ISSN: 2008-2258
Vol 14, No 4 (2021): Autumn
Candida colonization of the esophagus and gastric mucosa; a comparison of patients taking proton pump inhibitors and those taking histamine receptor antagonist drugs
Gastroenterology and Hepatology from Bed to Bench,
,
https://doi.org/10.22037/ghfbb.v14i4.2178
Abstract
Aim: Investigation of Candida colonization of the esophagus and gastric mucosa in patients taking proton pump inhibitors in comparison to those taking histamine-2 receptor antagonists.
Background: Candida species are normal flora of alimentary tract can cause infection of the esophagus and gastro-intestinal tract in immunocompromised patients. Consumption of proton pump inhibitors, and histamine-2 receptor antagonists have shown to alter the gastric pH which may predispose to floral transmission and colonization of the esophagus and stomach.
Patients and methods: Two hundred and forty-five clinical specimens were obtained from 91 patients underwent endoscopy from September 2019 to February 2020. Direct microscopy with KOH 10% and subculture on sabouraud dextrose agar containing chloramphenicol used as primary screening. PCR with ITS primers was performed to amplify ITS1-5.8SrDNA-ITS2 region and MspI restriction enzyme used for RFLP to identify clinical isolates.
Results: Seventy cultures out of 245 specimens were positive for Candida colonization (28.5%). Colonization of Candida species in gastric acid and gastric tissue biopsies of patients who took PPIs and H2 blockers was significantly higher than those were in control group (p = 0.001). The use of ranitidine, pantoprazole and omeprazole increased the risk of gastric candidiasis by 10.60, 9.20, and 12.99 times, respectively (p < 0.05).
Conclusion: The use of PPIs and H2 blockers, ageing, and consumption of vegetables were main risk factors for gastric infection in the present survey, and some other variables such as Candida species, cigarette smoking, drinking alcohol, etc. were not implicated in the development of gastroesophageal lesions. We need further investigations to know how these predisposing factors change the host defenses mechanisms and increase colonization of fungi at mucosal surfaces.
Keywords:
- Candida colonization, Gastroesophageal, Proton pump inhibitors, Histamine receptor antagonist
How to Cite
Mottaghi, B., Emami, M. H., Riahi, P., Fahim, A., Rahimi, H., & Mohammadi, R. (2021). Candida colonization of the esophagus and gastric mucosa; a comparison of patients taking proton pump inhibitors and those taking histamine receptor antagonist drugs . Gastroenterology and Hepatology from Bed to Bench, 14(4). https://doi.org/10.22037/ghfbb.v14i4.2178
References
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10. Silva GAd, Bernardi TL, Schaker PDC, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Braz Arch Biol Technol 2012;55:319-27.
11. Scott B, Jenkins D. Gastro-oesophageal candidiasis. Gut 1982;23:137-9.
12. Neal K, Logan R. Potential gastrointestinal effects of long‐term acid suppression with proton pump inhibitors. Aliment Pharmacol Ther 2001 Jul;15(7):1085-6.
13. Freedberg DE, Lamousé-Smith ES, Lightdale JR, Jin Z, Yang Y-X, Abrams JA. Use of acid suppression medication is associated with risk for C. difficile infection in infants and children: a population-based study. Clin Infect Dis 2015;61:912-7.
14. Mimidis K, Papadopoulos V, Margaritis V, Thomopoulos K, Gatopoulou A, Nikolopoulou V, et al. Predisposing factors and clinical symptoms in HIV‐negative patients with Candida oesophagitis: are they always present? Int J Clin Pract 2005;59:210-3.
15. Mullaoglu S, Turktas H, Kokturk N, Tuncer C, Kalkanci A, Kustimur S, editors. Esophageal candidiasis and Candida colonization in asthma patients on inhaled steroids. Allergy & Asthma Proceedings; 2007.
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17. Naito Y, Yoshikawa T, Oyamada H, Tainaka K, Morita Y, Kogawa T, et al. Esophageal candidiasis. Gastroenterol Jpn 1988;23:363-70.
18. Jacobs C, Coss Adame E, Attaluri A, Valestin J, Rao SSC. Dysmotility and proton pump inhibitor use are independent risk factors for small intestinal bacterial and/or fungal overgrowth. Aliment Pharmacol Ther 2013;37:1103-11.
19. Von Rosenvinge EC, Song Y, White JR, Maddox C, Blanchard T, Fricke WF. Immune status, antibiotic medication and pH are associated with changes in the stomach fluid microbiota. The ISME J 2013;7:1354-66.
20. Karczewska E, Wojtas I, Sito E, Trojanowska D, Budak A, Zwolinska-Wcislo M, et al. Assessment of co-existence of Helicobacter pylori and Candida fungi in diseases of the upper gastrointestinal tract. J Physiol Pharmacol 2009;60:33-9.
21. Husebye E, Skar V, Høverstad T, Iversen T, Melby K. Abnormal intestinal motor patterns explain enteric colonization with gram-negative bacilli in late radiation enteropathy. Gastroenterol 1995;109:1078-89.
22. Bühling A, Radun D, Müller W, Malfertheiner P. Influence of anti‐Helicobacter triple‐therapy with metronidazole, omeprazole and clarithromycin on intestinal microflora. Aliment Pharmacol Ther 2001;15:1445-52.
23. Karmeli Y, Stalnikowitz R, Eliakim R, Rahav G. Conventional dose of omeprazole alters gastric flora. Dig Dis Sci 1995;40:2070-3.
24. Gościmski A, Matras J, Wallner G. Microflora of gastric juice in patients after eradication of Helicobacter pylori and treatment with a proton pump inhibitor. Wiadomosci Lekarskie 2002;55:19-28.
25. Safe M, Chan WH, Leach ST, Sutton L, Lui K, Krishnan U. Widespread use of gastric acid inhibitors in infants: are they needed? Are they safe? World J Gastrointest Pharmacol Ther 2016; 7: 531–39.
26. De Bruyne P, Ito S. Toxicity of long-term use of proton pump inhibitors in children. Arch Dis Child 2018;103:78-82.
27. Motegi H, Abe S, Tansho S, Suzuki D, Yamaguchi H, Hoshino E. Suppressive effect of lansoprazole on anti-Candida activity of murine macrophages. Kansenshogaku Zasshi 2001;75:137-43.
28. Imhann F, Bonder MJ, Vila AV, Fu J, Mujagic Z, Vork L, et al. Proton pump inhibitors affect the gut microbiome. Gut 2016;65:740-8.
29. Wang K, Lin HJ, Perng CL, Tseng GY, Yu KW, Chang FY, et al. The effect of H2-receptor antagonist and proton pump inhibitor on microbial proliferation in the stomach. Hepato-gastroenterology 2004;51:1540-3.
30. Cohen S, Bueno de Mesquita M, Mimouni FB. Adverse effects reported in the use of gastroesophageal reflux disease treatments in children: a 10 years literature review. Br J Clin Pharmacol 2015;80:200-8.
31. Guillet R, Stoll BJ, Cotten CM, Gantz M, McDonald S, Poole WK, et al. Association of H2-blocker therapy and higher incidence of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2006;117:e137-e42.
32. Stoll BJ, Temprosa M, Tyson JE, Papile L-A, Wright LL, Bauer CR, et al. Dexamethasone therapy increases infection in very low birth weight infants. Pediatrics 1999;104(5):e63. DOI: https://doi.org/10.1542/peds.104.5.e63.
33. Saiman L, Ludington E, Pfaller M, Rangel-Frausto S, Wiblin TR, Dawson J, et al. Risk factors for candidemia in neonatal intensive care unit patients. Pediatr Infect Dis J 2000;19:319-24.
34. Ross AL, Slain D, Cumpston A, Bryant AM, Hamadani M, Craig M. Evaluation of an alternative posaconazole prophylaxis regimen in haematological malignancy patients receiving concomitant stress ulcer prophylaxis. Int J Antimicrob Agents 2012;40:557-61.
35. Sasaki K. Candida-associated gastric ulcer relapsing in a different position with a different appearance. World J Gastroenterol 2012;18:4450-53.
36. Soysa N, Samaranayake L, Ellepola A. Antimicrobials as a contributory factor in oral candidosis–a brief overview. Oral Dis 2008;14:138-43.
37. Gow NA, Brown AJ, Odds FC. Fungal morphogenesis and host invasion. Curr Opin Microbiol 2002;5:366-71.
38. Belazi M, Velegraki A, Fleva A, Gidarakou I, Papanaum L, Baka D, et al. Candidal overgrowth in diabetic patients: potential predisposing factors. Mycoses 2005;48:192-6.
39. Kumar B, Padshetty N, Bai K, Rao M. Prevalence of Candida in the oral cavity of diabetic subjects. J Assoc Phys India 2005;53:599-602.
40. Daniluk T, Tokajuk G, Stokowska W, Fiedoruk K, Sciepuk M, Zaremba M, et al. Occurrence rate of oral Candida albicans in denture wearer patients. Adv Med Sci 2006;51:77-80.
41. Kadir T, Pisiriciler R, Akyüz S, Yarat A, Emekli N, Ipbüker A. Mycological and cytological examination of oral candidal carriage in diabetic patients and non‐diabetic control subjects: thorough analysis of local aetiologic and systemic factors. J Oral Rehabil 2002;29:452-7.
42. Amiri HM, Frandah W, Colmer-Hamood J, Raj R, Nugent K. Risk factors of Candida colonization in the oropharynx of patients admitted to an intensive care unit. J Mycol Med 2012;22:301-7.
43. Delisle M-S, Williamson DR, Perreault MM, Albert M, Jiang X, Heyland DK. The clinical significance of Candida colonization of respiratory tract secretions in critically ill patients. J Crit Care 2008;23:11-7.
44. Garbino J, Lew DP, Romand J-A, Hugonnet S, Auckenthaler R, Pittet D. Prevention of severe Candida infections in nonneutropenic, high-risk, critically ill patients: a randomized, double-blind, placebo-controlled trial in patients treated by selective digestive decontamination. Intensive Care Med 2002;28:1708-17.
45. El-Ebiary M, Torres A, Fabregas N, de la Bellacasa JP, Gonzalez J, Ramirez J, et al. Significance of the isolation of Candida species from respiratory samples in critically ill, non-neutropenic patients: an immediate postmortem histologic study. Am J Respir Crit 1997;156:583-90.
46. Olaechea P, Palomar M, León-Gil Ct, Alvarez-Lerma F, Jorda R, Nolla-Salas J, et al. Economic impact of Candida colonization and Candida infection in the critically ill patient. Eur J Clin Microbiol 2004;23:323-30.
2. Tsukamoto H. Clinicopathological studies on fungus infections of the digestive tract. Nihon Shokakibyo Gakkai Zasshi 1986;83:2341-50.
3. Zwolińska-Wcisło M, Budak A, Bogdał J, Trojanowska D, Stachura J. Fungal colonization of gastric mucosa and its clinical relevance. Med Sci Monit 2001;7:982-88.
4. Savino JA, Agarwal N, Wry P, Policastro A, Cerabona T, Austria L. Routine prophylactic antifungal agents (clotrimazole, ketoconazole, and nystatin) in nontransplant/nonburned critically ill surgical and trauma patients. J Trauma 1994;36:20-5.
5. Daniell H. Acid suppressing therapy as a risk factor for Candida esophagitis. Dis Esophagus 2016;29:479-83.
6. Alshamsi F, Belley-Cote E, Cook D, Almenawer SA, Alqahtani Z, Perri D, et al. Efficacy and safety of proton pump inhibitors for stress ulcer prophylaxis in critically ill patients: a systematic review and meta-analysis of randomized trials. Crit Care 2016;20:120. doi: 10.1186/s13054-016-1305-6.
7. Reimer C. Safety of long-term PPI therapy. Best Pract Res Clin Gastroenterol 2013;27:443-54.
8. Safavi M, Sabourian R, Foroumadi A. Treatment of Helicobacter pylori infection: Current and future insights. World J Clin Cases 2016;4:5-19.
9. Shah N, Cavanagh Y, Shulik O, Patel P, DeBari VA, Baddoura W. Proton Pump Inhibitors and Corticosteroids as Synergistic Risk Factors for Candida Esophagitis. Am J Gastroenterol 2015;110: S737-S738.
10. Silva GAd, Bernardi TL, Schaker PDC, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Braz Arch Biol Technol 2012;55:319-27.
11. Scott B, Jenkins D. Gastro-oesophageal candidiasis. Gut 1982;23:137-9.
12. Neal K, Logan R. Potential gastrointestinal effects of long‐term acid suppression with proton pump inhibitors. Aliment Pharmacol Ther 2001 Jul;15(7):1085-6.
13. Freedberg DE, Lamousé-Smith ES, Lightdale JR, Jin Z, Yang Y-X, Abrams JA. Use of acid suppression medication is associated with risk for C. difficile infection in infants and children: a population-based study. Clin Infect Dis 2015;61:912-7.
14. Mimidis K, Papadopoulos V, Margaritis V, Thomopoulos K, Gatopoulou A, Nikolopoulou V, et al. Predisposing factors and clinical symptoms in HIV‐negative patients with Candida oesophagitis: are they always present? Int J Clin Pract 2005;59:210-3.
15. Mullaoglu S, Turktas H, Kokturk N, Tuncer C, Kalkanci A, Kustimur S, editors. Esophageal candidiasis and Candida colonization in asthma patients on inhaled steroids. Allergy & Asthma Proceedings; 2007.
16. Fidan F, Uslan İ, Çetinkaya Z, Sezer M, Kara Z, Ünlü M. Prevalance of esophageal candidiasis in patients treated with ınhaled and short course systemic steroids. Med J Kocatepe 2006;6:45-8.
17. Naito Y, Yoshikawa T, Oyamada H, Tainaka K, Morita Y, Kogawa T, et al. Esophageal candidiasis. Gastroenterol Jpn 1988;23:363-70.
18. Jacobs C, Coss Adame E, Attaluri A, Valestin J, Rao SSC. Dysmotility and proton pump inhibitor use are independent risk factors for small intestinal bacterial and/or fungal overgrowth. Aliment Pharmacol Ther 2013;37:1103-11.
19. Von Rosenvinge EC, Song Y, White JR, Maddox C, Blanchard T, Fricke WF. Immune status, antibiotic medication and pH are associated with changes in the stomach fluid microbiota. The ISME J 2013;7:1354-66.
20. Karczewska E, Wojtas I, Sito E, Trojanowska D, Budak A, Zwolinska-Wcislo M, et al. Assessment of co-existence of Helicobacter pylori and Candida fungi in diseases of the upper gastrointestinal tract. J Physiol Pharmacol 2009;60:33-9.
21. Husebye E, Skar V, Høverstad T, Iversen T, Melby K. Abnormal intestinal motor patterns explain enteric colonization with gram-negative bacilli in late radiation enteropathy. Gastroenterol 1995;109:1078-89.
22. Bühling A, Radun D, Müller W, Malfertheiner P. Influence of anti‐Helicobacter triple‐therapy with metronidazole, omeprazole and clarithromycin on intestinal microflora. Aliment Pharmacol Ther 2001;15:1445-52.
23. Karmeli Y, Stalnikowitz R, Eliakim R, Rahav G. Conventional dose of omeprazole alters gastric flora. Dig Dis Sci 1995;40:2070-3.
24. Gościmski A, Matras J, Wallner G. Microflora of gastric juice in patients after eradication of Helicobacter pylori and treatment with a proton pump inhibitor. Wiadomosci Lekarskie 2002;55:19-28.
25. Safe M, Chan WH, Leach ST, Sutton L, Lui K, Krishnan U. Widespread use of gastric acid inhibitors in infants: are they needed? Are they safe? World J Gastrointest Pharmacol Ther 2016; 7: 531–39.
26. De Bruyne P, Ito S. Toxicity of long-term use of proton pump inhibitors in children. Arch Dis Child 2018;103:78-82.
27. Motegi H, Abe S, Tansho S, Suzuki D, Yamaguchi H, Hoshino E. Suppressive effect of lansoprazole on anti-Candida activity of murine macrophages. Kansenshogaku Zasshi 2001;75:137-43.
28. Imhann F, Bonder MJ, Vila AV, Fu J, Mujagic Z, Vork L, et al. Proton pump inhibitors affect the gut microbiome. Gut 2016;65:740-8.
29. Wang K, Lin HJ, Perng CL, Tseng GY, Yu KW, Chang FY, et al. The effect of H2-receptor antagonist and proton pump inhibitor on microbial proliferation in the stomach. Hepato-gastroenterology 2004;51:1540-3.
30. Cohen S, Bueno de Mesquita M, Mimouni FB. Adverse effects reported in the use of gastroesophageal reflux disease treatments in children: a 10 years literature review. Br J Clin Pharmacol 2015;80:200-8.
31. Guillet R, Stoll BJ, Cotten CM, Gantz M, McDonald S, Poole WK, et al. Association of H2-blocker therapy and higher incidence of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2006;117:e137-e42.
32. Stoll BJ, Temprosa M, Tyson JE, Papile L-A, Wright LL, Bauer CR, et al. Dexamethasone therapy increases infection in very low birth weight infants. Pediatrics 1999;104(5):e63. DOI: https://doi.org/10.1542/peds.104.5.e63.
33. Saiman L, Ludington E, Pfaller M, Rangel-Frausto S, Wiblin TR, Dawson J, et al. Risk factors for candidemia in neonatal intensive care unit patients. Pediatr Infect Dis J 2000;19:319-24.
34. Ross AL, Slain D, Cumpston A, Bryant AM, Hamadani M, Craig M. Evaluation of an alternative posaconazole prophylaxis regimen in haematological malignancy patients receiving concomitant stress ulcer prophylaxis. Int J Antimicrob Agents 2012;40:557-61.
35. Sasaki K. Candida-associated gastric ulcer relapsing in a different position with a different appearance. World J Gastroenterol 2012;18:4450-53.
36. Soysa N, Samaranayake L, Ellepola A. Antimicrobials as a contributory factor in oral candidosis–a brief overview. Oral Dis 2008;14:138-43.
37. Gow NA, Brown AJ, Odds FC. Fungal morphogenesis and host invasion. Curr Opin Microbiol 2002;5:366-71.
38. Belazi M, Velegraki A, Fleva A, Gidarakou I, Papanaum L, Baka D, et al. Candidal overgrowth in diabetic patients: potential predisposing factors. Mycoses 2005;48:192-6.
39. Kumar B, Padshetty N, Bai K, Rao M. Prevalence of Candida in the oral cavity of diabetic subjects. J Assoc Phys India 2005;53:599-602.
40. Daniluk T, Tokajuk G, Stokowska W, Fiedoruk K, Sciepuk M, Zaremba M, et al. Occurrence rate of oral Candida albicans in denture wearer patients. Adv Med Sci 2006;51:77-80.
41. Kadir T, Pisiriciler R, Akyüz S, Yarat A, Emekli N, Ipbüker A. Mycological and cytological examination of oral candidal carriage in diabetic patients and non‐diabetic control subjects: thorough analysis of local aetiologic and systemic factors. J Oral Rehabil 2002;29:452-7.
42. Amiri HM, Frandah W, Colmer-Hamood J, Raj R, Nugent K. Risk factors of Candida colonization in the oropharynx of patients admitted to an intensive care unit. J Mycol Med 2012;22:301-7.
43. Delisle M-S, Williamson DR, Perreault MM, Albert M, Jiang X, Heyland DK. The clinical significance of Candida colonization of respiratory tract secretions in critically ill patients. J Crit Care 2008;23:11-7.
44. Garbino J, Lew DP, Romand J-A, Hugonnet S, Auckenthaler R, Pittet D. Prevention of severe Candida infections in nonneutropenic, high-risk, critically ill patients: a randomized, double-blind, placebo-controlled trial in patients treated by selective digestive decontamination. Intensive Care Med 2002;28:1708-17.
45. El-Ebiary M, Torres A, Fabregas N, de la Bellacasa JP, Gonzalez J, Ramirez J, et al. Significance of the isolation of Candida species from respiratory samples in critically ill, non-neutropenic patients: an immediate postmortem histologic study. Am J Respir Crit 1997;156:583-90.
46. Olaechea P, Palomar M, León-Gil Ct, Alvarez-Lerma F, Jorda R, Nolla-Salas J, et al. Economic impact of Candida colonization and Candida infection in the critically ill patient. Eur J Clin Microbiol 2004;23:323-30.
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