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PREVOTELLA SPECIES – THE MOST PREVALENT
Original Articles
BLACK-PIGMENTED ANAEROBIC BACTERIA AMONG
OROPHARYNGEAL ISOLATES OBTAINED FROM
A SAMPLE OF HEALTHY YOUNG ADULTS
Gabriela Băncescu1a* , Lidia Sfetcu1b , Andreea Cristiana Didilescu2c , Adrian Anton Băncescu3d
1
Department of Microbiology, Faculty of Dental Medicine, "Carol Davila" University of Medicine and Pharmacy Bucharest, Bucharest, Romania
2
Department of Embryology, Faculty of Dental Medicine, "Carol Davila" University of Medicine and Pharmacy Bucharest, Bucharest, Romania
3
Department of Epidemiology, Faculty of Medicine, "Carol Davila" University of Medicine and Pharmacy Bucharest, Bucharest, Romania
a
MD, MSc, PhD, Professor, Head; e-mail: gabi.bancescu@yahoo.com; ORCIDiD: https://orcid.org/0000-0003-2827-2465
b
DMD, PhD, Assistant Professor; e-mail: lidia.ciobanu@ymail.com; ORCIDiD: https://orcid.org/0000-0002-4023-5053
c
DMD, MPhil, PhD, Professor, Head, Vice-Dean; e-mail: andreea.didilescu@gmail.com; ORCIDiD: http://orcid.org/0000-0002-2915-5124
d
MD, MSc, PhD, Associate Professor; e-mail: adrianbancescu@yahoo.com; ORCIDiD: https://orcid.org/0000-0003-4164-9810
ABSTRACT https://doi.org/10.25241/stomaeduj.2020.7(2).art.1
Introduction The black-pigmented Prevotella - Porphyromonas group comprises members of the normal
flora of the oral cavity, oropharyngeal, intestinal and genitourinary tract, but may be associated with various
infections too. The purpose of this study was to identify the species of this anaerobic group which frequently
colonize the oropharynx in clinically healthy young adults.
Methodology The microbiological investigation was carried out on a strain collection of 93 dark-pigmented
anaerobic isolates originated from the oropharynx of healthy dental students, at the Department of
Microbiology, Faculty of Dental Medicine, “Carol Davila” University of Medicine and Pharmacy - Bucharest.
All isolates of Gram-negative bacilli were identified at the genus and species level by conventional methods,
MASTRING ID (MAST Group Ltd., U.K.) and Rapid ID 32 A system (BioMérieux, France), while the isolates of
anaerobic cocci were tested only by MASTRING ID.
Results The microscopy of the Gram-stained smears and the results of the MASTRING ID test performed
with the 93 black-pigmented anaerobic isolates indicated that 77 strains were Gram-negative bacilli and/
or coccobacilli, while 16 strains were Gram-positive cocci. The identification of the Gram-negative bacilli
at the species level concluded that 57 strains belonged to Prevotella denticola, 18 strains to Prevotella
melaninogenica and 2 strains to Prevotella intermedia.
Conclusion P. denticola and P. melaninogenica might be considered the main species of the black-pigmented
Prevotella-Porphyromonas group which colonize the oropharynx in healthy young adults. These species are
usually beta-lactamase producers and their high rate of oropharyngeal colonization should be considered
when antibiotics are needed in oral infections therapy.
KEYWORDS
Oropharynx, Microbiota, Anaerobes, Black-Pigmented Bacteria, Prevotella.
1. INTRODUCTION secretion. The oropharynx microbiota is complex
and comprises hundreds of microbial species [2,3],
The oropharynx comprises the palatine tonsils, most of them organized in biofilms associated
tongue base, soft palate and posterior pharyngeal with the respective microenvironment [4]. About
wall and is lined by a nonkeratinized stratified 80% of the local normal flora is represented by the
squamous epithelium [1]. The oropharynx mucosa viridans streptococci and commensal species of
comes in contact with saliva and nasopharyngeal Haemophilus and Neisseria [5,6]. Besides different
OPEN ACCESS This is an Open Access article under the CC BY-NC 4.0 license.
Peer-Reviewed Article
Citation: Băncescu G, Sfetcu L, Didilescu AC, Băncescu AA. Prevotella species – the most prevalent black-pigmented anaerobic bacteria among
oropharyngeal isolates obtained from a sample of healthy young adults. Stoma Edu J. 2020;7(2):87-93.
Received: March 19, 2020; Revised: April 17, 2020; Accepted: May 20, 2020; Published: May 22, 2020
*Corresponding author: Professor Gabriela Băncescu, MD, MSc, PhD, Department of Microbiology, Faculty of Dental Medicine, "Carol Davila"
University of Medicine and Pharmacy (CDUMPB), D. Gerota Str. 19-21, RO-020032-Bucharest, Romania.
Tel./Fax: +40 771027131; e-mail: gabi.bancescu@yahoo.com
Copyright: © 2020 the Editorial Council for the Stomatology Edu Journal.
Stoma Edu J. 2020;7(2): 87-93 pISSN 2360-2406; eISSN 2502-0285 87
Băncescu G, et al.
www.stomaeduj.com
species of Mycoplasma, Corynebacterium and in human pathology [23]. The present study intended
Original Articles staphylococci, the oropharynx may harbor also to contribue to the investigation of black-pigmented
pathogenic or potentially pathogenic bacteria like: Gram-negative anaerobic bacilli, since the anaerobic
Streptococcus pyogenes, Streptococcus agalactiae, bacteria are not commonly cultivated by many
Streptococcus dysgalactiae subsp. equisimilis, S. microbiology laboratories. Thus, the aim of this
pneumoniae, Neisseria meningitidis, Haemophilus study was to identify the species belonging to this
influenzae or Moraxella catarrhalis [6-14]. Some bacterial category which colonize the oropharynx in
studies reported that the dominant bacteria of healthy young adults most frequently.
the normal oropharyngeal flora are the anaerobes
[15]. The persistence of anaerobic bacteria is 2. METHODOLOGY
favored by the anaerobic conditions found into the
depth of the biofilm covering the oropharyngeal The microbiological investigation was performed
mucosa, mainly due to the oxygen consumption on a collection of 93 black-pigmented anaerobic
by aerobic and facultative anaerobic bacteria. The bacterial strains stored at -700C, at the laboratory of
mucosal convolutions and especially the tonsils the Department of Microbiology, Faculty of Dental
crypts may be considered important anaerobic Medicine, “Carol Davila” University of Medicine
microhabitats. At these sites, the strictly anaerobes and Pharmacy (CDUMP) Bucharest. The respective
are found in high proportion with Prevotella being strains originated from oropharyngeal swab samples
the most frequently isolated species [16,17]. Most collected from 29 male dental students and 64
Gram-negative anaerobic bacteria colonizing the female dental students, aged 20-34 years, at the
oropharynx in healthy adults belong to the following same Microbiology department, in April 2018. They
genera: Prevotella, Fusobacterium, Leptotrichia were second-year students, were clinically healthy
and Veillonella [2,18-22]. Some researchers also and had not taken antibiotics in the last 6 months.
found Porphyromonas at this site, but except for Twenty-four of them were smokers: 7 male subjects
Prevotella spp., the other anaerobes were isolated and 17 female subjects. Prior to the present study,
in much smaller percentages than the facultative cultures from the 93 oropharyngeal swab samples
anaerobes, such as: streptococci, staphylococci were performed on Schaedler agar with 5% sheep
and diphteromorphs [16]. The conclusion of a blood (BioMérieux, France), which were incubated
Norwegian-American research team that applied in GENbox, with GENbox anaer sachet and Anaer
cultural-independent molecular techniques to indicator (BioMérieux, France), at 350C, for 10
determine the microbial diversity of the oral flora days, with examination every 48h. All isolates that
was that there is a distinctive dominant oral flora developed black pigment and showed negative
in healthy subjects, with site-specificity and high results in the aerotolerance test were stored in
diversity [23]. The same team found an unexpected cryobiles, at -700C and constituted the collection of
high diversity at tonsils level (more than 50 different strains used in the present study. At the beginning
species) with high variation between subjects [23]. of this study conducted in the second semester
Thus, Prevotella and Porphyromonas spp. were of 2018, the black-pigmented anaerobic strains
isolated from some subjects, but were missing belonging to the above mentioned collection were
in others who were harboring mostly bacteria checked for their morphotinctorial characteristics by
belonging to the phylum Firmicutes [23]. microscopic examination of Gram-stained smear. All
Some bacterial community analysis indicated Gram-negative bacilli strains were further identified
that the main group associated with the throat by the conventional methods, MAST ID MID8
microbiota comprises: species belonging to ANAEROBE ID RING/MASTRING ID (MAST Group Ltd.,
Streptococcus and other genera of Firmicutes, U.K.) and Rapid ID 32 A system (BioMérieux, France).
species belonging to the family of Pasteurellaceae, The presumptive identification of the Gram-negative
Fusobacterium spp. and Actinomyces spp., while the bacilli strains was performed by testing their ability to
main group associated with the tonsils includes grow in the presence of 20% bile (by streaking them
species of Streptococcus, Mogibacterium and other on Bacteroides bile-esculin agar, BBE) and by testing
Firmicutes, Fusobacterium spp., Prevotella spp. and their susceptibility to: vancomycin (5 μg), kanamycin
members of the family Pasteurellaceae [24]. In healthy (1000 μg), colistin sulphate (10 μg), erythromycin
persons, the core microbiome plays a major role (60 μg), penicillin G (2 units) and rifampicin (15 μg)
in homeostasis [25]. In children, an oropharyngeal by applying the MASTRING ID on blood agar plates
microbiome similar to that of adults was described, (BioMérieux, France) seeded with bacterial inoculum
but richer in Prevotella, Neisseria, Granulicatella, adjusted to the turbidity of 2 McFarland standard.
Porphyromonas and Fusobacterium [26]. At present The plates were incubated in anaerobic atmosphere,
high efforts are required for advanced research at 350C, for 48h. Bacteroides fragilis ATCC 25285 was
of normal flora of the oral cavity and oropharynx, used as quality control. These tests were interpreted
estimating that future findings may substantially based on the indication mentioned in the textbooks
contribute to understanding the role played by the of diagnostic microbiology [27], completed with
microorganisms with oral or oropharyngeal habitat the recommendation given by the MASTRING ID
88 Stoma Edu J. 2020;7(2): 87-93 pISSN 2360-2406; eISSN 2502-0285
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Original Articles
Figure 1. MASTRING ID test applied on a strain of black-pigmented Figure 2. The distribution of the 77 strains of black-pigmented
Gram-negative anaerobic bacilli. Gram-negative anaerobic bacilli by species.
found susceptible to penicillin. The interpretation
of the tests according to the textbook of diagnostic
microbiology [27] and MASTRING ID producer
indicated that all these bacilli strains belonged to the
genus Prevotella. The Rapid ID 32 A system indicated
that 57 strains were Prevotella denticola, 18 strains
were Prevotella melaninogenica and 2 strains were
Prevotella intermedia (Fig. 2). In 5 subjects, pairs of P.
denticola - P. melaninogenica were isolated. Twenty
of the 72 students with black-pigmented Prevotella
oropharyngeal colonization were smokers. Figure 3
Figure 3. P. intermedia strain identified by the Rapid ID 32 A system.
presents the biochemical profile of a P. intermedia
strain obtained with the Rapid ID 32 A gallery (Fig. 3).
A p-value of 0.5737 was found when applying the
producer. In addition, the MASTRING ID test was also Fisher exact test, indicating no statistically significant
applied to the coccus-shaped anaerobic isolates. correlation between smoking and colonization
The Fisher exact test was used to find any statistically of the oropharynx with black-pigmented Gram-
significant association between smoking (data on negative anaerobic bacilli.
this habit being received from students prior to this
study, when oropharyngeal swab samples were 4. DISCUSSION
collected) and oropharynx colonization with black-
pigmented Gram-negative anaerobic bacilli species. The normal oropharyngeal flora may show variability
The chosen significance level was p ≤ 0.05. among healthy individuals due to external factors
and ecological relationship. The investigation of the
3. RESULTS microbial relationship may contribute to clarifying
many underlying aspects [28]. Anaerobic bacteria
The microscopic examination of the Gram-stained are not currently investigated by many laboratories
smears from the culture of dark-pigmented due to the laborious and expensive work required.
anaerobic strains indicated that 77 of the 93 isolates Porphyromonas and Prevotella (previously belonging
were Gram-negative bacilli and/or coccobacilli. The to the genus Bacteroides) also include, besides
microscopy showed that the other 16 strains were non-pigmented species, dark-pigmented species
Gram-positive cocci (arranged mainly in irregular like: Porphyromonas gingivalis, Porphyromonas
clusters) and this was in complete agreement with endodontalis, Porphyromonas asaccharolytica, and
the results of the MASTRING ID. Figure 1 illustrates Prevotella intermedia, Prevotella nigrescens, Prevotella
the result of the MASTRING ID test applied to a melaninogenica, Prevotella loescheii, Prevotella
strain of black-pigmented Gram-negative anaerobic denticola and Prevotella corporis, respectively
bacilli (Fig. 1). The microbiological investigation [29]. This study focused on the investigation of
carried out on the dark-pigmented Gram-negative the oropharynx colonization by dark-pigmented
anaerobic bacilli and/or coccobacilli isolates Prevotella and Porphyromonas species. The culture
showed that all of them were susceptible to 20% method allowed the isolation of the black-pigmented
bile, rifampicin and erythromycin, but resistant to anaerobic strains. Because the development of
kanamycin and vancomycin. The results concerning dark-pigment is usually a delayed process, primary
the susceptibility to colistin and penicillin G varied, cultures (which were obtained prior to this study)
45 strains being found susceptible and 32 strains were checked throughout the incubation period.
resistant to colistin, while only 19 strains were The present study began with the selection of
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the bacilli strains among the 93 black-pigmented greater number of species belonging to the genera:
Original Articles anaerobic isolates and continued with the species Megasphaera, Streptococcus, Veillonella, Atopobium,
identification, based on both conventional and Eggerthella, Dorea, Anaerovorax, Eubacterium and
rapid methods. P. denticola, P. melaninogenica and P. to the family Erysipelotrichaceae [24]. Many of these
intermedia were the only black-pigmented anaerobic bacteria can also be involved in oral infections.
bacilli species isolated from the oropharynx in this Some researchers found that significant changes
group of 93 healthy young dental students. The occurring in the resident microbial population from
results obtained with the Rapid ID 32 A system oral and nasopharyngeal microbiota in smokers are
showed very good to excellent identification for all correlated with higher frequencies of infections than
but 6 strains. The identification at species level of the in non-smokers [40]. Oropharyngeal flora varies due
6 strains mentioned above indicated P. denticola as to many other factors, such as age and health status.
the first choice and Prevotella oralis as the second In most studies focusing on the upper respiratory
choice. These isolates were considered to belong to tract flora, mainly oral and nasopharyngeal flora
P. denticola because P. oralis is known to not produce have been investigated in children, the elderly and
colonies with dark pigment. Atypical phenotypic patients suffering from various diseases [41-47].
characteristics of isolates can sometimes lead to However, updated data on changes in oropharynx
misidentification of species. Therefore, the culture- flora in healthy young adults are also needed.
independent methods are highly recommended for Influenced by data from recent specialty literature,
the detection of anaerobic species. However, both special attention was paid in the present research
culture-based method and detection by molecular to analyze the association between smoking and
techniques also have advantages and limitations. colonization of oropharynx with black-pigmented
Previous studies performed in adults and children Gram-negative anaerobic bacilli in the group
reported P. melaninogenica in a higher percentage of healthy young adults from whom the strains
in patients with tonsilar crypts who suffer from were isolated. Although the findings showed
recurrent tonsillitis, compared to healthy subjects no statistically significant correlation, for a more
with adenotonsillar hyperplasia [17]. Recent studies accurate interpretation of the results, this study
reported that P. melaninogenica colonizes the tonsils should be continued on a larger sample size.
in large quantities [30]. Isolates of this species are It is important to understand that maintaining
usually beta-lactamase producers [31] and this may a normal oropharyngeal and nasopharyngeal
explain the failure of penicillin treatment in recurrent microbiota is an important step in maintaining good
tonsillitis [32]. The bacteria that produce enzymes health.
that destroy the beta-lactam ring of penicillin
indirectly protect penicillin-sensitive bacteria such 5. CONCLUSIONS
as S. pyogenes [33]. Changes in the oropharyngeal
ecology can variably affect the oropharyngeal The findings of this study indicated P. denticola and
microbiota. Smoking is one of the main external P. melaninogenica as the main species of black-
factors that can directly influence the composition pigmented Gram-negative anaerobic bacilli that
of the upper airway microbiota [2]. Both active and colonize oropharynx in healthy young adults. The
passive smoking can contribute to colonization well-known beta-lactamase activity of these bacteria
of the upper respiratory tract with pathogenic should be strongly considered when antibiotics are
microorganisms [34,35] by impairing the immune needed in oral infection therapy.
response and favoring bacterial colonization, either
by stimulating microbial adhesion to the epithelium CONFLICT OF INTEREST
or by other means [36,37]. Prevotella comprises The authors declare no conflict of interest.
commensal species from the human microbiota,
which usually protect the upper respiratory tract AUTHOR CONTRIBUTIONS
against colonization of pathogenic bacteria [24,35].
Some studies have reported that nasopharynx in All authors had equal contribution to the paper.
smokers frequently hosts Streptococcus pneumoniae,
Haemophilus influenzae and Moraxella catarrhalis, ACKNOWLEDGEMENTS
while Prevotella is absent [24,35]. It has been
observed that the oral cavity and the nasopharynx This study was part of the internal research plan for 2018 of the
became colonized again with the normal resident Department of Microbiology, Faculty of Dental Medicine, "Carol
flora when smoking was abandoned [38,39]. Recent Davila" University of Medicine and Pharmacy (CDUMPB) and was
research using univariate analysis and machine carried out in co-operation with the Head of the Department of
learning approaches has concluded that smokers Embryology and a member of the Department of Epidemiology,
compared to non-smokers are colonized with a "Carol Davila" University of Medicine and Pharmacy (CDUMPB).
90 Stoma Edu J. 2020;7(2): 87-93 pISSN 2360-2406; eISSN 2502-0285
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Gabriela BĂNCESCU
MD, MSc, PhD, Professor, Head
Department of Microbiology, Faculty of Dental Medicine
“Carol Davila” University of Medicine and Pharmacy Bucharest
Bucharest, Romania
CV
Professor Gabriela Băncescu is the Head of the Microbiology Department, Faculty of Dental Medicine, “Carol Davila” University
of Medicine and Pharmacy Bucharest, Bucharest, Romania. She was awarded a Master’s degree in Oral Microbiology by the
University of Bergen, Norway. She was a member of the board of the European Society of Chemotherapy - Infectious Diseases.
She is a member of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and was a member of ESCMID
Study Group for Anaerobic Infections. She was the Secretary General of the Romanian Society of Laboratory Medicine (2009-
2014) and a member of the editorial board of the Bacteriol Virusol Parazitol Epidemiol, Infectio.ro and the Roum Arch Microbiol
Immunol. At present, she is an Editor of the Stoma Edu J and Associate Editor of Rom J Rhinol.
92 Stoma Edu J. 2020;7(2): 87-93 pISSN 2360-2406; eISSN 2502-0285
Black-pigmented anaerobes that colonize the oropharynx
www.stomaeduj.com
Questions
Original Articles
1. Prevotella originated from the genus?
qa. Bacteroides;
qb. Fusobacterium;
qc. Tannerella;
qd. Porphyromonas.
2. Prevotella comprises species of?
qa. Gram-positive anaerobic bacilli;
qb. Gram-negative anaerobic bacilli;
qc. Gram-negative anaerobic cocci;
qd. Gram-negative aerobic bacilli.
3. Exemples of black-pigmented anaerobic species?
qa. Prevotella melaninogenica, Prevotella oralis and Prevotella nigrescens;
qb. Porphyromonas gingivalis, Porphyromonas endodontalis and Prevotella oralis;
qc. Prevotella melaninogenica, Prevotella intermedia and Prevotella nigrescens;
qd. Prevotella intermedia, Porphyromonas gingivalis and Prevotella oralis.
4. The beta-lactamase?
qa. Is never produced by black-pigmented anaerobic strains;
qb. Enhances the penicillin effect against anaerobic bacteria;
qc. Enhances the penicillin effect against aerobic bacteria;
qd. Cleaves the beta-lactam ring of beta-lactam antibiotics.
Stoma Edu J. 2020;7(2): 87-93 pISSN 2360-2406; eISSN 2502-0285 93