Colonization of Helicobacter pylori in the oral cavity – an endless controversy?

Figures & data

Figure 1. Morphology of H. pylori. Field-emission scanning electron microscopic (FESEM) image of a spiral-shaped H. pylori with five to seven sheathed polar flagella. The scale bar is 0.5 μm. This figure is reprinted from references (O’Rourke 2001; Reshetnyak and Reshetnyak 2017) with kind permission from the publishers.

Table 1. Studies published since 2010 detecting oral H. pylori with molecular methods.

Authors	Nation	Sample	Sample capacity	Method	Target genes	Total detection rate	Detection rate in gastric H. pylori- positive patients	Detection rate in gastric H. pylori-negative patients	Detection rate of other genes in H. pylori-positive samples
Šeligová et al. (2020)	Slovakia	Saliva	81 patients admitted for upper gastrointestinal endoscopy	nested PCR	16S rRNA	9.9%	13.2%	6.1%	–
Flores-Treviño et al. (2019)	Mexico	Dental plaque	38 patients attending a dental clinic	qPCR	16S rRNA	60.5%	–	–	vacA: 100%; cagA: 21.7%
Hamada et al. (2019)	Japan	Saliva and extracted teeth	87 patients requiring tooth extraction	PCR	ureA	18.4% saliva only: 9.2% extracted teeth only: 14.9% both sample types: 5.7%	–	–	–
Zhao et al. (2019)	China	Tongue	80 patients diagnosed with chronic non-atrophic gastritis	gene sequencing	16S rRNA	60%	–	–	–
Matamala-Valdés et al. (2018)	Chile	Oral swabs	53 term newborns	PCR	16S rRNA	1.9%	–	–	–
Kadota et al. (2019)	Japan	Dental plaque	A 29-year-old Japanese female admitted to the Gastroenterology clinic	Nested PCR	ureA	100%	–	–	–
Ansari et al. (2018)	Pakistan	Dental plaque	567 patients with periodontal infections	PCR	16S rRNA	44.6%	–	–	–
Nomura et al. (2018)	Japan	Inflamed dental pulp	131 subjects treated at Osaka University Dental Hospital	Nested PCR	ureA	40%	–	–	–
Wongphutorn et al. (2018)	Thailand	Saliva	110 healthy persons	Real-time PCR; nested PCR	16SrRNA; vacA	Total: 64.5%	Total: 67.1%	–	vacA: 29.6%
Mendoza-Cantú et al. (2017)	Mexico	Dental plaque	100 Mexican children	qPCR	16SrRNA; cagA	38%; 27%	–	–	–
Urban et al. (2017)	Poland	Saliva and dental plaque	108 adults with gastric H. pylori infection	PCR	not mentioned	46%#	–	–	–
Medina et al. (2017)	Argentina	Saliva and dental plaque	61 patients admitted to the Service of Gastroenterology	PCR	ureA	50.8%#	–	–	vacA: 100%; cagA: 29%; babA2:17.6%
Aksit Bıcak et al. (2017)	Turkey	Saliva and dental plaque	70 admitted to endoscopy with a gastro-duodenoscope and 30 controls	real-time PCR	16S rRNA	Study group saliva: 80% dental plaque: 84.3% control group saliva: 46.7% dental plaque: 100%	Study group saliva: 79.3% dental plaque: 84.5%	Study group saliva: 83.3% dental plaque: 83.3%
Valadan Tahbaz et al. (2017)	Iran	Dental plaque	50 patients with chronic periodontitis and 50 periodontally healthy subjects	PCR	16S rRNA	5% in both groups	–	–	vacA: 40%; cagA: 80%; babA2: 100%
Castro-Muñoz et al. (2017)	Mexico	Oral swabs	162 Mexican children	PCR	16S rRNA; glmM	13%; 5.5%	–	–	–
Pataro et al. (2016)	Brazil	Saliva and tongue swabs	154 obese adult individuals	PCR	not mentioned	Saliva: 40.9% tongue swabs: 33.8%	–	–	–
Ismail et al. (2016)	UK	Dental plaque	49 patients admitted for a gastrointestinal endoscopy	Nested PCR	295 bp fragment	40.8%	–	–	–
Kazanowska-Dygdała et al. (2016)	Poland	Dental plaque	54 patients with oral leukoplakia; 72 patients with oral lichen planus (OLP); 40 healthy controls	Nested PCR	417 bp DNA	20% in leukoplakia 23% in OLP 0% in control	–	–	–
Amiri et al. (2015)	Iran	Dental plaque	45 patients referred to the Department of Periodontology	PCR and LAMP	glmM	PCR: 44%; LAMP: 66.7%	–	–	–
Ogaya et al. (2015)	Japan	Inflamed dental pulp and saliva	40 children and adolescents attending Osaka University Dental Hospital	PCR	ureA	Inflamed dental pulp 15% saliva 0%	–	–	–
Bharath et al. (2014)	India	Dental plaque	56 dyspeptic adult patients	Real-time PCR	ureA	33.9%	–	–	–
Boyanova et al. (2013)	Bulgaria	Dental plaque	43 subjects living in Sofia	PCR	ureA; cagA; vacA	All: 2.3%	–	–	–
Cai et al. (2014)	China	Dental plaque and gargle	46 children with upper gastrointestinal symptoms and gastric H. pylori infection	PCR	16s rRNA;	56.5%#	16S rRNA: 56.5%	–	cagA: 46.1%
Agarwal and Jithendra (2012)	India	Subgingival plaque	30 patients with gastric H. pylori infection	PCR	16S rRNA	60%	60%	–	–
Sepúlveda et al. (2012)	Chile	Dental plaque and tongue	18 patients admitted for endoscopy	Real-time PCR	cagA; vacA	cagA: 16.7%; vacA: 5.6%#	–	–	3 vacA–/cagA+ samples and 1 vacA+/cagA– sample; no vacA+/cagA + sample
Hirsch et al. (2012)	Germany	Root canal; plaque	3 children with endodontically-infected deciduous teeth (10 samples)	PCR	16S rRNA	Root canal: 20%; plaque: 40%	–	–	–
Al-Ahmad et al. (2012)	Germany	Plaque; saliva, periapical exudate; tongue swabs	15 patients who tested positive for gastric H. pylori infection (163 oral samples)	PCR; nested PCR	417 and 109 bp fragment	Periapical exudate and tongue swabs: 6.6% plaque and saliva: 0%	6.6%	–	–
Wichelhaus et al. (2011)	Germany	Dental plaque	11 adolescent patients aged 11–15 years (93 samples)	Nested PCR	417 bp fragment	82%	–	–	–
Gao et al. (2011)	China	Dental plaque; gargle; tongue swabs	96 patients with chronic gastric diseases	PCR	glmM	Dental plaque: 82.3% gargle: 51.1% tongue swabs: 37.5%	59.6%	–	cagA: 14.6%
Silva et al. (2010)	Brazil	Supragingival and subgingival plaque	115 patients with complaints regarding the upper digestive tract	PCR	16S rRNA	Supragingival plaque: 11.3%; subgingival plaque: 0%	14.9%	6.3%	–
Assumpção et al. (2010)	Brazil	Dental plaque	99 adult patients admitted to upper gastrointestinal endoscopy	PCR	vacA	72%	–	–	cagA: 81.7%

Sort order by decreasing publication year. –: not investigated in the respective study.

#No separate detection of each sample type given in the respective study.

Table 2. Studies published since 2010 detecting oral H. pylori with immunological and biochemical methods.

Author	Nation	Sample	Sample capacity	Method	Detection rate
Zhao et al. (2019)	China	Tongue scraping and swabs	80 patients diagnosed with chronic non-atrophic gastritis	Anti-cagA igG antibody	43.7%
Matamala-Valdés et al. (2018)	Chile	Oral swabs	53 term newborns	Anti-H. pylori IgG antibody	1.9%
Wongphutorn et al. (2018)	Thailand	Saliva	110 healthy persons	Indirect IFA using a mouse anti-H. pylori IgG antibody	51%
Yu et al. (2017)	China	Dental plaque	4321 adults	Saliva H. pylori antigen (HPS) test	59.6%
Dane and Gurbuz (2016)	Turkey	Dental plaque	35 patients with gastric H. pylori infection and 35 patients without gastric H. pylori infection (control)	CLO gel test	patients: 82.8%; controls: 22.9%
Ding et al. (2015)	China	Saliva	1050 patients admitted for oral health examination	HPS	60.3%
Hulimavu et al. (2014)	India	OLP and buccal mucosa biopsies	tissue blocks from 50 OLP cases and buccal mucosa biopsies from 10 healthy cases	Anti-H. pylori antibody (rabbit polyclonal)	0%
Wang et al. (2014)	China	Saliva	201 patients (110 with stomach pain and 91 with no stomach complaints)	HPS & H. pylori flagellin test (HPF)	HPS & HPF positive: symptomatic: 87.3% asymptomatic: 49.5%
Boyanova et al. (2013)	Bulgaria	Dental plaque	43 subjects living in Sofia	Immunofluorescence with monoclonal antibodies (MCAs) (121F3, 122Е9, 123B11, and 161F8)	2.3%
Namiot et al. (2010)	Poland	Supragingival plaque	155 patients aged 19–78 years	Immunological test (horseradish peroxidase-labeled monoclonal antibodies against H. pylori)	65.6%

Sort order by decreasing publication year. –: not investigated in the respective study.

Table 3. Studies published since 2000 detecting oral H. pylori by culture techniques.

Author	Nation	Sample	Sample capacity	Culture medium	Total detection rate	Detection rate in gastric H. pylori-positive patients	Detection rate in gastric H. pylori-negative patients
Wang et al. (2014)	China	Saliva	277 patients (159 with stomach pain and 118 with no stomach complaints)	Trypticase soy agar (TSA) + 5% blood plate	Symptomatic: 86.7% asymptomatic: 85.6%	-	-
Boyanova et al. (2013)	Bulgaria	Dental plaque	43 subjects living in Sofia	blood agar with Columbia agar base and 1% Isovitalex	2.3%	–	–
Agarwal and Jithendra (2012)	India	Subgingival plaque	30 patients from the gastroenterology department	Columbia blood agar + 5% defibrinated sheep blood with antibiotic supplements	30%	–	–
Hirsch et al. (2012)	Germany	Root canal; plaque	3 children with endodontically-infected deciduous teeth (10 samples)	Gonococci (GC) agar plates with 10% horse serum (containing vancomycin, trimethoprim, nystatin, and colistin)	Root canal: 20%; plaque: 0%	–	–
Al-Ahmad et al. (2012)	Germany	Plaque, saliva, subgingival exudate; tongue	15 patients tested positive for H. pylori in stool antigen test (163 oral samples)	H. pylori selective supplement (DENT) agar, yeast-cysteine blood agar and Columbia blood agar	0%	–	–
Teoman et al. (2007)	Turkey	Dental plaque	67 dyspeptic patients admitted for upper gastrointestinal endoscopy	Brain heart infusion (BHI) agar containing 7% horse blood and DENT agar	0%	–	–
Cześnikiewicz-Guzik et al. (2004, 2005)	Poland	Saliva and supragingival plaque	100 female subjects	solid selective, enriched medium (H. pylori agar, Becton Dickinson) with 5% horse blood	Saliva: 54.1%; plaque: 48.3%	saliva: 54.9%; plaque: 56.9%	saliva: 53.2%; plaque: 42.9%
Umeda et al. (2003)	Japan	Dental plaque; saliva; tongue plaque	18 Japanese subjects suffering from gastritis and peptic ulcers admitted to the hospital of Tokyo Medical and Dental University	H. pylori selective medium	5.6%#	-	-
Allaker et al. (2002)	UK	Dental plaque	100 children admitted for upper gastrointestinal tract endoscopy	BHI agar containing H. pylori selective supplement (Oxoid SR147)	0%	–	–
Goosen et al. (2002)	South Africa	Dental plaque and saliva	58 randomly-selected clinically healthy volunteers	brain heart infusion agar plates with 5% sheep blood	Dental plaque: 1.7% saliva: 1.7%	–	–

Sort order by decreasing publication year. –: not investigated in the respective study. #No separate detection of each sample type given in the respective study.

Figure 2. Morphological transformation of H. pylori from spiral to coccoid form under stress conditions. Transmission electron microscopic (TEM) images exhibiting the morphology transformation of H. pylori from its spiral to its coccoid form under stress conditions. H. pylori was cultured on Brucella blood agar with 5% horse serum and antimicrobial agents (10 mg/L vancomycin, 5 mg/L colistin, 5 mg/L trimethoprim and 5 mg/L amphotericin B) for a total of 15 days. On day 2, day 7, day 9, and day 15, its morphology was pictured by TEM: A: Day 2 (2D): bacillary form of H. pylori; B: Day 7 (7D): U-shaped form; C: Day 9 (9D): doughnut shaped form; D: Day 15 (15D): full coccoid form. The scale bar shows 1 μm. This figure is reprinted from reference (Roe et al. 1999) with kind permission from the publisher.

Figure 3. The cycle of H. pylori in the human body. The question on whether H. pylori is resident or transient in the oral cavity (saliva, dental plaque, or tongue microbiota) remains to be clarified. H. pylori can be introduced in the oral cavity by contaminated substances including food and drinking water. There may also be a relationship between gastric and oral H. pylori infection. H. pylori can be swallowed and may subsequently cause infections in the stomach. Conversely, reflux can bring back viable organisms, DNA fragments or antigens of H. pylori to the oral cavity from the stomach of H. pylori-infected individuals. This may lead to positive results in detection with molecular methods, immunological methods or culture methods. Furthermore, H. pylori may be present in a viable, but not-culturable (VBNC) state (i.e. coccoid form).

Figure 4. Future research directions. Important aspects for future studies investigating the potential colonization of H. pylori in the oral cavity: • Whole genome sequencing of oral H. pylori isolates. • Deposition of oral H. pylori in national or international culture collections. • Research on the VBNC state and the coccoid form of H. pylori. • Studies on the effects of saliva on viability of H. pylori and on the ability of H. pylori to colonize biofilms formed from oral bacteria in vitro. • Effects of consumed substances and reflux on the detection of oral H. pylori. • Cross-reaction tests with H. pylori-like microorganisms when using molecular or immunological methods. To achieve these goals, we advocate establishing a network of researchers who have reported isolating H. pylori from the oral cavity.

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