Skip to main content

Table 3 Summary of reviewed articles

From: A systematic, realist review of zooprophylaxis for malaria control

References Geographic location Sample Findings Accounted for bed net? Accounted for socio-economic factors? Predominant mosquito species and characteristics (as reported by authors) Animal-related variable Effect
Bogh et al. [11] The Gambia 102 pairs of children An. gambiae s.s. and An. melas: no difference in HBI between cattle and non-cattle group. An. arabiensis: reduction of HBI by 30% in presence of cattle. No significant difference in sporozoite rate of all mosquito species in cattle compounds (0.97%) compared to non-cattle compounds (1.28%) Yes No An. gambiae s.s. (72%), An. arabiensis (10%): relatively zoophilic, An. melas (18%): relatively zoophilic Cattle present: children sleeping <20 m from at least one cow vs cattle absent: children sleeping >50 m from nearest cow (other livestock present but not considered) Zooprophylaxis (An. arabiensis), none (An. gambiae s.s. and An. melas)
Bogh et al. [10] The Gambia 102 pairs of children No difference in parasite prevalence odds ratio between cattle and non-cattle group after adjusting for wealth. Adjusted OR 1.69 (CI 0.67–4.24), p = 0.26 Yes Yes As above As above None
Bouma and Rowland [16] Pakistan 2,042 slides examined over 2 years Higher parasite prevalence in children from households owning cattle (15.2%) than children without (9.5%) Mantel–Haenszel χ2 = 9.6, p < 0.005. Mean parasite rates and prevalence of cattle keeping were positively correlated for seven villages (r = 0.79, p = 0.036) No No Anopheles culicifaces: zoophilic, Anopheles stephensi: zoophilic, Anopheles subpictus: zoophilic Cattle or water buffalo kept within the household compound Zoopotentiation
Bulterys et al. [40] Zambia 34 case households, 27 control households Cattle ownership was associated with reduced odds of recurrent malaria infection (adjusted OR 0.19, CI 0.05–0.69). Households with the most cattle, goats, dogs, or cats had reduced odds of recurrent infection (adjusted OR 0.13, CI 0.03–0.56) Yes No An. arabiensis: anthropophilic/opportunistic, An. funestus Animal ownership (location not measured) Zooprophylaxis
Ghebreyesus et al. [23] Ethiopia 2,114 children (<10 years) Animals sleeping indoors increased the incidence rate ratio for malaria infection (adjusted RR 1.92, CI 1.29–2.85). Cattle ownership was not associated with malaria infection (1–2 cows: aRR 0.75, CI 0.39–1.45; 3–4 cows: aRR 1.18, CI 0.65–2.14; ≥5 cows: aRR 1.18, CI 0.64–2.17) nor was sheep and goat ownership (1-4 sheep/goats: aRR 0.93, CI 0.58–1.50; ≥5 sheep goats: aRR 0.81, CI 0.54–1.22) No Yes An. arabiensis Cattle ownership, sheep and goat ownership, animals sleep inside house Zoopotentiation for animals sleeping indoors. No effect for sheep/goat or cattle ownership.
Habtewold et al. [12] Ethiopia 278 mosquitoes No significant difference in proportion of mosquitoes feeding on humans and livestock for people sleeping with livestock indoors (site B) vs livestock housed separately (site A). Higher proportion of mosquitoes feeding on cattle (93.7%) compared to humans (3.1%) for people sleeping on elevated platforms (site C) above livestock (p < 0.05). Higher proportion of cattle feeding in site C (93.7%) vs sites A (42.7%) and B (54.7%) (p < 0.001) No No An. arabiensis: moderately zoophilic Humans sleep in traditional houses with cattle in separate enclosures (site A), humans sleep in houses with livestock sharing dwelling at night (site B), humans sleep in tree platforms above cattle (site C) Zooprophylaxis
Habtewold et al. [13] Ethiopia 18 study replications, total mosquito catch not reported No effect of untreated ox on HBC for An. arabiensis but ox odour increased HBC (mean catch/person/night = 22 without cattle odour, 32 with, p < 0.05). For An. pharoensis HBC was significantly reduced in the presence of untreated ox (catch/person/night = 50 without and 26 with, p < 0.01) but increased in presence of cattle odour (catch/person/night = 6 without and 18 with, p < 0.001). CIs included but graph printing obscures visualization for most values NA NA An. arabiensis: zoophilic, exophagic. Secondary vector: An. pharoensis “Nearby” specific distance not reported None (An. arabiensis), zooprophylaxis (An. pharoensis)
Hadis et al. [36] Ethiopia 611 An. arabiensis mosquitoes Mosquitoes collected from mixed human-livestock dwellings had significantly lower HBI (20.2%) than mosquitoes collected from human-only dwellings (91.5%) p < 0.001 No No An. arabiensis Human dwellings vs mixed human-cattle dwellings vs cattle sheds Zooprophylaxis
Hewitt et al.a [24] Pakistan 643 anopheline mosquitoes HLC increased in presence of a cow (38%, CI 8–68%), and two goats (50%, CI 16–84%) NA NA An. stephensi: zoophilic A cow or two goats tethered 6 m from male mosquito collectors Zoopotentiation
Hiscox et al. [38] Lao PDR 879 anopheline mosquitoes Cow ownership doubled the risk of anopheline house entry (IRR 2.32, CI 1.29–4.17, p = 0.005) Yes Yes Anopheles philippinensis Ownership of chickens, ducks, pigs, cows, or buffaloes, and keeping large animals (pigs, cows, buffaloes below the house) Zoopotentiation for cow ownership but no effect of owning any other animals or keeping large animals below the house
Iwashita et al. [33] Kenya 104 houses, 1,664 anopheline mosquitoes An. arabiensis abundance increased by 10% with each additional goat/sheep tethered around the house. [Exp (β) = 1.10, β = 0.10, p = 0.02]. Odds of human blood feeding were decreased 0.99 times by each goat or sheep tethered within 500 m of the household [Exp (β) = 0.99, β = −0.01, p < 0.01] Yes No An. arabiensis: zoophilic, exophagic, An. funestus s.s.: anthropophilic, endophagic, An. gambiae s.s. anthropophagic, endophagic Cattle or goats/sheep kept within 20 m of house None (An. gambiae s.s., An. funestus s.s), zoopotentiation (An. arabiensis)
Lardeux et al.a [54] Bolivia 384 blood fed mosquitoes Anopheles pseudopunctipennis preferred small ruminants (forage ratio 1.99, CI 1.80–2.19) to equids (1.95, CI 1.38–2.52) to humans (1.47, CI 1.25–1.69) to cows (1.15, CI 0.65–1.66) and avoided pigs (0.34, CI 0.20–0.48) and chickens (0.03, CI 0–0.75) No No An. pseudopunctipennis: opportunistic Various collection locations including outdoor traps and indoor resting collections Zooprophylaxis
Maia et al.a [21] Ghana 1,017 anopheline mosquitoes Presence of cattle reduced the number of An. gambiae s.s. for HLC by 66% (p < 0.0001) but increased the density of Anopheles ziemanni (not statistically significant). Cattle presence did not influence the HLC number from 20 m away NA NA An. gambiae s.s.: NA, An. ziemanni: zoophilic Cattle inside 6 × 7 m experimental pen Zooprophylaxis (An. gambiae s.s)
Mala et al. [37] Kenya 20 households, 417 mosquitoes Odds of An. arabiensis occurrence decreased in presence of animals (OR 0.4, p = 0.03) and odds decreased with increasing distance to animal shelters (OR = 0.88, p < 0.001) No No An. arabiensis (66%), An. funestus (18%), An. pharoensis (15%) Presence of animals, relative distance to animal sheds Unclear
Mutero et al. [8] Kenya 420 households Low malaria prevalence in irrigated villages compared to non-irrigated villages (p < 0.05). Authors attribute this to preference for cattle feeding by An. arabiensis in the irrigated villages No No An. arabiensis: zoophilic Mean tropical livestock units per village Zooprophylaxis
Palsson et al. [35] Guinea Bissau 30 households Presence of pigs indoors associated with increased mosquito abundance (χ2 = 17.63, p < 0.001) but the presence of goats was not (χ2 = 1.08, p < 0.30). Goats were relatively uncommon compared to pigs (relative prevalence of livestock not reported) No No An. gambiae s.l. (An. gambiae s.s. most abundant) Presence of pigs or goats inside the house Zoopotentiation
Temu et al. [41] Mozambique 8,338 children from 2,748 households Pig keeping associated with increased odds of malaria infection (OR 3.2, CI 2.1–4.9) Yes Yes An. gambiae s.s.: anthropophilic, An. funestus: anthropophilic Children living in households with chickens, goats, sheep, cows, pigs Zoopotentiation
Tirados et al. [34] Ethiopia 63,194 mosquitoes HLC caught significantly more mosquitoes (163 mosquitoes/trap/night) than CBT (26 mosquitoes/trap/night, F = 35.9, p < 0.001) outdoors in areas of high cattle: human ratio compared to areas of low cattle: human ratio (HLC = 3.1, CBT = 2.1, no significant difference reported) NA NA An. arabiensis: anthropophilic, exophagic Cattle: human ratio 0.6:1 vs 17:1. Zoopotentiation
Tirados et al.a [22] Ethiopia Not reported Outdoor HLC of An. arabiensis was not affected by the presence of a surrounding cattle ring, while the presence of a surrounding cattle ring reduced the outdoor HLC for An. pharoensis by 44% (p < 0.05). Indoor HLC did not differ from outdoors for either vector species. The indoor HLC decreased by 49% (p < 0.01) in presence of cattle ring for An. arabiensis. The catch of An. arabiensis in HBT was 25 times greater than in CBT (p < 0.001) whereas, for An. pharoensis there was no significant difference. HBT and CBT catches were unaffected by a ring of cattle for either vector species NA NA An. arabiensis: opportunistic, exophagic Presence of a ring of 20 cattle surrounding the place where a person was (either outside or inside hut) Zooprophylaxis
Yamamoto et al. [43] Burkina Faso 117 cases, 221 controls (women and children <9 years) In univariable analyses, keeping donkeys (OR 0.59, CI 0.34–1.01), rabbits (OR 0.52, CI 0.25–1.09), and pigs (0.26, CI 0.07–0.89) within the compound had a significantly protective effect at the p < 0.20 level. While no effect was found for cows (OR 0.84, CI 0.45–1.54), sheep (OR 0.84, CI 0.51–1.37), goats (OR 0.08, CI 0.60–1.93), or poultry (OR 1.14, CI 0.68–1.90). No difference between malaria cases and controls associated with animal ownership after adjusting for bed net use and level of education (odds ratio of multivariate analysis not reported) Yes Yesb An. gambiae, An. funestus, An. arabiensis Animals kept in compound None
  1. NA not applicable due to nature of study design, HBI human blood index, OBET odor baited entry trap, PSC pyrethrum spray catch, HLC human landing catch, HBT/CBT human/cattle baited trap, OR odds ratio, aRR adjusted rate ratio, CI 95% confidence interval.
  2. aExperimental design, observational design if not otherwise stated.
  3. bControlled for education level.