Skip to main content Accessibility help


  • Access
  • Cited by 2


      • Send article to Kindle

        To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

        Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

        Find out more about the Kindle Personal Document Service.

        Review: Are we using probiotics correctly in post-weaning piglets?
        Available formats

        Send article to Dropbox

        To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

        Review: Are we using probiotics correctly in post-weaning piglets?
        Available formats

        Send article to Google Drive

        To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

        Review: Are we using probiotics correctly in post-weaning piglets?
        Available formats
Export citation


Intensive farming may involve the use of diets, environments or management practices that impose physiological and psychological stressors on the animals. In particular, early weaning is nowadays a common practice to increase the productive yield of pig farms. Still, it is considered one of the most critical periods in swine production, where piglet performance can be seriously affected and where they are predisposed to the overgrowth of opportunistic pathogens. Pig producers nowadays face the challenge to overcome this situation in a context of increasing restrictions on the use of antibiotics in animal production. Great efforts are being made to find strategies to help piglets overcome the challenges of early weaning. Among them, a nutritional strategy that has received increasing attention in the last few years is the use of probiotics. It has been extensively documented that probiotics can reduce digestive disorders and improve productive parameters. Still, research in probiotics so far has also been characterized as being inconsistent and with low reproducibility from farm to farm. Scientific literature related to probiotic effects against gastrointestinal pathogens will be critically examined in this review. Moreover, the actual practical approach when using probiotics in these animals, and potential strategies to increase consistency in probiotic effects, will be discussed. Thus, considering the boost in probiotic research observed in recent years, this paper aims to provide a much-needed, in-depth review of the scientific data published to-date. Furthermore, it aims to be useful to swine nutritionists, researchers and the additive industry to critically consider their approach when developing or using probiotic strategies in weaning piglets.


Present address: Department of Animal and Poultry Science, University of Saskatchewan, Saskatchewan, Canada S7N 5A8. E-mail:


This review critically examines the use of probiotics in post-weaning piglets, focusing on challenge situations, and proposes potential strategies to increase consistency in probiotic effects. Given the current lack of reproducibility commonly described with probiotic use, this approach could have significant positive effects upon the efficacy of probiotic products and economic viability of the swine industry.


In intensive farming systems, piglets are weaned at much earlier ages (between 3 and 5 weeks) than are those that would be expected in a natural environment (around 17 weeks (Jensen and Recén, 1989)). This early weaning situation is considered one of the most critical periods in swine production, in which the animals have to face multiple stressors. Piglets undergo complex social changes, such as separation from their mothers and littermates (Pluske et al., 1997). In addition, they have to adapt to abrupt changes in the feed regime and in the environment (Weary et al., 2008), leading to a variable period of hypo- or anorexia (Bruininx, 2001). All of this happens at a time when the animals still have an immature immune system (Lallès et al., 2004), low thermoregulation (Le Dividich and Herpin, 1994) and digestive capacities (Lallès et al., 2007a), together with unstable intestinal microbiota (Wang et al., 2013). Weaning is, therefore, a time where the performance of the pigs is seriously affected (Lallès et al., 2007b), and where piglets are predisposed to the overgrowth of opportunistic pathogens like Salmonella or Escherichia coli (Pluske et al., 1997; Fouhse et al., 2016). Altogether, the process is known as a post-weaning syndrome and has been extensively studied and reviewed (Pluske et al., 1997; Lallès et al., 2007a; Heo et al., 2013).

The traditional approach to overcome this situation has been the use of in-feed antibiotics. However, in Europe, the use of antibiotics as growth promoters has been banned (Regulation (EC) No. 1831/2003), and worldwide authorities are also pressing to limit its therapeutic use (National Pork Board, 2015; European Food Safety Authority and European Medicines Agency, 2017). With this context, the pig industry and researchers are making great efforts in trying to find biosecurity (Madec et al., 2000), management (Weary et al., 2009; Heo et al., 2013), genetic (Lunney, 2007) and feeding (Pluske et al., 2002; Lallès et al., 2007b) strategies to help piglets overcome the challenges of weaning. Among them, a nutritional strategy that has received increasing attention in recent years is the use of probiotics. It has been extensively documented that probiotics can reduce digestive disorders and improve productive parameters (Ahasan et al., 2015; Bajagai et al., 2016). Still, research in probiotics so far has been characterized as being inconsistent and with low reproducibility from farm to farm. Consequently, although probiotics have demonstrated good potential, many farmers do not consider them to be reliable.

The objective of this review is to critically examine the use of probiotics in the post-weaning phase, focusing on challenge situations, in order to assess whether we are making good use or not of these types of products. Thus, scientific literature related to probiotic effects in experimental models of disease will be reviewed, and subsequently, a discussion about the actual practical approach when using probiotics and how it could be improved will be presented.

Considering the boost in probiotic research observed in the last few years, this paper aims to provide a much-needed, in-depth review of the scientific data published to-date. Furthermore, it aims to be useful to swine nutritionists, researchers and the additive industry to critically consider their approach when using or developing probiotic strategies in post-weaning piglets.

Use of probiotics against pathogens

A vast amount of research is published yearly in relation to probiotic capacities to improve gastrointestinal health and fight digestive pathogens. It is worth mentioning that the interest of finding probiotic strategies to fight these pathogens not only exists in animal production, but it is also present in human medicine, which, in many cases, uses pigs as a One Health approach (Mardones et al., 2017) or as a human model of disease (Meurens et al., 2012). This fact enriches the amount of information available and may be useful for the pig industry. Table 1 recalls main scientific studies published to-date, assessing the use of probiotics against pathogens in piglet experimental models of disease.

Table 1 Pig in vivo scientific works evaluating the use of probiotics against digestive bacterial pathogens (Escherichia coli and Salmonella sp.)

N/A=not available.

1 Daily mix: probiotic suspended on a daily basis and mixed with feed.

Limits on therapeutic use of probiotics

The first important factor observed is that many authors reported a positive effect by using probiotics, but there is also a considerable amount of research not supporting their use in a disease situation. In general terms, there is a higher number of articles describing beneficial effects with the use of probiotics (>80%) rather than negative effects. However, we must consider that we may have a positive-outcome bias, as many times there may not be industrial interest to publish neutral or negative results (Fanelli, 2012). Still, in view of the current published data, it can be concluded that in the majority of cases probiotic effects against pathogens were positive, although they tended to be rather discrete. Spectacular improvements, such as eliminating pathogen excretion or important increases in productive parameters have not been reported. Hence, with this background, a first takeaway message would be to stop looking for probiotics as direct replacements for antibiotics, as their effects are not comparable. Alternatively, as proposed by the European Food Safety Authority, probiotics should be considered as zoo-technical additives, in the category of digestibility enhancers or gut flora stabilizers (European Food Safety Authority, 2007). This change of mindset implies that, although with probiotics we may potentially target the same objectives than with antibiotics, when using probiotics our approach should be different. In other words, we should not include a probiotic and expect the same effects than with an antibiotic on its own, but we should combine them with other feed and/or management strategies with a more holistic approach.

Uncertainties around probiotics effects

Another apparent aspect of the reported results is that it is extremely difficult to discuss and extract conclusions with the data reported to-date because the conditions in which the probiotics have been tested are highly variable. There are important differences in experimental factors such as piglet days of age, treatment concentrations and dosing methods, or other aspects not reflected in Table 1, such as genetics, sanitary status, treatment days or diets. Probiotic effects are known to be treatment specific, depending on the particular strain, dose and context (Bosi and Trevisi, 2010; Li et al., 2012), and host specific, depending on host-related physiological parameters (e.g. health status and genetics) or environment (e.g. sanitary status and diet) (Collado et al., 2007; Mulder et al., 2009; Dinan and Cryan, 2016). Thus, it would be possible that probiotic strains that were not used in a certain trial turned out to be useful in another one, or vice versa. Undoubtedly, this background of uncertainty has made probiotics to be regarded as untrustworthy, being one of the main reasons preventing them from being widespread in the swine industry (Bosi and Trevisi, 2010). A first approach to reduce this variability could be to standardize conditions in which probiotics are studied to have tight control of the variables. However, although this strategy may potentially increase consistency in probiotic research, this would preclude even more the extrapolations of scientific results to the wide array of real-life situations present in pig production. Finally, another approach would be to increase basic research to investigate in-depth the physiological reasons for this variability, with the aim of developing tailored strategies to each situation.

Potential risks of probiotics

Furthermore, another important point is that results shown in Table 1 suggest that there may be potential risks when using certain probiotics in animals with damaged gut health or pathogen pressure. It has been documented in scientific literature that a baseline of bacterial translocation, possibly due to the increased para/trans-cellular permeability in the enterocyte determined by inflammatory stress, is normally associated with weaning (Lallès et al., 2004). This permeability has been reported to be affected by probiotic treatments such as in Trevisi et al. (2008), who reported an increase in translocation with a Bifidobacterium animalis and fructo-oligosacccharide treatment in post-weaning piglets. Consequently, an elevated risk of sepsis could be forecast in post-weaning animals when using probiotics (Verna and Lucak, 2010). Moreover, it has also been reported that some probiotics may have immune-suppressive effects in the host (Siepert et al., 2014). This effect has no disadvantageous consequence in a healthy context. Nevertheless, in the need of a rapid humoral response, the immune activation is less efficient (Bosi and Trevisi, 2010) and therefore would also be deleterious in a disease situation. Thus, in a context of increased permeability, it can been hypothesized that some probiotics could impair the immune response and increase risk of sepsis in some animals, despite the observed reductions in pathogen loads.

As stated before, the increase of basic research on probiotics is fundamental to improve the use-criteria of probiotics in the field and to obtain reproducible outcomes. Such a tailored use of probiotics requires a great amount of knowledge of probiotic intrinsic capacities and also of how probiotics modify ecological dynamics of the intestinal microbiota, depending on factors like sanitary status, genetics or feeding practices, among others. Fortunately, there has been great technological development during the last few decades. Nowadays, we have a sufficient amount of quality trials to begin to characterize the strains in relation to their mechanisms of action and interactions with the hosts. This is interesting because it opens a door to knowledge-based treatments, taking into account the context in which they are applied.

How to improve the use of probiotics in early life stages

In view of the present situation, it goes without saying that improving the use of probiotics in the swine industry relies on a drift from an empirical use to a more knowledge-based strategy. This section provides a few suggestions to be considered in the use of probiotics in early life stages, and in particular in post-weaning disorders. However, its aim is solely to provide a starting point for the reader to critically evaluate the use of probiotics, rather than a dissertation on their use.

To start with, assessment of the probiotic strains should be done in a wide range of health conditions. As commented by Bosi and Trevisi (2010), the identification of strains with positive effects in a broad range of gut health situations, and even capable of working in different species is economically interesting for the additive industry. However, in some cases, although specific strains had demonstrated positive effects in a normal physiological situation, they were reported to be detrimental in challenge situations in piglets (see Table 1). Hence, in our opinion, it would be highly recommended to characterize the possible risks of using a probiotic in a disease context, building clear differences whether probiotic usage is intended as a therapy or as prophylaxis. For instance, in human studies, a clear distinction is made between research aimed at maintaining health and that which aimed to treat a disease, and this difference has important implications when designing trials and in regulatory affairs (Hill et al., 2014).

A second issue to address is the capacity of probiotics to modulate microbiota. As commented before, until today one major interest when using probiotics has been to replace antibiotics via production of in situ antimicrobial compounds or enzymes to cure infections (Patil et al., 2015). Although some particular strains may have demonstrated effects here (Bhandari et al., 2008; Cheikhyoussef et al., 2008), their usefulness in this aspect is limited and spectacular improvements such as eliminating pathogen excretion are rarely reported (see Table 1). However, probiotics become much more powerful and valuable when we use them as ‘preventive’ health promoters and gut microbiota stabilizers (Simmering and Blaut, 2001). There is an increasing amount of scientific publications supporting that probiotic effects in gut ecology and/or immune stimulation may provide support to keep animals healthy (Zhang et al., 2010; Klaenhammer et al., 2012; Prieto et al., 2014; Zacarías et al., 2014). In addition, new selection criteria based on the mechanisms of action of the strains can allow the apparition of other probiotics that have not been previously considered in animal production but can enhance gut health and make it more robust. Besides, to increase control on their effects, probiotic strategies should be more focused. Strains should be selected depending on the objectives being looked for, and not as if probiotics were beneficial for everything. Effects should target specifically to a site. Targeting, for example, M cells if applications seek to boost intestinal immunity by enhancing development of secretory IgA (Corthésy et al., 2007), or targeting the hypothalamic–pituitary–adrenal axis if we want to improve animal well-being and reduce effects of common stressors (Hardy et al., 2013; Zhou and Foster, 2015). In addition, some specific probiotic strains adapted to the colonic environment could be good candidates to fight gut dysbiosis (Corthésy et al., 2007), but other strains could be better to enhance productive performance based on their enzymatic hydrolysis properties (Kim et al., 2007) or biosynthetic pathways for amino acids’ new synthesis (Pridmore et al., 2004). Hence, further assessment and classification of commercial probiotics in relation to their mechanisms of action are desirable, to be able to implement strategies that are more precise and oriented to specific needs of these animals.

Another point to take into account is the variability in the response to a probiotic, depending on the host or the herd in which it is introduced. It has been described how a probiotic strategy may have ‘responder’ and ‘non-responder’ individuals in a homogenous group of animals, and also how different microbial environments can determine variability among herds (Klaenhammer et al., 2012; Arora et al., 2013; Starke et al., 2013). For instance, it has been described how the genetically determined different presence of sugar complexes along the host gut surface may facilitate the adhesion on the glycocalix of some enteropathogens, possessing specific colonization factors (such as E. coli F18 and K88) and, possibly, of commensal bacteria (Krogfelt, 1991; Lee et al., 2013). Moreover, the emerging ‘-omic’ technologies clearly open a window to refine our approach and understand better the interactions between a probiotic strain and the ecosystem in which it is going to be introduced. It is expected that by increasing our understanding in pig microbiome knowledge, we will identify key microbial groups of the piglets gut with an important role in maintaining a productive and disease-resistant ecosystems (Kim and Isaacson, 2015). In addition, we will eventually be able to identify the most appropriate strain (or strains) to use as specific probiotic treatments for a particular situation depending on the targeted microbial ecosystem (Sanders et al., 2013). For instance, two enterotype-like clusters have recently been identified in pig microbiota significantly correlated with performance (Ramayo-Caldas et al., 2016). Likewise, to correlate probiotic effects to specific enterotypes would reasonably reduce the variability of empirical use. On the other side, our understanding in probiotic interactions with the host and in particular with the intestinal cells gene expression has greatly improved in recent years. For example, a common mechanism for the anti-inflammatory activity of several probiotics has been described to be regulated by the micro-organisms pattern recognition receptors toll-like receptor 2 (TLR-2) (Villena et al., 2012; Tomosada et al., 2013). In addition, it has been described how selective pressures among European pig populations have derived into specific TLR-2 gene variants (Darfour-Oduro et al., 2016). Overall, this is interesting because it provides a common mechanism for the anti-inflammatory activity of several probiotics (including different strains such as Lactobacillus spp. and Bifidobacterium spp.) (Tomosada et al., 2013). Moreover, it provides a potential biomarker for the screening and selection of new immune-regulatory strains, to be used efficiently at a population level to enhance immunity.

Furthermore, another possibility to potentiate probiotic effects would be to combine probiotics with complementary actions, with many beneficial examples reported in the bibliography (Casey et al., 2007; Lessard et al., 2009; Zhou et al., 2015; Barba-Vidal et al., 2017b). Probiotic combinations can be multi-strain probiotics, containing more than one strain of the same species or closely related species (for instance, Lactobacillus acidophilus and L. casei), or multispecies probiotics, containing strains of different probiotic species that belong to one or more genera (e.g. L. acidophilus, Bifidobacterium longum and Enterococcus faecium) (Timmerman et al., 2004). It has been suggested that the greater variety of probiotic genera present within a mixture may reduce its effectiveness, through mutual inhibition by the different species, antimicrobial compounds or competition for either nutrients or binding sites (Chapman et al., 2011 and 2012). However, multispecies probiotics have also been related to a broader spectrum of activity (e.g. inhibition of a wider variety of pathogenic bacteria), and if well-designed, a greater amount of synergism and symbiosis when different probiotic effects are combined (Timmerman et al., 2004). Hence, although bacterial combinations have a high potential, beneficial properties of different strains are not always additive (Chapman et al., 2011). This is not an easy field of research and bacterial interactions inside the pig gut ecosystem should be further explored to be able to construct effective strategies. Still, unfortunately in vivo studies comparing single strains to probiotic combinations are still rare. Additional approaches to strengthen effects could be the addition of specific prebiotic substrates (symbiotic concept) to selectively improve the growth of the introduced strain (Shenderov, 2011; Arboleya et al., 2016) or to promote a microbiota more favorable for the probiotic to exert its action (Guerra-Ordaz et al., 2014). Another option to improve and to specifically select the effects of a probiotic would be the genetic manipulation of the strain (Bjerre et al., 2016; Xu et al., 2016). However, introduction of GMO in the animal feed is nowadays a very controversial issue.

The way a probiotic is administered to the piglets can also be a critical point to consider as, sometimes, reduced stability and viability of the probiotic cells can limit the use of the potentially most beneficial strains. Some bacterial genera are particularly sensitive to be introduced in the dry feed, as they cannot stand chemical–physical conditions of the feed or the manufacturing process (Angelis et al., 2006). In this sense, the development of acclimatization procedures or protective coating to enable them to stand environmental aggression (Sewell, 2016) is a promising field of development for the use or probiotics as in-feed additives. Still, dry feed is not the only way a probiotic can be administered to piglets. Daily administration of fresh probiotic as a solid or liquid suspension by mixing it with the feed (top dressing) is a common procedure in research trials (see Table 1). However, although it may be a good strategy to increase the viability of probiotics when delivered, it is a highly time-consuming routine difficult to be implemented in commercial pig farms. Alternatively, fermented milk, suspension in milk or even suspension in water can be considered. For instance, Gebert et al. (2011) supplemented a milk replacer with a Lactobacillus probiotic strain and saw positive effects on pre-weaning animals.

Besides, early dosing of probiotics in the pre-weaning period should be considered. Gut microbiota plays a critical role in the adaptation from a neonatal-immature gut to a functional adult system, resistant to adverse ecological shifts at challenges such as weaning (Lewis et al. 2012). Hence, providing probiotics at this point could potentially permit the establishment of early and life-long health benefits (Kenny et al., 2011). Sows should be given more importance here, as many studies have shown how introducing probiotics in the sow diet is an effective way to modify the gut ecosystem and the health of piglets (Alexopoulos et al., 2004; Bohmer et al., 2006; Apic et al., 2014; Siepert et al., 2014; Kritas et al., 2015; Scharek-Tedin et al., 2015). Alternatively, the introduction of probiotic strategies via ‘creep feed’ is increasingly being studied (Alexopoulos et al., 2004; Shim et al., 2005; Giang et al., 2010). Nevertheless, results of these experiments are largely variable, probably due to the fact that piglets usually ingest small or null quantities of them (Pajor et al., 1991).


A systematic approach should be undertaken when designing a probiotic intervention to identify potential risk factors of the target animals, the suitability of a specific probiotic strain and the appropriateness of the dosing method. This process is difficult in pig production where a collectivity is being treated. More research is needed to further characterize the mechanisms of action of probiotics and their interaction in different gut health situations. We are, nowadays, able to make science-based prescriptions of probiotics in a limited amount of situations. However, eventually, when sufficient evidence is built up, we will be able to make reliable recommendations for every particular situation. Once at this point, probiotics will be used much more efficiently and the swine industry will be able to obtain the most by investing in these products.


The authors would like to thank Mr Chuck Simmons, native English-speaking University Instructor, for his correction of this article’s language and style.

Declaration of interest

Authors declare no conflict of interest.

Ethics statement


Software and data repository resources



Ahasan, A, Agazzi, A, InverniKzzi, G, Bontempo, V and Savoini, G 2015. The beneficial role of probiotics in monogastric animal nutrition and health. Journal of Dairy, Veterinary & Animal Research 2, 120.
Ahmed, S, Hoon, J, Hong-Seok, M and Chul-Ju, Y 2014. Evaluation of Lactobacillus and Bacillus-based probiotics as alternatives to antibiotics in enteric microbial challenged weaned piglets. African Journal of Microbiology Research 8, 96104.
Alexopoulos, C, Georgoulakis, IE, Tzivara, A, Kyriakis, CS, Govaris, A and Kyriakis, SC 2004. Field evaluation of the efficacy of a probiotic containing Bacillus licheniformis and Bacillus subtilis spores, on the health status and performance of sows and their litters. Journal of Animal Physiology and Animal Nutrition 88, 381392.
Angelis, M De, Siragusa, S, Berloco, M, Caputo, L and Settanni, L 2006. Selection of potential probiotic lactobacilli from pig feces to be used as additives in pelleted feeding. Research in Microbiology 157, 792801.
Apic, I, Savic, B, Stancic, I, Zivkov-Balas, M, Bojkovski, J, Jovanovic, S, Radovic, I, Zvekic, D and Maksimovic, Z 2014. Litters health status and growth parameters in the sows feeding diets supplemented with probiotic Actisaf Sc 47® within pregnancy or lactation. In International Symposium of Animal Science, Belgrade, Serbia.
Arboleya, S, Stanton, C and Ryan, C 2016. Bosom buddies: the symbiotic relationship between infants and Bifidobacterium longum ssp. longum and ssp. infantis . Genetic and Probiotic Features. Annual review of 7, 121.
Arora, T, Singh, S and Sharma, RK 2013. Probiotics: interaction with gut microbiome and antiobesity potential. Nutrition 29, 591596.
Bajagai, YS, Klieve, AV, Dart, PJ and Bryden, WL 2016. Probiotics in animal nutrition – production, impact and regulation. In FAO Animal Production and Health Paper (ed. HPS Makkar), 179pp. Rome.
Barba Vidal, E, Castillejos, L, López Colom, P, Rivero Urgell, M, Muñoz, JAM and Martín Orúe, SM 2017a. Evaluation of the probiotic strain Bifidobacterium longum subsp. infantis CECT 7210 capacities to improve health status and fight digestive pathogens in a piglet model. Frontiers in Microbiology 8, 533.
Barba-Vidal, E, Castillejos, L, Roll, VFB, Cifuentes-Orjuela, G, Moreno Muñoz, JA and Martín-Orúe, SM 2017b. The Probiotic Combination of Bifidobacterium longum subsp. infantis CECT 7210 and Bifidobacterium animalis subsp. lactis BPL6 Reduces pathogen loads and improves gut health of weaned piglets orally challenged with Salmonella typhimurium . Frontiers in Microbiology 8, 1570.
Barba-Vidal, E, Roll, VFB, Castillejos, L, Guerra-Ordaz, AA, Manteca, X, Mallo, JJ and Martín-Orúe, SM 2017c. Response to a Salmonella typhimurium challenge in piglets supplemented with protected sodium butyrate or Bacillus licheniformis: effects on performance, intestinal health and behavior. Translational Animal Science 1, 186200.
Bhandari, SK, Opapeju, FO, Krause, DO and Nyachoti, CM 2010. Dietary protein level and probiotic supplementation effects on piglet response to Escherichia coli K88 challenge: performance and gut microbial population. Livestock Science 133, 185188.
Bhandari, SK, Xu, B, Nyachoti, CM, Giesting, DW and Krause, DO 2008. Evaluation of alternatives to antibiotics using an Escherichia coli K88+ model of piglet diarrhea: Effects on gut microbial ecology. Journal of Animal Science 86, 836847.
Bjerre, K, Cantor, MD, Nørgaard, JV., Poulsen, HD, Blaabjerg, K, Canibe, N, Jensen, BB, Stuer-Lauridsen, B, Nielsen, B and Derkx, PMF 2016. Development of Bacillus subtilis mutants to produce tryptophan in pigs. Biotechnology Letters 39, 289295.
Bohmer, BM, Kramer, W and Roth-Maier, DA 2006. Dietary probiotic supplementation and resulting effects on performance, health status, and microbial characteristics of primiparous sows. Journal of Animal Physiology and Animal Nutrition 90, 309315.
Bosi, P and Trevisi, P 2010. New topics and limits related to the use of beneficial microbes in pig feeding. Beneficial Microbes 1, 447454.
Bruininx, E 2001. The IVOG® feeding station: a tool for monitoring the individual feed intake of group‐housed weanling pigs. Journal of Animal Physiology and Animal Nutrition 85, 8187.
Casey, PG, Gardiner, GE, Casey, G, Bradshaw, B, Lawlor, PG, Lynch, PB, Leonard, FC, Stanton, C, Ross, RP, Fitzgerald, GF and Hill, C 2007. A Five-Strain Probiotic Combination Reduces Pathogen Shedding and Alleviates Disease Signs in Pigs Challenged with Salmonella enterica Serovar Typhimurium . Applied and Environmental Microbiology 73, 18581863.
Chapman, CMC, Gibson, GR and Rowland, I 2011. Health benefits of probiotics: are mixtures more effective than single strains? European Journal of Nutrition 50, 117.
Chapman, CMC, Gibson, GR and Rowland, I 2012. In vitro evaluation of single- and multi-strain probiotics: Inter-species inhibition between probiotic strains, and inhibition of pathogens. Anaerobe 18, 405413.
Cheikhyoussef, A, Pogori, N, Chen, W and Zhang, H 2008. Antimicrobial proteinaceous compounds obtained from bifidobacteria: from production to their application. International Journal of Food Microbiology 125, 215222.
Collado, MC, Grześkowiak, Ł and Salminen, S 2007. Probiotic strains and their combination inhibit in vitro adhesion of pathogens to pig intestinal mucosa. Current Microbiology 55, 260265.
Corthésy, B, Gaskins, HR and Mercenier, A 2007. Cross-talk between probiotic bacteria and the host immune system. The Journal of nutrition 137, 781S790S.
De Cupere, F, Deprez, P, Demeulenaere, D and Muylle, E 1992. Evaluation of the effect of 3 probiotics on experimental Escherichia coli enterotoxaemia in weaned piglets. Journal of veterinary medicine. Series B 39, 277284.
Darfour-Oduro, KA, Megens, H-J, Roca, A, Groenen, MAM and Schook, LB 2016. Evidence for adaptation of porcine Toll-like receptors. Immunogenetics 68, 179189.
Daudelin, J-F, Lessard, M, Beaudoin, F, Nadeau, E, Bissonnette, N, Boutin, Y, Brousseau, J-P, Lauzon, K and Fairbrother, JM 2011. Administration of probiotics influences F4 (K88)-positive enterotoxigenic Escherichia coli attachment and intestinal cytokine expression in weaned pigs. Veterinary research 42, 69.
Dinan, TG and Cryan, JF 2016. Microbes, immunity and behaviour: psychoneuroimmunology meets the microbiome. Neuropsychopharmacology 115.
Le Dividich, J and Herpin, P 1994. Effects of climatic conditions on the performance, metabolism and health status of weaned piglets: a review. Livestock Production Science 38, 7990.
European Food Safety Authority 2007. Introduction of a Qualified Presumption of Safety (QPS) approach for assessment of selected microorganisms referred to EFSA – Opinion of the Scientific Committee. EFSA Journal 5, 587.
European Medicines Agency and European Food Safety Authority 2017. EMA and EFSA Joint Scientific Opinion on measures to reduce the need to use antimicrobial agents in animal husbandry in the European Union, and the resulting impacts on food safety (RONAFA). EFSA Journal 5, 245.
Fanelli, D 2012. Negative results are disappearing from most disciplines and countries. Scientometrics 90, 891904.
Fouhse, JM, Zijlstra, RT and Willing, BP 2016. The role of gut microbiota in the health and disease of pigs. Animal Frontiers 6, 30.
Gebert, S, Davis, E, Rehberger, T and Maxwell, C 2011. Lactobacillus brevis strain 1E1 administered to piglets through milk supplementation prior to weaning maintains intestinal integrity after the weaning event. Beneficial Microbes 2, 3545.
Giang, HH, Viet, TQ, Ogle, B and Lindberg, JE 2010. Growth performance, digestibility, gut environment and health status in weaned piglets fed a diet supplemented with potentially probiotic complexes of lactic acid bacteria. Livestock Science 129, 95103.
Guerra-Ordaz, A, Gónzalez-Ortiz, G, La Regione, RM, Woodward, M, Collins, J, Pérez, JF and Martín-Orúe, SM 2014. Lactulose and Lactobacillus plantarum, a potential complementary synbiotic to control postweaning colibacillosis in piglets. Applied and Environmental Microbiology 80, 48794886.
Hardy, H, Harris, J, Lyon, E, Beal, J and Foey, AD 2013. Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients 5, 18691912.
Heo, JM, Opapeju, FO, Pluske, JR, Kim, JC, Hampson, DJ and Nyachoti, CM 2013. Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. Journal of Animal Physiology and Animal Nutrition 97, 207237.
Hill, C, Guarner, F, Reid, G, Gibson, GR, Merenstein, DJ, Pot, B, Morelli, L, Canani, RB, Flint, HJ, Salminen, S, Calder, PC and Sanders, ME 2014. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews. Gastroenterology & Hepatology 11, 506514.
Jensen, P and Recén, B 1989. When to wean – observations from free-ranging domestic pigs. Applied Animal Behaviour Science 23, 4960.
Kenny, M, Smidt, H, Mengheri, E and Miller, B 2011. Probiotics – do they have a role in the pig industry? Animal 5, 462470.
Kim, HB and Isaacson, RE 2015. The pig gut microbial diversity: understanding the pig gut microbial ecology through the next generation high throughput sequencing. Veterinary Microbiology 177, 242251.
Kim, E-Y, Kim, Y-H, Rhee, M-H, Song, J-C, Lee, K-W, Kim, K-S, Lee, S-P, Lee, I-S and Park, S-C 2007. Selection of Lactobacillus sp. PSC101 that produces active dietary enzymes such as amylase, lipase, phytase and protease in pigs. The Journal of General and Applied Microbiology 53, 111117.
Klaenhammer, TR, Kleerebezem, M, Kopp, MV and Rescigno, M 2012. The impact of probiotics and prebiotics on the immune system. Nature Reviews Immunology 12, 728734.
Konstantinov, SR, Smidt, H, Akkermans, ADL, Casini, L, Trevisi, P, De Filippi, S, Bosi, P and De Vos, WM 2008. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiology Ecology 66, 599607.
Krause, DO, Bhandari, SK, House, JD and Nyachoti, CM 2010. Response of nursery pigs to a synbiotic preparation of starch and an anti- Escherichia coli K88 probiotic. Applied and Environmental Microbiology 76, 81928200.
Kreuzer, S, Janczyk, P, Assmus, J, Schmidt, MFG, Brockmann, GA and Nöckler, K 2012. No beneficial effects evident for Enterococcus faecium NCIMB 10415 in weaned pigs infected with Salmonella enterica serovar Typhimurium DT104. Applied and Environmental Microbiology 78, 48164825.
Kritas, SK, Marubashi, T, Filioussis, G, Petridou, E, Christodoulopoulos, G, Burriel, AR, Tzivara, A, Theodoridis, A and Pískoriková, M 2015. Reproductive performance of sows was improved by administration of a sporing bacillary probiotic (C-3102). Journal of Animal Science 93, 405.
Krogfelt, KA 1991. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli . Clinical Infectious Diseases 13, 721735.
Lallès, J-P, Bosi, P, Smidt, H and Stokes, CR 2007a. Weaning – a challenge to gut physiologists. Livestock Science 108, 8293.
Lallès, J-P, Bosi, P, Smidt, H and Stokes, CR 2007b. Nutritional management of gut health in pigs around weaning. The Proceedings of the Nutrition Society 66, 260268.
Lallès, J-P, Boudry, G, Favier, C, Le Floc’h, N, Luron, I, Montagne, L, Oswald, IP, Pié, S, Piel, C and Sève, B 2004. Gut function and dysfunction in young pigs: physiology. Animal Research 53, 301316.
Lee, SM, Donaldson, GP, Mikulski, Z, Boyajian, S, Ley, K and Mazmanian, SK 2013. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426429.
Lessard, M, Dupuis, M, Gagnon, N, Nadeau, É, Matte, JJ, Goulet, J and Fairbrother, JM 2009. Administration of Pediococcus acidilactici or Saccharomyces cerevisiae boulardii modulates development of porcine mucosal immunity and reduces intestinal bacterial translocation after Escherichia coli challenge. Journal of Animal Science 87, 922934.
Lewis, MC, Inman, CF, Patel, D, Schmidt, B, Mulder, I, Miller, B, Gill, BP, Pluske, J, Kelly, D, Stokes, CR and Bailey, M 2012. Direct experimental evidence that early-life farm environment influences regulation of immune responses. Pediatric Allergy and Immunology 23, 265269.
Li, X-Q, Zhu, Y-H, Zhang, H-F, Yue, Y, Cai, Z-X, Lu, Q-P, Zhang, L, Weng, X-G, Zhang, F-J, Zhou, D, Yang, J-C and Wang, J-F 2012. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PloS one 7, e40666.
Lunney, JK 2007. Advances in swine biomedical model genomics. International Journal of Biological Sciences 3, 179184.
Madec, F, Bridoux, N, Cariolet, R, Duval-i, Y and Hampson, DJ 2000. Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field. Veterinary Microbiology 15, 34.
Mardones, FO, Hernandez-Jover, M, Berezowski, JA, Lindberg, A, Mazet, JAK and Morris, RS 2017. Veterinary epidemiology: Forging a path toward one health. Preventive Veterinary Medicine 137, 147150.
Meurens, F, Summerfield, A, Nauwynck, H, Saif, L and Gerdts, V 2012. The pig: a model for human infectious diseases. Trends in Microbiology 20, 5057.
Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, C-D, Musk, CC and Kelly, D 2009. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7, 79.
Naqid, IA, Owen, JP, Maddison, BC, Gardner, DS, Foster, N, Tchórzewska, MA, La Ragione, RM and Gough, KC 2015. Prebiotic and probiotic agents enhance antibody-based immune responses to Salmonella typhimurium infection in pigs. Animal Feed Science and Technology 201, 5765.
National Pork Board (NPB) 2015. Antibiotics on the farm: what you need to know about new regulations. NPB, Des Moines, IA, USA.
Pajor, E, Fraser, D and Kramer, D 1991. Consumption of solid food by suckling pigs: individual variation and relation to weight gain. Applied Animal Behaviour Science 32, 139155.
Patil, AK, Kumar, S, Verma, AK and Baghel, RPS 2015. Probiotics as feed additives in weaned pigs: a review. Livestock Research International 3, 3139.
Pluske, JR, Hampson, DJ and Williams, IH 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215236.
Pluske, JR, Pethick, DW, Hopwood, DE and Hampson, DJ 2002. Nutritional influences on some major enteric bacterial diseases of pig. Nutrition Research Reviews 15, 333371.
Pridmore, RD, Berger, B, Desiere, F, Vilanova, D, Barretto, C, Pittet, A-C, Zwahlen, M-C, Rouvet, M, Altermann, E, Barrangou, R, Mollet, B, Mercenier, A, Klaenhammer, T, Arigoni, F and Schell, MA 2004. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proceedings of the National Academy of Sciences 101, 25122517.
Prieto, ML, O’Sullivan, L, Tan, SP, McLoughlin, P, Hughes, H, O’Donovan, O, Rea, MC, Kent, RM, Cassidy, JP, Gardiner, GE and Lawlor, PG 2014. Evaluation of the efficacy and safety of a marine-derived Bacillus strain for use as an in-feed probiotic for newly weaned pigs. PloS one 9, e88599.
Ramayo-Caldas, Y, Mach, N, Lepage, P, Levenez, F, Denis, C, Lemonnier, G, Leplat, J-J, Billon, Y, Berri, M, Doré, J, Rogel-Gaillard, C and Estellé, J 2016. Phylogenetic network analysis applied to pig gut microbiota identifies an ecosystem structure linked with growth traits. The ISME Journal 10, 29732977.
Sanders, ME, Guarner, F, Guerrant, R, Holt, PR, Quigley, EMM, Sartor, RB, Sherman, PM and Mayer, EA 2013. An update on the use and investigation of probiotics in health and disease. Gut 62, 787796.
Scharek-Tedin, L, Kreuzer-Redmer, S, Twardziok, SO, Siepert, B, Klopfleisch, R, Tedin, K, Zentek, J and Pieper, R 2015. Probiotic treatment decreases the number of CD14-expressing cells in porcine milk which correlates with several intestinal immune parameters in the piglets. Frontiers in Immunology 6, 108.
Sewell, J 2016. Lactoplan. A heat-stable lactobacillus. Technical Bulletin Nutraferma No 3.
Shenderov, BA 2011. Probiotic (symbiotic) bacterial languages. Anaerobe 17, 490495.
Shim, SB, Verstegen, MWA, Kim, IH, Kwon, OS and Verdonk, JMAJ 2005. Effects of feeding antibiotic-free creep feed supplemented with oligofructose, probiotics or synbiotics to suckling piglets increases the preweaning weight gain and composition of intestinal microbiota. Archives of Animal Nutrition 59, 419427.
Shu, Q, Qu, F and Gill, H 2001. Probiotic treatment using Bifidobacterium lactis HN019 reduces weanling diarrhea associated with rotavirus and Escherichia coli infection in a piglet model. Journal of Pediatric Gastroenterology and Nutrition 33, 171177.
Siepert, B, Reinhardt, N, Kreuzer, S, Bondzio, A, Twardziok, S, Brockmann, G, Nöckler, K, Szabó, I, Janczyk, P, Pieper, R and Tedin, K 2014. Enterococcus faecium NCIMB 10415 supplementation affects intestinal immune-associated gene expression in post-weaning piglets. Veterinary Immunology and Immunopathology 157, 6577.
Simmering, R and Blaut, M 2001. Pro- and prebiotics – the tasty guardian angels? Applied Microbiology and Biotechnology 55, 1928.
Starke, IC, Pieper, R, Neumann, K, Zentek, J and Vahjen, W 2013. Individual responses of mother sows to a probiotic Enterococcus faecium strain lead to different microbiota composition in their offspring. Beneficial microbes 4, 345356.
Szabó, I, Wieler, LH, Tedin, K, Scharek-Tedin, L, Taras, D, Hensel, A, Appel, B and Nöckler, K 2009. Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica serovar Typhimurium DT104 infection in a porcine animal infection model. Applied and Environmental Microbiology 75, 26212628.
Timmerman, HM, Koning, CJM, Mulder, L, Rombouts, FM and Beynen, AC 2004. Monostrain, multistrain and multispecies probiotics – a comparison of functionality and efficacy. International Journal of Food Microbiology 96, 219233.
Tomosada, Y, Villena, J, Murata, K, Chiba, E, Shimazu, T, Aso, H, Iwabuchi, N, Xiao, J, Saito, T and Kitazawa, H 2013. Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression. PloS one 8, e59259.
Trevisi, P, Casini, L, Coloretti, F, Mazzoni, M, Merialdi, G and Bosi, P 2011. Dietary addition of Lactobacillus rhamnosus GG impairs the health of Escherichia coli F4-challenged piglets. Animal 5, 13541360.
Trevisi, P, Colombo, M, Priori, D, Fontanesi, L, Galimberti, G, Calò, G, Motta, V, Latorre, R, Fanelli, F, Mezzullo, M, Pagotto, U, Gherpelli, Y, D’inca, R and Bosi, P 2015. Comparison of three patterns of feed supplementation with live Saccharomyces cerevisiae yeast on postweaning diarrhea, health status, and blood metabolic profile of susceptible weaning pigs orally challenged with Escherichia coli F4ac. Journal of Animal Science 93, 22252233.
Trevisi, P, De Filippi, S, Minieri, L, Mazzoni, M, Modesto, M, Biavati, B and Bosi, P 2008. Effect of fructo-oligosaccharides and different doses of Bifidobacterium animalis in a weaning diet on bacterial translocation and Toll-like receptor gene expression in pigs. Nutrition (Burbank, Los Angeles County, Calif.) 24, 10231029.
Trevisi, P, Latorre, R, Priori, D, Luise, D, Archetti, I, Mazzoni, M, D’Inca, R and Bosi, P 2017. Effect of feed supplementation with live yeast on the intestinal transcriptome profile of weaning pigs orally challenged with Escherichia coli F4. Animal 11, 3344.
Upadhaya, SD, Shanmugam, SK, Kang, DK and Kim, IH 2017. Preliminary assessment on potentials of probiotic B. subtilis RX7 and B. methylotrophicus C14 strains as an immune modulator in Salmonella-challenged weaned pigs. Tropical Animal Health and Production 49, 10651070.
Verna, EC and Lucak, S 2010. Use of probiotics in gastrointestinal disorders: what to recommend? Therapeutic Advances in Gastroenterology 3, 307319.
Villena, J, Suzuki, R, Fujie, H, Chiba, E, Takahashi, T, Tomosada, Y, Shimazu, T, Aso, H, Ohwada, S, Suda, Y, Ikegami, S, Itoh, H, Alvarez, S, Saito, T and Kitazawa, H 2012. Immunobiotic Lactobacillus jensenii modulates the Toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigen-presenting cells. Clinical and Vaccine Immunology 19, 10381053.
Walsh, MC, Rostagno, MH, Gardiner, GE, Sutton, AL, Richert, BT and Radcliffe, JS 2012. Controlling Salmonella infection in weanling pigs through water delivery of direct-fed microbials or organic acids. Part I: effects on growth performance, microbial populations, and immune status. Journal of Animal Science 90, 261271.
Wang, M, Radlowski, EC, Monaco, MH, Fahey, GC, Gaskins, HR and Donovan, SM 2013. Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. The Journal of Nutrition 143, 795803.
Wang, A, Yu, H, Gao, X, Li, X and Qiao, S 2009. Influence of Lactobacillus fermentum I5007 on the intestinal and systemic immune responses of healthy and E. coli challenged piglets. Antonie van Leeuwenhoek 96, 8998.
Weary, DM, Huzzey, JM and von Keyserlingk, MAG 2009. Board-invited review: using behavior to predict and identify ill health in animals. Journal of Animal Science 87, 770777.
Weary, DM, Jasper, J and Hötzel, MJ 2008. Understanding weaning distress. Applied Animal Behaviour Science 110, 2441.
Xu, Y-G, Yu, H, Zhang, L, Liu, M, Qiao, X-Y, Cui, W, Jiang, Y-P, Wang, L, Li, Y-J and Tang, L-J 2016. Probiotic properties of genetically engineered Lactobacillus plantarum producing porcine lactoferrin used as feed additive for piglets. Process Biochemistry 51, 719724.
Yang, G-Y, Zhu, Y-H, Zhang, W, Zhou, D, Zhai, C-C and Wang, J-F 2016. Influence of orally fed a select mixture of Bacillus probiotics on intestinal T-cell migration in weaned MUC4 resistant pigs following Escherichia coli challenge. Veterinary Research 47, 71.
Yin, F, Farzan, A, Wang, Q (Chuck), Yu, H, Yin, Y, Hou, Y, Friendship, R and Gong, J 2014. Reduction of Salmonella enterica Serovar Typhimurium DT104 infection in experimentally challenged weaned pigs fed a Lactobacillus -fermented feed. Foodborne Pathogens and Disease 11, 628634.
Zacarías, MF, Reinheimer, J, Forzani, L, Grangette, C and Vinderola, G 2014. Mortality and translocation assay to study the protective capacity of Bifidobacterium lactis INL1 against Salmonella typhimurium infection in mice. Beneficial Microbes 5, 427436.
Zhang, L, Xu, Y, Liu, H, Lai, T, Ma, J, Wang, J and Zhu, Y 2010. Evaluation of Lactobacillus rhamnosus GG using an Escherichia coli K88 model of piglet diarrhoea: effects on diarrhoea incidence, faecal microflora and immune responses. Veterinary Microbiology 141, 142148.
Zhang, W, Zhu, Y-H, Zhou, D, Wu, Q, Song, D, Dicksved, J and Wang, J-F 2017. Oral administration of a select mixture of Bacillus probiotics affects the gut microbiota and goblet cell function in newly weaned MUC4 resistant pigs following Escherichia coli challenge. Applied and Environmental Microbiology 83, e02747-16.
Zhou, L and Foster, JA 2015. Neuropsychiatric disease and treatment dovepress psychobiotics and the gut–brain axis: in the pursuit of happiness. Neuropsychiatric Disease and Treatment 11, 715723.
Zhou, D, Zhu, Y-H, Zhang, W, Wang, M-L, Fan, W-Y, Song, D, Yang, G-Y, Jensen, BB and Wang, J-F 2015. Oral administration of a select mixture of Bacillus probiotics generates Tr1 cells in weaned F4ab/acR− pigs challenged with an F4+ ETEC/VTEC/EPEC strain. Veterinary Research 46, 95.
Zhu, Y-H, Li, X-Q, Zhang, W, Zhou, D, Liu, H-Y and Wang, J-F 2014. Dose-dependent effects of Lactobacillus rhamnosus on serum interleukin-17 production and intestinal T-cell responses in pigs challenged with Escherichia coli . Applied and Environmental Microbiology 80, 17871798.