Social acceptance and practicality of cattle-administered endectocides for malaria control in Vhembe District, Limpopo Province, South Africa

doi:10.21203/rs.3.rs-1537278/v1

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Social acceptance and practicality of cattle-administered endectocides for malaria control in Vhembe District, Limpopo Province, South Africa

https://doi.org/10.21203/rs.3.rs-1537278/v1

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Background: Malaria continues to be a leading cause of morbidity and mortality in Africa and conventional malaria control strategies such as indoor residual spraying (IRS) and insecticide-treated bednets (ITNs) are increasingly losing their effectiveness. Consequently, the development of alternative or supplementary strategies is required. One potential strategy is the use of cattle/livestock-administered endectocides to control vector mosquitoes that feed outdoors on livestock. However, since this strategy requires support from local communities and livestock owners consenting for their animals to be treated, it can only be implemented if acceptance by affected communities is sufficiently high. The aim of this study was to assess the social acceptance and practicality of the use of cattle/livestock-administered endectocides in the malaria endemic villages of Vhembe District, Limpopo Province, South Africa, where malaria incidence is high.

Methods: Questionnaires were administered in the Vhembe District in 103 livestock-owning households from four villages, namely, Gumbu, Malale, Manenzhe and Bale. The assessment included questions on the acceptability of the strategy, the type and number of livestock owned, distances between houses and kraals (overnight pens) as well as previous use and awareness of endectocides. The results were analysed using descriptive statistics and multinomial logistic regression.

Results: The types of livestock owned by the participants comprised, cattle, goats, sheep and donkeys, with the most dominant being goats (n = 1040) and cattle (964). The majority of the participants had their kraals less than 10 meters from their houses. Most participants (72.5%) reported that they were already using chemicals to treat their livestock for parasites. About 33.3% of the livestock owners reported that they or their family members had previous infections of malaria. All participants indicated that they would accept the implementation of the strategy and would give consent for their animals to be treated by endectocides.

Conclusions: The use of cattle/livestock-administered endectocides appears to be a feasible and acceptable approach for control of animal-feeding malaria vector species in the malaria endemic villages of Vhembe District in Limpopo Province. This is based on a high percentage of rural residents keeping suitable livestock close to their homes and expressing willingness to use endectocides for mosquito control.

Malaria

Endectocides

Cattle

Livestock

Community engagements

Social acceptability

Vector control

Malaria is a major global public health threat that continues to impact the well-being of people and nations. The 2021 Malaria Report of the World Health Organization (WHO) states that in 2020, there were 241 million cases associated with 627 000 deaths globally [1]. This increase of 14 million cases compared to the 229 million cases that were reported in 2019 occurred one year after commencement of the COVID-19 pandemic and the resulting service disruptions [1, 2]. Most of the cases (95%) were from the WHO African region followed by WHO Eastern Mediterranean and South-East Asian region which had 2.4% and 2% cases, respectively [1]. Malaria is caused by Plasmodium parasites, the most lethal and common in Africa being Plasmodium falciparum [3]. Female Anopheles mosquitoes of a particular range of species are responsible for transmitting Plasmodium parasites to human hosts [4]. Major malaria vectors in Africa are Anopheles arabiensis, An. gambiae and An. funestus [4, 5]. Several other Anopheles species are primary vectors in more limited geographic areas, while some species transmit malaria as secondary vectors [6]. Anopheles arabiensis is the primary malaria vector in South Africa [7, 8]. It is zoophilic, preferring to feed on cattle but will also readily feed on humans, mostly outdoors where they prefer to rest [9, 10]. These attributes make it much more difficult to target An. arabiensis using conventional vector control tools such as insecticide-treated bednets (ITNs) and indoor residual spraying (IRS).

In South Africa, malaria transmission is seasonal and most intense in the warm rainy season, which is typically from September to May [11, 12]. There are three malaria endemic provinces, Limpopo, Kwazulu-Natal and Mpumalanga [13, 14]. Since 2003, Limpopo has experienced the highest annual number of malaria cases [10, 15]. The majority of cases in Limpopo Province occur in the Vhembe District which accounts for more than 60% of malaria cases reported in South Africa [11, 12, 16]. The primary malaria control strategy in the Vhembe District is IRS [12, 17]. The IRS coverage in the malaria-affected areas of Limpopo Province was between 85% and 90% over the period of year 2010 to 2014 [15, 17]. Despite annual implementation of IRS, the Vhembe District remains heavily burdened with malaria, strongly suggesting that suitable supplementary or new control methods should be identified for deployment [15, 18].

Vhembe District (Fig. 1) in Limpopo Province is in the far north of South Africa and borders with Zimbabwe, Mozambique and Botswana [19]. Mozambique and Zimbabwe are high-transmission malaria-endemic countries and this contributes to the number of cases due to imported malaria, such cases setting up local foci for mosquito infection [13, 18, 20]. Vhembe is one of the least developed districts in South Africa with the greatest proportion of rural inhabitants [21]. It has approximately 1.3 million people and it is estimated that 65% of the population lives in poverty [22, 23]. Malaria is recognized as a disease of poverty and is concentrated in poor areas [24]. Poor housing structures without screened windows and doors in malaria-endemic villages increases contact between humans and mosquitoes, leading to an increase in malaria transmission [25].

The main activities in the Vhembe District include livestock and crop farming for subsistence purposes [26–28]. The district receives an average estimated annual rainfall of 820 mm [28]. Over 70% of land in the Limpopo Province is suitable for grazing [26, 29]. A large number of households in the malaria-endemic rural areas of the Vhembe District own livestock [30, 31]. Livestock can provide a blood meal to a large number of malaria vectors including An. arabiensis [32]. Therefore, cattle/livestock-administered endectocides seem a promising strategy that could be added to the current vector control strategies to control malaria in this region [33–35].

Endectocides, such as ivermectin and fipronil, are antiparasitic drugs that are active against both ecto- and endoparasites in humans and animals [36, 37]. Several studies have investigated the effect of endectocides against various malaria vectors such as An. arabiensis, An. coluzzii and An. gambiae in livestock, cattle in particular and show significant decreases in survival and fecundity [33–35]. The different routes of endectocides administration (injection, topical and oral) yield different degrees of effectivity and this must be considered before the strategy can be implemented [33]. Subcutaneous injections, which is the most expensive option, is more effective than topical and oral administrations [33–35]. Although the use of cattle/livestock-administered endectocides in the Vhembe District could be beneficial in malaria control programs, it is unclear how such a strategy would be perceived by the local communities. Before the implementation of any public health strategy, it is important to consider the community perception, attitude and knowledge towards such a strategy as acceptance can have significant impacts in its effectiveness [38]. For instance, in the Ebola outbreak that occurred in the West Africa in 2014, the local community played a key role in reducing the transmission, implementing community-based interventions including reducing body to body contact, wearing of protective gear and avoidance of crowding [39–42]. Another example of how the community’s acceptance is linked with the success of a health control strategy would be the patient separation from families and communities that was implemented to control the Marburg filovirus haemorrhagic fever outbreak that occurred in Angola in 2005 [43, 44].

The willingness of local farmers to enrol their livestock in an endectocide administration malaria control scheme would be similarly crucial for any planned intervention using endectocides. As chemical intervention strategies also come at a cost, effective interventions need to consider a number of factors for targeted applications. These include not only treating a sufficient number of livestock [36] but also preferentially treating those which are closer to human habitation and are thus, most likely to attract blood-seeking mosquitoes that may then feed on human hosts [45]. Consequently, livestock in close proximity of the houses and kraals (animal pens) should preferentially be targeted for interventions. Some vector control strategies require behavioural changes and may need to be maintained over time in order for them to be cost-effective, thus reinforcing the need for effective and sustained community engagement [46]. In the past, community livestock dipping programs in South Africa used to be popular and the costs were covered by the government [47]. However, due to lack of resources and funds, such programs were abandoned in most areas and livestock owners became responsible for treating their livestock for diseases and parasites [47–48]. The use of inexpensive endectocides therefore becomes critical, if such costs were to be paid by local rural poor livestock owners.

The aim of this study was to assess the social acceptance and practicality of potential future livestock endectocide administration as an additional tool for malaria control in the malaria endemic villages of Vhembe District. Our approach to assess the acceptability and feasibility of this strategy included capturing (1) possible determinants such as the type and size of livestock, (2) the relative proximity of houses and kraals (animal enclosures), (3) contributions of previous malaria experience to the communities attitudes towards the proposed strategy and (4) the nature and extent of already used chemicals to treat livestock.

Ethical statement

Ethical approval for this study was obtained from the University of Pretoria Ethics Committee (Ethics no: EC063-18, 180000035). A pre-visit meeting arranged for this study by community leaders with chiefs and livestock owners was held in each of the four villages. Permission from the chiefs and community leaders of the villages was obtained before the interviews commenced. The communities were informed about the project and we obtained support in advance. The purpose of the study and how questionnaires would be administered was explained. Livestock owners were notified that the interviewers would approach them in their households. The interviewers explained to each participant that their participation was voluntary, confidential and that they could withdraw from the study at any time without explanation. Each participant was requested to sign an informed consent form after the study was explained and they had agreed to participate. Illiterate participants were asked to put a cross next to their names that the interviewers had written for them on the consent forms. This occurred after the purpose of the study and the content of the questionnaire was explained to them in their native tongue (Tshivenda language). The community field workers acted as witnesses.

Study site and population

This study was conducted in the Vhembe District (Fig. 1) of Limpopo Province, a 25,597 km²area located around 22º85’ latitude and 30º71’ longitude [19, 27]. Vhembe district is populated by the Tshivenda speaking people. The study included four malaria-endemic villages; Gumbu, Malale, Manenzhe and Bale. Villages were chosen based on high malaria incidence and livestock population. The University of Pretoria Institute for Sustainable Malaria Control (UP ISMC) had previously conducted research in the area and the community was therefore familiar with such visits [49].

Questionnaire format

A questionnaire (see appendix) with 10 closed-ended questions and 1 open-ended question was designed to assess the social acceptability and practicality of the use of cattle/livestock-administered endectocides in malaria-endemic rural communities. It included both qualitative and quantitative questions. In order to allow estimates of the amount of endectocides required and the financial implications of an endectocide strategy in the region, the questionnaire sought to gather information about the composition and size of the livestock kept by respondents as well as the distance they were kept from human dwellings overnight. It is also important to know the kind of livestock owned by the households to decide on which animals should be treated with the endectocides in the community. Questions on the respondents’ view on the use of endectocides and the extent of their own use and experience with endectocide treatment of livestock for protection against parasites as well as personal experience with malaria infection were also included. The questionnaire was translated into the Tshivenda language and was validated by two Tshivenda speaking field workers from the malaria offices in the Vhembe District.

Data collection

Data were collected over a period of eight days. Cattle owners were the main target group as the endectocide strategy for malaria control has primarily been investigated in cattle. However, ownership of other livestock such as goats, sheep and donkeys were also noted. Interviewers selected every second household which had livestock. The aim was to interview as many livestock owners as possible with a minimum target of 30 households. In cases where the animals were away from the houses for grazing, the presence of a kraal was used to determine if a family owned livestock. As the majority of cattle owners were illiterate, interviewers read the questionnaires to the participants and recorded the answers. In houses where cattle owners were absent, an alternative adult family member who had information about the cattle was interviewed.

Data analysis

Collected data was analysed using the Statistical Package for the Social Sciences (IBM SPSS version 25) for statistical analyses. Due to the highly skewed responses received (see results section) this was largely restricted to descriptive statistics. In order to assess whether the number of livestock owned and the amount of chemicals previously used affected the preferred type of chemical application methods used by livestock owners, we employed a multinomial regression. The dependent variable was the type of application, comprising three categories: injection, topical and oral. The actual number of livestock (continuous variable) and the volume of chemicals (low: ≤ 4 litres, medium: 5-9 litres and high use: ≥10 litres) were included as independent variables.

We interviewed a total of 103 participants from households with livestock. Of these, 44 were from Gumbu village while 42, 9 and 8 were from Malale, Manenzhe and Bale villages, respectively. Cattle and goats made up the majority of ruminant livestock owned (Table 1) and 69% (71/103) participants owned cattle. Over half of the cattle owners (51%) also owned goats. Only 6% of the cattle owners also owned both goats and sheep. Two participants (2%) owned all four livestock species.

Table 1: The total numbers of cattle, sheep, goats and donkeys owned by the participants.

Animal	Numbers
Cattle	1040
Goats	964
Donkeys	74
Sheep	64

The majority of farmers (68%) owned 10 or less cattle and only a small number (7%) more than 30 (Fig. 2).

All of the participants supported the implementation of cattle-administered endectocides and said they would be willing to let their animals be treated. The participants provided several reasons for their support of endectocides as malaria control strategy. The majority (45.6%) desired to improve the health of their animals, while 36.9% of the participants aimed to reduce malaria cases, 17.5% were concerned about both malaria and animal health. About 33.3% of the participants reported that they themselves or their family members have had malaria. Among these participants, the vast majority (85.7%) also expressed their wish to reduce malaria cases in their rationale for accepting the strategy. Based on memory, participants reported the year they or their family members contracted malaria, ranging from 1979 to the interview date. There was an apparent increase in cases from 2015 onwards (Fig. 3). When asked if they thought malaria was a problem in their communities, only few participants (6.7%) responded with “no”. These participants or their family members did not have any history of contracting malaria. The rest of the participants were aware of the malaria burden and those that have not contracted it themselves reported that they knew people that have had malaria.

The majority of livestock owners (63.8%) kept their animals in kraals at their homes at night generally less than 10 meters from the house (Fig. 4). The remainder (36.2%) kept their animals at distant farms and only fetched them several times a month for health observations and treatment as necessary. The reasons for using distant farms were the limited water and food supplies available at their homes.

The majority of the participants (75.2%) reported that they had already been using chemicals to treat their livestock for ticks, worms and wounds. When they did not know the names of the chemicals, the information was collected by inspection of the containers. Redline Dip®, Supona Aerosol® and Deadline® were most frequently used (Table 2). Most participants (71.4%) could not distinguish whether the chemicals they were using treated worms or ticks specifically. However, the participants that used Ami-Tick® and Tick-Tack® reported that these were specifically for treatment against ticks. All participants that used Supona Aerosol® indicated that it was for treating wounds. All participants stated that they only used the chemicals occasionally when the animals were sick or had ticks and/or worms due to financial constraints. When asked how much of each chemical they used on their animals, some participants (22.4%) indicated that it depended on presence of parasites and how often the animals got sick. Other participants (21.1%) estimated that their chemicals lasted for a period of ± 3 months, while 15.8% and 19.7% reported that theirs lasted for ± 6 months and ± 1 month respectively. Only few participants (5.1%) reported that they continued to take their animals for community dipping while others complained that they were no longer receiving any services from these programmes. Participants’ responses for this question depended on how many animals they owned and how often they used the chemicals. For instance, a participant with 73 cattle and 21 goats reported that they purchase 20 litres of dip, which lasts them for approximately 3 months. This participant indicated that they mix the dip with water and spray on the animals. A participant with 16 cattle and 20 goats reported that they buy 1 litre bottles of Amitraz, Deadline and Tick-Tack which lasts them for approximately 2 months. All the participants indicated that they found chemicals expensive. The multinomial logistic regression indicated no significant relationship between the preferred methods of chemical applications (i.e. injection, topical and oral) and the number of livestock owned, as well as amount of chemicals used (X²= 45.417, df = 64, p = 0.962).

Table 2: Chemicals used on livestock and the number of participants using each of them.

Product name ®	Chemical class	Number of participants (%)	Target parasites	Active ingredients (%)	Method of Administration
Amitraz	Amidine	13 (12.4)	Lice, mites, ticks	Amitraz	Topical
Deadline Dip	Pyrethroid	22 (21.0)	Ticks, lice, flies	Flumethrin (1)	Topical
Supona Aerosol	Organophosphate	23 (21.9)	Maggots in wounds, ticks	Dichlorphos (0.74) Chlorfenvinphos (0.48)	Topical
Redline Dip	Pyrethroid	39 (37.1)	Ticks, lice	Flumethrin (1)	Topical
Tick-tack	Amidine	2 (1.9)	Ticks, mites	Amitraz (12.5)	Topical
Swavet	Retinoids (Vitamin A) & tocopherols (Vitamin E)	2 (1.9)	Supplement	Vitamin A & E	Oral
Ami-Tick	Acaricide	2 (1.9)	Ticks, fleas	Amitraz	Topical
Vit-B-Co	vitamin B1 (thiamine), B2 (pyridoxine), vitamin B12 (cyanocobalamine)	1 (0.95)	Supplement	Vitamin B	Oral
Triatix	Acaricide	2 (1.9)	Ticks, lice, mites	Amitraz	Topical
Terramycin	Tetracycline antibiotics	1 (0.95)	Tick-borne gall-sickness, pneumonia, footrot	Oxytetracycline	Injection
Valbazen	Anthelmintic benzimidazole	1 (0.95)	Liver flukes, tapeworms, stomach worms	Albendazole (11.36)	Oral

This study was conducted to assess the practicality and social acceptability of cattle/livestock-administered endectocides as additional malaria control strategy in the rural areas of Vhembe District, Limpopo Province, South Africa. Successful implementation of this technique would contribute evidence for potential application of endectocides in many other similar settings in Africa where Anopheles arabiensis predominates. Subsistence livestock farming is important in the study area [27, 50, 51], despite the cattle herds of most participants being small. Several previous studies conducted in the Vhembe District also reported small cattle herds for most farmers. Stroebel et al. (2011) reported that almost 60% of farmers in the Vhembe District own less than 10 head of cattle. Studies by Sikhweni et al. (2014) and Stroebel (2004), also in the Vhembe District, reported average herd sizes of 9 and 10.3, respectively. It will be crucial to determine a minimum herd size required for an effective treatment strategy. Possible treatment of other livestock such goats and sheep might increase the efficacy of the strategy. However, the use of endectocides for malaria control has mainly been on cattle. Several semi-field experiments on the use of cattle-administered endectocides for mosquito control have been conducted in Africa [33-35], while other host species such as pigs and sheep have also been experimented on in parts of Asia-Pacific [52].

Most livestock in the Vhembe District owners keep their livestock very close to the houses (0-4 m) which would be an advantage for an endectocide-based control strategy [53]. At the same time, the small herd size may make such a strategy more affordable for livestock owners if it is not publicly funded. The closer the kraals are to the participants’ houses, the higher an impact the transmission reduction strategy is likely to have [53-54]. Mosquito vector density in the homes might also increase when cattle serve as an attractant drawing mosquitoes from the surrounding area. Combining endectocide application with larval source management might also serve as an additional method to limit the symbiotic relationship between cattle and mosquitoes [55]. This involves the application of chemical or microbial insecticides, or predatory fish, to water bodies to target the immature, aquatic stages of the mosquito in order to reduce the emergence and abundance of adult vectors, or habitat and environmental modification to reduce breeding sites [55].

The large support for implementation of cattle/livestock-administered endectocides by participants from the Vhembe District appeared to be influenced primarily by the prospect of benefits to animal health and secondarily by the high incidence of malaria. Belonging to the poorest regions of the country means many subsistence farmers rely heavily on their livestock for income and food [27, 56]. Most participants were pleased to know that endectocides would also treat their livestock for other parasites such as tick and worms. The livestock owners indicated that they can barely afford the cost of the chemicals and would appreciate it if the animals can be treated at no cost. Since malaria is linked with poverty, improving livestock health can also reduce poverty [57, 58]. The majority of owners indicated that they used to take their animals for community dipping but the supply of such dipping had stopped. In South Africa, community dipping programs were conducted by the government and were aimed at controlling parasites such as ticks [59, 60]. The discontinuation of such programs in most areas means that livestock owners must purchase their own chemicals, which places the livestock health of those who cannot afford the chemicals at a risk [61]. Reinstating such programs using cattle/livestock-administered endectocides should be a cost-effective way to not only improve human but also animal health and combat poverty.

Most participants indicated awareness of the local malaria burden and many had personal experience with the disease in their family. The debilitating effects this may have had on their health but also the lack of funds for appropriate health care and deficiencies in the healthcare infrastructure in Vhembe District make this a financial as well as a public health challenge. This may have been a strong motivator for the positive attitude towards the proposed control strategy. The majority of participants had family members previously infected with malaria mostly between 2015 until 2019. Although this may partially be attributed to better memory of more recent incidences, this period also coincides with the global malaria increase in cases reported by the World Malaria Report (WHO 2019), which also calls for urgent action in the development and implementation of new strategies [62]. Based on the responses of the participants, it appears that cattle/livestock-administered endectocides for malaria control strategy would be a well-accepted strategy by the community, which bodes well for its application in the future. It has been shown repeatedly that community acceptance is crucial for the success of disease-control strategies. Studies that were conducted to assess the community acceptance of strategies implemented to break the transmission of the Ebola haemorrhagic fever highlighted the significance of community acceptance of the affected communities [63, 64]. The interventions that were implemented during the Marburg filovirus haemorrhagic fever outbreak in Angola in 2005 provides further evidence on how high community acceptance influences the efficacy of particular disease control strategies [43, 43].

The fact that a significant number of participants already had experience with the use of chemicals for animal health may have further affected their attitudes towards the use of such chemicals for malaria control. However, there may also be risks or disadvantages associated with the use of cattle/livestock-administered endectocides as a malaria control strategy. Different endectocides have different withdrawal periods applicable to slaughtering and consumption of milk products [65]. It is critical that livestock owners are informed of the withdrawal or waiting period. During our community meetings, we followed the instructions from the manufacturers for informing livestock owners of the withdrawal periods. We emphasized that earlier slaughtering could lead to drug residues present in meat and dairy products that could cause health effects in humans such as hypersensitivity reactions, allergies and reproductive disorders [66]. Since many respondents already used chemicals to treat the livestock in the area, livestock owners were aware of the concept of withdrawal period. However, due to the short duration of efficacy of endectocides [35], which may cause them to be administered more often, livestock owners might raise some concerns. Most of the chemicals already used by livestock owners have a withdrawal period of seven days before cattle or sheep can be slaughtered [67] but this period increases to 28 days for Terramycin® and Valbazen® [68]. While the withdrawal period for one of the proposed endectocides (ivermectin, 21 days) falls within this time frame it is substantially longer for fipronil with 105 days [65]. The longer withdrawal periods for fipronil might influence the communities not to allow their animals participate in an endectocide-based program. Hence, careful consideration has to be given before choosing a particular endectocide before implementation of such control.

The size of the livestock population and the farming practices, including overnight securing of such animals close to human habitation in one of the malaria hotspots (Vhembe District) of South Africa, suggest that the use of cattle/livestock-administered endectocides for malaria control would be a feasible strategy in Vhembe. Acceptance by livestock owners appears very high as a result of the awareness of benefits to both animal and human health, as well as familiarity with chemicals used to control livestock parasites. The implementation of such a strategy could thus not only reduce the malaria mosquito vector density but improve animal health and alleviate poverty. Financial constraints would constitute the largest impediment to its implementation and would require financial assistance from government. This may similarly apply to other African regions with a comparable community structures.

Ethics Approval

Ethical clearance for use of cattle was obtained from the University of Pretoria Animals Ethics Review Committee (Ethics reference number: EC063-18, 180000035).

Consent for publication

Not applicable.

Availability of data and materials

The datasets can be made available by the corresponding author upon reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

TM was the recipient of a Dr Sylvia Meek scholarship from the Malaria Consortium, which enabled this study. We also acknowledge the financial support received from the National Research Foundation of South Africa.

Authors' contributions

TM, LB and HL designed the study. TM conducted the interviews. TM wrote the initial draft of the manuscript. MB assisted with the revision of the manuscript. All authors edited and approved the final manuscript.

Acknowledgements

The University of Pretoria Institute for Sustainable Malaria Control (UP ISMC, MRC-collaborating Centre) is acknowledged for assisting with the organization and conduction of the interviews. We also thank the livestock owners from the Vhembe District who participated in the project.

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Social acceptance and practicality of cattle-administered endectocides for malaria control in Vhembe District, Limpopo Province, South Africa

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