P ro b i o t i c U s e i n E q u i n e

G a s t ro i n t e s t i n a l D i s e a s e
Angelika Schoster, DVM, Dr Med Vet, PD, DVSc, PhD

KEYWORDS
 Lactobacillus  Bifidobacterium  Saccharomyces boulardii  Microbiota
 Fecal microbial transplantation

KEY POINTS
 Mechanisms of action include modulation of the immune system, antimicrobial produc-
tion, bacterial toxin inactivation, and an increase in colonization resistance.
 Probiotics are generally considered safe, and adverse effects are rare; however, adverse
effects have been reported in foals and therefore should be used with caution.
 The quality control of commercial human and veterinary probiotics products is poor and
the content of over-the-counter probiotics is often inaccurate regarding bacterial species
and amount of live organisms contained in a product.
 The evidence behind efficacy of probiotics in equine gastrointestinal disease is weak and
their beneficial effects are questionable.
 Future research on the use of probiotics should focus on using different strains, such as
members of families with high abundance in the gastrointestinal system of horses, or a mix
of many bacterial strains, similar to fecal microbial transplantation.

INTRODUCTION

Elie Metchnikoff1 studied the longevity of a group of Bulgarians in the 1900s. He

observed that these people ate large amounts of fermented milk and postulated
that the bacteria responsible for fermentation had a positive effect on the health of
the consumers. These bacteria were named Lactobacillus bulgaricus and the idea
of probiotics was born. Metchnikoff initially defined probiotics as “live microorgan-
isms, which exhibit a health promoting effect” in 1908.1 Although research initially
flourished and more probiotic bacterial strains were discovered, it then drifted to
the fringe of medical practice and was rediscovered in the mid-1990s. The idea of pro-
biotics exerting beneficial effects has since re-entered the humane medical field and
achieved mainstream medical interest. The Food and Agricultural Organization and
World Health Organization modified the initial definition to “live microorganisms,

Vetsuisse Faculty, Equine Department, University of Zurich, Winterthurerstrasse 260, Zurich

8057, Switzerland
E-mail address: [email protected]

Vet Clin Equine 34 (2018) 13–24

https://doi.org/10.1016/j.cveq.2017.11.004 vetequine.theclinics.com
0749-0739/18/ª 2017 Elsevier Inc. All rights reserved.
14 Schoster

that when administered orally at adequate concentrations, provide a beneficial effect

beyond that of their nutritional value.”2

GENERAL CONSIDERATIONS

Information regarding probiotics is accumulating rapidly and is widely available on the

Internet and from various sources; thus, it is important to understand some practical
aspects regarding formulation and labeling of probiotics that make it challenging to
provide direct comparisons and interpret results of studies.
Several microorganisms, including yeasts and bacteria are used as probiotics
(Box 1). Some bacterial families, mainly lactic acid producers, such as lactobacilli
and bifidobacteria, are commonly used. Not all members of the same family have pro-
biotic properties; for example, not all lactobacilli are suitable for probiotic use. Lacto-
bacilli per se are often called probiotics or used as such, but not all lactobacilli have
probiotic properties; therefore, the administration of commercial yoghurts is unlikely
to be of benefit to the horse. Potential probiotic strains need to be evaluated for suit-
ability of their probiotic characteristics.3 Potential probiotic strains should be able to
survive the gastric environment, have antimicrobial properties, and adhere to mucus
and epithelial cells.2 Not all strains survive the extrusion and drying, which leads to
low numbers of active colonies in the end product. The manufacturing process affects
the ability of bacteria to maintain desirable traits. Manufacturing a probiotic strain un-
der different conditions, such as varying culture media or coculturing with prebiotics or
other probiotic strains, leads to expression of different traits and differences in the final
product.4,5 It is crucial to remember, when comparing results of commercial probiotic

Box 1
Bacterial genera and yeasts typically used as probiotics

Saccharomyces (yeast)a
Lactobacillusa
Bacteroides
Escherichia coli
Enterococcusa
Bacillusa
Nitrobacter
Nitrosomonas
Streptococcusa
Rhodobacter
Fusobacterium
Butyrivibrio
Rhodobacter
Clostridium
Eubacterium
Bifidobacteriuma

Genera are bacteria unless stated otherwise.

a
Evaluated as probiotics in horses.
 Probiotic Use in Equine Gastrointestinal Disease 15

product studies, that manufacturing methods matter and products containing the
same strain at the same concentration cannot be directly compared.
Most diseases of the gastrointestinal tract in horses affect the large intestine.
Accordingly, a probiotic used for horses should ideally exert effects in the cecum
and colon of horses. Recent advances in research have shown that the most
commonly used genera for probiotics, namely Lactobacillus spp, Bifidobacterium
spp, and Enterococcus spp are not the most abundant species in the large colon of
the hosts. In fact, these species constitute less than 1% of the large intestinal micro-
biota in healthy horses.6–8 In horses these bacteria are more abundant in the small
compared with the large intestine. In younger animals (less than two months), they
are more abundant independently of the gastrointestinal segment; however, still
have low abundance when taken into relation with other bacteria.6,8 The most abun-
dant phylum in the equine gastrointestinal tract is Firmicutes, which contains the class
of Clostridia. Important members of the Clostridia class, including Ruminococcaceae
and Lachnospiraceae, have consistently been associated with gastrointestinal health
in humans and animals, including horses.9–11 Lactobacilli and bifidobacteria are not
consistently associated with gastrointestinal health and might, therefore, have less in-
fluence on the gastrointestinal health of horses. To date, studies investigating effects
of members of the Clostridia class are lacking. These might have better effects than
currently available probiotic strains.
Studies in healthy animals are often used to assess the ability of a microorganism
to survive transit in the gastrointestinal tract and persist after cessation of adminis-
tration. Effective transit is defined as identification of probiotic microorganisms in
fecal material, as determined by bacterial culture or polymerase chain reaction
(PCR) assay. Identification of DNA with PCR does not imply viability, rather that a
microorganism was present in the probiotic and recognizable DNA sequences sur-
vived gastrointestinal passage. Some investigators presume that colonization of
the gastrointestinal tract with the probiotic strain is superior to mere effective transit
because probiotics could act beyond the period of administration. In vitro studies
have revealed, however, that effects of nonviable organism may be greater than
the effects of viable organism. Therefore, lack of viability or persistence does not
imply lack of effect.
Generally, host-specific strains are believed to be able to colonize the gastrointes-
tinal tract of the indigenous host for longer periods of time. Colonization of the adult
equine gastrointestinal tract with Lactobacillus rhamnosus LGG of human origin was
shown to be poor.12 After a 5-day course of probiotic administration at 3 different
dosages (1  109, 1  1010, and 5  1010 colony-forming units [CFUs]/g), fecal re-
covery in 21 adults was shown to be 71%, 29%, and 86% after 24 hours for each
dose, respectively. After 48 hours, the probiotic was recovered from the feces of
14%, 14%, and 56% of the total dose administered, respectively, whereas 3 days
after administration only one horse in each of the lower two dosage groups remained
positive. Fecal recovery was longer in foals, where the probiotic could be recovered
up to nine days after administration in some foals.12 This suggests that the immature
gastrointestinal flora of foals could facilitate probiotic survival.
As described previously, foals and adults showed a lack of dose response, making it
difficult to determine an ideal dose to use.12 Similar results were obtained when
administering Saccharomyces boulardii.13 After administration of 10  109 CFUs/g
to 3 horses and 20  109 CFUs/g to 2 horses for 10 days, fecal samples were negative
for S boulardii on day 20. On day five, all horses had viable S boulardii in their feces.13
Similarly, S cerevisiae has been shown to survive but not colonize the ceca and colons
of horses.14–16 This indicates that any beneficial effect of probiotics might not continue
16 Schoster

beyond the period of administration, making long-term or repeated treatment a

necessity.
To assess the effect of probiotics on the composition of the gastrointestinal micro-
biota, reduction of pathogens in vivo studies, in particular, have been conducted in
other animal species. Knowledge regarding composition and function of the micro-
biota is not fully understood. For example, enteric pathogens, such as Clostridium
difficile and Salmonella, can be isolated from feces of healthy animals17; therefore,
presence of presumed pathogenic organisms does not necessarily cause disease
and any attempt to reduce carriage might be ill advised. Recently, studies have shown
that microbiota diversity and certain members of the Clostridia class, such as Lachno-
spiraceae and Ruminococcaceae, are consistently associated with gastrointestinal
health.8,10,18 Maintaining diversity and increasing the abundance of these Clostridia
could be a potential target of probiotic development. In horses, to date only one study
has assessed the effect of probiotics on the composition of the microbiota in a small
number of foals. A significant effect was not seen.19

REGULATION OF COMMERCIAL PROBIOTICS AND QUALITY CONTROL

In North America (NA), most commercial probiotics are sold over the counter, without
published efficacy or safety studies or ongoing quality control. In the United States,
probiotics, also called direct-fed microbials, can be classified as a drug or as a dietary
or feed supplement. If classified as a drug, the product needs to be approved and un-
dergo quality control based on rules set forth by the Food and Drug Administration
(FDA). Currently there are no approved probiotic products classified as drugs for hors-
es in NA. If probiotics are classified as dietary or feed supplement, they fall under the
category, “generally regarded as safe (GRAS),” and do not need to go through FDA
drug-level approval. The FDA requires that supplements be labeled in a truthful and
not misleading manner. The producers just provide an expert opinion on why the prod-
uct should be considered GRAS and be approved by the FDA. The labels need to
contain information to identify the feed additive, its concentration, and details on its
safe and effective use. Claims that a feed additive can be used to cure, treat, or pre-
vent disease named expressed or implied care are not allowed. The Center for Veter-
inary Medicine of the FDA, however, permits the use of meaningful health information;
for example, “gastrointestinal health” claims on horse feed fall under this policy.
Consequently, in NA, there are numerous probiotic products for use in horses on
the market that can be obtained over the counter and claim to benefit the horse in
various ways. Peer-reviewed published studies proving the efficacy of these products,
however, are limited or in most cases lacking.
Even though the FDA regulates the labeling of probiotic products, many commercial
veterinary and human probiotic preparations are not accurately represented by label
claims. Studies evaluating labels of detailed contents of human and veterinary prod-
ucts showed that only 43% of human products and 8% of veterinary products from
Canada were adequately labeled. There were inadequate descriptions of the bacterial
content, including missing names, unspecified strains, nonexisting names, potentially
pathogenic genera (eg, Staphylococcus) and outdated names.20,21 Quality control of
the active ingredient of commercial probiotics is also poor. Only 15% of veterinary
and human probiotics contained the specified organism at the label claimed concen-
trations. Some products were missing organisms entirely or contained too little or too
much of an active ingredient (0%–215% of the claimed amounts). All veterinary prod-
ucts contained less than 2% of the listed concentration of bacteria.22 The effect of pro-
biotics in a clinical setting might, therefore, not be predictable due to inadequate and
 Probiotic Use in Equine Gastrointestinal Disease 17

inconsistent content of commercial probiotic formulations. Currently available pub-

lished or claimed results of studies are likely also affected by this poor quality control.
Commercial products used in research studies and evaluated as part of such, con-
tained up to 100 times less active ingredient than what was claimed on the label.23
The lack of effect seen in this particular study could be due to the inadequate content
of the product rather than actual lack of biological effect. Even when using specifically
designed (self-made) formulations, the content can be inadequate due to storage or
production issues, and should be evaluated.19

MECHANISMS OF ACTION OF PROBIOTICS

Proposed mechanisms for the effect of probiotics include modulation of the host im-
mune system, production of antimicrobial substances, inhibition or inactivation of bac-
terial toxins, displacement of pathogenic microorganisms (competitive exclusion),
improvement in micronutrient absorption, and improvement in epithelial barrier func-
tion (Fig. 1).
The local intestinal and general immune system, including innate and adaptive re-
sponses are influenced by probiotics.24 Conserved recognition receptors of the intes-
tinal epithelial cells (IECs) and gut-associated immune cells recognize probiotics, and
their metabolites, process them and evoke a signaling cascade. The effects include
maintenance and fortification of the intestinal barrier by maintaining tight junctions,
production of mucus, and survival and growth of IECs. This results in a stronger
mucosal barrier against invading pathogens. Furthermore, the gut associated
lymphoid follicles are presented with components of the probiotic strains by antigen
presenting cells and induce differentiating of B cells into plasma cells. As a result,
IgA, which is important for mucosal immunity, is released into the intestinal lumen

Fig. 1. Mechanism of action of probiotics. Green, probiotic; purple, pathogen.

18 Schoster

by plasma cells.25 The IgA and b-defensin, produced and released by IECs results in
suppression of growth of pathogens as well as systemic and local anti-inflammatory
effects.24 Probiotics also modify the cytokine production by IECs and cells of the
innate immune system, such as macrophages and dendritic cells, and therefore
show an anti-inflammatory effect.26 Systemically, probiotics can influence immuno-
globulin production by altering systemic immunoglobulin isotope profiles.27 Most of
these studies assessing the effects of probiotics on the host have been conducted us-
ing human or laboratory animal cell lines, but to date no similar studies for horses have
been published. Given the close conservation of the immune system across species, it
is likely that similar effects do occur in horses.
Some probiotic strains produce antimicrobial metabolites in large quantities. These
include fatty acids, lactic acid, and acetic acid. Other antimicrobial substances, such
as formic acids, free fatty acids, ammonia, hydrogen peroxide, diacetyl, bacteriolytic
enzymes, bacteriocins, antibiotics, and several undefined substances, are produced
in much smaller amounts.28
Competitive exclusion refers to the ability of probiotic strains to decrease the
amount of pathogens present in the intestinal lumen and their capacity to adhere to
epithelial cells. Probiotic strains adhere to epithelial cells, block receptors and in-
crease mucin production. Subsequently pathogens can no longer adhere or gain
entrance into epithelial cells.29 Additionally, probiotic strains occupy ecological niches
and compete for nutrients, thus making it more difficult for pathogenic bacteria to sur-
vive in the gastrointestinal lumen.
Toxins are important and well-described virulence factors for enteropathogenic
bacteria. Probiotics have been shown to inactivate toxins, reduce toxin production,
and sometimes render toxigenic enteropathogens nonpathogenic.30 The antitoxin
effect of some probiotics may be beneficial in positively managing infectious
diarrhea.

SAFETY OF PROBIOTICS

Adverse effects of probiotic administration have been rarely reported. In humans, the
few reports available describe extraintestinal infections rather than enteric disease.31
Fungaemia due to treatment with S boulardii has been reported in human neo-
nates.32 Whether this could be a problem in horses is unknown, because studies
with S boulardii in equine neonates have not been performed.33
Probiotics typically are used in individuals with enteric disease and adverse enteric
consequences might be hard to distinguish from the primary disease present. It is
reasonable to assume that the incidence of adverse events is very low, consistent
with the GRAS classification of probiotics. In adult horses, there are no published
reports of enteric disease after probiotic administration.12,34 Doses are generally
extrapolated from human recommendations and adjusted by weight.13,35 Even admin-
istration of up to three times the manufacturers’ recommended doses to healthy hors-
es did not result in any adverse effects.36 The effect of probiotics in horses with enteric
disease might differ from the effect in healthy horses, but no adverse clinical effects
have so far been reported in horses with gastrointestinal diseases either.13,33,36
Most investigators, therefore, consider probiotics safe to be used in healthy and
diseased adult horses.
The safety of probiotic use in foals has to be assessed independently of adults
because there are major differences in immune system function and gastrointestinal
microbiota composition between adults and foals.37 Particularly, during the first
month, the diversity is significantly decreased compared with older foals.38 Although
 Probiotic Use in Equine Gastrointestinal Disease 19

several published studies demonstrate safety of commercially available and self-made

probiotics in foals,34,39 there are also reports on adverse enteric effects.19,35 In both
cited studies a self-made probiotic was evaluated as a preventative measure for
neonatal diarrhea in a placebo-controlled trial. The treatment group showed increased
incidence of diarrhea and need for veterinary intervention in both studies.35,40
Although it is unclear why these foals developed diarrhea, the immature microbiota
of the foals could have allowed overgrowth of lactic acid bacteria, resulting in osmotic
imbalances and diarrhea. Alternatively, the probiotics could have changed the micro-
biota to allow for pathogen adhesion to epithelial cells. The microbiota remains rela-
tively stable in foals after two months of life but compared with adult horses
differences are still present38; therefore, probiotic administration to foals more than
two months old is less likely to result in severe side effects. Probiotics should be
used with caution in foals, and safety studies should be performed before a product
is administered.

CURRENT EVIDENCE FOR PROBIOTIC EFFICACY IN TREATMENT OR PREVENTION OF

EQUINE GASTROINTESTINAL DISEASE

Probiotics have been administered to adult horses with acute enteropathies and to
decrease Salmonella shedding. Although some studies have shown beneficial effects
of probiotics, other studies could not corroborate these results (Fig. 2).13,23,33,36,41–43
Overall, few studies are available, and these cannot be compared easily due to differ-
ences in study design, outcome parameters, and formulations used. Often one
outcome parameter was influenced positively, such as duration of diarrhea; however,
no effect on mortality or duration of hospitalization was seen. The more outcome pa-
rameters studied, the more likely significant effects are observed. Consequently, to
date, the overall evidence is weak. The effect of a probiotic in a specific clinical context
is likely unique to that context. The effect of a probiotic in horses with a specific dis-
ease cannot be extrapolated from results of studies in healthy horses or on horses with
another disease. Also, extrapolation from humans or other species should not be
done. Because clinical context is important, studies on the use of probiotics should
ideally define the study population (healthy horses, horses with a specific disease,
and so forth) and fully describe the probiotic (exact strain, dose, dosage regimen,
and manufacturing details).

Fig. 2. Summary of effects of probiotics on preventing or treating gastrointestinal disease in

horses.
20 Schoster

Use of Probiotics for Treatment of Acute Enterocolitis in Adult Horses

S boulardii has been used with equivocal results. In one randomized, blinded,
placebo-controlled clinical trial, horses receiving the probiotic had a shorter duration
of diarrhea and watery diarrhea but not loose feces.13 Despite this potential positive
effect, the results of this study must be interpreted with caution, because there was
no difference between the groups in relation to outcome, duration of hospitalization,
and recurrence of diarrhea. In addition to the confounding factor of additional treat-
ments, the number of cases was low, with only seven horses in each group.13 In the
second randomized placebo-controlled clinical trial involving 12 horses, no signifi-
cant differences were observed between groups for occurrence of normal fecal con-
sistency or cessation of watery diarrhea.33 Also, days to improvement in attitude,
resolution of leukopenia, appetite, normalization of heart rate, respiratory rate, and
temperature, length of stay in hospital, survival to discharge, and occurrence of sec-
ondary complications were not different between groups.33 Although this study was
influenced by fewer confounding factors and evaluated more clinical variables
compared with the previously cited study,13 the number of cases was low and
adjunct treatment was variable among horses, making interpretation of the results
more difficult. Although both studies investigated the same probiotic, they are diffi-
cult to compare due to a heterogeneous horse population and different inclusion
and outcome criteria. In summary, the evidence for an effect of S boulardii as an
adjunctive treatment of enterocolitis in horses is weak. Additional probiotic strains
have not been studied in adult horses with acute enterocolitis. Overall studies in
horses provided weak evidence for the use of probiotics.

Salmonella Infection and Shedding

In horses, the effect of probiotics on Salmonella shedding has been investigated but
results have been disappointing to date. No differences in Salmonella shedding rates,
prevalence of postoperative diarrhea, leukopenia, length of antimicrobial therapy,
and length of hospitalization were found between groups.36,41 The overall number
of horses shedding Salmonella was small, fecal samples were taken at irregular, arbi-
trary intervals, and, given that Salmonella shedding can be intermittent, some cases
might have been missed.23,44 These limitations could have influenced the results of
these study. In contrast, administration of a probiotic decreased the incidence of Sal-
monella shedding by 65% in another study, but the difference was not significant
(P 5 .19) due to low power of the study.23 In other species, it is known that the effect
of probiotics depends on the agent studied, and so far few probiotics have been
evaluated in horses. Additional studies are necessary before excluding the beneficial
effects of probiotics on Salmonella shedding in horses. There is currently little evi-
dence supporting the use of probiotics to decrease Salmonella shedding or salmo-
nellosis in horses.

Current Evidence for use of Probiotics in Foals

Probiotic administration has been studied as a preventative measure for foal diarrhea
in several studies with variable results (see Fig. 2).35,39,40,45,46 Probiotic administration
was associated with a significantly higher incidence of diarrhea, presence of clinical
signs (lethargy, fever, and anorexia colic) and the need for veterinary examination
and treatment in two studies.35,40 In another study, foals in the probiotic group showed
statistically significant larger weight gain after treatment and a significantly lower inci-
dence of diarrhea.39 These effects, however, were only significant at specific time
points. It is unlikely that the diarrhea was clinically important as evidenced by a lack
 Probiotic Use in Equine Gastrointestinal Disease 21

of difference in the need for medical intervention between the 2 groups. In a fourth
study on prevention of neonatal diarrhea in foals, a reduction of diarrhea incidence
by 60% could be achieved with probiotic administration.45 Although this result seems
promising, there were several limitations to this study, including unequal treatment
groups and inconsistent monitoring (every two weeks), which could have resulted in
oversight of many diarrhea episodes. Additionally it is unclear how often foals were
treated with the probiotic and the study was not blinded. In another study, Bacillus ce-
reus supplementation did not have an effect on incidence of diarrhea during the first
58 days of life in a study in 25 foals, irrespective of the dose used.46 These studies
cannot be directly compared because different products were used. In summary,
every probiotic product that is used in neonatal foals should be evaluated for safety
and efficacy before administration. Larger-scale controlled studies of different strains
and products are necessary before conclusions can be drawn on the clinical efficacy
of probiotics in foals with diarrhea.

FECAL MICROBIAL TRANSPLANTATION

All current probiotics consist of one or a few strains that comprise a minor component
of the intestinal microbiota. Therefore, they might have limited ability to influence the
entire gastrointestinal microbiota. Scientists and clinicians are now evaluating the
other end of the probiotic complexity spectrum, fecal transplants. Fecal transplants
consist of an intact, highly complex microbial community composed by thousands
of species. Fecal microbial transplantation constitutes the transfer a fecal suspension
from a healthy donor into the bowel of the recipient. Fecal microbial transplantation
has been shown to be highly effective in treating recurrent Clostridium difficile infec-
tions in humans. Although there are no published studies or abstracts in horses, anec-
dotal reports suggest that this form of therapy also might be effective in horses with
acute colitis or chronic diarrhea.47,48

SUMMARY

Although probiotics have shown promise in treatment of selected diseases in humans,

the evidence in horses is weak. For any given disease, only few probiotic organisms
have been evaluated so far and most studies were underpowered or confounded.
On the basis of examination of existing data, no specific product can be recommen-
ded for use. The aim of developing the one probiotic to aid in prevention or treatment
of all diseases is unrealistic. The choice and combination of strains for a therapeutic
formulation needs to be specific for each disease and should be based on the
in vitro properties of the strains and tested in clinical placebo controlled randomized
trials. Based on lack of regulation regarding quality control of commercial products,
use of over-the-counter products is questionable, particularly in the absence of scien-
tific information on safety and clinical efficacy. Probiotics likely have a different effect
in foals because the gastrointestinal microbiota transitions to the adult microbiota dur-
ing the first months of life. Adverse effects have been reported in foals and probiotics
should be evaluated for safety before use in foals. Despite all these limitations, probi-
otics generally are regarded as safe, and easy to administer. Therefore, additional
research is warranted to test possible applications in equine veterinary practice.
Exploiting new knowledge of the composition of the equine microbiota, the focus of
probiotic research should shift from currently used agents to species that are abun-
dant in the intestinal microbiota of the horse. By combining microbiota research,
research on fecal microbial transplantation and probiotic research, a designer probi-
otic containing all beneficial microbes could eventually be developed.
22 Schoster

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