Salmonellosis is a foodborne, zoonotic disease that is generally self-limiting (1). Worldwide, non-typhoidal Salmonella is ascribed to ~93.8 million human cases of acute gastroenteritis and 155,000 deaths annually (2, 3). In the United States, the cost of human salmonellosis is estimated to be around $2.9 billion per year (4). Denmark has carried out intensive programs to control Salmonella in the animal production chain since 1990s which has resulted in a low human incidence, i.e., 11.8 Salmonella cases per 100,000 habitants were registered in 2021 (5). In Colombia, human salmonellosis is underreported and considered an endemic disease with sporadic outbreaks. According to the Colombian National Institute of Health, 7,219 Salmonella cases were reported between 2000 and 2013 with S. Typhimurium (33.7%) being the most common serotype detected followed by S. Enteritidis (28.6%), S. Dublin (3.3%) and S. Derby (2.1%) (6, 7).

The distribution of the different Salmonella serotypes varies according to food source and geographical area (6). Infection with S. Enteritidis is often associated with consumption of eggs and poultry meat, whereas the other globally important serotype S. Typhimurium is related mainly to consumption of pork (6, 8). In 2020, 13.0% of the human cases of salmonellosis reported in the European Union (EU) were due to consumption of contaminated pork. In 2015, the Salmonella prevalence was 28.2% on pork carcasses at abattoirs in Colombia with S. Typhimurium, S. Agama and S. Agona being the main serotypes found (9). Comprehensive control of Salmonella throughout the food value chain can decrease the incidence of human salmonellosis (6, 10, 11).

Subclinical salmonellosis in pigs constitutes a source of Salmonella. After weaning, the pigs excrete Salmonella and infect other pigs in the pen. Excretion of Salmonella may increase at times of stress such as during transport to the abattoir and in the lairage area, resulting in high risks for contamination of the carcasses during slaughter unless adequate measures are taken (11–14). In Colombia, the between-farm Salmonella seroprevalence was 42.9% (n = 350) in 2020 in the seven main pig producing provinces (8, 15–17). Half of the Salmonella strains tested (n = 41) showed concurring resistance to penicillin, cefuroxime, tetracycline and trimethoprim/sulfamethoxazole. These types of antimicrobial resistances (AMR) in Salmonella may be ascribed to the routine use of antimicrobials supplemented to pig feed used in Colombia (3, 18) and is of concern for effective treatment of human salmonellosis (16). Moreover, reduced AMR levels are not just of benefit to human health but will also ensure that pigs suffering from diseases caused by bacterial pathogens can be treated.

Although the use of antimicrobial growth promoters is banned in some parts of the world including the EU, they are still allowed and commonly used in Colombia for disease control and to improve growth in livestock. However, use of such growth promoters leads to development of AMR. For this reason, alternatives have been sought to replace the antimicrobial growth promoters including preventive measures focusing on improving the health of pigs while maintaining productivity (19). Without maintenance of productivity, the farmers cannot be expected to change habits and replace antimicrobial growth promoters with alternatives.

Organic acids (OA) can be used to control Salmonella and promote growth in pigs. When administrated in water and/or feed, the OA cause a decreased pH to 3.8–4.2 at which the growth of many gastro-intestinal bacteria except lactobacilli is altered or directly inhibited. OA also modulate the intestinal fermentation patterns of feed creating a better gastro-intestinal environment with improved utilization of feed and growth (20–23). These positive effects of OA on feed conversion rate and growth performance are also described in poultry including increased egg production. The ability to decrease Salmonella colonization depends on the type of OA used (24). Although the antibacterial effect of OA is well known in theory, published results of efficacy in on-farm studies vary, with some reporting beneficial effects (25–28) while others fail to demonstrate any effect (29–31). Thus, further evidence is needed to establish at which concentrations and combinations OA could be used to control Salmonella spp. in pigs and to elucidate their effect on productivity (21, 32).

The purpose of this pilot study was to evaluate the effect of OA on the productivity and the Salmonella seroprevalence in pigs from weaning to slaughter. We undertook a clinical trial, comparing the effect of provision of OA with antimicrobial growth promoters in a pig farm in Antioquia, Colombia. The hypothesis was that OA supplements to water and feed were equally effective as the growth promoters. This would open up for a possible replacement of antimicrobial growth promoters with OA in line with the principles of prudent use of antimicrobials.

The baseline results showed a high Salmonella seroprevalence of 59.0%, which did not concord with the low proportion of pigs excreting the bacteria as shown by the culture-based detection method (1.0%) (36). To investigate this further, several methods and growth media were used to increase the sensitivity (37). However, these efforts were not successful in increasing the number of Salmonella-positive samples. This may be because of the known low sensitivity of culturing Salmonella spp. in fecal samples from pigs (8, 32, 38–40). Moreover, the regular administration of growth promoters to piglets on the farm could have reduced the Salmonella spp. excretion (40). Therefore, it was decided to measure only Salmonella seroprevalence during the study as an indication of the Salmonella prevalence.

There was a significantly lower Salmonella seroprevalence in the group of pigs provided organic acids (OA) (18.3%) compared with the control group (47.7%) at T2 (11 weeks). Contrary, at T1 (6 weeks) and T3 (15 weeks), there was no statistical difference in seroprevalence. OA favor the growth of lactobacilli, which contributes to a low pH, limit bacterial growth in the intestines and stimulates the immune system in a non-specific way; all of which decrease the probability of Salmonella colonization (3, 22, 41, 42). For this reason, the use of OA may have delayed the excretion and spread of Salmonella during the post-weaning period. However, as the observation period progressed, the majority of the pigs were eventually exposed to Salmonella spp. at some point. These findings are in agreement with the literature (3, 41, 43). Pigs develop partial immunity to Salmonella when the spread and exposure to the pathogen is reduced. Such partial immunity development is the core of a Salmonella reduction strategy as pigs at the time of slaughter will have a lower probability excreting Salmonella (36, 44). It is well-known that Salmonella cannot be eradicated without culling the farm (36, 44). There is a positive association between herd serology and the prevalence of Salmonella on the carcass as a low seroprevalence is associated with less prevalence on the carcass, less excretion and less overall contamination with Salmonella at the abattoir (45).

In Colombia, it is customary practice to use growth promoters like tylosin and zinc bacitracin. However, this is not in line with the principles of prudent use as it will lead to development of AMR and growth promoters are now banned in many countries (46, 47). Growth promoters are used as they are believed to support increased growth and reduce the severity of post-weaning diarrhea. In our study, pigs provided OA had a better cumulative DWG and weight productively than pigs administered growth promoters. The OA are feed additives that are metabolized by the animal, allowing their use without the risk of residues accumulating in the meat. The use of OA is already increasing as a response to strengthened regulations and consumer concerns on the use of antimicrobials in many countries (48). The mode of action of OA includes modulating stimulus that benefits the development of the mucosa, the length of microvilli, intestinal cell growth and therefore the absorptive capacity of the intestine is improved (3, 19).

The weight measured at time points W4 (17 weeks) and W5 (23 weeks) and the cumulative DWG during the study showed a better growth performance of pigs administered OA compared with the control group, which supports findings in other studies (49–56). van der Heijden et al. concluded that Selko pH^® added to water at a concentration of 0.2% significantly reduced the seroprevalence of Salmonella and improved the productive performance of pigs (57). Likewise, formic, citric and benzoic acids can lead to improved growth when added to feed provided to weaned and growing pigs (23). A better DWG translates into less time spent by the pig in the herd, as well as a more efficient use of feed nutrients that represent one of the main costs of production (58).

Although there was a statistically significant difference (P = 0.025) at FCR3 and FCR4 (P = 0.009), favoring the intervention group and control group respectively, there was no significant difference in the cumulative FCR between the two groups. This may because the staff in charge of supplying the feed to the pigs did not fully take into account the pigs that died during the trial when calculating the feed to be administered. Therefore, the number of pigs used to calculate the feed provided was likely a little too high which may explain that no difference was found in the cumulative FCR between the groups (59).

The cleaning of the water pipes on the farm with citric acid before and during the study improved the water quality, which likely also resulted in healthier pigs (60, 61). Water is a potential source of various pig pathogens causing diseases that affect weight gain and feed conversion (62). For this reason, it is recommended to clean the water pipes regularly. The combination of cleaning of the pipes and the use of OA may be responsible for the higher overall productivity and apparently slower spread of Salmonella in the group administered OA. At the abattoir, such pigs are expected to have a lower probability of excreting Salmonella (44).

Salmonella antibodies can remain at measurable levels up to 3 months in the pig, which means that positives animals can be found even when they no longer are infected or excreting Salmonella spp. (36). Pigs included in the clinical trial may have experienced exposure to the pathogen without excreting Salmonella during sampling. Additionally, presence of antibodies in the individual animal may not be directly related to a carrier stage or probability of shedding Salmonella spp. (63). Hence, it is a limitation of our study that no other diagnostic tests were applied that could confirm whether pigs were excreting Salmonella (13). Post-harvest sampling of lymph nodes and ileocecal contents of the pigs may have increased the likelihood of detecting Salmonella if present, and thereby allowing a better assessment of how OA impacted the Salmonella levels in the pigs (37).

Selacid^® was supplied at different concentrations during the study. It is known that different concentrations of OA can affect the Salmonella seroprevalence in pigs as shown by Calveyra et al. who concluded that at a concentration of 0.1%, OA had no significant effect on the Salmonella level whereas it did have a significant effect on improving daily weight gain in the pigs (64).

The dosage of Selko pH^® we administered to drinking water (0.8 ml/L) was slightly lower than the dosage recommended by the technical data sheet (1–2 ml/L) from the manufacturer (65). The total estimated cost of the growth promoters added to the administered feed was 32 US$ as compared to 57 US$ for OA added to water and feed. The relative low dosage of OA may have had a reduced effect on Salmonella in the intervention group (25, 30, 66). On the other hand, the additional supplement of OA in the feed probably compensated for the lower concentration of Selko pH^® used in the water. The types and concentrations of different OA products—as well as their costs—should be further investigated for their effect on Salmonella and overall productivity as the effect of the acids varies significantly depending on the components present in the feed (23, 59, 63). Moreover, attention should be given to palatability of the OA to ensure that the pigs do not consume less water or feed. Contrary to traditional organic acids, Selko pH^® has the advantage that it is safe to use as it can be given to pigs in relative high concentrations without risking that the pigs stop drinking because of palatability issues.

For future research, it is recommended to include pig farms with known high prevalence of Salmonella spp., serial sampling and analyses of 25-g of fecal samples to increase the sensitivity.

This pilot study indicates that administration of OA in combination with regular cleaning of water pipes can improve productivity and delay exposure to Salmonella spp. when compared with commonly used antimicrobial growth promoters. A substitution of antimicrobial growth promoters with OA will lower antimicrobial use and resistance, while ensuring productivity. However, the study should be repeated before firmer conclusions can be drawn regarding productivity and the Salmonella spp. reduction potential of OA.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

This study was endorsed by the Institutional Committee Cuidado y Uso de los Animales (CICUA) at the CES University, Medellin, Colombia (Code No. 206/Act No. 38).

AD, LA, and MR-H were responsible for the conception of the study, experimental design, and manuscript writing. MR-H was responsible of collection of samples in the farm, data analysis, and interpretation. NC-C, LR-R, and LV-A were responsible for conception of the study and experimental design. All authors contributed to the article and approved the submitted version.