Disease reporting, epidemio-surveillance, value chain and implications for amplification of inter-farm, inter-district and national spread of ASF in Tanzania
Immediate incidences of diseases are reported by farmers to the field extension officer (EO), agricultural officer (AO) or livestock field officer (LFO), or where these are not available, to the village or ward executive officers (VEO or WEO), who in turn report to the responsible district veterinary officer (DVO). The shortfalls in number of staff needed at district levels sometimes have implications for the effectiveness of delivery of animal health services including reporting and timely responses (Table 1). Sometimes, the delayed reporting by the farmers increased the intensities and impacts of the outbreaks and this influences the morbidity and mortality rates. The plausible explanations for this delay include inadequate staffing at wards level, poor knowledge regarding the disease by field staff, resorting to self-help by farmers, as well as poor knowledge of biosecurity, the hazard, and its transmission pathways among the farmers. For instance, in some districts under investigation, farmers indicated to have administered pen-strep, tylosin or other antibiotics, and only reported later to the official authorities when no positive response was obtained. Oftentimes, on receipt of reports, the DVOs conduct clinico-pathologic examination, report to the Directorate of Veterinary Services, and liaise with the relevant zonal veterinary centres and Zonal veterinary laboratory under the TVLA for sample collection. These facilities have competent manpower and medium-level resources for sampling but may not be effective for confirmatory diagnosis of ASF, often due to lack of reagents and consumables. With the introduction of Event Mobile Application (EMA-i) in over 60% of LGAs in Tanzania, the quantity and quality of animal disease reports have improved as the DVOs can interconnect and undertake near real-time reporting electronically. In the current evaluation, approximately 66.7% of the districts under investigation have submitted recent ASF reports through the EMA-i applications within weeks of outbreaks.
With regard to awareness, the field officers, pig farmers, butchers/traders and many of the stakeholders could clearly describe ASF symptoms and clinical signs, a useful attribute for epidemio-surveillance. However, the knowledge of infection and transmission varied widely among work groups, best among the veterinarians and the animal health/livestock field officers, medium to high among the extension and agricultural officers, medium among the farmers, traders and butchers, but medium to poor among the ward and village executive officers [12, 13].
Inter-district complementarities in movement restrictions during outbreaks are often lacking among contiguous districts and regions. For example, when quarantine was imposed in an infected district during the period of intense outbreaks, it was initially in the affected wards only, however, because the compliance level was poor, such quarantines were often extended to cover the whole district, yet inter-district movement sometimes occurs from non-infected districts into infected districts and vice versa. Typically, the non-infected districts have no quarantine imposition and no border vigilance, primarily because of the overstretched workforce. Similarly, intra-district, multi-district distribution and international cross-border movements, particularly to the large livestock markets and slaughter slabs are depicted by the DVOs in charge in each district (Supplementary Figs. 4–6).
The smallholder farmers sourced their pigs from within their immediate wards, districts, regions or from distant districts. Some purchase directly from nearby livestock markets or from the traders who purchase pigs for slaughters. These farmers, particularly those who live in border towns and villages sometimes source pigs from Burundi, Rwanda, Uganda and Kenya but also from Zambia, Malawi and Mozambique.
There exists an official movement and import permit system, however, farmers and traders sometimes evade the official systems by moving the pigs and pig products across intra-national and international borders in the night and at odd hours. Due to the extensive stretch of Tanzania’s borders, it is difficult to effectively police, or carry out effective vigilance and surveillance duties due to limitations in available manpower in the government system. In addition, the stakeholders most often do not seek professional guidance ahead of purchase, and the traders and butchers sometimes intentionally or inadvertently buy infected pigs, which are sold much cheaper (between 20 and 50% of the normal trade values). Similar observation has been reported from earlier works from Vietnam [14]. Furthermore, there is a tendency for traders/butchers to source pigs for slaughter from Burundi and Rwanda, and neither these traders nor farmers do isolate the new arrivals.
Identified drivers and risk factors
Upstream water source
A good number of the smallholder farmers depend on water from streams as drinking source for their pigs, and for washing the pig houses/pens and equipment, and the run off goes back to the stream. This consequently regularly contaminates the stream, especially if any of the farms along the stream are infected. This phenomenon was clearly demonstrated in Sengerema as well as Geita where following ASF infections in the upstream farms, the ASF infection spread down streams and affected other pig farms. Similar observation was earlier noticed in the Southern Highlands through contaminations from slaughter slabs upstream, which later flow downstream towards Lake Nyanza [4]. In some areas, such as Mabatini in Mwanza, and in the city centres such as Dodoma, smallholder farmers have abandoned the use of water from the streams and rather utilize piped or well water, following infections from the previous outbreaks of 2017; anecdotal evidence pointed to causation between the contaminated waters and ASF infection of pig farms. The possibility of carcasses being thrown into streams, thus creating heavy contamination and a source of infection is not impossible. A high oral dose is needed to produce infections in pigs, which is plausible for streams with low volumes of water, which are receiving a lot of run-off from farms and slaughter slabs. With large rivers, the source of infection is more likely to be carcasses that wash up on the banks and are feasted upon by scavenging pigs. In our evaluation, most commercial farmers constructed and use boreholes and treated water for their farms.
Slaughter slabs/areas
There are no appropriate handling and slaughter facilities for pig farmers and traders to take their animals for slaughter. Neither has any standard design been constructed as a proof of concept for the farmers and other stakeholders. In addition, because many communities have a significant number of Muslim populations, the construction of pig slaughter facilities cannot be combined with that of other livestock species, and such facilities must be constructed in societally acceptable locations. Given the foregoing constraints, pigs are slaughtered mostly in poor, unhygienic or decrepit slaughter slabs, often located within the pig farms, or in some distant location. Selected numbers of stakeholders have made personal efforts to improve the standard of the slaughter slabs but these facilities still lack the necessary equipment and tools expected for a standard abattoir facility. Pigs slaughtered in these slabs come from various sources within the different districts, or from other districts, and as far as from outside the country. In case of illegally imported animals, efforts are made by farmers and traders to mix them with the owned stock within the farms as decoys to evade confiscation and destruction of untested but imported pigs. Most of these slaughter slabs lack disposal pits and are not fenced hence easily accessed by dogs and free-roaming pigs.
Selected farm management practices
a) Sharing of boars
Most farmers tend to hire/borrow boars from fellow farmers during breeding. A farmer in one of the investigated districts hypothesized that her sows were probably infected from the neighboring farm. Following the dispatch of her sow to the other farm for mating, and the observation of pig deaths in the other farm, she retrieved her sow and return same to the farm. In total, she lost 14 sows, 7 growers and 44 piglets and had only six survivors left. Similarly, Muleba alone experienced 101 incidences of ASF outbreaks. Following traceback, it was concluded that the outbreaks in Muleba started from a ward where a farmer brought in a boar from another district for the purpose of genetic diversity and improving his productivity (mating). The imported boar became morbid and was slaughtered and shared in the community. Thereafter, disseminated outbreaks of ASF were reported in many wards in Muleba. At least 24 of the interviewed persons identified the practice of sharing of boar as a high risk activity that contributes significantly to spreading ASF in pig farms.
b) Unrestricted inflow and outflow of people/animals with lack of biosecurity measures
Many pig farms lack adequate fencing or are unfenced making them easily accessible to visitors, scavenging animals (dogs, cats and rodents) or stray pigs. In addition, pig traders and farm gate buyers move from one piggery to another and from pen to pen when selecting potential pigs to purchase for redistribution or for slaughter. Sometimes, these farm gate buyers, traders and butchers, who operate without observing biosecurity protocol, inadvertently serve as sources of infection through intra-district pig mobility, carriage of fomites in their shoes, clothes, knives or other tools/vehicles, on in the process of multi-sourcing of pigs from farm to farm. In addition, the inter-district and transboundary movements of people and pigs end up in farms with high possibility of inadvertent infection of farm with ASF virus. Furthermore, hardly any footbath, change of clothing and gumboots usage was observed (Fig. 4). Because most of the buildings for smallholder farms were constructed with wooden materials or scrap metal with concrete or earthen floor, it makes thorough cleaning and disinfection very difficult. Such conditions expose the pigs to risk of infection with viral, bacterial, fungal and parasitic diseases.
c) Waste disposal
None of the farms visited had a standard waste disposal pit for infected carcass and secured farm manure management. In addition, no slurry pit was sighted for the collection of solid waste mixed with liquid and these just flow freely in the gutters outside the pigpen. It was observed that many of the farms throw the manure over the pen or over the fence with predisposition to contaminate the environment. Such practices also attract more scavengers and rodents into the farm premises thereby increasing the risk of introduction of animal diseases.
d) Humans as virus spreaders (Animal attendants, farm managers, farm owners, para-veterinarian and veterinarians)
In most smallholder farms, the farm attendants, typically one per farm, are hardly trained in the good farm management practices that should provide efficient pig management and welfare to the pigs, but they are expected to gather experience in the course of farm management. These attendants serve all the pig pens, and in most cases do not observe the systematic movement protocol of going from the young to older animals, or hardly practice any biosecurity principles. Hence, the risk of random introduction of animal diseases and transmitting them within the farm is high. In addition, farm managers and owners often used their positions to invite visitors to visit their farms. These visitors are in most cases persons with interests in animal farming, and have high potentials for inter-farm introduction of diseases. Farm-gate buyers, traders, butchers are also invited by farm managers to select pigs as mentioned above. During epizootics and animal health crises like the widespread outbreaks of ASF, para-veterinarians and veterinarians are often invited to provide animal health services. Due to the shortage of these categories of workers in the peri-urban and rural areas, as well as shortfall of resources, these individuals often have to move from farm to farm rationing biosecurity-related materials like instruments and disinfectant, and may inadvertently transmit infection to new premises. Human activities (anthropogenic factors) have been identified as critical to the long-distance jumps of ASF introduction to new premises [4, 12, 14, 15]. For instance, the transport of contaminated meat or meat products, which may end up as waste or kitchen leftovers for feeding pigs, the purchase and introduction of untested boars, the transboundary informal purchase of new pigs and subsequent mixing with the local stock in order to evade confiscation all pose extreme risk of introduction of the hazard, the ASF virus.
e) Farm-level and community-level biosecurity
Based on our evaluation, only 5.7% of the smallholder pig farms practiced approximately 68% (17/25) of all identified biosecurity items, and not a single farm implemented all the 25 item measures in their pig farm. It should be understood that a breach in biosecurity protocol, particularly at a period when the farm is at a high risk of infection, or in an overwhelming endemic condition, can eliminate all the gains and hard work put into biosecurity implementation before the breach.
Trans-national, cross- border and country-level risks of ASF entry, re-introduction and exposure
Pig movements across the United Republic of Tanzania is random and diffuse, and long distance animal movements are observed along the primary and secondary roads [4]. Within-village movements are done by trekking the pigs on foot or on bicycles. However, the other forms of movements rely on motorcycles, tricycles, and motor vehicles (small vehicles and trucks). In this work, we clearly identified five patterns of movements for pig and pig products including the following:
- Inter-ward/inter-village movements within a district.
- Inter-district and trans-district movements across contiguous or distant districts, and from region to region.
- Trans-boundary movements across national borders, particularly with Burundi and Rwanda in the north, and from Zambia, Malawi and Mozambique to the South, but also from Uganda and Kenya.
- Farm → open market → abattoir/slaughter slab → Farm.
- Farm → Farm.
The value chain, marketing and trade systems closely drive these pig and pig-products movements with many forms of sale practices: formal, informal, farm-gate and random types. These movement patterns have huge implications for disease introduction and transmission. Traders, marketers and farm-gate buyers move among farms without observing any biosecurity protocol with consequent biosecurity breaches. They often move with their potentially contaminated tools, knives, shoes, clothes, vehicles, and restraining materials. In a few instances, formal movements may prevail, wherein pigs and their products are subjected to physical clinical examination and or laboratory testing, but the largely informal movements utilized unscrupulous means to evade veterinary authority detection through night and unofficial periodic movement, through unpatrolled border areas and through smuggled pig products from across national and international borders. A key informant from Burundi (through a phone call across the border) indicated as follows:
‘ASF will never stop circulating in the sub-region unless a regional approach at tackling the disease is implemented’.
He confirmed that cheaper pigs, which are a regular occurrence during outbreaks, are traded across borders freely and there are not enough officials to manage intra-national and cross-border animal health, surveillance, border vigilance and disease control along the extensive borders. Hence, the cross- border and country-level risks of ASF entry, re-introduction and or exposure from neighbouring countries remain very high.
Almost all of the farm management practices listed are anthropogenic factors, since these are human-driven factors. Similar factors were recently found in Uganda in the work of Aliro et al. [13]. In other instance, humans act directly as vectors of the virus, hence an intensified risk communication and community engagement, as well as behavioural change to target the identified anthropogenic factors should reduce the burden of ASF [13]. While the ongoing transmission in the 1) wild boar populations, 2) the wild boar – environment cycle and 3) the tick to pig transmission cycle, which cannot be linked to any specific human practice or activity are examples of non-anthropogenic transmission; the large jumps of ASF from distant infected wild boar populations to uninfected wild boars hundreds or thousands of km away, and the situation observed in the current outbreaks in Tanzania, are definitely anthropogenic [16].
Consequences of the outbreak and its socio-economic importance to the pig industry, including identification
Among the individual stakeholders interviewed, the majority (86%) had experienced ASF in their herds between June 2020 and February 2021, most of the respondents have lost between ≤ 95% and 100% of their stock due to ASF. The salvaged pigs were sold rapidly or slaughtered to recover approximately 25–30% of the normal market values; sometimes the young ones (piglets and weaners) were recovered and kept as replacement stock. There are deficiencies in the knowledge of transmission, mitigation measures and application of biosecurity in order to reduce the risk of infection. The farmers have lost businesses including 1) the loss of supply of pork to a niche market in the mining sector, 2) loss of major sources of income and livelihoods, 3) loss of food security and ability to support the family by providing funds for school/college fees and hospital bills and constructions in the homes. Narrating his experience, a farmer stated as below,
‘The children are back from school/college for the Easter break and I am disturbed and heartbroken; my pens are empty and I have lost everything. In total, I have lost as much as TSh 80 million (≈ US$ 34,500) based on the scale of my operations’.
A mission farm, which is supporting a popular community health program through the money accrued from the sales of live pigs and pig products, and which supplied multiplier herds to smallholder farmers and reaching ≈ 1,000 farm families in remote settings of Ngara, lost approximately 98% of the herd. Another farmer lost over 400 pigs, and in another instance, a farmer withdrew two children from educational facilities (one in the university and another in the secondary school). Stakeholders, particularly farmers were sentimental and expressed negative emotions against the authorities, whom they perceived to have left the stakeholders to their woes. The government will need to consider a reorganization of the pig farming system and associated value chain in order to mitigate risks associated with ASF.
Information and knowledge gaps
Due to the shortage of animal health staff, agriculture officers (AO), extension officers (EO), Ward Executive Officers (WEO) and Village Executive Officers (VEO) sometimes double in their roles of administration and issuing animal movement permits and attending to other animal health matters. These roles are often undertaken without relevant animal health training, hence the gaps in awareness and knowledge of ASF were obvious. Farmers indicated that such officers sometimes promote and advise on the treatment of high fever using penicillin-streptomycin, sulphur-based antimicrobials, tylosin and multivitamins. In addition, the border control staff and officers certify animals crossing the official borders while collecting revenues for the government. The FGD and KII revealed that many of such officers were untrained in the matters of animal health despite being tasked with the responsibility of issuing movement permits. A number of these officials interviewed could not identify enough clinical signs, symptoms, and pathological details associated with ASF, and could not list the risk factors or facilitators of transmission. There is a need to develop a training package customized for the need of cross-border animal health service providers.
In addition, the knowledgeable farmers only gained sufficient knowledge based on their own farm experiences of pig farm infections. Many are, however, unaware that neither treatment nor vaccine are available, and of the specific risk factors and the benefits of biosecurity in mitigating ASF risk. Traders confirmed that they prefer to continue to buy cheaply-priced pigs, even though they acknowledge that it may contribute to spreading the disease, which may damage the pig industry. Their motivation was enhanced profit margin. The butchers similarly slaughtered infected pigs, purchased at a take away price from desperate farmers during ongoing outbreaks of ASF thereby contributing to the spread of disease.
Based on the evaluation conducted, it is recommended that:
- The relevant authorities should consider the designing and building of prototype dedicated and biosecure pig slaughter slabs that reduce environmental contamination. The siting of such slaughter slabs should be decided through consultative process taking note of socio cultural as well as religious considerations of the community and guidance from the environmental authorities.
- Enforceable by-laws should be in place to forbid homestead or farm-directed movement of adult pigs meant for the abattoirs or slaughter slabs.
- The knowledgeable animal health officers, especially the DVOs and the LFOs should develop scheduled timetables for training of farmers, traders and other stakeholders on biosecurity, good farming practices, movement and marketing networks that minimise the risk of infection and transmission of ASF. Resource allocation to support such training should be made available from the revenues and fees generated from animal resources within the districts or region, with support from the national government and other stakeholders.
- The need for training and retraining of regional, district and border officials involved in the animal health services cannot be overemphasised. The training should focus particularly on emergency preparedness and response, as well as disease reporting. This should prevent delay in reporting animal health emergencies at district or regional level and facilitate coordination with the central veterinary system.
- The issue of inadequate staffing, particularly in the more rural districts should be prioritised and addressed. This has earlier been identified in the findings of the 2016 Joint External Evaluation (JEE) in Tanzania [17]. It should include the conduct of a comprehensive inventory of the animal health personnel in the country and determine the personnel gaps at the national, regional and district levels.
- The delivery of effective animal health services at district level needs adequate mobilization to respond promptly. The lack of mobility (motorcycles, vehicles and bicycles), identified by the district level officers must be addressed in a phased approach.
- A comprehensive animal resources evaluation at district, regional and national levels in Tanzania must be undertaken to determine the comprehensive animal dataset, the total economic values, and the inapparent opportunities, in order for the government to generate revenues internally, some of which can be utilised to provide for the need of the animal health services at subnational level.
The authorities may consider the setting up of pig demonstration and training farms, and multiplication centres (breeding centres) in strategic districts/regions in the country. Such centres should be used to provide training on the pig value chain, integrated farm-level biosecurity, good husbandry practices and Good Management Practices (GMP) [18]. It should be understood however, that training on biosecurity practices may positively affect gain in knowledge, but it may have little or no effect on farmers’ attitudes and practices [12]. In this study, despite the intensive training on biosecurity, farmers would still allow veterinarians who may not have practiced biosecurity measures into their farms, even during outbreaks, would not restrict visitors from farm visits, not likely to deny traders access to the farms, and the less educated farms are still likely to sell pigs during ASF outbreaks [12]. In the long term, the progressive reorganization of the livestock industry to align with the Tanzania Livestock Modernization Initiative and Tanzania Livestock Master Plan is imperative [19, 20].