Распространенность синдрома избыточного бактериального роста в тонкой кишке у пациентов с функциональной диспепсией: метаанализ
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Kucheryavyy Yu.A., Andreev D.N., Maev I.V. Prevalence of small bowel bacterial overgrowth in patients with functional dyspepsia: a meta-analysis. Therapeutic Archive. 2020; 92 (12): 53–58.
DOI: 10.26442/00403660.2020.12.200433
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Материалы и методы. Поиск исследований проводился в электронных базах данных MEDLINE/PubMed, EMBASE, Cochrane, Google Scholar, Российский индекс научного цитирования (РИНЦ) до июля 2020 г. Дополнительно выполнялся поиск релевантных абстрактов по электронным базам данных конференций Объединенной европейской гастроэнтерологической недели (United European Gastroenterology Week – UEG), Американского колледжа гастроэнтерологов (American College of Gastroenterology – ACG), Международной конференции по вопросам питания и пищевых продуктов (International Conference on Nutrition and Food – ICNF). В финальный анализ отбирались публикации, в которых применялись валидированные тесты оценки СИБР (дыхательный водородный тест с применением глюкозы или лактулозы) с подробной описательной статистикой, позволяющей включить результирующие данные в метаанализ.
Результаты. В итоговый анализ включено 7 исследований с участием 1248 пациентов с ФД. Обобщенная частота СИБР у пациентов с ФД составила 34,73% (95% доверительный интервал 24,807–45,383). Выявлена значительная гетерогенность между результатами (p<0,0001; I2=89,91%). При исключении из метаанализа исследования, в котором частота СИБР изучалась у пациентов с рефрактерной ФД, обобщенная распространенность составила 38,98% (95% доверительный интервал 28,964–49,490).
Заключение. Настоящий метаанализ продемонстрировал, что СИБР достаточно часто ассоциирован с ФД и наблюдается примерно у каждого третьего пациента с данным функциональным заболеванием желудочно-кишечного тракта.
Ключевые слова: диспепсия, функциональная диспепсия, синдром избыточного бактериального роста.
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Aim. Systematization of data on the frequency of detection of the syndrome of bacterial overgrowth in the small intestine (SIBO) in patients with functional dyspepsia (FD).
Materials and methods. MEDLINE/PubMed, EMBASE, Cochrane, Google Scholar, the Russian Science Citation Index (RSCI) through July 2020 were searched to identify studies evaluating the prevalence of SIBO in FD. In addition, a search for relevant abstracts was carried out in the electronic databases of the United European Gastroenterology Week (UEG), American College of Gastroenterology (ACG), International Conference on Nutrition and Food (ICNF). For the final analysis, publications were selected that used validated tests for the assessment of SIBO (hydrogen breath test using glucose or lactulose) with detailed descriptive statistics, allowing the resulting data to be included in the meta-analysis.
Results. The final analysis included 7 studies with 1248 patients with FD. Overall pooled prevalence of SIBO in patients with FD was 34.73% (95% CI 24.807–45.383). There was significant heterogeneity between the results (p<0.0001; I2=89.91%). When excluded from the meta-analysis of a study in which the incidence of SIBO was studied in patients with refractory FD, the pooled prevalence was 38.98% (95% CI 28.964–49.490).
Conclusion. This meta-analysis has demonstrated that SIBO is often associated with FD and is observed in about every third patient with this functional gastrointestinal tract disease.
Keywords: dyspepsia, functional dyspepsia, bacterial overgrowth syndrome.
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4. Кучерявый Ю.А., Андреев Д.Н. Клинические и патогенетические параллели функциональной диспепсии и синдрома избыточного бактериального роста в тонкой кишке. Эффективная фармакотерапия. 2020;16(24):40-4 [Kucheryavyy YuA, Andreev DN. Clinical and pathogenetic parallels of functional dyspepsia and the syndrome of excessive bacterial growth in the small intestine. Effective pharmacotherapy. 2020;16(24):40-4 (In Russ.)]. doi: 10.33978/2307-3586-2020-16-24-40-44
5. Tziatzios G, Giamarellos-Bourboulis EJ, Papanikolaou IS, et al. Is small intestinal bacterial overgrowth involved in the pathogenesis of functional dyspepsia? Med Hypotheses. 2017;106:26-32. doi: 10.1016/j.mehy.2017.07.005
6. Shah A, Morrison M, Burger D, et al. Systematic review with meta-analysis: the prevalence of small intestinal bacterial overgrowth in inflammatory bowel disease. Aliment Pharmacol Ther. 2019;49(6):624-35. doi: 10.1111/apt.15133
7. Losurdo G, Marra A, Shahini E, et al. Small intestinal bacterial overgrowth and celiac disease: A systematic review with pooled-data analysis. Neurogastroenterol Motil. 2017;29(6). doi: 10.1111/nmo.13028
8. Capurso G, Signoretti M, Archibugi L, et al. Systematic review and meta-analysis: Small intestinal bacterial overgrowth in chronic pancreatitis. United European Gastroenterol J. 2016;4(5):697-705. doi: 10.1177/2050640616630117
9. Wijarnpreecha K, Lou S, Watthanasuntorn K, et al. Small intestinal bacterial overgrowth and nonalcoholic fatty liver disease: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2020;32(5):601-8. doi: 10.1097/MEG.0000000000001541
10. Maslennikov R, Pavlov C, Ivashkin V. Small intestinal bacterial overgrowth in cirrhosis: systematic review and meta-analysis. Hepatol Int. 2018;12(6):567-76. doi: 10.1007/s12072-018-9898-2
11. Shah A, Talley NJ, Jones M, et al. Small Intestinal Bacterial Overgrowth in Irritable Bowel Syndrome: A Systematic Review and Meta-Analysis of Case-Control Studies. Am J Gastroenterol. 2020;115(2):190-201. doi: 10.14309/ajg.0000000000000504
12. Chen B, Kim JJ, Zhang Y, et al. Prevalence and predictors of small intestinal bacterial overgrowth in irritable bowel syndrome: a systematic review and meta-analysis. J Gastroenterol. 2018;53(7):807-18. doi: 10.1007/s00535-018-1476-9
13. de Bortoli N, Tolone S, Frazzoni M, et al. Gastroesophageal reflux disease, functional dyspepsia and irritable bowel syndrome: common overlapping gastrointestinal disorders. Ann Gastroenterol. 2018;31(6):639-48. doi: 10.20524/aog.2018.0314
14. Mahadeva S, Goh KL. Epidemiology of functional dyspepsia: a global perspective. World J Gastroenterol. 2006;12(17):2661-6. doi: 10.3748/wjg.v12.i17.2661
15. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol. 2014;6:71-80. doi: 10.2147/CLEP.S40245
16. Ford AC, Marwaha A, Lim A, Moayyedi P. Systematic review and meta-analysis of the prevalence of irritable bowel syndrome in individuals with dyspepsia. Clin Gastroenterol Hepatol. 2010;8:401-9. doi: 10.1016/j.cgh.2009.07.020
17. von Wulffen M, Talley NJ, Hammer J, et al. Overlap of Irritable Bowel Syndrome and Functional Dyspepsia in the Clinical Setting: Prevalence and Risk Factors. Dig Dis Sci. 2019;64(2):480-6. doi: 10.1007/s10620-018-5343-6
18. Costa MB, Azeredo IL Jr, Marciano RD, et al. Evaluation of small intestine bacterial overgrowth in patients with functional dyspepsia through H2 breath test. Arq Gastroenterol. 2012;49(4):279-83. doi: 10.1590/s0004-28032012000400009
19. Shimura S, Ishimura N, Mikami H, et al. Small Intestinal Bacterial Overgrowth in Patients with Refractory Functional Gastrointestinal Disorders. J Neurogastroenterol Motil. 2016;22(1):60-8. doi: 10.5056/jnm15116
20. Ramanathan S, Karunakaran P, Shaikh Mohamed K, et al. A study on the role of small intestinal bacterial overgrowth in patients with functional dyspepsia. IAIM. 2017;4(5):88-97.
21. Petzold G, Amanzada A, Gress TM, et al. High Prevalence of Pathological Hydrogen Breath Tests in Patients with Functional Dyspepsia. Digestion. 2019;100(3):186-91. doi: 10.1159/000494718
22. Nojkov B, Baker J, Watts L, et al. Small Intestinal Bacterial Overgrowth (SIBO) in Functional Dyspepsia (FD): Does Dyspeptic Symptom Pattern Make a Difference? Am J Gastroenterol. 2019;114:S293-S294. doi: 10.14309/01.ajg.0000591544.75510.8d
23. Adriana B, Antonio B, Matthew D, et al. Gastric Fermentation in Functional Dyspepsia. Gastroenterol Hepatol Intl J. 2019;4(1). doi: 10.23880/ghij-16000145
24. Chojnacki CJ, Konrad P, Błońska A, et al. Usefulness of the hydrogen breath test in patients with functional dyspepsia. Gastroenterol Rev. 2020;15. doi: 10.5114/pg.2020.92690
25. Stanghellini V, Chan FK, Hasler WL, et al. Gastroduodenal Disorders. Gastroenterology. 2016; 150(6):1380-92. doi: 10.1053/j.gastro.
2016.02.011
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27. Mahadeva S, Ford AC. Clinical and epidemiological differences in functional dyspepsia between the East and the West. Neurogastroenterol Motil. 2016;28(2):167-74. doi: 10.1111/nmo.12657
28. Losurdo G, Leandro G, Ierardi E, et al. Breath Tests for the Non-invasive Diagnosis of Small Intestinal Bacterial Overgrowth: A Systematic Review With Meta-analysis. J Neurogastroenterol Motil. 2020;26(1):16-28. doi: 10.5056/jnm19113
29. Su T, Lai S, Lee A, et al. Meta-analysis: proton pump inhibitors moderately increase the risk of small intestinal bacterial overgrowth. J Gastroenterol. 2018;53(1):27-36. doi: 10.1007/s00535-017-1371-9
30. Salem AE, Singh R, Ayoub YK, et al. The gut microbiome and irritable bowel syndrome: State of art review. Arab J Gastroenterol. 2018;19(3):136-41. doi: 10.1016/j.ajg.2018.02.008
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32. Андреев Д.Н., Дичева Д.Т. Нарушение проницаемости слизистой оболочки кишечника как фактор этиопатогенеза функциональных заболеваний желудочно-кишечного тракта. Мед. cовет. 2020;5:87-95 [Andreev DN, Dicheva DT. A breach in the intestinal permeability as a factor of etiopathogenesis of functional gastrointestinal diseases. Meditsinskiy sovet = Medical Council. 2020;5:87-95 (In Russ.)]. doi: 10.21518/2079-701X-2020-5-87-95]
33. Farré R, Vicario M. Abnormal Barrier Function in Gastrointestinal Disorders. Handb Exp Pharmacol. 2017;239:193-217. doi: 10.1007/164_2016_107
34. Camilleri M, Oduyebo I, Halawi H. Chemical and molecular factors in irritable bowel syndrome: current knowledge, challenges, and unanswered questions. Am J Physiol Gastrointest Liver Physiol. 2016;311(5):G777-G784. doi: 10.1152/ajpgi.00242.2016
35. Ng QX, Soh AYS, Loke W, et al. The role of inflammation in irritable bowel syndrome (IBS). J Inflamm Res. 2018;11:345-9. doi: 10.2147/JIR.S174982
36. Du L, Chen B, Kim JJ, et al. Micro-inflammation in functional dyspepsia: A systematic review and meta-analysis. Neurogastroenterol Motil. 2018;30(4):e13304. doi: 10.1111/nmo.13304
37. Miwa H, Oshima T, Tomita T, et al. Recent understanding of the pathophysiology of functional dyspepsia: role of the duodenum as the pathogenic center. J Gastroenterol. 2019;54(4):305-11. doi: 10.1007/s00535-019-01550-4
38. Pinto-Sanchez MI, Yuan Y, Hassan A, et al. Proton pump inhibitors for functional dyspepsia. Cochrane Database Syst Rev. 2017;11(11):CD011194. doi: 10.1002/14651858.CD011194.pub3
39. Pittayanon R, Yuan Y, Bollegala NP, et al. Prokinetics for Functional Dyspepsia: A Systematic Review and Meta-Analysis of Randomized Control Trials. Am J Gastroenterol. 2019;114(2):233-43. doi: 10.1038/s41395-018-0258-6
40. Calanni F, Renzulli C, Barbanti M, Viscomi GC. Rifaximin: beyond the traditional antibiotic activity. J Antibiot (Tokyo). 2014;67(9):667-70. doi: 10.1038/ja.2014.106
41. Gatta L, Scarpignato C. Systematic review with meta-analysis: rifaximin is effective and safe for the treatment of small intestine bacterial overgrowth. Aliment Pharmacol Ther. 2017;45(5):604-16. doi: 10.1111/apt.1392
42. Tan VP, Liu KS, Lam FY, et al. Randomised clinical trial: rifaximin versus placebo for the treatment of functional dyspepsia. Aliment Pharmacol Ther. 2017;45(6):767-76. doi: 10.1111/apt.13945
________________________________________________
1. Pimentel M, Saad RJ, Long MD, Rao SSC. ACG Clinical Guideline: Small Intestinal Bacterial Overgrowth. Am J Gastroenterol. 2020;115(2):165-78. doi: 10.14309/ajg.0000000000000501
2. [Maev IV, Kucheryavyy YuA, Andreev DN, Ivashkina NYu. Syndrome of bacterial overgrowth in the small intestine: clinical significance, diagnostic criteria and therapeutic tactics. Infectious Diseases: News. Opinions. Training. 2016;3:118-25 (In Russ.)].
3. Losurdo G, Salvatore D'Abramo F, et al. The Influence of Small Intestinal Bacterial Overgrowth in Digestive and Extra-Intestinal Disorders. Int J Mol Sci. 2020;21(10):3531. doi: 10.3390/ijms21103531
4. [Kucheryavyy YuA, Andreev DN. Clinical and pathogenetic parallels of functional dyspepsia and the syndrome of excessive bacterial growth in the small intestine. Effective pharmacotherapy. 2020;16(24):40-4 (In Russ.)]. doi: 10.33978/2307-3586-2020-16-24-40-44
5. Tziatzios G, Giamarellos-Bourboulis EJ, Papanikolaou IS, et al. Is small intestinal bacterial overgrowth involved in the pathogenesis of functional dyspepsia? Med Hypotheses. 2017;106:26-32. doi: 10.1016/j.mehy.2017.07.005
6. Shah A, Morrison M, Burger D, et al. Systematic review with meta-analysis: the prevalence of small intestinal bacterial overgrowth in inflammatory bowel disease. Aliment Pharmacol Ther. 2019;49(6):624-35. doi: 10.1111/apt.15133
7. Losurdo G, Marra A, Shahini E, et al. Small intestinal bacterial overgrowth and celiac disease: A systematic review with pooled-data analysis. Neurogastroenterol Motil. 2017;29(6). doi: 10.1111/nmo.13028
8. Capurso G, Signoretti M, Archibugi L, et al. Systematic review and meta-analysis: Small intestinal bacterial overgrowth in chronic pancreatitis. United European Gastroenterol J. 2016;4(5):697-705. doi: 10.1177/2050640616630117
9. Wijarnpreecha K, Lou S, Watthanasuntorn K, et al. Small intestinal bacterial overgrowth and nonalcoholic fatty liver disease: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2020;32(5):601-8. doi: 10.1097/MEG.0000000000001541
10. Maslennikov R, Pavlov C, Ivashkin V. Small intestinal bacterial overgrowth in cirrhosis: systematic review and meta-analysis. Hepatol Int. 2018;12(6):567-76. doi: 10.1007/s12072-018-9898-2
11. Shah A, Talley NJ, Jones M, et al. Small Intestinal Bacterial Overgrowth in Irritable Bowel Syndrome: A Systematic Review and Meta-Analysis of Case-Control Studies. Am J Gastroenterol. 2020;115(2):190-201. doi: 10.14309/ajg.0000000000000504
12. Chen B, Kim JJ, Zhang Y, et al. Prevalence and predictors of small intestinal bacterial overgrowth in irritable bowel syndrome: a systematic review and meta-analysis. J Gastroenterol. 2018;53(7):807-18. doi: 10.1007/s00535-018-1476-9
13. de Bortoli N, Tolone S, Frazzoni M, et al. Gastroesophageal reflux disease, functional dyspepsia and irritable bowel syndrome: common overlapping gastrointestinal disorders. Ann Gastroenterol. 2018;31(6):639-48. doi: 10.20524/aog.2018.0314
14. Mahadeva S, Goh KL. Epidemiology of functional dyspepsia: a global perspective. World J Gastroenterol. 2006;12(17):2661-6. doi: 10.3748/wjg.v12.i17.2661
15. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol. 2014;6:71-80. doi: 10.2147/CLEP.S40245
16. Ford AC, Marwaha A, Lim A, Moayyedi P. Systematic review and meta-analysis of the prevalence of irritable bowel syndrome in individuals with dyspepsia. Clin Gastroenterol Hepatol. 2010;8:401-9. doi: 10.1016/j.cgh.2009.07.020
17. von Wulffen M, Talley NJ, Hammer J, et al. Overlap of Irritable Bowel Syndrome and Functional Dyspepsia in the Clinical Setting: Prevalence and Risk Factors. Dig Dis Sci. 2019;64(2):480-6. doi: 10.1007/s10620-018-5343-6
18. Costa MB, Azeredo IL Jr, Marciano RD, et al. Evaluation of small intestine bacterial overgrowth in patients with functional dyspepsia through H2 breath test. Arq Gastroenterol. 2012;49(4):279-83. doi: 10.1590/s0004-28032012000400009
19. Shimura S, Ishimura N, Mikami H, et al. Small Intestinal Bacterial Overgrowth in Patients with Refractory Functional Gastrointestinal Disorders. J Neurogastroenterol Motil. 2016;22(1):60-8. doi: 10.5056/jnm15116
20. Ramanathan S, Karunakaran P, Shaikh Mohamed K, et al. A study on the role of small intestinal bacterial overgrowth in patients with functional dyspepsia. IAIM. 2017;4(5):88-97.
21. Petzold G, Amanzada A, Gress TM, et al. High Prevalence of Pathological Hydrogen Breath Tests in Patients with Functional Dyspepsia. Digestion. 2019;100(3):186-91. doi: 10.1159/000494718
22. Nojkov B, Baker J, Watts L, et al. Small Intestinal Bacterial Overgrowth (SIBO) in Functional Dyspepsia (FD): Does Dyspeptic Symptom Pattern Make a Difference? Am J Gastroenterol. 2019;114:S293-S294. doi: 10.14309/01.ajg.0000591544.75510.8d
23. Adriana B, Antonio B, Matthew D, et al. Gastric Fermentation in Functional Dyspepsia. Gastroenterol Hepatol Intl J. 2019;4(1). doi: 10.23880/ghij-16000145
24. Chojnacki CJ, Konrad P, Błońska A, et al. Usefulness of the hydrogen breath test in patients with functional dyspepsia. Gastroenterol Rev. 2020;15. doi: 10.5114/pg.2020.92690
25. Stanghellini V, Chan FK, Hasler WL, et al. Gastroduodenal Disorders. Gastroenterology. 2016; 150(6):1380-92. doi: 10.1053/j.gastro.
2016.02.011
26. [Andreyev DN, Zaborovsky AV, Trukhmanov AS,
et al. Evaluation of the functional gastrointestinal diseases concept from standpoints of Rome IV (2016) diagnostic criteria (review). Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2017;27(1):4-11 (In Russ.)]. doi: 10.22416/1382-4376-2017-27-1-4-11
27. Mahadeva S, Ford AC. Clinical and epidemiological differences in functional dyspepsia between the East and the West. Neurogastroenterol Motil. 2016;28(2):167-74. doi: 10.1111/nmo.12657
28. Losurdo G, Leandro G, Ierardi E, et al. Breath Tests for the Non-invasive Diagnosis of Small Intestinal Bacterial Overgrowth: A Systematic Review With Meta-analysis. J Neurogastroenterol Motil. 2020;26(1):16-28. doi: 10.5056/jnm19113
29. Su T, Lai S, Lee A, et al. Meta-analysis: proton pump inhibitors moderately increase the risk of small intestinal bacterial overgrowth. J Gastroenterol. 2018;53(1):27-36. doi: 10.1007/s00535-017-1371-9
30. Salem AE, Singh R, Ayoub YK, et al. The gut microbiome and irritable bowel syndrome: State of art review. Arab J Gastroenterol. 2018;19(3):136-41. doi: 10.1016/j.ajg.2018.02.008
31. [Andreev DN. The role of alterations in permeability of the intestinal mucosa in the genesis of functional gastrointestinal disorders. Consilium Medicum. 2019;21(8):29-34 (In Russ.)]. doi: 10.26442/20751753.2019.8.190539
32. [Andreev DN, Dicheva DT. A breach in the intestinal permeability as a factor of etiopathogenesis of functional gastrointestinal diseases. Meditsinskiy sovet = Medical Council. 2020;5:87-95 (In Russ.)]. doi: 10.21518/2079-701X-2020-5-87-95]
33. Farré R, Vicario M. Abnormal Barrier Function in Gastrointestinal Disorders. Handb Exp Pharmacol. 2017;239:193-217. doi: 10.1007/164_2016_107
34. Camilleri M, Oduyebo I, Halawi H. Chemical and molecular factors in irritable bowel syndrome: current knowledge, challenges, and unanswered questions. Am J Physiol Gastrointest Liver Physiol. 2016;311(5):G777-G784. doi: 10.1152/ajpgi.00242.2016
35. Ng QX, Soh AYS, Loke W, et al. The role of inflammation in irritable bowel syndrome (IBS). J Inflamm Res. 2018;11:345-9. doi: 10.2147/JIR.S174982
36. Du L, Chen B, Kim JJ, et al. Micro-inflammation in functional dyspepsia: A systematic review and meta-analysis. Neurogastroenterol Motil. 2018;30(4):e13304. doi: 10.1111/nmo.13304
37. Miwa H, Oshima T, Tomita T, et al. Recent understanding of the pathophysiology of functional dyspepsia: role of the duodenum as the pathogenic center. J Gastroenterol. 2019;54(4):305-11. doi: 10.1007/s00535-019-01550-4
38. Pinto-Sanchez MI, Yuan Y, Hassan A, et al. Proton pump inhibitors for functional dyspepsia. Cochrane Database Syst Rev. 2017;11(11):CD011194. doi: 10.1002/14651858.CD011194.pub3
39. Pittayanon R, Yuan Y, Bollegala NP, et al. Prokinetics for Functional Dyspepsia: A Systematic Review and Meta-Analysis of Randomized Control Trials. Am J Gastroenterol. 2019;114(2):233-43. doi: 10.1038/s41395-018-0258-6
40. Calanni F, Renzulli C, Barbanti M, Viscomi GC. Rifaximin: beyond the traditional antibiotic activity. J Antibiot (Tokyo). 2014;67(9):667-70. doi: 10.1038/ja.2014.106
41. Gatta L, Scarpignato C. Systematic review with meta-analysis: rifaximin is effective and safe for the treatment of small intestine bacterial overgrowth. Aliment Pharmacol Ther. 2017;45(5):604-16. doi: 10.1111/apt.1392
42. Tan VP, Liu KS, Lam FY, et al. Randomised clinical trial: rifaximin versus placebo for the treatment of functional dyspepsia. Aliment Pharmacol Ther. 2017;45(6):767-76. doi: 10.1111/apt.13945
ФГБОУ ВО «Московский государственный медико-стоматологический университет им. А.И. Евдокимова» Минздрава России,
Москва, Россия
________________________________________________
Yu.A. Kucheryavyy, D.N. Andreev, I.V. Maev
Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia