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Plasticity of blood feeding behavior of Anopheles mosquitoes in Ethiopia: a systematic review

Parasites & Vectors volume 17, Article number: 408 (2024) Cite this article

Abstract

Background

The efficacy of vector control tools depends on the behavior of the vector species. Many studies have sought to determine the feeding behavior of Anopheles mosquitoes in different settings of Ethiopia. We have performed a systematic review aimed to generate pooled evidence on the overall and species-specific blood meal sources of Anopheles mosquitoes in Ethiopia.

Methods

A search for relevant articles was performed in two electronic databases (PubMed and Science Direct) and three search engines (Google Scholar, Research Gate and Google) between 11 March and 2 April 2024. Following the initial identification of articles, we used EndNote X8 software and removed duplicate articles and screened the remaining articles by careful reading of their titles and abstracts. The full text of articles that passed this screening phase was retrieved, read and evaluated against predetermined selection criteria. The final decision for inclusion in the systematic review was made after a methodological quality check using the JBI critical appraisal checklist. All relevant data were extracted from tables, figures and texts of the included articles using a premade template in Excel, and the data were analyzed using Stata version 14 software.

Results

Of the 2431 studies identified, 27 met the inclusion criteria; all were published between 1997 and 2024. At 215 data points (frequency of tests of each Anopheles species by location and method of mosquito collections), 18,771 Anopheles mosquitoes belonging to 23 species or species complexes were tested for blood meal sources. The commonest sources of blood meals for Anopheles mosquitoes were bovine (36.0%, n = 6758) and human (29.4%, n = 5520). Among the tested anophelines, Anopheles (An.) arabiensis accounted for 67.9% (n = 12,741), followed by An. pharoensis, An. demeilloni and An. stephensi at 10.0%, 5.6% and 4.4%, respectively. Overall, there was no difference in the mean proportion of An. arabiensis detected with domestic animal blood (33.4%, 95% confidence interval [CI] 32.4–34.4%) and those detected with human blood (31.8%, 95% CI 30.9–32.8%). However, a greater proportion of the outdoor collected An. arabiensis were found to feed on bovines (47.9%, 95% CI 35.3–60.6) compared to humans (12.9%, 95% CI 0.8–24.9, P < 0.01). The foraging ratio (FR), which accounts for host availability, was greater for bovines (FR = 0.7) than for humans (FR = 0.2) for An. arabiensis, indicating preferential feeding on bovine hosts. This host preference was supported by the host preference index (human:bovine = 0.4). Anopheles pharoensis was detected with a slightly higher human blood index (53.5%, n = 1005) compared to bovine blood index (45.2%, n = 849). In contrast, An. demeilloni, An. coustani and An. marshalli were detected with a higher bovine blood index. Recently invaded urban malaria vector, An. stephensi was found with a higher ovine blood index.

Conclusions

Bovine and human hosts are common sources of a blood meal for Anopheles mosquitoes. In terms of host availability, An. arabiensis showed preferential feeding on bovines/cattle. Targeting domestic animals, bovines and ovines with endectocides could supplement current vector control interventions.

Study registration

The protocol of this study was registered on the International Prospective Register of Systematic Reviews, registration no. CRD42024515725.

Graphical Abstract

Background

Plasmodium parasites are transmitted to humans when an infected female Anopheles mosquito feeds on a susceptible host [1, 2]. Thus, in addition to supporting the sporogonic development of Plasmodium parasites, the host preference of Anopheles mosquitoes determines their vectorial capacity [3,4,5]. The major African malaria vectors mostly prefer feeding on human hosts to obtain blood for egg maturation [6]. In Ethiopia, multiple attempts have been made to determine the blood meal sources of malaria vectors [7,8,9,10,11,12,13]. Current evidence suggests that malaria vectors have a wide range of host preferences across different ecoepidemiological contexts.

To date, in Ethiopia, approximately 46 Anopheles mosquito species and subspecies have been recorded [14, 15]. However, only a few Anopheles species, including An. arabiensis, An. pharoensis, An. funestus, An. nili and An. stephensi have been implicated as vectors of malaria [16,17,18,19]. Anopheles arabiensis is the primary vector in most malaria-endemic areas in Ethiopia [16, 20], but the host preference (selective feeding behavior) of An. arabiensis has been found to vary across ecological gradients and epidemiological settings. Anopheles arabiensis has a human blood meal index (HBI) of 44% in the southwest region, 32.2% in the Southcentral region, 80% in irrigated villages and 73% in nonirrigated villages of central Ethiopia [7, 10, 19]. Anopheles pharoensis is of secondary importance in terms of being malaria vectors [16, 19], with An. funestus, An. nili and An. stephensi playing minor roles [8, 11, 17, 19].

Insecticide-treated nets (ITNs) and indoor residual spray (IRS) have been widely used to prevent malaria transmission by reducing human-vector contact inside human dwellings [21]. However, the effectiveness of IRS and ITNs is partly dependent on the biting and resting behavior of local malaria vectors. The greatest impacts of indoor-based vector control interventions can be achieved in areas where major malaria vectors feed and rest indoors [22, 23]. In addition, the peak biting time and location of local malaria vectors with nighttime human activities can affect the efficiency of these interventions [24].

In Ethiopia, several entomological studies have been conducted to determine the blood meal source and biting behavior of Anopheles mosquitoes. However, to our knowledge, no consolidated data on the overall and species-specific blood meal sources of Anopheles mosquitoes are currently available. A better understanding of the host feeding ranges and preferences of Anopheles mosquitoes can help to identify potential bottlenecks and gaps for future studies. This evidence could also support the tailoring of existing and new interventions to the behavior of local vectors for maximum effect. Therefore, the aim of this review is to summarize the overall and species-specific blood meal sources of Anopheles mosquitoes in Ethiopia.

Methods

Protocol registration

The protocol of this systematic review was registered in the International Prospective Register of Systematic Reviews with registration number CRD42024515725.

Search strategies

A comprehensive and exhaustive literature search was performed by two authors to identify all relevant studies on blood meal sources of Anopheles mosquitoes in Ethiopia. The review question was: “What are the blood meal sources of Anopheles mosquito species in Ethiopia?”. Condition, context and population format were employed to develop the review question and search for relevant studies.

Between 15 March and 02 April 2024, published articles were retrieved from the following electronic databases: PubMed, Science Direct, the Google Scholar search engine and the Research Gate search engine. The reference lists of the identified studies were screened further to determine those studies eligible for inclusion in the systematic review. A separate Google search was performed for articles that fulfilled the selection criteria using predetermined search terms. This search was conducted using keywords and Medical Subject Headings (MeSH) with various combinations of search terms: ‘Anopheles,’ ‘malaria vector,’ ‘blood meal source,’ ‘blood meal index,’ ‘host preference,’ ‘blood meal origin’ and ‘Ethiopia.’ The search terms were used in combination with Boolean operators such as “OR” or “AND” (Additional file 1: Table S1). The Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines were followed (Fig. 1).

Fig. 1
figure 1

Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) flow diagram of the identification and selection of studies for inclusion in a systematic review of blood meal sources of Anopheles mosquitoes in Ethiopia

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Eligibility criteria

Original articles that reported the blood meal sources of Anopheles mosquitoes from Ethiopia were considered for this review. Articles published in English reporting the source of the blood meal of Anopheles mosquitoes across all years of publication were considered. Studies in which the blood meal of Anopheles mosquitoes was tested for at least two host species using either direct enzyme-linked immunosorbent assay (ELISA) or multiplex-polymerase chain reaction (mPCR) were considered. The tested anopheline mosquito population needed to have been collected from the wild and freshly fed using standard entomological collection techniques. Findings on blood meal sources of non-Anopheles mosquitoes were excluded from the systematic review, and publications that were based on secondary data sources, including reviews and meeting proceedings, were not considered for inclusion.

Study selection

Databases of all located studies was created on EndNote X8 (Bld 10,063; EndNote™; Clarivate, Philadelphia, PA, USA) and duplicate studies were removed. The initial assessment of the articles was performed by two reviewers independently by reading the titles and abstracts of each study. Full-text retrieval and further evaluation of relevant articles were performed by reading the full-text of each article. Studies without full texts were excluded after attempts to contact the primary author at least twice via email had no response. During the full-article review, reports that did not include adequate information on the blood meal source of Anopheles mosquitoes, reports of blood meal sources of unidentified anopheline species or articles that contained previously reported data were excluded. The level of agreement between two reviewers was evaluated using Kappa statistics and found to be 0.9, indicating the presence of good agreement between the reviewers. Any differences in article selection between assessors were settled by discussion and referral to a third author.

Critical appraisal

The methodological quality and possibility of bias of the selected studies were assessed before inclusion in the review by performing a critical appraisal. Two authors independently evaluated the quality of each article using a standard quality assessment instrument adapted from the JBI critical appraisal checklist for studies reporting prevalence data [25]. Disagreements between two appraisers were settled by discussion and referral to a third author.

Data extraction and management

Data extraction was independently conducted by two authors using a standardized data extraction tool that was adapted from the JBI data extraction tool for systematic reviews. Discrepancies in the data extracted by the two investigators were resolved by discussion and referral to a third reviewer. All required data, such as name of primary author, year of publication, year of data enumeration (mosquito collection), host density (proportion of specific hosts in the study area), study location (geographic location as reported in the original study), entomological sampling techniques used and location (indoor, outdoor or both) of mosquito collection, Anopheles mosquito species tested for blood meal source, number of mosquitoes tested and detected with specific host blood, host species tested for blood meal source detection, blood meal indices of specific Anopheles species for tested host species and methods used for detection of blood meal sources, were extracted into Excel format (Excel 2016; Microsoft Corp., Redmond, WA, USA).

The data extraction tool was developed so that the data were curated by data points. Data points are the frequency of test of specific Anopheles species in each of the reviewed articles by location (indoor, outdoor and both) and method of mosquito collection. Thus, the number of each Anopheles mosquito species tested and detected with specific host blood was extracted separately for each collection location and method (Table 1).

Table 1 Characteristics of the original studies (data points) included in the systematic review of blood meal origin/source of Anopheles mosquitoes, Ethiopia, 1997–2024
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Data synthesis

The data extracted using the Excel spreadsheet were exported to Stata software release 14 (StataCorp LP, College Station, TX, USA) for producing the statistical summaries. The characteristics of the original studies were summarized and presented. The test frequency of each Anopheles species by location and method of mosquito collection (data points) and species composition are presented graphically. The species-specific and overall indices of the blood meal of Anopheles mosquitoes were determined as the fraction of specific Anopheles species positive for a specific host blood to the number of that species tested for blood meal detection. A Kruskal–Wallis test was used to quantify the variation in the median proportion of Anopheles mosquitoes detected with human and bovine blood across collection locations (An. arabiensis, An. coustani, An. demeilloni and An. pharoensis) and year of mosquito collection (An. arabiensis). The foraging ratio (FR) was calculated as the percentage of each Anopheles species (An. arabiensis, An. coustani, An. demeilloni, An. funestus and An. pharoensis) detected with the blood of a particular host divided by the percentage of that particular host species in the total available host population [26, 27]; and was used to determine the avoidance (value < 1) or preference (value > 1) of a specific host species. Similarly, host preference indices (HPIs), an indicator of the observed proportion of fed mosquitoes on human hosts compared to bovine hosts divided by the expected comparative proportion of fed mosquitoes on these two hosts, were calculated to determine the preferential feeding of Anopheles mosquitoes on either human or bovine hosts [27, 28]. The mean proportion of human and bovine host blood was compared among An. arabiensis mosquitoes collected indoors and outdoors using the independent t-test.

Results

Literature search

The search for studies on the electronic databases and manually on search engines and other sources identified 2431 studies. After 165 duplicates had been removed, an initial screening of 2266 studies was conducted by reading the title and abstract of each study. This initial screening identified 31 studies that met the inclusion criteria; of these, full texts of 29 studies were successfully retrieved. An additional two studies were excluded following reading of the full texts (data had been presented in previous studies). Ultimately, 27 studies (with 215 data points/frequency of test of each species by method and locations of collection) that were published between 1997 and 2024 were included in this systematic review [8, 9, 11,12,13, 19, 29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49].

Quality assessment

Overall, the 27 articles included in the systematic review were evaluated against the JBI appraisal criteria for quality and bias assessment. All critically appraised articles were judged to satisfy eight of the nine critical appraisal inquiries and met the predetermined cutoff for inclusion in the systematic review [20]. Since, the use of standard mosquito sampling method was considered to be one of the selection criteria, the critical appraisal inquiry that requests for appropriateness of sampling methods was not found to be applicable to studies selected for this systematic review ((Fig. 1; Additional file 1: Table S2)

Characteristics of the original studies via data points

A total of 215 data points were identified in the 27 articles that included in this systematic review, of which 54.4% (n = 117) were based on entomological sampling after 2016. The data points were disproportionally distributed across geographical ranges/locations, with most (40.5%, n = 87) being from the central part of the country, followed by the eastern region (14.9%, n = 32). In earlier publications, based on mosquito collections up to 2005, the U.S. Centers for Disease Control and Prevention light trap (CDC LT) was used at one point for collecting host-seeking mosquitoes. Resting mosquito collections were made by a standard mouth aspirator at 13 data points and pyrethrum spray catches (PSCs) were used at 18 data points. The use of entomological sampling techniques that target either resting or host-seeking Anopheles mosquitoes has been more diversified in recent publications (mosquito collection since 2016). The frequency of using CDC LTs for collecting host-seeking mosquitoes has increased to 98 data points. Animal-baited tent traps have also been used for collecting host-seeking mosquitoes. The entomological techniques employed for collecting resting mosquitoes were expanded in more recent years to include prokopack and backpack aspirators, clay pots and black resting boxes. Overall, CDC LTs were the most frequent (45.0%, n = 140) entomological sampling technique, followed by PSCs (20.6%, n = 64) and prokopack aspirators (13.2%, n = 41). The latter two sampling methods were used for collecting resting mosquitoes indoors (PSCs) and both indoors and outdoors of human and animal shelters (prokopack aspirator) (Table 1).

Blood meal source determination among freshly fed Anopheles mosquitoes followed standard procedures [50, 51]. At most (91.6%, n = 197) of the data points, blood meal source detection was performed by ELISA. Two host species, human and bovine blood meals, were tested across all of the data points. One-fourth of the data points were tested for goat and dog blood meals; pigs, chickens and equines were tested less frequently.

Abundance and composition of Anopheles species

A total of 18,771 freshly fed Anopheles mosquitoes, belonging to 23 species or species complexes, were tested for blood meal source detection (Table 2). Anopheles arabiensis, the primary vector of malaria in most malaria-endemic regions of Ethiopia, accounted for 67.9% (n = 12,741) of the tested Anopheles mosquito species for blood meal source detection, followed by An. pharoensis, 10.0% (n = 1879) and An. demeilloni, 5.6% (n = 1060). The new invasive urban malaria vector in the Horn of Africa, An. stephensi, accounted for 4.4% (n = 830) of the tested Anopheles mosquito species. A number of studies reported the tested mosquitoes as a species complex, including Anopheles gambiae sensu lato (An. gambiae s.l.), which accounted for 5.0% (n = 916) of the tested Anopheles mosquito species (Additional file 1: Table S3). However, molecular identification of 2271 morphologically identified An. gambiae s.l. confirmed that 95.6% (n = 2179) were An. arabiensis and 3.4% were not amplified; the remaining 14 mosquitoes were found to be Anopheles amharicus [30]. Anopheles arabiensis was the most frequently (n = 79) tested Anopheles mosquito species, followed by An. pharoensis (n = 26), An. coustani (n = 24), An. demeilloni (n = 16), An. funestus (n = 14) and An. stephensi (n = 9) (Fig. 2).

Table 2 Origin of blood meal and blood meal indices (proportion of fed mosquitoes on specific host species) of Anopheles mosquitoes, Ethiopia, 1997–2024
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Fig. 2
figure 2

Frequency of occurrence of Anopheles mosquito species in blood meal sources analysis in the original studies included in the systematic review, Ethiopia, 1997–2024

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Common sources of blood meal for Anopheles species

Among the Anopheles mosquito specimens analyzed for blood meal source, host species were successfully identified in 83.3% (n = 15,640). Of the identified blood meal sources, bovine blood meal accounted for 36.0% (n = 6758), followed by human blood meal, accounting for 29.4% (n = 5520) (Table 2). A nonnegligible proportion of specimens (12.9%, n = 2418) were also identified with blood from two host species (mixed blood meal sources), especially bovines and humans. Blood from other host species was also detected in Anopheles mosquito specimens, including ovines (14.3%, n = 448) and canines (1.1%, n = 32). Among the reviewed studies, two reported the detection of chicken blood [36, 43], and one of these also reported equine host blood in a small proportion of tested Anopheles mosquitoes [43]. None of the tested mosquitoes tested positive for pig blood, and 16.7% (n = 3131) of the tested Anopheles mosquitoes had fed on an unidentified host species.

Blood from at least one of the tested Anopheles mosquito species was detected in each of the data points. Of the tested (n = 12,741) An. arabiensis mosquitoes, 31.8% (n = 4056) and 32.2% (n = 4107) had fed on human and bovine host blood, respectively; the remaining proportion of An. arabiensis had fed on unidentified (19.2%, n = 2450), mixed (13.4%, n = 1706), ovine and canine host blood. Overall, there was no difference in the mean proportion of An. arabiensis detected with domestic animal (bovine, ovine and canine) blood (33.4%, 95% confidence interval [CI] 32.4–34.4%) compared with human blood (31.8%, 95% CI 30.9–32.8%). A slightly higher proportion of An. pharoensis, a malaria vector of secondary importance in terms of malaria transmission in Ethiopia, was detected with human blood content (53.5%, n = 1005) compared to bovine blood content (45.2%, n = 849), with most of the mosquitoes collected inside human houses. However, a higher bovine blood meal index (BBI) compared to the HBI was recorded for An. demeilloni (64.8% vs 8.2%), An. coustani (57.8% vs 23.8%) and An. marshalli (47.0% vs 10.4%), bovine and human, respectively. The blood meal indices of the invasive urban malaria vector An. stephensi were higher for ovines (36.4%, n = 302) than for bovines (5.5%, n = 46) and humans (1.9%, n = 16). Most (59.9%, n = 202) of the tested An. funestus were detected with mixed blood meals (human and bovine) (Table 2).

The median proportions of HBIs and BBIs varied across collection locations for An. arabiensis. The HBI was higher among An. arabiensis mosquitoes collected indoors (median HBI 32.0, interquartile range [IQR] 14.1, 50.0) than among those collected outdoors (median 3.4, IQR 1.9, 18.5; P < 0.01). In contrast, the BBI was higher among An. arabiensis collected outdoors (median 48.4, IQR 42.8, 55.5) compared to those collected indoors (median 20.8, IQR 6.8, 44.1; P < 0.01) (Table 3). However, there was no difference in the blood meal index of An. pharoensis that fed on bovine hosts across collection locations, indoors (median 55.8, IQR 0.0, 70.0) and outdoors (median 83.3, IQR 83.3, 83.3, P = 0.31).

Table 3 Variations in human and bovine blood meal indices of the four most abundant Anopheles mosquito species across collection locations, Ethiopia, 1997–2024
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The preferential feeding of An. arabiensis was determined by comparing the mean proportion of An. arabiensis that fed on bovine and human hosts. The mean proportion of An. arabiensis that fed on bovine hosts among outdoor catches (47.9, 95% CI 35.3–60.6) was significantly higher than the proportion that fed on human hosts (12.9, 95% CI 0.8–24.9) (t(22) = − 4.4, P < 0.01) (Table 4). However, there was no statistically significant difference between the BBIs (26.3, 95% CI 18.8–33.9) and HBIs (34.7, 95% CI 26.7–42.7) (t (68) = 1.5, P = 0.1) among An. arabiensis collected indoors.

Table 4 Preferred blood meal sources of Anopheles arabiensis across collection locations (t-test), Ethiopia, 1997–2024
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The human:bovine:ovine host ratios among the studies that surveyed the host population were 4.5:2.6:1.0, respectively. Thus, a comparison of the feeding preference of An. arabiensis was preformed among the most common host species (human and bovine) in the population and blood meal source tests. The FR of An. arabiensis for the bovine host (FR 0.7) was greater than that for the human host (FR 0.2). This preferential feeding of An. arabiensis on bovine hosts over humans was confirmed by the HPI (human:bovine 0.4) (Table 5).

Table 5 Foraging ratio and host preference index of five abundant Anopheles mosquito species, Ethiopia, 1997–2024
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Most (58.0%, n = 124) of the test results for blood meal source detection were reported by collection location, either indoors (40.9%, n = 88) or outdoors (17.2%, n = 37). However, 42.0% (n = 90) of the reported test results were not segregated by collection locations (Additional file 1: Table S3).

The overall proportion of An. arabiensis that fed on human hosts varied across the years of mosquito collection: before 2005 (median 26.3, IQR 9.3, 46.1), between 2005 and 20,115 (median 32.0, IQR 16.8, 66.7) and after 2015 (median 8.9, IQR = 0.0, 16.7; P = 0.01). However, this variation was not evident when the analysis was stratified according to the collection location. The proportion of An. arabiensis that fed on human hosts indoors did not vary across the years of mosquito collection: before 2005 (median 39.3, IQR 12.9, 48.1), 2005–2015 (median 29.8, IQR 13.2, 46.9) and after 2015 (median 50.0, IQR 14.3, 74.1; P = 0.53). Similarly, the was no difference in the HBI among An. arabiensis collected outdoors across the years of mosquito collection: before 2005 (median 2.6, IQR 0.9, 14.6), 2005–2015 (median 12.1, IQR 1.5, 43.9) and after 2015 (median 7.9, IQR 2.7, 14.2; P = 0.83) (Table 6). There was no variation in the overall BBI for An. arabiensis across the years of mosquito collection: before 2005 (median 40.6, IQR 10.5, 44.2), 2005–2015 (median 28.2, IQR 16.7, 39.1) and after 2015 (median 14.2, IQR 2.9, 43.1; P = 0.16).

Table 6 Blood meal sources of Anopheles arabiensis across years and locations of mosquito collection, Ethiopia, 1997–2024
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Discussion

The use of vector control interventions has played a significant role in reducing the malaria burden since the beginning of the twenty-first century [39, 40]. These vector control interventions primarily consist of targeting Anopheles mosquitoes that seek human hosts and rest indoors (within human houses). Thus, an understanding of the feeding behavior of local malaria vectors is critical for the effective selection and implementation of additional vector control interventions. Anopheles arabiensis, the primary malaria vector across most malaria-endemic regions of Ethiopia, has been found to show varying preferences for host species [13, 19, 42, 44], but most studies have shown its preference for nonhuman vertebrates, especially cattle [13, 33, 35, 36, 38, 42].

We conducted a systematic review of Anopheles mosquito blood meal sources in Ethiopia and showed that An. arabiensis exhibits anthropozoophilic feeding behavior. This study revealed that An. arabiensis can feed on multiple host species, the proportions of which vary between locations (indoor vs outdoor) where mosquitoes are collected. Anopheles arabiensis collected inside human dwellings had higher HBIs than those collected outdoors, while those collected outdoors were found with a high proportion of BBIs. Our finding is in line with a previous study which showed that the proportion of mosquitoes detected with different blood meal sources is primarily influenced by the location of collection (indoors vs outdoors) [6]. A recent study also demonstrated that An. arabiensis is amenable for zooprophylaxis [52], which is also in line with blood meal source analysis. However, we are cautious of its potential zoopotentiation effect, as easy access to blood meal sources prolongs the infectious life and reproductive potential of mosquitoes [53]. Perhaps such opportunistic feeding behavior of An. arabiensis might explain its success in thriving as the dominant vector, especially in rural settings.

Although the availability of a host is thought to determine the feeding behavior of Anopheles mosquitoes, it seems that An. arabiensis prefers to feed on bovine hosts. However, this result was not adjusted for the proportion of individuals protected by the physical barrier or the knockdown effect of the chemical on ITNs and the repellence effect of IRS. The potential diverting effect of insecticidal vector control interventions applied indoors toward unprotected animal hosts could also have contributed to the observed feeding preference on bovine hosts. Nevertheless, a significant proportion of An. arabiensis that were collected from inside human dwellings were detected with bovine blood. This finding corroborates the long-standing culture of sharing houses with cattle in many rural areas of Ethiopia [45, 49]. With this biting behavior on animal hosts, An. arabiensis might not be easily contained by existing indoor-based interventions. Anopheles pharoensis, one of the anopheline mosquitoes of secondary importance for malaria transmission in Ethiopia, was detected to have a high HBI. However, this might also be due to the location of mosquito collection, as observed for An. arabiensis, with most of the tested An. pharoensis having been captured from inside human dwellings. Other abundant Anopheles mosquitoes of secondary importance for malaria transmission in Ethiopia were found to be highly zoophagic, feeding on bovine (An. demeilloni, An. coustani, and An. marshalli) and ovine (An. stephensi) blood meal sources.

The recorded low proportion of Anopheles mosquitoes with human blood in comparison to those with blood of domestic animals (bovine, ovine and canine) might be indicative of the bottleneck in the feeding behavior of malaria vectors that can be targeted with supplemental interventions. Existing evidence shows that the application of the major insecticidal vector control interventions, IRS and ITNs, leads mosquitoes to change their resting and feeding habits to avoid the effects of insecticides (behavioral resistance) and to achieve easy access to blood meals [54,55,56]. However, our findings do not support this evidence, since neither the BBIs nor the HBIs significantly varied among mosquitoes collected from the same locations, especially for An. arabiensis. Thus, for anthropozoophilic mosquitoes, easy access to blood meal sources from unprotected animal hosts may support longevity and density and thus contribute to ongoing malaria transmission. Therefore, pushing mosquitoes away from human hosts and driving them to nearby domestic animals by existing and novel interventions and then targeting them with endectocides may be a future direction for supplemental interventions.

A significant proportion of the tested Anopheles mosquitoes were found to feed on unidentified blood meal sources, and this proportion varied across species. This unidentified proportion might imply a lack of primers or antibodies for common host species in the testing procedure. In all of the reviewed studies, cattle (bovine) and human primers and/or antibodies were commonly included for detecting blood meal sources in Anopheles mosquitoes. Other host species, including goats, dogs, pigs and chickens, have been tested infrequently. None of the reviewed studies assayed Anopheles mosquitoes for blood meal sources for some common (camel and sheep) domestic animals, and only one study tested them for equine (donkey, horse) hosts in Ethiopia. Thus, future studies need to consider unbiased and inclusive testing of Anopheles mosquitoes to determine the most common and preferred sources of blood meals across transmission settings. The impact of testing method and location of mosquito collection on sources of blood meal were not fully evaluated in this review since most of the data points in reviewed articles were unsegregated.

To our knowledge, this systematic review is the first of its kind to summarize the blood meal source of Anopheles mosquitoes in Ethiopia. The findings provide valuable evidence on the common sources of blood for Anopheles mosquitoes and the bottleneck in the feeding behavior that can be targeted by supplemental interventions. However, the findings might need to be interpreted with caution due to some limitations of the study. Although much effort was made to identify all relevant studies, some studies that satisfied the inclusion criteria may have remained unidentified. This systematic review is based on open access articles which were published in English. The curated data points across location, method and year of mosquito collections may not be sufficiently robust to determine the variation in host preferences. This might be more pronounced due to the lack of standard data reporting format for blood meal analysis across studies.

In conclusion, blood meal sources were successfully identified in most of the tested Anopheles mosquito specimens, but a nonnegligible proportion were found to fed on the blood of unidentified hosts. Domestic animals, particularly bovines and ovines, were reported to be the most common nonhuman sources of blood for Anopheles mosquitoes. Although the blood meal indices of An. arabiensis did not vary significantly between bovine and human host species, the foraging ratio and host preference index revealed the preferential feeding on bovine hosts. This evidence reveals the potential of targeting domestic animals, especially cattle and goats, with endectocide and/or calls for innovative topical agents that target Anopheles mosquitoes that seek blood from nonhuman animals as a supplemental vector control strategy.

Availability of data and materials

No datasets were generated or analyzed during the current study.

Abbreviations

BBI:

Bovine blood meal index

CDC:

U.S. Centers for Disease Control and Prevention

ELISA:

Enzyme-linked immunosorbent assay

FR:

Foraging ratio

HBI:

Human blood meal index

HPIs:

Host preference indices

IRS:

Indoor residual spray

ITNs:

Insecticide-treated nets

MeSH:

Medical subject headings

mPCR:

Multiplex PCR

OBI:

Ovine blood meal index

References

  1. Ponnudurai T, Lensen AHW, van Gemert GJA, Bolmer MG, Meuwissen JHET. Feeding behaviour and sporozoite ejection by infected Anopheles stephensi. Trans R Soc Trop Med Hyg. 1991;85:175–80.

    Article  CAS  PubMed  Google Scholar 

  2. WHO. Guidelines for malaria vector control. Geneva: World Health Organization; 2019.

    Google Scholar 

  3. Wu SL, Sánchez CHM, Henry JM, Citron DT, Zhang Q, Compton K, et al. Vector bionomics and vectorial capacity as emergent properties of mosquito behaviors and ecology. PLoS Comput Bio. 2020;16:e1007446.

    Article  Google Scholar 

  4. Garrett-Jones C. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ. 1964;30:241–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Dye C. Vectorial capacity: must we measure all its components? Parasitol Today. 1986;2:203–9.

    Article  CAS  PubMed  Google Scholar 

  6. Orsborne J, Furuya-Kanamori L, Jeffries CL, Kristan M, Mohammed AR, Afrane YA, et al. Using the human blood index to investigate host biting plasticity: a systematic review and meta-regression of the three major African malaria vectors. Malar J. 2018;17:479.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Massebo F, Balkew M, Gebre-Michael T, Lindtjorn B. Blood meal origins and insecticide susceptibility of Anopheles arabiensis from Chano in southwest Ethiopia. Parasit Vectors. 2013;6:44.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Animut A, Balkew M, Gebre-Michael T, Lindtjorn B. Blood meal sources and entomological inoculation rates of anophelines along a highland altitudinal transect in south-central Ethiopia. Malar J. 2013;12:76.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Adugna T, Yewhelew D, Getu E. Bloodmeal sources and feeding behavior of anopheline mosquitoes in Bure district, northwestern Ethiopia. Parasit Vectors. 2021;14:166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kenea O, Balkew M, Tekie H, Gebre-Michael T, Deressa W, Loha E, et al. Human-biting activities of Anopheles species in south-central Ethiopia. Parasit Vectors. 2016;9:527.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Tadesse FG, Ashine T, Teka H, Esayas E, Messenger LA, Chali W, et al. Anopheles stephensi mosquitoes as vectors of Plasmodium vivax and falciparum, Horn of Africa, 2019. Emerg Infect Dis. 2021;27:603–7.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Balkew M, Mumba P, Yohannes G, Abiy E, Getachew D, Yared S, et al. An update on the distribution, bionomics, and insecticide susceptibility of Anopheles stephensi in Ethiopia, 2018–2020. Malar J. 2021;20:263.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ashine T, Eyasu A, Asmamaw Y, Simma E, Zemene E, Epstein A, et al. Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia. Parasit Vectors. 2024;17:166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kyalo D, Amratia P, Mundia CW, Mbogo CM, Coetzee M, Snow RW. A geo-coded inventory of anophelines in the Afrotropical Region south of the Sahara: 1898–2016. Wellcome Open Res. 2017;2:57.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Irish SR, Kyalo D, Snow RW, Coetzee M. Updated list of Anopheles species (Diptera: Culicidae) by country in the Afrotropical Region and associated islands. Zootaxa. 2020;4747:3.

    Article  Google Scholar 

  16. Adugna F, Wale M, Nibret E. Review of Anopheles mosquito species, abundance, and distribution in Ethiopia. J Trop Med. 2021;2021:6726622.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Emiru T, Getachew D, Murphy M, Sedda L, Ejigu LA, Bulto MG, et al. Evidence for a role of Anopheles stephensi in the spread of drug- and diagnosis-resistant malaria in Africa. Nat Med. 2023;29:3203–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Massebo F, Balkew M, Gebre-Michael T, Lindtjorn B. Entomologic inoculation rates of Anopheles arabiensis in southwestern Ethiopia. Am J Trop Med Hyg. 2013;89:466–73.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kibret S, Wilson GG, Tekie H, Petros B. Increased malaria transmission around irrigation schemes in Ethiopia and the potential of canal water management for malaria vector control. Malar J. 2014;13:360.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Aschale Y, Getachew A, Yewhalaw D, De Cristofaro A, Sciarretta A, Atenafu G. Systematic review of sporozoite infection rate of Anopheles mosquitoes in Ethiopia, 2001–2021. Parasit Vectors. 2023;16:437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Taffese HS, Hemming-Schroeder E, Koepfli C, Tesfaye G, Lee MC, Kazura J, et al. Malaria epidemiology and interventions in Ethiopia from 2001 to 2016. Infect Dis Poverty. 2018;7:103.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Githeko AK, Service MW, Mbogo CM, Atieli FK, Juma FO. Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop. 1994;58:307–16.

    Article  CAS  PubMed  Google Scholar 

  23. Pappa V, Reddy MR, Overgaard HJ, Abaga S, Caccone A. Estimation of the human blood index in malaria mosquito vectors in Equatorial Guinea after indoor antivector interventions. Am J Trop Med Hyg. 2011;84:298–301.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Esayas E, Assefa M, Bennett A, Thomsen E, Gowelo S, Vajda E, et al. Bionomic characterization of Anopheles mosquitoes in the Ethiopian highlands and lowlands. Parasit Vectors. 2024;17:306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Munn Z, Moola S, Lisy K, Riitano DCT. Chapter 5: Systematic reviews of prevalence and incidence. In: Aromataris E, Munn Z, editors. JBI manual for evidence synthesis: JBI: Adelaide; 2020.

  26. Hess AD, Hayes RO, Tempelis CH. The use of the forage ratio technique in mosquito host preference studies. Mosq News. 1968;28:386–9.

    Google Scholar 

  27. Kay BH, Boreham PF, Edman JD. Application of the feeding index concept to studies of mosquito host-feeding patterns. Mosq News. 1979;39:68–72.

    Google Scholar 

  28. Richards SL, Ponnusamy L, Unnasch TR, Hassan HK, Apperson CS. Host feeding patterns of Aedes albopictus (Diptera: Culicidae) in relation to availability of human and domestic animals in suburban landscapes of central North Carolina. J Med Entomol. 2006;43:543–51.

    Article  PubMed  Google Scholar 

  29. Akirso A, Tamiru G, Eligo N, Lindtjorn B, Massebo F. High human blood meal index of mosquitoes in Arba Minch town, southwest Ethiopia: an implication for urban mosquito-borne disease transmission. Parasitol Res. 2024;123:102.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Abossie A, Demissew A, Getachew H, Tsegaye A, Degefa T, Habtamu K, et al. Higher outdoor mosquito density and Plasmodium infection rates in and around malaria index case households in low transmission settings of Ethiopia: implications for vector control. Parasit Vectors. 2024;17:53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Eshetu T, Eligo N, Massebo F. Cattle feeding tendency of Anopheles mosquitoes and their infection rates in Aradum village, North Wollo, Ethiopia: an implication for animal-based malaria control strategies. Malar J. 2023;22:81.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Assa A, Eligo N, Massebo F. Anopheles mosquito diversity, entomological indicators of malaria transmission and challenges of morphological identification in southwestern Ethiopia. Trop Med Health. 2023;51:38.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Tomas T, Eligo N, Tamiru G, Massebo F. Outdoor and early hour human biting activities of malaria mosquitoes and the suitability of clay pot for outdoor resting mosquito collection in malaria endemic villages of southern rift valley, Ethiopia. Parasite Epidemiol Control. 2022;19:e00278.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zemene E, Belay DB, Tiruneh A, Lee MC, Yewhalaw D, Yan G. Malaria vector dynamics and utilization of insecticide-treated nets in low-transmission setting in southwest Ethiopia: implications for residual transmission. BMC Infect Dis. 2021;21:882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Eba K, Habtewold T, Yewhalaw D, Christophides GK, Duchateau L. Anopheles arabiensis hotspots along intermittent rivers drive malaria dynamics in semi-arid areas of Central Ethiopia. Malar J. 2021;20:154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Degefa T, Githeko AK, Lee MC, Yan G, Yewhalaw D. Patterns of human exposure to early evening and outdoor biting mosquitoes and residual malaria transmission in Ethiopia. Acta Trop. 2021;216:105837.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Carter TE, Yared S, Getachew D, Spear J, Choi SH, Samake JN, et al. Genetic diversity of Anopheles stephensi in Ethiopia provides insight into patterns of spread. Parasit Vectors. 2021;14:602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bamou R, Rono M, Degefa T, Midega J, Mbogo C, Ingosi P, et al. Entomological and anthropological factors contributing to persistent malaria transmission in Kenya, Ethiopia, and Cameroon. J Infect Dis. 2021;223:155–70.

    Article  Google Scholar 

  39. Getachew D, Gebre-Michael T, Balkew M, Tekie H. Species composition, blood meal hosts and Plasmodium infection rates of Anopheles mosquitoes in Ghibe River Basin, southwestern Ethiopia. Parasit Vectors. 2019;12:257.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kindu M, Aklilu E, Balkew M, Gebre-Michael T. Study on the species composition and ecology of anophelines in Addis Zemen, South Gondar, Ethiopia. Parasit Vectors. 2018;11:215.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gari T, Kenea O, Loha E, Deressa W, Hailu A, Balkew M, et al. Malaria incidence and entomological findings in an area targeted for a cluster-randomized controlled trial to prevent malaria in Ethiopia: results from a pilot study. Malar J. 2016;15:145.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Massebo F, Balkew M, Gebre-Michael T, Lindtjorn B. Zoophagic behaviour of anopheline mosquitoes in southwest Ethiopia: opportunity for malaria vector control. Parasit Vectors. 2015;8:645.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Yewhalaw D, Kelel M, Getu E, Temam S, Wessel G. Blood meal sources and sporozoite rates of Anophelines in Gilgel-Gibe dam area, Southwestern Ethiopia. Afr J Vector Biol. 2014;14:166.

    Google Scholar 

  44. Kibret S, Lautze J, Boelee E, McCartney M. How does an Ethiopian dam increase malaria? Entomological determinants around the Koka reservoir. Trop Med Int Health. 2012;17:1320–8.

    Article  PubMed  Google Scholar 

  45. Tirados I, Costantini C, Gibson G, Torr SJ. Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control. Med Vet Entomol. 2006;20:425–37.

    Article  CAS  PubMed  Google Scholar 

  46. Yohannes M, Haile M, Ghebreyesus TA, Witten KH, Getachew A, Byass P, et al. Can source reduction of mosquito larval habitat reduce malaria transmission in Tigray, Ethiopia? Trop Med Int Health. 2005;10:1274–85.

    Article  PubMed  Google Scholar 

  47. Habtewold T, Walker AR, Curtis CF, Osir EO, Thapa N. The feeding behaviour and Plasmodium infection of Anopheles mosquitoes in southern Ethiopia in relation to use of insecticide-treated livestock for malaria control. Trans R Soc Trop Med Hyg. 2001;95:584–6.

    Article  CAS  PubMed  Google Scholar 

  48. Lulu M, Hadis M, Mekonnen Y, Asfaw T. Chromosomal inversion polymorphisms of Anopheles arabiensis from some localities in Ethiopia in relation to host feeding choice. Ethiopia J Health Dev; 1998;12:1.

  49. Hadis M, Lulu M, Makonnen Y, Asfaw T. Host choice by indoor-resting Anopheles arabiensis in Ethiopia. Trans R Soc Trop Med Hyg. 1997;91:376–8.

    Article  CAS  PubMed  Google Scholar 

  50. Kent RJ, Norris DE. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg. 2005;73:336–42.

    Article  CAS  PubMed  Google Scholar 

  51. Beier J, Perkkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, et al. Bloodmeal identification by direct-enzyme linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988;25:9–16.

    Article  CAS  PubMed  Google Scholar 

  52. Katusi GC, Hermy MRG, Makayula SM, Ignell R, Mnyone LL, Hill SR, et al. Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania. Malar J. 2023;22:340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Loha E. Association between livestock ownership and malaria incidence in south-central Ethiopia: a cohort study. Am J Trop Med Hyg. 2023;108:1145–50.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Sokhna C, Ndiath MO, Rogier C. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clin Microbiol Infect. 2013;19:902–7.

    Article  CAS  PubMed  Google Scholar 

  55. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Pombi M, Calzetta M, Guelbeogo WM, Manica M, Perugini E, Pichler V, et al. Unexpectedly high Plasmodium sporozoite rate associated with low human blood index in Anopheles coluzzii from a LLIN-protected village in Burkina Faso. Sci Rep. 2018;8:12806.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Arba Minch University, Arba Minch, Ethiopia

    Temesgen Ashine, Hailu Shibru, Alemayehu Bekele & Fekadu Massebo

  2. Malaria and NTD Research Division, Armauer Hansen Research Institute, Addis Ababa, Ethiopia

    Temesgen Ashine, Abena Kochora, Muluken Assefa, Bedasa Gidisa, Nigatu Negash & Endalamaw Gadisa

  3. Department of Vector Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L35QA, UK

    David Weetman

  4. University of Gondar, Gondar, Ethiopia

    Tadesse Awoke Ayele

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  1. Temesgen Ashine
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Contributions

FM and TA conceived the study. TA, AK, HS and AB performed the systematic review. All authors contributed to interpretation of the results and drafting of the manuscript. All authors read and approved the final manuscript.

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Supplementary Information

Additional file 1: Table S1.

Databases and search engines with the respective search teams and records identified for the systematic review. Table S2. Methodological quality and bias assessment results of original studies for the systematic review of blood meal sources of Anopheles mosquitoes in Ethiopia, 1997-2024. Table S3. All eligible studies and corresponding data points retrieved for the systematic review of blood meal sources of Anopheles mosquitoes, Ethiopia, 1997–2024.

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Ashine, T., Kochora, A., Shibru, H. et al. Plasticity of blood feeding behavior of Anopheles mosquitoes in Ethiopia: a systematic review. Parasites Vectors 17, 408 (2024). https://doi.org/10.1186/s13071-024-06493-1

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Parasites & Vectors

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