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Effects of Lactobacillus reuteri Intake on the Periodontal Pathogens
Int J Clin Prev Dent 2024;20(1):12-18
Published online March 31, 2024;  https://doi.org/10.15236/ijcpd.2024.20.1.12
© 2024 International Journal of Clinical Preventive Dentistry.

Hyun-Jin Kim1, Ja-Won Cho2, Da-Hui Kim3, Won-Ju Kang1

1Department of Oral Health, College of Health Science, Dankook University, Cheonan, 2Department of Preventive Dentistry, College of Dentistry, Dankook University, Cheonan, 3Department of Dental Hygiene, Andong Science College, Andong, Korea
Correspondence to: Won-Ju Kang
E-mail: rkddnjswn0@naver.com
https://orcid.org/0009-0005-1915-0222
Received February 19, 2024; Revised March 20, 2024; Accepted March 20, 2024.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Objective: The aim of this study was to determine the quantitative changes in four oral microorganisms associated with periodontitis after consumption of L. reuteri DSM 17938 and L. reuteri ATCC PTA5289, and to investigate the changes in oral microorganisms after consumption of L. reuteri, which is known to help improve periodontitis.
Methods: Subjects were 30 males and females aged 20 years or older who had periodontitis with a baseline pocket size of 4 mm or more in the buccal region and were asked to consume L. reuteri DSM 17938 and L. reuteri ATCC PTA5289 twice daily (morning and evening) for 1 month, and the results of oral bacteriological tests were compared using the real-time PCR method.
Results: The results of this study showed that the amount of P. gingivalis, T. forsythia and T. denticola decreased statistically significantly after consumption compared to before consumption. However, in the case of A. actinomycetemcomitans, most of them were not detected in Koreans.
Conclusion: The present study suggests that L. reuteri DSM 17938 and L. reuteri ATCC PTA 5289 can be used as a useful adjunct or alternative in non-surgical therapy and periodontal therapy, and the quantitative changes of the four oral microorganisms in this study were analysed and it was found that the quantities were statistically significantly decreased after administration compared to before administration.
Keywords : Lactobacillus reuteri, periodontal, probiotics
Introduction

Periodontal disease is an inflammatory disease of the gums and bone surrounding the teeth [1,2]. Periodontal disease is broadly divided into gingivitis and periodontitis, with periodontitis being a complex bacterial infection in which inflammation has invaded the periodontal tissues due to the proliferation of gram-negative bacteria [3-5].

Periodontal disease is primarily caused by oral bacteria. When plaque adheres to teeth and is not adequately removed by brushing, inflammation occurs, deepening the fissure that surrounds the neck of the tooth and causing it to lose its supporting tissue, forming a periodontal pocket around the tooth [6].

Bacteria associated with periodontal disease and causing periodontitis include the gram-negative bacilli Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia and Treponema denticola. These are found in the sub-gingival bacterial film and are anaerobic bacilli [7-10]. Other gram-negative bacteria include Prevotella intermedia and Fusobacterium nucleatum [11].

Compounds such as chlorhexidine, fluoride compounds, xylitol and sorbitol have been used to inhibit the growth of these oral bacteria, but they have side effects and other problems, such as disturbing the normal oral flora with prolonged use, which can lead to bacterial infections if the normal flora is disrupted [12]. There is therefore a need for a safe alternative with fewer side effects. In this context, non-pathogenic microorganisms called probiotics have come to the fore [13-17]. Recently, there has been a great deal of research into the use of oral probiotics to reduce oral pathogenic bacteria in order to prevent dental caries and reduce plaque [18,19]. Probiotics are defined as “live microorganisms that are safe for human consumption and have beneficial effects on human health when consumed in sufficient quantities” [20]. Probiotics have the benefit of stimulating the immune system, balancing the gut microbiota, reducing childhood allergies and balancing the oral flora [21-24]. Probiotics include lactic acid bacteria (LAB) with antimicrobial and anti-inflammatory properties, such as Lactobacillus reuteri, Lactobacillus fermentum and Lactobacillus casei Shirota, among which Lactobacillus reuteri produces reuterin, a broad-spectrum antimicrobial agent, It inhibited the growth of the oral pathogens Strep-tococcus mutans, Actinomyces actinomycetemcomitans, Prevo-tella intermedia, and Fusobacterium nucleatum, as well as Candida albicans, some fungi, and gram-positive and gram- negative bacteria [25-27].

L. reuteri DSM 17938 and L. reuteri ATCC PTA5289, strains isolated from human breast milk and saliva, have been noted for their oral cytokine-reducing effects and immunomodulatory roles in oral health care, and double-blind, randomised, placebo-controlled clinical trials in systemically healthy patients with chronic periodontitis evaluated their effects alone and in combination with scaling and root planing (SRP) [28]. actinomycetemcomitans, P. intermedia and P. gingivalis [28,29]. Furthermore, it has been reported that L. reuteri DSM 17938 and L. reuteri ATCC PTA5289 have plaque inhibitory, anti-inflammatory and antimicrobial effects, and that L. reuteri DSM 17938 and L. reuteri ATCC PTA5289 could be used as a useful adjunct or alternative in non-surgical therapy and at various stages of periodontal therapy [30].

Therefore, the aim of the present study was to determine the quantitative changes in the oral microbiota of four periodontitis pathogens, Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia and Treponema denticola, following administration of L. reuteri DSM 17938 and L. reuteri ATCC PTA5289 as adjuvants in periodontitis.

Materials and Methods

1. Research subjects

1) Sample collection

The sample collection population for this study included 30 men and women aged 20 years or older who had a pocket measurement of 4 mm or more in the palatal region at the initial stage of periodontitis.

2) Exclusion criteria for specimen collection

The following conditions were excluded.

(1)Patients who visited a dental clinic and had a pocket measurement of less than 4 mm in the buccal region.

(2)Those who had taken or were taking antibiotics within two weeks prior to sample collection.

(3)Those who consumed probiotic supplements and fermented milk continuously (at least 4 times a week) within 1 week of sample collection.

(4)Allergic to any of the product ingredients.

(5)Those who plan to participate in other clinical trials during this study.

(6)Anyone deemed unsuitable for this study by the investi-gator.

3) Criteria for discontinuation and withdrawal from the study for specimen collection

Subjects who met any of the following conditions were excluded from the study (Table 1).

Table 1 . Age and gender distribution of study subjects

AgeAllManWoman
≥20 (average 28)422
≥30 (average 36)321
≥40 (average 45.3)642
≥50 (average 55.4)17107
All301911


(1)Subjects who ingested antibiotics while consuming the applied product.

(2)Consumption of other oral products during the study.

(3)Unable to visit the dentist during the study.

2. Methods

1) Obtaining IBR

This study was approved by the Dankook University IRB (Approval No. DKU 2019-06-017), and the purpose of the study was fully explained to the subjects before the start of the study, and the “Consent Form for Human Derivative Research” was obtained in accordance with the [Enforcement Rules of the Act on Bioethics and Safety].

2) Specimen collection methods

Samples were collected from patients attending the dental clinic before and after ingesting L. reuteri DSM 17938 and L. reuteri ATCC PTA5289, which were taken twice a day (morning and evening) for 1 month. Samples were collected by gargling vigorously for approximately 20 seconds with mouthwash (Original Gargrin 10 ml, Dong-A Pharmaceutical) and then collected in a 50 ml sample tube. The collected samples were sent to the laboratory or refrigerated immediately after collection.

3) Sample collection conditions

Specimens were collected within approximately 1 hour after tooth brushing and after refraining from eating, drinking water and chewing gum.

4) Real-time quantitative PCR (real-time qPCR)

For the quantitative analysis of periodontitis-related oral microorganisms, the OBD (Oral Bacteria Diagnosis) test from DENOMICS was used to quantitatively analyse the four strains listed in Table 2. The PCR reaction solution was dispensed into a 96-well plate using DENOMICS premix to a total volume of 20 ml, including 2 ml of template DNA, and PCR was performed using the CFX96 Real-Time PCR Detection System (Bio-Rad Inc., USA) according to the conditions in (Table 3). Upon completion of the PCR, the Ct value was checked using CFX ManagerTM IVD software (version 1.6) (Bio-Rad Inc., USA) and quantified by converting the Ct value to copy number and log10 according to the established standard curve [25].

Table 2 . Four oral bacteria that cause periodontitis

No.Target bacteria
1Aggregatibacter actinomycetemcomitans
2Porphyromonas gingivalis
3Tannerella forsythensis
4Treponema denticola

Table 3 . PCR condition

StepTemp. (°C)TimeCycle
1505 min1
29410 min1
39420 sec40
45830 sec40
57230 sec40

5) Storage and disposal of samples

Samples were tested immediately upon arrival at the laboratory. After testing, the samples were discarded immedi-ately. However, the DNA extracted from the specimens was stored at −20°C until the end of the study and disposed of at the end of the study in accordance with the relevant regulatory procedures of the analysing organisation.

6) Statistical analysi

Statistical significance tests were performed using IBM SPSS Statistics 24.0 (IBM, New York, USA). The Kolmogorov- Smirnov test (KS test) and the Shapiro-Wilk test (SW test) were used to test for normality, and the paired t-test was used if normality was satisfied; if normality was not satisfied, the non-parametric Wilcoxon signed rank test was used. The significance criteria were p<0.05 or p<0.01. The copy number of all oral microorganisms was converted to a logarithmic index.

Results

1. Aggregatibacter actinomycetemcomitans test results

The values of Aggregatibacter actinomycetemcomitans in the samples before and after taking Biogeia prodentis lozenges were not statistically significantly different (p>0.05) (Table 4).

Table 4 . The effects of Lactobacillus reuteri intake on Aggregatibacter actinomycetemcomitans

No.Copy numberLog10


Before ingestionAfter ingestionBefore ingestionAfter ingestion
10000
20000
30000
40000
50000
60000
70000
80000
90000
100000
110000
120000
135,52561,5513.744.79
140000
150000
160000
170000
180000
190000
2043,58604.640
210000
220000
230000
240000
25660,25853,4994.824.73
260000
270000
280000
290000
300000
Mean23,6463,8350.4730.317
SD120,50114,6331.4701.207
p-value0.33910.3457


2. Porphyromonas gingivalis test results

There was a statistically significant difference (p<0.05) between the values of Porphyromonas gingivalis in the samples before and after taking Biogeia prodentis lozenges (Table 5).

Table 5 . The effects of Lactobacillus reuteri intake on Porphyromonas gingivalis

No.Copy numberLog10


Before ingestionAfter ingestionBefore ingestionAfter ingestion
1648,649126,4715.815.10
2518,14224,8135.714.39
3299,206454,5065.485.66
43,224,6318,0706.513.91
50000
6234,54720,8355.374.32
78,1716,9043.913.84
805,94403.77
90000
10551,5066,6515.743.82
1188,06663,6634.944.80
124,51703.650
1310,039,221843,0057.005.93
1426,24604.420
15110,93899,7725.054.99
16421,716437,8045.635.64
1738,16504.580
184,929,013388,8576.695.59
191,173,43806.070
20279,35737,9285.454.58
21511,7177,1685.713.86
2214,689,6019,3167.173.97
23374,567149,6795.575.18
240000
2521,227,55628,4647.334.45
260000
270000
287,348,52206.870
2916,851,168343,2347.235.54
30187,3795,412,6515.276.73
Mean2,851,619289,0195.1093.509
SD5,574,573986,9061.9692.276
p-value0.01980.0004


3. Tannerella forsythensis test results

There was a statistically significant difference (p<0.01) in the values of Tannerella forsythensis in the samples before and after taking Biogeia prodentis lozenges (Table 6).

Table 6 . The effects of Lactobacillus reuteri intake on Tannerella forsythensis

No.Copy numberLog10


Before ingestionAfter ingestionBefore ingestionAfter ingestion
14,985,239552,0656.705.74
23,093,542141,9046.495.15
31,425,647631,6846.155.8
414,813,511239,1837.175.38
5855,370603,9465.935.78
6635,24383,7195.804.92
70000
8138,75326,3395.144.42
91,393,9971,3986.143.15
101,715,79744,8966.234.65
11479,778180,6465.685.26
12289,48105.460
1336,780,1932,570,4087.576.41
14175,64605.240
152,336,447967,8106.375.99
16714,727279,8925.855.45
17159,65805.200
1826,558,8951,113,6287.426.05
19507,48185,1415.714.93
20808,675304,4825.915.48
212,111,89306.320
2211,125,51233,1557.054.52
231,559,624306,1966.195.49
24925,30705.970
2514,896,903376,8837.175.58
26067,63604.83
272,443,76867,2576.394.83
2812,035,164325,7007.085.51
2916,388,605946,3207.215.98
3016,388,60512,035,1647.217.08
Mean5,888,859746,3405.9024.204
SD8,965,9442,196,6551.7422.418
p-value0.00210.0005


4. Treponema denticola test results

There was a statistically significant difference (p<0.05) between the values of Treponema denticola in the specimens before and after taking Biogeia prodentis lozenges (Table 7).

Table 7 . The effects of Lactobacillus reuteri intake on Treponema denticola

No.Copy numberLog10


Before ingestionAfter ingestionBefore ingestionAfter ingestion
1422,17829,9815.634.48
20000
30000
4542,28605.730
54,75003.680
62,68303.430
70000
80000
9111,06905.050
100000
110000
120000
131,156,67792,7966.064.97
140000
1580,05839,5114.904.60
166,1403,6043.793.56
170000
182,70087,0263.434.94
1936,81804.570
2037,77504.580
2132,80004.520
221,112,97106.050
233,0317,4453.483.87
240000
250000
265,40103.730
270000
2812,60320,7934.104.32
290000
301,249,304179,7606.105.25
Mean156,78125,9682.3361.639
SD365,90965,0712.4792.224
p-value0.04910.1145

Discussion

A wide variety of microorganisms such as bacteria, viruses, yeasts and fungi live in symbiosis with humans to maintain homeostasis in the body. However, as the influence of these microorganisms on human disease has become increasingly apparent, many studies have been conducted on the microorganisms that co-exist in the human body. In particular, the oral cavity is a vital part of the human body where a wide variety of microorganisms exist, and the oral microbiota is increasingly being studied because of its close association with oral and systemic diseases [31-37].

Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia and Treponema denticola, referred to as the red complex, are known to be the major causative agents of periodontitis, while Prevotella intermedia, Eikenella corrodens, Campylobacter rectus and Fusobacterium nucleatum have been associated with periodontitis [38]. Inhi-biting the growth of these pathogens is the most effective way to prevent periodontal disease.

Therefore, to investigate the effect of L. reuteri on reducing anaerobic bacteria that can cause periodontal disease in the oral cavity, the authors studied changes in oral bacterial counts in 30 men and women aged 20 years and older with at least 4 mm of molars in the buccal region by consuming L. reuteri DSM 17938 and L. reuteri ATCC PTA5289.

A study by Iniesta M, Herrera DL reported that L. reuteri DSM 17938 and L. reuteri ATCC PTA 5289 can be used as a useful adjunct or alternative to non-surgical therapy and in phases of periodontal therapy [39]. In the present study, to evaluate the suitability of L. reuteri as an adjuvant in periodontitis, quantitative changes in the oral microbiota of four periodontitis pathogens, Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia and Treponema denticola, and A. actinomycetemcomitans was detected in four subjects before ingestion and decreased in three subjects after ingestion, with 91.44 to 100% of subjects being undetectable. P. gingivalis was reduced in 24 of 28 (85.71%) subjects with a mean reduction of 84.90%. T. forsythia was reduced in 28 out of 29 (96.55%) subjects with a mean reduction of 83.33%. T. denticola showed a reduction in 11 out of 17 (64.71%) with a mean reduction of 87.40%. With the exception of A. actinomycetemcomitans, P. gingivalis, T. forsythia and T. denticola showed statistically significant reductions after treatment com-pared to before treatment (p<0.05).

It has also been reported that oral pathogens such as S. mutant, A. actinomycetemcomitans, P. gingivalis and P. intermedia were reduced by antimicrobial susceptibility testing using L. reuteri or by consumption of probiotics containing L. reuteri [40], and it has been reported that L. reuteri supplementation in patients with gingivitis helped to reduce severe gingival inflammation and plaque [41]. In addition, the efficacy of treatment was evaluated by pro-inflammatory cytokines (TNF-α, IL-1β cand IL-17) in chronic periodontitis patients treated orally with probiotics containing L. reuteri and found that cytokine response and bleeding index (SBI), periodontal pocket depth (PPD) and clinical attachment level (CAL) were significantly reduced after treatment [42].

These results suggest that L. reuteri DSM 17938 and L. reuteri ATCC PTA 5289 are suitable for use as adjuvants in periodontitis.

Conclussion

The aim of this study was to determine the quantitative changes in four oral microorganisms associated with periodontitis after consumption of L. reuteri DSM 17938 and L. reuteri ATCC PTA5289, and to investigate the changes in oral microorganisms after consumption of L. reuteri, which is known to help improve periodontitis.

Subjects were 30 males and females aged 20 years or older who had periodontitis with a baseline pocket size of 4 mm or more in the buccal region and were asked to consume L. reuteri DSM 17938 and L. reuteri ATCC PTA5289 twice daily (morning and evening) for 1 month, and the results of oral bacteriological tests were compared using the real-time PCR method.

The results of this study showed that the amount of P. gingivalis, T. forsythia and T. denticola decreased statistically significantly after consumption compared to before consumption. However, in the case of A. actinomycetemcomitans, most of them were not detected in Koreans.

The present study suggests that L. reuteri DSM 17938 and L. reuteri ATCC PTA 5289 can be used as a useful adjunct or alternative in non-surgical therapy and periodontal therapy, and the quantitative changes of the four oral microorganisms in this study were analysed and it was found that the quantities were statistically significantly decreased after administration compared to before administration.

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

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