Next Article in Journal
European Non-Polio Enterovirus Network: Introduction of Hospital-Based Surveillance Network to Understand the True Disease Burden of Non-Polio Enterovirus and Parechovirus Infections in Europe
Previous Article in Journal
Correction: Ou et al. Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas. Microorganisms 2020, 8, 63
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Systematic Review

A Systematic Review on the Effectiveness of Pre-Harvest Meat Safety Interventions in Pig Herds to Control Salmonella and Other Foodborne Pathogens

Epidemiology Research Unit, Department of Veterinary and Animal Science, Northern Faculty, Scotland’s Rural College (SRUC), An Lòchran, 10 Inverness Campus, Inverness IV2 5NA, Scotland, UK
Pig Development Department, Teagasc, Animal and Grassland Research and Innovation Centre, Moorepark, Fermoy, P61 C997 Co. Cork, Ireland
Section of Herd Health and Animal Husbandry, School of Veterinary Medicine, University College Dublin, Belfield, 4 Dublin, Ireland
M3-BIORES-Measure, Model & Manage Bioresponses, KU Leuven, Kasteelpark Arenberg 30, 3001 Leuven, Belgium
Institute of Food Hygiene and Food Safety, Freie Universität Berlin, Working Group Meat Hygiene, Königsweg 67, D-14163 Berlin, Germany
Faculty of Veterinary Medicine, Department of Production Animal Clinical Sciences, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway
Author to whom correspondence should be addressed.
Microorganisms 2021, 9(9), 1825;
Received: 29 July 2021 / Revised: 19 August 2021 / Accepted: 20 August 2021 / Published: 27 August 2021
(This article belongs to the Special Issue Transmission and Ecology of Foodborne Pathogens)


This systematic review aimed to assess the effectiveness of pre-harvest interventions to control the main foodborne pathogens in pork in the European Union. A total of 1180 studies were retrieved from PubMed® and Web of Science for 15 pathogens identified as relevant in EFSA’s scientific opinion on the public health hazards related to pork (2011). The study selection focused on controlled studies where a cause–effect could be attributed to the interventions tested, and their effectiveness could be inferred. Altogether, 52 studies published from 1983 to 2020 regarding Campylobacter spp., Clostridium perfringens, Methicillin-resistant Staphylococcus aureus, Mycobacterium avium, and Salmonella spp. were retained and analysed. Research was mostly focused on Salmonella (n = 43 studies). In-feed and/or water treatments, and vaccination were the most tested interventions and were, overall, successful. However, the previously agreed criteria for this systematic review excluded other effective interventions to control Salmonella and other pathogens, like Yersinia enterocolitica, which is one of the most relevant biological hazards in pork. Examples of such successful interventions are the Specific Pathogen Free herd principle, stamping out and repopulating with disease-free animals. Research on other pathogens (i.e., Hepatitis E, Trichinella spiralis and Toxoplasma gondii) was scarce, with publications focusing on epidemiology, risk factors and/or observational studies. Overall, high herd health coupled with good management and biosecurity were effective to control or prevent most foodborne pathogens in pork at the pre-harvest level.

1. Introduction

In Europe, the current most important foodborne hazards in pork include microbiological agents (for example, Salmonella) [1,2]. The new risk-based meat inspection legislation was laid out in agreement with these hazards and proposes a risk-informed visual-only inspection where the focus is on the prevention and control of meat-borne hazards before slaughter, such as on-farm or at transport [3]. This integration of measures along the food chain requires cooperation between the different stakeholders and has the potential to consistently reduce the risks associated with meat-borne hazards.
In pig production, key concepts for interventions at the herd level are the control of the purchase and flow of animals, in particular, at the top of the breeding pyramid, the control of feed, internal and external biosecurity, and the categorisation of herds that are carriers of specific pathogens. Interventions at the herd level may also contribute to a more sustainable and “clean” production, while also solving general problems connected to the environment by avoiding recycling of zoonotic hazards like Salmonella at the farm level [3]. Many of these control measures are described in the literature but their effectiveness to control the different foodborne pathogens related to pork has not been addressed. This work aimed to collate and synthesize evidence on the effectiveness of pre-harvest interventions to control foodborne pathogens in pork.
The foodborne hazards targeted in this systematic review were based on the European Food Safety Authority [EFSA] scientific opinion on the public health hazards to be covered by inspection of pork [1]. This scientific opinion collated a list of relevant biological hazards for which there is evidence (in the literature and/or in data provided by Member States) that they occur or may occur in pigs in Europe and that can be transmitted via food to humans. Fifteen biological hazards were selected. Within these, Salmonella was considered of high relevance in the EU, while Toxoplasma gondii, Trichinella spp. and Yersinia enterocolitica, were considered of medium relevance. The control and prevention measures, especially pre-harvest interventions, indicated for Salmonella spp. and Y. enterocolitica would be beneficial for controlling other microbial hazards [1]. Other hazards such as Campylobacter spp., Clostridium botulinum, Clostridioides difficile, Clostridium perfringens, Hepatitis E virus, Listeria monocytogenes, Mycobacterium spp., Sarcocystis suihominis, Staphylococcus aureus (including Methicillin Resistant Staphylococcus Aureus (MRSA)), Taenia solium cysticercus, and Verotoxinogenic-producing Escherichia coli were considered of low relevance, but likely to be present based on the frequency of detection of hazards in pork carcasses after chilling, and so were equally included in this systematic review.

2. Materials and Methods

This systematic review is part of a set of three reviews on the effectiveness of pre-harvest interventions to control foodborne pathogens in broilers, pigs, and bovine. Such work was framed in the context of the RIBMINS Cost Action (please refer to the Acknowledgements section). Likewise, the methods followed are similar to those described by Pessoa et al. [4] and the work presented here was conducted by the same two review coordinators, and two volunteer researchers. The backbone of the methodology used followed the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement [5] and EFSA’s guidelines for conducting systematic reviews for food and feed safety assessments [6]. PRIMA’s checklist for systematic reviews has been completed and is available as Supplementary Material (S1).
All literature searches were conducted on two online databases (PubMed® and Web of Science) on 8 February 2021. Only peer-reviewed studies written in English and published before 31 December 2020 on the effectiveness of pre-harvest meat safety interventions to control 15 foodborne pathogens (those highlighted by EFSA [1]) in pigs were included. Searches were restricted to title and abstract.
Figure 1 shows the composition of the search strings used in PubMed® and in Web of Science. Keywords and search strings specific to each pathogen are presented in Table 1. The detailed search strings employed in each database are available as Supplementary Material (S2).
EndNote was used to import all search results. All duplicates were removed. The set of inclusion and exclusion criteria to filter titles and abstracts is presented in Table 2. One of these criteria was to only select scientific papers with experimental/controlled study designs. This decision was made to highlight the presumptive causal effect of the interventions tested. One co-author screened all 1180 records using these criteria and selected 87 papers for further analysis. After that, the selected papers were retrieved and two co-authors (in parallel and blinded to each other’s decisions) read the full texts using the same eligibility criteria (Table 2). Exclusion of records had to be agreed by both co-authors. Records upon which agreement was not reached were reviewed by a third co-author, producing a final decision. Table 1 shows the list of records included in all stages of the systematic review process.
The data within the final 52 records included in this work were extracted onto a database (stored in a Microsoft Office Excel® spreadsheet). Studies (i.e., any peer-reviewed original research in which the authors collected, analysed, and reported their own data) were documented and classified based on the pre-harvest intervention. Other information (country of study, year it took place, type of experiment, subject type, number of experimental units, sample type, outcome measured, and estimate of effectiveness) was also retrieved. Some studies assessed the efficacy of multiple interventions. For Salmonella studies, the comparison of each treatment (intervention) with the control was recorded as a trial and, if possible, detailed information was collected for each trial. For each Salmonella-related study, the results of the interventions tested were summarised according to whether there was a reduction of Salmonella shedding, reduction of Salmonella counts or improvement of protective immunity. Whenever the outcome of an intervention was measured through several time-points, data collected at the end of the study (i.e., closer to the slaughter date) were preferred.

3. Results

A total of 1180 unique studies published between 1968 and 2020 were retrieved through the search strings run on PubMed® and Web of Science for the 15 pathogens included in this systematic review. After the review process described, a final list of 52 studies published between 1983 and 2020 were retained. This list is available as Supplementary Material (S3). In the full text analysis and selection, the authors had an agreement rate of 95.4% (83/87). Four studies were reviewed by a third author to decide upon its selection. Due to the decision of the third reviewer, one study out of the four was retained in the systematic review. All authors were blinded to each other’s final decisions. The list of studies excluded during the full-text evaluation (n = 35) is available as Supplementary Material (S4). Only five of the pathogens listed had studies meeting the defined criteria (Table 1).

3.1. Campylobacter

The two studies retained for Campylobacter spp. tested the efficacy of probiotics to reduce the colonisation of this pathogen as competitive exclusion and consequently reduce the risk of carcass contamination during slaughter. Bratz et al. [7] tested the inhibitory activity of the strain E. faecium NCIMB 10,415 against C. coli in vivo. This probiotic was administered as a diet supplementation in sows (three weeks before parturition) and to their progeny from 12 days of age until the end of the trial. Sows and piglets from the control group were not fed any supplements. The authors reported that all piglets were already naturally colonised with C. coli before the challenge trial, which was a unique dosage of 7 × 107 cfu strain C. coli 5981 via an intragastric application. The excretion load of C. coli was monitored for 28 days and the results indicate that the tested probiotic did not significantly affect C. coli excretion levels in pigs. In the other Campylobacter spp.-related study, Hasan et al. [8] tested the effects of diet supplementation of resin acid-enriched composition (RAC) in the last week of gestation on colostrum yield, composition and gut microbiota. Three trials in three different commercial herds were performed. Apart from the colostrum yield and composition improvements, the diet supplementation with RAC seemed to shift the relative abundance of opportunistic and pathogenic agents, such as Campylobacter, potentially reducing the risk of piglet infection.

3.2. Clostridium Perfringens

Five studies assessing the efficacy of vaccinations (n = 4) and probiotics (n = 1) were retained. Of the vaccination studies, two of them tested sow and gilt vaccination strategies to control necrotizing enteritis (C. perfringens type C; [9]) and C. perfringens type A-associated diarrhoea in piglets [10]. Two other studies assessed the efficacy of piglet vaccination to control neonatal diarrhoea caused by Clostridioides difficile [11] and necrotizing enteritis (C. perfringens type C; [12]).
One study assessed the efficacy of competitive exclusion by administering a probiotic to control diarrhoea in piglets [13]. The cocktail tested contained living strains of attenuated C. perfringens type A and non-pathogenic Escherichia coli and it was administered per os to newborn piglets in a commercial farm with a history of neonatal diarrhoea caused by C. perfringens type A.
All studies reported positive outcomes for the interventions tested. Two studies reported a reduction in piglet mortality, which corresponded to a numerical but not statistical reduction in the study by Kelneric et al. [9] and to a statistically significant mortality rate reduction in the study by Unterweger et al. [13]. Hammer et al. [10] documented an increase of neutralizing antitoxins against C. perfringens type A in piglets born from vaccinated dams compared to those born of dams not vaccinated, and Richard et al. [12] reported higher titres against C. perfringens type C in vaccinated piglets when compared to those not vaccinated. Finally, in the study by Oliveira et al. [11], the authors documented a reduction of the isolation of C. perfringens in diarrhoea samples after administering a non-toxigenic strain of C. difficile to one-day-old piglets on a commercial pig farm.

3.3. Methicillin-Resistant Staphylococcus Aureus (MRSA)

Only one study on MRSA met the inclusion criteria. This study reported the results of a randomised control trial to test the efficacy of a thorough cleaning disinfection protocol for sows and the environment (farrowing house and nursery unit) to reduce the prevalence of livestock-associated MRSA in sows and their progeny [14]. Two farrow-to-finish commercial farms with a 3-week batch system were enrolled in the study, and, in each farm, six sow batches were tested (three batches tested and three batches as control, all with approximately 20 sows). Results showed that the tested disinfection protocol reduced temporarily the sow and piglet MRSA status, but it did not equate to a final reduction in MRSA at weaning or in the nursery unit.

3.4. Mycobacterium Avium Complex

Hines et al. [15] tested the efficacy of vaccination for Mycobacterium avium with two different vaccines in preventing infection and disease in experimentally challenged pigs. The study tested a killed “whole cell” M. avium serovar 2 as a vaccine, and a conjugated MIF-A3 subunit vaccine. The results showed that the killed vaccine did not prevent infection but attenuated its severity with regard to gross and macroscopic lesions, when compared to the pigs vaccinated with the subunit vaccine. The latter did not prevent infection and the lesions observed were very similar to pigs vaccinated with a sham vaccine (saline solution).

3.5. Salmonella

In total, 43 studies testing different pre-harvest interventions for the control of Salmonella infections in pigs were found [16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58]. Table 3 compiles a description of the studies retained, with a summary of the trials reported in them and their results. Forty-one studies were designed to investigate on-farm interventions, and four studies tested transport interventions [19,20,29,48].
In total, 86 trials were identified among the 43 Salmonella studies selected. The most tested type of intervention was in-feed and/or water treatments. Out of the 32 trials that tested different acids in-feed or water (i.e., sorbic acid, sodium butyrate, or blends of citric acid, formic acid and essential oils) and other feed-related interventions like fermentation or herbal extracts, including prebiotics, 23 (72%), reported positive results.
Most vaccination trials (88%, 21/24) reported positive results. The most common challenges reported were the lack of cross-protection of some vaccines against other serotypes and the potential interference of vaccination-induced antibodies in the meat juice sampling for Salmonella control purposes at slaughter. The three trials reporting vaccination interventions without positive results were: (1) a trial where an oral vaccine administered to piglets at 3 weeks of age lowered transmission (numerically) but failed to reduce excretion of Salmonella Typhimurium [36]; (2) a trial where the vaccination of sows with a commercial vaccine to control of Salmonella Typhimurium infections failed to decrease the prevalence of Salmonella Typhimurium field strain positive lymph nodes at slaughter in finisher pigs born to those sows [58]; and (3) a trial where a commercial oral vaccine based on Salmonella serovar Choleraesuis variety Kurzendorf was administered between 24 and 72 h after birth and was not effective in reducing the within-herd spread of Salmonella during the finishing phase or the frequency of carcass contamination at slaughter, with Salmonella Typhimurium being isolated from lymph nodes of vaccinated pigs [57].
Eight trials tested the efficacy of administering antimicrobials to control Salmonella infections [16,24,27,39,55]. The only trial with a positive result was reported in a study combining intramuscular administration of ceftiofur with off-site early weaning at 10–15 days of age, where Nietfeld et al. [18] concluded that this intervention prevented Salmonella spp. infection in grow-finish pigs.
Of the seven trials reporting results on the efficacy of cleaning and disinfection interventions, two exclusively tested it on transport [19,29], and only one other trial reported the effect of cleaning and disinfection on-farm alone [50]. Rajkowski et al. [19] tested the effect of washing and sanitizing lorries after each load and it significantly reduced levels of Salmonella detected on lorries. Similarly, Mannion et al. [29], who tested bacterial loads and isolates on lorries carrying pigs from high- and low-risk farms during and after transport, and also after washing, commented on the need for better cleaning of lorries after each transport (or load), especially when transporting pigs from “high-risk herds of Salmonella”. The authors found isolates identical to those on farm on lorries after washing. Finally, Martelli et al. [50] tested the application of a rigorous disinfection protocol of finisher facilities on-farm with the objective of eliminating Salmonella, comparing it to the normal procedures followed by farmers. The authors found that this protocol significantly reduced the prevalence of Salmonella in pigs prior to slaughter. Other studies reporting trials testing cleaning and disinfection have been described before or did not obtain positive results [17,24].
Several trials investigated the efficacy of a combination of different interventions. These included a combination of cleaning and disinfection with off-site early weaning [17]; feed withdrawal and duration of transport [20]; a combination of chlorate treatment and topical disinfection administered to piglets together with early weaning [28]; and a combination of different particle size and acids in feed [32]. All of the cited studies reported positive results in one or more of the interventions tested. Four trials (within three studies) testing combined interventions did not report positive effects [24,27,32].
Nineteen trials tested other types of interventions, either alone or in combination with the intervention types described above. Examples of other interventions tested are off-site early weaning [17,18], washing and disinfecting of lorries [19,29], split marketing [31], different space allowances [27,40], and feed withdrawal and transport times [20,48].

4. Discussion

Over the years, several studies have been published on pre-harvest interventions to control foodborne zoonoses in pork. In this systematic review, we aimed to identify controlled studies that could provide a certain level of confidence regarding the effectiveness of the interventions tested, rather than identifying risk factors for the control of infections by the biological hazards listed. The papers selected for full text analysis were published over an extended timeframe (1983 to 2020). Across these years, Salmonella was one of the biggest concerns, with related publications representing 49% (785/1606) of the initial search returns. This is a direct consequence of its high relevance as a biological hazard of concern in pork meat (EFSA, 2011) and of the vast research undertaken to address this issue. Indeed, Salmonella is currently the second most reported foodborne pathogen in the EU, having been the most reported pathogen for many years, and is commonly associated with the consumption of pork [59]. The fact that few studies were retrieved for other pathogens within the criteria defined highlights the need for further research on the effectiveness of pre-harvest interventions to control these hazards. Another possible explanation is that some of these pathogens may be more cost-efficiently controlled by post-harvest interventions.

4.1. Salmonella

S. Typhimurium is the most common Salmonella in pig herds in most European countries, and this agent is known to be introduced into the herds by healthy carriers among the breeding animals and also by contaminated feed [60]. However, there is an extensive list of additional risk factors connected to biosecurity that should be tackled at the herd level, such as birds, rodents, insects, water, manure, humans entering the piggery and environment, etc. [61]. Unsurprisingly, several types of interventions to control Salmonella were found in the literature. In line with the risk factors identified in the literature for Salmonella infections, the most common pre-harvest interventions identified were in-feed and/or water treatments as well as vaccination. Among the most effective interventions, cleaning and disinfection and vaccination appeared to have high success rates. Nevertheless, across all trials, the results for Salmonella are very encouraging, with 76% (65/86) of the trials assessed reporting positive results. Although there is no scope in this paper to debate the reasons for intervention failure, including vaccination failure, reported in the studies evaluated, other studies have systematically assessed the effect of vaccination as a control strategy against Salmonella infection in pigs [62], the efficacy and quality of evidence for five on-farm interventions for Salmonella reduction in grow-finish swine [63], and the evidence for effectiveness of primary production interventions to control Salmonella in pork [64]. In spite of these positive results and vast literature published, the endemic Salmonella spp. infections in pig herds across the world reflect how challenging it is to control this pathogen.
At national level, Finland, Norway and Sweden have documented that the successful control of Salmonella in cattle, pigs and poultry through pre-harvest interventions is possible. Heat-treatment of feed, and starting with breeding animals free from Salmonella at the top of the breeding pyramid have probably been the most important measures [61]. The food safety authorities have an important role following up positive herds to prevent transmission to other herds, humans and food, by prohibiting the purchase and transportation of animals and foods from infected farms. This highlights that prevention rather than control is a feasible pre-harvest intervention when targeting this hazard in pork.

4.2. Other Pathogens

4.2.1. Campylobacter

Multiple studies have shown that pigs are an important reservoir of C. coli and that it is difficult to control this species at the herd level [65,66,67]. It seems more cost-efficient to control this agent post-harvest. Given the sensitivity of Campylobacter to both freezing and drying, blast chilling has proved to significantly reduce this agent on carcasses’ surface [68]. Even after traditional slow chilling there is a significant decline of this agent [69]. Accordingly, pig carcasses and pork are not regarded as an important source of Campylobacter in a public health context as confirmed by most epidemiological studies [70,71]. According to Roux et al. [72], “The aetiology of human C. coli infections is similar in a number of respects to C. jejuni but there are important differences. There is an increased risk of C. coli infection in the older people, in people who live in rural areas and during the summer months. Public health together with national and international food safety agencies should take these differences into account when considering interventions to reduce the incidence of this gastrointestinal pathogen”.

4.2.2. C. perfringens

All of the C. perfringens-related studies reported outcomes referring to the control of disease in piglets and none reported or discussed the possible effects of the tested intervention to control shedding of this pathogen in the faeces. Thus, in spite of the apparent efficacy of the pre-harvest interventions tested, such as vaccination and competitive exclusion, these were not meant to control the risk of foodborne infections by C. perfringens acquired by pork consumption. This is likely to be related to the low risk this pathogen represents since the “risk of disease seems not to be correlated with occurrence in raw meat but rather to improper hygiene and storage” [1], meaning that this pathogen is mostly controlled by post-harvest interventions.

4.2.3. MRSA

The tested disinfection protocol in one study temporarily reduced the sow and piglet MRSA status, but it did not equate to a final reduction in MRSA at weaning or in the nursery unit.
Other similar trials testing thorough cleaning and disinfection of the facilities or sow washing and disinfection were captured in this review, but the absence of control groups dictated their exclusion.
However, more comprehensive measures have been successful. Norway has established a unique control strategy for MRSA in their pig population, which includes population-wide annual surveillance, in addition to contact tracing upon detection of MRSA in pig farms and farm workers. Restrictions prohibit trade of live pigs carrying MRSA, other than directly to slaughter. Following depopulation, the farm owner is responsible for thorough washing and disinfection of farm premises. After a mandatory down-time, the farm is repopulated with pigs from MRSA-negative herds [73]. The surveillance programme in 2019 detected only one pig herd with MRSA. In total, 722 herds were included in the survey [74].

4.2.4. Mycobacterium avium

The authors of the study [15] reported that it was not possible to determine if the vaccine tested had significantly reduced the bacterial load of the animals challenged, since low numbers of organisms were cultured. More importantly, the authors also note that the vaccines were not effective in controlling the foodborne zoonotic potential of M. avium given that the elimination of the organism was not achieved.

4.2.5. Hepatitis E Virus

One unexpected result was the absence of Hepatitis E virus-related papers retained for analysis, even after a relatively high number of papers were detected in the initial search (n = 77). This pathogen has been earning attention in the last few years. However, none of these papers fulfilled the criteria for inclusion in this systematic review. According to Meester et al. [75], pigs are the main reservoir of the HEV (genotypes 3 and 4) worldwide, and humans can become infected by consumption of pork or contact with pigs. As HEV is persistently present on most pig farms, current risk mitigation strategies should focus on lowering transmission within farms, especially between farm compartments. Vaccination of pigs may aid HEV control in the future [76].

4.2.6. Y. enterocolitica

Due to the exclusion criteria, studies on Y. enterocolitica were not retained. However, the risk assessment by EFSA [1] identified Y. enterocolitica as one of the most relevant biological hazards in the context of meat inspection of swine. Accordingly, this agent should be covered by preventive measures in the meat chain. At the farm level, some risk factors have been identified as contributors for seropositive herds, namely:
  • Buying animals from herds with an unknown carrier state for human pathogenic Y. enterocolitica [77,78];
  • Buying piglets from more than one farm [78,79,80]; and
  • Use of non-municipal water sources and having a continuous production (instead of applying an all-in/all-out strategy) [79].
One study indicated that clusters (health and breeding pyramids) of pig herds free from animal diseases (Specific Pathogen Free (SPF) herds) also seem to be free from Y. enterocolitica [81]. Some of these SPF herds were even free from Campylobacter spp. [82].
However, there are several control options at the slaughterhouse [83]. However, after slaughter, control measures seem ineffective, since Y. enterocolitica can survive and grow during cold storage and under modified atmospheres [83,84].

4.2.7. T. gondii

The risk assessment by EFSA [1] also identified T. gondii as one of the most relevant biological hazards in the context of meat inspection of swine, but no studies of T. gondii were retained. Former studies show that the prevalence of T. gondii in pigs has decreased considerably in areas with intensive farm management [85,86]. However, pork originating from outdoor pig husbandry systems including those that are more welfare friendly such as free roaming, poses a higher risk compared to the indoor system [87], and this was not the focus of this systematic review. Other interesting approaches to interrupt the zoonotic circle of T. gondii are the vaccination of cats [88] or the control of the cat population in endemic regions [89]. So far, no commercial vaccine for cats is available.

4.3. Limitations of This Review

The results of this review and the implications inferred from them are valid within the context of the inclusion and exclusion criteria as defined a priori. This means that papers which did not contain a control group and from which a causal effect of the intervention tested could not be inferred were rejected. This decision was made to minimize bias and to eliminate confounding factors. However, observational studies are prevalent in the literature and the quality of the evidence provided by some of these studies should be graded up, provided that their results are robust. For example, identifying a strong correlation between high biosecurity and cleaning standards and low Salmonella shedding across multiple farms is a strong indication that such interventions are likely to be effective under the various scenarios of each farm. Conversely, randomized control trials reporting positive effects (P < 0.05) rarely declare the magnitude of this effect (i.e., adjusted R-squared with the proportion of the variability explained by the factor tested in the outcome variable). Mapping and summarizing the risk factors for each foodborne pathogen and the pre-harvest interventions proposed to tackle them is a task yet to be undertaken.

5. Conclusions

Some foodborne pathogens appear to be best controlled at a post-harvest level. However, overall, high herd health status coupled with good management and biosecurity were effective to control or prevent most foodborne pathogens in pork at the pre-harvest level. In spite of not having been included in the review, the SPF herd principle, stamping out and repopulating with disease-free animals, has been reported as a feasible and effective intervention to control foodborne pathogens like Salmonella, Y. enterocolitica and MRSA.

Supplementary Materials

The following are available online at, S1: PRISMA checklist for systematic reviews; S2: Detailed search strings used in each database; S3: List of studies included in the systematic review (n = 52); S4: List of studies excluded after full text evaluation (n = 35).

Author Contributions

Conceptualization, D.M. and T.N.; Methodology, M.R.d.C., J.P., D.M. and T.N.; Validation, D.M. and T.N.; Searches and data collation, M.R.d.C. and J.P.; Record screening, M.R.d.C. and J.P.; Data extraction and Curation, M.R.d.C. and J.P.; Writing—Original Draft Preparation, M.R.d.C.; Writing—Review & Editing, M.R.d.C., J.P., D.M. and T.N.; Supervision, D.M. and T.N.; Funding Acquisition, D.M. and T.N. All authors have read and agreed to the published version of the manuscript.


This research received no external funding. This publication is based upon work from COST Ac-tion 18105 RIBMINS ( supported by COST (European Cooperation in Science and Technology;, funded by the Horizon 2020 Framework Programme of the Eu-ropean Union. The publication of this article was funded by RIBMINS COST Action (CA18105).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data generated and analysed during this study are included in this published article (and its Supplementary Information Files).

Conflicts of Interest

The authors declare no conflict of interest.


  1. EFSA. Scientific Opinion on the public health hazards to be covered by inspection of meat (swine). EFSA J. 2011, 9, 2351. [Google Scholar] [CrossRef][Green Version]
  2. Baer, A.A.; Miller, M.J.; Dilger, A.C. Pathogens of Interest to the Pork Industry: A Review of Research on Interventions to Assure Food Safety. Compr. Rev. Food Sci. Food Saf. 2013, 12, 183–217. [Google Scholar] [CrossRef]
  3. Blagojevic, B.; Nesbakken, T.; Alvseike, O.; Vågsholm, I.; Antic, D.; Johler, S.; Houf, K.; Meemken, D.; Nastasijevic, I.; Pinto, M.V.; et al. Drivers, opportunities, and challenges of the European risk-based meat safety assurance system. Food Control. 2021, 124, 107870. [Google Scholar] [CrossRef]
  4. Pessoa, J.; Rodrigues da Costa, M.; Nesbakken, T.; Meemken, D.; RIBMINS Cost Action. Assessment of the Effectiveness of Pre-harvest Meat Safety Interventions to Control Foodborne Pathogens in Broilers: A Systematic Review. Curr. Clin. Microbiol. Rep. 2021, 8, 21–30. [Google Scholar] [CrossRef]
  5. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G.; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. BMJ 2009, 339, b2535. [Google Scholar] [CrossRef][Green Version]
  6. EFSA. Application of systematic review methodology to food and feed safety assessments to support decision making. EFSA J. 2010, 8, 1637. [Google Scholar] [CrossRef]
  7. Bratz, K.; Gölz, G.; Janczyk, P.; Nöckler, K.; Alter, T. Analysis of in vitro and in vivo effects of probiotics against Campylobacter spp. Berl. Munch. Tierarztl. Wochenschr. 2015, 128, 155–162. [Google Scholar]
  8. Hasan, S.; Saha, S.; Junnikkala, S.; Orro, T.; Peltoniemi, O.; Oliviero, C. Late gestation diet supplementation of resin acid-enriched composition increases sow colostrum immunoglobulin G content, piglet colostrum intake and improve sow gut microbiota. Animal 2019, 13, 1599–1606. [Google Scholar] [CrossRef][Green Version]
  9. Kelneric, Z.; Naglic, T.; Udovicic, I. Prevention of necrotic enteritis in piglets by vaccination of pregnant gilts with a Clostridium perfringens type C and D bacterin-toxoid. Vet. Med. 1996, 41, 335–338. [Google Scholar]
  10. Hammer, J.M.; Fuhrman, M.; Walz, M. Serological evaluation of a Clostridium perfringens type A toxoid in a commercial swine herd. J. Swine Health Prod. 2008, 16, 37–40. [Google Scholar]
  11. Oliveira, C.A.; Silva, R.O.S.; Lage, A.P.; Coura, F.M.; Ramos, C.P.; Alfieri, A.A.; Guedes, R.M.C.; Lobato, F.C.F. Non-toxigenic strain of Clostridioides difficile Z31 reduces the occurrence of C. difficile infection (CDI) in one-day-old piglets on a commercial pig farm. Vet. Microbiol. 2019, 231, 1–6. [Google Scholar] [CrossRef]
  12. Richard, O.K.; Grahofer, A.; Nathues, H.; Posthaus, H. Vaccination against Clostridium perfringens type C enteritis in pigs: A field study using an adapted vaccination scheme. Porc. Health Manag. 2019, 5, 9. [Google Scholar] [CrossRef] [PubMed]
  13. Unterweger, C.; Kahler, A.; Gerlach, G.F.; Viehmann, M.; von Altrock, A.; Hennig-Pauka, I. Administration of non-pathogenic isolates of Escherichia coli and Clostridium perfringens type A to piglets in a herd affected with a high incidence of neonatal diarrhoea. Animal 2017, 11, 670–676. [Google Scholar] [CrossRef][Green Version]
  14. Pletinckx, L.J.; Dewulf, J.; De Bleecker, Y.; Rasschaert, G.; Goddeeris, B.M.; De Man, I. Effect of a disinfection strategy on the methicillin-resistant Staphylococcus aureus CC398 prevalence of sows, their piglets and the barn environment. J. Appl. Microbiol. 2013, 114, 1634–1641. [Google Scholar] [CrossRef]
  15. Hines, M.E., 2nd; Frazier, K.S.; Baldwin, C.A.; Cole, J.R., Jr.; Sangster, L.T. Efficacy of vaccination for Mycobacterium avium with whole cell and subunit vaccines in experimentally infected swine. Vet. Microbiol. 1998, 63, 49–59. [Google Scholar] [CrossRef]
  16. Jones, F.T.; Langlois, B.E.; Cromwell, G.L.; Hays, V.W. Effect of feeding chlortetracycline or virginiamycin on shedding of salmonellae from experimentally-infected swine. J. Anim. Sci. 1983, 57, 279–285. [Google Scholar] [CrossRef] [PubMed]
  17. Dahl, J.; Wingstrand, A.; Nielsen, B.; Baggesen, D.L. Elimination of Salmonella typhimurium infection by the strategic movement of pigs. Vet. Rec. 1997, 140, 679–681. [Google Scholar] [CrossRef] [PubMed]
  18. Nietfeld, J.C.; Feder, I.; Kramer, T.T.; Schoneweis, D.; Chengappa, M.M. Preventing Salmonella infection in pigs with offsite weaning. Swine Health Prod. 1998, 6, 27–32. [Google Scholar]
  19. Rajkowski, K.T.; Eblen, S.; Laubauch, C. Efficacy of washing and sanitizing trailers used for swine transport in reduction of Salmonella and Escherichia coli. J. Food Prot. 1998, 61, 31–35. [Google Scholar] [CrossRef]
  20. Isaacson, R.E.; Firkins, L.D.; Weigel, R.M.; Zuckermann, F.A.; DiPietro, J.A. Effect of transportation and feed withdrawal on shedding of Salmonella Typhimurium among experimentally infected pigs. Am. J. Vet. Res. 1999, 60, 1155–1158. [Google Scholar]
  21. Maes, D.; Gibson, K.; Trigo, E.; Saszak, A.; Grass, J.; Carlson, A.; Blaha, T. Evaluation of cross-protection afforded by a Salmonella Choleraesuis vaccine against Salmonella infections in pigs under field conditions. Berl. Munch. Tierarztl. Wochenschr. 2001, 114, 339–341. [Google Scholar]
  22. Van der Wolf, P.J.; van Schie, F.W.; Elbers, A.R.; Engel, B.; van der Heijden, H.M.; Hunneman, W.A.; Tielen, M.J. Administration of acidified drinking water to finishing pigs in order to prevent Salmonella infections. Vet. Q. 2001, 23, 121–125. [Google Scholar] [CrossRef]
  23. Van Winsen, R.L.; Keuzenkamp, D.; Urlings, B.A.P.; Lipman, L.J.A.; Snijders, J.A.M.; Verheijden, J.H.M.; van Knapen, F. Effect of fermented feed on shedding of Enterobacteriaceae by fattening pigs. Vet. Microbiol. 2002, 87, 267–276. [Google Scholar] [CrossRef]
  24. Roesler, U.; Vonaltrock, A.; Heller, P.; Bremerich, S.; Arnold, T.; Lehmann, J.; Waldmann, K.H.; Truyen, U.; Hensel, A. Effects of fluorequinolone treatment acidified feed, and improved hygiene measures on the occurrence of Salmonella Typhimurium DT104 in an integrated pig breeding herd. J. Vet. Med. B Infect. Dis. Vet. Public Health 2005, 52, 69–74. [Google Scholar] [CrossRef] [PubMed]
  25. Roesler, U.; Heller, P.; Waldmann, K.H.; Truyen, U.; Hensel, A. Immunization of sows in an integrated pig-breeding herd using a homologous inactivated Salmonella vaccine decreases the prevalence of Salmonella typhimurium infection in the offspring. J. Vet. Med. B Infect. Dis. Vet. Public Health 2006, 53, 224–228. [Google Scholar] [CrossRef]
  26. Creus, E.; Perez, J.F.; Peralta, B.; Baucells, F.; Mateu, E. Effect of acidified feed on the prevalence of Salmonella in market-age pigs. Zoonoses Public Health 2007, 54, 314–319. [Google Scholar] [CrossRef]
  27. Funk, J.; Wittum, T.E.; LeJeune, J.T.; Rajala-Schultz, P.J.; Bowman, A.; Mack, A. Evaluation of stocking density and subtherapeutic chlortetracycline on Salmonella enterica subsp. enterica shedding in growing swine. Vet. Microbiol. 2007, 124, 202–208. [Google Scholar] [CrossRef] [PubMed]
  28. Patchanee, P.; Crenshaw, T.D.; Bahnson, P.B. Oral sodium chlorate, topical disinfection, and younger weaning age reduce Salmonella enterica shedding in pigs. J. Food Prot. 2007, 70, 1798–1803. [Google Scholar] [CrossRef] [PubMed]
  29. Mannion, C.; Egan, J.; Lynch, B.P.; Fanning, S.; Leonard, N. An investigation into the efficacy of washing trucks following the transportation of pigs—A Salmonella perspective. Foodborne Pathog. Dis. 2008, 5, 261–271. [Google Scholar] [CrossRef]
  30. De Busser, E.V.; Dewulf, J.; Nollet, N.; Houf, K.; Schwarzer, K.; De Sadeleer, L.; De Zutter, L.; Maes, D. Effect of organic acids in drinking water during the last 2 weeks prior to slaughter on Salmonella shedding by slaughter pigs and contamination of carcasses. Zoonoses Public Health 2009, 56, 129–136. [Google Scholar] [CrossRef]
  31. Rostagno, M.H.; Hurd, H.S.; McKean, J.D. Split marketing as a risk factor for Salmonella enterica infection in swine. Foodborne Pathog. Dis. 2009, 6, 865–869. [Google Scholar] [CrossRef]
  32. Visscher, C.F.; Winter, P.; Verspohl, J.; Stratmann-Selke, J.; Upmann, M.; Beyerbach, M.; Kamphues, J. Effects of feed particle size at dietary presence of added organic acids on caecal parameters and the prevalence of Salmonella in fattening pigs on farm and at slaughter. J. Anim. Physiol. Anim. Nutr. 2009, 93, 423–430. [Google Scholar] [CrossRef] [PubMed]
  33. Farzan, A.; Friendship, R.M. A clinical field trial to evaluate the efficacy of vaccination in controlling Salmonella infection and the association of Salmonella-shedding and weight gain in pigs. Can. J. Vet. Res. Rev. Can. Rech. Vet. 2010, 74, 258–263. [Google Scholar]
  34. Arguello, H.; Carvajal, A.; Costillas, S.; Rubio, P. Effect of the Addition of Organic Acids in Drinking Water or Feed During Part of the Finishing Period on the Prevalence of Salmonella in Finishing Pigs. Foodborne Pathog. Dis. 2013, 10, 842–849. [Google Scholar] [CrossRef] [PubMed]
  35. Arguello, H.; Carvajal, A.; Naharro, G.; Rubio, P. Evaluation of protection conferred by a Salmonella Typhimurium inactivated vaccine in Salmonella-infected finishing pig farms. Comp. Immunol. Microbiol. Infect. Dis. 2013, 36, 489–498. [Google Scholar] [CrossRef]
  36. De Ridder, L.; Maes, D.; Dewulf, J.; Pasmans, F.; Boyen, F.; Haesebrouck, F.; Meroc, E.; Roels, S.; Leyman, B.; Butaye, P.; et al. Effect of a DIVA vaccine with and without in-feed use of coated calcium-butyrate on transmission of Salmonella Typhimurium in pigs. BMC Vet. Res. 2013, 9, 8. [Google Scholar] [CrossRef][Green Version]
  37. Foss, D.L.; Agin, T.S.; Bade, D.; Dearwester, D.A.; Jolie, R.; Keich, R.L.; Lohse, R.M.; Reed, M.; Rosey, E.L.; Schneider, P.A.; et al. Protective immunity to Salmonella enterica is partially serogroup specific. Vet. Immunol. Immunopathol. 2013, 155, 76–86. [Google Scholar] [CrossRef] [PubMed]
  38. De Ridder, L.; Maes, D.; Dewulf, J.; Butaye, P.; Pasmans, F.; Boyen, F.; Haesebrouck, F.; Van der Stede, Y. Use of a live attenuated Salmonella enterica serovar Typhimurium vaccine on farrow-to-finish pig farms. Vet. J. 2014, 202, 303–308. [Google Scholar] [CrossRef]
  39. Kim, H.B.; Singer, R.S.; Borewicz, K.; White, B.A.; Sreevatsan, S.; Johnson, T.J.; Espejo, L.A.; Isaacson, R.E. Effects of tylosin administration on C-reactive protein concentration and carriage of Salmonella enterica in pigs. Am. J. Vet. Res. 2014, 75, 460–467. [Google Scholar] [CrossRef] [PubMed][Green Version]
  40. Stojanac, N.; Stevancevic, O.; Potkonjak, A.; Savic, B.; Stancic, I.; Vracar, V. The impact of space allowance on productivity performance and Salmonella spp. shedding in nursery pigs. Livestig. Sci. 2014, 164, 149–153. [Google Scholar] [CrossRef]
  41. Yin, F.G.; Farzan, A.; Wang, Q.; Yu, H.; Yin, Y.L.; Hou, Y.Q.; Friendship, R.; Gong, J.S. Reduction of Salmonella enterica Serovar Typhimurium DT104 Infection in Experimentally Challenged Weaned Pigs Fed a Lactobacillus-Fermented Feed. Foodborne Pathog. Dis. 2014, 11, 628–634. [Google Scholar] [CrossRef] [PubMed]
  42. Artuso-Ponte, V.; Moeller, S.; Rajala-Schultz, P.; Medardus, J.J.; Munyalo, J.; Lim, K.; Gebreyes, W.A. Supplementation with Quaternary Benzo(c) phenanthridine Alkaloids Decreased Salivary Cortisol and Salmonella Shedding in Pigs After Transportation to the Slaughterhouse. Foodborne Pathog. Dis. 2015, 12, 891–897. [Google Scholar] [CrossRef] [PubMed]
  43. Grilli, E.; Foresti, F.; Tugnoli, B.; Fustini, M.; Zanoni, M.G.; Pasquali, P.; Callaway, T.R.; Piva, A.; Alborali, G.L. Microencapsulated Sorbic Acid and Pure Botanicals Affect Salmonella Typhimurium Shedding in Pigs: A Close-Up Look from Weaning to Slaughter in Controlled and Field Conditions. Foodborne Pathog. Dis. 2015, 12, 813–819. [Google Scholar] [CrossRef] [PubMed]
  44. Bearson, B.L.; Bearson, S.M.D.; Kich, J.D. A DIVA vaccine for cross-protection against Salmonella. Vaccine 2016, 34, 1241–1246. [Google Scholar] [CrossRef][Green Version]
  45. Rasschaert, G.; Michiels, J.; Tagliabue, M.; Missotten, J.; De Smet, S.; Heyndrickx, M. Effect of Organic Acids on Salmonella Shedding and Colonization in Pigs on a Farm with High Salmonella Prevalence. J. Food Prot. 2016, 79, 51–58. [Google Scholar] [CrossRef]
  46. Walia, K.; Argüello, H.; Lynch, H.; Leonard, F.C.; Grant, J.; Yearsley, D.; Kelly, S.; Duffy, G.; Gardiner, G.E.; Lawlor, P.G. Effect of feeding sodium butyrate in the late finishing period on Salmonella carriage, seroprevalence, and growth of finishing pigs. Prev. Vet. Med. 2016, 131, 79–86. [Google Scholar] [CrossRef] [PubMed]
  47. Casanova-Higes, A.; Andres-Barranco, S.; Mainar-Jaime, R.C. Effect of the addition of protected sodium butyrate to the feed on Salmonella spp. infection dynamics in fattening pigs. Anim. Feed Sci. Technol. 2017, 231, 12–18. [Google Scholar] [CrossRef][Green Version]
  48. Eicher, S.D.; Rostagno, M.H.; Lay, D.C. Feed withdrawal and transportation effects on Salmonella enterica levels in market-weight pigs. J. Anim. Sci. 2017, 95, 2848–2858. [Google Scholar] [CrossRef] [PubMed]
  49. Lynch, H.; Leonard, F.C.; Walla, K.; Lawlor, P.G.; Duffy, G.; Fanning, S.; Markey, B.K.; Brady, C.; Gardiner, G.E.; Arguello, H. Investigation of in-feed organic acids as a low cost strategy to combat Salmonella in grower pigs. Prev. Vet. Med. 2017, 139, 50–57. [Google Scholar] [CrossRef]
  50. Martelli, F.; Lambert, M.; Butt, P.; Cheney, T.; Tatone, F.A.; Callaby, R.; Rabie, A.; Gosling, R.J.; Fordon, S.; Crocker, G.; et al. Evaluation of an enhanced cleaning and disinfection protocol in Salmonella contaminated pig holdings in the United Kingdom. PLoS ONE 2017, 12, e0178897. [Google Scholar] [CrossRef][Green Version]
  51. Walia, K.; Arguello, H.; Lynch, H.; Leonard, F.C.; Grant, J.; Yearsley, D.; Kelly, S.; Duffy, G.; Gardiner, G.E.; Lawlor, P.G. Effect of strategic administration of an encapsulated blend of formic acid, citric acid, and essential oils on Salmonella carriage, seroprevalence, and growth of finishing pigs. Prev. Vet. Med. 2017, 137, 28–35. [Google Scholar] [CrossRef]
  52. Casanova-Higes, A.; Andres-Barranco, S.; Mainar-Jaime, R.C. Use of a new form of protected sodium butyrate to control Salmonella infection in fattening pigs. Span. J. Agric. Res. 2018, 16, 5. [Google Scholar] [CrossRef][Green Version]
  53. Leite, F.L.L.; Singer, R.S.; Ward, T.; Gebhart, C.J.; Isaacson, R.E. Vaccination Against Lawsonia intracellularis Decreases Shedding of Salmonella enterica serovar Typhimurium in Co-Infected Pigs and Alters the Gut Microbiome. Sci Rep. 2018, 8, 10. [Google Scholar] [CrossRef][Green Version]
  54. Smith, R.P.; Andres, V.; Martelli, F.; Gosling, B.; Marco-Jimenez, F.; Vaughan, K.; Tchorzewska, M.; Davies, R. Maternal vaccination as a Salmonella Typhimurium reduction strategy on pig farms. J. Appl. Microbiol. 2018, 124, 274–285. [Google Scholar] [CrossRef] [PubMed]
  55. Holman, D.B.; Bearson, B.L.; Allen, H.K.; Shippy, D.C.; Loving, C.L.; Kerr, B.J.; Bearson, S.M.D.; Brunelle, B.W. Chlortetracycline Enhances Tonsil Colonization and Fecal Shedding of Multidrug-Resistant Salmonella enterica Serovar Typhimurium DT104 without Major Alterations to the Porcine Tonsillar and Intestinal Microbiota. Appl. Environ. Microbiol. 2019, 85, 12. [Google Scholar] [CrossRef] [PubMed][Green Version]
  56. Peeters, L.; Dewulf, J.; Boyen, F.; Brossé, C.; Vandersmissen, T.; Rasschaert, G.; Heyndrickx, M.; Cargnel, M.; Pasmans, F.; Maes, D. Effects of attenuated vaccine protocols against Salmonella Typhimurium on Salmonella serology in subclinically infected pig herds. Vet. J. 2019, 249, 67–72. [Google Scholar] [CrossRef] [PubMed]
  57. Costa, E.D.; Kich, J.D.; Miele, M.; Mores, N.; Amaral, A.; Coldebella, A.; Cardoso, M.; Corbellini, L.G. Evaluation of two strategies for reducing the spread of Salmonella in commercial swine herds during the finishing phase and their incremental cost-effectiveness ratios. Semin. Cienc. Agrar. 2020, 41, 505–516. [Google Scholar] [CrossRef]
  58. Peeters, L.; Dewulf, J.; Boyen, F.; Brosse, C.; Vandersmissen, T.; Rasschaert, G.; Heyndrickx, M.; Cargnel, M.; Mattheus, W.; Pasmans, F.; et al. Bacteriological evaluation of vaccination against Salmonella Typhimurium with an attenuated vaccine in subclinically infected pig herds. Prev. Vet. Med. 2020, 182, 11. [Google Scholar] [CrossRef]
  59. European Food Safety Authority EFSA; European Centre for Disease Prevention and Control ECDC. The European Union One Health 2019 Zoonoses Report. EFSA J. 2021, 19, e6406. [Google Scholar] [CrossRef]
  60. Davies, P.R.; Scott Hurd, H.; Funk, J.A.; Fedorka-Cray, P.J.; Jones, F.T. The role of contaminated feed in the epidemiology and control of Salmonella enterica in pork production. Foodborne Pathog. Dis. 2004, 1, 202–215. [Google Scholar] [CrossRef][Green Version]
  61. Nesbakken, T.; Skjerve, E.; Lium, B. (Eds.) The succesful control of Salmonella in Norway. In Proceedings of the 13th Safepork, Berlin, Germany, 26–29 August 2019; pp. 91–92. [Google Scholar]
  62. De la Cruz, M.L.; Conrado, I.; Nault, A.; Perez, A.; Dominguez, L.; Alvarez, J. Vaccination as a control strategy against Salmonella infection in pigs: A systematic review and meta-analysis of the literature. Res. Vet. Sci. 2017, 114, 86–94. [Google Scholar] [CrossRef] [PubMed]
  63. Wilhelm, B.; Rajić, A.; Parker, S.; Waddell, L.; Sanchez, J.; Fazil, A.; Wilkins, W.; McEwen, S.A. Assessment of the efficacy and quality of evidence for five on-farm interventions for Salmonella reduction in grow-finish swine: A systematic review and meta-analysis. Prev. Vet. Med. 2012, 107, 1–20. [Google Scholar] [CrossRef] [PubMed]
  64. Wilhelm, B.J.; Young, I.; Cahill, S.; Nakagawa, R.; Desmarchelier, P.; Rajić, A. Rapid systematic review and meta-analysis of the evidence for effectiveness of primary production interventions to control Salmonella in beef and pork. Prev. Vet. Med. 2017, 147, 213–225. [Google Scholar] [CrossRef] [PubMed]
  65. Weijtens, M.J.; van der Plas, J.; Bijker, P.G.; Urlings, H.A.; Koster, D.; van Logtestijn, J.G.; Huis in’t Veld, J.H. The transmission of campylobacter in piggeries; an epidemiological study. J. Appl. Microbiol. 1997, 83, 693–698. [Google Scholar] [CrossRef]
  66. Young, C.R.; Harvey, R.; Anderson, R.; Nisbet, D.; Stanker, L.H. Enteric colonisation following natural exposure to Campylobacter in pigs. Res. Vet. Sci. 2000, 68, 75–78. [Google Scholar] [CrossRef]
  67. Humphrey, T.; O’Brien, S.; Madsen, M. Campylobacters as zoonotic pathogens: A food production perspective. Int. J. Food Microbiol. 2007, 117, 237–257. [Google Scholar] [CrossRef]
  68. Nesbakken, T.; Eckner, K.; Rotterud, O.J. The effect of blast chilling on occurrence of human pathogenic Yersinia enterocolitica compared to Campylobacter spp. and numbers of hygienic indicators on pig carcasses. Int. J. Food Microbiol. 2008, 123, 130–133. [Google Scholar] [CrossRef]
  69. Chang, V.P.; Mills, E.W.; Cutter, C.N. Reduction of bacteria on pork carcasses associated with chilling method. J. Food Prot. 2003, 66, 1019–1024. [Google Scholar] [CrossRef]
  70. Kapperud, G.; Skjerve, E.; Bean, N.H.; Ostroff, S.M.; Lassen, J. Risk factors for sporadic Campylobacter infections: Results of a case-control study in southeastern Norway. J. Clin. Microbiol. 1992, 30, 3117–3121. [Google Scholar] [CrossRef][Green Version]
  71. Kapperud, G.; Espeland, G.; Wahl, E.; Walde, A.; Herikstad, H.; Gustavsen, S.; Tveit, I.; Natas, O.; Bevanger, L.; Digranes, A. Factors associated with increased and decreased risk of Campylobacter infection: A prospective case-control study in Norway. Am. J. Epidemiol. 2003, 158, 234–242. [Google Scholar] [CrossRef]
  72. Roux, F.; Sproston, E.; Rotariu, O.; Macrae, M.; Sheppard, S.K.; Bessell, P.; Smith-Palmer, A.; Cowden, J.; Maiden, M.C.; Forbes, K.J.; et al. Elucidating the aetiology of human Campylobacter coli infections. PLoS ONE 2013, 8, e64504. [Google Scholar] [CrossRef][Green Version]
  73. Elstrom, P.; Grontvedt, C.A.; Gabrielsen, C.; Stegger, M.; Angen, O.; Amdal, S.; Enger, H.; Urdahl, A.M.; Jore, S.; Steinbakk, M.; et al. Livestock-Associated MRSA CC1 in Norway; Introduction to Pig Farms, Zoonotic Transmission, and Eradication. Front. Microbiol. 2019, 10, 139. [Google Scholar] [CrossRef][Green Version]
  74. Urdahl, A.M.; Norström, M.; Welde, H.; Bergsjø, B.; Grøntvedt, C.A. The Surveillance Programme for Methicillin Resistant Staphylococcus aureus in Pigs in Norway 2019; Norwegian Veterinary Institute: Ås, Norway, 2020. Available online: (accessed on 15 April 2021).
  75. Meester, M.; Tobias, T.J.; Bouwknegt, M.; Kusters, N.E.; Stegeman, J.A.; van der Poel, W.H.M. Infection dynamics and persistence of hepatitis E virus on pig farms—A review. Porc. Health Manag. 2021, 7, 16. [Google Scholar] [CrossRef]
  76. Krog, J.S.; Larsen, L.E.; Breum, S.Ø. Tracing Hepatitis E Virus in Pigs From Birth to Slaughter. Front. Vet. Sci. 2019, 6, 50. [Google Scholar] [CrossRef][Green Version]
  77. Skjerve, E.; Lium, B.; Nielsen, B.; Nesbakken, T. Control of Yersinia enterocolitica in pigs at herd level. Int. J. Food Microbiol. 1998, 45, 195–203. [Google Scholar] [CrossRef]
  78. Virtanen, S.; Salonen, L.; Laukkanen-Ninios, R.; Fredriksson-Ahomaa, M.; Korkeala, H. Piglets are a source of pathogenic Yersinia enterocolitica on fattening-pig farms. Appl. Env. Microbiol. 2012, 78, 3000–3003. [Google Scholar] [CrossRef][Green Version]
  79. Vilar, M.J.; Virtanen, S.; Heinonen, M.; Korkeala, H. Management practices associated with the carriage of Yersinia enterocolitica in pigs at farm level. Foodborne Pathog. Dis. 2013, 10, 595–602. [Google Scholar] [CrossRef] [PubMed]
  80. Virtanen, S.; Nikunen, S.; Korkeala, H. Introduction of infected animals to herds is an important route for the spread of Yersinia enterocolitica infection between pig farms. J. Food Prot. 2014, 77, 116–121. [Google Scholar] [CrossRef] [PubMed]
  81. Nesbakken, T.; Iversen, T.; Lium, B. Pig herds free from human pathogenic Yersinia enterocolitica. Emerg. Infect. Dis 2007, 13, 1860–1864. [Google Scholar] [CrossRef] [PubMed]
  82. Kolstoe, E.M.; Iversen, T.; Ostensvik, O.; Abdelghani, A.; Secic, I.; Nesbakken, T. Specific pathogen-free pig herds also free from Campylobacter? Zoonoses Public Health 2015, 62, 125–130. [Google Scholar] [CrossRef] [PubMed]
  83. Nesbakken, T. 2—Update on Yersinia as a foodborne pathogen: Analysis and control. In Advances in Microbial Food Safety; Sofos, J., Ed.; Woodhead Publishing: Oxford, UK, 2015; pp. 33–58. [Google Scholar] [CrossRef]
  84. Laukkanen-Ninios, R.; Fredriksson-Ahomaa, M.; Korkeala, H. Enteropathogenic Yersinia in the Pork Production Chain: Challenges for Control. Compr. Rev. Food Sci. Food Saf. 2014, 13, 1165–1191. [Google Scholar] [CrossRef]
  85. Tenter, A.M.; Heckeroth, A.R.; Weiss, L.M. Toxoplasma gondii: From animals to humans. Int. J. Parasitol. 2000, 30, 1217–1258. [Google Scholar] [CrossRef][Green Version]
  86. Skjerve, E.; Tharaldsen, J.; Waldeland, H.; Kapperud, G.; Nesbakken, T. Antibodies to Toxoplasma gondii in Norwegian slaughtered sheep, pigs and cattle. Bull. Scand. Soc. Parasitol. 1996, 6, 11–17. [Google Scholar]
  87. Gebreyes, W.A.; Bahnson, P.B.; Funk, J.A.; McKean, J.; Patchanee, P. Seroprevalence of Trichinella, Toxoplasma, and Salmonella in antimicrobial-free and conventional swine production systems. Foodborne Pathog. Dis. 2008, 5, 199–203. [Google Scholar] [CrossRef] [PubMed][Green Version]
  88. Mateus-Pinilla, N.E.; Dubey, J.P.; Choromanski, L.; Weigel, R.M. A field trial of the effectiveness of a feline Toxoplasma gondii vaccine in reducing T-gondii exposure for swine. J. Parasitol. 1999, 85, 855–860. [Google Scholar] [CrossRef] [PubMed]
  89. Ortega-Pacheco, A.; Acosta-Viana, K.Y.; Guzman-Marin, E.; Uitzil-Alvarez, B.; Rodriguez-Buenfil, J.C.; Jimenez-Coello, M. Infection dynamic of Toxoplasma gondii in two fattening pig farms exposed to high and low cat density in an endemic region. Vet. Parasitol. 2011, 175, 367–371. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Structure outline of text strings used for the searches conducted in PubMed® and the Web of Science databases on 8 February 2021 (reproduced from Pessoa et al. [4], which employed the same methods). The search strings used are available as Supplementary Material.
Figure 1. Structure outline of text strings used for the searches conducted in PubMed® and the Web of Science databases on 8 February 2021 (reproduced from Pessoa et al. [4], which employed the same methods). The search strings used are available as Supplementary Material.
Microorganisms 09 01825 g001
Table 1. Flow of information through the systematic review for 15 foodborne pathogens, including keyword and/or string searched for each pathogen.
Table 1. Flow of information through the systematic review for 15 foodborne pathogens, including keyword and/or string searched for each pathogen.
PathogenKeyword and/or String SearchedRecords IdentifiedRecords after Duplicates’ RemovalRecords Retained after Abstract ScreeningRecords Retained after Full Text Screening
Clostridium botulinumclostridium botulinum OR botulism3300
Clostridioides difficileclostridium difficile OR c. difficile OR clostridioides difficile8700
Clostridium perfringensclostridium perfringens OR c. perfringens OR clostridial diarrh *433395
Campylobacter spp.Campylobacter * OR “Campylobacter jejuni” OR “campylobacter coli”15611532
Herpes virus type Ehepatitis E OR hepE1017700
Listeria monocytogeneslisteria monocytogenes OR listeriosis121100
MRSAmethicillin resistant staphylococcus aureus OR MRSA OR resistant s.aureus19413991
Mycobacterium avium complexmycobacterium OR tuberculosis272331
Salmonella spp.Salmone *7855555743
Sarcocystis spp.sarcocystis9700
Taenia soliumtaenia solium cysticercus OR cysticercosis OR taeniasis121200
Toxoplasma gondiitoxoplasma gondii OR toxoplasmosis1017720
Trichinella spiralisTrichin *635020
VTECVTEC OR verotoxigenic E. coli OR verotoxigenic escherichia coli OR verocytotoxigenic E. coli OR shiga toxin-producing E. coli5510
Yersinia enterocoliticaYersini *876610
TOTAL 160611808752
Legend: MRSA—Methicillin-resistant Staphylococcus aureus (MRSA); VTEC—Verocytotoxin-producing Escherichia coli (VTEC). The “*” corresponds to the code/character used for the searches in the online databases. By using a * we indicate that the search motor should retrieve all words that start like the example given, regardeless of how they end.
Table 2. Eligibility (inclusion and exclusion) criteria used for the screening of title/abstracts and full texts. Reproduced and adapted from Pessoa et al. [4], where the same set of exclusion and inclusion criteria were used.
Table 2. Eligibility (inclusion and exclusion) criteria used for the screening of title/abstracts and full texts. Reproduced and adapted from Pessoa et al. [4], where the same set of exclusion and inclusion criteria were used.
PICO 1Inclusion CriteriaExclusion Criteria
PopulationAnimal species being evaluated: must include (but not limited to) pigsDoes not include actual or theoretical <pathogen> infection/contamination in pigs
Unit of study [animal, herd, house, barn, farm] and [surfaces, food, water, environment, drinkers, feeder, other animals]Others
InterventionInterventions to control/reduce/eradicate <pathogen> in pigsStudies not mentioning control/reduce/eradicate interventions for < pathogen> in pigs
Interventions on-farm or during transport (pre-harvest)Interventions on lairage, at slaughter and post-harvest
Field/experimental studiesLab/bench studies
ComparisonControl group present [group subjected to no intervention]Control group absent
OutcomesProvides some measure of the efficacy of the interventionEfficacy of the intervention not measured
OthersLanguage: EnglishOther languages
Peer-reviewsGrey literature
1 PICO (participants, interventions, comparisons, and outcome(s))-framework to formulate research questions, following the methods proposed in the PRISMA statement [5].
Table 3. Descriptive characteristics of the 86 trials described in the 43 studies investigating pre-harvest interventions to control Salmonella spp. in pork.
Table 3. Descriptive characteristics of the 86 trials described in the 43 studies investigating pre-harvest interventions to control Salmonella spp. in pork.
VariableCategorySalmonella Studies and Trials
43 studies, n (%)
Location of interventionOn-farm
41 (95.3)
4 (9.3) 1
Study settingCommercial farm
Research farm
34 (79.1)
10 (23.2) 2
86 trials, n (%)
Type of intervention 3 Cleaning & disinfection
Combination of measures
Feed and/or water treatments
Acids in water
Acids in feed
Other (i.e., fermentation)
Other 4
7 (8.1); positive results *: n = 6
19 (22.1); positive results *: n = 15
32 (37.2); positive results *: n = 23
4 (12.5)
21 (65.6)
9 (28.1)
8 (9.3); positive results *: n = 1
24 (27.9); positive results *: n = 21
19 (22.1); positive results *: n = 11
1 Two studies tested both on-farm and transport interventions. 2 One study had two trials, one performed in a commercial farm setting, and another performed under controlled research laboratory conditions. 3 The comparison of each treatment (intervention) with the control was recorded as a trial. Some trials consisted of a combination of approaches (i.e., acids in-feed and in water simultaneously). The trials are repeated across different categories if they fit in more than one type of intervention. 4 Examples of other interventions tested are off-site early weaning, washing and disinfecting of lorries, split marketing approaches, and different space allowances. * Trials which reported at least one positive result (i.e., reduction of Salmonella shedding, increase of protective immunity).
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Rodrigues da Costa, M.; Pessoa, J.; Meemken, D.; Nesbakken, T. A Systematic Review on the Effectiveness of Pre-Harvest Meat Safety Interventions in Pig Herds to Control Salmonella and Other Foodborne Pathogens. Microorganisms 2021, 9, 1825.

AMA Style

Rodrigues da Costa M, Pessoa J, Meemken D, Nesbakken T. A Systematic Review on the Effectiveness of Pre-Harvest Meat Safety Interventions in Pig Herds to Control Salmonella and Other Foodborne Pathogens. Microorganisms. 2021; 9(9):1825.

Chicago/Turabian Style

Rodrigues da Costa, Maria, Joana Pessoa, Diana Meemken, and Truls Nesbakken. 2021. "A Systematic Review on the Effectiveness of Pre-Harvest Meat Safety Interventions in Pig Herds to Control Salmonella and Other Foodborne Pathogens" Microorganisms 9, no. 9: 1825.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop