EFFECT OF REMOVABLE DENTURES ON COLONIZATION OF AEROBIC BACTERIA IN THE ORAL CAVITY AND ANTIBIOTIC PATTERN OF THE COMMON ISOLATED BACTERIA

Ibrahim Zaid Al-Shami1, Yaser Ahmed Salem Alrubaidi2, Khaled A AL-Haddad3, Mohammed Mohammed Ali Al-Najhi3,4, Hassan Abdulwahab Al-Shamahy5,6, 

Taghreed Ahmed M Al-Kibsi2, Abdulwahab Ismail Mohamed Al-Kholani

1Department of Conservative Dentistry and Oral Health, Faculty of Dentistry, Sana’a University, Republic of Yemen, 

2Department of Oral and Maxillo-Facial Surgery, Faculty of Dentistry, Sana’a University, Republic of Yemen.

3Orthodontics, Pedodontics and Prevention Department Faculty of Dentistry, Sana'a University, Yemen.

4Orthodontics, Pedodontics and Prevention Department Faculty of Dentistry, Genius University for Sciences & Technology, Dhamar city, Republic of Yemen. 

5Departement of Basic Sciences, Faculty of Dentistry, Sana’a University, Republic of Yemen.

6Medical Microbiology department, Faculty of Medicine, Genius University for Sciences &  Technology, Dhamar city, Republic of Yemen.

 

ABSTRACT 

Background and aims: Wearing a removable dental prosthesis causes a change in the micro flora of the mouth. The aim of this research was to verify the composition of aerobic bacterial in the oral cavity of patients with removable dentures and with normal teeth (without dentures), and antibiotics pattern for common isolates.

Methods: Bacteriological investigations were performed in 122 individuals (61 removable dentures: 61 normal teeth) attending dental clinics of Faculty of dentistry, Sana’a University, Yemen and private dental clinics. The culturing and antibiotic sensitivity were conducted in the Microbiology Department of the National Center of Public Health Laboratories (NCPHL) Sana'a, Yemen. Tongue dorsa and palate mucosa swabs were collected from normal teeth and denture groups, and as well swabs from mucosal part of denture surfaces in prosthetic patients. Cultivation in microaerophilic (5% CO2) and oxygenic conditions were performed on solid selective and non-selective media in addition to media enriched with 5% blood.

Results: Regarding the prosthetic patients, the rate of bacterial isolates from the palate, back, tongue and dental plaque smears was higher potential pathogenic bacteria as S. aureus and Enterobacteriaceae spp  in denture wearers, as E. coli (6.6% in dentures vs. 1.6% in the absence of dentures), Klebsiella pneumoniae (11.4% in dentures versus 1.6% in the normal teeth) and Pseudomonas aeruginosa (13.1% versus 0.0% ).While in viridians Streptococcus including Strept .mutans, there was a lower colonization rate in denture patients (18% in palate verses, 73.8% in individuals without dentures). 

Conclusion: The study demonstrated an elevated rate of bacterial isolates from palate, back, tongue and plaque swabs in denture patients of pathogenic bacteria such as S. aureus, E. coli, Klebsiella pneumoniae, and Pseudomonas aeruginosa; while in Streptococcus viridians including S. mutans, there was a lower colonization rate in denture patients verses a very high rate in individuals without dentures. 

Keywords: Antibiotic susceptibility testing, micro flora of the mouth, normal teeth, oral cavity, removable dental prosthesis.

 

INTRODUCTION

 

Oral microbiology is the study of microorganisms in the oral cavity and their interfaces with other microorganisms in the oral cavity or with the host itself1. The environment in the human mouth is accurate for the growth of the distinctive microorganisms existing there since it affords a source of nutrients and water, in addition to a temperate temperature2. Oral-resident microbes adhere to the teeth and gums and in unison to counteract the mechanical flow from the mouth to the stomach where acid-sensitive microbes are destroyed by hydrochloric acid3. Researchers found that oral bacteria have evolved mechanisms to influence their environment and avoid or modify the host's oral environment. Bacteria occupy the ecological niche provided by dental surfaces and mucosal epithelium4,5. A noteworthy factor that has been found to affect bacterial colonization in the oral cavity is the pH and oxygen concentration and availability on some surfaces of the mouth, which means that the loss of teeth and their replacement with dentures may lead to a change in their structure; As well as the mechanical forces acting on the surfaces of the mouth, the flow of saliva and fluids through the oral cavity, and ages of the host5. In spite of this, a highly effective innate host defense system constantly monitors bacterial colonization and prevents bacterial invasion of local tissues. There is a dynamic balance linking dental plaque bacteria and the host's innate defense system4.Of specific interest is the role of the oral micro biota in the two major dental diseases: periodontal diseases and dental caries4. Furthermore, research has connected deprived oral health and the resultant ability of oral bacteria to attack the body to affect heart health as well as cognitive function6. Wearing a removable dental prosthesis produces an alteration in oral bacteria7,8. For a number of individuals, this diverse environment is accountable for the development of a specific circumstance: denture-associated stomatitis and prosthetic stomatitis. Stomatitis is described by inflammation of the mucous membrane and redness under the dentures3. It is started by a microbial biofilm on the suitable surface of the denture from the surface of the mucosa, for example, the palate9. Denture-associated stomatitis (DAS) is one of the majority common irrefutable symptoms of oral candidiasis10, and involves 24-60% of well-worn dentures11. Roughly 90% of cases are believed to be caused by yeast9,12, typically C. albicans, even though lesions have also been connected with a diversity of further Candida species10-13 over and above bacteria from numerous genera3,10,14,15.

Nowadays, antimicrobial resistance (AMR) is the most important public health threat16-20, and AMR bacteria in various hospital departments are increasing exponentially21-23. According to a published study, 700,000 deaths by reason of antimicrobial resistance are described per annum, and it has been estimated that if proper control and prevention measures are not taken, antimicrobial resistance will turn out to be one of the most important causes of death among non-hospitalized or hospitalized patients all over the world24.

Oral bacteria such as Staphylococcus aureus, Streptococcus viridians group, and Enterobacteracea are also included as causative agent of systemic infections such as endocarditis, pneumonia, etc., so information on antibiotic profile is of importance in prescribing appropriate treatment in case of infection25. The aim of this study was to determine the aerobic bacterial composition of the oral cavity of patients with removable dentures and normal teeth individuals (without dentures), and to determine the antibiotic pattern of common isolates including S. aureus and S. viridians group.

 

MATERIALS AND METHODS 

 

Bacteriological examinations were performed on 122 individuals (61 removable dentures: 61 natural teeth) in the dental clinics of the Faculty of Dentistry, Sana'a University, Yemen and private dental clinics (Al-Mortadda Dental Clinics, Al-Kahara Dental Clinics) in Sana’a, over a period of 3 months, which began in December 2021 and ended in February 2022.

Microbiological procedure 

Cultivation and sensitivity to antibiotics were performed at the Microbiology Department of the National Center for Public Health Laboratories (NCPHL) Sana'a, Yemen. Swabs were collected from the mucous membrane of the palate and the tongue dorsa from dentures and natural teeth individuals, as well as swabs from the mucous part of the denture surfaces in prosthetic patients. Cultures were performed under oxygenated and microaerophilic conditions (5% CO2) on selective and non-selective solid media as well as media enriched with 5% blood. Standard procedures for bacterial culture and identification26 were applied.

Antibiogram: The antibiotic susceptibility profile was determined by disc diffusion method. The inoculums were adjusted to match the turbidity of 0.5 McFarland standards, and was swabbed on Brian heart infusion agar and allowed to dry for 10min27. Then antibiogram profiling was performed to determine the susceptibility of 4 β-Lactam antibiotics (Amoxicillin-Clavulanic Acid, Oxacillin (1μg), Cloxacillin (2μg), and Cefoxtine (30μg) and 8 non β-Lactam antibiotics (erythromycin (15μg), gentamicin (10μg), amikacin (30μg), cipro-floxacin (5μg), clindamycin (2μg) and vancomycin (30μg)) (Oxide, USA) by disc diffusion method.  Inhibition zone was measured after 24h of aerobically incubation at 37°C. The experiments of each antibiotic were performed in triplicate. The results were interpreted according to Clinical and Laboratory Standards Institute (CLSI) methodology28.

Ethical Consideration: Ethical approval for this study, No: 1771 dated September 11, 2021 was obtained from the Medical Ethics and Research Committee of the Faculty of Medicine and Health Sciences, Sana’a University. All procedures were according to the ethical guidelines of the review committee. A written informed consent was obtained from the selected participants. 

 

RESULTS 

 

There was an increased rate of colonization of S. aureus in denture patients (11.5% in the palate) versus 1.6% in individuals without dentures. While there was a decrease in the rate of Coagulase-negative colonization in denture patients (16.4% in the tongue) and a higher incidence of Coagulase (47.5%) in people without dentures. In viridians (apathy) Streptococcus including S. mutans, there was a lower colonization rate in denture patients equal to 18% in palate verses, a very high rate (73.8%) in individuals without dentures. Also, potentially pathogenic Enterobacteriaceae spp bacteria were more colonized in denture patients than in individuals without dentures: eg E. coli (6.6% in dentures vs. 1.6% in the absence of dentures), K. pneumoniae (11.4% in dentures versus 1.6% in the absence of dentures) and P. aeruginosa (13.1% in the dentures versus 0.0% in the absence of dentures).

S. aureus showed a high rate of resistant to tetracycline (83.3%), erythromycin (73.3%) and co-trimoxazole (40%), while isolates showed high frequency of sensitive to vancomycin (96.7%), clindamycin (96.7%), amikacin (93.3%), cefoxtine (93.3%) and cloxacillin (90%). CoNS showed a high rate of resistance to tetracycline (86.3%), erythromycin (80.8%) and co-trimoxazole (46.6%), while the isolates showed a high frequency of sensitivity to vancomycin (94.5%), clindamycin (94.5%), cloxacillin (93.2%), ciprofloxacin (87.7%), amikacin (86.3%), gentamicin (869.7%), and cefoxetine (79.5%). S. mutans showed a moderate rate of resistance to tetracycline (56.3%), and low rate of resistance to erythromycin (12.5%), co-trimoxazole (13.4%) and oxacillin (11.6%), while the isolates showed a high frequency of sensitivity to vancomycin (97.3%), clindamycin (99.1%), cloxacillin (98.2%), ciprofloxacin (97.3%), amikacin (98.2%), gentamicin (94.6%), and cefoxetine (95.5%). S. mitior showed a moderate rate of resistance to tetracycline (44.7%), and low rate of resistance to erythromycin (17%), and co-trimoxazole (10.6%), while the isolates showed a high frequency of sensitivity to vancomycin (97.9%), clindamycin (100%), cloxacillin (97.9%), ciprofloxacin (97.9%), amikacin (97.9%), gentamicin (97.9%), and cefoxetine (97.9%). S. sanguis showed a moderate rate of resistance to tetracycline (40.8%), and low rate of resistance to erythromycin (18.3%), and co-trimoxazole (14.3%), while the isolates showed a high frequency of sensitivity to vancomycin (98%), clindamycin (100%), cloxacillin (100%), ciprofloxacin (98%), amikacin (98%), gentamicin (95.9%), and cefoxetine (95.9%). S. alivarius showed a moderate rate of resistance to tetracycline (58.5%), and low rate of resistance to erythromycin (22.6%), and co-trimoxazole (20.8%), while the isolates showed a high frequency of sensitivity to vancomycin (98.1%), clindamycin (100%), cloxacillin (100%), ciprofloxacin (98.1%), amikacin (98.1%), gentamicin (96.2%), and cefoxetine (96.2%).

 

DISCUSSION 

 

A large amount of the adult population wears full or partial dentures. Reasons connected with tooth loss – dental caries, loss of periodontal support, tooth-alveolar trauma, and history of dental care are additive over time, and thus wearing dentures is more associated with older age although it can sometimes be recorded at earlier ages29.  Oral conditions especially connected with the wearing of dentures are denture-associated stomatitis (DAS)9-15,30 of bacterial or Candida origins. In the current study there was an increased rate of S. aureus colonization in dentures patients (11.5% in the palate) versus 1.6% in individuals without dentures. While there was a lower incidence of Coagulase-negative colonization in dentures patients (16.4% in the tongue) and a higher incidence of Coagulase-negative (47.5%) in subjects without dentures. In viridians (apathy) Streptococcus including S. mutans, there was an 18% lower colonization rate in dentures in the verses of the palate, which is very high (73.8%) in individuals without dentures. The results of the current study are similar to those reported in previous studies in that there are many similarities in the microbial composition, and there were some significant differences between the compositions in the adult population wearing full or partial dentures and adults with intact teeth29.There are relatively few studies on dental microbiology, and the factors affecting their quantity and types at the present time, although most of them were conducted in the eighties of last century29,31. Recent studies have discussed dentures in the adult population wearing full or partial dentures and adults with normal teeth and factors effected oral microbia8,29,32 and many publications have focused on Candida only3,7,29,30. Thus other groups of organisms may be overlooked in the mouth. This is especially true of obligate anaerobes, which are important if bad breath is the focus of study29,32,33.

In the current study, potentially pathogenic Enterobacteriaceae spp bacteria were more colonized in denture patients than in individuals without dentures: eg E. coli (6.6% in dentures versus 1.6% in the absence of dentures), K. pneumoniae (11.4% in dentures versus 1.6% in the absence of dentures) and P. aeruginosa (13.1% in the dentures versus 0.0% in the absence of dentures). Also respiratory pathogens such as S. aureus, S. pneumoniae, Haemophilus influenzae, and H. parainfluenzae were isolated in denture patients more than in normal individuals. Our result is similar to that reported by Tyrrell et al.,33, Sumi et al.,34, Goldberg et al.,35  and Senpuku et al.,36   where some uncommon microorganisms are found in oral microbiota but have been isolated from dentures and include respiratory pathogens such as S. aureus, S. pneumoniae, H. influenzae, H. para-influenzae, E. coli, K. pneumoniae, and P. mirabilis, Enterobacter cloacae and P. aeruginosa33-36. In a number of studies, 48% of sampled dentures harbored members of Enterobacteriaceae35,36. Inhalation pneumonia is a widespread cause of death among the debilitated elderly, and thus the role of dentures in harboring such potential pathogens may be important. A variety of potential respiratory pathogens had colonized the dentures (denture palague) of our examined patients, the predominant one being Staphylococcus spp. (33%), among them S. aureus contributes to 13.1%. The other putative respiratory pathogens were as follows: H. parainfluenzae (13.1%), K. pneumoniae (4.9%), and P. aeruginosa (16.4%) (Table 1). Dental plaque and tongue dorsa can serve as reservoirs for potential respiratory pathogens. Sumi et al.,37,38 concluded that denture plaque can act as a reservoir for potential pathogens to facilitate colonization in the oropharynx, and suggests that denture hygiene condition is an important factor in encouraging oropharyngeal bacterial colonization. It has been suggested that the surface of the tongue may also represent an additional, and probably more constant, reservoir of respiratory pathogens37,38. The majority of the antibiotics used in this study were usually prescribed by dentists39,40. The number of streptococci resistant to oral mutant is larger in people commonly exposed to antibiotics, even though resistant bacteria can also be established in healthy people who have not been in recent times treated with antibiotics39. β-Lactam antibiotics are the mainly commonly used chemo preventive agent’s in general dental practice. However, penicillin resistance among oral streptococci is increasing41.  The number of resistant oral streptococci is greater in people frequently exposed to antibiotics42, although these bacteria may also be found in healthy subjects who have not been recently treated with an antimicrobial43. Bacterial resistance to antibiotics such as penicillin and other β-Lactam is a health issue in numerous parts of the world. In current study it was observed that a significant level of oxacillin resistance (11.6%) in S. mutans isolates. The high prevalence of resistance to penicillin group in S. mutans in our study is like that previously observed in Yemen (14.9%)16, South Africa and Spain in oral S. viridans44,45. Several in-vitro studies have demonstrated the capability to transfer penicillin resistance determinants among related species46. These mecha-nisms, together with selective antibiotic pressure, may play an important role in the emergence and spread of penicillin resistance in oral streptococci. Also, the significant level of penicillin group resistance (11.6%) in S. mutans clinical isolates in our study is similar to Pasquantonio et al.,47 study that reported a significant level of penicillin resistance: 13.4% of 550 oral streptococcal clinical isolates, out of 50 isolates of S. mutans 14% were resistant to penicillin47. However, our result is lower than the rate of a study conducted in 2014 by Dhamodhar et al.,48 in which 38% isolates of S. mutans showed a complete resistance to penicillin and ampicillin. One-hour prior dental procedure, the American Heart Association suggests antimicrobial prophylaxis for high-risk cardiovascular patients, such as amoxicillin (2g) as first choice and clindamycin (600mg) as a second choice49. Production of β-lactamase is, however, unusual for most of streptococci, where resistance is happening by slightly altered of penicillin binding proteins50-52.

However, in our study we observed a significant level of tetracycline resistance (56.3%) in the isolates of S. mutans; and 13.4% for co-trimoxazole, and erythromycin (12.5%) and only 0.9% for clindamycin in the isolates. Thus, in this condition first choice should be going to clindamycin or cephalosporin’s in which resistance to cephalosporins is less than 4.5% (Table 4). Ultimately, the resistant developed by S. mutans is obscure. Updated information on antibiotic susceptibility testing such as reported in the present study helps to notify pharmaceutical makers to design new strategies for effective prophylaxis against dental infections. This result also gives an ideal choice to the dentist to prescribe a suitable antibiotic in Yemen.

 Limitations of the study

Verifying the composition of aerobic bacteria in the oral cavity of patients who have removable dentures and comparing them with those who have natural teeth in the world and Yemen has not been adequately studied. Conducting a prospective study to include more numbers of patients, studying anaerobic species, and testing other more numbers of antibiotics for common isolates.

 

CONCLUSION 

 

The study demonstrated an elevated rate of bacterial isolates from palate, back, tongue and plaque swabs in denture patients of pathogenic bacteria such as S. aureus and Enterobacteriaceae spp such as E. coli, K. pneumoniae, and P. aeruginosa; while in S. viridians including S. mutans, there was a lower colonization rate in denture patients verses a very high rate in individuals without dentures. Also, the study demonstrates significant levels of antibiotics resistance in S. aureus, CoNs and S. viridians oral isolates in dental patients.  Further study is required to know the minimum inhibitory concentration of β-Lactam and non β-Lactam antibiotics. In conclusion, denture hygiene is the obvious way to ensure that dentures stay clean. There are many oral hygiene products accessible for use by denture wearers.

 

ACKNOWLEDGEMENTS 

 

The authors thank the Faculty of Dentistry, Sana'a University, Sana'a, and Yemen for their generous support. 

 

AUTHOR’S CONTRIBUTIONS 

 

This article is part of a research supervised by Professor Hassan Al-Shamahy is the one who conceived the subject, wrote a draft of the manuscript and analyzed the data with other authors.

 

CONFLICT OF INTEREST 

 

No conflict of interest associated with this work. 

 

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