INTRODUCTION
Mosquitoes have consistently been recognized as the most dangerous organisms worldwide. These hematophagous organisms acquire pathogens while feeding on an infected host (either human or animal), then transmit the pathogens to a new host during their next blood meal [1]. Mosquitoes play crucial roles in the transmission of various hazardous diseases and parasites, including malaria, dengue, West Nile virus (WNV), chikungunya, yellow fever, and Zika virus [2,3]. These infections cause a significant number of fatalities annually and result in hundreds of thousands of deaths [4]. Despite extensive research funding and focus, the numbers of cases and fatalities caused by mosquito-borne diseases (MBDs) are increasing in countries with high MBD burden [5]. Because most MBDs currently lack approved vaccines, vector control through environmental management and behavioral modification is the primary approach to prevention [6].
Livestock rearing is critical and essential in urban areas in numerous tropical low- and middle-income nations. This activity supplies highly nutritious food in urban markets and offers livelihood opportunities to urban residents [5,7,8]. Nevertheless, the potential hazards of urban livestock husbandry must be acknowledged, including the transmission of zoonotic illnesses from animals to humans [9]. Pigs, which act as an amplifying host for Japanese encephalitis virus (JEV), and cattle can contribute to mosquito proliferation by providing a blood reservoir [10]. Economically disadvantaged livestock keepers are often susceptible to zoonotic diseases, because of their frequent interactions with livestock, their intake of livestock products, and their limited access to healthcare services for both themselves and their animals [11]. Moreover, rapid expansion of global human populations and urbanization have placed humans, animals, and mosquitoes in proximity, thus heightening humans’ susceptibility to diseases transmitted by mosquitoes [12].
Mosquito vectors can extract blood, which is required for egg production (Fig 1), from both human and non-human hosts, including animals [13,14]. Female mosquitoes locate their hosts by detecting the host’s scent, exhaled CO2, and other host-derived stimuli, such as visual cues in the surrounding environment; subsequently, the mosquitoes track these signals from near or far distances in the direction opposite from the wind [15]. Mosquitoes require a blood meal for egg development [15]. Different mosquito species exhibit diverse blood feeding behaviors: certain species exhibit a distinct preference for feeding solely on people, whereas other species prefer feeding on both animals and humans [13]. The odors emitted by hosts significantly influence the direction of mosquitoes toward hosts [16,17]. Animals’ breath and skin emit scents that influence mosquito behavior during the host search [18]. Adult female mosquitoes use host-emitted odors to seek hosts for blood meals [13,16]. Animal skin secretions have a kairomonal effect that attracts mosquitoes, whereas the volatile compounds in breath have an allomonal effect that repels insects [19]. Extensive research has revealed the relationships between cattle and mosquitoes, and highlighted their importance in the feeding ecology of mosquito vectors [20,21].
Gaining knowledge regarding malaria vectors’ blood feeding preferences and resting behaviors is critical for evaluating and developing effective vector control techniques. The existence of animals, such as cattle, which serve as hosts for blood meals for certain malaria vectors, can influence the dynamics of MBDs (Fig 2). The presence of cattle can provide an adequate supply of blood meals to vectors, thereby decreasing the vectors’ likelihood of biting people. However, the presence of cattle may also increase the number of blood meals available to mosquitoes, thus increasing the lifespan of infectious insects and consequently the likelihood of malaria transmission [22].
Divergent viewpoints have been described regarding the correlation between livestock rearing and the likelihood of MBD transmission. Whereas some research has indicated that maintaining livestock increases the risk of malaria transmission (zoopotentiation effect), others have implied that keeping livestock protects against malaria transmission (zooprophylaxis) [23]. Researchers and public health initiatives have dedicated substantial resources to studying the biology of parasites, vectors, and hosts. However, numerous unanswered concerns remain regarding the effects of local environmental factors on the prevalence of MBDs. Therefore, this article was aimed at evaluating the influence of livestock rearing MBD spread, exploring the feeding preferences of mosquitoes on hosts, examining the effects of livestock rearing on mosquito population density (Fig 2), raising awareness of how to protect the general population and livestock keepers/herders from MBDs, and suggesting additional areas for research.
MATERIALS AND METHODS
A comprehensive search for studies was conducted from June to October of 2024 in databases including PubMed, Google Scholar, BASE, Science Direct, and Semantic Scholar. Research articles, short communications, and conference proceedings were included. No limitations were imposed regarding language (Google Translate was used to translate other languages into English) or publication year.
The search approach entailed choosing suitable terms and phrases pertaining to mosquitoes, animal husbandry, MBDs, and host preference. We used search phrases in combination with Boolean operators (AND, OR, and NOT) to efficiently retrieve pertinent articles. The search string was as follows: (“mosquito” OR “Anopheles” OR “Culex” OR “Aedes”) AND (“livestock” OR “cattle” OR “goat” OR “pigs” OR “horses” OR “donkey” OR “sheep” OR “buffaloes”) AND (“malaria” OR “dengue” OR “Zika virus” OR “West Nile” OR “Japanese encephalitis” OR “chikungunya” OR “yellow fever” OR “Rift valley fever” OR “Saint Louis encephalitis” OR “Usutu virus”).
RESULTS
Our search strategy yielded 134 articles. The studies examined the effects of livestock rearing on mosquito population density and the occurrence of MBDs, as well as the possibility of zooprophylaxis. Livestock refers to the category of animals including large breeding animals, such as cattle, horses, and buffaloes, as well as midsized breeding animals, such as goats, sheep, and pigs [24].
Livestock rearing and mosquito populations
Six investigations identified a direct correlation between the practice of raising cattle in households and an observed rise in the mosquito population. Nguyen-Tien et al. [2] found that houses with animals had higher numbers of trapped mosquitoes, both indoors and outdoors, than those without livestock. That study, conducted in Vietnam, indicated that households with pigs had significantly higher total mosquito numbers, both indoors and outdoors, than those without pigs. Similarly, households with poultry had higher numbers of mosquitoes than those without poultry. Moreover, families that kept animals, specifically pigs, cattle, and poultry, had elevated abundance of Culex mosquitoes. Mwalugelo et al. [23] demonstrated that buildings housing large populations of livestock, particularly cattle, sheep, dogs, goats, and chickens, had a greater abundance of Anopheles mosquitoes, both inside and outside, than households without livestock. According to Nyarobi [25], a greater number of Anopheles spp. was observed in families that kept livestock than in those that did not. In contrast, households without animals had a higher number of Culex mosquitoes than those that kept livestock. Pigs had notable effects on the quantity of mosquitoes found in bedrooms, whereas goats had no discernible influence [26]. Shabani and Mboera [27] demonstrated that urban cattle farming significantly influenced the mosquito population in their study area. The presence of pigs and their quantity in households correlated with increases in mosquito populations. The mosquito species identified in the study area included Culex spp., Aedes spp., and Anopheles spp. However, Lindahl et al. [28] demonstrated that an increase in pig and non-porcine livestock led to an increase in Culex gelidus population in the area and the presence of non-porcine livestock in households.
In contrast, Jakobsen et al. [29] did not find any correlation between the practice of livestock keeping of animals, such as pigs, poultry, and ruminants, and the occurrence of Aedes mosquitoes. Chan et al. [30] observed no notable variations in the average number of malaria-carrying insects per family, regardless of whether the households had cattle. Habtewold [31] found that being near cattle, whether indoors or outdoors, did not appear to increase the mosquito population.
Host preference
Several studies identified cattle as the preferred host for blood feeding by mosquitoes [10,22,32–52]. In contrast, other studies, such as Lutomiah et al. [21], Hewitt et al. [53], and Echodu et al. [54], suggested that mosquitoes prefer goats. Additionally, Lutomiah et al. [21] and Katusi et al. [14] reported a preference for sheep. Humans have also been identified as a preferred host for mosquitoes by Dia et al. [55], Barrera et al. [56], Animut et al. [57], Ngom et al. [58], Meza et al. [47], and Getachew et al. [46]. Yamamoto et al. [59] reported that mosquitoes show a preference for donkeys over other domestic animals. In contrast, Pham-Thann [60] concluded that mosquitoes favor pigs, and Dieng et al. [61] reported that mosquitoes favor birds.
In contrast to other studies, Hiscox et al. [62] found that owning a cow in Lao PDR more than doubles the likelihood of anopheline mosquitoes entering a dwelling. Hasegawa et al. [63] reported that the presence of cows increased human mosquito bites by Japanese encephalitis (JE) vectors. Santos and Borges [64] discovered that the presence of cattle in Brazil changed the organization of the Culicidae population but did not necessarily affect the number of species or the overall abundance.
Minakawa et al. [65] showed that the distance between cattle and households affects the presence of mosquitoes. They observed that larval habitats located further from houses and closer to cowsheds showed fewer Anopheles gambiae larvae. No significant correlation was observed between the density of humans and cows, as well as the distance from houses to cowsheds, and the density of An. gambiae mosquitoes. The presence of cattle was associated with a decrease in the number of An. funestus mosquitoes found indoors, and this decrease was most pronounced when animals were located 1–15 meters from the home. The presence of cattle did not appear to affect the abundance of indoor resting An. gambiae and An. arabiensis, even when the distances between the home and the locations where the animals were kept the previous night were considered.
Rahma et al. [66] conducted a study in Indonesia examining the effects of housing conditions on the interaction between livestock and humans. The study focused on the human biting rates (HBRs) of mosquitoes in three distinct settlements: Maros, Pasangkayu, and North Toraja. The North Toraja and Pasangkayu communities maintain a distinct separation between animals and dwellings, whereas the Maros communities keep livestock animals near, or even underneath, elevated wooden buildings. Maros, where humans and animals coexist, had the highest HBR (77.5 mosquitoes per 1000 people), whereas North Toraja, where humans and animals live separately, had the lowest HBR (5 mosquitoes per 1000 people), and Pasangkayu had an intermediate mosquito population density (13.3 mosquitoes per 1000 people).
The effects of carabao (water buffalo) on the HBR has been examined in a single study [67]. During outdoor collection, the number of mosquitoes that bit humans was much lower in the presence (1353) than the absence (2687) of carabao. The presence of carabao in the Philippines decreased the number of An. flavirostris mosquito bites (617), whereas the absence of carabao nearby increased the number of bites (1052). However, in indoor collecting conditions, contrary results were observed: more mosquitoes were observed biting humans when a carbao was in proximity (809) than when no carabaos were nearby (470). The frequency of An. flavirostris bites increased when a carabao was in proximity (473 bites) and decreased when no carabaos were nearby (327 bites). Dissection of An. flavirostris mosquitoes collected from humans indicated a sporozoite rate of 1.55% (81 of 5210), whereas those collected from traps baited with carabaos had a significantly different sporozoite rate of 0.75% (14 of 1878; p < 0.01).
Malaria parasite prevalence and biting rate
Reports have indicated conflicting findings regarding the influence of livestock-keeping on malaria parasite incidence. Morgan et al. [5], Rowland et al. [68], Semakula et al. [69], Loha [70], and Bøgh et al. [71] found that livestock keeping decreased the incidence of malaria infection, whereas Hasyim et al. [24], Seyoum et al. [37], Ghebreyesus et al. [72], Membala et al. [73], Temu et al. [74], and Bourna and Rowland [75] observed that keeping livestock increased malaria prevalence.
Morgan et al. [5] discovered a link between owning hens and elevated occurrence of P. falciparum infection. However, owning cattle in the Democratic Republic of Congo was associated with diminished risk of Plasmodium falciparum infection. Specifically, the authors observed 9.6 fewer cases of P. falciparum infection per 100 people. In addition, Semakula et al. [69] and Loha [70] found that keeping cattle lowered the risk of malaria by 26%–49%, whereas keeping goats increased the risk by 26%–32%. Furthermore, as the number of animals in the household increased, the risk of contracting malaria decreased, and the number of cases with high-density parasitemia in the cattle group was significantly lower than that in the control group [71]. In addition, Rowland et al. [68] observed a 56% decrease in P. falciparum malaria and a 31% decrease in P. vivax malaria in areas treating cattle by sponging with deltamethrin. The parasite prevalence exhibited similar declines in cross-sectional surveys. In treated villages, the populations of An. stephensi and An. culicifacies showed decreased density and life expectancy. Although the effectiveness of livestock treatment was comparable to that of indoor spraying, it was 80% lower in cost. When implemented in a settlement with a high prevalence of P. falciparum malaria, the occurrence of malaria decreased from 280 to 9 occurrences per 1000 person-years, possibly because cattle served as another source of blood meal for mosquitoes and/or produced skin secretions that attracted mosquitoes.
In contrast, Ghebreyesus et al. [72] found a significantly higher occurrence of malaria among children from households keeping animals indoors rather than providing separate housing for animals in Ethiopia. Similarly, Hasyim et al. [24] found that the presence of pigs, goats, and sheep heightened the probability of acquiring malaria. The presence of animals might potentially have increased the number of carriers of Plasmodium species. Moreover, children in families with animals had elevated malaria parasite rates in their bloodstream, according to Seyoum et al. [37]. Among 36 respondents living near animals, 21 (58.3%) had malaria, and 15 (41.7%) remained unaffected; moreover, among 64 respondents without cattle near their homes, 23 (36%) had malaria, and 41 (64%) remained unaffected. Therefore, a correlation was found between the presence of livestock and the prevalence of malaria in the work area of Wania Health Center. Individuals who kept livestock around their houses had a 1.623 times higher chance of contracting malaria than those who did not [73]. Temu et al. [74] discovered a link between elevated malaria infection risk and keeping farm animals, particularly pigs and, to a lesser extent, sheep. According to a study conducted in Pakistan by Bourna and Rowland [75], families with cattle in their house courtyards had a higher occurrence of malaria than families without animals. Additionally, villages with greater percentages of people owning cattle had higher occurrence of malaria than villages with fewer cattle-owning families. The differences in these observation might be attributable to local environmental conditions, such as sanitation in and around houses and animal pens, cattle population and management practices, geographical location, and the mosquito species involved.
At the household level in Ethiopia, no significant correlation was observed between the risk of malaria and cattle-keeping [30]. Similarly, Bøgh et al. [76] observed no notable differences in the frequencies of P. falciparum sporozoites in mosquitoes collected from cattle compounds versus compounds without cattle.
Goat blood samples obtained in Thailand, Myanmar, Iran, Sudan, and Kenya have been found to have Plasmodium deoxyribonucleic acid [77]. Albadrani and Alabadi [78] examined the occurrence of malaria parasites in infected livestock species such as cattle, buffaloes, sheep, and goats admitted to the Veterinary Teaching Hospital at the University of Mosul in Mosul, Iraq. Every sample contained Plasmodium deoxyribonucleic acid.
Rift Valley fever virus
The presence of Rift Valley fever virus (RVFV) antibodies in humans within a specific area has been associated with the presence of RVFV antibodies in animals in studies conducted by Nyakarahuka et al. [79]. Moreover, Sindato et al. [80], Swai and Schoonman [81], LaBeaud et al. [82,83], and Nansikombi et al. [84] discovered a robust positive association between the percentages of animals testing positive for antibodies and the percentages of humans testing positive for antibodies to RVFV. In Tanzania, greater occurrence of RVFV antibodies in humans and animals has been observed in pastoral areas than in agro-pastoral and smallholder settings. Furthermore, individuals in contact with aborted materials had elevated likelihood of seropositivity [25].
Muturi et al. [85] and Rugarabamu et al. [86] reported that goats had the highest prevalence of RVFV among livestock, probably because of the high seroprevalence in humans with pastoral lifestyles [87]. Moreover, Sumaye et al. [83] and Tigoi et al. [88] reported that households that raise cattle are likely to have at least one person previously infected with RVF. Lutomiah et al. [21] reported that sheep are the main contributors to the spread of RVFV in two areas in Kenya.
In a study by Kumalija et al., 2.3% of Aedes aegypti pools were found to be positive for RVFV through polymerase chain reaction, as compared with 1.5% of Culex pipiens complex pools [89]. Additionally, Cx. pipiens and Cx. antennatus had major roles as carriers during the high transmission of RVFV in Sharqiya, primarily because of goat and sheep rearing [90]. On the basis of the findings from these studies, clear associations have been found between livestock husbandry and RVFV transmission in different locations, although the particular livestock species at a given location influences the prevalence of the virus.
Dengue virus
Although Jakobsen et al. [29] observed no correlations between the practice of livestock keeping and both the occurrence of dengue fever cases and the prevalence of the dengue mosquito vector, Aedes spp., Pham-Thanh et al. [60] discovered a potential indirect association between livestock and the prevalence of other flaviviruses in animals. The overall seroprevalence of flaviviruses in dogs in Hanoi reached a remarkable 70.7%. Dogs kept outdoors showed significantly higher seroprevalence than those kept indoors. Flavivirus seropositivity in households showed a significant correlation with the district’s geographical location, the presence of livestock such as pigs or chickens, a history of MBDs in the household, and mosquito coil burning procedures. Thai et al. [91], in a study in Vietnam, found a modest but notable correlation between the presence of pigs and the occurrence of dengue IgG antibodies in children.
Japanese encephalitis virus
A comprehensive study revealed 99% JEV seroprevalence in pigs in Can Tho City, Vietnam. The researchers collected all mosquito pools testing positive for Cx. tritaeniorhynchus and Cx. quinquefasciatus near pigs. These mosquitoes carried JEV genotypes I and III simultaneously [92]. Moreover, Gingrich et al. [93] extracted JEV from Cx. tritaeniorhynchus and Cx. gelidus mosquitoes collected in the same Bangkok suburb and suggested that presence of pigs might enhance the probability of contacting JEV.
According to Rajendran et al. [94], when approximately one-third of cattle and/or goats in an area have seroconverted to JEV, JE infection risk in the human population is elevated, as indicated by a higher load of JE-infected vectors in the environment or a higher rate of JE seroconversion (SC) in children. The presence of SC in goats indicates a high JE vector infestation in the environment. Thus, screening animals, specifically goats and/or cattle, for SC might provide a straightforward public health measure enabling existing healthcare systems to categorize locations according to JEV infection risk to the human population. In cattle and goats, compared with pigs, the seroprevalence of JE is a more accurate indicator of human infection risk. Peiris et al. [95] observed a significant incidence of JE antibodies in pigs in regions where porcine infection occurs asynchronously over long time periods. Moreover, Nilsson [96] has revealed a JEV seroprevalence exceeding 20% in dogs and 90% in pigs. Lee et al. [97] and Henriksson et al. [98] reported the seroprevalence of JEV in pigs. These studies collectively indicate that, although pigs are major reservoirs for JEV, cattle and goats also play major roles in certain regions.
West Nile virus
Lan et al. [99] found that dogs in in Shanghai, China, have 4.6% WNV-positive blood antibodies, whereas cats have 14.9%. Similarly, Currenti et al. [100] examined 580 animals and found neutralizing antibodies to WNV in 116 of 442 dogs (26%) and 13 of 138 cats (9%). The seroprevalence of WNV was considerably greater in dogs than cats. According to Kile et al. [101], among 246 dogs examined, 44 (18%), had antibodies to WNV. Specifically, 24 dogs (10%) had IgM antibodies, whereas 32 dogs (13%) had IgG antibodies; moreover, 50% of samples testing positive for IgM also tested positive for IgG, whereas 38% of samples testing positive for IgG also tested positive for IgM. The detection of SC occurred 6 weeks before the first documented case of infection in humans [102]. Of 426 dog samples evaluated, 70 tested positive for WNV with enzyme-linked immunosorbent assay (ELISA), accounting for 16.43% of the samples. Ana et al. [103] reported the presence of WNV-specific antibodies in 36% of tested dog sera (68 of 184) and 33.6% of tested horse sera (78 of 232). Ben-Mostafa et al. [104] examined 63 dog blood samples with complement ELISA to detect the presence of WNV antibodies, and identified 19 samples as positive. Molini et al. [105] suggested the utility of dogs as sentinel animals for WNV. The findings from these studies suggest that domestic animals, particularly dogs, might serve as sentinel animals for WNV.
WNV antibodies have been detected in ruminant animals in Egypt, thus indicating the prevalence of the virus. Substantial variations in prevalence have been observed among investigated species, with rates of 22%, 0%, 40%, 3.5%, and 5.3% in cattle, buffaloes, camels, sheep, and goats, respectively [106]. In a study in Ibadan, the prevalence of WNV-HI antibody-positive sera was 6% in cattle, 20% in sheep, 18% in goats, and 26% in camels [107].
According to Abutarbush and Al-Majali, of 253 horses surveyed in Jordan, 63 (24.9%) tested positive for WNV, and none tested positive for IgM antibodies for WNV [108]. In Palestine, 14.7% of 95 sheep and goats tested positive for WNV. Similarly, in Israel and Palestine, 430 of 587 sampled horses, donkeys, and mules were seropositive for WNV [109]. Mazzei et al. [110] found that 95 of 160 analyzed horse sera were positive for WNV. Complement ELISA testing of 574 horse serum samples revealed that 76 (13.2%) tested positive for WNV antibodies. Aharonson-Raz et al. [111] found that 153 of 179 horses tested positive for WNV, accounting for 85.5% of the sample. Selim et al. [112] analyzed 930 horse serum samples and found that 156 sera (16.8%) exhibited antibodies to WNV. The seroprevalence of WNV among horses and donkeys in Bulgaria, as reported by Rusenova et al. [113], was 3.97%. The seroprevalence of WNV among horses in Israel was 84.1% (275 of 327 horses), according to a study by Schvartz et al. [114]. Additionally, the seroprevalence of the Usutu virus was found to be 10.8% (20 of 185 horses). Durand et al. [115] found antibodies targeting WNVNS1 protein in 79% of horse sera. Ozkul et al. [116] detected WNV ribonucleic acid in cases of recent central nervous system infection in both humans and horses in Turkey. Moreover, 31.1% of the horses showed positive results for anti-WNV IgG antibodies. Among the 261 sera tested, 219 (84%) had a neutralizing titer greater than 1:30, according to Benjelloun et al. [117]. Davoust et al. [118] found that the prevalence of WNV infection in donkeys, horses, dogs, goats, cattle, and sheep was 86.2% (25 of 29), 68.7% (44 of 64), 27.3% (3 of 11), 6.9% (2 of 29), 0%, and 0%, respectively. In these studies, regardless of geographic location, horses consistently had high rates of WNV infection. Hence, horses are favorable sentinel animals for WNV.
Researchers have also obtained strains of WNV from ticks known to transmit deadly diseases, including Lyme disease and Powassian virus. Lwande et al. [119] obtained three strains of WNV from fully fed ticks (Amblyomma gemma and Rhipicephalus pulchellus) collected from cattle and warthogs. Nonetheless, no recorded evidence indicates that these animals play roles in the transmission and preservation of the WNV. The findings from this study indicate a need for further study of cross-species viral transmission.
Zooprophylaxis and endectocides
Mahande et al. [120] used odor-baited entry traps (OBETs) to capture mosquitoes, thus revealing compelling evidence that keeping cattle near residential areas provides effective protection against An. arabiensis mosquito bites and consequently decreases malaria occurrence. Mahande et al. [121] also demonstrated that treating cattle with the acaricide deltamethrin protects humans against An. arabiensis by repelling and killing the mosquitoes. St. Laurent et al. [122] revealed that cattle baited tents attract significantly more Anophelines than either human landing collection or human baited tents. Habtewold [36] found that, whereas An. arabiensis mosquitoes exhibited a strong preference for biting humans indoors, the presence of an ox near a person led to a 38% decrease in the number of An. arabiensis mosquitoes biting that person. However, the presence of an ox did not significantly influence the number of An. pharoensis mosquitoes biting humans, because these mosquitoes are attracted primarily to animals. Outdoors, the presence of an ox near a person did not affect the HBC of An. arabiensis but decreased the catches of An. pharoensis by half. Faraji-Fard et al. [123] demonstrated that calf baited net traps achieved significantly greater mosquito (Aedes spp. and Culex spp.) attraction than unbaited nets. In addition, net traps baited with human scent attracted fewer culicid mosquitoes than net traps baited with calf scent. A 46% greater presence of An. pharoensis within tents was observed when animals were placed at a minimum distance of 1 meter from tents than when no livestock were nearby, according to Zeru et al. [124]. Bøgh et al. [76] found that the presence of cattle decreased the human blood index of An. arabiensis from 82% to 52%. The presence of cattle notably increased the proportion of An. gambiae mosquitoes feeding on ruminant animals, from 19% to 29%. Using baited traps, the researchers collected malaria vectors and found that 32.2% were attracted to human-baited traps, whereas 67.8% were attracted to bovine-baited traps [20]. According to Habtewold et al. [125], the presence of an untreated ox near a human had no effect on the number of An. arabiensis mosquitoes caught in human-baited traps. These findings suggest that being close to cattle does not provide any protective effects against malaria transmission by this particular mosquito species. The presence of oxen decreased the capture of An. pharoensis, a secondary carrier of malaria in Ethiopia. These differences among studies on the attractiveness/repellency of mosquito species to different livestock might be attributable to the specific experimental conditions, the species of mosquitoes involved, or the environments in which the studies were conducted.
In contrast, An. arabiensis has been found to exhibit a significantly greater response to human odor than to cow odor or CO2 alone. Also, the response of the mosquitoes to the chicken odor was also significantly higher when compared to CO2 alone [126]. The presence of calves near a human-baited mosquito-electrocuting trap resulted in fewer caught mosquitoes than observed in a similar trap without cattle nearby, probably because the calves served as additional hosts for the mosquitoes and consequently decreased the HBR [127]. Abong’o et al. [128] demonstrated that bovine-scented bait is highly effective in collecting outdoor biting anopheline mosquitoes. Use of cattle-baited odor consistently captured a greater number of Anopheles mosquitoes, particularly An. arabiensis, than the human landing catch method.
Debebe et al. [129] indicated that odor-based mass trapping with synthetic cattle urine for malaria vectors notably decreased the HBR, sporozoite rate, entomological inoculation rate, and prevalence of malaria. Katusi et al. [130] found that the use of a synthetic cattle urine odor lure attracted more An. arabiensis mosquitoes than An. funestus, regardless of the lure amount or the trap’s distance from human dwellings. The lure’s attractiveness to Culex species, in contrast, varied according to on the amount used, regardless of the trapping distance from human dwellings. According to Kweka et al. [131], cow urine clearly affects the selection of egg-laying sites by mosquito species. Dawit et al. [132] evaluated whether An. arabiensis actively engages in puddling on cow urine to acquire nutrients and enhance their life cycle features. An. arabiensis mosquitoes were found to obtain and use bovine urine to enhance their vectorial capacity. Feeding bovine urine to vectors directly affects their ability to transmit diseases by increasing their day survival and population density, and also indirectly affects their flying activity.
Mosquitoes feeding on IVM-BEPO cattle consistently exhibited greater death rates than mosquitoes in the control group. The mortality probabilities of mosquitoes given IVOMEC-D consistently matched those in the control group. Mosquitoes that consumed blood from cattle treated with IVM-BEPO had low survival rates, and most died within 10 days [133]. The administration of therapeutic doses of ivermectin to local Burkinabé Metis cattle caused the blood meals of sympatric An. coluzii females to be poisonous, thus decreasing the survival and reproductive capacity of the mosquitoes that fed on the treated animals for a duration of 28 days [134]. Both ivermectin and fipronil decreased the survival rate of An. arabiensis. Exposure to ivermectin and fipronil increased the mortality rate by 77% and 70% that in the control group, respectively. Furthermore, surviving mosquitoes showed notably decreased ability to reproduce (90% and 60% decrease in fecundity for ivermectin and fipronil, respectively) [135]. Njoroge et al. [136] discovered that the application of deltamethrin to the entire body in cattle resulted in substantially fewer mosquitoes captured on the cows immediately after treatment than 8 days later. Lyimo et al. [137] showed that administering ivermectin to cattle decreased blood meal digestion, egg production, and survival of the An. arabiensis mosquito population in southeastern Tanzania. The administration of ivermectin to cattle decreased the effectiveness of blood meal digestion in An. arabiensis mosquitoes, and diminished their egg production for 2 weeks.
Traps baited with specific chicken volatile compounds, such as isobutyl butanoate, naphthalene, hexadecane, and trans-limonene oxide, as well as generic compounds such as limonene, cis-limonene oxide, and β-myrcene, caught significantly fewer An. arabiensis mosquitoes than negative control traps baited with solvent. Similarly, considerably fewer mosquitoes were caught chicken-baited traps [138].
Aedes spp. show a general preference for human odor over cattle odor. Moreover, An. arabiensis and An. gambiae have strong preferences for humans (as measured by the human blood index). OBETs baited with humans have been found to attract more individuals of these species than those baited with cattle [139]. OBET experiments and comparisons of traps baited with humans and cattle suggested that An. arabiensis has a natural inclination to feed on humans rather than cattle when both options are equally available in southern Ethiopia [140].
No indication of a higher incidence of host-seeking mosquitoes shifting their focus from treated livestock to humans was observed. Nonetheless, deltamethrin had the largest and longest-lasting effects, and decreased the numbers of blood-feeding anopheline and culicine mosquitoes by more than 50% in the first 2 weeks, and to zero after 1 month [141]. Loftin et al. [142], in a study on insecticide treatments for cattle, noted that the treatments influenced Ae. vexans and Psorophora confinnis attractiveness, swelling, and death rate, but had minimal or no effects on fertility or delayed mortality (after 48 hours). Vythilingam et al. [143] determined the duration of cyhalothrin remaining active on cattle. Both Mansonia uniformis and An. dirus exhibited mortality rates exceeding 90% on days 1 and 2 after treatment. An. maculatus showed a mortality rate of 79% on the first day and 69% on the second day. After a 7-day treatment period, the insecticide’s effectiveness significantly declined and became virtually ineffective by day 21. The presence of a significant number of cattle near a person resulted in an approximately 30%–50% decrease in the number of An. arabiensis and An. pharoensis mosquitoes landing on humans [144].
According to Tchouassi et al. [17], traps with a mix of sheep scents and CO2 attracted a greater number of mosquitoes than traditional CO2-baited light traps, thus making them the most effective bait in most situations. These findings verified that scents originating from sheep fur contribute to mosquitoes’ ability to locate their hosts.
DISCUSSION
Global urbanization has placed humans and animals in proximity, thus potentially increasing the likelihood of infectious diseases, such as vector-borne diseases [28,29]. Livestock husbandry can influence the proximity of vectors to humans, by generating more breeding grounds for mosquitoes. Currently, no clear consensus exists regarding the influence of livestock rearing on malaria transmission. Some research has proposed zooprophylactic effects (in which disease carrying vectors are diverted from humans to animals), whereas others have suggested zoopotentiation effects (n which livestock keeping poses a malaria transmission risk) [23]. The transportation of domestic animals has been found to facilitate the spread of some MBDs, such as RVFV, across locations during both outbreaks and periods between epidemics. Around the year 2000, the transportation of animals through trade led to the emergence of RVFV in regions outside of Africa, such as Saudi Arabia and Yemen [145,146]. Theoretically, large populations of livestock and humans in proximity could increase the likelihood of dengue virus (DENV) transmission, particularly if livestock keeping is associated with the presence of breeding grounds for larvae and an increased number of mosquitoes [28]. Hence, greater attention should be paid to the effects of animal husbandry on MBD transmission and mosquito populations.
Four studies have reported the geographical location influences on the contribution of livestock to MBDs (Table 1). In Ethiopia. Seyoum et al. [37] and Ghebreyesus et al. [72] found that the presence of cattle increased malaria incidence, whereas Loha [70] reported the opposite, and Chan et al. [30] found no correlation between cattle populations and malaria prevalence. Bourna and Rowland [75] indicated that cattle increased malaria prevalence, whereas Rowland et al. [68] reported contrary findings. These differences in findings might stem from differences in local environmental factors such as sanitation, geographical regions, livestock management techniques, climatic conditions during the study, and mosquito species. Nonetheless, cattle appeared to increase RVFV infection in humans.
Effects of livestock on MBDs transmission in various geographic locations.
| Country | Cattle | Horses | Buffaloes | Goats | Sheep | Pigs | Reference |
|---|---|---|---|---|---|---|---|
| Burundi, Liberia, Malawi, and Tanzania | M (+) | - | - | - | - | - | Semakula et al. [69] |
| Cambodia | - | - | - | - | - | JEV (+) | Henriksson et al. [123] |
| DR Congo | M (−) | - | - | - | - | - | Morgan et al. [5] |
| Ethiopia | M (+) | - | - | M (+) | - | - | Seyoum et al. [37] |
| Ethiopia | M (+) | - | - | M (−) | M (−) | - | Ghebreyesus et al. [72] |
| Ethiopia | M (−) | - | - | M (−) | M (−) | - | Loha [70] |
| Ethiopia | M (0) | - | - | - | - | - | Chan et al. [30] |
| Gambia | M (−) | - | - | - | - | - | Bøgh et al. [71] |
| Gambia | M (0) | - | - | - | - | - | Bøgh et al. [76] |
| India | JEV (+) | - | - | JEV (+) | - | - | Rajendran et al. [119] |
| Indonesia | - | - | - | M (+) | M (+) | M (+) | Hasyim et al. [24] |
| Indonesia | M (+) | - | - | - | - | - | Membala et al. [73] |
| Kenya | RVFV (+) | - | - | - | - | - | Tigoi et al. [88] |
| Kenya | - | - | - | - | RVFV (+) | - | Lutomiah et al. [21] |
| Kenya | - | - | - | RVFV (+) | RVFV (+) | - | Muturi et al. [85] |
| Kenya | RVFV (+) | - | - | RVFV (+) | - | - | LaBeaud et al. [82] |
| Mozambique | - | - | - | - | M (+) | M (+) | Temu et al. [74] |
| Pakistan | M (+) | - | - | - | - | - | Bourna and Rowland [75] |
| Pakistan | M (−) | - | - | - | - | - | Rowland et al. [68] |
| Sri Lanka | - | - | - | - | - | JEV (+) | Peiris et al. [95] |
| Tanzania | RVFV (+) | - | - | RVFV (+) | RVFV (+) | - | Sindato et al. [80] |
| Tanzania | RVFV (+) | - | - | - | - | - | Swai and Schoonman [83] |
| Tanzania | RVFV (+) | - | - | RVFV (+) | RVFV (+) | - | Ahmed et al. [87] |
| Tanzania | RVFV (+) | - | - | - | - | - | Sumaye et al. [83] |
| Thailand | - | - | - | - | - | JEV (+) | Gingrich et al. [93] |
| Uganda | RVFV (+) | - | - | RVFV (+) | RVFV (+) | - | Myakarahuka et al. [79] |
| Uganda | RVFV (+) | - | - | RVFV (+) | - | - | Nansikombi et al. [84] |
| Vietnam | DENV (0) | - | - | DENV (0) | - | DENV (0) | Jakobsen et al. [79] |
| Vietnam | - | - | - | - | - | DENV (+) | Thai et al. [91] |
| Vietnam | - | - | - | - | - | JEV (+) | Lindahl et al. [92] |
| Vietnam | - | - | - | - | - | JEV (+) | Nilsson et al. [96] |
| Vietnam | - | - | - | - | - | JEV (+) | Lee et al. [97] |
Key: RVFV: Rift Valley fever virus; M: malaria; DENV: dengue virus; JEV: Japanese encephalitis virus; -: decreases; +: increases; -: no changes.
In general, cattle husbandry increases mosquito populations. A range of potential factors might contribute to the rise in mosquito population among households with cattle,. Livestock, including cattle, goats, and other animals, emit scents that attract mosquitoes [13,15]. Livestock provide an alternative source of blood meals for mosquitoes that are actively searching for hosts, thus potentially increasing human vulnerability to malaria. Unlike humans, cattle typically lack mosquito shielding, particularly at night, if the animals remain untreated with insecticides, thus providing mosquitoes with an accessible blood source [13]. The proximity of animals to mosquito breeding grounds increases the supply of blood meals, which in turn attracts more mosquitoes, prolongs their lifespan, and heightens the risk of disease transmission to humans. This phenomenon is referred to as zoopotentiation [147]. In contrast, Loha [70] showed an inverse relationship between the quantity of animals and the likelihood of malaria. Therefore, a greater supply of animal blood meals might more effectively divert malaria mosquitoes from people. Nevertheless, increased domestic animal populations might also lead to potential risks of prolonging carrier lifespan and MBD transmission.
Humans and, to a lesser extent, non-human vertebrates serve as reservoirs for malaria parasites in anopheline mosquitoes [148]. In the ecology of these parasites, animals such as cows, pigs, goats, chickens, and dogs play major roles as blood meal hosts. The evolutionary process of malarial parasites frequently involves host switches [149–151]. Documenting the ability of large apes and other non-human primates to serve as reservoirs for human malarial parasites is crucial. Additionally, understanding their ability to serve as hosts for Plasmodium species that can transfer to human populations will be essential for future efforts to eradicate malaria [152]. As the scientific community strives to eliminate malaria, determining which Plasmodium species have non-human hosts that could act as reservoirs for ongoing infections will be critical [153]. Additional research is required to explore the correlation between farm animals and malaria illnesses in various seasons [74]. Furthermore, how the blood source affects the vector competence of mosquitoes to transmit malaria and other MBDs must be examined.
According to Sindato et al. [80], because RVFV is more common in people and cattle than in other domestic animals, the interaction between cattle and humans might be a more important cause of RVFV spread to humans than interactions with sheep or goats. Several activities, including handling animal tissue during slaughter or butchering, assisting with animal births, performing veterinary procedures, ingesting unpasteurized milk, or disposing of carcasses or fetuses, can transmit RVFV to humans [154]. Nevertheless, RVFV infections in animals have been found to occur before infections in humans [84]. Additionally, cases of humans contracting the virus through mosquito bites have been documented, and Aedes and Culex spp. mosquitoes are the most prevalent carriers [155]. RVFV has been shown to infect wild animals. However, additional research is required to determine whether these species maintain RVFV between outbreaks [156]. Furthermore, a comprehensive examination of the long-term movement patterns of animal herds might aid in the development of a strategic course of action to mitigate the occurrence of RVFV and other flaviviruses such as WNV [157]. Such efforts would be particularly relevant in countries extensive cattle production, such as Ethiopia and Nigeria.
WNV, a member of the Flavivirus family, transmits West Nile fever through mosquitoes. The virus originated primarily in birds and sustains itself in the environment through a cycle of transmission between mosquitoes and birds [118]. Both dogs and cats are considered dead-end hosts in the WNV transmission cycle, which involves mosquitoes as vectors and birds as hosts. Nonetheless, these animals can serve as sentinels, and serological markers are readily available to detect potential occurrences of these zoonotic diseases in the human population [100]. Findings from Resnick et al. [102] and Lan et al. [99] support that dogs and cats, particularly strays, can provide valuable indicators for monitoring the presence of WNV in specific regions during periods of transmission. Furthermore, the presence of anti-WNV antibodies in small ruminants, camels, and donkeys suggests that these species could serve as indicators for WNV activity [109].
Pigs are known to attract mosquitoes and to serve as amplifying hosts for JEV. Therefore, keeping pigs increases the risk of both the spread of viruses and the numbers of mosquitoes that spread them, such as Cx. tritaeniorhynchus, Cx. gelidus, and Cx. quinquefasciatus [28]. Insufficient awareness regarding the involvement of pigs and mosquitoes in the spread and multiplication of JEV highlights the need for enhanced education on the ecological dynamics of the virus. This education should particularly focus on individuals residing in rural areas near pig populations, given that Henriksson et al. [98] discovered the presence of JEV in pigs.
Reports on the effects of cattle on DENV have been conflicting. Jakobsen et al. [29] reported a lack of association, in agreement with Budodo et al. [158], who asserted that animals are not susceptible to DENV infection. Nevertheless, Thai et al. [91] observed a tenuous, although noteworthy correlation, and hypothesized that pig management might contribute to the presence of Aedes larvae habitat. Therefore, keeping livestock, particularly managing pigs, might possibly increase the likelihood of contracting dengue fever. Consequently, additional research is necessary regarding this topic.
On the basis of the reviewed studies, Anopheles spp., which are malaria vectors, have a preference for cattle over other livestock. The findings of Mburu et al. [22], Ijumba et al. [33], Githeko et al. [34], Rapuoda [35], Massebo et al. [40], Yewhalaw et al. [41], Massebo et al. [42], Meza et al. [47], Adugna et al. [51], Degefa et al. [50], and Iwashita et al. [54] support this conclusion. Mosquitoes might be drawn to cattle because these livestock are large and unlikely to defend themselves, their blood has certain physiological properties, such as proteins and iron, which is used for egg production by female mosquitoes [45,159,160]. In addition, cattle emit substantial quantities of CO2 [64], which might attract mosquitoes over extended distances [62]. Moreover, cattle hoofprints that fill with rainwater or places where cattle drink water might provide temporary well-lit homes for larvae, thus increasing the numbers of breeding pairs and producing large numbers of zoophagic An. arabiensis mosquito species. These mosquito species often favor such breeding sites [161].
Although mosquitoes exhibit similar neuroanatomy, other factors, such as genetic, environmental, and evolutionarily pressures, are likely to contribute to their diverse behaviors. They are an ideal organisms to investigate how brains might evolve to facilitate adaptive behaviors, such as the inclination toward various hosts. Future research examining all types of mosquitoes, including those that bite mammals and feed on nectar, is expected to identify the neurological reasons why some mosquito species prefer to feed on humans and animals that carry diseases [162]. Saul [163] suggested that zooprophylaxis, a viable environmental method to decrease malaria transmission, involves using alternative host species to divert malaria vectors away from humans. Raising cattle, goats, and sheep serves as a method of zooprophylaxis in certain malaria-endemic areas [44]. Increasing blood feeding in cattle decreases the chance of vector-borne infection, according to Iwashita et al. [54] and might have a zooprophylactic effect [5,164] on its own. Data suggest that keeping cattle might help control malaria by attracting malaria-carrying mosquitoes to places where insecticide-treated bed nets (ITNs) have hindered mosquitoes’ access to people. Exploiting the host-seeking behavior of female mosquito vectors is a method to enhance trapping efficiency [165].
Strategically placing many large animals near human populations can serve as a trap, thereby decreasing the numbers of disease-carrying mosquitoes and minimizing the spread of MBDs. Positioning lethal traps near or around animals can provide outdoor protection against important infections such as malaria. An effective method to trap mosquitoes might involve ITNs placed around enclosures housing large pigs or buffaloes. This method effectively increases the death rate of mosquitoes in the targeted region, decreases their overall population, and shifts populations toward younger mosquitoes that are incapable of transmitting certain pathogens, because an incubation period of 1–2 weeks is required. Consequently, this approach can serve as an outdoor measure to prevent the transmission of MBDs [66].
Many studies have examined how endectocides, such as ivermectin and fipronil, affect different types of malaria-carrying insects, such as An. arabiensis, An. coluzzii, and An. gambiae, particularly in animals such as cattle. These studies have demonstrated notable decreases in the lifespan and reproductive capacity of these mosquitoes [134,135,137,166]. Livestock owners in South Africa readily embraced endectocides as an effective method for managing malaria, as reported by Makhanthisa et al. [167]. Using endectocides to treat livestock can provide a valuable addition to current malaria control programs focused on distributing long-lasting insecticidal nets, which specifically target mosquitoes that feed on blood. We expect that this strategy could successfully combat vectors with diverse host preferences and biting behaviors, with the exception of species that are strongly inclined toward, and feed primarily on, humans, even in the presence of abundant non-human hosts [168]. The acceptance of livestock-administered endectocides by livestock owners in South Africa is high, owing to awareness of the benefits to both animal and human health, as well as familiarity with the chemicals used to manage livestock parasites [169]. Consequently, using endectocides on animals and applying other methods to stop malaria, such as ITNs, indoor residual spraying, and larval source management, might be ideal [162].
Considering the exophilic behavior of mosquitoes such as An. arabiensis is critical when developing control techniques. Residual house spraying has minimal effects in locations where the An. arabiensis population is dominant, because the targeted vector does not spend sufficient time on sprayed walls to acquire a fatal dose of pesticide. The vector’s biting habit plays a crucial role in the epidemiology of disease spread. Understanding blood-feeding patterns is crucial for implementing efficient vector control techniques [140]. Using both zooprophylaxis and ITNs is an essential integrated strategy to control An. arabiensis populations [54].
A comprehensive understanding of vector, host, and pathogen ecology (Fig 1), as well as responses to environmental and human-induced disturbances, is critical for accurately predicting and managing the spread of zoonotic arboviruses across regions. This knowledge would offer the best chance of effectively controlling these pathogens [43]. Strong links between seropositivity of MBDs in humans and animals highlight the importance of using specialized One Health strategies to monitor, prevent, and manage vector-borne diseases [170–172].
One Health strategy
The One Health strategy collaboratively addresses health concerns by acknowledging the convergence of human medicine, veterinary science, and environmental research [172,173]. The rise of MBDs and their expanding geographical distribution warrant a multidisciplinary approach incorporating public health, ecology, climatology, and other fields [174]. The implementation of a One Health framework in managing MBDs facilitates the identification of possible risks across human, animal, and environmental health sectors (Fig 3), thereby enabling the development of monitoring and risk mitigation strategies to prevent the transmission of one issue to another. One Health strategies that could be used to prevent the transmission of MBDs by leveraging livestock-mosquito-human interactions include the following:
To broaden the range of blood sources and potentially delay the selection of anthropophagic vectors, researchers could investigate strategies treating cattle with eprinomectin and humans with ivermectin, thus addressing both zoophagic and anthropophagic mosquitoes [175].
According to Massengo et al. [178], collaborative vaccination initiatives for nomadic pastoralist communities and their livestock achieve greater coverage than human-only vaccination efforts, thus suggesting that vaccination initiatives, the sharing of laboratory facilities, and surveillance databases can enhance the control of MBDs.
Implementing the One Health SMART approach encompasses identifying the cross-sectoral network; conducting key stakeholder interviews to establish the groundwork; delineating the system via process mapping; analyzing the system through multiagency workshops; recognizing opportunities to enhance system operations; and formulating an implementation plan [179].
Community involvement could be conducted via health education programs.
Measures emphasizing sustainable land use, conservation of forest ecosystems, and reduction of human-wildlife interactions could be implemented [173].
CONCLUSION
On the basis of the reviewed studies, our key observations are as follows: keeping livestock increases the populations of Anopheles and Culex mosquitoes, and to some extent, Aedes mosquitoes; keeping pigs increases the risk of contracting malaria, and pigs may serve as sentinel animals for JEV; goats may serve as sentinel animals for Plasmodium infection and JEV; keeping cattle increases the risk of contracting RVFV, and households with livestock are at elevated risk of contracting RVFV; dogs, cats, and horses may serve as sentinel animals for WNV; keeping cattle increases the risk of contracting RVFV, and households with livestock have elevated risk of contracting RVFV. Furthermore, housing conditions and environmental sanitation play roles in the interactions between livestock and mosquitoes. The findings indicate that One Health implementation is necessary for MBD management and control. Furthermore, providing public education regarding the potential zoonotic disease risks of livestock rearing is imperative in both rural and urban regions.