Haematopinus suis Infestation in Pig Farms in Busogo Sector, Rwanda

Haematopinus suis(H. suis) is a common ectoparasite of pigs and is economically important worldwide. H. suis is responsible for anemia and poor feed conversion rate that lead to poor growth in pig husbandry. This study assessed the prevalence and risk factors of H. suis in pigs through a cross-sectional survey in Busogo sector of Musanze district. Fifty-five (55) pigs, representing 10% of 555 pigs from 20 farms, were examined physically for the presence of H. suis, and a total number of 559 H. suis were collected from them in Busogo sector of Musanze district. Data were analyzed using the Statistical Package for the Social Sciences (SPSS). Results showed that out of 55 pigs, a total number of 35 pigs (63.6%), were found infested with H. suis in Busogo sector of Musanze district. The infestation by H. suis was associated with the farming system, animal breeds, animal's category, sex, pig hygiene, and piggery hygiene. Results showed a high (P < 0.05) prevalence in pigs reared in the intensive system (91.4%), whereas large whites were the most affected breed (60%). The prevalence of H. suis varied significantly (P < 0.05) among sexes, and females were the most affected (60%). Results related to pig hygiene revealed that all farmers were practicing washing skin three times per week, whereas only 60.0% of them were removing the bedding in their piggery. The study concluded that H. suis is present and remains a problem in the study area. Therefore, the study recommends to create farmer's awareness on the disease in pigs and its impact through training. Researchers should continue further studies on H. suis prevention with appropriate pig husbandry and management practices and the efficacy of acaricides used.


Introduction
Te livestock sector plays an important role in sustainability of the world economy and attains food security in terms of protein availability and poverty alleviation [1,2]. It can also provide livelihood and employment [3]. Most pigs are raised by smallholders in extensive, semiextensive, and intensive systems [4,5]. Pig farming requires in general too much attention related to biosecurity measures, control, and management. Despite the biosecurity measures, ectoparasite such as Haematopinus suis remains a problem that is not well known and may be difcult to control. Tis parasite is one of the zoonotic ectoparasites of public importance and the common and largest prevalent ectoparasite of pigs in very cold environments and during high rainfall [6,7]. H. suis is the only species of louse that infests pigs of all ages worldwide. It is a sucking louse which gets blood meals from the host through its penetrating mouth parts [8].
Most frequently, H. suis is responsible for persistent irritation, and biting witches may lead to reduction of feed efciency with the possibility of anemia caused by loss of blood, hair loss, and disease spread [9,10]. Tis happens mainly in pigs reared in poor infrastructures which lead to a low level of implementation of biosecurity measures [11].
In domesticated pigs, the parasites and their eggs can be found in the fence lines, dry feed, and mangers as well, with the ear, tail regions, and neck being the favored living site of the pig with restriction to the skin surface [12].
Te following risk factors have been attributed to new purchased infected animals: lack of proper hygiene and disinfection, lack or inadequate parasite control, lack of housing, age of pigs, season, methods of cleaning [14,19], and existence of infected pigs in the neighbouring farms [6].
Regardless of that, H. suis heavy infestations afect growth rates, cause anemia, and lead to economic loss in pig farming systems; there is no information of H. suis infestations in pigs in Rwanda. For that reason, this is the frst work of H. suis infestation in Rwanda.

Study Sites and Questionnaire.
Te study was conducted in Busogo Sector (Figure 1), located in Musanze District in Northern Province of Rwanda. Busogo Sector is made of 4 cells which are Gisesero, Sahara, Kavumu, and Nyagisozi. It has a mean altitude of 2300 m with the highest point being at 2800 m. Te climate has a mean temperature of 16.7°C and much rain comprising between 1400 and 1800 mm. Busogo Sector has 4 seasons, which are divided as follows: a short dry season from mid-December to mid-February, a heavy rainy season from mid-February to the end of June, a heavy dry season extending from June to August, and a short rainy season from August to mid-December. Busogo Sector has mainly volcanic soil which is very permeable with low depth on mountains and moderate depth in lower altitude. Tis kind of soil is subjected to many erosion phenomena in the area of abrupt slope. Te population is around 15,795 inhabitants, where 45.1% are male and 54.9% are female. Te total surface area is 20.5 km 2 with the population density of 787.8 inhabitants per km 2 . Most of the people in Busogo Sector are involved in agriculture, and the main crops grown are potatoes, maize, beans, and vegetables. Te fauna is not dominating in those sectors because a good number of wild animals have migrated in the national parks because of hunters. On the side of fora, the natural vegetation is no longer present because of agricultural activities [20].

Study Design and Data Collection.
A cross-sectional survey was conducted to collect qualitative data through face-to-face interviews using a structured questionnaire. Te survey targeted pig's smallholder farmers who were identifed and selected using the snowballing method at the cell level. However, the population size of pigs raised in Busogo sector was unknown; the larger sample size such as 10% of pigs was determined and used to determine the population size of a given pen. Data collected included the type of farming system, breeds, age, and hygienic management. At the animal level, observation and examination of the pig skin and skin lesions throughout the external surface of the body were performed and H. suis presence was also recorded.

Data Analysis.
Data collected were recorded, encoded using Microsoft Excel 2007, and then exposed to the Statistical Package for Social Sciences (SPSS) version 21 for analysis. Descriptive statistics were used to summarize the social characteristics of farmers, farm characteristics, the infestation level, and the distribution of infested animals according to the farming system, breed, animal sex, and piggeries and pig hygiene. Results were interpreted using tables and fgures.

Social Characteristics of Farmers in Busogo Sector (n � 20).
A total of 20 pig smallholder farmers were interviewed in Busogo sector of Musanze District. Results from Table 1 shows that all (100%) farmers interviewed were within the age range between 60 and 70 years old and 85.0% of them were males. Out of the 20 smallholder farmers interviewed, 85.0% were involved in farming while the remaining 15% were involved in other activities as a primary occupation but took on farming as a secondary occupation. Majority 90.0% of them are practicing the intensive system, while 50.0% have experience of 1 to 2 years and another 50.0% have experience of 3 to 4 years. In the area studied, the educational level of the farmers shows that the majority 35.0% of farmers interviewed attended the university. Considering the location of majority of pig farmers interviewed, 55.0% are located in Sahara cells, while 40.0% and 5.0% are from Gisesero and Kavumu cells, respectively. Te majority of farmers are using piggery constructed of wall timber (95.0%).

Farm Animal's Characteristics in Busogo Sector (n � 55).
Results (Figure 2) indicate that the total number of pigs by the cell was 27, 27, and 1, for Sahara, Gisesero, and Kavumu cells, respectively. Results also show that the majority of pigs reared in the study area was represented by the large white breed (85.5%) and adult female category (45.5%).   Pig production experience (years)

Discussion
Out of 55 pigs, 35 (63.6%) of them were found infested with H. suis after practical examination of the skin. Te prevalence of infestation was found more in pigs reared in the intensive system (90.0%) than the pigs maintained in individual houses in village condition (10.0%). According to the number of pigs observed, the results indicated that the Sahara cell has a high number of pigs infested by H. suis (54.4%) compared to Nyagisozi and Kavumu cells. Te study elsewhere indicated that congestion and inefective hygiene in piggeries are contributing factors in most farms to infestation by H. suis. Te high number of infested pigs by H. suis in Sahara cells may be attributed to the fact that the Sahara cell has a high number of pigs reared in the intensive system which has been shown to have more pigs infested (91.4%) than other farming systems. Tis will require training farmers on the prevention and control of ectoparasites in pigs. Tese results difered from those reported by Kagira et al. [15] in Kenya and Islam et al. [5].
Tese results confrm the results by Islam et al., [22], and Islam et al., [7] reported high infestation by H. suis (100.0%) in intensive pigs in Bangladesh. Tese results do not agree with what Radostits et al. [23] reported, that pigs kept outdoors and those in poor body condition are more susceptible to H. suis than pigs in pens. Results suggest that there is a chance of spread of H. suis infestation in the housed farms which occurred by close contact between pigs or by contact with recently contaminated surfaces.
Results related to the sex of pigs indicated that the females are more attacked by H. suis than males. Tese results are in agreement with Kagira et al. [15], who reported the highest prevalence of H. suis in male (96.7) than in female (94.8) pigs in Kenya. Te prevalence of H. suis was associated with the category of pigs, being highest in adult females but lowest in piglets and adult males. Tese corroborate with the results by Odo et al., [16] in Nigeria. Te higher prevalence of H. suis in adult females could be attributed to the period the adult female pigs had been kept in the farm compared to the other categories of pigs. Tese results are in agreement with Samuel et al., [24] in USA, who reported that the higher prevalence of H. suis in sows could be related to the age of pigs.
Based on the piggery and pig's hygiene, the results revealed that piggery hygiene was done by cleaning with water (50.0%), removing bedding (60.0%), and using different materials such as soaps and brushes (75.0%), while at the animal level, pigs were washed three times per week. Tese results difered from those by Nsoso et al. [14], who reported that only 50% of farmers were removing the manure without any other form of disinfection or cleaning. Tis way of practice in pig husbandry may expose pigs to various parasites and the spread of many other pig diseases. Tese results suggest that the low hygiene in piggeries and on pigs could be the contributing factor of the high infestation by H. suis. Terefore, we would recommend a good and effective protocol of cleaning and disinfection of piggeries in Busogo sector, which will help in the disease control, reduction of antibiotic usage, risk of zoonosis, and reduction in disease.

Conclusion
Te study concluded that H. suis is present in Busogo sector and afects more pigs reared in the intensive system with inefective removal of bedding in piggery. Terefore, there are no data on the H. suis of domesticated pigs in Rwanda Journal of Tropical Medicine 5 and yet the adoption of an intensive system is mandatory in pig husbandry in Rwanda. Studies to detect the H. suis parasites are needed because of their negative economic impact on the farmer's livelihood. However, appropriate steps should be taken by the government to create awareness on the parasite and its economic impact and promote the protocol of use of acaricides in the prevention of H. suis in pig husbandry. Further studies are recommended on the efcacy of acaricides used in the prevention of H. suis.

Data Availability
Te data used are available in the manuscript.

Ethical Approval
Te permission for conducting this study was provided by University of Rwanda, College of Agriculture, Animal Science and Veterinary Medicine in collaboration with Busogo sector. Farmers were given explanations about the purpose of this research before data collection, and their participation was voluntary.

Conflicts of Interest
Te authors declare that they have no conficts of interest.