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Methane Production in Children


Bacterial Overgrowth and Methane Production in Children with Encopresis
Alycia Leiby, MD, Devendra Mehta, MD, Vani Gopalareddy, MD, Susan Jackson-Walker, PhD, and Karoly Horvath, MD, PhD Objectives To assess the prevalence of small intestinal bacterial overgrowth (SIBO) and methane production in children with encopresis. Study design Radiographic fecal impaction (FI) scores were assessed in children with secondary, retentive encopresis and compared with the breath test results. Breath tests with hypoosmotic lactulose solution were performed in both the study patients (n = 50) and gastrointestinal control subjects (n = 39) groups. Results The FI scores were signi?cantly higher in the patients with encopresis who were methane producers (P < .01). SIBO was diagnosed in 21 of 50 (42%) patients with encopresis and 9 of 39 (23%) of control subjects (P = .06). Methane was produced in 56% of the patients with encopresis versus 23.1% of the control subjects in the gastrointestinal group (P < .01). Fasting methane level was elevated in 48% versus 10.3 %, respectively (P < .01). Conclusions Children with FI and encopresis had a higher prevalence of SIBO, elevated basal methane levels, and higher methane production. Methane production was associated with more severe colonic impaction. Further study is needed to determine whether methane production is a primary or secondary factor in the pathogenesis of SIBO and encopresis. (J Pediatr 2010;156:766-70).
t has been shown that the onset of constipation may be associated with a diet change early in life, toilet training during the toddler years, or a painful defecation episode associated with either anal ?ssures or an infectious colitis, leading to withholding.1 Untreated chronic constipation may result in fecal incontinence. Encopresis was the most frequent accompanying symptom (84%) in children presenting with constipation to pediatric gastroenterologists.2 Encopresis is frustrating for patients and families and often requires a signi?cant period of time for treatment and bowel retraining. The recovery rates vary from 30% to 50% after 1 year and from 48% to 75% after 5 years of treatment.3 Orocecal transit time is prolonged in children with constipation.4,5 Animal studies have shown that methane, a product of colonic bacterial fermentation in human beings, prolongs intestinal transit.6 Methane production on breath tests has been associated with prolonged intestinal transit time.6-8 Soares et al8 reported that breath methane production is associated with a prolonged colonic transit time in children with constipation. It was also reported that methane production is more common in children with encopresis when compared with children with constipation only and in control subjects.8,9 Anaerobic bacteria in the terminal ileum and colon are responsible for the production of methane gas. Elevated pH and increased anaerobic states result in higher methane production in the gut.10 Up to one third of control subjects exhaled methane11 over 1 ppm, and there was a negative correlation between frequency of bowel movements and breath methane concentration. Increased breath methane level has been reported in many disorders, including cystic ?brosis, diverticulosis, constipation-predominant irritable bowel syndrome, and colon cancer.12-15 In healthy subjects, bacterial proliferation in the upper gastrointestinal tract is controlled by gastric acid secretion, intestinal motility, and the mucosal immune system. Prolonged intestinal transit time represents a risk factor for small intestinal bacterial overgrowth (SIBO). SIBO is de?ned by an excessive amount of bacteria, particularly anaerobes, in the upper gastrointestinal tract at levels >105-7 organisms/mL.16 Despite the data on the effect of methane on intestinal transit, there is no published report examining the prevalence of SIBO in children with encopresis. The aim of this study was to assess SIBO prevalence measured by the lactulose breath test in children with secondary, retentive encopresis with and without methane-producing ?ora and to compare the results with control subjects.

I

Methods
The study was conducted at the Gastroenterology and Nutrition Outpatient Clinic of the Alfred I. duPont Hospital for Children in Wilmington, DE, from January 2005 to June 2008. The study enrolled otherwise healthy school age children (6 to 12 years) with normal general intellectual functioning who had a history and physical examination consistent with secondary retentive encopresis. All
FI LBT SIBO Fecal impaction Lactulose breath test Small intestinal bacterial overgrowth

From the Division of Pediatric Gastroenterology and Nutrition (A.L., D.M., V.G., K.H.) and Division of Behavioral Health (S.J.), Alfred I. duPont Hospital for Children, Wilmington, DE, and the Thomas Jefferson University (A.L., D.M., V.G., S.J., K.H.), Philadelphia, PA Funding for the project was obtained through the Nemours Foundation. The authors declare no con?icts of interest.
0022-3476/$ - see front matter. Copyright ? 2010 Mosby Inc. All rights reserved. 10.1016/j.jpeds.2009.10.043

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Vol. 156, No. 5  May 2010 patients had daily or weekly episodes of fecal soiling for a minimum of 2 months before evaluation. Patients were not excluded if they had previously been treated for encopresis, because all were still symptomatic and non-adherent to the prescribed therapies. Children with a history of gastrointestinal surgeries, or neuroanatomic disorders were excluded. Fifty children with encopresis were included in the study, and 68% (34 of 50) were male patients. Mean duration of constipation was 3.47 ? 2.56 years. The control group consisted of 39 children of whom 61% were male. Control patients had various gastrointestinal problems but had no signs or symptoms of constipation or encopresis. The indications for the test included abdominal pain, ?atulence, vomiting, and diarrhea. Although there was no signi?cant age difference between the groups, the body mass index (BMI), weight, and height percentiles were signi?cantly higher in the encopresis group (data not shown). Fecal Impaction Scores An abdominal ?at-plate radiograph was obtained for all the patients with encopresis before the start of therapy. The degree of fecal impaction was assessed by a scoring system ranging from 0 to 3.17 A grade of ‘‘0’’ was designated for feces in the rectum and cecum only; a grade of ‘‘1’’ for feces in the rectum, cecum, and discontinuous elsewhere; a grade of ‘‘2’’ for feces in the rectum, cecum, and continuous (allowing for gas) and affecting all segments; and a grade of ‘‘3’’ for feces in the rectum, cecum, continuous elsewhere, and a dilated colon and impacted rectum. Figure 1 (available at www.jpeds. com) shows examples of impaction scores. The radiographs were reviewed at the ?rst of?ce visit and independently by 2 investigators. In cases of discrepancy the score that was in agreement between 2 of the 3 physicians was used. Lactulose Breath Test The lactulose breath test (LBT) was performed at the ?rst visit before starting the therapy. To reduce osmotic effect, the test solution consisted of lactulose 10 g in water 240 mL. This solution had an osmolality of 121 mosmol/L. All patients completed the lactulose breath test after an overnight fast of 10 hours. Patients were given a list of foods high in carbohydrates to avoid the afternoon and evening before the day of testing and were advised to avoid smoke exposure and vigorous exercise on the testing day. Testing was rescheduled if the patient had been on an antibiotic within the previous 2 weeks or had signi?cant carbohydrate consumption the night before. An initial baseline breath sample was collected. Additional samples were then collected at 15, 30, 45, 60, 90, 120, 150, and 180 minutes after the ingestion of test solution. End-expiratory breath samples were collected with the GaSampler system (QuinTron Instrument Company, Milwaukee, Wisconsin). Two samples were taken at each collection point. The second sample was used if the level of carbon dioxide in the ?rst sample was too low. Samples were measured with the Microlyzer model SC analyzer (QuinTron Instrument Company). Hydrogen and methane concentrations were expressed in ppm. The machine was calibrated with the QuinGas-3 (QuinTron Instrument Company) standard gas mixture containing 100 ppm hydrogen, 50 ppm methane, and 5% carbon dioxide. Criteria for Methane Production and SIBO Patients were considered methane producers if their level was more than 3 ppm at any point in the study (based on ambient air containing about 1.8 ppm).18 High basal methane was diagnosed if the baseline sample was >10 ppm. SIBO was diagnosed if the hydrogen level was $20 ppm or the methane level was $10 ppm above baseline at #60 minutes.19 Ethics The Nemours Clinical Research Review Committee and Institutional Review Board approved the protocol. Permission for participation was obtained from the guardian and assent for participation from children ages 7 to 12 years. Statistical Analysis The c2 test for a 2-tailed P value was used for comparing frequencies between 2 groups. Odds ratios and 95% con?dence intervals were calculated. For comparing means between the 2 groups, the 2-tailed t test was used. P < .05 was considered as statistically signi?cant.

Results
The mean fecal impaction (FI) radiographic score was 1.9 ? 0.65 for the entire encopretic group. There was a signi?cant difference (P < .01) in the mean FI score between methane producers (2.03 ? 0.32; n = 24) and non-methane–producing patients (1.72 ? 0.44; n = 26). The mean FI scores of the SIBO-positive patients (1.9 ? 0.49) and the SIBO-negative patients (1.89 ? 0.39) were not different (P = .06). SIBO was found in 21 of the 50 (42%) children with encopresis. The prevalence of SIBO was lower (23.1%) in the gastrointestinal control group. The difference did not reach statistical signi?cance (P = .06). Of the patients with encopresis and SIBO, the diagnosis was made on the basis of elevated methane levels in 8 patients, elevated hydrogen levels in 11 patients, and both elevated methane and hydrogen levels in 2 patients. The diagnosis of SIBO is sometimes based on a ‘‘double peak,’’ which is de?ned as an early peak of 2 consecutive hydrogen values more than 10 ppm above the baseline value that is clearly distinguishable from a colonic peak of >20 ppm above baseline20 or a rise of 20 ppm occurring more than 15 minutes before a colonic peak.19 In our group, a double peak was found in 10 patients with encopresis and 2 gastrointestinal control subjects. There was no difference between groups in sex or existence of SIBO. High basal methane concentration was measured in 24 of 50 (48%) patients with encopresis versus 4 of 39 (10.3%) control subjects (P < .001). Methane production ($3 ppm)
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Vol. 156, No. 5 were methane producers according to the initial LBT and remained so on the repeat LBT.

Discussion
Because the bacterial ?ora in the small intestine is controlled by motility and methane production is associated with slower motility, patients with encopresis and methane production are at risk for SIBO. We hypothesized that methane production increases the risk for SIBO by slowing small intestinal transit time. SIBO was diagnosed more frequently in our patients with encopresis compared with the children with other gastrointestinal disorders, but this did not reach signi?cance (P = .06). However, we did not use healthy control subjects; our control group consisted of gastroenterology patients without constipation. In a study by Rhodes et al,19 all 37 healthy control subjects had negative lactulose breath test results. Methane in the gut is the sole result of anaerobic bacterial production predominantly from the organism Methanobrevibacter smithii.12 Lactulose does not in?uence methane-producing ?ora; therefore it can be used as substrate for the LBT.18 Bond et al18 showed that newborns and children younger than 2 years do not excrete methane. Levels then slowly rise until the age of 10 years, when adult values are reached. There seem to be many factors in?uencing the production of methane in the gut.11 A signi?cant concentration of methanogenic bacteria must be reached to produce a rise of 1 ppm above atmospheric level.12 Bacterial culture in adults revealed that an average concentration of 9.45 log10 methanogenic organisms per gram dry weight of stool was needed to produce methane. People who had an average concentration of 4.9 log10 methanogenic organisms per gram dry weight of stool or less did not produce detectable methane on breath testing.12 In animal experiments, Pimentel et al6 demonstrated that methane infusions slowed small intestinal transit and altered contractile activity. They hypothesized that methane may activate a re?ex pathway similar to the way fat stimulates the ‘‘ileal brake,’’ triggering nonpropulsive contractions. It can be hypothesized that a methane-overgrowth cycle exists by methane slowing the small intestinal transit, resulting in SIBO and subsequent increase of the anaerobic bacterial load producing more methane and perpetuating prolonged transit time and constipation. In this study, 56% of the patients with encopresis produced methane, and 48% had high basal methane levels. These values are higher than those found in our control group consisting of children with other gastrointestinal disorders, in which 23% produced methane and 10% had high baseline values. These results are in accordance with the previously published reports describing that higher percentage of children with encopresis and constipation produced methane.8,9 Fiedorek et al9 found that 65% of the patients with encopresis were methane producers compared with the control group without constipation or encopresis, for whom 15% of patients had
Leiby et al

Figure 2. Average methane and hydrogen productions in the SIBO-positive and SIBO-negative patients in the encopretic and control groups (Mean ? SEM).

at any time during the LBT was present in 28 of 50 (56%) patients with encopresis and 9 of 39 (23.1%) controls (P < .01). Figure 2 illustrates the average methane and hydrogen productions in the SIBO-positive and SIBO-negative patients in the 2 study groups. It clearly shows the higher methane levels in the encopretic group. We were able to retest 6 of the 21 patients with encopresis who had SIBO. The other 15 patients refused retesting or were lost to follow-up. Of these 6 patients, 3 had responded to therapy as de?ned by daily, soft stools and no soiling during the 4 weeks before the repeat LBT. Two of the 6 patients (33%) still had SIBO; both were nonresponders and were nonadherent to therapy. Four of the 6 retested patients
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May 2010 a methane level >3 ppm. Similar results were also found in a study of 40 children in which 75% with soiling had increased breath methane, compared with 16% of children in a group with constipation and no soiling.8 Both pediatric and adult studies reported a negative correlation between frequency of bowel movements and breath methane concentration in methane producers.9,11 There are reports showing that successful management of constipation may eliminate methane production after 6 to 8 weeks of dietary and laxative therapy.9 Methane has consistently been associated with constipation-predominant irritable bowel syndrome in adults undergoing lactulose breath testing.11,21 Older studies of healthy adults also have shown longer transit time in methane producers.7,22 Methane producers had signi?cantly higher colonic fecal load (FI score) as was shown in our study. Our study also suggests that methane not only increases fecal load but also provides a favorable environment for increased growth of methanogenic bacteria and SIBO. High intestinal bacterial load might also exacerbate the symptoms of constipation, ?atulence, and encopresis. The effect of rectal distension on the upper gastrointestinal motility has been documented in both animal and human studies. The effect of continuous isobaric rectal distension on gastric emptying and orocecal transit was evaluated in young females. The rectal distension signi?cantly prolonged the gastric half-emptying time; however, the mean orocecal transit time during rectal distension were not signi?cantly different.23 In a study on 77 patients with slow transit constipation, 43% exhibited altered motor function in the esophagus or small bowel.24 The frequency of bowel movements in those with upper gastrointestinal dysmotility was less (0.5 ? 0.1 vs 1.3 ? 0.3 bowel movements/per week, P = .04).24 The prevalence of altered motility (43%) is similar to the percentage of our study group (42%) with SIBO. It is likely that small intestinal dysmotility can be an additional important factor in the increased prevalence of SIBO in patients with encopresis. Our study has some limitations. The gold standard test for SIBO is the direct culture. The breath hydrogen/methane test is an indirect test for SIBO. The lactulose breath test was chosen to prove it because it is easy to perform and noninvasive. The lactulose used without dilution is a hypertonic substrate25 that will likely alter transit time; therefore we used a hypoosmolar solution. We were not able to retest all of the patients with encopresis and SIBO because many either refused retesting or were lost to follow-up. Our control subjects were patients seen in the outpatient gastroenterology clinic for symptoms other than constipation or encopresis and were therefore not ‘‘healthy’’ volunteers. There is no clear agreement in the literature regarding the optimal substrate, cut-off values for hydrogen and methane and the time of their elevation for bacterial overgrowth. Lactulose and glucose are the most commonly used substrates. Various de?nitions have been used to de?ne a positive test result. Some advocate the use of the ‘‘double peak’’ method, which has been de?ned as an early peak of 2 consecutive hydrogen values >10 ppm above the baseline value that is

ORIGINAL ARTICLES
clearly distinguishable from a colonic peak of >20 ppm above baseline20 or a rise of 20 ppm occurring more than 15 minutes before a colonic peak.19 Although this double peak is rarely seen in clinical practice,26 in our study we found that greater than one third of patients with SIBO had a double peak. There is no optimal noninvasive study for the diagnosis of SIBO. In a review of published papers regarding SIBO, Khoshini et al27 concluded that the intestinal culture studies, which are considered the gold standard, did not meet the quality standards. Their analysis suggests that glucose breath tests had somewhat better speci?city and sensitivity then those studies that used lactulose as substrate. We conclude that children with fecal impaction and encopresis had a higher prevalence of SIBO, and signi?cantly elevated basal methane levels and higher methane production. Methane production was associated with more severe colonic impaction. Methane not only in?uences small intestinal transit time but is strongly associated with constipation. This raises an interesting question; do factors (diet, antibiotic use, etc) that in?uence colonic ?ora and increase methane production contribute to the development of constipation and fecal impaction or is methane production just the consequence of fecal impaction? A larger study looking at changes in motility, methane production, and symptoms after antibiotic treatment in constipated patients with encopresis with documented SIBO would provide important information. n
The authors thank Jerrianne Kuntz, RN, for her assistance with breath testing.
Submitted for publication Jun 22, 2009; last revision received Sep 14, 2009; accepted Oct 30, 2009. Reprint requests: Karoly Horvath, MD, PhD, Alfred I. duPont Hospital for Children, 1600 Rockland Rd, Wilmington, DE 19803. E-mail: khorvath@ nemours.org.

References
1. Di Lorenzo C. Childhood Functional Gastrointestinal Disorders: Child/Adolescent. In: Drossman DA, editor. Rome III: The Functional Gastrointestinal Disorders. McLean, Virginia Degnon Associates, Inc., 2006:723-77. 2. Voskuijl WP, Heijmans J, Heijmans HS, Taminiau JA, Benninga MA. Use of Rome II criteria in childhood defecation disorders: applicability in clinical and research practice. J Pediatr 2004;145:213-7. 3. Loening-Baucke V. Encopresis. Curr Opin Pediatr 2002;14:570-5. ? 4. Gutierrez C, Marco A, Nogales A, Tebar R. Total and segmental colonic transit time and anorectal manometry in children with chronic idiopathic constipation. J Pediatr Gastroenterol Nutr 2002;35:31-8. 5. Corazziari E, Cucchiara S, Staiano A, Romaniello G, Tamburrini O, Torsoli A, et al. Gastrointestinal transit time, frequency of defecation, and anorectal manometry in healthy and constipated children. J Pediatr 1985;106:379-82. 6. Pimentel M, Lin HC, Enayati P, van den Burg B, Lee HR, Chen JH, et al. Methane, a gas produced by enteric bacteria, slows intestinal transit and augments small intestinal contractile activity. Am J Physiol Gastrointest Liver Physiol 2006;290:G1089-95. ? 7. El Ou?r L, Flourie B, Bruley des Varannes S, Barry JL, Cloarec D, Bornet F, et al. Relations between transit time, fermentation products, and hydrogen consuming ?ora in healthy humans. Gut 1996; 38:870-7. 769

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olism of the methane-producing colonic bacteria. J Exp Med 1971;133: 572-88. Rhodes JM, Middleton P, Jewell DP. The lactulose hydrogen breath test as a diagnostic test for small-bowel bacterial overgrowth. Scand J Gastroenterol 1979;14:333-6. Corazza GR, Menozzi MG, Strocchi A, Rasciti L, Vaira D, Lecchini R, et al. The diagnosis of small bowel bacterial overgrowth. Reliability of jejunal culture and inadequacy of breath hydrogen testing. Gastroenterology 1990;98:302-9. Pimentel M, Chatterjee S, Chow EJ, Park S, Kong Y. Neomycin improves constipation-predominant irritable bowel syndrome in a fashion that is dependent on the presence of methane gas: subanalysis of a double-blind randomized controlled study. Dig Dis Sci 2006;51: 1297-301. Stephen AM. Dietary ?bre and colonic nitrogen metabolism. Scand J Gastroenterol Suppl 1987;129:110-5. Coremans G, Geypens B, Vos R, Tack J, Margaritis V, Ghoos Y, Janssens J. In?uence of continuous isobaric rectal distension on gastric emptying and small bowel transit in young healthy women. Neurogastroenterol Motil 2004;16:107-11. Zarate N, Knowles CH, Yazaki E, Lunnis PJ, Scott SM. Clinical presentation and patterns of slow transit constipation do not predict coexistent upper gut dysmotility. Dig Dis Sci 2009;54:122-31. Joseph F Jr., Rosenberg AJ. Breath hydrogen testing: diseased versus normal patients. J Pediatr Gastroenterol Nutr 1988;7:787-8. Saad RJ, Chey WD. Breath tests for Gastrointestinal disease: The Real Deal or Just a lot of Hot Air? Gastroenterology 2007;133: 1763-6. Khoshini R, Dai SC, Lezcano S, Pimentel M. A systematic review of diagnostic tests for small intestinal bacterial overgrowth. Dig Dis Sci 2008; 53:1443-54.

8. Soares AC, Lederman HM, Fagundes-Neto U, de Morais MB. Breath methane associated with slow colonic transit time in children with chronic constipation. J Clin Gastroenterol 2005;39:512-5. 9. Fiedorek SC, Pumphrey CL, Casteel HB. Breath methane production in children with constipation and encopresis. J Pediatr Gastroenterol Nutr 1990;10:473-7. 10. Stephen AM, Wiggins HS, Englyst HN, Cole TJ, Wayman BJ, Cummings JH. The effect of age, sex and level of intake of dietary ?bre from wheat on large-bowel function in thirty healthy subjects. Br J Nutr 1986;56:349-61. 11. Levitt MD, Furne JK, Kuskowski M, Ruddy J. Stability of human methanogenic ?ora over 35 years and a review of insights obtained from breath methane measurements. Clin Gastroenterol Hepatol 2006; 4:123-9. 12. Weaver GA, Krause JA, Miller TL, Wolin MJ. Incidence of methanogenic bacteria in a sigmoidoscopy population: an association of methanogenic bacteria and diverticulosis. Gut 1986;27:698-704. 13. Chatterjee S, Park S, Low K, Kong Y, Pimentel M. The degree of breath methane production in IBS correlates with the severity of constipation. Am J Gastroenterol 2007;102:837-41. ? ? ? 14. Pique JM, Pallares M, Cuso E, Vilar-Bonet J, Gassull MA. Methane production and colon cancer. Gastroenterology 1984;87:601-5. 15. Bujanover Y, Peled Y, Blau H, Yahav J, Katzenelson D, Gilat T. Methane production in patients with cystic ?brosis. J Pediatr Gastroenterol Nutr 1987;6:377-80. 16. King CE, Toskes PP. Small intestine bacterial overgrowth. Gastroenterology 1979;76:1035-55. 17. Blethyn AJ, Verrier Jones K, Newcombe R, Roberts GM, Jenkins HR. Radiological assessment of constipation. Arch Dis Child 1995;73:532-3. 18. Bond JH Jr., Engel RR, Levitt MD. Factors in?uencing pulmonary methane excretion in man. An indirect method of studying the in situ metab-

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ORIGINAL ARTICLES

Figure 1. Abdominal radiograph-based scoring system for FI.

Bacterial Overgrowth and Methane Production in Children with Encopresis

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