Comparison of Salivary Bacterial Flora in Iranian Patients with Hiatal Hernia and Healthy Subjects

Farzaneh Pakdel, Mohammad Hossein Somi, Masoud Shirmohamadi, Leila Zaker Esna Ashari, Milad Ghanizadeh, Hossein Samadi Kafil, Marzieh Aghazadeh


Objective: To evaluate salivary microbial flora of patients with hiatal hernia and compare it with that of healthy subjects. Material and Methods: In this cross-sectional study, 50 patients with hiatal hernia measuring >1 cm and 50 healthy subjects (as the controls) were selected using simple random technique. One mL of salivary sample was taken from each patient, transferred into 50-mL Falcon tubes and immediately carried to the microbiology Laboratory of Tabriz Faculty of Medicine. The salivary samples were cultured on specific Streptococcus viridans (S. mitis, S. mutans, S. salivarius and S. sanguis), Enterococcus spp. and Lactobacillus culture media. Then the samples were incubated at 37°C for 7 days, followed by evaluation of the bacterial colonies. Statistical significance was defined at p<0.05. Results: A total of 34% of subjects with hiatal hernia and 26% healthy subjects exhibited Lactobacillus gasseri in their salivary samples; 16% of subjects with hernia and 6% of healthy subjects exhibited Enterococci spp. in their salivary samples. In addition, 82% of subjects with hernia and 72% of healthy subjects exhibited S. mutans in their salivary samples; 74% and 4% of subjects with hernia and 76% and 4% of healthy subjects exhibited gram-positive and gram-negative bacilli in their salivary samples, respectively. Furthermore, 98% of subjects with hernia and 86% of healthy subjects exhibited gram-positive cocci in their salivary samples, however without significant difference between the groups (p>0.05). Conclusion: No significant differences in the counts of Lactobacillus spp., Enterococcus spp., Streptococcus viridans and gram-positive and gram-negative bacterial species between healthy controls and subjects with hiatal hernia.


Hernia, Hiatal; Gastrointestinal Microbiome, Saliva.

Full Text:



Gryglewski A, Pena IZ, Tomaszewski KA, Walocha JA. Unsolved questions regarding the role of esophageal hiatus anatomy in the development of esophageal hiatal hernias. Adv Clin Exp Med 2014; 23(4):639-44.

Dean C, Etienne D, Carpentier B, Gielecki J, Tubbs RS, Loukas M. Hiatal hernias. Surg Radiol Anat 2012; 34(4):291-9. doi: 10.1007/s00276-011-0904-9.

Gordon C, Kang JY, Neild PJ, Maxwell JD. The role of the hiatus hernia in gastro-oesophageal reflux disease. Aliment Pharmacol Ther 2004; 20(7):719-32. doi: 10.1111/j.1365-2036.2004.02149.x.

Emerenziani S, Habib FI, Ribolsi M, Caviglia R, Guarino MP, Petitti T, et al. Effect of hiatal hernia on proximal oesophageal acid clearance in gastro-oesophageal reflux disease patients. Aliment Pharmacol Ther 2006; 23(6):751-7. doi: 10.1111/j.1365-2036.2006.02816.x.

Franzen T, Tibbling L. Is the severity of gastroesophageal reflux dependent on hiatus hernia size? World J Gastroenterol 2014; 20(6):1582-4. doi: 10.3748/wjg.v20.i6.1582.

Kahrilas PJ. Clinical practice. Gastroesophageal reflux disease. N Engl J Med 2008; 359(16):1700-7. doi: 10.1056/NEJMcp0804684.

Pace F, Pallotta S, Tonini M, Vakil N, Bianchi Porro G. Systematic review: Gastro-oesophageal reflux disease and dental lesions. Aliment Pharmacol Ther 2008; 27(12):1179-86. doi: 10.1111/j.1365-2036.2008.03694.x.

Katz PO, Gerson LB, Vela MF. Guidelines for the diagnosis and management of gastroesophageal reflux disease. Am J Gastroenterol. 2013; 108(3):308-28. doi: 10.1038/ajg.2012.444.

Filipi K, Halackova Z, Filipi V. Oral health status, salivary factors and microbial analysis in patients with active gastro-oesophageal reflux disease. Int Dent J 2011; 61(4):231-7. doi: 10.1111/j.1875-595X.2011.00063.x.

Linnett V, Seow WK, Connor F, Shepherd R. Oral health of children with gastro-esophageal reflux disease: A controlled study. Aust Dent J 2002; 47(2):156-62. doi: 10.1111/j.1834-7819.2002.tb00321.x.

Ersin NK, Oncag O, Tumgor G, Aydogdu S, Hilmioglu S. Oral and dental manifestations of gastroesophageal reflux disease in children: A preliminary study. Pediatr Dent 2006; 28(3):279-84.

Silva MA, Damante JH, Stipp AC, Tolentino MM, Carlotto PR, Fleury RN. Gastroesophageal reflux disease: New oral findings. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001; 91(3):301-10. doi: 10.1067/moe.2001.111139.

Correa MC, Lerco MM, Cunha ML, Henry MA. Salivary parameters and teeth erosions in patients with gastroesophageal reflux disease. Arq Gastroenterol 2012; 49(3):214-8. doi: 10.1590/S0004-28032012000300009.

Liu B, Faller LL, Klitgord N, Mazumdar V, Ghodsi M, Sommer DD, et al. Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One 2012; 7(6):4. doi: 10.1371/journal.pone.0037919.

Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005; 43(11):5721-32. doi: 10.1128/JCM.43.11.5721-5732.2005.

Yip KH, Smales RJ. Implications of oral biofilms in medically at risk persons. J Biomed Res 2012; 26(1):1-7. doi: 10.1016/S1674-8301(12)60001-3.

Gholizadeh P, Eslami H, Yousefi M, Asgharzadeh M, Aghazadeh M, Kafil HS. Role of oral microbiome on oral cancers, a review. Biomed Pharmacother 2016; 84:552-8. doi: 10.1016/j.biopha.2016.09.082.

Ames NJ, Sulima P, Ngo T, Barb J, Munson PJ, Paster BJ, et al. A characterization of the oral microbiome in allogeneic stem cell transplant patients. PLoS One 2012; 7(10):e47628. doi: 10.1371/journal.pone.0047628.

Norder Grusell E, Dahlen G, Ruth M, Ny L, Quiding-Jarbrink M, Bergquist H, et al. Bacterial flora of the human oral cavity, and the upper and lower esophagus. Dis Esophagus 2013; 26(1):84-90. doi: 10.1111/j.1442-2050.2012.01328.x.

Docktor MJ, Paster BJ, Abramowicz S, Ingram J, Wang YE, Correll M, et al. Alterations in diversity of the oral microbiome in pediatric inflammatory bowel disease. Inflamm Bowel Dis 2012; 18(5):935-42. doi: 10.1002/ibd.21874.

Asgharzadeh M, Kafil HS, Khakpour M. Comparison of mycobacterial interspersed repetitive unit-variable number tandem repeat and IS6110-RFLP methods in identifying epidemiological links in patients with tuberculosis in Northwest of Iran. Ann Microbiol 2008; 58:333. doi: 10.1007/BF03175339.

Kafil HS, Mobarez AM. Spread of Enterococcal surface protein in antibiotic resistant entero-coccus faecium and enterococcus faecalis isolates from urinary tract infections. Open Microbiol J 2015; 9:14-7. doi: 10.2174/1874285801509010014.

Roy Cullimore D. Practical Atlas for Bacterial Identification. 2.nd. ed. New York: CRC Press/Taylor and Francic Group, 2010. 327p.

Kafil HS, Mobarez AM, Moghadam MF, Hashemi ZS, Yousefi M. Gentamicin induces efaA expression and biofilm formation in Enterococcus faecalis. Microb Pathog 2016; 92:30-5. doi: 10.1016/j.micpath.2015.12.008.

Jabbari V, Mokarram RR, Khiabani MS, Askari F, Ahmadi E, mohammad Hassanzadeh A, et al. Molecular Identification of Lactobacillus acidophilus as a probiotic potential from traditional doogh samples and evaluation of their antimicrobial activity against some pathogenic bacteria. Biomed Res 2017; 28(4):1458-63.

Jabbari V, Khiabani MS, Mokarram RR, Hassanzadeh AM, Ahmadi E, Gharenaghadeh S, et al. Lactobacillus plantarum as a probiotic potential from kouzeh cheese (traditional Iranian cheese) and its antimicrobial activity. Probiotics Antimicrob Proteins 2017; 9(2):189-93. doi: 10.1007/s12602-017-9255-0.

Gholizadeh P, Pormohammad A, Eslami H, Shokouhi B, Fakhrzadeh V, Kafil HS. Oral pathogenesis of Aggregatibacter actinomycetemcomitans. Microb Pathog 2017; 113:303-11. doi: 10.1016/j.micpath.2017.11.001.

Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, et al. Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 2008; 87(11):1016-20. doi: 10.1177/154405910808701104.

Gholizadeh P, Eslami H, Kafil HS. Carcinogenesis mechanisms of Fusobacterium nucleatum. Biomed Pharmacother 2017; 89:918-25. doi: 10.1016/j.biopha.2017.02.102.