Importance of Yeasts in Oral Canine Mucosa

*Claudete Rodrigues Paula, Bianca Silva Navarro, Mário Mendes Bonci and Diana Costa Nascimento*

## **Abstract**

Dentistry science is a new specialty in veterinary medicine that has been growing in recent years, accompanied by the development of professionals who seek to improve the quality of life of pets. Cases related to problems in the oral cavity have gained significant importance in the medical clinic of professionals who treat small animals. Due to lack of professional knowledge or due to animal behavioral problems, such as aggressiveness, the anamnesis of the oral cavity is not performed most of the time, which ends up delaying the diagnosis of the pathology. In addition, an animal with a problem in the oral cavity may take years to show signs of the disease. In general, animals have an oral microbiota composed of various species of fungi, which, under specific conditions, can change from saprophytes to pathogens, compromising their health. Thus, the pre-knowledge of potentially pathogenic yeasts belonging to oral microbiota of dogs and their susceptibility profile compared to the main drugs used in antifungal therapy, is of fundamental importance as it ensures a clinical auxiliary support for the diagnosis and treatment of most diseases of the oral cavity.

**Keywords:** yeasts, oral cavity, dogs, antifungal, microbial resistance, fungi

#### **1. Introduction**

Fungi are eukaryotic, heterotrophic organisms, multinucleated like molds, or only with one nucleus, like yeasts. These organisms can be unicellular, or multicellular, which we call mycelium. Yeasts are unicellular and do not present, in general, morphological differences. The cells are rounded, ovoid or elongated, but some yeast under special conditions may have successive sprouts in a chain, which we call pseudomycelium [1].

The classification of fungi is based on morphological, reproductive and physiological characteristics. The taxonomy of fungi is still varied, but we can classify them in the Kingdom Fungi in the six phylas: Basidyomycota, Ascomycota, Glomeromycota, Chytridiomycota, Blastocladiomycota and Neocallimastigomycota [2, 3].

Approximately 200 out of a total of 100,000 species of yeast are considered pathogenic. Of these pathogenic species, 50 of them are regularly associated with mycoses. Yeasts are the ones that cause the greatest number of mycoses, both in man and in animals and we highlight the genera *Candida*, *Cryptococcus*, *Malassezia* and *Trichosporon* [3].

**Figure 1.** *Mixed breed dog.*

These yeasts can be assexual (anascoporogenous), or sexual (ascoporogenous or basidioporogenous). In general, they are considered opportunists "waiting" for their "opportunity", that is, the drop in the immunity of man and animals, thus causing a case of ringworm.

Among domestic animals, the ones that have the closest proximity to people are dogs. *Canis lupus familiaris* is believed to have emerged approximately 130,000 years ago, from the domestication of the gray wolf. Crossbreeding and selection of characteristics gave rise to different breeds, including Poodle, Yorkshire, Terrier and Labrador Retriever, but mixed breed animals are prevalent in homes around the world (**Figure 1**) [4].

In addition to being mere companions in people's homes dogs have established themselves with essential functions such as security and hunting. These dogs have gained these and other noble functions and thus brought them even closer to human beings in places and situations that would otherwise be dispensed with. Today they also act as guides for the visually impaired, accompanying people to the hospital, monitoring blood glucose levels for diabetic people and even detecting pathogens in hospital environments [5].

These new functions, with consequently greater proximity between dogs and people, also result in a possible greater exchange of microorganisms between these beings, including yeasts. Among these fungi, the most present in the oral mucosa of dogs are the genera *Malassezia* and *Candida* and found less the genus *Cryptococcus* [6].

In the field of public health, these microorganisms have in common the ability to cause disease in both animals and people, and therefore this possible increase in the sharing of microbiota between these beings must be monitored by health specialists.

It is important to emphasize that the exchange of microorganisms occurs in both directions, and that the health of the animals must also be considered in these cases.

The vigilance of the clinical mycologist must be maintained for a better understanding of how future changes can become serious public health problems, especially for yeasts, as we have already seen in several situations.

#### **2. Ecology and sources of yeast infection**

Yeasts can be found in plants, soil, air, aquatic environment, in invertebrate and vertebrate animals, that is, in almost all ecosystems. These microorganisms can be in their symbiotic state, in mutualism, or in parasitism. In humans, several species

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*Importance of Yeasts in Oral Canine Mucosa DOI: http://dx.doi.org/10.5772/intechopen.95905*

immunodepression of the host [7].

can occur in sexual relations [8].

ing environments.

organism [9].

cases of fungemia [12].

uncommon [13].

susceptibility [14].

can be part of their natural microbiota, in the gastrointestinal tract, in mucocutaneous tissues and skin. In man, a large part of yeast infections, especially of the genus *Candida*, are of endogenous origin and are linked to risk factors such as old age, prematurity, avitaminosis, antibiotic therapy, cancer, and other diseases that cause

Extrinsic factors can also be important, such as the rupture of the natural barrier of the skin and mucous membranes, the use of invasive hospital material and contact with contaminated ecological niches. Direct transmission between people

The licking of the paws and other areas of the body explains the considerable presence of *Malassezia pachydermatis* in the oral cavity of dogs. Considered a saprophyte in the skin of dogs, this microorganism can cause dermatitis in several situations, and in these cases, there is also an increase in its presence in the oral mucosa. Other relevant yeasts of these animals belong to the genera *Candida*, *Rhodotorula* and *Trichosporon*, which are, in most cases, in balance with the dogs'

It is also reported that *Cyniclomyces guttulatus*, present in the stomach, intestine and feces, which in situations of imbalance with the commensal microbiota, may be

The habit of sniffing the soil, in parks and gardens, hunting in forests and dens, favors the sharing of microorganisms among animals linked to these environments. The organic matter present in these places, mainly in the feces of birds and bats, favors colonization by fungi such as *Cryptococcus* spp. and *Histoplasma capsulatum*, which in situations favorable to microorganisms (host immunosuppression; high

Advances in veterinary hospital techniques, especially surgical procedures and hospitalizations, also brings new sources of infection for dogs. The ability of microorganisms of the genera *Candida* and *Malassezia* to form biofilms makes equipment such as specula, probes and other surgical materials possible sources of transmission of these microorganisms. For this reason, the correct asepsis and sterilization for handling this equipment is extremely important to avoid mycoses and severe

There are several yeasts that are of interest to the veterinarian, which can cause superficial, subcutaneous, mucosal lesions, and even granulomatous and systemic processes, and, in most cases, suspicion about the fungal etiology of cases is neglected, hence advanced and severe cases of mycosis in dogs are not

The transition from the yeast stage to commensal to pathogenic will depend

The factors that can predispose humans and animals to a yeast infection are innumerable, resulting from alterations in the defense mechanisms or by compro-

both on factors related to the agent's virulence, as well as on the host's own

mising the anatomical barriers of protection of the organism [15–17].

related to clinical conditions that affect the gastrointestinal tract [10].

microbial inoculum load) can cause serious diseases [11].

**3. Predisposing and virulence factors to yeast infections**

In dogs, the main yeast found on the skin and mucocutaneous surfaces is *Malassezia pachydermatis*, which easily recovers in the folds of the skin and especially in the various parts of the ear. The prevalence of some types of yeasts in the oral mucosa of dogs is related to several habits, such as licking, sniffing and explor-

#### *Importance of Yeasts in Oral Canine Mucosa DOI: http://dx.doi.org/10.5772/intechopen.95905*

*Canine Genetics, Health and Medicine*

causing a case of ringworm.

**Figure 1.** *Mixed breed dog.*

hospital environments [5].

*Cryptococcus* [6].

specialists.

homes around the world (**Figure 1**) [4].

These yeasts can be assexual (anascoporogenous), or sexual (ascoporogenous or basidioporogenous). In general, they are considered opportunists "waiting" for their "opportunity", that is, the drop in the immunity of man and animals, thus

Among domestic animals, the ones that have the closest proximity to people

In addition to being mere companions in people's homes dogs have established themselves with essential functions such as security and hunting. These dogs have gained these and other noble functions and thus brought them even closer to human beings in places and situations that would otherwise be dispensed with. Today they also act as guides for the visually impaired, accompanying people to the hospital, monitoring blood glucose levels for diabetic people and even detecting pathogens in

These new functions, with consequently greater proximity between dogs and people, also result in a possible greater exchange of microorganisms between these beings, including yeasts. Among these fungi, the most present in the oral mucosa of dogs are the genera *Malassezia* and *Candida* and found less the genus

In the field of public health, these microorganisms have in common the ability to cause disease in both animals and people, and therefore this possible increase in the sharing of microbiota between these beings must be monitored by health

It is important to emphasize that the exchange of microorganisms occurs in both directions, and that the health of the animals must also be considered in these cases. The vigilance of the clinical mycologist must be maintained for a better understanding of how future changes can become serious public health problems,

Yeasts can be found in plants, soil, air, aquatic environment, in invertebrate and vertebrate animals, that is, in almost all ecosystems. These microorganisms can be in their symbiotic state, in mutualism, or in parasitism. In humans, several species

especially for yeasts, as we have already seen in several situations.

**2. Ecology and sources of yeast infection**

are dogs. *Canis lupus familiaris* is believed to have emerged approximately 130,000 years ago, from the domestication of the gray wolf. Crossbreeding and selection of characteristics gave rise to different breeds, including Poodle, Yorkshire, Terrier and Labrador Retriever, but mixed breed animals are prevalent in

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can be part of their natural microbiota, in the gastrointestinal tract, in mucocutaneous tissues and skin. In man, a large part of yeast infections, especially of the genus *Candida*, are of endogenous origin and are linked to risk factors such as old age, prematurity, avitaminosis, antibiotic therapy, cancer, and other diseases that cause immunodepression of the host [7].

Extrinsic factors can also be important, such as the rupture of the natural barrier of the skin and mucous membranes, the use of invasive hospital material and contact with contaminated ecological niches. Direct transmission between people can occur in sexual relations [8].

In dogs, the main yeast found on the skin and mucocutaneous surfaces is *Malassezia pachydermatis*, which easily recovers in the folds of the skin and especially in the various parts of the ear. The prevalence of some types of yeasts in the oral mucosa of dogs is related to several habits, such as licking, sniffing and exploring environments.

The licking of the paws and other areas of the body explains the considerable presence of *Malassezia pachydermatis* in the oral cavity of dogs. Considered a saprophyte in the skin of dogs, this microorganism can cause dermatitis in several situations, and in these cases, there is also an increase in its presence in the oral mucosa. Other relevant yeasts of these animals belong to the genera *Candida*, *Rhodotorula* and *Trichosporon*, which are, in most cases, in balance with the dogs' organism [9].

It is also reported that *Cyniclomyces guttulatus*, present in the stomach, intestine and feces, which in situations of imbalance with the commensal microbiota, may be related to clinical conditions that affect the gastrointestinal tract [10].

The habit of sniffing the soil, in parks and gardens, hunting in forests and dens, favors the sharing of microorganisms among animals linked to these environments. The organic matter present in these places, mainly in the feces of birds and bats, favors colonization by fungi such as *Cryptococcus* spp. and *Histoplasma capsulatum*, which in situations favorable to microorganisms (host immunosuppression; high microbial inoculum load) can cause serious diseases [11].

Advances in veterinary hospital techniques, especially surgical procedures and hospitalizations, also brings new sources of infection for dogs. The ability of microorganisms of the genera *Candida* and *Malassezia* to form biofilms makes equipment such as specula, probes and other surgical materials possible sources of transmission of these microorganisms. For this reason, the correct asepsis and sterilization for handling this equipment is extremely important to avoid mycoses and severe cases of fungemia [12].

## **3. Predisposing and virulence factors to yeast infections**

There are several yeasts that are of interest to the veterinarian, which can cause superficial, subcutaneous, mucosal lesions, and even granulomatous and systemic processes, and, in most cases, suspicion about the fungal etiology of cases is neglected, hence advanced and severe cases of mycosis in dogs are not uncommon [13].

The transition from the yeast stage to commensal to pathogenic will depend both on factors related to the agent's virulence, as well as on the host's own susceptibility [14].

The factors that can predispose humans and animals to a yeast infection are innumerable, resulting from alterations in the defense mechanisms or by compromising the anatomical barriers of protection of the organism [15–17].

Among these factors we can mention: stress; use of broad-spectrum antibiotics or prolonged antibiotic therapy; antineoplastic agents; neutropenia; immunosuppression; age (senility/puppy); inadequate environment (overcrowding); long-term use of corticosteroids; nutritional deficiencies; diets with a high concentration of carbohydrates; pH changes, vitamin A deficiency, trichomoniasis; presence of autoimmune diseases; changes in anatomical barriers due to trauma (maceration); aplastic anemia; hematological infections; periodontal diseases (**Figure 2**) and other concomitant diseases [17, 18].

Prolonged antibiotic therapy and a high concentration of carbohydrates in the diet can lead to the destruction or inhibition of the competitive bacterial microbiota, disrupting its balance with the host organism, thus allowing the accentuated growth of yeasts [15].

Probably due to the poor oral hygiene of dogs throughout their life and associated with the other predisposing factors already mentioned, senility is considered a significant condition for predisposition to periodontal disease. Animals older than 4 years, according to a study with stray dogs, are more likely to develop this disease, ranging from mild gingivitis to severe periodontitis (**Figure 3**).

Virulence factors attributed to microorganisms must also be taken into account, such as production of hydrolytic enzymes, proteases and phospholipases, adhesion, formation of germ tube and biofilms. These factors favor the invasive power and interfere with the host's metabolism. All these factors, from hosts and yeasts, can lead to superficial, or systemic, conditions. It is worth mentioning that the high concentration of viable cells of the microorganism in an ecological niche of the host is another factor that must be considered, as they may be part of the oral microbiota.

**Figure 2.** *Dog with periodontal disease.*

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**Figure 4.**

*Importance of Yeasts in Oral Canine Mucosa DOI: http://dx.doi.org/10.5772/intechopen.95905*

loosening and loss of this tooth [22].

**4. Importance of animals' oral health**

decreased immunity and clinical complications [21].

provision of oral hygiene care is worrying [22, 23].

dogs with periodontal disease is frequent (**Figure 4**).

narian regarding the etiopathogenesis of diseases, such as yeasts.

*Connection: Presence of Periodontal Disease x Positive isolation of yeast [19].*

in the bloodstream.

Disorders of the oral cavity are of great importance in veterinary medicine due to their high prevalence in dogs and their serious consequences, which can even affect the systemic health of the animal [20]. Abnormalities, injuries or disorders of this organ can cause discomfort and pain, leading the animal to anorexia, due to lack of food, and adipsia, not water intake, predisposing it to conditions of

In addition to this great discomfort and the involvement of other organs, the inflammatory response caused by diseases in the oral cavity can lead to the gingival tissue a progressive loss of tooth fixation to the alveolar bone and, consequently, the

The dentistry specialty in veterinary medicine has been evolving in recent years, gaining space in the curriculum of some colleges. Even though the food industry has undergone great advances in the production of diets aimed at improving oral health, the number of professionals who perform an adequate clinical examination is still not significant. In addition to this important factor, the lack of adequate

Among dogs over one year of age, 95% have some degree of the disease, and in the clinic, it is believed that 100% of adult animals have varying degrees of periodontal disease [23]. The most common signs associated with periodontal disease are halitosis, dental calculus, inflammation and gingival bleeding, anorexia and the consequent weight loss, ptyalism, difficulty in chewing and grinding food, mobility and migration of teeth, loss of alveolar bone, gingival retraction and behavioral changes [24]. Periodontal disease is, therefore, the most common disease affecting dogs of all breeds, formed from proliferative microorganisms, defense cells (leukocytes and macrophages), epithelial cells, bacterial polysaccharides and salivary glycoproteins, which over time become organize, occurring mineralization and formation of dental calculus [25]. It is believed that this clinical condition is usually caused by the formation of bacterial plaques, but the isolation of yeasts from the oral cavity of

The greatest risk in periodontopathic is not only the loss of teeth or the development of local infections, but the possible systemic effects of the pathological agent

Thus, the oral health of dogs is extremely important and still needs a greater focus on microbiological research and awareness of those responsible, regarding food, the importance of oral hygiene, and the attention of the tutor and the veteri-

**Figure 3.** *Connection: Age x Presence of Periodontal Disease in dogs [19].*

*Canine Genetics, Health and Medicine*

other concomitant diseases [17, 18].

growth of yeasts [15].

microbiota.

Among these factors we can mention: stress; use of broad-spectrum antibiotics or prolonged antibiotic therapy; antineoplastic agents; neutropenia; immunosuppression; age (senility/puppy); inadequate environment (overcrowding); long-term use of corticosteroids; nutritional deficiencies; diets with a high concentration of carbohydrates; pH changes, vitamin A deficiency, trichomoniasis; presence of autoimmune diseases; changes in anatomical barriers due to trauma (maceration); aplastic anemia; hematological infections; periodontal diseases (**Figure 2**) and

Prolonged antibiotic therapy and a high concentration of carbohydrates in the diet can lead to the destruction or inhibition of the competitive bacterial microbiota, disrupting its balance with the host organism, thus allowing the accentuated

Probably due to the poor oral hygiene of dogs throughout their life and associated with the other predisposing factors already mentioned, senility is considered a significant condition for predisposition to periodontal disease. Animals older than 4 years, according to a study with stray dogs, are more likely to develop this disease,

Virulence factors attributed to microorganisms must also be taken into account, such as production of hydrolytic enzymes, proteases and phospholipases, adhesion, formation of germ tube and biofilms. These factors favor the invasive power and interfere with the host's metabolism. All these factors, from hosts and yeasts, can lead to superficial, or systemic, conditions. It is worth mentioning that the high concentration of viable cells of the microorganism in an ecological niche of the host is another factor that must be considered, as they may be part of the oral

ranging from mild gingivitis to severe periodontitis (**Figure 3**).

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**Figure 3.**

**Figure 2.**

*Dog with periodontal disease.*

*Connection: Age x Presence of Periodontal Disease in dogs [19].*
