Management and biosecurity practices on pig farms in the Western Highlands of Cameroon (Central Africa)

Abstract African swine fever (ASF), erysipelas and many other infectious and parasitic diseases have seriously compromised the future of pig industry in the Western Highlands of Cameroon. Since implementation of biosecurity measures (BM) is known to reduce the risk of disease transmission, the objective of this study was to describe the pig farming management system as well as the biosecurity practices on pig farms in the Western Highlands of Cameroon. Therefore, 97 farms were investigated using a face‐to‐face interview‐based questionnaire. Biosecurity practices were divided in three components: isolation, traffic control and sanitation. The results revealed that the majority of farms were extensive (73.22%), farrow‐to‐finish farms (59.79%) and essentially raising crossed‐bred (72.75%). The most practiced BM regarding ‘isolation’ were as follows: maintenance of the minimum distance between farms (56.06%) and dispatching of animals of same age in the same room (97.16%); for ‘traffic control’, the measures included the following: assignment of specific tools and equipment (96.86%) to a specific piggery; concerning ‘sanitation’, daily cleaning (97.06%), as well as using disinfectants (89.13%) were mostly implemented. The measures less implemented for ‘isolation’ included fencing (11.83%), compliance with the all‐in all‐out principle (10.11%), use of specific clothing (6.03%) and quarantine (7.69%); for ‘traffic control’, the less adopted measures comprised visitor hands washed before animal handling (11.65%), respect of linear flow principle (13.52%). Concerning ‘sanitation’, these measures included functional footbath (29.90%), processing of drinking water (27.84%) and cleanout (18.14%). The biosecurity level was low, intermediate and high for 73.71, 21.55 and 4.73% of farms, respectively. This low level suggests that ASF and other diseases are likely to remain endemic. The most important measures of concern and to improve are as follows: not feeding kitchen waste to pigs; keeping other livestock species away from pigs; fencing pig barn; keeping newly arrived animals in quarantine, not exchanging boars; not selling sick animals.


| INTRODUC TI ON
Pig production has been increasing in the world, with animal number growing from 856 241 to 977 021 thousand heads in 2000and 2013, respectively (FAO, 2015. The production in Cameroon is following the world trend (from 2 440 404 heads in 2010 to 2 896 271 heads in 2012) due to high demand resulting from the growing population.
Though the country is the largest pig producer in Central Africa (MINEPIA, 2009), the demand is not satisfied due to a number of constraints including poor technical inputs in the production system (untrained personnel, old, defective, and worn equipment, inappropriate building among other), poor feeding (low standard feed and lack of feed supplement) and poor health (MINEPIA, 2009). Among the disease challenges, African swine fever (ASF) and erysipelas alone are responsible for heavy losses due to outbreaks that occur almost every year in Cameroon (MINEPIA, 2009). Other infectious diseases reported to occur include hog cholera, porcine encephalomyelitis, Aujeszky's disease, enteritis, transmissible gastroenteritis, porcine encephalomyelitis, erysipelas, dysentery, pasteurellosis, tuberculosis and salmonellosis (MINEPIA, 2009 (Kouam, Ngueguim & Kantzoura, 2018) are not the least, causing considerable economic losses due to reduced weight gain, litter size, poor growth rates, visceral organ condemnation at slaughter and deaths (Kauffman, 1996;Pitman, 2010;Stewart & Hale, 1988). Thus, one of the important measures to increase pig productivity should be in the area of disease control. Due to the large number of diseases in pigs, implementation of biosecurity measures (BM) in pig production is of paramount importance. For instance, the prevalence of porcine reproductive and respiratory syndrome and Mycoplasma hyopneumoniae has been associated with the level of biosecurity at farm level (Austin, Weigek, Hungerford, & Biehl, 1993;Lambert, Arsenault, Polkak, & D'Allaire, 2012). Reversely, several pig diseases (intestinal and miscellaneous diseases) have been successfully controlled through the respect of biosecurity practices in some countries (Wallgren, 2009).
Nowadays, the implementation of BM is regarded as a powerful tool in the control of diseases on the farm; its main advantage is the potential to keep pathogens off the farm and to prevent pathogens from spreading to other farms. Biosecurity can be defined as a set of management practices or measures to prevent introduction and spread of pathogens within and between farms (Fasina, Lazarus, Spencer, Makinde, & Bastos, 2012;Gueye, 2008;Gunn, Heffernan, Hall, McLeod, & Hovi, 2008). In pig production specifically, biosecurity is defined as 'the implementation of measures that reduce the risk of introduction and spread of disease agents; it requires the adoption of a set of attitudes and behaviours by people to reduce risk in all activities involving domestic, captive/exotic and wild animals and their products' (FAO/ OIE/ World bank, 2010). BM are divided into three components: isolation, traffic control and sanitation (Cardona & Kuney, 2001;FAO/ OIE/ World bank, 2010). Isolation can be regarded as measures related to physical barriers (fence, showers or footbath) and distance between farms in order to limit contacts between infected animals and contaminated objects with diseasefree farms (FAO, 2008). Traffic control can be considered as the restriction of feedstuff, human, equipment and animal movement onto the farm (FAO, 2008). Sanitation refers to the cleaning and disinfection of animal housing, people material and equipment (Cardona & Kuney, 2001).
Despite the usefulness and impact of BM adoption, no information to assist policymakers in pig industry is available regarding the level of biosecurity implementation in pig farming in the Western Highlands of Cameroon where a number of infectious and parasitic diseases occur (MINEPIA, 2009). Therefore, the overall aim of this study was to describe the pig production management system as well as the associated biosecurity practices in the Western Highlands of Cameroon. Specifically, the three main objectives of this study were (a) to provide the general characteristics of pig farming, (b) to characterize the biosecurity practices and (c) to assess the biosecurity level of pig farms.

| Study area
The study was carried out from May to July 2017 on pig farms located in Menoua Division of the Western Highlands of Cameroon.
The subdivisions, Dschang, Fokoue and Penka Michel within the Menoua Division, were chosen due to the importance of pig farming in these locations, as advised by the local veterinary health officials.
The area lies between longitude 9°49'-10°20' East of the Greenwish meridian and latitude 5°17'-6°22' North of the equator (Figure 1). The region is characterized by a typical climate with two main seasons, the dry season ranging from November to mid-March and the rainy season which prevail from mid-March to October. Temperature ranges between 15° and 24°C (IRAD, 2012). Livestock species include pigs, small ruminants, cattle, cavies and poultry. The Western Highlands are one of the largest pig production areas of the country and one of the foci of ASF outbreak in the country (MINEPIA, 2009;MINEPIA/FAO, 2009).

| Questionnaire design
The questionnaire consisted of closed question sets (the tables in this manuscript include all the questionnaire items) related to production characteristics (farm size, breed and production system, among others) and biosecurity components (isolation, traffic control and sanitation items). Questions were constructed based on the epidemiology of common pig diseases in Cameroon, with special focus on ASF and erysipelas (MINEPIA, 2009). Before starting the present study, the questionnaire was tested. Testing of the questionnaire was carried out by interviewing a sub-sample of farmers (n = 15) in the study area to check the accuracy and clarity of questions, and whether some questions were missing or redundant. Adjustments were made accordingly.

| Selection of farms
In absence of the official registry of pig farms, farms were first located with the help of the local veterinary health officials. The next farms were located using the snow ball technique where the previously located farmer helped to identify the next farmer and so on.
The process continued until no new farm could be found within the study area. The survey with the aid of a questionnaire was carried out through a face-to-face interview between the researcher and the farmers and through the personal observations of the researcher.

| Determination of the adoption level of biosecurity measures by farmers
The adoption level of a given measure was obtained by dividing the total number of farms applying that measure by the total number of farms; the ratio was expressed as a percentage.

| Determination of the overall observance of biosecurity measures on the farm
The overall observance is the ratio of applied BM to the required measures expressed in percentage (Racicot & Vaillanourt, 2009). If the ratio is equal or less than 25%, the biosecurity level on the farm is qualified as low. If the ratio falls between 26% and 74%, then the adoption level of BM is intermediate, and the biosecurity level is referred to as intermediate. If it is equal or more than 75%, then the biosecurity level is good (Racicot & Vaillanourt, 2009).

| Statistical analysis
The responses obtained were subjected to descriptive statistics (frequency and mean). Data were analysed using the SPSS statistical package (version 13.0, SPSS Inc., USA). Only 11.34% of farmers only gave concentrate to pigs while none exclusively gave kitchen waste to animals. The mean age at first farrowing was 8.70 ± 1.33 months and piglets were weaned within 52.39 ± 7.80 days. The average flock size was 16.87 ± 11.04 pigs and the number of litter per year was 2.

| Biosecurity measures related to the 'isolation' component
More than half of the farms (55.08%) were located in less than 500 m from the main road, whereas 51.06% complied with the minimum distance of 500 recommended between two farms. Only 11.83% of farms were fenced and none had a sign board forbidding access to Annual farrowing number 2 ± 00 2 ± 00 2 ± 00 2 ± 00 Note: N = total number of farms. n = number of farm per subdivision. *Values in the table are in percentage, except for continuous variables (age at first farrowing, weaning age, herd size and annual farrowing number) which are presented as mean ± standard deviation. a extensive system = animals of relatively small number (local and/or crossed breed) are permanently penned and feed on agriculture by-products and kitchen wastes; semi-intensive system = crossed bred animals are permanently penned in piggeries with a roughcast floor, feed on kitchen waste, agricultural by-products and often industrial feed; intensive system = animals are improved breeds, indoors, in high number; the piggery is a modern building; feedstuff is exclusively industrial; management system is modern Building according to the linear flow principle means that the piggery is built in such a way that a farmer or a visitor must move in one direction only, generally from the clean to the dirty area and from the young to the old, without turning back. It was unusual for visitors (11.65%) to wash their hands before touching pigs, whereas 28.87% of farmers reintroduced pigs returning from markets into the herd.
Dedication of tools and equipment to a specific piggery within a farm was close to 100% (96.86%). Among farms, exchange of tools and equipment was very uncommon (4.63%). About 32% of farmers borrowed boars from neighbouring farms for breeding purposes.

| Biosecurity measures related to the 'sanitation' component
Results on sanitation practices (

| Overall observance of biosecurity measures
As a whole, the vast majority (73.71%) of farms had a low biosecurity level (adoption rate of BM equal or less than 25%). A very few (4.73%) farms had a good level of biosecurity (

| D ISCUSS I ON
This study described the general characteristics of pig husbandry in an area within the Western Highlands of Cameroon, one of the largest pig production regions of the country (MINEPIA, 2009). The extensive production system was found to be the most predominant.
Our result is similar to previous findings by the Ministry of livestock, fisheries and animal industry (MINEPIA, 2011). This may be partly explained by the family attachment to traditions and secondly by the lack of financial means and adequate training. Most farmers were engaged in both piglets production and fattening (farrow-to-finish) and the least preferred production option was fattening. This could be due to the fact that piglets are readily sold. The crossed breeds were reared by most farmers (72.75%). This percentage (72.75%) is higher than 56.80% reported by Ndébi, Kamajou, and Ongla (2009) and could be related to the fact that with time farmers have noticed that the mixed breeds are zoo-technically more efficient than the pure local breeds (heterosis effect). Man power in the study area was essentially made up of family members, confirming the results obtained by other authors (Ndébi et al., 2009)

in the Western
Highlands of Cameroon. This may be explained by the low income which precludes farmers from hiring off-family workers. The insufficient income corroborates with the low herd size (16.08 ± 11.04), the production system and the feedstuff (kitchen waste and concentrate) used in most farms (88.65%). Combining kitchen waste with concentrate is more economical than using concentrate alone.
However, since kitchen waste is not heated before supply to animals, TA B L E 4 Overall level of biosecurity measures according to biosecurity components in Menoua Division may be due to the fact that the majority of farms belong to the extensive management system. Other animal species were found in 91% of farms, which is a serious biosecurity problem since cross transmission of pathogens between different species has been demonstrated (Pensaert, Ottis, Vandeputte, Kaplan, & Bachmann, 1981;Wall et al., 1995). The poor situation is worsened by the fact that the fence was absent around most piggeries, making a contact between pigs and wildlife possible. Some diseases/pathogens that can be transmitted from other animals to pigs or vice versa include: Bordetella spp., avian tuberculosis, Salmonella spp. and avian influenza (Anonymous, 2010;Pensaert et al., 1981;Vangroenweghe et al., 2009) from birds to pigs; classical swine fever (Fritzemeier et al., 2000) and Aujesky's disease (Artois et al., 2002) from wild boar to pigs; Salmonella Typhimurium between pigs, poultry and ruminants (Wall et al., 1995). The all-in/all-out principle was followed In fact, this principle was shown to break the infectious cycle of pathogens from one production round to another (Clark, Freeman, Scheidt, & Knox, 1991). Similarly, there was a poor implementation of quarantine area (7.69%). This might be explained by the fact that the vast majority of farmers have not been trained in pig farming and in biosecurity practices. Also, only 6.03% of farmers used farmspecific clothes and boots, which is very risky as humans can act as mechanical vectors of disease to pigs. In this case, transmission may occur through leftovers of urine and faeces from infected animals on footwear and clothing as has been proven through experiments for several germs, among which E. coli (Amass et al., 2003) and classical swine fever virus (Ribbens, Dewulf, Koenen, Maes, & Kruif, 2007). A vast majority of farmers (97.16%) kept animals of same age-group in the same unit (piglets, growers and adults separated and kept in different units). This is a good measure that reduces the risk of infections spread. Another good measure is the fact that most employees did not raise pigs at home; this result is probably explained by the fact that most farms (80.10%) had family members as the main work force.
As far as 'traffic control' is concerned, implementation of BM appears to be related to the husbandry system. The low adoption level (13.52%) of the linear flow principle is consistent with the low number of farms under intensive and semi-intensive system (4.33 and 22.45%, respectively). The main advantage of the principle is that the 'clean area' cannot be contaminated by a pathogen from the dirty area, unless rodents and insect control is poor or the clean road is used by unclean and non-disinfected vehicles (Neumann, 2012). The majority of farms assigned a specific employee to a specific piggery. As the number of visitors should be limited on a farm, so also should the number of workers per animal barn be limited.
Otherwise, an employee taking care of several buildings can transmit pathogen from one building to another (Kapperud et al., 1993).
This result is explained by the fact that most farms are made up of a single animal barn. In a few farms (11.65%), visitors washed their hands before touching an animal; again, this finding is consistent with the low number of farms under semi-intensive and intensive husbandry system where the biosecurity level has been reported to be higher than in extensive system (FAO/OIE/Work Bank, 2010); the fact that only this percentage of farms adopted this measure is a serious biosecurity flaw in the area. In general, production tools and equipment were specific for a piggery, which is in line with the fact that these tools and equipment were exchanged among farms only by a very limited number of farmers. However, the protective effect of these measures was jeopardized by the habit to exchange boars among 31.96% of farms for reproduction purposes. It is well established that introduction of new genetic materials (semen) or animals from different source herds increases the risk of disease introduction into the pig farm (Hege, Zimmermann, Scheidegger, & Stärk, 2002;Lo Fo Wong, 2004;Pritchard et al., 2005). Exchange of animals among farms is one of the most rapid ways for disease dissemination because an animal may apparently look healthy while it is a chronic, As a whole, the biosecurity level on farms in the study area was low, with up to 73.71% of farms having an adoption rate equal or less than 25.00%. The low biosecurity level is probably related to the fact that the majority of farms operated under extensive system. Our finding is in accordance with the FAO/OIE/Work Bank (2010) observations. Considering the three components of biosecurity, the highest percentage of farms with an adoption rate of BM equal or more than 75.00% was not greater than 10.00%, with the 'traffic control' component enjoying the first position (9.70%), followed by the 'isolation' (4.70%) component and finally the 'sanitation' component occupying the last position (2.97%). This low level of biosecurity observed for all the components suggests that farmers do not have any understanding of biosecurity principles in pig farming, and that steps (training and sensitization) should be taken to fill the gap.
In conclusion, the production system in the Menoua Division was dominated by the extensive pig production system. The low implementation level of BM suggests that farmers still have a long way to go and that government officials should handle the issue of biosecurity in pig farming sectors very seriously. With these alarming results, it is not surprising that ASF has become endemic in pig production areas of the country and is still causing a tremendous harm to the pig industry. Parasitic diseases as well as diarrhoea have also become an important health constraint in pig production probably as a result of the very poor biosecurity level on the farms. The most important measures of concern and to improve are; not feeding kitchen waste to pigs; keeping other livestock species away from pigs; fencing pig barns; keeping newly arrived animals in quarantine, not exchanging boars; not selling sick animals. Other countries with similar husbandry systems might probably face the same flaw in biosecurity practices. Future works will focus on the relationship between biosecurity and production performance, incidence of different diseases and culling rates in the area.

ACK N OWLED G EM ENTS
The authors would like to thank the pig producers of the Menoua Division for their kind cooperation for the success of the study. The local officials of the Ministry of Livestock, Fisheries and Animal Industry are also acknowledged.

CO N FLI C T O F I NTE R E S T
The authors declare that they have no conflict of interest.

E TH I C A L S TATEM ENT
N/A. The study is not reporting results from an experiment on animals or humans.