Aerococcus viridans and Public Health: Oral Carriage and Antimicrobial Resistance in Stray Dogs and Cats in Algeria

Abstract

The current study aimed to determine the occurrence and antimicrobial resistance of oral Aerococcus viridans in stray dogs and cats in Algeria. Oral swabs from 200 stray animals (100 dogs and 100 cats) were collected and cultured on Columbia agar medium supplemented with 5% defibrinated sheep blood. Isolates were identified using analytical profile index Rapid 20 Strep commercial kits, and antibiotic susceptibility was determined using the disk diffusion method. Of the 200 animals sampled, 34 carried A. viridans in their oral cavities, with 26 isolates (76.47%) resistant to at least 2 drugs. Multidrug resistance profiles (to more than three different antimicrobials) were observed only in cats (26.08% of isolates). More isolates were resistant to erythromycin and tetracycline (71% and 65%, respectively) than to other antimicrobials. This is the first research study in Algeria detecting antimicrobial resistance in oral A. viridans isolated from dogs and cats and highlights potential public health concerns. Clinical trials registration number: 01/2018.

Introduction

The natural dog and cat oral flora contains a wide range of bacterial species, including opportunistic pathogens, which may not only be transmitted to humans and other animals through bites but also play an important role in the dissemination of antimicrobial resistance in the environment posing a public health hazard.^1,2 In addition, the transfer of antibiotic-resistance genes between different bacterial species in the oral cavity, as well as between oral bacteria and bacteria from other environments has previously been described.^3,4

Aerococcus viridans, a member of the Streptococcaceae family, is a microaerophilic catalase-negative and oxidase-negative Gram-positive coccus, that produces green alpha hemolysis on blood agar.^5,6 In microbiology laboratories, this bacterium is frequently misidentified as Streptococcus or Enterococcus, or considered a contaminant (nonpathogenic), resulting in its underestimation as a source of human infection.^5,7,8

Although A. viridans is an infrequent human pathogen and seems to have low virulence, it can occasionally cause systemic infections, especially in immunocompromised individuals, such as meningitis, urinary tract infection, osteomyelitis, septic arthritis, wound infections, and most commonly bacteremia and endocarditis.^7–9

In veterinary medicine, A. viridans is responsible for a variety of diseases in animals, including aquatic animal infections in lobster and tilapia, swine arthritis, meningitis, and pneumonia.^5,6,9,10 This bacterium has also been isolated from wild animals, the normal gut flora of chickens, as well as from the milk of cows with subclinical and clinical mastitis.^5,10,11 However, the status of dogs and cats as potential carriers of oral A. viridans remains unclear.¹²

It is generally known that dogs and cats can play a role in the spread of opportunistic pathogens and multidrug-resistant bacteria, such as viridans streptococci and enterococci.^3,4 These bacteria are recognized for acquiring antibiotic resistance genes via mobile genetic elements (plasmids, transposons), transferable to other more pathogenic bacteria in the oral cavity or the environment.^3,12–14

A. viridans, which has a colony morphology similar to viridans streptococci (small semitransparent alpha-hemolytic) and antibiotic resistance patterns similar to enterococci, is frequently misidentified or reported as a contaminant.^6,7,11,15 Hence, its pathogenicity and spread in humans and animals, including dogs and cats, are still unknown.^11,15

In Algeria, the number of stray dogs and cats has increased recently, which may increase the risk of zoonosis spread and environmental contamination with multidrug-resistant bacteria.^12,16,17 This issue deserves even more attention considering the high annual frequency in Algeria of hospital visits related to dog bites and the high number of human die of rabies (annual average of 18 deaths).^17,18 However, only one study on the zoonotic oral flora of these animals has been published, without identifying A. viridans.¹² Thus, the role of dogs and cats as A. viridans reservoirs is still unclear.

This study aimed to determine the presence of A. viridans in the oral cavity of stray dogs and cats in Algeria and characterize the antimicrobial resistance profile of the isolates recovered.

Materials and Methods

Study area

The study was conducted in the Department of Algiers (Algeria's capital), which is located on the country's central coast between 3°2’31.09’’ east longitude and 36°45’9’’ north latitude. This department includes 57 districts with a total area of 1,190 km² and a population of around 2.9 million inhabitants. Three departments border Algiers, Blida to the south, Boumerdes to the east, and Tipaza to the west. To the north, it is bordered by the Mediterranean Sea.

Ethics statement

The ethics committee and decision board of Public Industrial and Commercial Company (P.I.C.C.) and Urban Hygiene and Environmental Protection (U.H.E.P.) of Algiers approved the procedure (Application No. 01/2018).

In 1996, Algeria launched the Rabies Prevention Program.¹⁸ In this context, P.I.C.C-U.H.E.P, an affiliate of the Algerian Ministry of Water Resources and Environment tasked with preventing zoonosis and vector-borne diseases like rabies and leishmaniosis, catches stray dogs and cats in the 57 districts of the department of Algiers.^17,18 Captured animals were subsequently placed in the dog pound of El-Harrach during the legal term (7 days) before being euthanized.¹⁹

Samples collection

Between January 2018 and July 2019, a total of 200 oral swabs (tongue, gum, palate, cheeks, and teeth) were collected at irregular intervals from 100 stray dogs and 100 stray cats that were chosen at random without regard to age, sex, or breed. All the sampled animals were caught by the P.I.C.C-U.H.E.P. from the 57 districts of Algiers during the study period, and they appeared to be healthy and had not received any previous antibiotic treatment.

A retaining clip was placed around the animal's neck before swabbing to keep it immobilized.

A dry, sterile cotton swab (without transport medium) was then introduced into the oral cavity and rubbed over the buccal area for a few seconds to obtain an oral sample.

All swabs were stored in an icebox (+4°C) and sent to the microbiology laboratory within 60 minutes of being collected.

Isolation and biochemical identification of A. viridans

After arriving in the laboratory, each oral swab was directly plated on Columbia agar medium supplemented with 5% of defibrinated sheep blood (Pasteur Institute, Algeria) and incubated for 24–48 hours at 37°C in a 5% carbon dioxide atmospheric chamber.^5,20,21

Following purification, presumptive A. viridans colonies were tested for Gram staining (Gram-positive cocci), hemolysis type (alpha-hemolytic), and a catalase test (negative) was performed. The strains were finally identified using analytical profile index (API) Rapid 20 Strep commercial kits (Biomérieux, Marcy l'Etoile, France), according to the manufacturer's instructions.^5,20

Antimicrobial susceptibility testing

The test for all A. viridans isolates was conducted according to the Clinical and Laboratory Standards Institute guidelines²² using a conventional Kirby–Bauer disk diffusion method. Five common antibiotics used to treat bites-wounds were tested: Amoxicillin/clavulanate 30 μg (Oxoïd, Basingstoke, UK), Penicillin 10 I.U. (Oxoïd, Basingstoke, UK), Ampicillin 10 μg (Oxoïd), Tetracycline 30 μg (Oxoïd), and Erythromycin 5 μg (Oxoïd) on Muller–Hinton agar supplemented with 5% of blood sheep (Oxoïd). As control quality, the following strains were used: Escherichia coli American Type Culture Collection (ATCC) 25922, the resistant Staphylococcus aureus ATCC 43300, the sensitive S. aureus ATCC 25923, and Pseudomonas aeruginosa ATCC 27853. As there are no specific inhibition zone diameter (IZD) breakpoints established for A. viridans,^5,20 the IZD breakpoints used in this study followed the recommended protocol for testing viridans group streptococci, as suggested by the Clinical and Laboratory Standards Institute (CLSI)²³ and European Committee on Antimicrobial Susceptibility Testing (European Committee for the Study of Antimicrobial Susceptibility; Table 1).²³

Table 1.

Zone Diameter Breakpoints Used for Each Antibiotic Against Aerococcus viridans Isolates as Suggested by the Clinical and Laboratory Standards Institute and European Committee on Antimicrobial Susceptibility Testing

Antimicrobial agents	Zone diameter breakpoints (mm)
Antimicrobial agents	S ≥	R <
Penicillin	21	12
Ampicillin	21	15
Amoxicillin-clavulanate	19	14
Erythromycin	20	17
Tetracycline	20	16

R, resistant; S, sensible.

Results

In this study, 34 of 200 sampled animals (17%) carried A. viridans in their oral cavities. The number of A. viridans isolates recovered from cats (n = 23) was more than double that of dogs (n = 11; Table 2).

Table 2.

Occurrence of Oral Aerococcus viridans in Dogs and Cats Examined in the Present Study

Characteristic	Dog	Cat	Total populations
Sampled animals	100	100	200
No. (%) of animals carrying A. viridans	11 (11)	23 (23)	34 (17)
No. (%) Animals negative for A. viridans	77 (77)	89 (89)	166 (83)
No. of isolates	11	23	34

No., number.

Regarding the results of antibiotic sensitivity, the majority (76.47%) of A. viridans isolates were resistant to at least two drugs, in particular against erythromycin and tetracycline (64.70% of the strains), while only six isolates (17.64%) were susceptible to all drugs tested. Strains resistant to several drugs (more than three different antimicrobials)^12,24 were observed only in cats (26.08% of the isolates; Table 3).

Table 3.

Antimicrobial Resistance Pattern Among Aerococcus viridans Isolates

Pattern (%)	Isolates from dog (n = 11)	Isolates from cat (n = 23)	Total (n = 34)
S^ble	2 (18.18)	4 (17.39)	6 (17.64)
Erythromycin	1 (9.09)	1 (4.34)	2 (5.88)
Ery-Tet	6 (54.54)	9 (39.13)	15 (44.11)
Ery-Tet-Amx/cl	1 (9.09)	0 (0)	1 (2.94)
Pen-Amp-Amx/cl	1 (9.09)	3 (13.04)	4 (11.76)
Ery-Tet-Pen–Amx/cl	0 (0)	5 (21.73)	5 (14.70)
Ery-Tet-Pen–Amp-Amx/cl	0 (0)	1 (4.34)	1 (2.94)

Amp, ampicillin; Amx/cl, amoxicillin-clavulanate acid; Ery, erythromycin; Pen, penicillin; S^ble, sensible; Tet, tetracycline.

Almost all isolates were susceptible to ampicillin, penicillin, and amoxicillin-clavulanate (85%, 71%, and 68%, respectively), while the majority of isolated were resistant to erythromycin and tetracycline (71% and 65%, respectively; Table 4).

Table 4.

Antimicrobial Susceptibility of Aerococcus viridans Strains Isolated from Oral Cavities of Dogs and Cats Analyzed in the Present Study

Antimicrobial agents	Isolates from dog (n = 11)		Isolates from cat (n = 23)		Total (n = 34)
Antimicrobial agents	R + I (%)	S (%)	R + I (%)	S (%)	R + I (%)	S (%)
Penicillin	1 (9)	10 (91)	9 (39)	14 (61)	10 (29)	24 (71)
Ampicillin	1 (9)	10 (91)	4 (17)	19 (83)	05 (15)	29 (85)
Amoxicillin-clavulanate	2 (18)	9 (82)	9 (39)	14 (61)	11 (32)	23 (68)
Erythromycin	8 (73)	3 (27)	16 (70)	7 (30)	24 (71)	10 (29)
Tetracycline	7 (64)	4 (36)	15 (65)	8 (35)	22 (65)	12 (35)

I, intermediate resistance.

Discussion

The transmission of opportunistic pathogens found in the oral cavity of dogs and cats to humans has already been described, either directly via bites or indirectly through food or domestic environment contamination.^3,4,12

A. viridans, a fastidious Gram-positive coccus, associated with a wide range of diseases in humans and animals, has been isolated from the environment (dust, raw vegetables, air, water, and soil), aquatic animals, wild animals, livestock, and animal products.^{5,7,10,11,15,25} The occurrence of A. viridans has been reported in dogs during urinary tract infections²⁶ while reports looking at A. viridans in the oral cavity of dogs and cats are lacking.

In this study, 34 of the 200 stray animals (100 dogs and 100 cats) sampled had A. viridans in their oral cavities, resulting in carriage rates of 11% in dogs and 23% in cats.

Saphir and Carter isolated many alpha-hemolytic streptococci (41% of the isolates) from gingival flora of dogs; however, the authors didn't identify the isolates.²⁷ In another study looking at the oral flora of stray cats, alpha-hemolytic streptococci were found in the oral cavity of 15 out of 34 animals (44.11%).²⁸

Oral streptococci, formerly known as viridans streptococci, are native colonizers of the oral cavity of humans and many other animals, including dogs and cats; for this reason, they are very abundant in oral samples, though the frequency varies depending on the sampling area.^28,29 In this regard, Elliot et al. have identified the oral microbiota of domestic dogs; the genera Actinomyces (26%), Stretpcoccus (18%), and Granulicatella (17%) were mostly isolated from saliva samples, while the genera Porphyromonas (20%), Actinomyces (12%), and Neisseria (10%) from the dental plaques.³⁰

A. viridans colonies on blood agar have similar morphology to viridans streptococci colonies.^6,11,15 Therefore, it is possible that A. viridans was misidentified as Streptococcus viridans in previous studies based on classical microbiology (colony morphology, Gram staining, and hemolytic activity). In our study species, identification was not confirmed by matrix assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) or 16s rRNA gene sequencing. However, the API Rapid 20 Strep commercial kits herein used allow for good-to-excellent identification as previously reported by other authors.^5,6,20 In this regard, Liu et al. reported good (%id ≥90.0% and T value ≥ 0.25) to excellent (%id ≥99.9% and T value ≥ 0.75) identification for 75% of A. viridans isolates tested using the API Rapid 20 Strep commercial kits, while the remaining 25% of isolates were identified as Aerococcus spp.⁵

Even though A. viridans is opportunistic and rarely harmful to humans, it can cause serious infections in immunocompromised patients, including endocarditis, meningitis, and bacteremia.^6,7,11,31 As a result, the presence of this bacterium in the oral cavity of dogs and cats may pose a zoonotic risk, either directly through bites or indirectly through a contaminated environment.

Dogs and cats may play a role in the emergence and dissemination of antimicrobial-resistant bacteria.^3,12 However, in Algeria, no data on the resistance patterns of A. viridans coming from these animals are available.

In this study, the majority (76.47%) of A. viridans isolates were resistant to at least two drugs, with only six (17.64%) isolates being susceptible to all drugs tested. These findings are consistent with previous studies in animals and hospitalized patients that found this bacterium to be extremely resistant to several antimicrobials, such as penicillin, ampicillin, streptomycin, and tetracycline.^5,15,24

A. viridans isolates are frequently sensitive to betalactam antibiotics,^6,11,15 including penicillin, which is the standard treatment for infections caused by this bacterium.^15,31 However, the antimicrobial resistance of A. viridans to penicillin and other betalactam antibiotics is increasing.^11,15

In this study, a significant percentage of A. viridans isolates were sensitive to amoxicillin-clavulanate (68%), penicillin (71%), and ampicillin (85%).

These findings are consistent with the penicillin susceptibility pattern of strains isolated from blood cultures of patients with endocarditis (68.19%),²⁹ as well as the amoxicillin-clavulanate (84.6%), and ampicillin (76.9%) susceptibility pattern of swine strains.²⁴

In studies conducted by Colombo et al. in Brazil and Martin et al. in Spain, all the A. viridans strains (100%) isolated from wild animals and swine clinical specimens, respectively, were susceptible to betalactam antimicrobials (amoxicillin-clavulanate, penicillin, and ampicillin).^10,20 Another study by Liu et al. in China showed low levels of resistance to these three antimicrobials (5%) among A. viridans strains isolated from subclinical bovine mastitis.⁵ However, higher resistance to penicillin in swine isolates was reported (46.2%) by Nguyen et al. in Korea.²⁴

Although this bacterium was previously known to be susceptible to commonly used antibiotics in human health care settings,²⁰ recent studies indicate that A. viridans has developed resistance not only to penicillin but also to other antibiotics.^11,24,31

In this regard, it is reported that in enterococci and viridans group streptococci with penicillin resistance, the penicillin-binding protein is altered leading to resistance also against other betalactam antibiotics.^32,33

In vitro, A. viridans is susceptible to macrolides, such as erythromycin and tetracyclines,¹¹ which can be used as a penicillin substitute in people who are allergic to penicillin.^5,33 However, resistance to this antibiotic in oral streptococci and enterococci is increasing.^3,33

In this study, the majority of A. viridans isolates were resistant to erythromycin and tetracycline (71% and 65%, respectively).

These findings are similar to those published in a Korean study, which reported a 61.5% tetracycline resistance rate in A. viridans isolated from pig fetuses.²⁴ Two other studies conducted in China on the antibiotic resistance of A. viridans isolated from bovine mastitis revealed high levels of tetracycline resistance (more than 50%). However, lower rates of erythromycin resistance were observed (31.6% and 10%, respectively).^5,34

In Portugal, oral enterococci isolated from dogs and cats with periodontal disease showed high resistance (95%) to tetracycline, but not to erythromycin (20%).³

A. viridans share some characteristics of antibiotic resistance with enterococci,¹⁵ which is recognized to be multidrug-resistant having the ability to acquire antibiotic resistance via additional mobile genetic elements.³ In addition, oral bacteria, including enterococci and streptococci serve as an essential reservoir for tetracycline and erythromycin resistance genes,^3,32,35 which are commonly linked with plasmids or transposons.³⁶ These mobile genetic elements can therefore be exchanged horizontally, not only between bacteria of the same family but also between bacteria from different families in the oral cavity or environment.^3,4,35

In this study, 22 out of 34 A. viridans isolates were resistant to both erythromycin and tetracycline. According to Villedieu et al., tetracycline and erythromycin resistance genes may be associated with the same conjugative transposon, suggesting that resistance to both antibiotics may be acquired through a single mobile genetic element.³⁵

This study can be considered a first preliminary investigation isolating A. viridans from the oral cavity of dogs and cats. It provides valuable insights into the carriage rate of these bacteria in dogs and cats, as well as their antibiotic resistance profile.

However, it's important to note that the study utilized conventional microbiological identification methods, which may not provide a perfect confirmation of species/strains. Therefore, further studies employing alternative techniques such as MALDI-TOF and sequencing 16S RNA are strongly recommended to enhance the accuracy reliability of species identification.

Conclusion

To the best of our knowledge, this study is the first assessing the occurrence of oral A. viridans in dogs and cats and characterizing the antimicrobial resistance profile of recovered isolates. Our results suggest that dogs and cats in Algeria serve as carriers of A. viridans strains that exhibit resistance to multiple antibiotics within their oral flora. This discovery underscores a concerning potential public health risk. Urgent attention and further research are needed to effectively address this issue and mitigate the associated implications.

Footnotes

Acknowledgment

The authors would like to express their gratitude to the Director of P.I.C.C-U.H.E.P for authorizing us access to the dog-pound of El-Harrach to collect the samples.

Authors' Contributions

K.R: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Writing—Original Draft. L.N.: Validation, Writing—Original Draft, Writing—Review and Editing. F.G.: Writing—Original Draft, Writing—Review and Editing.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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