Plasmodium species infecting primates

Red blood cell infected with malaria
Plasmodium species infecting primates
Scientific classification
Kingdom: Protista
Phylum: Apicomplexa
Class: Aconoidasida
Order: Haemosporida
Family: Plasmodiidae
Genus: Plasmodium
Species

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

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 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.[4]

A possible infection with Plasmodium tenue has been reported.[5] 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.[6] Since perusal of the older literature may be confusing some currently defunct species names are listed here.

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)[7] and bonobos[8] There has been a single report of P. falciparum in a brown howler monkey (Alouatta guariba) and in black howler monkeys (Alouatta caraya)[9] 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.[10]

A species that clusters with P. falciparum and P. reichenowi has been identified in Gabon, Africa in chimpanzees (Pan troglodytes).[11] 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.[7] A third report has confirmed the existence of this species.[12]

Night monkeys (Aotus nigriceps) can be infected with P. falciparum. This infection may occur naturally.[13] 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.[7] and bonobos[8] 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.[14][15] The presence of P. malaria in chimpanzees has been reported in Japan suggesting that this species may be able to act as a host.[16] A second paper has described the presence of P. malaria in wild chimpanzees.[12] Another paper has reported several cases of P. malariae in brown howler monkey (Alouatta guariba) and black howler monkeys (Alouatta caraya)[9] It has been shown that splectomised three-striped night monkey (Aotus trivirgatus) can be infected with P. malariae.[17] Another paper has confirmed the presence of P. malaria in chimpanzees.[18]

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[19] and the brown howler monkey (Alouatta guariba clamitans)[9] P. vivax has been reported from chimpanzees living in the wild.[12] 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.[20]

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 zooenosis 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[21] but this needs confirmation. P. ovale has since been described from chimpanzees living in the wild.[12] 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.[22] 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

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.

Notes

Subspecies

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

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

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

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

References

  1. ↑ Coatney GR, Chin W, Contacos PG, King HK; Chin; Contacos; King (1966). "Plasmodium inui, a quartan-type malaria parasite of Old World monkeys transmissible to man". J Parasitol. 52 (4): 660–666. doi:10.2307/3276423. JSTOR 3276423.
  2. ↑ Contacos PG, Coatney GR, Orihel TC, Collins WE, Chin W; Coatney; Orihel; Collins; Chin; Jeter (1970). "Transmission of Plasmodium schwetzi from the chimpanzee to man by mosquito bite". Am J Trop Med Hyg. 19 (2): 190–5. PMID 5443069.
  3. ↑ Rodhain J, Dellaert R (1955). "Contribution a l'etude de Plasmodium schwetzi E. Brumpt (2eme note). Transmission de Plasmodium schwetzi a l'homme". Ann. Soc. Belg. Med. Trop. 35: 757–75.
  4. ↑ Tsukamoto M (1977). "An imported human malarial case characterized by severe multiple infections of the red blood cells". Ann. Trop. Med. Parasitol. 19 (2): 95–104.
  5. ↑ Russel PF (1928). "Plasmodium tenue (Stephens): A review of the literature and a case report". Am. J. Trop. Med. s1–8 (5): 449–79.
  6. ↑ Coatney GR, Roudabush RL; Roudabush (1936). "A catalog and host-index of the genus Plasmodium". J. Parasitol. 22 (4): 338–53. doi:10.2307/3271859. JSTOR 3271859.
  7. 1 2 3 Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, Etienne L, Mpoudi-Ngole E, Nkoghe D, et al. (2010). "African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum". Proc. Natl. Acad. Sci. USA. 107 (4): 1458–1463. doi:10.1073/pnas.0914440107. PMC 2824423Freely accessible. PMID 20133889.
  8. 1 2 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 (2010) On the Diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from bonobos. PloS Pathog. 12;6(2):e1000765
  9. 1 2 3 Duarte AM, Malafronte Rdos S, Cerutti C; Malafronte Rdos; Cerutti Jr; Curado; De Paiva; Maeda; Yamasaki; Summa; Neves Ddo; De Oliveira; Gomes Ade (August 2008). "Natural Plasmodium infections in Brazilian wild monkeys: Reservoirs for human infections?". Acta Trop. 107 (2): 179–85. doi:10.1016/j.actatropica.2008.05.020. PMID 18620330.
  10. ↑ Ayouba A, Mouacha F, Learn GH, Mpoudi-Ngole E, Rayner JC, Sharp PM, Hahn BH, Delaporte E, Peeters M (2012) Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malarial parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans). Int J Parasitol
  11. ↑ Ollomo B, Durand P, Prugnolle F; Durand; Prugnolle; Douzery; Arnathau; Nkoghe; Leroy; Renaud (May 2009). "A new malaria agent in African hominids". PLoS Pathog. 5 (5): e1000446. doi:10.1371/journal.ppat.1000446. PMC 2680981Freely accessible. PMID 19478877.
  12. 1 2 3 4 5 6 7 8 9 Kaiser M, Lowa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, Zommers Z, Couacy-Hymann E, Babweteera F, et al. (Dec 2010). "Wild chimpanzees infected with 5 Plasmodium species". Emerg Infect Dis. 16 (12): 1956–1959. doi:10.3201/eid1612.100424. PMID 21122230.
  13. ↑ Da Silva, Araújo M; Messias, MR; Figueiró, MR; Gil, LH; Probst, CM; de Medeiros Vidal, N; Katsuragawa, TH; Krieger, MA; et al. (2013). "Natural Plasmodium infection in monkeys in the state of Rondonia (Brazilian Western Amazon)". Malar J. 12 (1): 180. doi:10.1186/1475-2875-12-180.
  14. ↑ Rodhain J (1940) 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. C. R. Soc. Biol. 133:276-277
  15. ↑ Rodhain J and Dellaert R (1943) L'infection á Plasmodium malariae du chimpanzé chez l'homme. Etude d'une premiére souche isolée de l'anthropoide Pan satyrus verus. Ann. Soc. Belge. Med. Trop. 23:19-46
  16. ↑ Hayakawa T, Arisue N, Udono T; Arisue; Udono; Hirai; Sattabongkot; Toyama; Tsuboi; Horii; Tanabe (2009). "Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees". PLoS ONE. 4 (10): e7412. doi:10.1371/journal.pone.0007412. PMC 2756624Freely accessible. PMID 19823579.
  17. ↑ Collins WE, Contacos PG; Contacos (1969). "Infectivity of Plasmodium malariae in the Aotus trivirgatus monkey to Anopheles freeborni mosquitoes". J Parasitol. 55 (6): 1253–1257. doi:10.2307/3277270. JSTOR 3277270. PMID 4982903.
  18. ↑ Pacheco MA, Cranfield M, Cameron K, Escalante AA (2013) Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malar J 12(1):328
  19. ↑ Reid MJ, Ursic R, Cooper D; Ursic; Cooper; Nazzari; Griffiths; Galdikas; Garriga; Skinner; Lowenberger (December 2006). "Transmission of human and macaque Plasmodium spp. to ex-captive orangutans in Kalimantan, Indonesia". Emerging Infect. Dis. 12 (12): 1902–8. doi:10.3201/eid1212.060191. PMC 3291341Freely accessible. PMID 17326942.
  20. ↑ 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 (2013) Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci USA
  21. ↑ Duval L, Nerrienet E, Rousset D; Nerrienet; Rousset; Sadeuh Mba; Houze; Fourment; Le Bras; Robert; Ariey (2009). "Chimpanzee malaria parasites related to Plasmodium ovale in Africa". PLoS ONE. 4 (5): e5520. doi:10.1371/journal.pone.0005520. PMC 2677663Freely accessible. PMID 19436742.
  22. ↑ 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; Tanomsing; Nolder; Oguike; Jennison; Pukrittayakamee; Dolecek; Hien; Do Rosário; Arez; Pinto; Michon; Escalante; Nosten; Burke; Lee; Blaze; Otto; Barnwell; Pain; Williams; White; Day; Snounou; Lockhart; Chiodini; Imwong; Polley (2010). "Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally". J Infect Dis. 201 (10): 1544–50. doi:10.1086/652240. PMID 20380562.
  23. ↑ Collins WE, Sullivan JS, Nace D, Williams T, Williams A, Barnwell JW; Sullivan; Nace; Williams; Williams; Barnwell (February 2008). "Observations on the sporozoite transmission of Plasmodium vivax to monkeys". J. Parasitol. 94 (1): 287–8. doi:10.1645/GE-1283.1. PMID 18372652.
  24. ↑ Collins WE, Richardson BB, Morris CL, Sullivan JS, Galland GG; Richardson; Morris; Sullivan; Galland (July 1998). "Salvador II strain of Plasmodium vivax in Aotus monkeys and mosquitoes for transmission-blocking vaccine trials". Am. J. Trop. Med. Hyg. 59 (1): 29–34. PMID 9684622.
  25. ↑ Collins WE, Sullivan JS, Nace D; Sullivan; Nace; Williams; Sullivan; Galland; Grady; Bounngaseng (April 2002). "Experimental infection of Anopheles farauti with different species of Plasmodium". J. Parasitol. 88 (2): 295–8. doi:10.1645/0022-3395(2002)088[0295:EIOAFW]2.0.CO;2. JSTOR 3285576. PMID 12054000.
  26. ↑ Collins WE, Morris CL, Richardson BB, Sullivan JS, Galland GG; Morris; Richardson; Sullivan; Galland (August 1994). "Further studies on the sporozoite transmission of the Salvador I strain of Plasmodium vivax". J. Parasitol. 80 (4): 512–7. doi:10.2307/3283184. JSTOR 3283184. PMID 8064516.
  27. ↑ Wharton RH, Eyles DE.; Eyles (1961). "Anopheles hackeri, a vector of Plasmodium knowlesi in Malaya". Science. 134 (3474): 279–80. doi:10.1126/science.134.3474.279. PMID 13784726.
  28. ↑ Vythilingam I, Tan CH, Asmad M, Chan ST, Lee KS, Singh B.; Tan; Asmad; Chan; Lee; Singh (2006). "Natural transmission of Plasmodium knowlesi to humans by Anopheles latens in Sarawak, Malaysia". Trans R Soc Trop Med Hyg. 100 (11): 1087–88. doi:10.1016/j.trstmh.2006.02.006. PMID 16725166.
  29. ↑ Tan CH, Vythilingam I, Matusop A, Chan ST, Singh B; Vythilingam; Matusop; Chan; Singh (2008). "Bionomics of Anopheles latens in Kapit, Sarawak, Malaysian Borneo in relation to the transmission of zoonotic simian malaria parasite Plasmodium knowlesi". Malar. J. 7: 52. doi:10.1186/1475-2875-7-52. PMC 2292735Freely accessible. PMID 18377652.
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