Year 2020 / Volume 112 / Number 5
Original
Factors associated with the presence of abnormal levels of fecal calprotectin in patients with negative panenteric studies

373-379

DOI: 10.17235/reed.2020.6508/2019

Juan Egea Valenzuela, Elena Iglesias Jorquera, Francisco Javier Álvarez-Higueras, María Muñoz Tornero, Ana Pereñíguez López, Esther Estrella Díez, Fernando Alberca de las Parras,

Abstract
Background: fecal calprotectin is a selection tool prior to endoscopic studies in patients with gastrointestinal symptoms. However, some symptomatic patients with altered fecal calprotectin will not have any endoscopic lesions. The aim of the study was to determine the factors associated with the presence of altered fecal calprotectin in patients with negative endoscopic studies of the colon and small bowel. Methods: this was an observational, prospective study of patients with digestive symptoms. The association of different clinical factors with elevated fecal calprotectin in the absence of endoscopic lesions of the colon and small bowel were analyzed. Results: 143 patients were included in the study, 98 were female (68.5 %) and the mean age was 40.06 ± 16.42 (15-82) years. Smoking and non-steroidal anti-inflammatory drug intake were associated with altered fecal calprotectin in patients with a negative endoscopy of the colon and small bowel (p = 0.029 and p = 0.006). The mean values of fecal calprotectin were significantly higher in smokers, users of non-steroidal anti-inflammatory drugs and patients with small intestine bacterial overgrowth. Smoking (OR: 3.505; p = 0.028), non-steroidal anti-inflammatory drugs intake (OR: 3.473; p = 0.021) and small intestine bacterial overgrowth (OR: 3.172; p = 0.013) were independent risk factors for altered fecal calprotectin in the absence of endoscopic lesions. No association was found for any of the other variables. Conclusions: smoking and the use of non-steroidal anti-inflammatory drugs are strongly associated with elevated levels of fecal calprotectin in symptomatic patients with a negative colonoscopy and capsule endoscopy of the small bowel. Small intestine bacterial overgrowth is also associated.
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References
1. D’Angelo F, Felley C, Frossard JL. Calprotectin in Daily Practice: Where Do We Stand in 2017? Digestion 2017; 95: 293-301.
2. Lozoya Angulo ME, de las Heras Gómez I, Martinez Villanueva M, et al. Faecal calprotectin, an useful marker in discriminating between inflammatory bowel disease and functional gastrointestinal disorders. Gastroenterol Hepatol 2017; 40: 125–31.
3. Reenaers C, Bossuyt P, Hindryckx P, et al. Expert opinion for use of faecal calprotectin in diagnosis and monitoring of inflammatory bowel disease in daily clinical practice. United Eur Gastroenterol J 2018; 6: 1117-25.
4. Brookes MJ, Whitehead S, Gaya DR, et al. Practical guidance on the use of faecal calprotectin. Frontline Gastroenterol 2018; 9: 87-91.
5. Aziz M, Melchior C, Zalar A, et al. Does calprotectin level identify a subgroup among patients suffering from irritable bowel syndrome? Results of a prospective study. United Eur Gastroenterol J 2016; 5: 261–9.
6. Koulaouzidis A, Douglas S, Rogers MA, et al. Fecal calprotectin: A selection tool for small bowel capsule endoscopy in suspected IBD with prior negative bi-directional endoscopy. Scand J Gastroenterol 2011; 46: 561–6.
7. Egea-Valenzuela J, Alberca-de-las-Parras F, Carballo-Álvarez F. Fecal calprotectin as a biomarker of inflammatory lesions of the small bowel seen by videocapsule endoscopy. Rev Esp Enferm Dig 2015; 107: 211-4.
8. Kopylov U, Yung D, Engel T, et al. Fecal calprotectin for the prediction of small-bowel Crohn’s disease by capsule endoscopy: a systematic review and meta-analysis. J Gastroenterol Hepatol 2016; 28: 1137-44.
9. Bar-Gil Shitrit A, Koslowsky B, Livovsky DM, et al. A prospective study of fecal calprotectin and lactoferrin as predictors of small bowel Crohn’s disease in patients undergoing capsule endoscopy. Scand J Gastroenterol 2017; 52: 328-33.
10. Monteiro S, Barbosa M, Cúrdia Gonçalves T, et al. Fecal Calprotectin as a Selection Tool for Small Bowel Capsule Endoscopy in Suspected Crohn’s Disease. Inflamm Bowel Dis 2018; 24: 2033–8.
11. K. Sunny J, Garcia CJ, McCallum RW. Interpreting the Lactulose Breath Test for the Diagnosis of Small Intestinal Bacterial Overgrowth. Am J Med Sci 2016; 351: 229–32.
12. Egea Valenzuela J, Antón Ródenas G, Sánchez Martínez A. Marcadores de actividad en la enfermedad inflamatoria intestinal. Med Clin (Barc) 2019; 152: 310-6.
13. Van Rheenen PF, Van de Vijver E, Fidler V. Faecal calprotectin for screening of patients with suspected inflammatory bowel disease: Diagnostic meta-analysis. BMJ 2010; 341: c3369.
14. Egea Valenzuela J, Pereñíguez López A, Pérez Fernández V, et al. Fecal calprotectin and C-reactive protein are associated with positive findings in capsule endoscopy in suspected small bowel Crohn’s disease. Rev Esp Enferm Dig 2016; 108: 394-400.
15. Lundgren D, Eklöf V, Palmqvist R, et al. Proton pump inhibitor use is associated with elevated faecal calprotectin levels. A cross-sectional study on subjects referred for colonoscopy. Scand J Gastroenterol 2019; 54: 152-7.
16. Berkowitz L, Schultz BM, Salazar GA, et al. Impact of cigarette smoking on the gastrointestinal tract inflammation: Opposing effects in Crohn’s disease and ulcerative colitis. Front Immunol 2018; 9: 74.
17. Li LF, Chan RL, Lu L, et al. Cigarette smoking and gastrointestinal diseases: The causal relationship and underlying molecular mechanisms (Review). Int J Mol Med 2014; 34: 372–80.
18. Allais L, Kerckhof F-M, Verschuere S, et al. Chronic cigarette smoke exposure induces microbial and inflammatory shifts and mucin changes in the murine gut. Environ Microbiol 2016; 18: 1352–63.
19. Hosseinzadeh A, Thompson PR, Segal BH, et al. Nicotine induces neutrophil extracellular traps. J Leukoc Biol 2016; 100: 1105–12.
20. Urban CF, Ermert D, Schmid M, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5: e1000639.
21. MacQueen BC, Christensen RD, Yost CC, et al. Elevated fecal calprotectin levels during necrotizing enterocolitis are associated with activated neutrophils extruding neutrophil extracellular traps. J Perinatol 2016; 36: 862–9.
22. Wéra O, Lancellotti P, Oury C. The Dual Role of Neutrophils in Inflammatory Bowel Diseases. J Clin Med 2016; 5: 118.
23. Xu N, Yu Z, Cao X, et al. Characteristics of Nonsteroidal Anti-Inflammatory Drugs (NSAIDs)-Induced Small Bowel Injury Identified by Single-Balloon Endoscopy or Capsule Endoscopy. Med Sci Monit 2017; 23: 5237–45.
24. Maiden L, Thjodleifsson B, Theodors A, et al. A Quantitative Analysis of NSAID-Induced Small Bowel Pathology by Capsule Enteroscopy. Gastroenterology 2005; 128: 1172–8.
25. Rendek Z, Falk M, Grodzinsky E, et al. Effect of oral diclofenac intake on faecal calprotectin. Scand J Gastroenterol 2016; 51: 28–32.
26. Tachecí I, Kopácová M, Rejchrt S, et al. Non-steroidal anti-inflammatory drug induced injury to the small intestine. Acta Medica (Hradec Kralove) 2010; 53: 3–11.
27. Poullis A, Foster R, Mendall MA, et al. Proton pump inhibitors are associated with elevation of faecal calprotectin and may affect specificity. Eur J Gastroenterol Hepatol 2003; 15: 573–4.
28. Guslandi M. Steroid ulcers: Any news? World J Gastrointest Pharmacol Ther 2013; 4: 39–40.
29. Becattini S, Taur Y, Pamer EG. Antibiotic-Induced Changes in the Intestinal Microbiota and Disease. Trends Mol Med 2016; 22: 458–78.
30. Fundarò C, Fantacci C, Ansuini V, et al. Fecal calprotectin concentration in children affected by SIBO. Eur Rev Med Pharmacol Sci 2011;15:1328–35.
31. Montalto M, Santoro L, Dalvai S, et al. Fecal Calprotectin Concentrations in Patients with Small Intestinal Bacterial Overgrowth. Dig Dis 2008; 26: 183–6.
32. David L, Babin A, Picos A, et al. Small Intestinal Bacterial Overgrowth is Associated with Intestinal Inflammation in the Irritable Bowel Syndrome. Clujul Med 2014; 87: 163–5.
33. Lee SH, Kim CR, Kim KN. Changes in Fecal Calprotectin After Rifaximin Treatment in Patients With Nonconstipated Irritable Bowel Syndrome. Am J Med Sci 2019; 357: 23-8.
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Egea Valenzuela J, Iglesias Jorquera E, Álvarez-Higueras F, Muñoz Tornero M, Pereñíguez López A, Estrella Díez E, et all. Factors associated with the presence of abnormal levels of fecal calprotectin in patients with negative panenteric studies. 6508/2019


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Publication history

Received: 16/07/2019

Accepted: 04/11/2019

Online First: 27/04/2020

Published: 08/05/2020

Article revision time: 94 days

Article Online First time: 286 days

Article editing time: 297 days


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