Helicobacter pylori and oral pathology: Relationship with the gastric infection

Table 1 Helicobacter pylori detection in dental plaque and saliva n (%)

Ref.	Sample	Diagnostic method	Patient profile	Helicobacter pylori detection rate
Krajden et al[10]	Pq	MCT	Dys	1/71 (1)
Shames et al[11] (Canada)	Pq/Sal	MCT, REA	Dys	Pq: 1/29 (3)
				Sal: 0/29 (0)
Majmudar et al[12]	Pq	MCT	Dys	40/40 (100)
Desai et al[13]	Pq	RUT	Dys	Gc: 0/24 (0)
			Tripe-H. pyloriET	Pq: 24/24 (100)
D'Alessandro et al[14]	Pq	MCT, Giemsa, RUT	Dys	16/20 (80)
Nguyen et al[15]	Pq	RT-PCR (16S rRNA)	Dys	18/25 (72)
Bernander et al[16]	Pq	MCT	Dys	0/94 (0)
Mapstone et al[17]	Pq/Sal	PCR	Dys	Pq: 3/13 (23)
				Sal: 2/13 (15)
Von Recklinghausen et al[18]	Pq	MCT, RUT	Dys	0/55 (0)
Li et al[19]	Sal	PCR (860-bp DNA)	Dys	30/40 (75)
Hardo et al[20]	Pq	MCT, N-PCR (16S rRNA)	Dys	1/62 (2)
Cammarota et al[21]	Pq	Giemsa: PCR (ureA), RUT	Dys	0/31 (0)
Luman et al[22]	EGB	MCT	Dys	EGB: 52/109 (47)
	Pq/Sal			Pq/Sal: 0/120 (0)
Pustorino et al[23]	Pq	MCT	Dys	5/83 (6)
Pytko-Polonczyk et al[24]	Pq/Sal	RUT, 13-UBT	100 Dys	Post-triple H. pyloriET
			50 DU	DU Gc: 1/30 (3)
				DU Pq: 30/30 (100)
Cheng et al[25]	Pq	MCT, RUT	Dys	MCT: 1/122 (1)
				RUT: 71/122 (58)
Oshowo et al[26]	Pq/Sal	MTC, Giemsa, RUT, REA	Dys	EGB: 116/116 (100)
	OS			Pq: 15/116 (13)
Améndola et al[27]	Pq	MCT	Dys	1/20 (5)
Mattana et al[28]	Pq	MCT	Dys	1/62 (2)
Song et al[29]	Pq	N-PCR1	Dys	41/42 (97)
Doré-Davin et al[30]	Pq/Sal	N-PCR (16S rRNA-ureC), UBT	DU	9/22 (40)
Kim et al[31]	Pq/Sal	MCT, Giemsa, PCR1, RUT	Dys	Gc: 29/46 (63)
				Pq: 2/29 (7)
				Sal: 4/29 (14)
Miyabayashi et al[32]	Pq/Sal	N-PCR (ureA)	Gtis, DU, H. pylori-pos	Diagnosis: 23/47 (49)
		MCT		Pos-H. pyloriET: 11/23 (48)
Ozdemir et al[33]	Pq	RUT	Dys	Pq: 63/81 (78)
	Tg			Tg: 48/81 (59)
Allaker et al[34]	EGB	PCR (ureA-cagA)	Dys, Children	EGB: 22/100 (22)
	Pq			Pq: 15/22 (68) and 21/88 (24)
Suk et al[35]	Pq	PCR (cag-A)	Dys	Gc: 38/65 (58)
		RUT		Pq: 28/65 (43)
Wang et al[36]	Sal	PCR-Sequence (cagA-vacA)	Gtis, DU	More than one H. pylori strain in Gc and Sal, in same patient
Berroteran et al[37]	EGB	PCR (urease gene cluster)	32 Dys	Gc: 24/32 (75)
	Pq		20 Asym	Pq: 12/32 (38), 3/20 (15)
Gürbüz et al[38]	Pq	RUT	Dys	Gc: 65/75 (86)
				Pq: 68/75 (90)
Nasrolahei et al[39]	Pq	MCT, PCR1, RUT	Dys	P > 0.05
Siddiq et al[40]	EGB	Giemsa, 13-UBT	Dys	Gc: 32/52 (62)
	Pq			Pq: 48/52 (92)
Czesnikiewicz-Guzik et al[41]	Pq/Sal	MCT, 13-UBT	Dys	Gc: 51/100 (51)
				Pq-Sal: 54/100 (54), P > 0.05
Kignel et al[42]	Pq/Sal	PCR	Dys	Gc: 20/49 (41)
				Pq-Sal: 1/20 (5)
Chitsazi et al[43]	Pq	RUT	Dys	Gc H. pylori: 16/44 (36)
			44 Gc H. pylori	No-Gc H. pylori: 14/44 (32)
			44 no-Gc H. pylori	P = 0.7
De Sousa et al[44]	EGB	MCT, Giemsa, RUT	97 Dys	Gc: 111/147 (76)
	Pq/Sal		50 Asym	Pq/Sal (RUT): 0/147 (0)
Sudhakar et al[45]	Pq	MCT, RUT	50 Dys	Pq MCT: 5/50 (1)
			25 control	Pq RUT: 37/50 (74)
Bürgers et al[46]	SP-P	MCT, Ser (ELISA), PCR	Dys	Gc: 29/94 (31)
	Sal			SP-P: 3/94 (3)
				Sal: 7/94 (7)
Liu et al[47]	EGB,	Giemsa, PCR, RUT	Dys	EGB: 273/443 (62)
	Pq			Pq: 263/443 (59)
Silva et al[48]	Pq/Sal	PCR (vacA)	Dys	Gc: 30/62 (48)
				Pq: 11/30 (37)
				Sal: 16/30 (53)
Rasmussen et al[49]	EGB	SBlot	Dys	Gc: 66/78 (85), P < 0.0001
	Pq/Sal
Medina et al[50]	EGB	PCR (ureA)	43 Dys	18/98 (18)
	Pq		55 control	EGB: 38/43 (88)
				Pq/Sal: 15/43 (35)
Assumpção et al[51]	EGB	PCR (cagA-vacA), Giemsa, RUT	Dys	Gc PCR: 95/99 (96)
	Pq			Gc Giemsa: 39/99 (48)
				Gc RUT: 47/99 (49)
				Pq PCR: 71/99 (72)
				Pq RUT: 48/99 (52)
Navabi et al[52]	MAS	MCT, PCR, RUT	Dys	925/1861 (49.7)
				(95%CI: 16-83.4)
Zou et al[9]	MAS	MCT, PCR, RUT	Dys	490/1088 (45)
				OR 3.61 (95%CI: 191-6.82)
Chaudhry et al[53]	Pq	PCR (ureA-16S rRNA-860 bp DNA)	Dys	46/89 (52)
	TBF
Momtaz et al[54]	EGB, Pq/Sal, Stool sample	PCR (cagA-vacA-ureC), RUT	Dys	PCR: EGB: 233/300 (78), Pq: 0/300 (0), Sal: 32/300 (11), Stool: 215/300 (72)
				RUT: 271/300 (90)
Román-Román et al[55]	EGB, Sal	PCR (vacA)	162 Gtis	EGB/Sal: 47/196 (24)
		N-PCR (cagA)	32 GU	EGB: 103/196 (53)
				Sal: 13/196 (7)
Cai et al[56]	Pq	PCR (16S rDNA-CagA), RUT	Dys, Children	46/235 (20)
				Pq: 26/46 (57)

¹Data not shown. Asym: Asymptomatic subject; Bs: Biopsy; DU: Duodenal ulcer; Dys: Dyspepsia; EGB: Endoscopic gastric biopsy; Gc: Gastric; Gtis: Gastritis; GU: Gastric ulcer; H. pyloriET: Helicobacter pylori eradication therapy; MAS: Meta-analysis study; MCT: Microbial culture techniques; N: Nested; OR: Odds ratio; OS: Oral swab; PCR: Polymerase chain reaction; Pq: Plaque; PS-P: Periodontal status; Ptis: Periodontitis; REA: Restriction endonuclease analysis; RT: Reverse transcription; RUT: Rapid urease test; Sal: Saliva; SBlot: Southern-blotting; SB-P: Subgingival plaque; Ser: Serology; SP-P: Supragingival plaque; TBF: Tooth brushing frequency; Tg: Tongue;

¹³-UBT: ¹³C-urea breath test.

Table 2 Helicobacter pylori detection in periodontal disease n (%)

Ref.	Sample	Diagnostic method	Patient profile	Helicobacter pylori detection rate
Asikainen et al[58]	SB-Pq (United States)	PCR (urease A)	Ptis	0/336 (0)
Riggio et al[59]	SB-Pq	PCR (16S rRNA)	Chronic Ptis	11/29 (38)
Avcu et al[60]	SB-Pq, SP-Pq	Camphylobacter- like organism test gels	Gastric H. pylori and B12 deficiency: (1) good oral hygiene; (2) fair oral hygiene; (3) poor oral hygiene	(1) 6/21 (28); (2) 46/51 (90); (3) 36/36 (100) post-H. pyloriET: (1) 58%; (2) 41%; (3) 5%
Dye et al[61]	BL	Ser (ELISA)	NHANES III; 1988-1991	Periodontal pocket ≥ 5 mm: 493 (41)
Gebara et al[62]	SB-Pq, SP-Pq, Tg, Sal	PCR (16S rRNA)	GDis, RUT pos (15 gingivitis, 15 chronic Ptis)	13/30 (43)
Gebara et al[63]	EGB, SB-Pq, SP-Pq, Tg, Sal	PCR (16S rRNA)	Post-H. pyloriET: GDis RUT pos (15 gingivitis, 15 Chronic Ptis)	Gastric eradication 90% H. pylori: 3/30 (10). Oral eradication: 40% H. pylori: 18/30 (60)
Anand et al[64]	PS	Oral Hygiene	65 pos Ser/RUT/Giemsa; 69 control	Ptss: 30/65 (46);
Al Asqah et al[8]	SB-Pq	RUT	H. pylori-IgG	PDss: 37/50 (60)
Eskandari et al[65]	SB-Pq, SP-Pq	PCR (16S rRNA)	Chronic Ptis (23/67 Gtis)	4/67 (6)
Agarwal et al[66]	SB-Pq	MCT, PCR (16S rRNA)	Chronic Ptis (30 GDss-pos; 20 GDss-neg)	18/30 (60); 3/20 (15)
Bouziane et al[67]	MAS		Gtis (post-H. pyloriET)	RR 63%; [0.37 (95%CI: 0.21-0.64), P = 0.0004]

BL: Blood; EGB: Endoscopic gastric biopsy; Gtis: Gastritis; GDss: Gastric disease; H. pyloriET: Helicobacter pylori eradication therapy; H. pylori-IgG: Presence of anti-H. pylori-IgG; MAS: Meta-analysis study; MCT: Microbial culture techniques; Neg: Negative; PDss: Negative periodontal disease; PS: Periodontal status; Ptis: Periodontitis; PCR: Polimerase chain reaction; Pos: Positive; RUT: Rapid urease test; Sal: Saliva; SB-Pq: Subgingival plaque; Ser: Serology; SP-Pq: Supragingival plaque; Tg: Tongue.

Table 3 Helicobacter pylori detection in aphthous stomatitis n (%)

Ref.	Sample (study design)	Diagnostic method	Patient profile	H. pylori detection rate
Leimola-Virtanen et al[69]	Bs (TS)	Giemsa, ISH	RAS	Giemsa: 14/29 (50); ISH: 6/29 (20)
Porter et al[70]	BL (CCS)	Ser (ELISA)	75 RAS, 83 (15 other oral ulcerative disorders, 41 other oral mucosal lesions, 27 oral dysaesthesia), 25 control	23/75 (31) 27/83 (33) 6/25 (24)
Birek et al[71]	OS (CCS)	PCR (ureC)	RAS	23/32 (72)
Riggio et al[72]	Bs (CCS)	PCR (16S rRNA)	28 RAS, 20 OLP, 13 control	3/28 (11), 0/20 (0); 0/13 (0)
Shimoyama et al[73]	BL, OS (CCS)	MCT, Ser (ELISA)	RAS	0/12 (0)
Victória et al[74]	OS (CCS)	N-PCR1	36 RAS, 48 control	14/36 (38); 16/48 (33)
Iamaroon et al[75]	OS (CCS)	N-PCR (H. pyloriaA)	22 RAU, 15 control (Tg)	1/22 (5); 3/15 (20)
Elsheikh et al[76]	Bs (CCS)	PCR (16S rRNA)	58 RAS and Lymp 88 RAS, 20 control	39/58 (67); 9/88 (10); 0/20 (0)
Mansour-Ghanaei et al[77]	BL, OS (CCS)	Ser (ELISA), PCR1	RAS	H. pylori-IgG: 26/50 (52); PCR: 1/50 (2)
Albanidou-Farmaki et al[78]	Sal, BL, RUT (CSS)	Ser (ELISA), 13-UBT	RAS	34/48 (71)
Karaca et al[79]	Gastric Bs (CSS)	Giemsa (PTE)	RAS	20/23 (89); P < 0.05
Maleki et al[80]	RUT (CCS)	13-UBT	43 RAS, 44 control	16/43 (37); 14/44 (32); P = 0.597
Taş et al[81]	Gastric Bs, BL (CSS)	13-UBT (PTE)	MAL (vitamin B12)	Pre: 30/46 (65); post: 12/30 (40)

¹Data not shown. Helicobacter pylori: H. pylori; BL: Blood; Bs: Biopsy; CCS: Case-control study; CSS: Cross-sectional study; H. pylori-IgG: Presence of anti-H. pylori-IgG; ISH: In situ hybridization; Lymp: Lymphoma; MAL: Minor aphthous lesions; MCT: Microbial culture techniques; N: Nested; OLP: Oral lichen planus; OS: Oral swab; PCR: Polymerase chain reaction; PTE: Post-treatment evaluation; RAS: Recurrent aphthous stomatitis; RAU: Recurrent aphthous ulceration; RUT: Rapid urease test; Ser: Serology; Sal: Saliva; Tg: Tongue; TS: Transversal study;

¹³-UBT: ¹³C-urea breath test.

Table 4 Helicobacter pylori detection in oral cancer n (%)

Ref.	Sample (study design)	Diagnostic method	Patient profile	H. pylori detection rate
Grandis et al[88]	BL (CCS)	Ser (ELISA)	21 HNSCC 21 controls	12/21 (57) 13/21 (62), P > 0.05
Singh et al[89]	Bs (CCS)	MCT, Giemsa, RUT	26 OC 26 controls	MTC: 0/26 (0); 0/26 (0) Giemsa: 4/26 (15); 0/26 (0) RUT: 3/26 (11); 0/26 (0)
Okuda et al[90]	Bs, OS (PRS)	MTC, RT PCR1	GDss (58 OC)	Bs: 54/116 (46); OS: 14/116 (12); OC: 11/58 (19)
Kanda et al[91]	Bs, urine (PRS)	MTC, Ser (ELISA), PCR1, IHC	HNSCC	Bs: 0/31 (0) MTC, IHC, PCR. Urine: 21/31 (68) Ser
Fernando et al[92]	BL (CCS)	Ser (ELISA)	53 cases 60 controls	14/53 (23) 10/60 (17)
Dayama et al[93]	Bs (CCS)	MTC; PCR (16S rRNA)	20 OC 20 controls	OC: 3/20 (15) MCT, PCR Controls: 1/20 (5) MTC and 2/20 (10) PCR

¹Data not shown. BL: Blood; Bs: Biopsy; CCS: Case-control study; GDss: Gastric disease; HNSCC: Head and neck squamous cell carcinomas; ISH: In situ hybridization; MCT: Microbial culture techniques; OC: Oral cancer; OS: Oral swab; PCR: Polymerase chain reaction; PRS: Prospective study; RUT: Rapid urease test; Ser: Serology.

Table 5 Helicobacter pylori detection in burning, halitosis, and lingual dorsum hyperplasia n (%)

Ref.	Diagnostic method	Patient profile	H. pylori detection rate	Hal detection rate
Tiomny et al[111]	SHal	6 Hal	5/6 (83)	Post-H. pyloriET: 0/11(0)
Ierardi et al[112]	OHal	Dys [Hal: 52 (90)]	Diagnosis: 30/52 (58)	Diagnosis: 52/52 (100)
			Double H. pyloriET: 11/30 (64)	Double H. pyloriET: 11/30 (64)
			Triple H. pyloriET: 2/11 (18)	Triple H. pyloriET: 2/11 (18)
Adler et al[113]	EGB, SHal, OHal, Giemsa, PCR (SSA)	Dys, BHH	Tg: 1/1; Gc: 1/1	Case report
Gall-Troselj et al[114]	N-PCR (ureA)	AG: 87 (32)	Tg: 43/268 (16)	17/87 (20),
		BMG: 37 (14)		1/37 (3),
		BMS: 144 (54)		12/54 (22),
		(54 Tg, 90 no-Tg)		13/90 (14)
Serin et al[115]	EGB, Giemsa	Dys, Hal, EGB: H. pylori-pos, no lesion and no atrophy	EGB pos-H. pyloriET: 39/148 (26)	Hal post-H. pyloriET: 40/148 (3)
Adler et al[113]	EGB, SHal, OHal, Giemsa, PCR (SSA) y (16SrRNA)	GDSS [BHH: 46 (37), no-BHH: 78 (63)]	40/46 (87); 2/78 (3)	RR 13.01 CI 6-28.20
Brailo et al[116]	Ser (ELISA)	150 BMS	29/150 (19)	19/150 (13)
Katsinelos et al[117]	EGB, Giemsa, RUT	Dys, Hal,	Diagnosis: 18/18 (100)	Diagnosis: 18/18 (100)
			Triple H. pyloriET: 4/18 (22)	Triple H. pyloriET: 2/18 (11)
			Quad H. pyloriET: 0/18 (0)	Quad H. pyloriET: 2/18 (11)
Moshkowitz et al[118]	EGB, RUT	GDSS [GERD: 72 (55)]	H. pylori vs Hal: P > 0.05	Hal vs GERD: P < 0.05
Suzuki et al[119]	OLT, GC, PCR (16S rRNA)	Non-Dys (251 Hal, 75 no-Hal)	Sal: 21/326 (6)	H. pylori-pos: Higher VSC and OLT Score
Yoo et al[120]	OHal, GC, 13-UBT	H. pylori-pos [EGL: 24 (33), NEGL: 48 (675)]	72/72 (100)	VSC: EGL vs NEGL: P < 0.01
Lee et al[121]	EGB, OHal	Dys, Hal	Gc: 68/88 (77)	Korea Red Ginseng Supplementation
Kinberg et al[122]	EGB	Hal [GDSS: 36 (38)]	14/94 (15)	OHal: 74/94: (78)
Tangerman et al[123]	EGB, OLT, GC, RUT	GDSS, Hal	11/49 (22)	VSC: 9/49 (18); H. pylori: 1/9 (11)

AG: Atrophic glossitis; BHH: Burning, halitosis, and lingual dorsum hyperplasia; BMS: Burning mouth syndrome; BMG: Benign migratory glossitis; Dys: Dyspepsia; EGB: Endoscopic gastric biopsy; EGL: Erosive gastric lesions; GC: Gas chromatography; Gc: Gastric; GERD: Gastroesophageal reflux disease; GDSS: Gastric disease; Hal: Halitosis; H. pyloriET: Helicobacter pylori eradication therapy; N: Nested; NEGL: Non-erosive gastric lesions; OHal: Objective halimeter levels > 100 ppb; OLT: Organoleptic test; PCR: Polymerase chain reaction; Pos: Positive; Quad: Quadruple; RR: Relative risk; RUT: Rapid urease test; Sal: Saliva; Ser: Serology; SHal: Subjective halitosis; SSA: 26-kDa species-specific antigen gene; Tg: Tongue; VSC: Volatil sulfur compounds; ¹³-UBT: ¹³C-urea breath test.