The primate malaria parasites Plasmodium malariae, Plasmodium brasilianum and Plasmodium ovale spp.: genomic insights into distribution, dispersal and host transitions

Fuehrer, Hans-Peter; Campino, Susana; Sutherland, Colin J.

doi:10.1186/s12936-022-04151-4

Table 2 Geographic distribution and prevalence of P. malariae

From: The primate malaria parasites Plasmodium malariae, Plasmodium brasilianum and Plasmodium ovale spp.: genomic insights into distribution, dispersal and host transitions

Country	Region	Diagnostic Technique	Prevalence	References
Afghanistan	Jalalabad	PCR	0.3% (1/306)	Mikhail et al. 2011	[34]
	Laghman District	Microscopy	1 case	Ramachandra 1951	[35]
	Chardhi	Microscopy	1.4% (1/71 infants)	Ramachandra 1951	[35]
Angola	Bengo povince	PCR	8.1% of malaria positives; 1.3% general	Fancony et al. 2012	[36]
	Luanda	PCR	1.2% (1/81 symptomatic)	Pembele et al. 2015	[37]
Bangladesh	Bandarban	PCR	2.7% (60/2246); 8% of 746 malaria positives; 4.3% of symptomatic patients	Fuehrer et al. 2014	[38]
Belize		MoH official data	0.04% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
Benin		PCR	8.3% (12/144)	Doderer-Lang et al. 2014	[39]
Botswana	Tutume	PCR	0.6% (2/320 asymptomatic)	Motshoge et al. 2016	[40]
	Francistown	PCR	0.5% (1/195 asymptomatic)	Motshoge et al. 2016	[40]
	Kweneng East	PCR	0.4% (3/687 asymptomatic)	Motshoge et al. 2016	[40]
Brazil		MoH official data	0.08% (1990–2008)	Bardach et al. 2015	[31]
	Apiacás—Mato Grosso State	PCR	11.9% (59/497)	Scopel et al. 2004	[41]
	Amazon Region	PCR	33.3% (42/126 malaria positives)	Cunha et al. 2021	[42]
	Espírito Santo	PCR	2.3% (2/92)	de Alencar et al. 2018	[43]
Burkina Faso		PCR	0.1% (1/695 pregnant)	Williams et al. 2016	[44]
	Kossi District	PCR	2.1–13.4% prevalence (decreasing from 2000–2011)	Geiger et al. 2013	[45]
	Bassy and Zanga	PCR	7.4% (8/108) of Pf positives	Culleton et al. 2008	[46]
	Laye	Microscopy	0.9–13.2% (children)	Gnémé et al. 2013	[47]
Burma/Myanmar	Kachin State	PCR	0.1% (3/2598)	Li et al. 2016	[48]
	northern Myanmar	Microscopy	0.04 (2/5585)	Wang et al. 2014	[49]
Burundi	Karuzi	Microscopy	6.7% (228/3393)	Protopopoff et al. 2008	[50]
	Northern Imbo Plain	Microscopy	5% (23/459 malaria positives)	Nimpaye et al. 2020	[51]
Cambodia		PCR	–	Khim et al. 2012	[52]
	Ratanakiri	PCR	2.1% (33/1792)	Durnez et al. 2018	[53]
	2007 Cambodian National Malaria Survey	PCR	0.2% (17/7707)	Lek et al. 2016	[54]
Cameroon		PCR	–	Khim et al. 2012	[52]
	Yaoundé region	PCR	–	Tahar et al. 1998	[55]
	Adamawa region	PCR	17.7% (of 1367)	Feufack-Donfack et al. 2021	[56]
	Yaoundé region	PCR	12% (of 122 asymptomatic children)	Roman et al. 2018	[57]
Central African Republic	Dzanga-Sangha Protected Area	PCR	0.2% (2/95 asymptomatic)	Mapua et al. 2018	[58]
	Dzanga-Sangha region	PCR	11.1% (of 540 symptomatic)	Bylicka-Szczepanowska et al. 2021	[59]
Chad		Microscopy	1 case (infant; mixed with Pf)—imported case in the Netherlands	Terveer et al. 2016	[60]
China	Yunnan	PCR	1% (1/103)	Li et al. 2016	[48]
Colombia	Colombia’s Amazon department	PCR	38.65% (of 1392 symptomatic)	Nino et al. 2016	[61]
		MoH official data	0.03% (1990–2008)	Bardach et al. 2015	[31]
	Colombian Amazon trapezium	PCR	43.2% (862/1995 symptomatic)	Camargo et al. 2018	[62]
Comores	Grande Comore	PCR	0.62% (1/159)	Papa Mze et al. 2016	[63]
Congo DRC	Kinshasa province	PCR	39% asymptomatic and 7% symptomatic (of malaria positives)	Nundu et al. 2021	[64]
		PCR	3.7% (mixed with Pf of malaria positives)	Kiyonga Aimeé et al. 2020	[65]
		PCR	1.5% (1/65; mixed with Pf; asymptomatic children)	Podgorski et al. 2020	[66]
		PCR	4.9% (7/142; 6 mixed with Pf; symptomatic)	Kavunga-Membo et al. 2018	[67]
Congo Republic		PCR	0.9% (8 of 851)	Culleton et al. 2008	[46]
Costa Rica		PCR	4 cases	Calvo et al. 2015	[68]
Cote d'Ivoire		PCR		Khim et al. 2012	[52]
	Yamoussoukro	PCR	1.6% (7/438) febrile; 2.3% (8/346) afebrile	Ehounoud et al. 2021	[69]
Dominican Republic		MoH official data	0.02% (1990–2008)	Bardach et al. 2015	[31]
El Salvador		MoH official data	0.01% of malaria positives (1990–2008); free of malaria since 2021	Bardach et al. 2015	[31]
Equatorial Guinea	Bioko Island (Ureka, Bareso, Sacriba)	PCR	10–31% (asymptomatic < 10 years)	Guerra-Neira et al. 2006	[70]
	Bioko Island	PCR	15.3% (9/59; blood donors)	Schindler et al. 2019	[71]
Eritrea	Eritrean migrants		0.7% (of 146)	Schlagenhauf et al. 2018	[72]
Ethiopia	Southern Ethiopia Omo Nada	PCR	2 mono and 2 mixed with Pf	Mekonnen et al. 2014	[73]
	Amhara Regional State	PCR	0.3% (1/359)	Getnet et al. 2015	[74]
French Guyana		MoH official data	1.39% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
		PCR	Case (GenBank: AF138881)	Fandeur et al. 2000	[7]
Gabon	Franceville	PCR	2.5% (4/162); febrile children	Maghendji-Nzondo et al. 2016	[75]
	Lambarene	PCR	0.5% (1/206)	Culleton et al. 2008	[46]
	Fougamou and villages in the surroundings	PCR	23% (193/834)	Woldearegai et al. 2019	[76]
Gambia		Microscopy	rarely	http://www.rollbackmalaria.org/files/files/countries/Gambia.pdf (accessed: July 25^th, 2017)
Ghana	Kwahu-South	PCR	12.7% (18/142)	Owusu et al. 2017	[77]
		PCR	12.8% (45/352) coinfections with Pf	Culleton et al. 2008	[46]
	Ahafo Ano South District of the Ashanti region	PCR	28% (76/274) school children	Dinko et al. 2013	[27]
Guatemala		MoH official data	0.01% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
Guinea		PCR		Khim et al. 2012	[52]
		Microscopy	0.3% (2/724) in young infants, 12.0% (90/748) in children 1–9 years of age, and 5.8% (43/743) in children 10–15y. 97% (131/135) mixed with Pf	Ceesay et al. 2015	[78]
Guinea-Bissau		PCR		Tanomsing et al. 2007	[79]
	Antula	PCR	18% (of 60) in 1995; 4% (of 71) in 1996	Arez et al. 2003	[80]
Guyana	Georgetown	PCR	3 PCR confirmed cases	Baird et al. 2002	[81]
		MoH official data	0.03% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
Haiti		PCR	Imported to Jamaica	Lindo et al. 2007	[82]
India		PCR	GenBank ID: KU510228	Krishna et al. unpublished
		various	rare	Reviewed in Chatuverdi et al. 2020	[83]
	Odisha	PCR	9.1% (10/110) mono; 10.9% (12/110) mixed; febrile malaria positives	Pati et al. 2017	[84]
Indonesia	Papua	PCR		Tanomsing et al. 2007	[79]
	Flores—Ende District	PCR	1.9% (of 1509)	Kaisar et al. 2013	[85]
	North Sumatra	PCR	3.4% of 3731 participants; 2.9–11.5% of malaria positives	Lubis et al. 2017	[29]
Iran	Baluchestan	PCR	1.4% (2/140)	Adel and Ashgar 2008	[86]
Kenya	Lake Victoria basin Western Kenya	PCR	5.3% (35/663) of asymptomatic infections and 3.3% (8/245) of clinical cases	Lo et al. 2017	[87]
	Kisii district	PCR	11.6% (84 of 722)	Culleton et al. 2008	[46]
Laos		PCR		Tanomsing et al. 2007	[79]
	northern provinces	PCR	0.05% (3/5082); 7.7% of PCR positives for malaria; 2 mono + 1 mixed Pv	Lover et al. 2018	[88]
Liberia	Far	microscopy	39%	Björkman et al. 1985	[89]
		PCR	3 cases imported to China	Cao et al. 2016	[90]
Madagascar		PCR		Khim et al. 2012	[54]
	Ampasimpotsy	PCR	2.1% (12/559 malaria positives)	Mehlotra et al. 2019	[91]
Malawi		PCR	1 case imported to China	Cao et al. 2016	[90]
	Dedza and Mangochi	PCR	9.4% of 2918	Bruce et al. 2011	[92]
Malaysia	Malaysian Borneo	PCR	2.8% (1/47)	Lee et al. 2009	[93]
	Sabah	PCR	0.6% (8/1366); 7 mono + 1 mixed with Pf	William et al. 2014	[94]
	Peninsular Malaysia	PCR	18% (20/111) of malaria positives; 16 mono; 1 with Pf and 3 with Pk	Vythilingam et al. 2008	[95]
Mali		PCR		Khim et al. 2012	[52]
		PCR	14/603; 3 mono, 10 Pf mix, 1 Pf, PoC mix; pregnant	Williams et al. 2016	[44]
	Northern Mali	PCR	9.4–22.5% of malaria positives—asymptomatic	Koita et al. 2005	[96]
Mauritania	Boghe-Sahelian zone	Microscopy	0.03% (1/3445 children); 0.7% (1/143 malaria positives)	Ouldabdallahi Moukah et al. 2016	[97]
	Hodh Elgharbi (Sahelian zone)	Microscopy	1.1% (4/378) of malaria positives febrile patients; 0.3% (4/1161) in febrile patiens	Ould Ahmedou Salem et al. 2016	[98]
Mayotte	Mayotte Island	Microscopy	4% of all malaria positive cases	Maillard et al. 2015	[99]
Mozambique	Manchiana and Ilha Josina	PCR	Manchiana: 19.3% (27/140); Ilha Josina: 28.7% (54/188)	Marques et al. 2005	[100]
Namibia	Bushmanland	Microscopy	rare	mentioned in Noor et al. 2013	[101]
Niger	south-eastern	Microscopy	1.7% of malaria positves	Doudou et al. 2012	[102]
Nigeria	Ibadan area	PCR	11.7% (69/590), children; mainly mixed infections	May et al. 1999	[103]
	Eboyi State	PCR	6.67% mono; 2% mixed with pf of 150 HIV positive patients	Nnoso et al. 2015	[104]
	Lafia	PCR	0.7% (7/960)—3 mono and 4 mixed Pf, asymptomatic children	Oyedeji et al. 2017	[105]
	Ibadan	PCR	66% (352/530) of malaria positive asymptomatic adolescents (ages 10–19 years), mainly mixed	Abdulraheem et al. 2021	[106]
Pakistan		PCR	1 case imported to China	Cao et al. 2016	[90]
		Microscopy	0.4% (2/521) hospitalized patients	Beg et al. 2008	[107]
Panama		MoH official data	0.01% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
			Eradicated?—Last case in 1972	Hurtado et al. 2020	[108]
Papua New Guinea	East Sepik Province	PCR	4.62% (100/2162); 75 mono and 25 mixed	Mehlotra et al. 2000	[109]
		PCR	Oro (0.7%); Eastern Highlands (0.2%); Madang (1.5%); New Ireland (1.3%); East New Britain (0.3%); Bougainville (0.1%)	Hetzel et al. 2015	[110]
Peru	south-east Amerindian population	microscopy	above 80% of all malaria infections	Sulzer et al. 1975	[111]
		MoH official data	0.02% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
Philippines	Palawan	Microscopy	0–0.5%	Oberst et al. 1988	[112]
	Mindanao	PCR	0.03% (1/2639) asymptomatic	Dacuma et al. 2021	[113]
Rwanda	Rukara Health Centre	PCR	1% (1/99)	Culleton et al. 2008	[46]
Sao Tome/Principe	Principe	Microscopy	11 cases	Lee et al. 2010	[114]
Saudi Arabia	Western regions	Microscopy	0.5% (48/8925 malaria positives)	Amer et al. 2020	[115]
Senegal	Kedougou	PCR	GenBank ID: KX417705	unpublished
	southeastern Senegal	PCR	3.3% of 122 asymptomatic participants	Badiane et al. 2021	[116]
Sierra-Leone	Moyamba District	Microscopy	2.1% Pm mono	Gbakima et al. 1994	[117]
	Bo	PCR	0.4% (2/534) febrile patients	Leski et al. 2020	[118]
Somalia		microscopy	5% of all malaria positives	reviewed in Oldfield et al. 1993	[119]
	Imported to USA—marines	microscopy	0.9% (1/106)	Newton et al. 1994	[120]
South Sudan	Jonglei State	microscopy	6 of 392; 7.7% of malaria positives	Omer et al. 1978	[121]
Sudan	Gezira	microscopy	38 of 1987; 4.1% of malaria positives	Omer et al. 1978	[121]
	East Sudan	PCR	case report	Imirzalioglu et al. 2006	[122]
	Red Sea State	microscopy	1.1% (3/283 malaria positives)	Ageep 2013	[123]
Suriname		MoH official data	5.25% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
		microscopy	12% of 86 Pf positives	Peek et al. 2004	[124]
Swaziland		PCR	0.02% (1/4028)	Hsiang et al.2012	[125]
Tanzania	Zanzibar	PCR	24—14 mono and 10 mixed Pf	Xu et al. 2015	[126]
	Zanzibar	PCR	0.5% (3/594) febrile patients but Pf-RDT negative	Baltzell et al. 2013	[127]
	Kibiti District	PCR	2.4% in 2016 (11.3–16.2% in the 1990’s)	Yman et al. 2019	[128]
Thailand		PCR	Various GenBank entries (e.g. EF206337)	Tanomsing et al. 2007	[79]
	Kanchanaburi Province	PCR	0.2% (2/812)	Yorsaeng et al. 2019	[129]
		MoH	2012: 0.3% (48/16196 malaria positives) 2013: 0.5% (80/14740 malaria positives) 2015: 0.2% (26/12637 malaria positives) 2016: 0.2% (26/15451 malaria positives)	Summarized in Yorsaeng et al. 2019	[129]
Timor-Leste		Microscopy	0.57% (6 cases)	Bragonier et al. 2002	[130]
	Imported to Australia		0.6% (3/501 malaria positives from East Timor; 1 mono and 2 mixed)	Elmes 2010	[131]
Togo		PCR		Khim et al. 2012	[52]
		microscopy		Dorkenoo et al. 2016	[132]
Uganda		PCR	GenBank ID:AB354570	Hayakawa et al. 2008	[133]
		PCR	4.8% (48/1000) blood donors; 31.2% of all malaria positives	Murphy et al. 2020	[134]
Vanuatu				Mentioned in Maguire et al. 2006	[135]
Venezuela		PCR	Various; e.g. KM016331	Lalremruata et al. 2015	[13]
	Yanomami villages	PCR	11.8% (75/630); 25 mixed infections	Lalremruata et al. 2015	[13]
		MoH official data	0.09% of malaria positives (1990–2008)	Bardach et al. 2015	[31]
Vietnam		PCR	Various GenBank entries (e.g. EF206329)	Tanomsing et al. 2007	[79]
	Khanh Hoa Province	PCR	4.8% (6/125) malaria positives	Maeno et al. 2017	[136]
	Ninh Thuan Province	PCR	30.4% (204/671) of malaria positives; 95 mono and 109 mixed infections	Nguyen et al. 2012	[137]
Yemen	Taiz-region	Microscopy	0.06% (1/1638) asymptomatic	Al-Eryani et al. 2016	[138]
	highlands	Microscopy	0.2% (1/455) symptomatic; 1.3% (1/78) Plasmodium positives	Al-Mekhlafi et al. 2011	[139]
Zambia	Nchelenge District	Microscopy	0.6% (5/782) Children < 10 years; 2.1%, (5/236) of malaria positives	Nambozi et al. 2014	[140]
	Western and Southern Province	PCR	1.7% (5/304); 2 mono and 3 mixed Pf	Sitali et al. 2019	[141]
	Choma District, Southern Province	PCR	0.2% of 3292 participants; 2 Pm and 5 Pm + Pf; low transmission area	Laban et al. 2015	[142]
Zimbabwe		Microscopy	1.8% of 51,962; 8.3% of malaria infections (1972–1981)	Taylor and Mutambu 1986	[143]

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