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List of Plasmodium species infecting primates

{{Short description|none}}

{{italic title|string=Plasmodium}}

{{Taxobox

| image_caption =

| image =

| domain = Eukaryota

| unranked_regnum = SAR

| unranked_superphylum = Alveolata

| phylum = Apicomplexa

| classis = Aconoidasida

| ordo = Haemosporida

| familia = Plasmodiidae

| genus = Plasmodium

| subdivision_ranks = Species

| subdivision =

Plasmodium billbrayi

Plasmodium billcollinsi

Plasmodium bouillize

Plasmodium brasilianum

Plasmodium bucki

Plasmodium cercopitheci

Plasmodium coatneyi

Plasmodium coulangesi

Plasmodium cynomolgi bastianelli

Plasmodium cynomolgi ceylonensis

Plasmodium cynomolgi cynomolgi

Plasmodium eylesi

Plasmodium falciparum

Plasmodium fieldi

Plasmodium foleyi

Plasmodium fragile

Plasmodium girardi

Plasmodium georgesi

Plasmodium gonderi

Plasmodium gonderi

Plasmodium gora

Plasmodium gorb

Plasmodium inui

Plasmodium jefferyi

Plasmodium joyeuxi

Plasmodium knowlesi

Plasmodium lemuris

Plasmodium malariae

Plasmodium ovale curtisi

Plasmodium ovale wallikeri

Plasmodium percygarnhami

Plasmodium petersi

Plasmodium reichenowi

Plasmodium rodhaini

Plasmodium sandoshami

Plasmodium semnopitheci

Plasmodium schwetzi

Plasmodium silvaticum

Plasmodium simiovale

Plasmodium simium

Plasmodium uilenbergi

Plasmodium vivax

Plasmodium youngei

}}

File:P vivax trophozoite4.jpg]]

The Plasmodium species infecting primates include the parasites causing malaria in humans.

Species infecting humans

= Common infections =

= Rare cases =

While infection of humans by other species is known, they are quite rare, in some instances, only a single case. In a number of the cases, the means of infection is unknown, and may be due to accident, i.e. infection by laboratory equipment or a bite by an animal. With the use of the polymerase chain reaction additional species have been and are still being identified that infect humans.

  • Plasmodium cynomolgi (spp. cynomolgi, bastianellii)
  • Plasmodium inui{{cite journal | author = Coatney GR, Chin W, Contacos PG, King HK | year = 1966 | title = Plasmodium inui, a quartan-type malaria parasite of Old World monkeys transmissible to man | journal = J Parasitol | volume = 52 | issue = 4| pages = 660–666 | doi=10.2307/3276423| jstor = 3276423 | last2 = Chin | last3 = Contacos | last4 = King | pmid = 5969104 }}
  • Plasmodium schwetzi{{cite journal |author=Contacos PG, Coatney GR, Orihel TC, Collins WE, Chin W |title=Transmission of Plasmodium schwetzi from the chimpanzee to man by mosquito bite |journal=Am J Trop Med Hyg |volume=19 |pages=190–5 |year=1970 |pmid=5443069 |issue=2|last2=Coatney |last3=Orihel |last4=Collins |last5=Chin |last6=Jeter |doi=10.4269/ajtmh.1970.19.190 }}{{cite journal |vauthors=Rodhain J, Dellaert R |title=Contribution a l'etude de Plasmodium schwetzi E. Brumpt (2eme note). Transmission de Plasmodium schwetzi a l'homme |pmid=14388460 |trans-title=Study of Plasmodium schwetzi E. Brumpt. II. Transmission of Plasmodium schwetzi to man |language=fr |journal=Ann. Soc. Belg. Med. Trop. |volume=35 |issue=1 |pages=757–75 |year=1955}}
  • Plasmodium semiovale{{citation needed|date=March 2014}}
  • Plasmodium simium{{cite journal |doi=10.1016/S2214-109X(17)30333-9 |pmid=28867401 |title=Outbreak of human malaria caused by Plasmodium simium in the Atlantic Forest in Rio de Janeiro: A molecular epidemiological investigation |journal=The Lancet Global Health |volume=5 |issue=10 |pages=e1038–e1046 |year=2017 |last1=Brasil |first1=Patrícia |last2=Zalis |first2=Mariano Gustavo |last3=De Pina-Costa |first3=Anielle |last4=Siqueira |first4=Andre Machado |last5=Júnior |first5=Cesare Bianco |last6=Silva |first6=Sidnei |last7=Areas |first7=André Luiz Lisboa |last8=Pelajo-Machado |first8=Marcelo |last9=De Alvarenga |first9=Denise Anete Madureira |last10=Da Silva Santelli |first10=Ana Carolina Faria |last11=Albuquerque |first11=Hermano Gomes |last12=Cravo |first12=Pedro |last13=Santos De Abreu |first13=Filipe Vieira |last14=Peterka |first14=Cassio Leonel |last15=Zanini |first15=Graziela Maria |last16=Suárez Mutis |first16=Martha Cecilia |last17=Pissinatti |first17=Alcides |last18=Lourenço-De-Oliveira |first18=Ricardo |last19=De Brito |first19=Cristiana Ferreira Alves |last20=De Fátima Ferreira-Da-Cruz |first20=Maria |last21=Culleton |first21=Richard |last22=Daniel-Ribeiro |first22=Cláudio Tadeu |doi-access=free }}

(Plasmodium brasilianum and Plasmodium rhodiani which have been reported to infect humans, are likely synonymous with P. malariae)

One possible experimental infection has been reported with Plasmodium eylesi. Fever and low grade parasitemia were apparent at 15 days. The volunteer (Dr Bennett) had previously been infected by Plasmodium cynomolgi and the infection was not transferable to a gibbon (P. eylesi 's natural host) so this cannot be regarded as definitive evidence of its ability to infect humans. A second case has been reported that may have been a case of P. eylesi but the author was not certain of the infecting species.{{cite journal |author=Tsukamoto M |title=An imported human malarial case characterized by severe multiple infections of the red blood cells |journal=Ann. Trop. Med. Parasitol. |volume=19 |issue=2 |pages=95–104 |year=1977}}

A possible infection with Plasmodium tenue has been reported.{{cite journal |author=Russel PF |title=Plasmodium tenue (Stephens): A review of the literature and a case report |journal=Am. J. Trop. Med. |volume=s1-8 |issue=5 |pages=449–79 |year=1928|doi=10.4269/ajtmh.1928.s1-8.449 }} This report described a case of malaria in a three-year-old black girl from Georgia, United States, who had never been outside the US. She suffered from both P. falciparum and P. vivax malaria and while forms similar to those described for P. tenue were found in her blood even the author was skeptical about the validity of the diagnosis.

Confusingly Plasmodium tenue was proposed in the same year (1914) for a species found in birds. The human species is now considered to be likely to have been a misdiagnosis and the bird species is described on the Plasmodium tenue page.

= Former names =

Taxonomy in parasitology until the advent of DNA based methods has always been a problem and revisions in this area are continuing. A number of synonyms have been given for the species infecting humans that are no longer recognised as valid.{{cite journal |author=Coatney GR, Roudabush RL |title=A catalog and host-index of the genus Plasmodium |journal=J. Parasitol. |volume=22 |issue=4 |pages=338–53 |year=1936 |doi=10.2307/3271859 |jstor=3271859|last2=Roudabush }} Since perusal of the older literature may be confusing some currently defunct species names are listed here.

{{columns-list|colwidth=18em|

P. camerense

P. causiasium

P. golgi

P. immaculatum

P. laverani var. tertium

P. laverani var. quartum

P. malariae var. immaculatum

P. malariae var. incolor

P. malariae var. irregularis

P. malariae var. parva

P. malariae var. quartanae

P. malariae var. quotidianae

P. perniciosum

P. pleurodyniae

P. praecox

P. quartana

P. quotidianum

P. sedecimanae

P. tenue

P. undecimanae

P. vegesio-tertaniae

P. vivax-minuta

}}

Plasmodium shortii and Plasmodium osmaniae are now considered to be junior synonyms of Plasmodium inui.

= Notes =

;Falciparum

Until recently the only known host of P. falciparum was humans but this species has also been described in gorillas (Gorilla gorilla){{cite journal |vauthors=Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, Etienne L, Mpoudi-Ngole E, Nkoghe D, etal | year = 2010 | title = African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum | journal = Proc. Natl. Acad. Sci. USA | volume = 107 | issue = 4| pages = 1458–1463 | doi=10.1073/pnas.0914440107 | pmid=20133889 | pmc=2824423 | bibcode = 2010PNAS..107.1458P | doi-access = free }} and bonobos{{cite journal |vauthors=Krief S, Escalante AA, Pacheco MA, Mugisha L, André C, Halbwax M, Fischer A, Krief JM, Kasenene JM, Crandfield M, Cornejo OE, Chavatte JM, Lin C, Letourneur F, Grüner AC, McCutchan TF, Rénia L, Snounou G | year = 2010 | title = On the Diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from bonobos | journal = PLOS Pathog | volume = 6 | issue = 2| page = e1000765 | doi=10.1371/journal.ppat.1000765 | pmid=20169187 | pmc=2820532 | doi-access = free }} There has been a single report of P. falciparum in a brown howler monkey (Alouatta guariba) and in black howler monkeys (Alouatta caraya){{cite journal |author=Duarte AM, Malafronte Rdos S, Cerutti C |title=Natural Plasmodium infections in Brazilian wild monkeys: Reservoirs for human infections? |journal=Acta Trop. |volume=107 |issue=2 |pages=179–85 |date=August 2008 |pmid=18620330 |doi=10.1016/j.actatropica.2008.05.020 |last2=Malafronte Rdos |last3=Cerutti Jr |last4=Curado |last5=De Paiva |last6=Maeda |last7=Yamasaki |last8=Summa |last9=Neves Ddo |last10=De Oliveira |last11=Gomes Ade |url=http://patua.iec.gov.br/handle/iec/670 }} but until this is confirmed its validity should be considered dubious.

A possible report of P. falciparum in a greater spot-nosed monkeys (Cercopithecus nictitans) has not been confirmed in a large survey.{{cite journal |vauthors=Ayouba A, Mouacha F, Learn GH, Mpoudi-Ngole E, Rayner JC, Sharp PM, Hahn BH, Delaporte E, Peeters M | year = 2012 | title = Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malarial parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans) | url = https://www.pure.ed.ac.uk/ws/files/9179925/IJP_2012_Sharp.pdf| journal = Int J Parasitol | volume = 42| issue = 8| pages = 709–713 | doi = 10.1016/j.ijpara.2012.05.004 | pmid = 22691606 | pmc = 3751399 | hdl = 20.500.11820/fc884365-2e37-49e2-be1d-823b87492d32 }}

A species that clusters with P. falciparum and P. reichenowi has been identified in Gabon, Africa in chimpanzees (Pan troglodytes).{{cite journal |author=Ollomo B, Durand P, Prugnolle F |title=A new malaria agent in African hominids |journal=PLOS Pathog. |volume=5 |issue=5 | pages=e1000446 |date=May 2009 |pmid=19478877 |pmc=2680981 | doi=10.1371/journal.ppat.1000446 |last2=Durand |last3=Prugnolle |last4=Douzery |last5=Arnathau |last6=Nkoghe |last7=Leroy |last8=Renaud |doi-access=free }} This appears to have diverged from these two species about 21 million years ago. It has only been identified from the sequence of its mitochondrion to date and further work is needed to characterise the species. A second report has confirmed the existence of this species in chimpanzees. A third report has confirmed the existence of this species.{{cite journal |vauthors=Kaiser M, Lowa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, Zommers Z, Couacy-Hymann E, Babweteera F, etal |date=Dec 2010 | title = Wild chimpanzees infected with 5 Plasmodium species | journal = Emerg Infect Dis | volume = 16 | issue = 12| pages = 1956–1959 | doi=10.3201/eid1612.100424|pmid=21122230 | pmc=3294549}}

Night monkeys (Aotus nigriceps) can be infected with P. falciparum. This infection may occur naturally.{{cite journal | last1 = Da Silva | first1 = Araújo M | last2 = Messias | first2 = MR | last3 = Figueiró | first3 = MR | last4 = Gil | first4 = LH | last5 = Probst | first5 = CM | last6 = de Medeiros Vidal | first6 = N | last7 = Katsuragawa | first7 = TH | last8 = Krieger | first8 = MA | last9 = Pereira da Silva | first9 = LH | year = 2013 | title = Natural Plasmodium infection in monkeys in the state of Rondonia (Brazilian Western Amazon) | journal = Malar J | volume = 12 | issue = 1| page = 180 | display-authors = 8|doi=10.1186/1475-2875-12-180 | pmid = 23731624 | pmc = 3680335 | doi-access = free }} Their potential role - if any - as a source of human infection is unknown.

Two additional species within the subgenus Laverania have been identified on the basis of DNA sequences alone: Plasmodium billbrayi and Plasmodium billcollinsi. and bonobos P. billbrayi was found in two subspecies of chimpanzee (Pan troglodytes troglodytes and Pan troglodytes schweinfurthii). P. billcollinsi was found in only one subspecies of chimpanzee (Pan troglodytes troglodytes). Further work is needed to characterise these species.

; Malariae

Humans are currently considered to be the only host for P. malariae. However Rodhain and Dellaert in the 1940s showed with transmission studies that P. malariae was present in chimpanzees.{{cite journal | author = Rodhain J | year = 1940 | title = Les plasmodiums des anthropoids de l'Afrique centrale et leurs relations avec les plasmodiums humains. Récepticité de l'homme au Plasmodium malariae. (Plasmodium rodhaini Brumpt) du chimpanzé | journal = C. R. Soc. Biol. | volume = 133 | pages = 276–277 }}{{cite journal |vauthors=Rodhain J, Dellaert R | year = 1943 | title = L'infection á Plasmodium malariae du chimpanzé chez l'homme. Etude d'une première souche isolée de l'anthropoide Pan satyrus verus | journal = Ann. Soc. Belge. Med. Trop. | volume = 23 | pages = 19–46 }}

The presence of P. malaria in chimpanzees has been reported in Japan suggesting that this species may be able to act as a host.{{cite journal |author=Hayakawa T, Arisue N, Udono T |title=Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees |journal=PLOS ONE |volume=4 |issue=10 |pages=e7412 |year=2009 |pmid=19823579 |pmc=2756624 |doi=10.1371/journal.pone.0007412 |last2=Arisue |last3=Udono |last4=Hirai |last5=Sattabongkot |last6=Toyama |last7=Tsuboi |last8=Horii |last9=Tanabe |bibcode=2009PLoSO...4.7412H |doi-access=free }} A second paper has described the presence of P. malaria in wild chimpanzees. Another paper has reported several cases of P. malariae in brown howler monkey (Alouatta guariba) and black howler monkeys (Alouatta caraya) It has been shown that splectomised three-striped night monkey (Aotus trivirgatus) can be infected with P. malariae.{{cite journal | author = Collins WE, Contacos PG | year = 1969 | title = Infectivity of Plasmodium malariae in the Aotus trivirgatus monkey to Anopheles freeborni mosquitoes | journal = J Parasitol | volume = 55 | issue = 6| pages = 1253–1257 | doi=10.2307/3277270| pmid = 4982903 | jstor = 3277270 | last2 = Contacos }} Another paper has confirmed the presence of P. malaria in chimpanzees.{{cite journal |vauthors=Pacheco MA, Cranfield M, Cameron K, Escalante AA | year = 2013 | title = Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens | journal = Malar J | volume = 12 | issue = 1| page = 328 | doi=10.1186/1475-2875-12-328| pmid = 24044371 | pmc = 3848613 | doi-access = free }}

The existence of multiple independent reports seem to suggest that the chimpanzee and possibly other species may act as a host to P. malaria at least occasionally.

; Vivax

P. vivax will infect chimpanzees. Infection tends to be low grade but may be persistent and remain as source of parasites for humans for some time. P. vivax is also known to infect orangutans{{cite journal |author=Reid MJ, Ursic R, Cooper D |title=Transmission of human and macaque Plasmodium spp. to ex-captive orangutans in Kalimantan, Indonesia |journal=Emerging Infect. Dis. |volume=12 |issue=12 |pages=1902–8 |date=December 2006 |pmid=17326942 |pmc=3291341 |doi=10.3201/eid1212.060191|last2=Ursic |last3=Cooper |last4=Nazzari |last5=Griffiths |last6=Galdikas |last7=Garriga |last8=Skinner |last9=Lowenberger }} and the brown howler monkey (Alouatta guariba clamitans) P. vivax has been reported from chimpanzees living in the wild. It has been suggested that vivax infection of the great apes in Africa may act as a reservoir given the prevalence of Duffy antigen negative humans in this area.{{cite journal |vauthors=Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, Arnathau C, Ngoubangoye B, Menard S, Willaume E, Ayala FJ, Fontenille D, Ollomo B, Durand P, Paupy C, Renaud F | year = 2013 | title = Diversity, host switching and evolution of Plasmodium vivax infecting African great apes | doi = 10.1073/pnas.1306004110| pmid = 23637341 | journal = Proc Natl Acad Sci USA | volume = 110| issue = 20| pages = 8123–8128 | pmc = 3657773| bibcode = 2013PNAS..110.8123P | doi-access = free }}

;Ovale

Like P. vivax, P. ovale has been shown to be transmittable to chimpanzees. P. ovale has an unusual distribution pattern being found in Africa, Myanmar the Philippines and New Guinea. In spite of its admittedly poor transmission to chimpanzees given its discontigous spread, it is suspected that P. ovale may in fact be a zoonosis with an as yet unidentified host. If this is actually the case, the host seems likely to be a primate. A report has been published suggesting that P. ovale may be a natural parasite of chimpanzees{{cite journal |author=Duval L, Nerrienet E, Rousset D |title=Chimpanzee malaria parasites related to Plasmodium ovale in Africa |journal=PLOS ONE |volume=4 |issue=5 |pages=e5520 |year=2009 |pmid=19436742 |pmc=2677663 |doi=10.1371/journal.pone.0005520 |last2=Nerrienet |last3=Rousset |last4=Sadeuh Mba |last5=Houze |last6=Fourment |last7=Le Bras |last8=Robert |last9=Ariey |bibcode=2009PLoSO...4.5520D |doi-access=free }} {{open access}} but this needs confirmation. P. ovale has since been described from chimpanzees living in the wild. This suggests that human infection with this species may as previously suspected be a zoonosis.

It has been recently shown that P. ovale is actually two genetically distinct species that coexist. These species are Plasmodium ovale curtisi and Plasmodium ovale wallikeri.{{cite journal|title=Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally|author=Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S, Dolecek C, Hien TT, do Rosário VE, Arez AP, Pinto J, Michon P, Escalante AA, Nosten F, Burke M, Lee R, Blaze M, Otto TD, Barnwell JW, Pain A, Williams J, White NJ, Day NP, Snounou G, Lockhart PJ, Chiodini PL, Imwong M, Polley SD |journal=J Infect Dis |year=2010 |volume=201 |issue=10 |pages=1544–50 |pmid=20380562 |doi=10.1086/652240 |last2=Tanomsing |last3=Nolder |last4=Oguike |last5=Jennison |last6=Pukrittayakamee |last7=Dolecek |last8=Hien |last9=Do Rosário |last10=Arez |last11=Pinto |last12=Michon |last13=Escalante |last14=Nosten |last15=Burke |last16=Lee |last17=Blaze |last18=Otto |last19=Barnwell |last20=Pain |last21=Williams |last22=White |last23=Day |last24=Snounou |last25=Lockhart |last26=Chiodini |last27=Imwong |last28=Polley |doi-access=free }} These two species separated between 1.0 and 3.5 million years ago.

; Knowlesi

Plasmodium knowlesi has a natural reservoir in the macaques of Southeast Asia, and was only in 1965 identified as being transmissible to humans.

;Other species

The remaining species capable of infecting humans all have other primate hosts.

''Plasmodium'' taxonomy

  • P. cynomolgi - P. cynomolgi bastianelli, P. cynomolgi ceylonensis and P. cynomolgi cynomolgi.
  • P. inui - P. inui inui and P. inui shortii
  • P. knowlesi - P. knowlesi edesoni and P. knowlesi knowlesi.
  • P. ovale - P. ovale curtisi and P. ovale wallikeri
  • P. vivax - P. vivax hibernans, P. vivax chesson and P. vivax multinucleatum.

Interrelatedness - The evolution of these species is still being worked out and the relationships given here should be regarded as tentative. This grouping, while originally made on morphological grounds, now has considerable support at the DNA level.

  • P. brasilianum, P. inui and P. rodhaini are similar to P. malariae (quartan malaria group)
  • P. cynomolgi, P. fragile, P. knowlesi, P. simium and P. schwetzi are similar to P. vivax
  • P. fieldi and P. simiovale are similar to P. ovale
  • P. falciparum is closely related to P. reichenowi.

= Notes =

  • P. kochi has been described as a parasite of monkeys. This species is currently classified as Hepatocystis kochi. This may be subject to revision.
  • P. brasilianum and P. rodhaini seem likely to be the same species as P. malariae.
  • P. lemuris may actually belong to the genus Haemoproteus. Clarification of this point awaits DNA examination.
  • P. shortii is currently (2007) regarded as a junior synonym of P. inui.

=Subspecies=

Many species of Plasmodium which infect primates have been divided into subspecies. Examples are listed below:

class="wikitable collapsible"

! Subspecies infecting primates

*P. cynomolgi — P. cynomolgi bastianelli and P. cynomolgi ceylonensis.

  • P. inui — P. inui inui and P. inui shortii
  • P. knowlesi — P. knowlesi edesoni and P. knowlesi knowlesi.
  • P. vivax — P. vivax hibernans, P. vivax chesson and P. vivax multinucleatum.

Species infecting other hosts

{{lacking overview|section|date=March 2014}}

Most if not all Plasmodium species infect more than one host: the host records shown here should be regarded as incomplete.

It has been proposed that the species P. gora and P. gorb should be renamed P. adleri and P. blacklocki respectively.

Primate groups and Plasmodium species

New World monkeys of the family Cebidae: P. brasilianum and P. simium

Old World monkeys of the family Cercopithecidae: P. coatneyi, P. cynomolgi, P. fieldi, P. fragile, P.gonderi, P. georgesi, P. inui, P. knowlesi, P. petersi, P. shortti and P. simiovale

Gibbons of the family Hylobatidae: P. eylesi, P. hylobati, P. jefferyi and P. youngi

Orangutans (Pongo): P. pitheci and P. silvaticum

Gorillas and chimpanzees: P. billcollini, P. billbrayii, P. falciparum, P. gabonensi, P. gora, P. gorb, P. reichenowi, P. rodhaini and P. schwetzi

Mosquitoes known to transmit human malaria listed by region

{{lacking overview|section|date=March 2014}}

This listing may be incomplete as the taxonomy of this genus is under revision.

North American

Central American

South American

North Eurasian

Mediterranean

Afro-Arabian

Afrotropical

Indo-Iranian

Indo-Chinese hills

Malaysian

Chinese

Australasian

Primate mosquito vectors and associated ''Plasmodium'' species

{{lacking overview|section|date=March 2014}}

References

{{reflist}}

{{DEFAULTSORT:Plasmodium Species Infecting Humans And Other Primates}}

List of Plasmodium species infecting primates

Category:Parasites of primates