwell JW, Varki A. Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid. Proc Natl Acad Sci U S A. 2005;102:12819-24. PubMed DOI: 10.1073/pnas.0503819102 15. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420-5. DOI: 10.1038/nature09442 Page 6 of 9
Table. Tissue and fecal samples from wild chimpanzees examined for Plasmodium species, Tai National Park, Cote d'Ivoire, and Budongo Forest, Uganda*
Type of sample and name
or species of chimpanzee
Genetic sequence
copies/mg tissue Plasmodium species detected GenBank accession nos. Necropsy
Loukoum 530 P. gaboni GU815507 ( CytB ), GU815523 ( 18S ) Noah 50 P. gaboni GU815508 ( CytB ), GU815524 ( 18S ) Orest 2.2 x 10 P. gaboni GU815509 ( CytB ), GU815525 ( 18S ) Candy 65 P. reichenowi GU815510 ( CytB ), GU815526 ( 18S ) Atra 100 P. reichenowi GU815511 ( CytB ) Louise 160 P. reichenowi GU815512 ( CytB ), GU815527 ( 18S ) EastChip 06 105 P. reichenowi , P. gaboni GU815512_13 ( CytB ) Olduvai 130 P. reichenowi , P. malariae GU815514_15 ( CytB ), GU815528_29 ( 18S ) Leo 850 P. malariae GU815516 ( CytB ), GU815530 ( 18S ) Kady 105 P. ovale GU815517 ( CytB ), GU815531 ( 18S ) Sagu 760 P. vivax GU815518 ( CytB ), GU815532 ( 18S ) Dorry Neg
Virunga Neg
Ophelia Neg
Akruba Neg
Akwaba Neg
Fecal samples, n = 30 Positive qPCR results
P. t. verus 21 (2) P. gaboni GU815519 ( CytB ) P. t. schweinfuthii 12 (3) P. reichenowi P. gaboni GU815520_22 ( CytB ) *All chimpanzees were Pan troglodytes verus from Tai except P. t. schweinfuthii chimpanzees, which were from Budongo Forest. Parentheses indicate the number of samples for which sequences were obtained and used for phylogenetic tree analyses. Neg, negative.
Figure 1. Maximum-likelihood trees of Plasmodium spp. obtained from the analysis of a 1,087-bp CytB alignment. Blue indicates sequences determined from chimpanzee hosts, green bonobos, gray gorillas, and red humans; black indicates sequences obtained from nonprimate hosts. Plasmodium spp. sequences derived from chimpanzees in this study are marked with an asterisk. Bootstrap values are shown when > 70. The tree was rooted using avian plasmodium sequences. Accession numbers of all sequences used are shown in the Table.
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Progress regarding MDGs 3, 4 and 5. Draft conclusions from WHO meeting of national focal points for family and community health in Durres, Albania.
06-10-2010
Government officials, UN agencies and other partners from more than 25 countries met in Durres, Albania last week to take stock of the progress in achieving MDGs 3 (Promote gender equality and empower women), 4 (Reduce child mortality) and 5 (To improve maternal health) in the WHO European Region.
Aims of the meeting
The meeting aimed to achieve four main objectives:
• to present an overview of countries’ progress in achieving MDGs 3, 4 and 5;
• to identify factors and health system actions that contribute to, or obstruct, the achievement of MDGs 3, 4 and 5;
• to identify actions - by the health and other sectors - to exploit best synergies between MDGs 3, 4 and 5, as well as other health-related MDGs;
• to agree on specific steps to be taken at regional, sub-regional and national levels in order to accelerate progress towards MDGs 3, 4 and 5.
• to present an overview of countries’ progress in achieving MDGs 3, 4 and 5;
• to identify factors and health system actions that contribute to, or obstruct, the achievement of MDGs 3, 4 and 5;
• to identify actions - by the health and other sectors - to exploit best synergies between MDGs 3, 4 and 5, as well as other health-related MDGs;
• to agree on specific steps to be taken at regional, sub-regional and national levels in order to accelerate progress towards MDGs 3, 4 and 5.
Draft conclusions
The full report of the meeting is in progress but some of the draft conclusions can be found below:
• Advocates for health must persuade ministers (not just health ministers) in their countries that health is not a deficit model, but is an asset model that contributes enormously to the economic and social prosperity of countries.
• To improve the health of vulnerable groups, the interaction between gender and other social determinants of health, such as income, education, ethnicity and migration status, needs to be well integrated in policies and interventions.
• Under-five mortality reductions are on target in most countries, but neonatal mortality remains a challenge – this has direct links to maternal health.
• Maternal mortality is decreasing throughout the region: actions to ensure that appropriate interventions reach vulnerable women should be accelerated.
• It is important to ensure free reproductive, maternal and child health services at point of access.
• Countries and international partners should give urgent, focused attention to achieving “universal access to reproductive health” (MDG 5b).
• There is an essential requirement to invest in agreed data collection and monitoring systems, with mechanisms being put in place to ensure their use.
• Political commitment to achieving MDGs is high within countries, although that does not guarantee action.
• The specific contribution of civil society in addressing inequities and reaching vulnerable groups is recognized – this needs to be supported by governments.
• Progress has been made in establishing quality assurance mechanisms, but much still needs to be done on this issue across the region.
• Urgent action is needed to develop comprehensive human resource plans that will forecast future workforce needs.
• A broad range of tools on improving maternal and child health is available throughout the region − urgent action is required to scale-up and accelerate their application.
• Progress has been made in increasing the quality of service delivery, but more action is required to promote use of services, particularly by vulnerable groups.
• Issues of equity are paramount: even countries that are doing very well face equity issues with particular groups.
• Education of girls and women is one of the key determinants of maternal and child health.
• Education and access to economic resources are crucial in allowing women to make informed choices regarding their health and the health of their children.
• Existing negative gender norms and values that impact on health, such as gender-based violence and early marriage, need to be challenged by the health sector.
• Economic-security issues for women are linked to education, employment and social protection.
• Maternal and child health services should be equitably represented in decision-making processes on how health budgets are set and priorities identified.
• Multisectoral action is required to tackle inequities. The meeting encourages ministries of health to support and facilitate multisectoral collaboration as a means to improving health and well-being.
• Individuals and communities should be involved in the planning, delivery and monitoring of services.
• To improve the health of vulnerable groups, the interaction between gender and other social determinants of health, such as income, education, ethnicity and migration status, needs to be well integrated in policies and interventions.
• Under-five mortality reductions are on target in most countries, but neonatal mortality remains a challenge – this has direct links to maternal health.
• Maternal mortality is decreasing throughout the region: actions to ensure that appropriate interventions reach vulnerable women should be accelerated.
• It is important to ensure free reproductive, maternal and child health services at point of access.
• Countries and international partners should give urgent, focused attention to achieving “universal access to reproductive health” (MDG 5b).
• There is an essential requirement to invest in agreed data collection and monitoring systems, with mechanisms being put in place to ensure their use.
• Political commitment to achieving MDGs is high within countries, although that does not guarantee action.
• The specific contribution of civil society in addressing inequities and reaching vulnerable groups is recognized – this needs to be supported by governments.
• Progress has been made in establishing quality assurance mechanisms, but much still needs to be done on this issue across the region.
• Urgent action is needed to develop comprehensive human resource plans that will forecast future workforce needs.
• A broad range of tools on improving maternal and child health is available throughout the region − urgent action is required to scale-up and accelerate their application.
• Progress has been made in increasing the quality of service delivery, but more action is required to promote use of services, particularly by vulnerable groups.
• Issues of equity are paramount: even countries that are doing very well face equity issues with particular groups.
• Education of girls and women is one of the key determinants of maternal and child health.
• Education and access to economic resources are crucial in allowing women to make informed choices regarding their health and the health of their children.
• Existing negative gender norms and values that impact on health, such as gender-based violence and early marriage, need to be challenged by the health sector.
• Economic-security issues for women are linked to education, employment and social protection.
• Maternal and child health services should be equitably represented in decision-making processes on how health budgets are set and priorities identified.
• Multisectoral action is required to tackle inequities. The meeting encourages ministries of health to support and facilitate multisectoral collaboration as a means to improving health and well-being.
• Individuals and communities should be involved in the planning, delivery and monitoring of services.
World Health Organisation: Maternal and Newborn Health
Maternal and newborn health
Persisting inequity in maternal health
18-10-2010
Inequities in access to essential health services, particularly reproductive health services and antenatal care, persist in all countries in the WHO European Region. In some of the poorest countries, for example, only 20% of the poorest women have access to at least 4 antenatal care visits during pregnancy, compared to over 80% of the richest women. In all countries, some groups of women are excluded from skilled birth attendance, owing to extreme poverty or discrimination.
Government officials, United Nations agencies and other partners from more than 25 countries met in Durres, Albania on 28–30 September 2010 to take stock of the Region’s progress towards achieving Millennium Development Goals (MDGs) 3–5, for promoting gender equality and empowering women, reducing child mortality and improving maternal health, respectively.
Interrelated MDGs
At the meeting, most countries reported that they are on track to achieve MDGs 4 and 5, but inequalities and inequities between and within countries persist. Progress has been made in reducing mortality in children aged under 5 years, but neonatal mortality remains a problem. The close links between the MDGs make achieving gender equality essential. Promoting girls’ education is a vital part of efforts to reduce child mortality, as deaths in children under 5 are directly linked to mothers’ level of education.
The link between early marriage and pregnancy complications gives another example of the links between the MDGs. Girls in several countries (including Azerbaijan, Ukraine, Albania, the Republic of Moldova and Tajikistan) may be married young. Early pregnancy increases the risk of complications and reduces the possibilities of spacing births (extending the intervals between them to maintain the mother’s health).
The link between early marriage and pregnancy complications gives another example of the links between the MDGs. Girls in several countries (including Azerbaijan, Ukraine, Albania, the Republic of Moldova and Tajikistan) may be married young. Early pregnancy increases the risk of complications and reduces the possibilities of spacing births (extending the intervals between them to maintain the mother’s health).
Member States reported that good policies are in place, but implementation and financing remain a challenge.
Looking beyond the numbers
Eliminating inequities in maternal health requires exploring the social, cultural and contextual reasons for the inequalities. The most recent edition of “Entre Nous”, the European magazine on sexual and reproductive health, explores how various countries throughout the Region are using the “Beyond the Numbers” tool developed by the WHO Making Pregnancy Safer programme.
Beyond the Numbers provides approaches for examining the background of maternal deaths and major complications and defining requirements for further improving the quality of care. These stories – reported through verbal autopsies, confidential inquiries, near-miss case reviews and case audits – provide social and cultural insights that number counting cannot.
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