The silent threat: asymptomatic parasitemia and malaria transmission

Figures & data

Figure 1. The proportion of malaria infections that are asymptomatic compared with population prevalence of malaria across 16 sites in 14 countries.

Error bars correspond to the 95% CI. Hollow and filled shapes indicate diagnosis by microscopy and PCR, respectively. Diamonds, triangles and squares indicate surveys conducted in Asia, Latin America and Africa, respectively.

Data taken from [35,36,51,52,94,114,120,124,126–132].

Figure 2. Studies reporting on the proportion of the asymptomatic population with malaria parasitemia as diagnosed by PCR, by estimated malaria transmission intensity (n = 39).

The top and bottom of the error bars indicate the maximum and minimum malaria prevalence, respectively; the dark line in the box indicates the median prevalence; and the top and bottom of the box indicate the 75th and 25th percentile, respectively.

Data taken from [51–53,77,91,95,98–126].

Figure 3. Proportion of malaria infections detected by PCR that are asymptomatic by age across three studies in five sites.

The error bars correspond to the 95% CI for the proportion.

Data taken from [90,110,131].

Table 1. Examples of diagnostic criteria used for defining malaria patients as asymptomatic.

Study (year), region	Criteria used for identifying asymptomatic malaria cases	Study subjects, sample size (n)	Follow-up protocol and duration	Ref.
Africa
Abdel-Latif et al. (2003), Gabon	No clinical symptoms of malaria with a Plasmodium falciparum positive blood smear, asymptomatic for at least 5 days during follow-up	Children 6 months to 10 years of age (60)	Examined once daily for 7 days; thereafter, once every 2 days	[92]
Rottmann et al. (2006), Tanzania	Presence of P. falciparum on blood smear, axillary temperature of <37.5°C and no other symptoms or signs of malaria	Children 4–59 months of age (127)	No follow-up	[93]
South America
Alves et al. (2002), Brazilian Amazon	Individuals tested positive with microscopy and/or with PCR, and individuals tested negative with microscopy, which subsequently became positive using PCR	All age groups (172)	Follow-up on days 10 and 60	[94]
Cucunubá et al. (2008), Colombia	Presence of patent asexual parasite stages of P. falciparum, Plasmodium vivax or Plasmodium malariae or of mixed infections in blood, which persisted for at least 2 weeks without causing any symptoms, or as the detection of parasite DNA by PCR on day 0 in people who remained asymptomatic during the follow-up period	Individuals 2–78 years of age (21)	Follow-up on days 14 and 28	[95]
Asia
Boutlis et al. (2003), Papua	No fever history or treatment for malaria within the past week, no clinical evidence of malaria or other infection, no diarrhea and no current pregnancy but both P. falciparum- and P. vivax-positive individuals	Adults >16 years of age (105)	Supervised overnight at local health center. A third axillary temperature was recorded the following morning	[96]
de Mast et al. (2010), Indonesia	Presence of asexual P. falciparum or P. vivax parasitemia in the absence of fever (temperature ≤37.9°C) and clinical signs or symptoms that are suggestive for malaria or another infectious disease	Children 5–15 years of age (381)	No follow-up	[97]

A more comprehensive list of studies is given in the supplementary material of [29].

Table 2. Studies reporting on malaria prevalence in asymptomatic individuals diagnosed using PCR.

Study (year), country	Study design	Age group (years)	Patients tested (n)	Patients positive for malaria (%)	Patients positive for Plasmodium falciparum (%)	Patients positive for Plasmodium vivax (%)	Ref.
Low transmission
Fernando et al. (2009), Sri Lanka	Cross-sectional	All age groups	1854	0			[98]
Turki et al. (2012), Iran	Cross-sectional	4–60	500	0			[99]
Zoghi et al. (2012), Iran	Cohort of 500 patients in each of two study areas (three cross-sectional surveys)	2–60+	1000	0			[100]
Atkinson et al. (2012), Solomon Islands	Cross-sectional	All age groups	541	0.6	0	0.6	[101]
Kumudunayana et al. (2011), Sri Lanka	Cross-sectional	All age groups	140	1.4	0	1.4	[102]
Hoyer et al. (2012), Cambodia	Focused screening and treatment	All age groups	6310	1.8	0.9	1.0	[52]
Congpuong et al. (2012), Thailand	Cross-sectional	All age groups	475	1.9			[103]
Diallo et al. (2012), Senegal	Stratified urban sample	2–10	2231	2.2			[104]
Eisele et al. (2011), Haiti	Cross-sectional	All age groups	647	2.2	2.2	0	[105]
Barracks et al. (2010), Vanuatu	Cross-sectional	2–12	4230	2.5			[106]
Hsiang et al. (2010), Uganda	Cohort	1–10	472	3.2	3.2	0	[107]
Harris et al. (2010), Solomon Islands	Cross-sectional	All age groups	8107	3.6			[51]
da Silva et al. (2010), Brazil	Cross-sectional	5+	334	4.8	2.4	2.4	[108]
Kritsiriwuthinan and Ngrenngarmlert (2011), Thailand	Cross-sectional	Adults	241	6.2	3.3	2.5	[109]
Stresman et al. (2010), Zambia	Cohort	All age groups	176	7.4	7.4	0	[91]
Harris (2010), Solomon Islands	Cross-sectional	All age groups	9,491	8.2	4.5	2.8	[51]
Roper et al. (1998), Sudan	Serial cross-sectional studies	All age groups	77	10.4	10.4	0	[110]
Rodulfo et al. (2007), Venezuela	Cross-sectional	All age groups	133	10.5	3.8	6.0	[111]
Gahutu et al. (2011), Rwanda	Cross-sectional	0–5	529	13.2	13.2	0	[112]
Katsuragawa et al. (2010), Brazil	Cross-sectional	5+	324	13.9	1.2	12.7	[113]
Cucunubá et al. (2008), Colombia	Cross-sectional with follow-up on days 14 and 28	All age groups	212	14.6	4.2	9.4	[95]
Camargo et al. (1999), Brazil	Longitudinal	All age groups	169	14.8	0	14.8	[114]
Alves et al. (2002), Brazil	Cross-sectional	All age groups	147	15.0	4.8	9.5	[53]
Färnert et al. (2009), Kenya	Cross-sectional survey with follow-up	0–11	273	16.8	16.8	0	[115]
Moderate transmission
Ladeia-Andrade et al. (2009), Brazil	Five cross-sectional surveys (different villages)	All age groups	644	9.6	3.4	6.2	[116]
Vafa et al. (2008), Senegal	Cross-sectional survey as part of cohort study	2–10	372	13.7	13.7	0	[117]
Suarez-Mutis and Coura (2007), Brazil	Cross-sectional	All age groups	98	20.4	0	20.4	[118]
Baliraine et al. (2009), Kenya	Pooled data from 12 monthly cross-sectional surveys of a cohort	5–14	81	22.6	22.6	0	[119]
Baliraine et al. (2009), Kenya	Pooled data from 12 monthly cross-sectional surveys of a cohort	5–14	81	25.8	25.8	0	[119]
Baliraine et al. (2009), Kenya	Pooled data from 12 monthly cross-sectional surveys of a cohort	5–14	2611	33.3	33.3	0	[119]
Pinto et al. (2000), São Tome and Principe	Cross-sectional	All age groups	81	35.7	28.6	2.4	[120]
Kern et al. (2011), Kenya	Cross-sectional survey with follow-up	0–11	264	36.7	36.7	0	[77]
Crookston et al. (2010), Ghana	Cross-sectional	0–5	84	51.9	51.9	0	[121]
Liljander et al. (2011), Kenya	Cross-sectional	1–6	360	58.9	58.9	0	[122]
High transmission
Koukouikila-Koussounda et al. (2012), Congo	Cross-sectional survey of cohort of children	1–9	313	16.3	16.3	0	[123]
Bereczky et al. (2007), Tanzania	Cross-sectional part of cohort study	1–84	756	38.0	38.0	0	[124]
Dal-Bianco et al. (2007), Gabon	Cross-sectional	18–51	470	51.9	51.9	0	[125]
Pinto et al. (2000), São Tome and Principe	Cross-sectional	All age groups	563	53.3	51.6	2.9	[120]
Owusu-Agyei et al. (2002), Ghana	Cross-sectional	All age groups	297	82.5	82.5	0	[126]

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