Gastric adenocarcinoma and periodontal disease: A systematic review and meta-analysis<sup/>

Aguiar, Francisco José Nunes; Menezes, Fabrício dos Santos; Fagundes, Marcela de Araújo; Fernandes, Gisele Aparecida; Alves, Fabio de Abreu; Goncalves Filho, João; Curado, Maria Paula

doi:10.1016/j.clinsp.2023.100321

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Review articles • Clinics 79 • 2024 • https://doi.org/10.1016/j.clinsp.2023.100321 copy

Gastric adenocarcinoma and periodontal disease: A systematic review and meta-analysis^☆ ☆ Supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior ‒ Brasil (CAPES) ‒ student fellowship by Finance Code 001.

Authorship SCIMAGO INSTITUTIONS RANKINGS

Highlights

Patients presenting periodontal disease increased the risk of developing gastric adenocarcinoma by 17 %.
The association remained regardless of the diagnostic method for periodontal disease, i.e., clinical examination and self-report.
Moreover, Asian patients with periodontal disease had a higher risk of having gastric adenocarcinoma than American and European patients.

Abstract

Background

The oral cavity is a link between of external environment with gastrointestinal tract. Studies are controversial on the presence of Periodontal Disease (PD) and its association with Gastric Adenocarcinoma (GAC).

Methods

The authors performed a systematic review and meta-analysis to verify the association between PD and GAC. Six electronic databases were evaluated between 1961 and 2022. Titles and abstracts were reviewed independently according to the eligibility criteria, assessing full texts of selected studies. The quality of the included research was verified using the Newcastle-Ottawa Scale for case-control and cohort studies. Statistical analyses were performed based on fixed and/or random effects models to calculate the summarized Relative Risk (RR) and its 95 % Confidence Interval (95 % CI).

Results

There were 639 studies, of which nine articles were included (3 case-controls and 6 cohorts). Overall, the authors identified 1,253 cases of GAC 2,501 controls in case-control studies, and 1,631 patients with GAC enrolled in cohort studies. Patients presenting PD increased the risk of developing GAC by 17 % (RR=1.17; 95 % CI 1.03‒1.32), which remained regardless of the diagnostic method for PD, i.e., clinical examination (RR = 1.19; 95 % CI 1.14‒1.24) and self-report (RR = 1.34; 95 % CI 1.06‒1.69). Moreover, Asian patients (RR=1.17; 95 % CI 1.00‒1.36) with PD had a higher risk of having GAC than American and European patients (RR = 1.18; 95 % CI 0.84‒1.66).

Conclusions

The presence of PD the risk of GAC suggesting that its infectious-inflammatory process of PD may be related to GAC development. Further investigations on the oral-gastric microbiota and its role in the carcinogenesis of gastric cancer should be carried out, and the screening of patients with potential risk for GAC should be considered in the clinical practice of dentists.

Keywords
Gastric neoplasia; Periodontal disease; Periodontitis; Epidemiology

DATABASE	WEBSITE	SEARCH STRATEGY	TOTAL
Medline/PUBMED via National Library of Medicine	http://www.ncbi.nlm.nih.gov/pubmed	(((((((Periodontal Diseases [mh]) OR (Periodontal Diseases)) OR (Periodontal Diseases [tiab])) OR (periodontitis)) OR (periodont)) OR (((((gingivitis [mh]) OR (gingivitis)) OR (gingivitis [tiab])) OR (gingivitis)) OR (gingivitis))) OR ((((((tooth loss [mh]) OR (tooth loss)) OR (tooth loss [tiab])) OR (tooth loss)) OR (tooth loss*)))) AND (((((((Stomach Neoplasms [mesh]) OR (Stomach Neoplasms)) OR (stomach cancer)) OR (gastric adenocarcinoma)) OR (adenocarcinoma [tiab])) OR (gastric cancer)))	353
Embase	www.embase.com	('periodontal disease' OR gingivitis OR periodontitis OR 'tooth loss') AND 'gastric cancer'	74
Scopus	www.scopus.com	(TITLE-ABS-KEY (periodontal AND disease) OR TITLE-ABS-KEY (periodontitis) OR TITLE-ABS-KEY (gingivitis) OR TITLE-ABS-KEY (tooth AND loss) AND TITLE-ABS-KEY (gastric AND cancer))	137
Lilacs	https://lilacs.bvsalud.org/	"(periodontal diseases OR periodontitis OR gingivitis OR tooth loss) AND (stomach neoplasms OR gastric cancer)"	0
Web of science	www.webofknowledge.com	TI=(cancer) AND TS=(periodontal* diseases OR gingivitis OR periodontitis OR tooth* loss AND gastric cancer*) AND AB=(stomach cancer OR gastric cancer AND periodontal disease OR gingivitis OR periodontitis OR tooth loss) AND TI=(stomach cancer OR gastric cancer AND periodontal disease OR gingivitis OR periodontitis OR tooth loss)	75
OpenGrey	http://www.opengrey.eu	"periodontal disease" OR “gingivitis” OR “periodontitis” OR “tooth loss” AND "gastric"	0

Author/ Year/ Country	Design/ Study period	Sample/ Sex/ Age	Exposure	Diagnostic Method for Exposure	Outcome	Diagnostic Method for Theutcome	Association measure and 95 % CI	Adjustment variables
Watabe et al./ 1998/ Japan[37]	case-control 1996 to 1997	Cases: 242 F = 62 (25. 6 %) M = 180 (74. 4 %) Controls: 484 40 - 79 years	Gingivitis Tooth loss	Self-report	Gastric Cancer	Pathology	Gingivitis OR= 1.2 (0.8-1.8) Tooth loss OR=1.7 (1.2-2.4)	-
Hiraki et al./ 2008/ Japan[38]	case-control 2001 to 2005	Cases: 5240 F = 2541 (48.5 %) M = 2699 (51.5 %) Controls: 10,480 F = 5082 (48.5 %) M = 5398 (51. 5 %) 20 - 79 years	Tooth loss	Self-report	Gastric Cancer N = 702	Hospital record	21 teeth left OR=1.0 (reference) 9-20 teeth remaining OR= 1.0 (0.8-1.3) 1-8 teeth remaining OR= 1.1 (0.8-1.5) 0 teeth remaining OR= 0.9 (0.5-1.4)	It acts; Fri; Smoking; Alcohol; Intake of vegetables and fruits; BMI; Regular physical activity.
Shakeri et al./ 2013/ Iran[39]	case-control 2004 to 2011	Cases: 309 F = 83 (26.9 %) M = 226 (73.1 %) Controls: 613 F = 167 (27.2 %) M = 446 (72. 8 %) 40 - 75 years	Tooth loss: Category 1 (≤ 12); Category 2 (13-18); Category 3 (19-24); Category 4 (25-31); Category 5 (32)	Clinical examination	Cardia GC N = 1 61 Non-cardia GC N = 118	Histology	Tooth loss All gastric adenocarcinomas OR= (reference= Category 1(≤12)) Category 2(13-18) OR=0.5(0.2-1.1) Category 3(19-24) OR =0.9(0.4-1.7) Category 4(25-31) OR =1.6(0.8-3.2) Category 5(32) OR =1.4(0.6-3.0) Cardia GC OR = (reference = Category 1(≤12)) Category 2(13-18) OR = 0.6 (0.2-1.9) Category 3(19-24) OR = 1.6 (0.6-4.35) Category 4(25-31) OR = 3.5 (1.2-9.7) Category 5(32) OR = 1.4 (0.4-4.5) Non-cardia GC OR = (reference= Category 1(≤12)) Category 2(13-18) OR = 0.3 (0.1-1.2) Category 3(19-24) OR = 0.4 (0.1-1.3) Category 4(25-31) OR = 1.7 (0.5-5.6) Category 5(32) OR = 2.1 (0.6-6.9)	It acts; Andthnicity; Education; Consumption of fruits and vegetables, Opium or Tobacco; Denture use. Socioeconomic status

Author/ Year/ Country	Design/ Study period	Sample/ Sex/ Age	Exposure	Diagnostic Method for Exposure	Outcome	Diagnostic Method for Outcome	Association measure and 95 % CI	Adjustment variables
Michaud et al./ 2008/ USA[31]	Prospective 1986 to 2004	48,375 men health professionals 40 - 75 years	Periodontal disease; Tooth loss.	Self-report and imaging	Gastric Cancer N = 106	Self-report and Medical records	Periodontal disease In HR=1.0 (reference) Yes HR= 1.1 (0.7-1.7) tooth loss (reference=25-32 teeth) HR= 1.0 17-24 teeth HR=1.1 (0.6-1.8) 0-16 teeth HR= 1.1 (0.5-2.1) Periodontal disease In HR= 1.0 (reference) Yes HR= 1.3 (0.8-2.0) tooth loss (reference=25-32 teeth) HR= 1.0 17-24 teeth HR=1.2 (0.7-2.0) 0-16 teeth HR*= 1.3 (0.6-2.5)	Smoking history (never; former smoker < 10 years; former smoker >10 years; current smoker 1-14 cigarettes/day; 15-24 cigarettes/day; 25+ cigarettes/day) and packets-year (continuous). *Age (continuous), race (white, Asian and black), physical activity, history of diabetes (yes/no), alcohol (quartile), BMI (<22.22-24.9.25-29.9.30+), geographic location (south, east, northeast, midwest) height (quintiles), calcium intake (quintiles), total caloric intake (quintiles), red meat intake (quintiles), fruit and vegetable intake (quintiles), vitamin D (deciles).
Arora et al./ 2010/ Sweden[43]	Prospective Cohort 1963 to 2004	15. 333 F = 8. 433 (55 %) M = 6. 900 (45 %) 38 - 77 years	Periodontal disease	Self-report	Gastric Cancer N = 193	National Registry	Periodontal disease HR= 0.8 (0.4-1.5) Less mobility HR= 0.8 (0.5-1.3) in disease HR= 1.00 (reference)	Sex (male/female), age (years), education (no schooling/secondary/vocation/other), employment (yes/no/housewife/pensioner/other), number of siblings (ordinal), smoking status (smoker current > 1 pack/day; smoker 〈1 pack/day; former smoker 〉 1 pack/day; former smoker < 1 pack/day; never smoked), partner's smoking status (smoker/ex-smoker/never smoked), smoking status of alcohol (alcohol drinker/ex drinker/never), diabetes (yes/no) and BMI (<20, 20-24.9, 25-29.9.>30 kg/m2).
Wen et al./ 2013/ Taiwan[44]	Retrospective Cohort 1997 to 2010	144.896 F = 71,086 (49. 1 %) M = 73,810 (50. 9 %) >20 years	Periodontitis (ICD-9: 523.3 and 523.4) and Gingivitis (ICD-9: 523.0 and 523.1)	Positive diagnosis and treated at least 3 times	Gastric Cancer N = 151	Histology through national registry	RR= 1.0 (1.0-1.1) Adjusted HR= 0.9 (0.7-1.1)*	*Fri; It acts; Presence of comorbidity.
Chung et al./ 2015/ Taiwan[45]	Retrospective Cohort 2002 to 2009	40.140 F = 20,190 (50. 3 %) M = 19,950 (49. 7 %) >40 years	chronic periodontitis	Positive diagnosis based on symptoms, medical history and diagnostic test result.	Gastrointestinal cancer (ICD-9: 150-159) N = 1084	Medical records	Adjusted HR= 1.2 (1.1-1.2)	Monthly income; Geographic region; Diabetes.
Nwizu et al./ 2017/ USA[30]	Prospective Cohort 1999 to 2013	65,869 post-menopausal women 50 - 79 years	Periodontal disease	Self-report	Stomach	Self-report in biennial questionnaires and medical records	Stomach HR=1.5 (0.9-2.6)	-
Chou et al./ 2018/ Taiwan[46]	Retrospective Cohort 2001 to 2010	50,970 F = 24,850 (48.7 %) M = 26,120 (51.3 %) 35 - 80 years	Moderate and severe periodontal disease	Database: diagnosed patients who received an additional procedure code for periodontitis.	Stomach (N = 101)	Patients diagnosed with gastrointestinal cancer according to the ICD-O-3 (C-16)	HR=1.0 (0.6-1.4)	It acts; Fri; Comorbidities (diabetes mellitus/colectomy); index of Charlson; Medication (aspirin/NSAIDs); Socioeconomic level (estimated monthly income and educational level).

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[1] ⁎ Corresponding author. E-mail address:mp.curado@accamargo.org.br (M.P. Curado).

Brasil

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Gastric adenocarcinoma and periodontal disease: A systematic review and meta-analysis☆ ☆ Supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior ‒ Brasil (CAPES) ‒ student fellowship by Finance Code 001.

Highlights

Abstract

Background

Methods

Results

Conclusions

Gastric adenocarcinoma and periodontal disease: A systematic review and meta-analysis^☆ ☆ Supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior ‒ Brasil (CAPES) ‒ student fellowship by Finance Code 001.