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Recent advances in the use of bacterial probiotics in animal production

Published online by Cambridge University Press:  11 December 2023

Alberto Gonçalves Evangelista Open the ORCID record for Alberto Gonçalves Evangelista [Opens in a new window] ,
Jessica Audrey Feijó Corrêa Open the ORCID record for Jessica Audrey Feijó Corrêa [Opens in a new window] ,
Anne Caroline Marques Schoch Pinto Open the ORCID record for Anne Caroline Marques Schoch Pinto [Opens in a new window] ,
Francieli Dalvana Ribeiro Gonçalves Open the ORCID record for Francieli Dalvana Ribeiro Gonçalves [Opens in a new window]  and
Fernando Bittencourt Luciano Open the ORCID record for Fernando Bittencourt Luciano [Opens in a new window]
Alberto Gonçalves Evangelista*
Affiliation:
Graduate Program in Animal Science, Pontifícia Universidade Católica do Paraná, R. Imaculada Conceição 1155, Prado Velho, Curitiba, PR 80215-901, Brazil
Jessica Audrey Feijó Corrêa
Affiliation:
Graduate Program in Animal Science, Pontifícia Universidade Católica do Paraná, R. Imaculada Conceição 1155, Prado Velho, Curitiba, PR 80215-901, Brazil
Anne Caroline Marques Schoch Pinto
Affiliation:
Graduate Program in Animal Science, Pontifícia Universidade Católica do Paraná, R. Imaculada Conceição 1155, Prado Velho, Curitiba, PR 80215-901, Brazil
Francieli Dalvana Ribeiro Gonçalves
Affiliation:
Graduate Program in Animal Science, Pontifícia Universidade Católica do Paraná, R. Imaculada Conceição 1155, Prado Velho, Curitiba, PR 80215-901, Brazil
Fernando Bittencourt Luciano*
Affiliation:
Graduate Program in Animal Science, Pontifícia Universidade Católica do Paraná, R. Imaculada Conceição 1155, Prado Velho, Curitiba, PR 80215-901, Brazil
*
Corresponding authors: Alberto Gonçalves Evangelista; Email: [email protected]; Fernando Bittencourt Luciano; Email: [email protected]
Corresponding authors: Alberto Gonçalves Evangelista; Email: [email protected]; Fernando Bittencourt Luciano; Email: [email protected]
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Abstract

Animal husbandry is increasingly under pressure to meet world food demand. Thus, strategies are sought to ensure this productivity increment. The objective of this review was to gather advances in the use of bacterial probiotics in animal production. Lactobacilli correspond to the most used bacterial group, with several beneficial effects already reported and described, as well as the Enterococcus and Pediococcus genera – being the latter expressively used in aquaculture. Research on the Bifidobacterium genus is mostly focused on human health, which demonstrates great effects on blood biochemical parameters. Such results sustain the possibility of expanding its use in veterinary medicine. Other groups commonly assessed for human medicine but with prospective expansion to animal health are the genera Leuconostoc and Streptococcus, which have been demonstrating interesting effects on the prevention of viral diseases, and in dentistry, respectively. Although bacteria from the genera Bacillus and Lactococcus also have great potential for use in animal production, a complete characterization of the candidate strain must be previously made, due to the existence of pathogenic and/or spoilage variants. It is noteworthy that a growing number of studies have investigated the genus Propionibacterium, but still in very early stages. However, the hitherto excellent results endorse its application. In this way, in addition to the fact that bacterial probiotics represent a promising approach to promote productivity increase in animal production, the application of other strains than the traditionally employed genera may allow the exploitation of novel mechanisms and enlighten unexplored possibilities.

Keywords

animal healthanimal husbandryfood productionlactic acid bacteriazootechnical parameters
Type
Review Article
Information
Animal Health Research Reviews , First View , pp. 1 - 13
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Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

Introduction

The world population has grown rapidly in the past few decades, and this increase puts huge pressure on the food production chain to meet the demand. As the intensive production system guarantees a high yield per unit of land, it has been applied all over the world. However, the high density of animals, the confinement conditions, and practices such as the indiscriminate use of antibiotic growth promoters may promote the spread of illnesses in the animal production environment, despite the association with the antimicrobial resistance crisis. Therefore, alternatives are being sought to, not only assure productivity, maintain food quality and safety, and improve animal welfare (Ritchie et al., Reference Ritchie, Rosado and Roser2020; Evangelista and Luciano, Reference Evangelista and Luciano2021; Evangelista et al., Reference Evangelista, Corrêa, Pinto and Luciano2021a).

For this purpose, the use of probiotics figures as one of the main biotechnological approaches in all types of commercial animal production. They are constituted by live microorganisms that confer health benefits to the host when consumed, exerting, for instance, bioprotective activity towards pathogenic bacteria through different mechanisms, including competitive exclusion and the production and excretion of antimicrobial substances (Corrêa et al., Reference Corrêa, Evangelista, de Nazareth and Luciano2019; Martín and Langella, Reference Martín and Langella2019; Danielski et al., Reference Danielski, Evangelista, Luciano and de Macedo2022).

Lactic acid bacteria are the most used group of probiotics, along with specific strains of Escherichia coli, species of Bacillus, and yeast strains from the genus Saccharomyces (Fijan, Reference Fijan2014; Danielski et al., Reference Danielski, Evangelista, Luciano and de Macedo2022). Besides promoting animal health, probiotics can also improve zootechnical indexes (productive parameters), such as growth rate, final weight, and feed conversion ratio (Jatobá et al., Reference Jatobá, Moraes, Rodrigues, Vieira and Pereira2018; Bordin et al., Reference Bordin, Pilotto, Pesenatto, de Mendonça, Daroit, Rodrigues, dos Santos and Dickel2021). In addition, it has been shown that they may also present immunomodulatory effects, balancing inflammatory responses and acting in both innate and adaptive immune cells (Yahfoufi et al., Reference Yahfoufi, Mallet, Graham and Matar2018).

Several effects attributed to the use of probiotics do not have their mechanism completely elucidated, such as immunomodulation and the improvement of zootechnical indices. Although the beneficial effect achieved is known, what causes this effect is not yet fully determined (Wang et al., Reference Wang, Ni, Qing, Liu, Xin, Luo, Khalique, Dan, Pan, Jing and Zeng2018a). The main mechanism of action of probiotics is competitive exclusion, occupying binding sites that are limited in the host, in addition to the consumption of available nutrients (Corrêa et al., Reference Corrêa, Evangelista, de Nazareth and Luciano2019). Some authors consider that the beneficial effects are caused by the interaction between intestinal cells or mucus with bacterial surface-associated proteins and other non-covalently surface-bound proteins, involved in stress tolerance, survival within the host digestive tract, and modulation of intestinal inflammation (do Carmo et al., Reference do Carmo, Rabah, De Oliveira Carvalho, Gaucher, Cordeiro, da Silva, Le Loir, Azevedo and Jan2018). Other factors involved in the interaction between intestinal cells and probiotics, influencing host response, are tight adherence pili, sortase-dependent pili, fibronectin, or collagen-binding proteins (Abdelhamid et al., Reference Abdelhamid, El-Masry and El-Dougdoug2019).

Authors postulate that the anti-inflammatory action of probiotics is modulated by the increase in the expression of interleukin-10 (IL-10), which may even play a role in reducing metabolic disorders because IL-10 has the potential to regulate insulin sensitivity. Other beneficial effects mentioned are the reduction of systemic blood pressure by the production of peptides that inhibit the activity of angiotensin I-converting enzymes (Zoumpopoulou et al., Reference Zoumpopoulou, Tzouvanou, Mavrogonatou, Alexandraki, Georgalaki, Anastasiou, Papadelli, Manolopoulou, Kazou, Kletsas, Papadimitriou and Tsakalidou2018); the potential to promote the expression of host defence peptides (Wang et al., Reference Wang, Zeng, Wang, Liu, Zhang, Zhang, Wang and Ji2018b); and the improvement of serum lipid levels, explained by the competition between the host and the probiotic for nutrients from the diet, such as fatty acids, resulting in decreased absorption by the host, which, consequently, decreases weight gain, body fat mass, and hepatic lipid accumulation (Jang et al., Reference Jang, Park, Kang, Chung, Nam, Lee, Park and Lee2019). Research into the mechanisms of action of probiotics is still required, and strategies such as bioinformatics and advanced molecular techniques are an option for a complete understanding of the mechanisms underlying the beneficial effects of probiotics.

As research on probiotics has been expanding in recent years, this review gathers the latest advances in the use of bacterial probiotics in animal production, while identifying gaps in the existing knowledge, both on the bacterial species used and on the use in different types of animal production.

Methodology

A literature review was planned to investigate the use of probiotics in animal production. Search strategies were applied in the online databases PubMed, Scopus, and Google Scholar, using the following descriptors: [(Bacterial species or genus) AND (probiotic* OR bioprotection OR preservative* OR bioprotective* OR biopreservation OR biopreservative*)]. The search collected original research and review articles written in English and published since 2016. Interventional studies were included in this review. Duplicate articles, reports, commentaries, letters to the editor, and publication types other than journal articles were excluded from the analysis. Previously published reviews were included as reference sources. Older studies were used for bacteria that showed probiotic potential, but no published articles in the area in recent years were found.

A three-stage screening (title, abstract, and full text) and data extraction were performed. Mendeley software (Mendeley Desktop for Windows v. 1.80.3) was used for the management and screening of the searched results.

Although E. coli strains considered safe have been used as probiotics for decades, recent research indicates that their use may pose risks to the consumer (Massip et al., Reference Massip, Branchu, Bossuet-Greif, Chagneau, Gaillard, Martin, Boury, Sécher, Dubois, Nougayrède and Oswald2019; Nougayrède et al., Reference Nougayrède, Chagneau, Motta, Bossuet-Greif, Belloy, Taieb, Gratadoux, Thomas, Langella and Oswald2021). The authors understand that probiotic E. coli requires a more specific and in-depth approach, which requires the elaboration of a specific review on the subject. Therefore, it was decided to keep the species out of those included in the study.

Lactobacilli as probiotics

In 2020, Zheng et al. (Reference Zheng, Wittouck, Salvetti, Franz, Harris, Mattarelli, O'Toole, Pot, Vandamme, Walter, Watanabe, Wuyts, Felis, Gänzle and Lebeer2020) reclassified the former Lactobacillus genus into 25 new genera, in addition to uniting the Lactobacillaceae and Leuconostocaceae families, in order to solve taxonomic inconsistencies. The former Lactobacillus genus comprised of 261 species, including Gram-positive, fermentative, facultatively anaerobic, and non-spore-forming microorganisms. In this review, we use the generic term ‘Lactobacilli’ to designate all organisms formerly classified as Lactobacillaceae, and adopt the reclassified taxonomy to refer to Lactobacilli species. After the three-stage screening, 12 studies were included in the review.

Lactobacilli are the most explored bacteria for probiotic and/or bioprotective purposes, presenting numerous previously described positive effects in animal health and zootechnical indexes (Evangelista et al., Reference Evangelista, Corrêa, dos Santos, Matté, Milek, Biauki, Costa and Luciano2021b). It can be inferred that Lactobacilli use as a feed supplement is a viable option for many species, in different dosages, varying from 5 to 9.6 log CFU (colony-forming units)/g or ml (Liu et al., Reference Liu, Ni, Zeng, Wang, Jing, Yin and Pan2017a, Reference Liu, Zhu, Chang, Yin, Song, Li, Wang and Lu2017b), applied directly in feed (Phuoc and Jamikorn, Reference Phuoc and Jamikorn2016), drinking water (Qin et al., Reference Qin, Xie, Wang, Li, Ran, He and Zhou2018), and milk (Shen et al., Reference Shen, Cui and Xu2020) (Table 1).

Table 1. Use of Lactobacilli in animal production to improve zootechnical indexes and health parameters

The results of the use of Lactobacilli probiotics in animal feeding include an increase in daily weight gain and better feed conversion ratio; improvement of the immune profile, such as the enhanced proliferation of immune cells in the blood; and changes in the gastrointestinal microbiology, with reduction of pathogenic bacteria population (Wang et al., Reference Wang, Ni, Qing, Liu, Xin, Luo, Khalique, Dan, Pan, Jing and Zeng2018a; Saleh et al., Reference Saleh, Amber and Mohammed2020; Shen et al., Reference Shen, Cui and Xu2020) (Table 1).

Research on Lactobacilli is at an advanced level, with extensive in vitro characterization of several species in addition to in vivo studies with different production animals and methods of administration. Consequently, there is a current vast application of these microorganisms in animal production. However, some controversial issues have been raised through the years, such as the possible development of adaptation and pathogen resistance, to be further discussed in this review. Thus, it is essential to exploit different technologies to address the problem from different approaches, increasing our range of options to improve the sanitary quality of herds and, consequently, of the produced food.

Among the Lactobacilli, the species Lacticaseibacillus rhamnosus, Lactiplantibacillus plantarum, Lacticaseibacillus casei, and Lactobacillus acidophilus stand out as the most used for probiotic purposes, for almost all animal species. Referring to human health, Lactobacilli are also the most famous probiotics used, mainly in dairy products.

Use of genus Bifidobacterium as probiotics in animal production

Bacteria of the genus Bifidobacterium are commonly applied as probiotics in human diets, although research on their use for production animals is still scarce. The genus is composed of Gram-positive, anaerobic, non-spore-forming, and non-motile bacteria (Duranti et al., Reference Duranti, Lugli, Viappiani, Mancabelli, Alessandri, Anzalone, Longhi, Milani, Ossiprandi, Turroni and Ventura2020). After the three-stage screening, five studies were included in the review.

Bifidobacterium use in rodent models has demonstrated that these bacteria induce changes in the gut microbiota, in addition to attenuation of endothelial dysfunction, and decrease in blood pressure in low-renin hypertension (Robles-Vera et al., Reference Robles-Vera, Visitación, Toral, Sánchez, Romero, Gómez-Guzmán, Yang, Izquierdo-García, Guerra-Hernández, Ruiz-Cabello, Raizada, Pérez-Vizcaíno, Jiménez and Duarte2020). Its effects as a psychobiotic have also been observed, reducing depressive-like behaviour in the forced swimming test of mice (Yunes et al., Reference Yunes, Poluektova, Vasileva, Odorskaya, Marsova, Kovalev and Danilenko2020).

Intravenous treatment with probiotic Bifidobacterium bifidum (100 μl containing 108 CFU) reportedly caused antigen-specific responses, resulting in (1) elevation of IL-12 and interferon (IFN)-γ (pro-inflammatory cytokines), (2) lymphocyte proliferative responses, (3) CD8+ cytolytic effects in the spleen, (4) significantly enhanced expression of IL-6 (pro-inflammatory cytokine and anti-inflammatory myokine) in the tumour microenvironment, (5) antitumour responses, and (6) inhibition of tumour growth in tumour-bearing mice (Abdolalipour et al., Reference Abdolalipour, Mahooti, Salehzadeh, Torabi, Mohebbi, Gorji and Ghaemi2020). Bifidobacterium longum infantis, orally administered, demonstrated the potential to reduce intestinal colonization by pathogens (Salmonella and E. coli) and to stimulate a local immune response in a weaned piglet model (Barba-Vidal et al., Reference Barba-Vidal, Castillejos, López-Colom, Rivero Urgell, Moreno Muñoz and Martín-Orúe2017).

Reduction of visceral fat accumulation and improvement in glucose tolerance have been observed during treatment using Bifidobacterium animalis lactis in 5-week-old male C57BL/6J mice. Also, the levels of acetate and glucagon-like peptide-1 had increased in both gut and plasma, indicating that the bacteria can mitigate metabolic disorders by modulating gut microbiota, leading to an elevation of short-chain fatty acids (Aoki et al., Reference Aoki, Kamikado, Suda, Takii, Mikami, Suganuma, Hattori and Koga2017), suggesting improved digestibility.

There is a wide possibility of the use of Bifidobacterium to promote beneficial effects in animal production; however, few studies have explored them to date. Several strains of Bifidobacterium are used as probiotics and supplements for human consumption, and there is huge potential for their application in animal production. To enable their use, further research must focus on in vivo model studies that evaluate the positive effects of this genus on animal health and performance, just as it has been done with Lactobacilli for many years.

Enterococcus as probiotics for farm animals

The genus Enterococcus is widely used as a probiotic in animal production. They are Gram-positive bacteria with an ovoid shape, forming neither spores nor capsules, but some species may be capable of movement by a flagellum (Růžičková et al., Reference Růžičková, Vítězová and Kushkevych2020). After the three-stage screening, nine studies were included in this review.

Among the probiotic species, Enterococcus faecium stands out as the most studied bacteria, regarded in 77.8% of the Enterococcus research articles gathered for this review (n = 7). With lower incidence, Enterococcus faecalis (n = 1), and Enterococcus durans (n = 1) are also present in the literature. The bacterial concentration assessed in these studies varied between 8.54 and 9.83 log CFU g−1 or ml (Hanczakowska et al., Reference Hanczakowska, Świątkiewicz, Natonek-Wiśniewska and Okoń2017; Wang et al., Reference Wang, Cai, Zhang, Chen, Chang, Liu, Deng, Bryden and Zheng2020), which has been administered in feed (Sato et al., Reference Sato, Kuroki, Oka, Takahashi, Rao, Sukegawa and Fujimura2019), drinking water (Ognik et al., Reference Ognik, Cholewińska, Krauze, Abramowicz and Matusevicius2019), or through a Ringer solution (Lauková et al., Reference Laukova, Pogany Simonova, Kubasova, Gancarcikova, Placha, Scerbova, Revajova, Herich, Levkut Sn and Strompfova2017b) (Table 2).

Table 2. Use of Enterococcus in animal production to improve zootechnical indexes and health parameters

The observed effects summarized in Table 2 include improvement in important zootechnical indexes, such as feed conversion ratio and daily weight gain, and in biochemical parameters, such as serum concentration of immunoglobulins (IMs) – which supports the immunomodulatory potential of enterococci. Another observed effect was the decrease of pathogenic microorganisms in the host gut (Liu et al., Reference Liu, Zhu, Chang, Yin, Song, Li, Wang and Lu2017b; Ognik et al., Reference Ognik, Cholewińska, Krauze, Abramowicz and Matusevicius2019; Wang et al., Reference Wang, Wan, Shuju, Yang, Celi, Ding, Bai, Zeng, Mao, Xu, Zhang and Li2021).

The Enterococcus genus is comprised of 14 species, three of which are extensively characterized: E. faecium, E. faecalis, and E. durans. Studies using other Enterococcus species as probiotic agents – e.g. Enterococcus casseliflavus and Enterococcus raffinosus (Divya et al., Reference Divya, Varsha, Nampoothiri, Ismail and Pandey2012; Liang et al., Reference Liang, He, Zhang, Muhammad, Lu and Shao2022) – may also be promising due to previously favourable results, thus requiring in vitro characterization studies and further in vivo evaluations to allow successful applications in the future.

The vast use of Lactococcus in aquaculture

Bacteria of the Lactococcus genus, especially Lactococcus lactis, are largely used as probiotics, majorly in aquaculture, for the great success observed in research and commercial applications. They are Gram-positive, facultatively anaerobic, catalase-negative, motile, do not constitute cytochrome and do not form spores (Yerlikaya, Reference Yerlikaya2019). After the three-stage screening, 11 studies were included in this review.

In the studies evaluated in this review, L. lactis was administered through supplementation in feed, in doses between 6 and 10 log CFU g−1 (Sun et al., Reference Sun, He, Cao, Xie, Liu, Wang, Guo, Zhang and Zhou2018). The possibility of combinations of Lactococcus with bacteria of other genera – Pediococcus acidilactici, for instance (Soltani et al., Reference Soltani, Badzohreh, Mirzargar, Farhangi, Shekarabi and Lymbery2019) – to enhance results is also noteworthy (Table 3).

Table 3. Use of Lactococcus in animal production to improve zootechnical indexes and health parameters

a Analysis performed in combination with P. acidilactici at 7–10 log CFU g−1 of feed.

The use of this group as a probiotic feed supplement can improve zootechnical indexes and intestinal health, also showing immunomodulatory effects, in addition to combating important pathogens in aquaculture, such as Vibrio harveyi (Adel et al., Reference Adel, El-Sayed, Yeganeh, Dadar and Giri2017a; Ghasemzadeh et al., Reference Ghasemzadeh, Saljughi, Akbary and Hasani2018; Won et al., Reference Won, Hamidoghli, Choi, Bae, Jang, Lee and Bai2020) (Table 3). Furthermore, strains of L. lactis are potential producers of antimicrobial peptides, such as nisin (Corrêa et al., Reference Corrêa, Evangelista, de Nazareth and Luciano2019), and thus can provide additional mechanisms for pathogen control in animal production.

It is worth noting that, although L. lactis is widely used as a probiotic in aquaculture, certain species of Lactococcus may present pathogenic or deteriorating characteristics, such as Lactococcus garvieae, associated with Lactococcosis and high mortality rates in fish farming (Halimi et al., Reference Halimi, Alishahi, Abbaspour, Ghorbanpoor and Tabandeh2020). Thus, a thorough characterization of potential new probiotic strains must be carried out with caution, including genotypic tests to avoid the introduction of harmful bacteria to production systems, causing economic and animal welfare losses.

Leuconostoc: a potential probiotic for farm animals

The use of the genus Leuconostoc is already well characterized in human and animal models. The bacteria exhibit Gram-positive, facultatively anaerobic, non-spore-forming and catalase-negative characteristics (Sharma and Chandra, Reference Sharma and Chandra2018). After the three-stage screening, six studies were included in this review.

Bae et al. (Reference Bae, Kim, Park, Yoo, Kim, Joo, Ryu, Park, Lee and Park2018) observed that Leuconostoc mesenteroides administration increased the length and rates of survival of mice infected with human seasonal and avian influenza viruses. In the study conducted by Traisaeng et al. (Reference Traisaeng, Batsukh, Chuang, Herr, Huang, Chimeddorj and Huang2020), L. mesenteroides increased insulin secretion in MIN6 cell culture and in streptozotocin-induced diabetic mice; while Le and Yang (Reference Le and Yang2019) described a strong cholesterol-lowering activity of the species. In addition, Yi et al. (Reference Yi, Lim, Gu, Lee, Oh, Lee and Oh2017) reported that L. mesenteroides had shown remarkable resistance to lead and a capacity to remove this heavy metal.

Bacteria of the Leuconostoc genus are still underutilized in animal production, yet one particular species has been showing interesting properties for this use. Chang-Liao et al. (Reference Chang-Liao, Lee, Chiu, Chang and Liu2020) showed that the intracellular extracts of L. mesenteroides exerted in vitro prophylactic, therapeutic, and direct inhibitory effects against porcine epidemic diarrhoea virus in a Vero cell culture model. The expression levels of type-I IFN-dependent genes – including myxovirus resistance 1 (MX1) and IFN-stimulated gene 15 – had significantly increased after treatment with the extracts. In the study of Seo et al. (Reference Seo, Rather, Kumar, Choi, Moon, Lim and Park2012), L. mesenteroides exhibited antiviral activity against low-pathogenic avian influenza virus (H9N2) both in vitro and in vivo, respectively in Madin–Darby canine kidney cell line and in specific-pathogen-free chickens.

L. mesenteroides strains have a peculiar ability to prevent viral infections, a characteristic not yet described in common probiotics genera/species, which represents a promising unexplored field of research in animal science, considering the beneficial effects achieved in human health. Like Bifidobacterium, the use of Leuconostoc shows unexplored potential, with the need for greater investment and attention from the scientific community. Among the needs for its application in animal production, in vitro tests to evaluate its survival in the gastrointestinal tract of production animals and in vivo tests to determine health and zootechnical effects are warranted.

Pediococcus in aquaculture

Pediococci are coccoidal or ovoid, Gram-positive, non-motile, non-spore-forming and anaerobic to microaerophilic. Most species are catalase- and oxidase-negative, although Pediococcus pentosaceus has been reported to possess pseudo-catalase activity (Wade et al., Reference Wade, Strickland, Osborne and Edwards2019). After the three-stage screening, 12 studies were included in this review. The use of Pediococcus in animal production is also well characterized, especially in aquaculture, corresponding to 58.3% of the gathered articles (n = 7). Among them, P. acidilactici stands out, having been surveyed in 66.7% of the studies (n = 8).

Pediococcus-based probiotics were supplemented mainly through feeding, in concentrations between 6 and 10 log CFU g−1 (Mikulski et al., Reference Mikulski, Jankowski, Mikulska and Demey2020; Yu et al., Reference Yu, Hao, Zhiyue, Haiming and Lei2020). It is noteworthy that, like the Leuconostoc strains, P. acidilactici also demonstrates antiviral action through the modulation of genes associated with the immune system (Jaramillo-Torres et al., Reference Jaramillo-Torres, Rawling, Rodiles, Mikalsen, Johansen, Tinsley, Forberg, Aasum, Castex and Merrifield2019) (Table 4).

Table 4. Use of Pediococcus in animal production to improve zootechnical indexes and health parameters

a Analysis performed in combination with L. lactis at 7–10 log CFU g−1 of feed.

In order to make the most of their abilities and beneficial activities, Pediococcus strains should be thoroughly characterized and evaluated for application as probiotics in animal production. Likewise, different supplementation strategies and combinations with other species may also be assessed, posing great gaps to be filled by researchers in this field.

From the data presented, it is possible to observe the great importance of the use of Pediococcus in aquaculture. In this way, other branches of animal husbandry can explore this effectiveness in their production systems, in order to promote an increase in productivity through a sustainable approach.

Streptococcus strains have great potential for animal probiotic application

The use of probiotic Streptococcus species remains unexplored in animal production; however, it has been widely investigated in human health. The genus is composed of Gram-positive, non-spore-forming, facultatively anaerobic bacteria whose members include potent probiotics as well as animal and human pathogens (Patel and Gupta, Reference Patel and Gupta2018). After the three-stage screening, three studies were included in the review.

Esteban-Fernández et al. (Reference Esteban-Fernández, Ferrer, Zorraquín-Peña, López-López, Moreno-Arribas and Mira2019) described a strong inhibitory action of Streptococcus dentisani supernatant against periodontal pathogens, such as Porphyromonas gingivalis and Fusobacterium nucleatum. The oral probiotic strongly increased the secretion of an anti-inflammatory cytokine, IL-10, and significantly reduced IFN-γ expression.

Humphreys and McBain (Reference Humphreys and McBain2019) reported that Streptococcus salivarius significantly reduced viable counts of potentially pathogenic streptococci and staphylococci in pharyngeal microbiota. Also, Bidossi et al. (Reference Bidossi, De Grandi, Toscano, Bottagisio, De Vecchi, Gelardi and Drago2018) reported that S. salivarius and Streptococcus oralis can inhibit the biofilm formation capacity of certain pathogens, including Staphylococcus aureus, S. epidermidis, S. pneumoniae, S. pyogenes, Propionibacterium acnes, and Moraxella catarrhalis, and even disperse their pre-formed biofilms. Diffusible molecules secreted by the two streptococci and a decrease in the pH of the culture medium were implied mechanisms of the anti-biofilm activity.

As observed, the use of Streptococcus is widely characterized for the promotion of human health, mainly in the field of dentistry, which substantiates its possibility of application in animal production for different purposes. However, due to the existence of pathogenic species, such as S. pneumoniae and S. pyogenes, it is extremely important to fully characterize the microorganisms before their use.

Bacillus as probiotic agent

The probiotic use of Bacillus, mainly Bacillus subtilis, has been widely described in the most varied animal production systems, from aquaculture to sheep farming. The Bacillus genus is comprised of Gram-positive, obligate aerobes or facultative anaerobes, and spore-forming rods. Due to their ability to form endospores, they are able to survive in different niches including extreme environmental conditions (Tiwari et al., Reference Tiwari, Prasad, Lata, Singh and Singh2019). After the three-stage screening, 21 studies were included in this review.

Studies with B. subtilis and associations comprise 71.4% of the articles gathered in this review for this genus (n = 15). Bacterial concentration varied between 3 and 10.4 log CFU g−1 or ml (Deng et al., Reference Deng, Xiao, Ma, Tu, Diao, Chen and Jiang2018; Abdel-Moneim et al., Reference Abdel-Moneim, Selim, Basuony, Sabic, Saleh and Ebeid2020) applied to feed (Deng et al., Reference Deng, Wang, Ma, Yu, Liu, Dai and Zhao2021) or drinking water (Tarnecki et al., Reference Tarnecki, Wafapoor, Phillips and Rhody2019), resulting in improved zootechnical indexes, including weight gain and feed conversion ratio, and also immunomodulatory effects, such as stimulation of anti-inflammatory cytokine production (Du et al., Reference Du, Jiao, Dai, An, Lv, Yan, Wang and Han2018; Keerqin et al., Reference Keerqin, Rhayat, Zhang, Gharib-Naseri, Kheravii, Devillard, Crowley and Wu2021) (Table 5).

Table 5. Use of Bacillus in animal production to improve zootechnical indexes and health parameters

a Analysis performed in combination with Saccharomyces boulardii at 7 log CFU g−1 of feed.

This genus is especially interesting for commercial use due to its spore-formation ability, which may facilitate product development (Elisashvili et al., Reference Elisashvili, Kachlishvili and Chikindas2019). However, there are pathogenic and toxigenic species within the Bacillus genus, such as Bacillus cereus, classified in hazard group 2 due to the ability of some strains to produce toxins that may be fatal (e.g. cereulide) (Andersson et al., Reference Andersson, Hakulinen, Honkalampi-Hämäläinen, Hoornstra, Lhuguenot, Mäki-Paakkanen, Savolainen, Severin, Stammati, Turco, Weber, von Wright, Zucco and Salkinoja-Salonen2007; Advisory Committee on Dangerous Pathogens, 2013).

Beyond B. subtilis, several species of this genus demonstrate great potential for probiotic use – e.g. Bacillus amyloliquefaciens (Wealleans et al., Reference Wealleans, Walsh, Romero and Ravindran2017), Bacillus licheniformis (Zhao et al., Reference Zhao, Zeng, Wang, Qing, Sun, Xin, Luo, Khalique, Pan, Shu, Jing and Ni2020), Bacillus megaterium (Deng et al., Reference Deng, Wang, Ma, Yu, Liu, Dai and Zhao2021), Bacillus pumilus (Elsabagh et al., Reference Elsabagh, Mohamed, Moustafa, Hamza, Farrag, Decamp, Dawood and Eltholth2018), and Bacillus toyonensis (Roos et al., Reference Roos, de Moraes, Sturbelle, Dummer, Fischer and Leite2018), which may suggest a wide range of directions for future research.

Can Propionibacterium be an effective probiotic?

The use of the genus Propionibacterium has not yet been fully investigated as a probiotic agent for animal production or human health. Propionibacterium are Gram-positive, non-motile, non-spore-forming, catalase-positive bacilli. They are recognized as either anaerobic or relatively anaerobic bacteria (Piwowarek et al., Reference Piwowarek, Lipińska, Hać-Szymańczuk, Kieliszek and Ścibisz2018). After the three-stage screening, two studies were included in the review.

Although not widely used as a probiotic, Nair et al. (Reference Nair, Vazhakkattu Thomas, Dewi, Noll, Brannon and Kollanoor Johny2019, Reference Nair, Vazhakkattu Thomas, Dewi, Brannon, Noll, Johnson, Cox and Kollanoor Johny2021) described the bioprotective effects of Propionibacterium freudenreichii freudenreichii against multidrug-resistant Salmonella Heidelberg in finishing turkeys, including reduction of caecal colonization and internal organ dissemination.

Hence, the research on Propionibacterium as probiotic agents has ample potential for growth. Due to the current limited use of Propionibacterium as a probiotic, the chance of adaptation and/or resistance of pathogenic bacteria is reduced, which may lead to the development of more efficient products.

Limits on the use of probiotics in animal production

Probiotics, although a viable and increasingly used option, can still promote some disadvantages to animal production (Table 6). After the three-stage screening, three studies were included in this review.

Table 6. Negative results reported on the research on probiotics in animal production

Some studies reviewing possible limitations to the use of probiotics are available in indexing databases, mainly reporting (1) worsening of dysbiosis in environments with a high degree of stress, (2) problems related to the dynamics of gastrointestinal microbial communities, (3) worsening of dysbiosis in immunocompromised groups, (4) excessive stimulation of the immune system, (5) increased costs related to production and storage of inputs and/or feed, and (5) sensory changes in the host. Some points also reported as problematic involved the different dose–response for each individual, in addition to the difference obtained in the effects, often observed in the same individual exposed to successive doses (Ayichew et al., Reference Ayichew, Belete, Alebachew, Tsehaye, Berhanu and Minwuyelet2017; Evivie et al., Reference Evivie, Huo, Igene and Bian2017; Amenyogbe et al., Reference Amenyogbe, Chen, Wang, Huang, Huang and Li2020; Zommiti et al., Reference Zommiti, Chikindas and Ferchichi2020).

However, it is worth mentioning that the results are still presented in a generic way. Several authors report the lack of depth in the safety of probiotics, mainly due to the lack of publications reporting negative results (Mehta, Reference Mehta2019) – only three articles reporting negative results were found for this review – which may reflect their undervaluation in high-impact journals. Although negative results do not generate the same scientific expectations as positive results, they still have importance, especially to guide new studies. Even with the issues mentioned, most researchers emphasized that probiotics remain one of the most viable options for reducing the use of antibiotics in animal production.

Conclusions and future perspectives

The use of probiotics is extremely widespread in animal production, with the use of Lactobacilli, Bacillus, and Pediococcus well characterized and largely investigated in the literature, in addition to certain species such as L. lactis and E. faecium. The Propionibacterium, Streptococcus, Bifidobacterium, and Leuconostoc genera, as well as other species of Lactococcus and Enterococcus, still need to be assessed to validate the potential abilities observed in exploratory studies.

With the gradual increase in food production demand, it is expected that the use of probiotics will also grow considering their positive association with the production indexes and the prevention of certain infectious diseases both in human and animal health. As an example, the great impact of probiotics on weight gain and mortality reduction in herds, in addition to the control of important pathogens, such as Salmonella and E. coli. In addition, studies involving combined applications and synergisms show great possibilities, being an open field for new research.

Few studies go beyond the in vitro stage and present benefits in animal health and production; in this review, only 84 articles were selected after a three-stage screening. Research in the area is advanced enough to extend in vitro studies and in vivo validation methods for transforming scientific findings into commercially viable technological innovations. Furthermore, research on the mechanism of action of probiotics must advance. Newly available techniques allow novel approaches to ensure more safety and efficacy in the use of probiotics.

Future studies focused on the use of neglected bacteria and the use of knowledge built over the past few decades about probiotics used in human health must be used for the development of new strategies and products for animal production. Partnerships between research centres and industries in the animal production sector are of paramount importance to enable the application of novel and safe technologies in the consumer market. With recent technological advances in all areas of biotechnology, probiotics are a thriving option for controlling pathogens in animal production and provide zootechnical gains, enabling a more sustainable production, allied to the principles of promoting animal health and welfare.

Author contributions

A. G. E., J. A. F. C., A. C. M. S. P., F. D. R. G.: conceptualization; investigation; writing – original draft. F. B. L.: conceptualization; writing – review and editing; supervision.

Funding statement

This work was supported by the National Council for Scientific and Technological Development, Brazil, processes CNPq 142196/2019-3, 437728/2018-8, and 308598/2020-2; the Coordination for the Improvement of Higher Education Personnel, Brazil, financial code CAPES 001 and 88887.512219/2020-00; and the Pontifical Catholic University of Paraná, Brazil.

Competing interests

None.

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Table 1. Use of Lactobacilli in animal production to improve zootechnical indexes and health parameters

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Table 2. Use of Enterococcus in animal production to improve zootechnical indexes and health parameters

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Table 3. Use of Lactococcus in animal production to improve zootechnical indexes and health parameters

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Table 4. Use of Pediococcus in animal production to improve zootechnical indexes and health parameters

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Table 5. Use of Bacillus in animal production to improve zootechnical indexes and health parameters

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Table 6. Negative results reported on the research on probiotics in animal production