Respiratory diseases cause significant economic losses to swine producers globally due to reduced productivity, increased production costs and reduced market opportunities (1–3). Economic losses vary considerably between countries due to differences in production systems, study methodologies applied and types of pathogens involved, as the interactions produce varying levels of disease severity.

Economic losses due to swine diseases result from mortalities, reduced weight gains (4), poor reproductive performance, negative effects on feed conversion and increased costs of treatment (5–7). Reduced market value of sick animals represents indirect disease effects, which producers often encounter. Other losses result from carcass condemnations due to lung lesions or reduced carcass quality (8, 9). Previous studies have shown that multiple infections increase the severity and duration of clinical disease (10, 11). To provide a framework for design of interventions at the pig production node of the value chain, it is necessary to quantify possible production losses. This information is useful for producers and extension services to support investment decisions to improve herd profitability.

The disease burden is higher in developing countries due to poor biosecurity practices and poor nutrition, suggesting the extent of possible economic losses may be considerable (12–14). In Uganda, despite existence of opportunities for improving livelihoods (15, 16), the pig sector faces many constraints among which are endemic diseases. Much research focus has been on African swine fever (ASF), a major disease of devastating economic consequences (17, 18). However, other respiratory pathogens of significant economic losses in pig production (PCV2, PRRSv, M. hyo, App and Streptococcus suis) have been reported (19–21).

In Uganda, economic losses associated with pig respiratory diseases are largely unknown, as no such studies exist. This study aimed to quantify economic losses (average daily weight gains, ADGs) due to exposure to selected respiratory pathogens and GI parasites. Furthermore, it sought to determine effect of management level on treatment costs.

Table 2 shows 288 pigs from ninety-four (94) farms that were sampled and monitored. Male household heads constituted 53.4% (n = 53), while females accounted for 43.6% (n = 41).

Results showed significant correlations between live weights and ADGs (r = 0.37, t = 11.8, p < 0.000), live weights and visits (r = 0.50, t = 16.9, p < 0.000), and between live weights and pig age (r = 0.68, t = 27.7, p < 0.000). The mean live weight (Mean ± SD) of pigs in this study was found to be 18 ± 6.9 kg for pigs of 2–4 months, 29.7 ± 11.8 kg for pigs of 5–8 months and 47.4 ± 15.5 kg for pigs of 9–15 months. This suggests pigs were generally underweight for their age, as reflected by poor body condition scores (from data). The value of pigs sold, and mortality observed varied between subcounties (Table 3).

In all, ninety-nine (99) out of 864 pigs raised from 94 farms (11.5%) were reported to have died during the study, whose perceived total value at farm-gate price before death was UGX 13,200,000 (USD 3,646.4). However, total mortalities reported were due to several causes, which were indistinguishable from each other.

This study highlights the role of farm management and the impacts of respiratory infections on pig daily weight gains in Uganda. To support farm decision making, a clear understanding of farm management practices and their relationship with weight gains and production costs is required. Ultimately, the goal of any producer is to minimize production costs, reduce or eliminate economic losses, which translate into better profit margins. These findings compare favorably with other studies elsewhere, which reveal negative effects of respiratory diseases on daily weight gains (38, 39), increased financial expenditures (1, 6), and reduced profit margins (40). A recent study which reported high prevalence of pneumonia lesions in slaughtered pigs highlights the likely contribution of respiratory infections to lung pathology (41).

Our findings align with other studies elsewhere, which reported a drop in mean ADGs with increase in respiratory disease prevalence (39). In this study, pigs within the same farm and observations within pig differed significantly with pathogen exposure status. While pigs exposed to PRRSv and Ascaris spp. gained less (marginally significant) ADGs compared to those unexposed (Table 6), it suggests adverse effects of pathogens on weight gains. As expected, age was a significant predictor of ADGs, but showed a negative association with ADGs. This is perhaps due the observation that pigs tended to gain less weight as they aged, as shown by wide variations in live weights relative to age.

These findings are consistent with other studies which reported a reduction in ADGs by between 8 and 14%, and increased mortality of 19.9% in farms with a high disease challenge (5). A study reported a reduction in ADGs of between 16 and 29% for respiratory and between 8.4 and 19.4% for parasitic infections (42). The mean ADG of pigs reported in this study compares to that in other studies in East Africa in similar settings. In Uganda, a study reported that the ADG of nursery pigs fed on forage-based diet was 160 gr/day (43), while another recent study in Lira district reported 101 gr/day (14). In Western Kenya, (25) reported ADG of 130 gr/pig/day, while in Tanzania, Lipendele and colleagues reported ADG of 136 gr/pig/day (44). However, these ADG values are generally much lower compared to those in other countries, which attain 600 gr/day or higher (5, 39).

The low ADGs of pigs in this study (compared to that in developed economies) could be explained by endemic infections, underfeeding and inferior genetics as reported in recent studies in Uganda (14, 43, 45). The adverse effects of mixed infections on ADGs confirm findings from previous studies which showed mixed infections reduced ADGs, led to more severe and prolonged duration of respiratory disease (10, 46). The effect of infective dose, pathogen type and strains involved, their interactions with environmental stressors and the subsequent response of the pig’s immune system play a significant role in the induction of clinical disease. These interactions lead to subclinical, mild, or severe disease outcome, producing varying effects on weight gains and other productive indices as previously reported (47, 48).

This study revealed that mean treatment costs declined with improvement in management standard score. Farms with a high level of management (MSS 3) spent significantly lower mean treatment costs compared to those with poor (MSS 1) management level (Table 4). This is unsurprising, since farms with poor management were reported to have higher disease incidence in previous studies (39, 49). These findings suggest farmers could make substantial monetary savings from adverse disease impacts if they adopted better management practices, i.e., move from level two to level three MSS. These include improved housing, hygiene and biosecurity measures, better nutrition, and regular deworming of pigs.

In this study, we show that monetary losses per pig associated with PRRSv and Ascaris spp. infections were substantial for smallholder farmers. These estimates are quite conservative and likely represent a fraction of potential total losses encountered as other productivity indices (e.g., abortions, mortalities) were not captured. In this study, partly due to underfeeding, farmers often kept pigs for longer than 200 days (6.5 months), which adds to possible losses from extra feeds needed to raise pigs to market weight. In the US, (5) reported that financial costs under commercial conditions in high disease challenge farms varied between USD 8.5 and 29.8 per marketed pig, while Dee and Joo (50) reported costs due to PRRSv infection between 2005 and 2010 ranged from 10.5 to 12.5 USD per marketed pig. However, these studies were done in intensive, high-efficiency settings, in contrast to smallholder production systems in our study.

Housing type and quality have a direct and indirect effect on pathogen transmission between pigs. Floor types (deep litter, elevated timber platform, cement, and rammed soil/murram) influences pig welfare and hygiene. Farmer attitude and behaviour determines the frequency with which wastes are removed from pens. These management factors directly influence the pathogen load that may accumulate and multiply in pens, particularly if the floor was poorly designed. Accumulation of pathogens in pens due to lack of cleaning may facilitate transfer of infection(s) between pigs. Cargill (35) reported that pigs reared in an all-in-all-out (AIAO) system with cleaning grew by 15% faster than pigs reared with no cleaning. The same study showed that pigs on dry floors gained higher ADGs (5% higher) than pigs on wet floors. A similar finding was reported in a study by Pastorelli et al., which found that pigs raised in poor sanitary conditions gained 11% significantly lower ADG compared to those under good sanitary conditions (42). Evidence of the role of good hygiene in pig health, overall welfare, and efficiency of the value chain, generating better financial returns to the producer is documented (1). Our study provides a framework to measure the quality of pig housing and management level in smallholder settings, both of which influence health, welfare and productivity. It can be adapted to a given context to include other management practices (e.g., beddings), which most farmers did not provide.

The fact that only a third of farmers in this study had access to extension services justifies a necessity to strengthen these services to provide technical advice on herd health and biosecurity. While prophylactic use of antibiotics against bacterial pathogens is known to reduce the burden of opportunistic infections (51, 52), their judicious use should be promoted to guard against possible misuse, which could escalate the problem of antimicrobial resistance (AMR). The practice of isolating sick pigs helps minimize the risk of further pathogen spread between pigs. These herd preventive practices are critical as they influence the level of contamination, risk and extent of pathogen spread between pigs. A study showed routine management factors (e.g., routine removal of manure) had a greater impact on Ascaris suum infection than regular deworming (53). This underscores the importance of “good” management in reducing adverse effects of disease. Management is a combination of a farmer’s socio-economic attitude, behaviour and practices, which reflects their skills and knowledge of possible disease impacts on herd performance. However, farmers’ adoption of biosecurity measures for disease control should be supported by incentives that increase their financial returns, as previously highlighted (54). The observation that farmers’ education level directly correlated with management level underscores the importance of education in reducing adverse disease impacts. It is therefore important to consider the social context when designing health management interventions.

This study was limited to estimation of direct costs due to respiratory and worm infections. However, it was impossible to estimate other indirect economic costs (specific to respiratory diseases) attributable to deaths and salvage prices of sick pigs due to lack of reliable farm data. That these indirect costs were not captured suggests economic losses encountered by farmers in this study may have been underestimated. Besides, because not all farmers treated their pigs despite showing clinical disease due to lack of cash or no access to extension worker, it’s probable that errors in estimates of treatment costs may have been introduced. Because ELISA tests used reflect prior exposure of pigs to respiratory pathogens, knowledge gaps remain on the duration of infection(s), and the time lapse to induce clinical disease during individual or mixed infections, both of which ultimately influence growth rates.

To the best of our knowledge, this is the first study in Uganda to document evidence of adverse effects of respiratory and helminth infections on weight gains in pigs. We showed that a grower pig in a given farm exposed to PRRSv and Ascaris spp. infection had significantly lower daily weight gains (ADG) by 17.10 gr/day and 16.80 grams/day respectively, compared to a similar unexposed pig of the same age. Mean treatment costs per pig declined with improvement in management level scores (MLS), from USD 1.13 in MLS 1 (poor management) farms to USD 0.95 per pig for MLS 3 (better management) farms. We show that monetary losses encountered by farmers due to PRRSv and Ascaris spp. infection amounted to USD 6.60 ± 2.7 and 6.50 ± 3.2 (Mean ± SEM) per pig, respectively during 200 days of fattening.

This study highlights the role good management plays in mitigating against adverse effects of respiratory infections in pigs. To reduce possible economic losses from disease, it is important for farmers to adopt good herd management practices using welfare concept, which include proper housing, nutrition, and biosecurity. These prerequisites are necessary for optimal growth and health of pigs, which enhances farm profitability. Further studies are required to establish the full extent of other possible indirect losses (e.g., reproductive disorders) considering pathogen interactions and variations in disease severity.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.

The animal study was reviewed and approved by ILRI’s Institutional Research Ethics Committee (IREC no. IREC2018-23) ILRI’s Institutional Animal Care and Use Committee (IACUC2018-22) Institutional Review Board (IRB no. SBLS/REC/18/008), College of Veterinary Medicine, Animal Resources and Biosecurity (CoVAB), Makerere University. Written informed consent was obtained from the owners for the participation of their animals in this study.

MD, PO, JE, FM, BW, and EO designed the study. PO performed data collection. PO, MD, and EO analyzed data. PO and EO prepared draft manuscript. All authors contributed to the article and approved the submitted version.

We acknowledge funding support from the CGIAR Research Programme on Livestock and the OneCGIAR initiative “Sustainable Animal Productivity for Livelihoods, Nutrition and Gender (SAPLING) inclusion” (https://www.cgiar.org/initiative/17-sustainable-animal-productivity-for-livelihoods-nutrition-and-gender-inclusion-sapling/) and all donors and organizations which globally support its work through their contributions to the CGIAR Trust Fund https://www.cgiar.org/funders/trust-fund/. The support received from the German Academic Exchange (DAAD) Service (Personal ref. no 91672538) for Peter Oba’s PhD programme at Makerere University is acknowledged.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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