Anaerobe 34 (2015) 14e23

Contents lists available at ScienceDirect

Anaerobe
journal homepage: www.elsevier.com/locate/anaerobe

Microbiota and probiotics in canine and feline welfare

Łukasz Grze
skowiak a, *, Akihito Endo b, Shea Beasley c, Seppo Salminen a
a
Functional Foods Forum, Univeristy of Turku, Turku, Finland
b
Department of Food and Cosmetic Science, Faculty of Bioindustry, Tokyo University of Agriculture, Hokkaido, Japan
c €ntsa
Vetcare Ltd., Ma € la
€, Finland

a r t i c l e i n f o a b s t r a c t

Article history: Dogs and cats have been cohabiting with us for thousands of years. They are the major human com-
Received 3 January 2015 panions. Today, dogs and cats live in urban areas. Cats and most dogs are on high carbohydrate diets and
Received in revised form face similar life-style challenges as the human beings. The health and well-being of companion animals,
2 April 2015
just as their owners, depends on the gut microbes. Providing a proper care and nutritionally balanced
Accepted 5 April 2015
Available online 8 April 2015
diet to companion animals is recognised as a part of our responsibility to maintain the health and well
being of our pet. However, as microbiota differences may facilitate exposure to pathogens and harmful
environmental influences, it is prudent to search for novel tools to protect dogs and cats and at the same
Keywords:
Dog
time the human owners from pathogens. Specific probiotic strains and/or their defined combinations
Cat may be useful in the canine and feline nutrition, therapy, and care. Probiotic supplementations have been
Gut microbiota successful in the prevention and treatment of acute gastroenteritis, treatment of IBD, and prevention of
Probiotic allergy in companion animals. New challenges for probiotic applications include maintenance of obesity
Prebiotic and overweight, urogenital tract infections, Helicobacter gastritis and parasitic infections. The probiotics
Veterinary care of human origin appear to be among the new promising tools for the maintenance of pets' health.
Health However, the host-derived microorganisms might be the most appropriate probiotic source. Therefore,
more controlled trials are needed to characterise new and safe probiotic preparations with an impact on
general health and well being as well as health maintenance in dogs and cats.
© 2015 Elsevier Ltd. All rights reserved.

1. Introduction composition and activity have been associated with several dis-
eases in both the animals and their owners [4e6]. This interrela-
Pet population is increasing especially in westernised countries, tionship would benefit from more exact knowledge on microbiota
and dogs and cats are the major human companions. Both have in pets and information on how the microbiota affects the health of
been domesticated and are co-existing with humans for thousands the pets in the long-term.
of years. Most of pet owners consider the animals to be family A major part of the animal health derives from the intestine. The
members, and other consider their pet as companions [1]. Domestic ‘healthy gut’ is known to be crucial for the physiology and well
dogs and cats still live in conjuction with humans benefiting from being of the host. The gastrointestinal tract (GIT) harbours a com-
each other. Mutual interest has evolved into companion animals plex microbial community. This microbial ecosystem acts in several
being a stable part of human life and therefore, the health and well ways, affecting both absorption and metabolism of nutrients, tro-
being of pets have increasingly raised interest during last decades. phic and protective functions of the host. Any disturbances within
Dogs and cats are carnivores with a history of high protein diets the gut microbiota may lead to the development of a multitude of
[2,3]. Today, cats and most dogs are on high carbohydrate diets diseases and disorders e.g. diarrhoea, allergies, obesity, and stress
living in urban areas and thus face similar life-style challenges as symptoms [5].
the human beings. The health and well-being of companion ani- Knowledge on the canine and feline intestinal microbiota is still
mals, just as their owners, depends on the gut microbes. Microbiota expanding. Most studies on microbial community in the dog and
cat GIT implemented in traditional microbiological techniques,
however several recent reports characterised microbiota using
* Corresponding author. Functional Foods Forum, Univeristy of Turku, Itainen novel molecular methods such as qPCR, FISH or 16S rRNA
Pitkakatu 4 A, 20014 Turku, Finland. sequencing [7,8]. To balance the disturbed microbiota and to
E-mail address: [email protected] (Ł. Grze
skowiak).

http://dx.doi.org/10.1016/j.anaerobe.2015.04.002
1075-9964/© 2015 Elsevier Ltd. All rights reserved.
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skowiak et al. / Anaerobe 34 (2015) 14e23 15

combat infections, different therapeutic agents have been pro- (1.3%), and Actinobacteria (0.6%) low [22].
posed, among them probiotics. However, published papers on Feline faeces have been found to contain high numbers of
probiotic applications in companion animals are greatly limited obligate anaerobes, and such quantities are considered abnormal in
compared to data regarding humans. The aim of this review is to dogs and humans [23]. Based on the analysis of 16S rRNA, it was
describe the current knowledge on the gut microbial community reported that the feline GIT is often represented by five phyla where
and advances in probiotic therapy in dogs and cats. Firmicutes dominate (68%), followed by Proteobacteria (14%), Bac-
teroidetes (10%), Fusobacteria (5%), and Actinobacteria (4%), [15].
2. Canine and feline microbiota However, a more recent study using the metagenomic approach
revealed that the feline gut microbiota is predominated by Bac-
All animals harbour a vast and complex community of mi- teroidetes/Chlorobi group bacterial phylum comprising around 68%
croorganisms. Dogs and cats have high numbers of microor- of total classified diversity and followed by Firmicutes (~13%) and
ganisms in the GIT which in fact outnumber those living in Proteobacteria (~6%) respectively, while known Archaea, fungi
human gut. However, both dogs and cats have distinct bacterial (Ascomycota), and viruses represent minor communities in the
species that differ between each other and also vary in different overall microbial diversity [10,24]. Minamoto and collaborators
dog and cat species, various gut niches and geographical areas. [25] summarised the studies on feline small and large intestine
Microbial diversity and concentration increase along the length microbiota showing in detail microbiota to genus level. Most
of the gastrointestinal tract. The predominant bacterial phyla in studies have been conducted in shorthair cats [8] which leaves
the colon and faeces of both dogs and cats are represented by much of the microbiota of other pet cats in different breeds to be
Firmicutes, Bacteroidetes, Proteobacteria, and Fusobacteria as well studied more in detail. Thus, the composition appears to be
as Eubacterium in cats. The microbial differences between dogs distinctly different from both canine and human studies. Since
and cats are demonstrated in the microbial groups and species different techniques may create bias from one report to another and
levels. Molecular fingerprinting has also revealed that every the result, more studies are needed to uncover the details of vari-
individual pet has a unique and stable microbial ecosystem [9]. ation within the canine and feline community and also between
Molecular analysis using 16S rRNA sequencing revealed that individual animals.
Firmicutes, Fusobacteria, Bacteroidetes, and Proteobacteria An increasing numbers of reports have changed the old dogma
commonly inhabit the canine GIT [7,10]. Clostridia predominate in suggesting initiation of microbiota development at birth. These
the duodenum and jejunum and are highly abundant in the ileum reports clearly demonstrate that humans and mice are colonised by
and colon [11], while Fusobacteria and Bacteroides bacteria are the microbiota already in utero and prior to birth [26,27]. There are no
most abundant in the ileum and colon [7,11]. Fungi, such as Asco- studies on canine and feline microbial colonisation prior to de-
mycota, Basidiomycota, Glomeromycota, and Zygomycota have been livery, however similar possibilities cannot be excluded since both
identified as well [10]. are mammals and share similar physiological and some anatomical
Lactobacilli inhabit commonly all parts of the dog intestine [11], patterns with humans.
ranging from 104 to 108 CFU/ml and among them Lactobacillus ac- The skin microbiota plays an important role in skin function,
idophilus is dominant [12]. Lactobacillus fermentum, Lactobacillus potentially enhancing the skin barrier and reducing the colonisa-
rhamnosus, and Lactobacillus salivarius are reported being a part of tion by potentially pathogenic microorganisms. One recent study
health canine intestine [13]. Other canine lactobacilli are repre- using pyrosequencing demonstrated that canine skin is inhabited
sented by Lactobacillus murinus and Lactobacillus reuteri [12], by rich and diverse microbial communities. Healthy dogs have high
Lactobacillus animalis, Lactobacillus sanfranciscensis and Lactoba- individual microbial variation between samples collected from
cillus paraplantarum [14]. different skin sites. Also higher species richness and microbial di-
Lactobacilli found in cats are typical intestinal lactobacilli, e.g. versity are observed in the samples from haired skin when
L. acidophilus, L. salivarius, Lactobacillus johnsonii, L. reuteri and compared to mucosal surfaces or muco-cutaneous junctions. The
Lactobacillus sakei, which can be seen in other animals, including most abundant phyla and families identified in the different regions
human [15]. However, Lactobacillus distribution, similar to bifido- of skin and mucosal surfaces are members of Proteobacteria and
bacteria, varies between individuals. Oxalobacteriaceae. On the other hand, the skin of allergic dogs is
Bifidobacteria have been difficult to characterise using pyrose- characterised by lower species richness when compared to the
quencing due to methodological difficulties, although the micro- healthy dogs, with lower proportions of the b-Proteobacteria Ral-
organisms are well known to be beneficial in several animals and stonia [28].
especially in human infants. Jia and collaborators reported that The composition of canine and feline microbiota is shown in
dogs contain over 108 cells/g of bifidobacteria in their faeces, as Fig. 1a, b.
determined by fluorescence in situ hybridisation (FISH) [8]. This is
consistent with the reports studied by culturing [16,17]. Both ani- 3. Microbial interaction between pets and owners e is there a
mal type (e.g. Bifidobacterium pseudolongum and Bifidobacterium connection?
animalis) and human type (e.g. Bifidobacterium catenulatum and
Bifidobacterium bifidum) of bifidobacteria have been found in dog Gastrointestinal disorders are one of the main reasons owners
faeces [18e20]. Bifidobacteria were major proportions in healthy bring their pets to the veterinarian for healthcare. In addition,
cats with cell number of 9.34 (log10 cells/g faeces), as determined specific bacterial canine enteropathogens such as Salmonella and
by FISH. Significantly lower numbers of bifidobacteria have been Campylobacter are well-documented zoonoses [4,29] being a chal-
found in cats with IBD [21]. Ritchie and co-workers [15] found lenge for pet owners, veterinary and medical care. Dogs may
several human-type and animal-type bifidobacteria in cats using harbour and shed cysts of protozoan parasite Giardia lamblia
clone library combined with Bifidobacterium group-specific primer without showing clinical signs [30] and ascariasis. Both are com-
set. They have also found that individual cats contained several mon potentially zoonotic diseases leading to human infections [31].
unique Bifidobacterium species. The enteric zoonotic agents in domestic cats are also important. A
A study on pet cat oral microbiota indicated Proteobacteria being study by Tun and collaborators [24] identified a range of potential
dominating (75.2%) leaving amounts of Bacteroides (9.3%), Firmi- enteric zoonotic pathogens (0.02e1.25%) and genes involved in
cutes (6.7%), unculturable (2.7%), Spirochaetes (1.8%), Fusobacteria antimicrobial resistance (0.02e0.7%) in feline excrements which
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skowiak et al. / Anaerobe 34 (2015) 14e23

Fig. 1. The canine (a) and feline (b) gastrointestinal tract and its dominant microorganisms. Skin microbiota included.

highlight the potential for transmission of opportunistic infections needs of companion animals. Well made feeds offer a good source
to human. of all necessary nutrients, vitamins, minerals, and other compo-
Recent studies on pet and human microbial interaction nents when feed quality is adequate. Often, canine and feline feed
demonstrate that having a dog at home increases the shared skin preparations are enriched with probiotics offering a microbiota
microbiota between cohabiting adults. In addition, dog-owners modulating and well-being targeted functional feeds.
adults share more ‘skin’ microbiota with their own dogs than A pilot study involving five beagle dogs fed different diets
with other dogs [32]. Studies suggest that exposure of infants to revealed that high-carbohydrate starch based feed leads to
farm animals is associated with a decreased risk of development of decrease in faecal ammonia. On the other hand, high-protein
asthma later in life [33]. Finally, it has been demonstrated that greaves-meals (a by-product which is produced when melting
perinatal pet exposure affects the compositional differences in the raw fat from e.g. pigs), commonly thought as low-grade meat meal,
gut microbiota and protects children from early wheezing [34]. lead to higher pH, decrease in propionic and acetic acids and in-
Reverse zoonotic occurrence has been acknowleged lately and crease in branched-chain fatty acids and valeric acid and changes in
could be interpered throughout microbiotal exchange in human- faecal total volatile fatty acids, higher faecal canine calprotectin
eanimal relationship [35]. concentration which was associated with increased valeric acid
concentration. In addition, all studied dogs fed high-protein
4. Effect of diet on microbiota greaves-meals developed diarrhoea [36].

The nutritional composition and contents of feed is known to 4.1. Prebiotics in canine and feline nutrition
significantly influence gastrointestinal function, microbiota
composition and their metabolic products in the animal gut. Only a few studies have been reported on prebiotics and canine
Companion animal diets have been evolving from hunted food and feeds suggesting that dogs may benefit from the addition of pre-
table scraps to scientifically and nutritionally balanced target biotics to their diet. Healthy dogs fed a diet supplemented with
formulated foods. Table scraps do not fulfil the basic metabolic chicory, a fermentable oligosaccharide, demonstrate firmer faecal
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skowiak et al. / Anaerobe 34 (2015) 14e23 17

consistency, a lower faecal pH, and increased levels of bifidobac- 5. Probiotics for dogs and cats
teria and decreased Clostridium perfringens counts in their stools as
compared to animals on a protein-rich diet [37]. On the contrary, Antibiotics used commonly to treat certain diseases can reduce
feeding dogs with low level of dietary fibre (beet pulp), 7.5 g/day for the population of beneficial bacteria and increase the levels of
2 weeks leads to decrease in Fusobacteria and increase in Firmicutes potentially harmful microorganisms and also lead to antimicrobial
[38]. resistance [49,50]. In addition, antibiotic therapy has been shown
New types of prebiotics are being constantly developed and to have a long-term effect on intestinal microbiota [51,52]. Mi-
they seem to be a promising additive in animal feed. The con- crobes with antimicrobial multiresistancy, such as ampicillin- and
sumption of new fermentable prebiotic polydextrose by dogs was tetracycline-resistant enterococci, may transfer from pets to pet
reported to increase faecal acetate, propionate and total SCFA owners occuring even in hospital infections [49,53,54]. An experi-
concentrations, while it decreased faecal pH and indole. In mental study evaluating the effect of macrolide antibiotic tylosin on
addition, faecal C. perfringens decreased but Escherichia coli, lac- microbial diversity in the canine small intestine using 16S rRNA
tobacilli and bifidobacteria remained unaffected in animals [39]. gene sequencing revealed decrease of Fusobacteria, Bacteroidales
Clearly, more extensive research should be conducted to provide and Moraxella, while the proportions of Enterococcus-like bacteria,
detailed coverage of the canine microbiome, to assess the effects Pasteurella, Dietzia, and Escherichia increased. Microorganisms
of age, genetic background or food environment on its compo- belonging to Spirochaetes, Streptomycetaceae, and Prevotellaceae
sition and activity. Such studies would provide a better under- were undetectable at the end of antibiotic challenge [55].
standing on the associations between intestinal microbiota and The origin of probiotics forms the basis to prevent and treat
disease and provide new possibilities of modulating the health of various disorders and diseases in farm animals. Recently, probiotic
dogs through diet. products aimed for pets, especially dogs and cats, have also gained
Feline diet which is characterised by high-animal-protein sup- popularity among their owners as science provides the first prod-
plemented by low-carbohydrate plant-based additives has been ucts with proven efficacy. Therefore, supplementing animal diet
found to favour the growth of faecal Clostridium, Faecalibacterium, with defined and undefined probiotics [56] seems to be an essential
Ruminococcus, Blautia, and Eubacterium in kittens, and affect way to help maintain and promote the optimal GIT health and well-
circulating hormones and metabolites that may be important in being of pets as companion animals.
terms of satiety and host metabolism. On the other hand, kittens Probiotic is defined as ‘live microorganism which when
fed with moderate-protein, moderate-carbohydrate diets, contain administered in adequate amounts confers a health benefit on the
greater amounts of faecal Actinobacteria, Dialister, Acidaminococcus, host’ [57]. The definition has been recently reformulated by an
Bifidobacterium, Megasphaera, and Mitsuokella, as well as lower international consensus panel and also different product classes
amounts of Fusobacteria and such changes may have a beneficial have been included [56]. The majority of probiotic strains for
effect on gut health [40]. Similarly, earlier study found that cats fed humans and animals belong to lactic acid bacteria (LAB) and for
diet containing high protein concentration show lower bifido- humans bifidobacteria [58]. There are several possible modes of
bacterial and higher C. perfringens counts as compared to animals action of probiotics on the host and they include: production of
fed moderate-protein diet [41]. antibacterial compounds, competition for nutrients and adhesion
Addition of prebiotics to feline diet may positively affect gut sites with potential pathogens, alteration of microbial metabolism,
microbial populations. Cats fed diet supplemented with FOS (4% stimulation of immunity among the others [59,60]. Possible bene-
of diet) had increased bifidobacterial concentrations while fits of the probiotic use in pets include: modulation of the immune
counts of E. coli decreased. Presence of pectins (4% of diet) in system, help in stress maintenance, protection from infections
feline diet increased C. perfringens and lactobacilli concentra- caused by enteropathogens, increased growth and development,
tions. These studies also suggest that while the cat is a carnivore, control of allergic disorders and recently also obesity (Fig. 2).
its gut microbiota is similar to omnivores in microbial phylogeny
[42e44]. 6. Origin of probiotics, survival in GIT and effect on
Thus, incorporating prebiotics in pets diet may beneficially microbiota
modulate gut microbiota and intestinal health and possibly protect
the animals from enteric infections. The probiotic characteristics of microorganisms are linked to
host specificity [61]. Thus, for successful use as a probiotic, the
bacterial species should be of host intestinal origin. Unfortunately,
4.2. Obesity and overweight in companion animals e a global issue most of the probiotics for companion animals are not originally
derived from the canine or feline GIT microbiota. The canine and
Obesity and overweight are major health problems in humans as feline intestine is, however, rich in microorganisms with probiotic
well as in pets. Inappropriate and high-caloric diet, sedentary potential [14]. In addition, few studies have been published on the
lifestyle and limited physical activity in urbanised pets are only few quality of probiotic products for pets and probiotic survival through
factors that lead to overweight in companion animals. the GIT.
Recent studies demonstrate that around 38% of dogs are over- Even though lactobacilli form a small part of the canine GIT
weight [45]. The prevalence of canine obesity is estimated to be 39% microbiome, they are wide spread, and several isolated LAB strains
in France [46] and 50% in the UK [47]. A recent study on the including Lactobacillus species demonstrate in vitro antimicrobial
microbiota in obese dogs revealed that the phylum Actinobacteria activity [13,14,62,63] and survive in and dominate the small-
and the genus Roseburia were significantly more abundant in obese intestinal LAB microbiota during feeding and have the ability to
dogs compared to lean animals [48]. Clearly more studies are modify the intestinal microecosystem [64]. Further, three canine
needed to reveal the microbial composition and activity associated lactobacilli, L. fermentum VET9A, Lactobacillus plantarum VET14A, L.
with overweight and the shifts in microbial community structure in rhamnosus VET16A and their mixture demonstrated good adhesion
canine obesity. ability to canine intestinal mucus and were able to exclude the
The problem of obesity also affects cats. However, to our adhesion of common enteropathogens (Enterococcus canis,
knowledge, no studies on microbiota in obese cats have been C. perfringens, Salmonella enterica ser. Typhimurium) from the
conducted. canine intestinal mucus in vitro [65,66]. Thus, specific LAB including
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Fig. 2. Documented health benefits and new challenges of probiotics in companion animal health.

lactobacilli may serve as potential probiotics for canine use. salts, and demonstrated strong auto-aggregation activity [18]. Thus,
A new potential probiotic L. fermentum AD1 strain isolated from these could be further tested as a potential novel probiotics for
canine faeces expressed in vitro survival by pH 3.0 after 3 h (86.8% dogs.
survival) and in the presence of 1% bile (75.4% survival). The strain Similar studies were performed in 15 healthy adult cats. The
adhered to the canine intestinal mucus. Given to 15 healthy animals probiotic strain L. acidophilus DSM13241 given at a dose of
for 7 days at a dose of 109 CFU/mL, it increased faecal lactobacilli 2
108 CFU/d for 4.5 weeks was able to alter the balance of
and enterococci levels in the canine faeces [67]. Also a canine- gastrointestinal microbiota by increasing numbers of lactobacilli
originated probiotic strain Enterococcus faecium EE3 administered and decreasing clostridia and Enterococcus faecalis microbiota. In
for 1 week to 11 healthy dogs at a dose of 109 CFU/mL was able to addition, the probiotic administration decreased faecal pH, plasma
survive the GIT passage and persisted in faeces for 3 months after endotoxin concentrations and resulted in systemic and immuno-
cessation of its administration at a level of 6.83 ± 0.95 log CFU/g. modulatory changes in treated cats [74]. Thus, L. acidophilus
This strain was able to decrease staphylococci and Pseudomonas- DSM13241 probiotic may have the potential to improve intestinal
like bacteria and increase concentration of other LAB while E. coli health in cats.
levels remained unaffected [68]. The present results call for further studies on the probiotic po-
In a study evaluating the quality of L. acidophilus DSM13241 as a tential of canine and feline microbiota including some human-
feed additive (109 CFU/mL for 4 weeks) to healthy adult dogs, the originated strains.
probiotic was found to be stable in dry feed. It also survived transit
through the canine GIT, increased numbers of lactobacilli and 6.1. Probiotic effect on the immune system
decreased clostridia in faeces, and resulted in improved blood and
immune parameters [69]. In addition, a canine originated L. ani- The effect of a probiotic administration on the canine immune
malis LA4 (10 day study with a daily dose of 0.5
109 CFU) as well system has little been studied. Several reports show that a dietary
as B. animalis AHC7 (a six-week trial with a daily dose of probiotics enhance specific immune functions in young dogs.
1.5
109 CFU) have been reported to reduce Clostridium difficile The administration of E. faecium SF68 (5
108 CFU/d) to dry dog
count in dogs [70,71]. feed in 14 growing puppies (from weaning to one year of age)
A study evaluating the ability of L. rhamnosus GG (LGG) to sur- demonstrated adjuvant effect at both mucosal and systemic levels,
vive gastrointestinal transit in dogs demonstrated that the LGG which could be relevant for improving protective immune re-
recovery after discontinuation of a probiotic administration was sponses against various infections during the critical weaning
dose dependent. LGG given at the dose of 5
1011 CFU per day was period as well as at later stages in life [75].
still recovered 4 days after cessation of administration. Also no side A symbiotic containing 5
109 CFU of a mixture of seven pro-
effects of the LGG administration were found [72]. biotic strains (E. faecium NCIMB 30183, Streptococcus salivarus ssp.
In a study conducted on healthy dogs, the 18-day application of thermophilus NCIMB 30189, Bifidobacterium longum NCIMB 30179,
the probiotic E. faecium NCIB 10415 at a dose of 9.2
109 CFU L. acidophilus NCIMB 30184, Lactobacillus casei ssp. rhamnosus
increased counts of Salmonella and Campylobacter while clostridial NCIMB 30188, L. plantarum NCIMB 30187, Lactobacillus delbrueckii
levels were significantly reduced [73]. Thus, the effect of novel ssp. bulgaricus NCIMB 30186) and a blend of fructooligosaccharides
probiotics should be tested with caution. and arabinogalactans, administered daily for three weeks in
Canine GIT microbiota may also be a source of bifidobacteria healthy dogs and cats, resulted in increased abundance of Entero-
with a probiotic potential. New canine (from 14 healthy German coccus and Streptococcus spp. during administration. There were no
Shepherd Dogs) isolates of B. animalis ssp. lactis survived in the changes in the major bacterial phyla as identified by 454-
simulated in vitro digestion assay, were resistant to low pH and bile pyrosequencing. In addition, no adverse gastrointestinal effects
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skowiak et al. / Anaerobe 34 (2015) 14e23 19

were recorded and no significant changes in gastrointestinal probiotic had decreased episodes of diarrhoea as compared to
function or immune markers were observed during the study placebo group. However, the probiotic had no effect on the inci-
period [76]. The study suggested that specific synbiotic adminis- dence of diarrhoea in dogs [83]. The probiotic action could thus be
tration is safe for dogs and cats. The lack of potential effect on gut related to specific animal target species.
function and immune markers may have resulted from too short, Probiotic supplementation including two lyophilised L. aci-
only 3-week period of probiotic trial. dophilus (NCC2628 and NCC2766) and one lyophilised L. johnsonii
Just as humans, dogs may suffer from a variety of allergic dis- (NCC2667) (1010 CFU/g of each strain) one gram a day following
eases. Although specific probiotics appear useful in prevention and specific diet for four weeks in 21 dogs with food responsive diar-
treatment of allergic diseases in humans, the studies on pets are rhoea resulted in beneficial effects on intestinal cytokine patterns
limited. The L. rhamnosus strain GG (LGG) was used for the allevi- and on microbiota, diminishing numbers of enterobacteria and
ation or prevention of clinical signs of atopic dermatitis in geneti- increasing lactobacilli in faeces. The probiotic treatment resulted in
cally predisposed dogs. The study found that early exposure of clinical improvement in all dogs [84].
puppies to LGG appeared to reduce immunologic indicators of Other study reported that German Shorthair Pointers dogs with
atopic dermatitis, significantly decreasing allergen-specific IgE in non-specific dietary sensitivity (NSS) receiving probiotic
the first 6 months of life [77], and the positive effect was seen 3 L. acidophilus strain DSM13241, showed improved faecal consis-
years after discontinuation of probiotic administration [78]. tency, faecal dry matter and defecation frequency as compared to a
control group. In addition, faecal concentrations of culturable lac-
6.2. Probiotics and clinical chemistry parameters tobacilli and bifidobacteria had a tendency to increase while the
numbers of C. perfringens and Escherichia spp. had a tendency to
Although this is not an issue in canine and feline health, pro- decrease in a group receiving the probiotic [85].
biotics have a potential in controlling the lipid and protein level in Dogs and cats are known to be a reservoir of Helicobacter-like
companion animals. A canine strain E. faecium EE3 administered bacteria. These microorganisms reside in the stomach and occa-
(109 CFU/mL) daily (2e3 mL) to 11 healthy dogs for a period of one sionaly in the mouth of the pets [86e88] form where they could
week was able to reduce total lipids and proteins and the choles- easily be transferred to humans through sniffing and licking
terol was brought to the physiological level, i.e. in blood samples behaviour of the animals. Suchodolski et al. [9] reported mucosa-
with low cholesterol values it increased to the physiological level adherent Helicobacter sp. being the main founding in the canine
and in those with high levels it decreased [68]. On the other hand, stomach. The presence of Helicobacter spp. has been associated
another canine-originated potential probiotic strain L. fermentum with gastritis in dogs and cats [89]. The only treatment is a ‘triple
AD1 (109 CFU/mL) given daily (3 mL) to 15 healthy dogs for one therapy’ composed of two antibiotics and a proton-pump inhibitor
week increased the total protein and total lipid and reduced glucose [90] but at least in humans this therapy is not always successful and
in serum of studied dogs [67]. Strompfova
et al. [79] demonstrated new alternatives are being developed [91]. Some probiotic strains,
that canine-derived strain B. animalis B/12 (109 CFU) increased such as L. casei DN-114 001, showed a high success rate of eradi-
organic acid levels in faeces and reduced triglyceride and albumin cation of Helicobacter in children(along with a standard treatment)
concentration in blood serum. Phagocytic activity of leucocytes at a high daily dosage of 1
1010 CFU [92]. Thus, probiotics could be
increased as well. A greater effort is needed to uncover any physi- a promising tool to combat Helicobacter infections in dogs and cats.
ological effects of the biochemical profiles observed and their
impact on dogs health. 6.4. Probiotic effect on inflammatory bowel diseases

6.3. Probiotic effect on gut health Dogs and cats may be challenged with inflammatory bowel
diseases (IBD). The clinical symptoms of IBD include vomiting,
Acute gastroenteritis is a common disorder in small animal diarrhoea, weight loss, and histopathologic lesions of inflammation
practice and a disturbance faced often by dog and cat owners. It that involves stomach, small intestine, or colon [93]. Dogs with IBD
may result from inadequate feeding practices, feed-borne patho- present dysbiosis of gut microbiota. Specific bacterial genera within
gens or specific nutrient sensitivity among other non-nutrient and Proteobacteria, including Diaphorobacter and Acinetobacter are
sometimes also unknown factors. Probiotics seem to be promising more abundant and more frequently found in the colon of IBD dogs,
tool in alleviating gastrointestinal illnesses in pets. while proportions of Fusobacteria, Bacteroidaceae, Prevotellaceae,
The probiotic cocktail consisting of thermo-stabilised 2.85 bil- and Clostridiales are found more abundant in healthy dogs [94].
lions live Lactobacillus farciminis (porcine origin), Pediococcus Also the small intestinal microbial communities of IBD dogs differ
acidilactici (unknown origin), Bacillus subtilis (soil origin) and Ba- from that of the healthy animals. The inflamed duodenum in IBD
cillus licheniformis (soil origin) and 1.35 billions L. acidophilus MA dogs is enriched with enterobacteria and clostridia but depleted in
64/4E (human origin), significantly reduced the convalescence time Bacteroides and lacks Spirochaetes [95].
(1.3 days in probiotic group vs. 2.2 days in placebo group) in acute Animals showing severe disease symptoms are usually treated
self-limiting gastroenteritis in 36 dogs [80]. with both dietary and pharmacologic interventions such as
Discussion could be raised on the safety of Bacillus sp. as feed immunosuppressive drugs, and elimination diet, as well as thera-
additives to cats and dogs since both pets are human companions peutic manipulation of the enteric microbiota through the use of
and the bacteria could easily be transferred from animal to human antibiotics and or prebiotic supplements [93,96]. Since probiotics
during the feeding, for instance. Particularly, B. licheniformis has are capable of altering the microbiota and immune responses in the
been reported to be fatal to newborn infants [81] and B. subtilis an gut, they seem to be promising future tools for IBD risk reduction
opportunistic pathogen [82]. Further studies are needed on the and nutritional therapy.
safety concern of Bacillus probiotics for pets use. Only one study evaluated the probiotic effect in IBD treatment in
Diarrhoeal diseases among dogs and cats are common in animal dogs so far. Twenty dogs with IBD were treated with either a
shelters, due to animal exposition on stress, diet change, and spread combination therapy (prednisone and metronidazole) or probiotic
of bacterial, viral, and parasitic agents. A study evaluating the effect VSL#3 (a mixture of strains belonging to species L. plantarum, L.
of E. faecium SF68 (2.1
109 CFU/g), on the incidence of diarrhoea in delbrueckii subsp. bulgaricus, L. casei, L. acidophilus, Bifidobacterium
sheltered 182 dogs and 217 cats demonstrated that cats fed the breve, B. longum, Bifidobacterium infantis, and Streptococcus
20 Ł. Grze
skowiak et al. / Anaerobe 34 (2015) 14e23

salivarius subsp. thermophilus) (112e225
109 CFU/10 kg) for 60 to assess e.g. whether the probiotic supplement could have a pro-
days. A protective effect of probiotic VSL#3 significantly decreased tective role against pyometra and other vaginal infections in dogs.
clinical and histological scores and decreased CD3þ T-cell infiltra-
tion in dogs with IBD. Probiotic-treated group demonstrated sig- 7. Safety issues with canine and feline probiotics
nificant enhancement of regulatory T-cell markers (FoxP3þ and
TGF-bþ) and normalisation of gut dysbiosis [97]. The results of this 7.1. Viable probiotics versus non-viable microorganisms
study show that VSL#3 may be successful in the IBD therapy in dogs
and call for further research in the area of probiotics and IBD. Numerous commercially available probiotic products for com-
IBD may affect also cats. Collecting duodenal biopsies from IBD panion animal consumption contain enterococci, mainly E. faecium
cat patients revealed mucosa-associated Enterobacteriaceae being or E. faecalis, which are natural habitants of the canine and feline
higher in cats with signs of gastrointestinal disease [98]. Inness GIT and specific strains may exert numerous benefits on the host as
et al. [21] reported total bacteria, Bifidobacterium spp., and Bacter- probiotics. On the other hand, enterococci can be pathogenic and
oides spp. being significantly higher in healthy cats than in cats have a notorious ability to rapidly develop, spread antibiotic
suffering from IBD where Desulfovibrio spp. producing toxic sul- resistance and favour the growth of potentially harmful microbes in
phides emerged higher in colitic cats. Bacterial count was measured animals and humans [49,106,107]. Therefore, even though no pro-
by in situ hybridisation FISH. Dietary intervention may be an biotic enterococcal infections have been reported in animals,
important aspect of their treatment and microbiota modulation theoretically they could possess certain safety risk. New research
could be a key to new dietary treatment regimens. However, on the identification of novel strains and the assessment of func-
studies on probiotic applications for IBD in cats are lacking. tional properties are being developed [14,80,108].
There are more studies on the use of viable than non-viable
6.5. Probiotic effect on intestinal parasites and viruses forms of probiotics [78,109,110], although viability is essential for
probiotics as described above. Non-viable preparations may have
To our knowledge, there are only few studies assessing the in- global economic advantages in terms of extended shelf life in non-
teractions of specific probiotics on parasites and viruses in com- refrigerated conditions and for storage in extreme temperature or
panion animals. In a double-blinded placebo controlled study a humidity. Their use could also reduce the risks of potential mi-
probiotic mix of L. fermentum VET9A, L. plantarum VET14A, and crobial translocation and infection.
L. rhamnosus VET16A at a total concentration of 2
109 CFU/ml was Recent findings demonstrate positive in vitro effect of three
administered 100 mL twice a day for seven days to 24 dogs probiotic canine-originated lactobacilli (L. fermentum VET9A,
suffering from acute and intermitted diarrhoea. Faecal parasites L. plantarum VET14A, and L. rhamnosus VET16A) against canine
(Toxocara canis, Uncinaria stenocephala, Diphyllobothrium latum, model enteropathogens when probiotics were used in viable and
Giardia sp.) and viruses (canine parvovirus CPV, canine rotavirus non-viable forms. In addition the inactivated forms of probiotic
CRV, canine calicivirus CaCV, canine coronavirus CCV) were moni- strains were also able to adhere to dog mucus in vitro. Thus, non-
tored prior to administrating the study product. Virus account was viable probiotics have a potential as a successful probiotic feed
detected also post administration at day 8 with no relevant findings additives in canine diet [65,66]. The in vivo study using non-viable
(Beasley, 2014, unpublished). forms of probiotics are also promising, although preparation
A study evaluating 6-week probiotic treatment with E. faecium method of non-viable form might have an impact on probiotic
SF68 (5
108 CFU/d) to dogs with chronic naturally acquired potential. Kanasugi and colleagues [111] demonstrated that oral
subclinical giardiasis did not affect giardial cyst shedding or antigen administration of a heat-killed E. faecalis (FK-23) stimulated non-
content and did not alter innate or adaptive immune responses specific immune responses in healthy dogs. A bacterial enter-
[99]. Administrating a genetically modified L. acidophilus for three ovaccine Colifagina which contains deactivated whole bacteria and
days to cats with feline immunodeficiency virus (FIV) suggested the lysates of E. coli 01, 02, 055, 0111, Bacillus pumilus, Morganella
probiotic having an upregulating role in transcellular transport morgani, Alcaligenes faecalis, Shigella flexneri, B. subtilis, E. faecalis,
across the gastointestinal ephitelial barrier [100]. There is a recent and Proteus vulgaris and is used in human medicine to treat in-
report in human infants suggesting that specific probiotics or pre- testinal symptoms, has been shown to improve symptoms and
biotics may have an impact on human respiratory tract infections faecal consistency in five dogs with recurrent episodes of diarrhoea.
caused by rhinoviruses [101]. The interaction has been suggested to Authors reported that such improvement lasted as long as the dogs
be modulated by binding viruses [102]. were monitored for diarrhoea, i.e. up to one month after discon-
tinuation of the probiotic treatment [112]. Thus, non-viable forms
6.6. Probiotics and urogenital tract infections of probiotics could be a good alternative to live probiotic cells, but
the current definition identifies only viable microorganisms as
Just as in women, the vaginal microbiota in healthy bitches is probiotics [56,57]. Nevertheless, more research on non-viable
predominantly colonised by LAB, which may reach up to 108 CFU. forms of probiotic bacteria could be useful to assess their anti-
Canine vaginal LAB have been found to exert antipathogenic ac- pathogenic and physiological effects on canine and feline health.
tivities thus have a probiotic potential [62] and could be used as
strategies to combat urinary tract infections in dogs. One study 7.2. Quality and stability of probiotic products
evaluated oral administration of a commercial probiotic mixture
containing lactobacilli (>64 bil CFU/g), bifidobacteria (30 bil CFU/g), It has been demonstrated that the production and
and bacilli species (24 bil CFU/g), (strains not specified) along with a manufacturing methods and the food carrier may influence the
combination of yeast, enzymes, vitamins, and prebiotics, once daily original properties of probiotics [113]. Since different sources of the
for either 2 weeks or 4 weeks to 35 healthy bitches and found that same probiotic may significantly alter strain properties, the
probiotic mixture supplementation did not have an effect on the outcome of intervention studies may be questioned. Recently, we
prevalence of vaginal LAB in studied animals [103]. have shown that growth media may significantly affect the adhe-
Pyometra, a uterine bacterial infection can be a life threatening sive ability of canine probiotics lactobacilli to dog mucus [66]. Their
for dogs and cats. The treatment includes antibiotics, hormonal impact on enteropathogen adhesion to canine mucus was also
therapy and also surgery [104,105]. Further studies are warranted altered depending on the growth media used to cultivate probiotics
 Ł. Grze
skowiak et al. / Anaerobe 34 (2015) 14e23 21

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kanen is gratefully acknowledged for drawing the dog and cat fig-
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