Skip to main content
Erschienen in: World Journal of Pediatrics 5/2018

16.03.2018 | Original Article

Elevated serum neopterin levels in children with functional constipation: association with systemic proinflammatory cytokines

verfasst von: Ceren Cıralı, Emel Ulusoy, Tuncay Kume, Nur Arslan

Erschienen in: World Journal of Pediatrics | Ausgabe 5/2018

Einloggen, um Zugang zu erhalten

Abstract

Background

Functional constipation is a clinical problem with an incompletely understood etiology. Functional bowel diseases have been shown to be related to inflammation in many studies in adults. In this study, we aimed to evaluate leukocytes, C-reactive protein, proinflammatory and anti-inflammatory cytokines, and neopterin levels in children with functional constipation.

Methods

Seventy-six children with constipation and 71 healthy controls (mean age 7.12 ± 3.46 years and 7.32 ± 4.33 years, respectively, P = 0.991) were included in the study. Leukocytes, C-reactive protein, interleukin (IL)-1β, IL-6, IL-10, IL-12, tumor necrosis factor-alpha (TNF-α) and neopterin levels were assessed in patients and healthy controls. Parameters were measured in the serum using enzyme-linked immunosorbent assay methods.

Results

Mean IL-6 (20.31 ± 12.05 vs. 16.2 ± 10.25 pg/mL, respectively, P = 0.003), IL-12 (181.42 ± 133.45 vs. 135.6 ± 83.67 pg/mL, respectively, P = 0.018) and neopterin levels (2.08 ± 1.12 vs. 1.52 ± 1.02 pg/mL, respectively, P = 0.001) were significantly higher in constipated children than healthy controls. Leukocyte and thrombocyte counts, C-reactive protein, and IL-1β, IL-10 and TNF-α levels did not show any difference between the two groups.

Conclusions

In this study, IL-6, IL-12 and neopterin levels of constipated patients were found to be higher than those of controls. These results indicate the presence of subclinical inflammation in children with functional constipation.
Literatur
1.
Zurück zum Zitat Hua MC, Lai MW, Kuo ML, Yao TC, Huang JL, Chen SM. Decreased interleukin-10 secretion by peripheral blood mononuclear cells in children with irritable bowel syndrome. J Pediatr Gastroenterol Nutr. 2011;52:376–81.CrossRefPubMed Hua MC, Lai MW, Kuo ML, Yao TC, Huang JL, Chen SM. Decreased interleukin-10 secretion by peripheral blood mononuclear cells in children with irritable bowel syndrome. J Pediatr Gastroenterol Nutr. 2011;52:376–81.CrossRefPubMed
2.
Zurück zum Zitat Sheikh Sajjadieh MR, Kuznetsova L, Bojenko V. Cytokine status in Ukrainian children with irritable bowel syndrome residing in a radioactive contaminated area. Iran J Immunol. 2012;9:248–53.PubMed Sheikh Sajjadieh MR, Kuznetsova L, Bojenko V. Cytokine status in Ukrainian children with irritable bowel syndrome residing in a radioactive contaminated area. Iran J Immunol. 2012;9:248–53.PubMed
3.
Zurück zum Zitat Vázquez-Frias R, Gutiérrez-Reyes G, Urbán-Reyes M, Velázquez-Guadarrama N, Fortoul-van der Goes TI, Reyes-López A, et al. Proinflammatory and anti-inflammatory cytokine profile in pediatric patients with irritable bowel syndrome. Rev Gastroenterol Mex. 2015;80:6–12 (in English, Spanish).PubMed Vázquez-Frias R, Gutiérrez-Reyes G, Urbán-Reyes M, Velázquez-Guadarrama N, Fortoul-van der Goes TI, Reyes-López A, et al. Proinflammatory and anti-inflammatory cytokine profile in pediatric patients with irritable bowel syndrome. Rev Gastroenterol Mex. 2015;80:6–12 (in English, Spanish).PubMed
4.
Zurück zum Zitat Caini S, Bagnoli S, Palli D, Saieva C, Ceroti M, Bendinelli B, et al. Total and cancer mortality in a cohort of ulcerative colitis and Crohn’s disease patients: the Florence inflammatory bowel disease study, 1978-2010. Dig Liver Dis. 2016;48:1162–7.CrossRefPubMed Caini S, Bagnoli S, Palli D, Saieva C, Ceroti M, Bendinelli B, et al. Total and cancer mortality in a cohort of ulcerative colitis and Crohn’s disease patients: the Florence inflammatory bowel disease study, 1978-2010. Dig Liver Dis. 2016;48:1162–7.CrossRefPubMed
5.
Zurück zum Zitat van den Heuvel TR, Wintjens DS, Jeuring SF, Wassink MH, Romberg-Camps MJ, Oostenbrug LE, et al. Inflammatory bowel disease, cancer and medication: cancer risk in the Dutch population-based IBDSL cohort. Int J Cancer. 2016;139:1270–80.CrossRefPubMed van den Heuvel TR, Wintjens DS, Jeuring SF, Wassink MH, Romberg-Camps MJ, Oostenbrug LE, et al. Inflammatory bowel disease, cancer and medication: cancer risk in the Dutch population-based IBDSL cohort. Int J Cancer. 2016;139:1270–80.CrossRefPubMed
6.
Zurück zum Zitat Sinha R, Doval DC, Hussain S, Kumar K, Singh S, Basir SF, et al. Lifestyle and sporadic colorectal cancer in India. Asian Pac J Cancer Prev. 2015;16:7683–8.CrossRefPubMed Sinha R, Doval DC, Hussain S, Kumar K, Singh S, Basir SF, et al. Lifestyle and sporadic colorectal cancer in India. Asian Pac J Cancer Prev. 2015;16:7683–8.CrossRefPubMed
7.
Zurück zum Zitat Hu LY, Ku FC, Lu T, Shen CC, Hu YW, Yeh CM, et al. Risk of cancer in patients with irritable bowel syndrome: a nationwide population-based study. Ann Epidemiol. 2015;25:924–8.CrossRefPubMed Hu LY, Ku FC, Lu T, Shen CC, Hu YW, Yeh CM, et al. Risk of cancer in patients with irritable bowel syndrome: a nationwide population-based study. Ann Epidemiol. 2015;25:924–8.CrossRefPubMed
8.
Zurück zum Zitat Guérin A, Mody R, Fok B, Lasch KL, Zhou Z, Wu EQ, et al. Risk of developing colorectal cancer and benign colorectal neoplasm in patients with chronic constipation. Aliment Pharmacol Ther. 2014;40:83–92.CrossRefPubMed Guérin A, Mody R, Fok B, Lasch KL, Zhou Z, Wu EQ, et al. Risk of developing colorectal cancer and benign colorectal neoplasm in patients with chronic constipation. Aliment Pharmacol Ther. 2014;40:83–92.CrossRefPubMed
9.
Zurück zum Zitat Berdowska A, Zwirska-Korczala K. Neopterin measurement in clinical diagnosis. J Clin Pharm Ther. 2001;26:319–29.CrossRefPubMed Berdowska A, Zwirska-Korczala K. Neopterin measurement in clinical diagnosis. J Clin Pharm Ther. 2001;26:319–29.CrossRefPubMed
10.
Zurück zum Zitat Skogmar S, Schön T, Balcha TT, Sturegård E, Jansson M, Björkman P. Plasma levels of neopterin and C-reactive protein (CRP) in tuberculosis (TB) with and without HIV coinfection in relation to CD4 cell count. PLoS One. 2015;10:e0144292.CrossRefPubMedCentralPubMed Skogmar S, Schön T, Balcha TT, Sturegård E, Jansson M, Björkman P. Plasma levels of neopterin and C-reactive protein (CRP) in tuberculosis (TB) with and without HIV coinfection in relation to CD4 cell count. PLoS One. 2015;10:e0144292.CrossRefPubMedCentralPubMed
11.
Zurück zum Zitat Oweira H, Lahdou I, Daniel V, Hofer S, Mieth M, Schmidt J, et al. Early post-transplant neopterin associated with one year survival and bacteremia in liver transplant recipients. Hum Immunol. 2016;77:115–20.CrossRefPubMed Oweira H, Lahdou I, Daniel V, Hofer S, Mieth M, Schmidt J, et al. Early post-transplant neopterin associated with one year survival and bacteremia in liver transplant recipients. Hum Immunol. 2016;77:115–20.CrossRefPubMed
12.
Zurück zum Zitat Arslan N, Tokgoz Y, Kume T, Bulbul M, Sayın O, Harmancı D, et al. Evaluation of serum neopterin levels and its relationship with adipokines in pediatric obesity-related nonalcoholic fatty liver disease and healthy adolescents. J Pediatr Endocrinol Metab. 2013;26:1141–7.CrossRefPubMed Arslan N, Tokgoz Y, Kume T, Bulbul M, Sayın O, Harmancı D, et al. Evaluation of serum neopterin levels and its relationship with adipokines in pediatric obesity-related nonalcoholic fatty liver disease and healthy adolescents. J Pediatr Endocrinol Metab. 2013;26:1141–7.CrossRefPubMed
13.
Zurück zum Zitat van Dijk RA, Rijs K, Wezel A, Hamming JF, Kolodgie FD, Virmani R, et al. Systematic evaluation of the cellular innate immune response during the process of human atherosclerosis. J Am Heart Assoc. 2016;5:e002860.PubMedPubMedCentral van Dijk RA, Rijs K, Wezel A, Hamming JF, Kolodgie FD, Virmani R, et al. Systematic evaluation of the cellular innate immune response during the process of human atherosclerosis. J Am Heart Assoc. 2016;5:e002860.PubMedPubMedCentral
14.
Zurück zum Zitat Palabiyik SS, Keles S, Girgin G, Arpali-Tanas E, Topdagi E, Baydar T. Neopterin release and tryptophan degradation in patients with uveitis. Curr Eye Res. 2016;41:1513–7.CrossRefPubMed Palabiyik SS, Keles S, Girgin G, Arpali-Tanas E, Topdagi E, Baydar T. Neopterin release and tryptophan degradation in patients with uveitis. Curr Eye Res. 2016;41:1513–7.CrossRefPubMed
15.
Zurück zum Zitat Volgger BM, Windbichler GH, Zeimet AG, Graf AH, Bogner G, Angleitner-Boubenizek L, et al. Long-term significance of urinary neopterin in ovarian cancer: a study by the Austrian Association for Gynecologic Oncology (AGO). Ann Oncol. 2016;27:1740–6.CrossRefPubMed Volgger BM, Windbichler GH, Zeimet AG, Graf AH, Bogner G, Angleitner-Boubenizek L, et al. Long-term significance of urinary neopterin in ovarian cancer: a study by the Austrian Association for Gynecologic Oncology (AGO). Ann Oncol. 2016;27:1740–6.CrossRefPubMed
16.
Zurück zum Zitat Beksac K, Sonmez C, Cetin B, Kısmalı G, Sel T, Tuncer Y, et al. Evaluation of proinflammatory cytokine and neopterin levels in women with papillary thyroid carcinoma. Int J Biol Markers. 2016;31:e446–50. CrossRefPubMed Beksac K, Sonmez C, Cetin B, Kısmalı G, Sel T, Tuncer Y, et al. Evaluation of proinflammatory cytokine and neopterin levels in women with papillary thyroid carcinoma. Int J Biol Markers. 2016;31:e446–50. CrossRefPubMed
17.
Zurück zum Zitat Zezulová M, Bartoušková M, Hlídková E, Juráňová J, Červinková B, Kasalová E, et al. Prognostic significance of serum and urinary neopterin concentrations in patients with rectal carcinoma treated with chemoradiation. Anticancer Res. 2016;36:287–92.PubMed Zezulová M, Bartoušková M, Hlídková E, Juráňová J, Červinková B, Kasalová E, et al. Prognostic significance of serum and urinary neopterin concentrations in patients with rectal carcinoma treated with chemoradiation. Anticancer Res. 2016;36:287–92.PubMed
18.
Zurück zum Zitat Guerrant RL, Leite AM, Pinkerton R, Medeiros PH, Cavalcante PA, DeBoer M, et al. Biomarkers of environmental enteropathy, inflammation, stunting, and impaired growth in children in Northeast Brazil. PLoS One. 2016;11:e0158772.CrossRefPubMedCentralPubMed Guerrant RL, Leite AM, Pinkerton R, Medeiros PH, Cavalcante PA, DeBoer M, et al. Biomarkers of environmental enteropathy, inflammation, stunting, and impaired growth in children in Northeast Brazil. PLoS One. 2016;11:e0158772.CrossRefPubMedCentralPubMed
19.
Zurück zum Zitat Campbell DI, McPhail G, Lunn PG, Elia M, Jeffries DJ. Intestinal inflammation measured by fecal neopterin in Gambian children with enteropathy: association with growth failure, Giardia lamblia, and intestinal permeability. J Pediatr Gastroenterol Nutr. 2004;39:153–7.CrossRefPubMed Campbell DI, McPhail G, Lunn PG, Elia M, Jeffries DJ. Intestinal inflammation measured by fecal neopterin in Gambian children with enteropathy: association with growth failure, Giardia lamblia, and intestinal permeability. J Pediatr Gastroenterol Nutr. 2004;39:153–7.CrossRefPubMed
20.
Zurück zum Zitat Coşkun K, Menteş O, Atak A, Aral A, Eryılmaz M, Onguru O, et al. Is neopterin a diagnostic marker of acute appendicitis? Ulus Travma Acil Cerrahi Derg. 2012;18:1–4.CrossRefPubMed Coşkun K, Menteş O, Atak A, Aral A, Eryılmaz M, Onguru O, et al. Is neopterin a diagnostic marker of acute appendicitis? Ulus Travma Acil Cerrahi Derg. 2012;18:1–4.CrossRefPubMed
21.
Zurück zum Zitat Nancey S, Boschetti G, Moussata D, Cotte E, Peyras J, Cuerq C, et al. Neopterin is a novel reliable fecal marker as accurate as calprotectin for predicting endoscopic disease activity in patients with inflammatory bowel diseases. Inflamm Bowel Dis. 2013;19:1043–52.CrossRefPubMed Nancey S, Boschetti G, Moussata D, Cotte E, Peyras J, Cuerq C, et al. Neopterin is a novel reliable fecal marker as accurate as calprotectin for predicting endoscopic disease activity in patients with inflammatory bowel diseases. Inflamm Bowel Dis. 2013;19:1043–52.CrossRefPubMed
22.
Zurück zum Zitat Frin AC, Filippi J, Boschetti G, Flourie B, Drai J, Ferrari P, et al. Accuracies of fecal calprotectin, lactoferrin, M2-pyruvate kinase, neopterin and zonulin to predict the response to infliximab in ulcerative colitis. Dig Liver Dis. 2017;49:11–6. CrossRefPubMed Frin AC, Filippi J, Boschetti G, Flourie B, Drai J, Ferrari P, et al. Accuracies of fecal calprotectin, lactoferrin, M2-pyruvate kinase, neopterin and zonulin to predict the response to infliximab in ulcerative colitis. Dig Liver Dis. 2017;49:11–6. CrossRefPubMed
23.
Zurück zum Zitat Clarke G, Fitzgerald P, Cryan JF, Cassidy EM, Quigley EM, Dinan TG. Tryptophan degradation in irritable bowel syndrome: evidence of indoleamine 2,3-dioxygenase activation in a male cohort. BMC Gastroenterol. 2009;9:6.CrossRefPubMedCentralPubMed Clarke G, Fitzgerald P, Cryan JF, Cassidy EM, Quigley EM, Dinan TG. Tryptophan degradation in irritable bowel syndrome: evidence of indoleamine 2,3-dioxygenase activation in a male cohort. BMC Gastroenterol. 2009;9:6.CrossRefPubMedCentralPubMed
24.
Zurück zum Zitat Hyman PE, Milla PJ, Benninga MA, Davidson GP, Fleisher DF, Taminiau J. Childhood functional gastrointestinal disorders: neonate/toddler. Gastroenterology. 2006;130:1519–26.CrossRefPubMed Hyman PE, Milla PJ, Benninga MA, Davidson GP, Fleisher DF, Taminiau J. Childhood functional gastrointestinal disorders: neonate/toddler. Gastroenterology. 2006;130:1519–26.CrossRefPubMed
25.
Zurück zum Zitat Rasquin A, Di Lorenzo C, Forbes D, Guiraldes E, Hyams JS, Staiano A, et al. Childhood functional gastrointestinal disorders: child/adolescent. Gastroenterology. 2006;130:1527–37.CrossRefPubMed Rasquin A, Di Lorenzo C, Forbes D, Guiraldes E, Hyams JS, Staiano A, et al. Childhood functional gastrointestinal disorders: child/adolescent. Gastroenterology. 2006;130:1527–37.CrossRefPubMed
26.
Zurück zum Zitat Lewis SJ, Heaton KW. Stool form scale as a useful guide to intestinal transit time. Scand J Gastroenterol. 1997;32:920–4.CrossRefPubMed Lewis SJ, Heaton KW. Stool form scale as a useful guide to intestinal transit time. Scand J Gastroenterol. 1997;32:920–4.CrossRefPubMed
27.
Zurück zum Zitat Bashashati M, Rezaei N, Shafieyoun A, McKernan DP, Chang L, Öhman L, et al. Cytokine imbalance in irritable bowel syndrome: a systematic review and meta-analysis. Neurogastroenterol Motil. 2014;26:1036–48.CrossRefPubMed Bashashati M, Rezaei N, Shafieyoun A, McKernan DP, Chang L, Öhman L, et al. Cytokine imbalance in irritable bowel syndrome: a systematic review and meta-analysis. Neurogastroenterol Motil. 2014;26:1036–48.CrossRefPubMed
28.
Zurück zum Zitat Bashashati M, Rezaei N, Andrews CN, Chen CQ, Daryani NE, Sharkey KA, et al. Cytokines and irritable bowel syndrome: where do we stand? Cytokine. 2012;57:201–9.CrossRefPubMed Bashashati M, Rezaei N, Andrews CN, Chen CQ, Daryani NE, Sharkey KA, et al. Cytokines and irritable bowel syndrome: where do we stand? Cytokine. 2012;57:201–9.CrossRefPubMed
29.
Zurück zum Zitat Ortiz-Lucas M, Saz-Peiró P, Sebastián-Domingo JJ. Irritable bowel syndrome immune hypothesis. Part two: the role of cytokines. Rev Esp Enferm Dig. 2010;102:711–7.PubMed Ortiz-Lucas M, Saz-Peiró P, Sebastián-Domingo JJ. Irritable bowel syndrome immune hypothesis. Part two: the role of cytokines. Rev Esp Enferm Dig. 2010;102:711–7.PubMed
30.
Zurück zum Zitat Seyedmirzaee S, Hayatbakhsh MM, Ahmadi B, Baniasadi N, Bagheri Rafsanjani AM, Nikpoor AR, et al. Serum immune biomarkers in irritable bowel syndrome. Clin Res Hepatol Gastroenterol. 2016;40:631–7.CrossRefPubMed Seyedmirzaee S, Hayatbakhsh MM, Ahmadi B, Baniasadi N, Bagheri Rafsanjani AM, Nikpoor AR, et al. Serum immune biomarkers in irritable bowel syndrome. Clin Res Hepatol Gastroenterol. 2016;40:631–7.CrossRefPubMed
31.
Zurück zum Zitat Hod K, Ringel-Kulka T, Martin CF, Maharshak N, Ringel Y. High-sensitive C-reactive protein as a marker for inflammation in irritable bowel syndrome. J Clin Gastroenterol. 2016;50:227–32.CrossRefPubMedCentralPubMed Hod K, Ringel-Kulka T, Martin CF, Maharshak N, Ringel Y. High-sensitive C-reactive protein as a marker for inflammation in irritable bowel syndrome. J Clin Gastroenterol. 2016;50:227–32.CrossRefPubMedCentralPubMed
32.
Zurück zum Zitat Murr C, Widner B, Wirleitner B, Fuchs D. Neopterin as a marker for immune system activation. Curr Drug Metab. 2002;3:175–87.CrossRefPubMed Murr C, Widner B, Wirleitner B, Fuchs D. Neopterin as a marker for immune system activation. Curr Drug Metab. 2002;3:175–87.CrossRefPubMed
33.
Zurück zum Zitat Niederwieser D, Fuchs D, Hausen A, Judmaier G, Reibnegger G, Wachter H, et al. Neopterin as a new biochemical marker in the clinical assessment of ulcerative colitis. Immunobiology. 1985;170:320–6.CrossRefPubMed Niederwieser D, Fuchs D, Hausen A, Judmaier G, Reibnegger G, Wachter H, et al. Neopterin as a new biochemical marker in the clinical assessment of ulcerative colitis. Immunobiology. 1985;170:320–6.CrossRefPubMed
34.
Zurück zum Zitat El-Salhy M, Gundersen D, Hatlebakk JG, Hausken T. Low-grade inflammation in the rectum of patients with sporadic irritable bowel syndrome. Mol Med Rep. 2013;7:1081–5.CrossRefPubMed El-Salhy M, Gundersen D, Hatlebakk JG, Hausken T. Low-grade inflammation in the rectum of patients with sporadic irritable bowel syndrome. Mol Med Rep. 2013;7:1081–5.CrossRefPubMed
35.
Zurück zum Zitat Hughes PA, Moretta M, Lim A, Grasby DJ, Bird D, Brierley SM, et al. Immune derived opioidergic inhibition of viscerosensory afferents is decreased in irritable Bowel Syndrome patients. Brain Behav Immun. 2014;42:191–203.CrossRefPubMed Hughes PA, Moretta M, Lim A, Grasby DJ, Bird D, Brierley SM, et al. Immune derived opioidergic inhibition of viscerosensory afferents is decreased in irritable Bowel Syndrome patients. Brain Behav Immun. 2014;42:191–203.CrossRefPubMed
36.
Zurück zum Zitat Darkoh C, Comer L, Zewdie G, Harold S, Snyder N, Dupont HL. Chemotactic chemokines are important in the pathogenesis of irritable bowel syndrome. PLoS One. 2014;9:e93144.CrossRefPubMedCentralPubMed Darkoh C, Comer L, Zewdie G, Harold S, Snyder N, Dupont HL. Chemotactic chemokines are important in the pathogenesis of irritable bowel syndrome. PLoS One. 2014;9:e93144.CrossRefPubMedCentralPubMed
37.
Zurück zum Zitat Pike BL, Paden KA, Alcala AN, Jaep KM, Gormley RP, Maue AC, et al. Immunological biomarkers in postinfectious irritable bowel syndrome. J Travel Med. 2015;22:242–50.CrossRefPubMed Pike BL, Paden KA, Alcala AN, Jaep KM, Gormley RP, Maue AC, et al. Immunological biomarkers in postinfectious irritable bowel syndrome. J Travel Med. 2015;22:242–50.CrossRefPubMed
38.
Zurück zum Zitat Sinagra E, Pompei G, Tomasello G, Cappello F, Morreale GC, Amvrosiadis G, et al. Inflammation in irritable bowel syndrome: Myth or new treatment target? World J Gastroenterol. 2016;22:2242–55.CrossRefPubMedCentralPubMed Sinagra E, Pompei G, Tomasello G, Cappello F, Morreale GC, Amvrosiadis G, et al. Inflammation in irritable bowel syndrome: Myth or new treatment target? World J Gastroenterol. 2016;22:2242–55.CrossRefPubMedCentralPubMed
39.
Zurück zum Zitat Schmulson M, Bielsa MV, Carmona-Sánchez R, Hernández A, López-Colombo A, López Vidal Y, et al. Microbiota, gastrointestinal infections, low-grade inflammation, and antibiotic therapy in irritable bowel syndrome: an evidence-based review. Rev Gastroenterol Mex. 2014;79:96–134 (in English, Spanish).PubMed Schmulson M, Bielsa MV, Carmona-Sánchez R, Hernández A, López-Colombo A, López Vidal Y, et al. Microbiota, gastrointestinal infections, low-grade inflammation, and antibiotic therapy in irritable bowel syndrome: an evidence-based review. Rev Gastroenterol Mex. 2014;79:96–134 (in English, Spanish).PubMed
40.
Zurück zum Zitat Zhu L, Liu W, Alkhouri R, Baker RD, Bard JE, Quigley EM, et al. Structural changes in the gut microbiome of constipated patients. Physiol Genomics. 2014;46:679–86.CrossRefPubMed Zhu L, Liu W, Alkhouri R, Baker RD, Bard JE, Quigley EM, et al. Structural changes in the gut microbiome of constipated patients. Physiol Genomics. 2014;46:679–86.CrossRefPubMed
41.
Zurück zum Zitat de Meij TG, de Groot EF, Eck A, Budding AE, Kneepkens CM, Benninga MA, et al. Characterization of microbiota in children with chronic functional constipation. PLoS One. 2016;11:e0164731.CrossRefPubMedCentralPubMed de Meij TG, de Groot EF, Eck A, Budding AE, Kneepkens CM, Benninga MA, et al. Characterization of microbiota in children with chronic functional constipation. PLoS One. 2016;11:e0164731.CrossRefPubMedCentralPubMed
42.
Zurück zum Zitat Piche T, Barbara G, Aubert P, Bruley des Varannes S, Dainese R, Nano JL, et al. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut. 2009;58:196–201.CrossRefPubMed Piche T, Barbara G, Aubert P, Bruley des Varannes S, Dainese R, Nano JL, et al. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut. 2009;58:196–201.CrossRefPubMed
43.
Zurück zum Zitat Cremon C, Carini G, Wang B, Vasina V, Cogliandro RF, De Giorgio R, et al. Intestinal serotonin release, sensory neuron activation, and abdominal pain in irritable bowel syndrome. Am J Gastroenterol. 2011;106:1290–8.CrossRefPubMed Cremon C, Carini G, Wang B, Vasina V, Cogliandro RF, De Giorgio R, et al. Intestinal serotonin release, sensory neuron activation, and abdominal pain in irritable bowel syndrome. Am J Gastroenterol. 2011;106:1290–8.CrossRefPubMed
44.
Zurück zum Zitat Borrelli O, Barbara G, Di Nardo G, Cremon C, Lucarelli S, Frediani T, et al. Neuroimmune interaction and anorectal motility in children with food allergy-related chronic constipation. Am J Gastroenterol. 2009;104:454–63.CrossRefPubMed Borrelli O, Barbara G, Di Nardo G, Cremon C, Lucarelli S, Frediani T, et al. Neuroimmune interaction and anorectal motility in children with food allergy-related chronic constipation. Am J Gastroenterol. 2009;104:454–63.CrossRefPubMed
45.
Zurück zum Zitat Irastorza I, Ibañez B, Delgado-Sanzonetti L, Maruri N, Vitoria JC. Cow’s-milk-free diet as a therapeutic option in childhood chronic constipation. J Pediatr Gastroenterol Nutr. 2010;51:171–6.CrossRefPubMed Irastorza I, Ibañez B, Delgado-Sanzonetti L, Maruri N, Vitoria JC. Cow’s-milk-free diet as a therapeutic option in childhood chronic constipation. J Pediatr Gastroenterol Nutr. 2010;51:171–6.CrossRefPubMed
46.
Zurück zum Zitat El-Hodhod MA, Younis NT, Zaitoun YA, Daoud SD. Cow’s milk allergy related pediatric constipation: appropriate time of milk tolerance. Pediatr Allergy Immunol. 2010;21:e407–12.CrossRefPubMed El-Hodhod MA, Younis NT, Zaitoun YA, Daoud SD. Cow’s milk allergy related pediatric constipation: appropriate time of milk tolerance. Pediatr Allergy Immunol. 2010;21:e407–12.CrossRefPubMed
47.
Zurück zum Zitat Syrigou EI, Pitsios C, Panagiotou I, Chouliaras G, Kitsiou S, Kanariou M, et al. Food allergy-related paediatric constipation: the usefulness of atopy patch test. Eur J Pediatr. 2011;170:1173–8.CrossRefPubMed Syrigou EI, Pitsios C, Panagiotou I, Chouliaras G, Kitsiou S, Kanariou M, et al. Food allergy-related paediatric constipation: the usefulness of atopy patch test. Eur J Pediatr. 2011;170:1173–8.CrossRefPubMed
Metadaten
Titel
Elevated serum neopterin levels in children with functional constipation: association with systemic proinflammatory cytokines
verfasst von
Ceren Cıralı
Emel Ulusoy
Tuncay Kume
Nur Arslan
Publikationsdatum
16.03.2018
Verlag
Childrens Hospital, Zhejiang University School of Medicine
Erschienen in
World Journal of Pediatrics / Ausgabe 5/2018
Print ISSN: 1708-8569
Elektronische ISSN: 1867-0687
DOI
https://doi.org/10.1007/s12519-018-0144-8

Weitere Artikel der Ausgabe 5/2018

World Journal of Pediatrics 5/2018 Zur Ausgabe

Update Pädiatrie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.