Association Between Infection with Campylobacter Species, Poor Oral Health and Environmental Risk Factors on Esophageal Cancer: a Hospital-based Case-control Study in Thailand

Overview

Journal Eur J Med Res

Publisher Biomed Central

Specialty General Medicine

Date 2021 Aug 1

PMID 34332608

Citations 8

Authors

Arisara Poosari

Thitima Nutravong

Prakasit Sa-Ngiamwibool

Wises Namwat

Supaporn Chatrchaiwiwatana

Piti Ungareewittaya

Affiliations

Soon will be listed here.

Abstract

Background: Previous studies have shown the association between Campylobacter species infection and that environmental factors, poor oral hygiene in particular, are linked to an increased risk of esophageal cancer (EC). However, no study has reported on these factors in Thailand. Thus, this study's objective was to evaluate the impact of the relationship between Campylobacter infection and environmental factors on EC incidence in the population of Thailand.

Methods: Data from a case-control study were collected from 105 newly diagnosed EC cases and 105 controls recruited from 2007 to 2017. Infection with Campylobacter spp. was detected in the formalin-fixed paraffin-embedded (FFPE) tissue of EC taken from gastroesophageal biopsy specimens obtained from the participants, and evaluated using TaqMan real-time PCR. Multivariable logistic regression was performed to calculate the odds ratios (ORs) and perform data analysis.

Results: Smoking, alcohol use, a family history of cancer, history of gastroesophageal reflux disease, poor oral hygiene and Campylobacter spp. infection were shown to be significant risk factors for EC (p < 0.05). The combination of poor oral hygiene and infection with Campylobacter spp. constituted significant risk for EC (p < 0.001). In addition, the risk of EC in subjects co-infected with C. rectus and C. concisus that practiced poor oral hygiene was even higher and was significant (ORadj = 4.7; 95% CI 2.41-9.98; p = 0.003).

Conclusions: In Thailand, the major risk factors for EC are smoking status, alcohol drinking, family history of cancer, GERD, poor oral hygiene and Campylobacter spp. infection. This study found Campylobacter spp. prevalence to be associated with EC and appears to be enhanced by poor oral hygiene, suggesting that a combination of poor oral hygiene and Campylobacter species infection may together act as an important etiological risk factor for EC.

Citing Articles

Prevalence and antimicrobial resistance of and over time in Thailand under a One Health approach: A systematic review and meta-analysis.

Phu D, Wongtawan T, Nam T, Truong D, Suttidate N, Carrique-Mas J One Health. 2025; 20:100965.

PMID: 39898318 PMC: 11782884. DOI: 10.1016/j.onehlt.2025.100965.

Global Burden of Esophageal Cancer and Its Risk Factors: A Systematic Analysis of the Global Burden of Disease Study 2019.

Ilic I, Zivanovic Macuzic I, Ravic-Nikolic A, Ilic M, Milicic V Life (Basel). 2025; 15(1).

PMID: 39859964 PMC: 11767048. DOI: 10.3390/life15010024.

Oral Bacteria, Virus and Fungi in Saliva and Tissue Samples from Adult Subjects with Oral Squamous Cell Carcinoma: An Umbrella Review.

Di Spirito F, Di Palo M, Folliero V, Cannata D, Franci G, Martina S Cancers (Basel). 2023; 15(23).

PMID: 38067244 PMC: 10705713. DOI: 10.3390/cancers15235540.

Microbiome analysis of saliva from oral squamous cell carcinoma (OSCC) patients and tobacco abusers with potential biomarkers for oral cancer screening.

Oyeyemi B, Kaur U, Paramraj A, Chintamani , Tandon R, Kumar A Heliyon. 2023; 9(11):e21773.

PMID: 38034672 PMC: 10685184. DOI: 10.1016/j.heliyon.2023.e21773.

Epidemiological evidence and association of human papillomavirus with esophageal cancer in northeastern Thailand: a case-control study.

Burassakarn A, Pientong C, Tongchai P, Wongjampa W, Poosari A, Udomsin A Front Microbiol. 2023; 14:1146322.

PMID: 37180234 PMC: 10172481. DOI: 10.3389/fmicb.2023.1146322.

References

Elsalem L, Jumah A, Alfaqih M, Aloudat O . The Bacterial Microbiota of Gastrointestinal Cancers: Role in Cancer Pathogenesis and Therapeutic Perspectives. Clin Exp Gastroenterol. 2020; 13:151-185. PMC: 7211962. DOI: 10.2147/CEG.S243337. View

Snider E, Compres G, Freedberg D, Khiabanian H, Nobel Y, Stump S . Alterations to the Esophageal Microbiome Associated with Progression from Barrett's Esophagus to Esophageal Adenocarcinoma. Cancer Epidemiol Biomarkers Prev. 2019; 28(10):1687-1693. PMC: 6774849. DOI: 10.1158/1055-9965.EPI-19-0008. View

Akutko K, Matusiewicz K . Campylobacter concisus as the etiologic agent of gastrointestinal diseases. Adv Clin Exp Med. 2017; 26(1):149-154. DOI: 10.17219/acem/61428. View

Yang L, Francois F, Pei Z . Molecular pathways: pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res. 2012; 18(8):2138-44. PMC: 3725293. DOI: 10.1158/1078-0432.CCR-11-0934. View

Carrique-Mas J, Bryant J, Cuong N, Hoang N, Campbell J, Hoang N . An epidemiological investigation of Campylobacter in pig and poultry farms in the Mekong delta of Vietnam. Epidemiol Infect. 2013; 142(7):1425-36. PMC: 4045178. DOI: 10.1017/S0950268813002410. View

Baba Y, Iwatsuki M, Yoshida N, Watanabe M, Baba H . Review of the gut microbiome and esophageal cancer: Pathogenesis and potential clinical implications. Ann Gastroenterol Surg. 2018; 1(2):99-104. PMC: 5881342. DOI: 10.1002/ags3.12014. View

Lofdahl H, Lu Y, Lagergren J . Sex-specific risk factor profile in oesophageal adenocarcinoma. Br J Cancer. 2008; 99(9):1506-10. PMC: 2579703. DOI: 10.1038/sj.bjc.6604701. View

Samosornsuk W, Asakura M, Yoshida E, Taguchi T, Nishimura K, Eampokalap B . Evaluation of a cytolethal distending toxin (cdt) gene-based species-specific multiplex PCR assay for the identification of Campylobacter strains isolated from poultry in Thailand. Microbiol Immunol. 2007; 51(9):909-17. DOI: 10.1111/j.1348-0421.2007.tb03974.x. View

Li D, He R, Hou G, Ming W, Fan T, Chen L . Characterization of the Esophageal Microbiota and Prediction of the Metabolic Pathways Involved in Esophageal Cancer. Front Cell Infect Microbiol. 2020; 10:268. PMC: 7333312. DOI: 10.3389/fcimb.2020.00268. View

10.

Amir I, Konikoff F, Oppenheim M, Gophna U, Half E . Gastric microbiota is altered in oesophagitis and Barrett's oesophagus and further modified by proton pump inhibitors. Environ Microbiol. 2013; 16(9):2905-14. DOI: 10.1111/1462-2920.12285. View

11.

Mozaffari Namin B, Mehdi Soltan Dallal M, Ebrahimi Daryani N . The Effect of Campylobacter concisus on Expression of IL-18, TNF-α and p53 in Barrett's Cell Lines. Jundishapur J Microbiol. 2016; 8(12):e26393. PMC: 4744463. DOI: 10.5812/jjm.26393. View

12.

Snider E, Freedberg D, Abrams J . Potential Role of the Microbiome in Barrett's Esophagus and Esophageal Adenocarcinoma. Dig Dis Sci. 2016; 61(8):2217-2225. PMC: 4945493. DOI: 10.1007/s10620-016-4155-9. View

13.

Macfarlane S, Furrie E, Macfarlane G, Dillon J . Microbial colonization of the upper gastrointestinal tract in patients with Barrett's esophagus. Clin Infect Dis. 2007; 45(1):29-38. DOI: 10.1086/518578. View

14.

Virani S, Bilheem S, Chansaard W, Chitapanarux I, Daoprasert K, Khuanchana S . National and Subnational Population-Based Incidence of Cancer in Thailand: Assessing Cancers with the Highest Burdens. Cancers (Basel). 2017; 9(8). PMC: 5575611. DOI: 10.3390/cancers9080108. View

15.

Samareh-Fekri M, Hashemi Bajgani S, Shafahi A, Asadi-Zarandi M, Mollaie H, Jamali Paghalhe A . Detection of in the Bronchoalveolar Lavage of Patients with Lung Cancer Using Real-Time PCR. Jundishapur J Microbiol. 2017; 9(11):e32144. PMC: 5240154. DOI: 10.5812/jjm.32144. View

16.

Abnet C, Kamangar F, Islami F, Nasrollahzadeh D, Brennan P, Aghcheli K . Tooth loss and lack of regular oral hygiene are associated with higher risk of esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2008; 17(11):3062-8. PMC: 2586052. DOI: 10.1158/1055-9965.EPI-08-0558. View

17.

Peters B, Wu J, Pei Z, Yang L, Purdue M, Freedman N . Oral Microbiome Composition Reflects Prospective Risk for Esophageal Cancers. Cancer Res. 2017; 77(23):6777-6787. PMC: 5726431. DOI: 10.1158/0008-5472.CAN-17-1296. View

18.

Elliott D, Walker A, ODonovan M, Parkhill J, Fitzgerald R . A non-endoscopic device to sample the oesophageal microbiota: a case-control study. Lancet Gastroenterol Hepatol. 2017; 2(1):32-42. PMC: 5656094. DOI: 10.1016/S2468-1253(16)30086-3. View

19.

Blackett K, Siddhi S, Cleary S, Steed H, Miller M, Macfarlane S . Oesophageal bacterial biofilm changes in gastro-oesophageal reflux disease, Barrett's and oesophageal carcinoma: association or causality?. Aliment Pharmacol Ther. 2013; 37(11):1084-92. DOI: 10.1111/apt.12317. View

20.

Bhat S, Coleman H, Yousef F, Johnston B, McManus D, Gavin A . Risk of malignant progression in Barrett's esophagus patients: results from a large population-based study. J Natl Cancer Inst. 2011; 103(13):1049-57. PMC: 3632011. DOI: 10.1093/jnci/djr203. View