Practical application and the possible emergence of tick resistance to commonly used acaricides in various districts of Tanzania

Yakob Petro Nagagi, Esther Gwae Kimaro and Violet Temba

Livestock and Human Diseases Vector Control Division, Tropical Pesticides Research Institute, P O Box 3024, Arusha, Tanzania
petnagagi@gmail.com

Abstract

The use of acaricides to control ticks is the most useful and economically feasible conventional method of killing ticks. This study assessed the practical acaricide use and the susceptibility of ticks collected from various districts of Tanzania to commonly used acaricides. A cross-sectional study was conducted to collect information on dipping practices along with full engorged adult female ticks. In the laboratory, collected ticks were reared to produce larvae for larval packet test (PLT) against the technical grade of cypermethrin (94%), alphacypermethrin (97%) and chlorpyrifos (97%). Manufacturers’ recommended effective concentrations of acaricides were considered as resistance diagnostic reference/discriminating dose (DD). Descriptive statistics and Probit analysis were done using Statistical Package for the Social Sciences (SPSS). The result showed that hand spraying (knapsack sprayers) was the major acaricide application technique by most respondents. While 14.2% were unable to tell, 22.8%, 59.8% and 3.1% were spraying at the correct acaricides strength, above and below recommended concentrations respectively. Additionally, 10.2 % ranked acaricides as poor, and the rest had varied opinions from fair to best (best 25%, good 49.2%, better 10.9% and fair 4.7%) something that could account for most respondents (79.7%) who denied to experience any problem associated with acaricide ineffectiveness as their counterparts (20.3%). On the other hand, susceptibility test of stocks of ticks from districts of Gairo, Mvomero, Bariadi as well as Iringa (Yuang farm) and Singida Municipals showed variable levels of tolerance and resistance to alphacypermethrin and cypermethrin. Also, Boophilus microplus and Rhipicephalus evertsi from Iringa (Yuang farm) and Singida Municipal respectively were resistant to Chlorpyrifos. It was concluded that there is an emerging tick populations that are resistant to commonly used acaricide generics something that should call for a rational approach to revert the situation.

Keywords: Amblyomma variegatum, chlorpyrifos, Rhipicephalus evertsi, tick control

Introduction

Livestock keeping is an important component of rural livelihoods in African communities. Factors that may affect the health and productivity of livestock are important constraints in the development and wellbeing of such communities (Torr et al 2002). Unfortunately, diseases and parasites are a serious constraint affecting cattle production in many African countries including those in east Africa. Ticks and tick-borne diseases (TBDs) in particular – theileriosis (East Coast fever), babesiosis, anaplasmosis and cowdriosis (heart-water) are the most prevalent and exert a greatest economic bottleneck on cattle production in the region (Rubaire-Akiiki et al 2004; Okuthe and Buyu 2006; Swai et al 2005). In Tanzania, the most important tick-borne diseases are theileriosis, anaplasmosis, babesiosis and heartwater. Approximately 80% of the national cattle herds are at risk of being infected with TBDs each year and the direct economic losses are estimated at US$ 248 million including an estimated mortality of 0.92 million animals per year (Kivaria 2006). These diseases affect livestock production in various ways, such as reduced growth rate, milk production, fertility and value of hides, and mortality. In this way, the economic burden of TBDs is a serious limiting factor to the economic development of the developing countries (Estrada Peńa and Salman 2013).

Several attempts have been made to control ticks and TBDs by non-acaricidal means and none of them have potentially proved up-to standards (Kagaruki 1996). The most useful and economically feasible tick and TBDs control is the conventional method of killing ticks through application of acaricides to the surface of the animal. This is either applied through plunge dipping, spraying or hand-washing. The frequency of acaricide application depends on the acaricidal molecule but assumed generally an average of twice per week.

In Tanzania, acaricide application practices are individually practiced or provided through privately owned and commercially-run dip tanks (Mbassa et al 2009). The situation is further compounded with free market access of acaricides, inadequate technical know-how on acaricide application techniques, and lack of periodic tick monitoring. As a consequence, livestock keepers have frequently been using acaricides within similar group for a prolonged period. Indisputably, lack of monitoring and strategic alternation of acaricide groups can promote selection pressure that can lead to emergence of resistant tick strains (Abbas et al 2014). The current acaricides circulating in the markets were introduced many years back after removal of organochlorine-based acaricides. The earlier generation being organophosphorus-based acaricides which were later on followed by amitraz and synthetic pyrethroids in 1980s and 1990s (Kagaruki 199). This implies that acaricides-based on either organophosphorus, amitraz or pyrethroids have been an important part of cattle tick control in the country despite increased concern of ineffectiveness and environmental pollution (Swai et al 2005). This study was conducted from the hypothesis that the practical acaricides application practiced in Tanzania by individual livestock keepers with little or no technical support could have led to increased selection pressure and eventually emergence of resistant tick strains against commonly used acaricides. The study reports on the practical application of acaricides and susceptibility status of ticks to commonly used acaricides generics from various districts in Tanzania.

Materials and methods

Study Area

The study areas from which the survey was conducted includes Bariadi, Kishapu, Nzega, Kaliua, Mvomero, Gairo and Kongwa districts, also Iringa and Singida Municipals. The tick susceptibility test was conducted at the Division of Livestock and Human Diseases Vector Control, Tropical Pesticides Research Institute, Arusha.

Study Design

This study was conducted from July 2017 through June 2019. Cross-sectional study using structured questionnaires was adopted to enhance the collection of information on dipping practices along with full engorged and semi engorged adult female ticks. Purposive sampling was adopted whereby fully engorged female ticks were collected from wards/villages at which acaricide failure to ward-off ticks following dipping/spraying is reported. Tick samples were collected from at least 5 herds per district and from livestock auction markets and farms depending on their availability and accessibility at the time of collection. In each herd, at least 5 or more full-engorged and semi-engorged ticks were sampled and placed in perforated bottles. Collection of ticks were coupled with an enquiry on dipping practices from cattle owners and or herdsmen using pre-tested semi-structured questionnaires coupled with un-informal personal interview. A total of 128 questionnaires were administered.

Tick Identification and Rearing

The collected ticks were identified to species level based on morphological features as described by (Walker et al 2014). The identified tick species were categorized in accordance with village/ward and respective district. They were then placed into labeled individual tubes with a gauze stopper and incubated in small cylindrical containers with half-filled moist sand in the room that had 27 ± 1 ^oC and 70 % relative humidity for oviposition. After hatching, the larvae were maintained under similar conditions until they were 14 days before conducting the susceptibility test.

Tick Susceptibility Test

The susceptibility test was done in accordance with the larval packet test (LPT) (Shaw 1966). From the technical grade material of alphacypermethrin (97 % purity), cypermethrin (94 % purity) and Chlorpyrifos (97 % purity), respectively; various concentrations were prepared including 0.00078, 0.00157, 0.00313, 0.00625, 0.0125, 0.025, 0.05 and 0.1 % using diluents composed of olive oil and trichloroethene at 1:2 ratio. For each particular acaricide concentration, 0.67 ml was impregnated on a respective Whatman filter paper no. 1 in duplicate in a fume chamber. At each particular test run, Whatman filter paper no. 1 impregnated only with diluent was included. Approximately, 60 – 100 larvae were put on the impregnated filter papers and sealed with bulldog clips. The sealed filter papers containing the larvae were incubated at 70 % relative humidity and 27 ± 1 ^oC for 24 hrs after which mortality was recorded and susceptibility assessed after correction by Abbott’s formula (Abbott 1925).

Data analysis

Information from administered questionnaires was sorted and compiled using Microsoft Excel 2007. Descriptive analysis was carried out using a Statistical Package for Social Science (SPSS) version 16 (Chicago, SPSS Inc., USA). Furthermore, the standard application rate for a particular acaricide generic from the manufacturer’s instructions guide was considered as the discriminatory dose for resistance diagnosis.

Results

Tick samples

The number of tick samples that were collected from various herds, auction markets and farms for each district are shown in Table 1. The results show that while a proportion of less than 10% of the sampled sites were from Kaliua, Iringa Municipal and Kongwa, those from Bariadi, Kishapu, Nzega, Singida, Gairo and Mvomero districts were at proportion of more than 10%. The study was able to collect full engorged female tick of four species namely Amblyomma variegatum, Rhipicephalus evertsi, Boophilus decoloratus and Boophilus microplus. Amblyomma variegatum were encountered at Bariadi, Kaliua, Kishapu, Nzega, Singida and Kongwa districts. While Rhipicephalus evertsi were from Singida and Gairo districts, Boophilus microplus and B. decoloratus were encountered at Iringa Municipal and Mvomero, respectively.

Types of acaricides

The types of acaricides reported to be used by respondents are shown in Figure 1. The commonly used acaricides were Paranex^® 100 EC (10% Alphacypermethrin), Cybadip^® 15 EC (15% Cypermethrin) and Tixfix ^® (12.5 % Amitraz) reported by 43%, 20.3% and 11.7%, respectively. The other acaricides mentioned in less than 5% namely Albadip ^® (10% Alphacypermethrin), Stelladone^® (Chlorfenvinphos 300g/l) and Tiktik^® (12.5% Amitraz) were sparingly used and either mixed with Paranex^® or Cybadip ^® resulting into several cocktails. The practice of mixing included Duduba^® (Cypermethrin 100g/l and Chlorpyrifos 350g/l) which is a pesticide for insect control on crops. The use of cocktails was more predominantly in Gairo and Mvomero districts (Figure 1). It was also noted that Vectoclor plus^® (Cypermethrin 15g, Chlorpyrifos 25g, Piperonyl butoxide 25g and Citronella 1g)/100 mls) and Twigatraz ^® (12.5% Amitraz) were the preferred acaricides at Kongwa ranch and AK farm, respectively.

In this study, it was found that, the main suppliers for acaricides were Veterinary pharmaceuticals/Agrovet shops and auction markets mentioned by 45.3% and 54.7% of respondents, respectively.

Figure 1. Types of Acaricides reported to be used for tick control (Bariadi, n=16; Kaliua, n=8; Kishapu, n=19; Nzega, n=20; Singida, n=16; Iringa Municipal, n=7; Gairo, =17; Mvomero, n=17; Kongwa, n=8). The word “Other”, stands for acaricides that were mentioned in less than 5% and were mixed with either Paranex® or Cybadip®. These were Albadip®, Stelladone®, Tiktik® and Duduba®. It also includes Vectoclor plus® and Twigatraz® as stand-alone acaricides in dipping vats

Perception and practical application of acaricides

The application methods and livestock keepers’ perception on the performance of acaricides is given in Table 2. The results showed that while a relatively small number of respondents were using dipping vats (3.1%) and piece of cloth (1.6%), many were applying dip wash on their cattle using knapsack sprayers (95.3%). Also, a substantial number of respondents were applying acaricides twice per month (33.6%) and once per week (19.5%). The other applications frequencies were twice per week (10.9%), once per month (8.6%), once a year (4.7%), once ticks are seen (6.2%), after 4 months (2.3%), thrice a month (3.1%), once per six months (7.8%) and thrice a week (3.1%). There was huge variation on the acaricide dilution rates (Figure 2), with 14.2 % of respondents unable to tell. While a substantial number of respondents (59.8 %) were spraying above the recommendable concentration, 22.8% and 3.1 % sprayed at the correct and below manufacturers’ recommended concentrations, respectively. It was revealed that a combined percentage (72.6 %) of respondents who were applying acaricides once per month, once per week, twice a month and twice per week was relatively far higher than those at other frequencies (27.4 %) combined. Additionally, 10.2 % ranked acaricides as poor, and the rest had varied opinions from fair to best (best 25%, good 49.2%, better 10.9%, and fair 4.7%) something that could account for most respondents (79.7%) who denied to experience any problem associated with acaricide ineffectiveness as their counterparts (20.3%).

Tick Susceptibility

The susceptibility of tick stocks that were collected from various wards/villages/farm in various districts against chlorpyrifos, alphacypermethrin and cypermethrin are presented in Tables 3A, 3B and 3C, respectively. The results showed that LC₉₉ (lethal concentration that can kill 99% of the test population) of chlorpyrifos against stocks of  Boophilus microplus from Yuang Farm, Iringa was 0.012 and that of Rhipicephalus evertsi from Tondo in Singida Municipal was 0.11. Both were over two-folds the discriminatory dose (DD) of 0.03 – 0.05%. It was also found that tick stocks of Rhipicephalus evertsi from Chogo Ali, Boophilus decolaratus from Wami Sokoine ward and Amblyomma variegatum from Mwasinasi, Manga, Igandu and Shagihilu were all susceptible to chlorpyrifos, their LC99 were 0.036, 0.043, 0.017, 0.017, 0.0056 and 0.0059, respectively and well below the DD.

Nevertheless, the LC₉₉ of alphacypermethrin against stocks of Rhipicephalus evertsi from Chogo Ali was 0.019 and that of Tondo, Singida Municipal were 0.02% equivalent to 3.8 and 4 folds the DD of 0.003 – 0.005%, respectively. The LC₉₉ of alphacypermethrin against B. microplus from Yuang Farm (Iringa Municipal) was 0.5% equivalent to 99.8-fold the DD. While the stocks of B. decoloratus from Wami Sokoine, Mvomero district had LC₉₉ of 0.038% equivalent to 7.6-fold the DD, the one against A. variegatum from Bariadi, Nzega and Kishapu districts as well as Singida Municipal were 0.016%, 0.006%, 0.0066% and 0.016% respectively, with an increase of 1.14 – 3.14 folds the DD.

Figure 2. Cross-tabulation of Acaricide dilution rates and type of acaricide used. When using knapsack sprayers, manufacturers’ instruction guides indicates that pyrethroid-based acaricides are diluted at ratio of 1:2, 10 mls/20 litres of water and that of amitraz-based at 2:1, 20mls/10 litres of water

Lastly, the results show that the LC₉₉ of cypermethrin against stocks of B. microplus from Yuang Farm (Iringa Municipal) was 3.04% with an increase of 202-fold the DD (0.01 – 0.015%). Nevertheless, B. decoloratus from Mvomero district had LC₉₉ of 0.058% equivalent to 3.8-fold the DD. Additionally, the LC₉₉ of cypermethrin against A. variegatum from Bariadi district and Singida Municipal were slightly above the DD, 0.018% and 0.0164% respectively. But, the same species from Nzega and Kishapu districts were all susceptible to cypermethrin, the LC₉₉ being 0.0073% and 0.006% respectively, all below the DD. Similarly, R. evertsi from Gairo district was susceptible to cypermethrin with LC₉₉ being 0.013% as opposed to similar species from Singida Municipal which had LC₉₉ of 0.028% above the DD.

Discussion

Acaricides Practical Application

The aim of this study was to assess the susceptibility status of ticks and the practical application of commonly used acaricides from the various districts of Tanzania. Findings on the practical use of acaricides by the livestock keepers were based on the data collected from Singida Municipal, Bariadi, Kishapu, Mvomero, Gairo, Nzega and Kaliua districts. In this study, three acaricides brands (Paranex^®, Cybadip^® and Tixfix^®) were found to be widely and commonly used for tick control in the surveyed areas. The first-two have synthetic pyrethroids as active ingredient namely alphacypermethrin 10% and cypermethrin 15%, respectively. The latter contains amitraz, an amidine compound which has a different mode of action in comparison to above mentioned. The other brand products which some belong to organophosphorus and or similar groups as above were also used as stand-alone or mixed with either Paranex^®, Cybadip^® or Tixfix ^® resulting in several cocktails. We found more than half (54.7%) of livestock keepers purchase acaricides from the auction market. The auction market involves vendors who usually do not observe proper handling and storage of acaricides, for instance, there is no any precautions taken for protecting their products from sunlight and temperature which can deter acaricides efficacies. Evidence-based study indicates that temperature and UV-light can alter the biological efficacy of some pesticides contributing to their ineffectiveness (Soliman 2012).

Hand spraying (95.3 %) was the major acaricide application technique used by most respondents. This result is in line with what reported by Chenyambuga and colleagues (2010) that hand spraying is the main means of acaricide application by the majority of the livestock keepers in Lake Zone. Other studies in northern Tanzania (Kimaro et al 2018) also found that hand spraying was the most common method for tick control in the area. It is reported that hand-spraying method is potentially the least effective method for tick control (De Meneghi et al 2016). Field observations have shown that this method is largely associated with acaricide misuse such as lack of personal protection during handling and spraying, use of chemical concentration that is too low or above the recommendable dilution rates and partial exposure to ticks due to amount to treat each cattle not enough to the required standards (Addah et al 2009; De Meneghi et al 2016; Vudriko et al 2016). This can in a long run endanger livestock keepers’ health, promote environmental pollution and possible emergence of acaricide resistance (Spickett and Fivaz 1992; Swai et al 2005). Other acaricides application methods were smearing on cattle using a piece of cloth and plunge dipping which were only practiced by a few individuals, 1.6 % and 3.1 % respectively. Using a piece of cloth to dress the acaricides to the preferred tick-host attachment sites (eg. ears, udder, scrotum, perianal region, neck) besides being a time consuming activity which can be easily afforded with fewer animals with low tick burdens, it can also predispose livestock keepers to acaricide-toxic exposure.

In this study, we found that 59.8 % of livestock keepers were spraying their cattle above the recommended dilution rates the phenomenon that may lead to acaricide poisoning in livestock, with potential harmful residues in meat and milk, and toxicity to workers who apply them, also unnecessary costs and environmental pollution. This could probably be due to livestock keepers’ ignorance or insensitivity of ticks at the recommended dosage. The substantially and relatively higher number of those spraying acaricides once per week, twice per week, once per month and twice per month than their counterparts is an indication that many livestock keepers are aware of importance of tick control. These findings indicate that livestock keepers are aware that tick control can prevent occurrence of TBDs (Kagaruki 1996). However, these livestock keepers practiced a relatively wide-range of acaricide application frequencies which could most likely due to their experiences and economic capability. A study from Mbassa and colleagues (2009) showed that the application of acaricides by dipping animals once in 2 weeks in pastoral and agro-pastoral community was economical as it reduces the cost of acaricide and limits mortalities of animals due to TBDs. In another study in Serengeti district in Mara region, it was discovered that strictly tick control measure through dipping in some of the wards reduced tick infestations but increased incidences of animals to succumb from Theileria parva infection and ECF compared to the wards in which there was no strictly dipping/spraying regime (Laisser et al 2014). Therefore, a thorough understanding of the epidemiology of TBDs, experience of local knowledge, and strategies tailored from need assessment is essential before advocating a certain acaricide treatment regime.

Only a small percentage of respondents showed to experience problems of acaricides ineffectiveness than the majority of the respondents. This could probably complement the findings of this study that many of the respondents were applying acaricides at a high dosage rate and hence getting a successful tick and TBDs control outcome.

Recently, there has been enforcement on dipping programmes and substantial efforts by the Ministry of Livestock and Fisheries to revamp all un-functional plunge dips across the country as per Tanzania Livestock Master Plan 2017/2018 – 2021/2022 (Michael et al 2018). Thus, reviving of regular dipping of livestock through plunge dips for control of ticks in the country might solve a lot of issues related to acaricides application methods and environmental concerns.

Tick susceptibility against acaricide generics

The tick susceptibility against commonly used acaricides generics was conducted using ticks collected from Bariadi, Kishapu, Nzega, Singida Municipal, Iringa, Gairo and Mvomero. The difference in the number of sites visited for collection of full engorged female ticks observed in this study is largely due to accessibility and the number of cattle present in a particular district. The later factor is likely to accounts for more livestock keepers to experience problems associated with acaricide ineffectiveness. The ticks that were collected include Amblyomma variegatum, Rhipicephalus evertsi, Boophilus decoloratus and B. microplus. The most predominant being A. variegatum which is considered as the most catholic tick species in Tanzania (Lynen et al 2007). The full engorged female ticks of this species were encountered in almost all surveyed areas except in Iringa Municipal, Gairo and Mvomero district.

The assessment of ticks against chlorpyrifos, alphacypermethrin and cypermethrin, showed marked variation in the levels of resistance and susceptibility. Generally, the findings of this study provide some evidence of emerging tick resistance against commonly used acaricide generics in the study areas. It was observed that stocks of Boophilus microplus and Rhipicephalus evertsi from Yuang farm (Iringa Municipal) and Tondo (Singida Municipal) respectively, were resistant against chlorpyrifos. Likewise, stocks of R. evertsi from Chogo Ali (Gairo) and Tondo (Singida Municipal) as well as B. microplus from Yuang farm (Iringa Municipal), and Wami Sokoine (Mvomero) were resistant against alphacypermethrin. Resistance to alphacypermethrin was also observed from the stocks of Amblyomma variegatum from Mwasinasi (Bariadi) and Manga (Singida Municipal). Other stocks of A. variegatum from Igandu (Nzega) and Shagihilu (Kishapu) were only tolerance against alphacypermthrin. Furthermore, the study shows that stocks of B. microplus from Yuang farm (Iringa) were very resistant against cypermethrin. Similarly, resistance to cypermethrin was also observed from B. decoloratus and R. evertsi from Wami Sokoine (Mvomero) and Tondo (Singida Municipal), respectively. However, A. variegatum from Mwasinasi (Bariadi) and Manga (Singida Municipal) showed some levels of tolerance against cypermethrin.

The commonly used acaricides in the study area belong to pyrethroids and organophosphorus compounds which were introduced in the country following tick resistance against organochlorines and their subsequent removal from the market in 1980s (Kagaruki 1991). Misuse, presence of substandard products in the market, poor packaging and storage, and prolonged use of acaricides with the same mode of action, coupled with inadequate skills on the practical application could be among the factors that have contributed to the identified resistance to chlorpyrifos, alphacypermethrin and cypermethrin in the study areas. Continued acaricide failure to ward-off ticks is likely to aggravate the situation. Livestock keepers try to respond through increased frequencies of application and mixing of several products to formulate a number of cocktails (Vudriko et al 2016). Vudriko and colleagues (2016) in Uganda have reported that this practice can lead to collateral damage to cattle, food safety and public health. It is hereby recommended that the application of acaricides with dilution above the recommended standards should be discouraged since it could associate with public health problems, financial losses and possibly environmental pollution. However, more studies are required with a bigger coverage of many places across the country to provide a better understand of the level of tick resistance and its associated adverse effects in Tanzania. The findings obtained from this study will provide usefully information for the policymakers and relevant bodies to take the necessary action to halt tick resistance against commonly used acaricides in Tanzania.

Conclusions

• This study was conducted to assess tick susceptibility status and practical application of commonly used acaricides in various districts of Tanzania.
  
  
• It is revealed that alphacypermethrin, cypermethrin and amitraz based-acaricide products are commonly used in Singida Municipal, Bariadi, Kishapu, Nzega, Mvomero and Kaliua districts.
  
  
• Hand spraying is the most common acaricide application method for tick control in Singida Municipal, Bariadi, Kishapu, Nzega, Mvomero and Kaliua districts.
  
  
• There is a wide variation among livestock keepers’ perception on the regularity of acaricide application for tick control which could be due to various reasons.
  
  
• It is suggested that before recommending a certain acaricide treatment regime, a thorough understanding of TBDs epidemiology, local knowledge and experience, also needs assessment should prior be carried out.
  
  
• Findings from this study, indicates an emerging resistance of some species of ticks against alphacypermethrin, cypermethrin and chlorpyrifos. This calls for collective action to better understand the extent of the problem and how it can be contained as early as possible.

Acknowledgments

Authors would like to thank the government of the United Republic of Tanzania through the Tropical Pesticides Research Institute for funding this study. We are highly indebted and words are not enough to explain the support provided by the District Livestock Departments in areas visited for tick collection. We thank Elly Kawiche, Ibrahim Sungi and Adrian Massawe from the Division of Livestock and Human Diseases Vector Control who participated in data collection, tick rearing and susceptibility test. We also thank the livestock keepers who received us, and our driver Emmanuel Tesha for his tireless drive.

Conflict of interest

The authors declare that they have no conflict of interest.

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