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Zamani S, Besharat S, Behnampour N, Behnam A, Asgari N, Mortazavi N. Detection and identification of Prevotella Melaninogenica in saliva samples of patients with ulcerative colitis. mljgoums 2024; 18 (2) :26-28
URL: http://mlj.goums.ac.ir/article-1-1697-en.html
URL: http://mlj.goums.ac.ir/article-1-1697-en.html
Samin Zamani1 
, Sima Besharat2 , Nasser Behnampour3 , Armina Behnam4 , Negar Asgari5 , Nazanin Mortazavi6
, Sima Besharat2 , Nasser Behnampour3 , Armina Behnam4 , Negar Asgari5 , Nazanin Mortazavi6
1- Department of Microbiology, School of Medicine, Golestan University of Medical Sciences, Gorgan, Iran;Infectious Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran
2- Golestan Research Center of Gastroenterology and Hepatology, Golestan University of Medical Sciences, Gorgan, Iran
3- Health Management and Social Development Research Center, Golestan University of Medical Sciences, Gorgan, Iran
4- Dental Research Center, Golestan University of Medical Sciences, Gorgan, Iran
5- Infectious Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran
6- Dental Research Center, Golestan University of Medical Sciences, Gorgan, Iran; Department of Oral and Maxillofacial Medicine, School of Dentistry, Golestan University of Medical Sciences, Gorgan, Iran ,mortazavi_nazanin@yahoo.com
2- Golestan Research Center of Gastroenterology and Hepatology, Golestan University of Medical Sciences, Gorgan, Iran
3- Health Management and Social Development Research Center, Golestan University of Medical Sciences, Gorgan, Iran
4- Dental Research Center, Golestan University of Medical Sciences, Gorgan, Iran
5- Infectious Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran
6- Dental Research Center, Golestan University of Medical Sciences, Gorgan, Iran; Department of Oral and Maxillofacial Medicine, School of Dentistry, Golestan University of Medical Sciences, Gorgan, Iran ,
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Introduction
Ulcerative colitis (UC), a chronic idiopathic inflammatory bowel disease (IBD) of the colon, results in a continuous, variable-intensity superficial mucosal inflammation that extends from the rectum to the more proximal colon. Relapsing and remitting symptoms are UC's defining features (1). The defining signs of UC are tenesmus, rectal urgency, and bloody diarrhea (2). The incidence of UC has been rising in Asia, especially in industrialized countries (3). The incidence of UC in 2020 was between 9 and 20 cases per 100,000 individuals annually (4). In a study conducted in Iran, Olfatifar et al. anticipated that between 2021 and 2030, there would be a 2.5-fold increase in the number of common cases of IBD (5).
According to studies, rather than being primarily due to genetic variances, ethnic and racial disparities are more closely tied to environmental factors, dietary preferences, and lifestyle choices. Population-based research has not revealed any appreciable gender disparities in UC. The incidence peak for UC is in the second and third decades of life, followed by a second high rate between 50 and 80 (6,7). Several epidemiological clues suggest that an imbalance in gut microbiota may be responsible for the development of Inflammatory Bowel Disease (IBD). Dysbiosis refers to the dysregulation of the immune system's reaction to bacterial antigens due to changed commensal bacterial population composition (8). Characterizing the dysbiotic state present in the gut microbiome of UC has been the focus of several studies. These studies have reported a decrease in bacterial diversity, a decrease in the relative proportions of Enterococcus and Bacteroides, a member of Clostridium subcluster XIVa, and an increase in several opportunistic pathogens (9). In addition, UC has also been linked to several extraintestinal symptoms, such as oral lesions, which can appear concurrently with intestinal symptoms or prior to the onset of the disease and may even be the main presenting symptom (10). IBD patients typically exhibit various oral symptoms, including aphthous stomatitis, oral ulcer, and pyostomatitis vegetans, suggesting a connection between these manifestations and the oral microbiota. The etiology of gastrointestinal disorders such as IBD may be influenced by the ectopic intestinal colonization of a specific oral bacterium (11-13). Prevotella is the largest genus in the oral cavity, and one of the major phyla is Bacteroides (14). P. melaninogenica resides in the oral cavity and colonizes the mucosal surfaces of infants in the first few months of life. Also, a high concentration of P. melaninogenica was observed in the back and lateral areas of the tongue and saliva (15,16). P. melaninogenica has hemagglutinating activity and agglutinates red blood cells despite its low pathogenicity (17). It has been observed that oral bacteria that survive the acidic conditions of the stomach gain access to the small intestine and large intestine, where they can interact with intestinal bacteria. Also, some studies recommended that P. melaninogenica was significantly increased in both ulcerative colitis and Crohn's disease patients, thus suggesting Prevotella as a potential predictor for these disorders (18).
This study aimed to examine P. melaninogenica in a group of UC patients and compare it with a control group to ascertain whether the oral cavity also demonstrates bacterial dysbiosis in the Golestan province, northeast of Iran.
Methods
This case-control study was conducted on patients with ulcerative colitis who were referred to the gastroenterology department of Shahid Sayad Shirazi Hospital in Gorgan between 2019 and 2020. Eighty individuals, including 40 UC patients and 40 healthy controls (HCs), participated in the study. A gastroenterologist conducted a clinical examination of the participants using the disease activity index. Individuals were identified as patients with IBD based on the criteria of history, clinical symptoms, clinical images, histopathology, and clinical standards. Healthy controls who did not have any known systemic diseases were selected after matching with the UC patients in terms of age and gender. The exclusion criteria were using systemic and topical antibacterial agents (such as chlorhexidine) in the last month, smoking in the last five years, and using corticosteroids in the last two years.
The study protocol was approved by the Ethics Committee of the Golestan University of Medical Science (IR.GOUMS.REC.1398.138) and was carried out following the rules outlined in the Helsinki Declaration. Before the study, all the participants were provided with detailed information about the study. After understanding the details, they signed a written consent form to confirm their willingness to participate.
The saliva samples were collected for both groups. Subjects were required to refrain from eating or drinking for one hour before taking the saliva samples. Saliva stimulation was obtained from individuals by directly spitting in two sterile plastic tubes. The samples were kept at -80 degrees Celsius until processing.
The DNA was extracted from a saliva sample using a DNA extraction kit (Favorgene). To extract DNA from saliva samples, suspensions were created in 400 microliters of buffer (TES (10 mM Tris [pH 8]), 5 mM EDTA, 50 mM NaCl) and centrifuged at 2000 rpm for 5 minutes to separate large particles. The supernatant was centrifuged again at 7000 rpm for 5 minutes to sediment the bacteria, and then DNA extraction was performed according to the kit protocol. At 260 nanometers, the isolated DNA's optical density (OD) was calculated. Then, the DNA was kept at minus 20 degrees (−20 °C) for real-time PCR.
The 16S rRNA gene sequence of P. melaninogenica was identified in the GenBank database, and the sequences were then aligned. The desired primer was finally verified (19) (Table 1). Each real-time PCR was performed in a 25-l volume with 10–100 picograms of template DNA and 100 nanomolar of each forward and reverse primer. The real-time PCR settings were 40 cycles of 95 °C for 15 s and 60 °C for 1 min each, followed by 50 °C for 2 min and 95 °C for 10 min (19).
Quantitative traits were calculated by estimating the mean and standard deviation, and frequency distribution tables were used for qualitative or classified data. According to the study design and the data features, if the normality of the data distribution was confirmed based on the Shapiro-Wilk test and the homogeneity of the variances based on the Lone test, the independent t-test was used to compare the average data in two groups. If the homogeneity of variances was not confirmed, the Welch t-test was applied. If the normality of the data distribution was not confirmed, the Mann-Whitney test was used. The analysis of the covariance method was used to adjust quantitative confounding variables, and the Mantel-Haenszel method for categorical variables was devoted. All data were analyzed using SPSS version 22.
Results
According to the independent t-test, the average age of people in the two groups was not significantly different (p =0.170). In addition, based on the chi-square test, the gender distribution in the two groups was not statistically significant (p =0.215).
As shown in Table 2, the frequency of P. melaninogenica in UC patients (77.5%) was significantly higher than in the control group (45%) (p = 0.003). The copy number of P. melaninogenica in UC patients (339 ± 1082.29) was also significantly higher than in the control group (61.29 ± 154.03) (p = 0.005). In women with UC, the number of P. melaninogenica was significantly higher than in the control group (p = 0.0342). Similarly, in men, the UC group (262.85 ± 664.97) had a significantly higher number than the control group (72.62 ± 222.76) (p = 0.015) (Table 2).
Discussion
Ulcerative colitis is a chronic and relapsing inflammatory disease of the large intestine that leads to the destruction and inflammation of the colonic mucosa. The main cause of this disease has not been discovered yet. However, it has been observed that some bacteria may play a role in predisposing patients to this disease. Previous studies have investigated the role of gut bacteria in UC. However, microbiota dysbiosis in other tissues, including the oral mucosa, has received less attention. Streptococcus, Prevotella, Haemophilus, and Veillonella are bacteria that have been extensively researched in this context. The presence of Prevotella may affect, positively or negatively, the severity of diseases, such as gastritis, Crohn’s disease, UC, and cancers. Prevotella spp. are obligate anaerobes that are isolated from the mouth cavity and primarily found on mucosal surfaces (20). Prevotella is thought to be a beneficial gut species since it is seen in greater abundance in the gut when a high-carbohydrate diet is followed (21). However, Prevotella species and other members of the natural microflora are responsible for a number of local reactions, including UC, arthritic conditions, and gastrointestinal disorders (22). Dysbiosis changes the immune system, disrupts homeostasis, and increases the production of several virulence factors; in this regard, it can cause Prevotella species to turn from a normal bacterium into a pathobiont. With the help of these factors, they can survive regardless of environmental change. Thus, they survive and inhibit the infected area. The interplay between pathogenicity and the host's defense mechanisms against them determines the onset and course of the disease (23,24).
In this regard, this study aimed to investigate the frequency of P. melaninogenica bacteria in UC patients compared to the control subjects, and the intensity of this bacterium was investigated in two groups. According to the results, the frequency of P. melaninogenica in UC patients was higher than in the healthy controls, and this difference was statistically significant (p=0.003). In a study conducted by Qi et al., Prevotella (besides Veillonella) and P. melaninogenica significantly increased in both Crohn’s disease and ulcerative colitis patients. The genus Prevotella was proposed as a potential marker linked to IBD, especially Crohn’s disease (18). In addition, a 2017 study revealed greater levels of several oral bacteria in the feces microbiota of UC patients, identifying species from the genus Prevotella (25). In another study, it was shown that the dysbiosis of distinct salivary microbiota was influential in the development of IBD. Some bacteria, including Leptotrichia, Prevotella, Bolidia, and Atopobium, showed a significant increase (18). However, in a study conducted in 2022, different species of Streptococcus, Uribacterium, Ruthia, Provetella, and Porphyromonas were not found in the saliva samples of the UC group (26). In this regard, it is noteworthy that the saliva samples of UC patients lacked several species that are important components of the oral core microbiome, such as Prevotella members (P. salivae, P. histicola, and P. melaninogenica). This finding has also been observed in IBD patients (27).
In addition, results showed a significantly higher count of P. melaninogenica bacteria in the patient group compared to the control group. A study by Ying Qi et al. showed that the dysbiosis of distinct salivary microbiota, such as Prevotella, which increased significantly, is influential in the development of IBD (18).
Conclusion
In conclusion, this study described that higher frequency and number of P. melaninogenica in UC patients' saliva could contribute to the oral dysbiosis observed in UC. This data supports the hypothesis that UC may be associated not only with gut microbial imbalance but also with other microbial community imbalances, such as oral dysbiosis. Currently, there is limited data to describe the relationship between P. melaninogenica in the oral cavity and gastrointestinal disorders. Further investigation on a larger scale with a more powerful design is necessary to recommend this bacterium as an oral biomarker for UC.
Acknowledgement
We would like to thank Dr. Alireza Norouzi and Dr. Taghi Amiriani for their contributions to our project. Their assistance in granting us access to their patients has been critical to the success of our research.
Funding sources
This research was supported by Golestan University of Medical Sciences (Grant No. 110619). The funding source did not participate in the study design, data collection, analysis, interpretation, or manuscript preparation.
Ethical statement
This study received ethical approval from the Golestan University of Medical Sciences Ethical Committee in Iran (IR.GOUMS.REC.1398.138). The study was conducted in accordance with the current and seventh edition of the Declaration of Helsinki. All participants provided written informed consent.
Conflicts of interest
The authors declare no conflict of interest.
Author contributions
SZ assisted in conceptualization, methodology, supervision, original draft preparation, review, and editing. SB assisted in conceptualization, review, and editing. NB assisted in statistical analysis, review, and editing. NA assisted in data collection and original draft preparation. AB assisted in sample collection. NM assisted in conceptualization, methodology, supervision, original draft preparation, review, and editing. All authors have read and approved the final manuscript.
Ulcerative colitis (UC), a chronic idiopathic inflammatory bowel disease (IBD) of the colon, results in a continuous, variable-intensity superficial mucosal inflammation that extends from the rectum to the more proximal colon. Relapsing and remitting symptoms are UC's defining features (1). The defining signs of UC are tenesmus, rectal urgency, and bloody diarrhea (2). The incidence of UC has been rising in Asia, especially in industrialized countries (3). The incidence of UC in 2020 was between 9 and 20 cases per 100,000 individuals annually (4). In a study conducted in Iran, Olfatifar et al. anticipated that between 2021 and 2030, there would be a 2.5-fold increase in the number of common cases of IBD (5).
According to studies, rather than being primarily due to genetic variances, ethnic and racial disparities are more closely tied to environmental factors, dietary preferences, and lifestyle choices. Population-based research has not revealed any appreciable gender disparities in UC. The incidence peak for UC is in the second and third decades of life, followed by a second high rate between 50 and 80 (6,7). Several epidemiological clues suggest that an imbalance in gut microbiota may be responsible for the development of Inflammatory Bowel Disease (IBD). Dysbiosis refers to the dysregulation of the immune system's reaction to bacterial antigens due to changed commensal bacterial population composition (8). Characterizing the dysbiotic state present in the gut microbiome of UC has been the focus of several studies. These studies have reported a decrease in bacterial diversity, a decrease in the relative proportions of Enterococcus and Bacteroides, a member of Clostridium subcluster XIVa, and an increase in several opportunistic pathogens (9). In addition, UC has also been linked to several extraintestinal symptoms, such as oral lesions, which can appear concurrently with intestinal symptoms or prior to the onset of the disease and may even be the main presenting symptom (10). IBD patients typically exhibit various oral symptoms, including aphthous stomatitis, oral ulcer, and pyostomatitis vegetans, suggesting a connection between these manifestations and the oral microbiota. The etiology of gastrointestinal disorders such as IBD may be influenced by the ectopic intestinal colonization of a specific oral bacterium (11-13). Prevotella is the largest genus in the oral cavity, and one of the major phyla is Bacteroides (14). P. melaninogenica resides in the oral cavity and colonizes the mucosal surfaces of infants in the first few months of life. Also, a high concentration of P. melaninogenica was observed in the back and lateral areas of the tongue and saliva (15,16). P. melaninogenica has hemagglutinating activity and agglutinates red blood cells despite its low pathogenicity (17). It has been observed that oral bacteria that survive the acidic conditions of the stomach gain access to the small intestine and large intestine, where they can interact with intestinal bacteria. Also, some studies recommended that P. melaninogenica was significantly increased in both ulcerative colitis and Crohn's disease patients, thus suggesting Prevotella as a potential predictor for these disorders (18).
This study aimed to examine P. melaninogenica in a group of UC patients and compare it with a control group to ascertain whether the oral cavity also demonstrates bacterial dysbiosis in the Golestan province, northeast of Iran.
Methods
This case-control study was conducted on patients with ulcerative colitis who were referred to the gastroenterology department of Shahid Sayad Shirazi Hospital in Gorgan between 2019 and 2020. Eighty individuals, including 40 UC patients and 40 healthy controls (HCs), participated in the study. A gastroenterologist conducted a clinical examination of the participants using the disease activity index. Individuals were identified as patients with IBD based on the criteria of history, clinical symptoms, clinical images, histopathology, and clinical standards. Healthy controls who did not have any known systemic diseases were selected after matching with the UC patients in terms of age and gender. The exclusion criteria were using systemic and topical antibacterial agents (such as chlorhexidine) in the last month, smoking in the last five years, and using corticosteroids in the last two years.
The study protocol was approved by the Ethics Committee of the Golestan University of Medical Science (IR.GOUMS.REC.1398.138) and was carried out following the rules outlined in the Helsinki Declaration. Before the study, all the participants were provided with detailed information about the study. After understanding the details, they signed a written consent form to confirm their willingness to participate.
The saliva samples were collected for both groups. Subjects were required to refrain from eating or drinking for one hour before taking the saliva samples. Saliva stimulation was obtained from individuals by directly spitting in two sterile plastic tubes. The samples were kept at -80 degrees Celsius until processing.
The DNA was extracted from a saliva sample using a DNA extraction kit (Favorgene). To extract DNA from saliva samples, suspensions were created in 400 microliters of buffer (TES (10 mM Tris [pH 8]), 5 mM EDTA, 50 mM NaCl) and centrifuged at 2000 rpm for 5 minutes to separate large particles. The supernatant was centrifuged again at 7000 rpm for 5 minutes to sediment the bacteria, and then DNA extraction was performed according to the kit protocol. At 260 nanometers, the isolated DNA's optical density (OD) was calculated. Then, the DNA was kept at minus 20 degrees (−20 °C) for real-time PCR.
The 16S rRNA gene sequence of P. melaninogenica was identified in the GenBank database, and the sequences were then aligned. The desired primer was finally verified (19) (Table 1). Each real-time PCR was performed in a 25-l volume with 10–100 picograms of template DNA and 100 nanomolar of each forward and reverse primer. The real-time PCR settings were 40 cycles of 95 °C for 15 s and 60 °C for 1 min each, followed by 50 °C for 2 min and 95 °C for 10 min (19).
|
Table 1. Sequences of oligonucleotide primers of P. melaninogenica (19)
.PNG) |
Results
According to the independent t-test, the average age of people in the two groups was not significantly different (p =0.170). In addition, based on the chi-square test, the gender distribution in the two groups was not statistically significant (p =0.215).
As shown in Table 2, the frequency of P. melaninogenica in UC patients (77.5%) was significantly higher than in the control group (45%) (p = 0.003). The copy number of P. melaninogenica in UC patients (339 ± 1082.29) was also significantly higher than in the control group (61.29 ± 154.03) (p = 0.005). In women with UC, the number of P. melaninogenica was significantly higher than in the control group (p = 0.0342). Similarly, in men, the UC group (262.85 ± 664.97) had a significantly higher number than the control group (72.62 ± 222.76) (p = 0.015) (Table 2).
|
Table 2. Demographic characteristics, the frequency and copy number of P. melaninogenica in UC patients, controls, and its distribution among females and males
.PNG) |
Discussion
Ulcerative colitis is a chronic and relapsing inflammatory disease of the large intestine that leads to the destruction and inflammation of the colonic mucosa. The main cause of this disease has not been discovered yet. However, it has been observed that some bacteria may play a role in predisposing patients to this disease. Previous studies have investigated the role of gut bacteria in UC. However, microbiota dysbiosis in other tissues, including the oral mucosa, has received less attention. Streptococcus, Prevotella, Haemophilus, and Veillonella are bacteria that have been extensively researched in this context. The presence of Prevotella may affect, positively or negatively, the severity of diseases, such as gastritis, Crohn’s disease, UC, and cancers. Prevotella spp. are obligate anaerobes that are isolated from the mouth cavity and primarily found on mucosal surfaces (20). Prevotella is thought to be a beneficial gut species since it is seen in greater abundance in the gut when a high-carbohydrate diet is followed (21). However, Prevotella species and other members of the natural microflora are responsible for a number of local reactions, including UC, arthritic conditions, and gastrointestinal disorders (22). Dysbiosis changes the immune system, disrupts homeostasis, and increases the production of several virulence factors; in this regard, it can cause Prevotella species to turn from a normal bacterium into a pathobiont. With the help of these factors, they can survive regardless of environmental change. Thus, they survive and inhibit the infected area. The interplay between pathogenicity and the host's defense mechanisms against them determines the onset and course of the disease (23,24).
In this regard, this study aimed to investigate the frequency of P. melaninogenica bacteria in UC patients compared to the control subjects, and the intensity of this bacterium was investigated in two groups. According to the results, the frequency of P. melaninogenica in UC patients was higher than in the healthy controls, and this difference was statistically significant (p=0.003). In a study conducted by Qi et al., Prevotella (besides Veillonella) and P. melaninogenica significantly increased in both Crohn’s disease and ulcerative colitis patients. The genus Prevotella was proposed as a potential marker linked to IBD, especially Crohn’s disease (18). In addition, a 2017 study revealed greater levels of several oral bacteria in the feces microbiota of UC patients, identifying species from the genus Prevotella (25). In another study, it was shown that the dysbiosis of distinct salivary microbiota was influential in the development of IBD. Some bacteria, including Leptotrichia, Prevotella, Bolidia, and Atopobium, showed a significant increase (18). However, in a study conducted in 2022, different species of Streptococcus, Uribacterium, Ruthia, Provetella, and Porphyromonas were not found in the saliva samples of the UC group (26). In this regard, it is noteworthy that the saliva samples of UC patients lacked several species that are important components of the oral core microbiome, such as Prevotella members (P. salivae, P. histicola, and P. melaninogenica). This finding has also been observed in IBD patients (27).
In addition, results showed a significantly higher count of P. melaninogenica bacteria in the patient group compared to the control group. A study by Ying Qi et al. showed that the dysbiosis of distinct salivary microbiota, such as Prevotella, which increased significantly, is influential in the development of IBD (18).
Conclusion
In conclusion, this study described that higher frequency and number of P. melaninogenica in UC patients' saliva could contribute to the oral dysbiosis observed in UC. This data supports the hypothesis that UC may be associated not only with gut microbial imbalance but also with other microbial community imbalances, such as oral dysbiosis. Currently, there is limited data to describe the relationship between P. melaninogenica in the oral cavity and gastrointestinal disorders. Further investigation on a larger scale with a more powerful design is necessary to recommend this bacterium as an oral biomarker for UC.
Acknowledgement
We would like to thank Dr. Alireza Norouzi and Dr. Taghi Amiriani for their contributions to our project. Their assistance in granting us access to their patients has been critical to the success of our research.
Funding sources
This research was supported by Golestan University of Medical Sciences (Grant No. 110619). The funding source did not participate in the study design, data collection, analysis, interpretation, or manuscript preparation.
Ethical statement
This study received ethical approval from the Golestan University of Medical Sciences Ethical Committee in Iran (IR.GOUMS.REC.1398.138). The study was conducted in accordance with the current and seventh edition of the Declaration of Helsinki. All participants provided written informed consent.
Conflicts of interest
The authors declare no conflict of interest.
Author contributions
SZ assisted in conceptualization, methodology, supervision, original draft preparation, review, and editing. SB assisted in conceptualization, review, and editing. NB assisted in statistical analysis, review, and editing. NA assisted in data collection and original draft preparation. AB assisted in sample collection. NM assisted in conceptualization, methodology, supervision, original draft preparation, review, and editing. All authors have read and approved the final manuscript.
Research Article: Research Article |
Subject:
Microbiology
Received: 2023/08/1 | Accepted: 2023/11/1 | Published: 2024/03/30 | ePublished: 2024/03/30
Received: 2023/08/1 | Accepted: 2023/11/1 | Published: 2024/03/30 | ePublished: 2024/03/30
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.