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Original Report| Volume 14, ISSUE 9, P921-930, September 2013

Endogenous Inhibition of Somatic Pain Is Impaired in Girls With Irritable Bowel Syndrome Compared With Healthy Girls

      Abstract

      Endogenous pain inhibition is often deficient in adults with chronic pain conditions including irritable bowel syndrome (IBS). It is unclear whether deficiencies in pain inhibition are present in young children with IBS. The present study compared endogenous pain inhibition, somatic pain threshold, and psychosocial distress in young girls with IBS versus controls. Girls with IBS did not show significant endogenous pain inhibition of heat pain threshold during a cold-pressor task in contrast to controls, who had significant pain inhibition. Girls with IBS did not differ from peers on measures of somatic pain but had more symptoms of depression, somatization, and anxiety than controls. When psychological variables were included as covariates, the difference in pain inhibition was no longer significant, although poor achieved power limits interpretation of these results. Higher-order cognitive processes including psychological variables may be contributing to observed pain inhibition. In girls with IBS, pain inhibition was positively related to the number of days without a bowel movement. To our knowledge, this is the first study to demonstrate deficiencies of endogenous pain inhibition in young children with IBS. Findings have implications for better understanding of onset and maintenance of IBS and other chronic pain conditions.

      Perspective

      This study found that young girls with IBS have deficient endogenous pain inhibition compared to healthy girls, which is consistent with the literature on adults. This information can facilitate clinicians in identification of risk factors for onset/maintenance of IBS and other chronic pain conditions.

      Key words

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      References

        • Apley J.
        The Child With Abdominal Pains.
        Blackwell Scientific, London1975
        • Barnes D.
        • Gatchel R.J.
        • Mayer T.G.
        • Barnett J.
        Changes in MMPI profiles of chronic low back pain patients following successful treatment.
        J Spinal Disord. 1990; 3: 353-355
        • Bouhassira D.
        • Bing Z.
        • Le Bars D.
        Studies of the brain structures involved in diffuse noxious inhibitory controls: The mesencephalon.
        J Neurophysiol. 1990; 64: 1712-1723
        • Bouhassira D.
        • Villanueva L.
        • Bing Z.
        • le Bars D.
        Involvement of the subnucleus reticularis dorsalis in diffuse noxious inhibitory controls in the rat.
        Brain Res. 1992; 595: 353-357
        • Campo J.V.
        • Bridge J.
        • Ehmann M.
        • Altman S.
        • Lucas A.
        • Birmaher B.
        • Di L.C.
        • Iyengar S.
        • Brent D.A.
        Recurrent abdominal pain, anxiety, and depression in primary care.
        Pediatrics. 2004; 113: 817-824
        • Cohen J.
        Statistical Power Analysis for the Behavioral Sciences.
        rev ed. Lawrence Erlbaum Associates, Inc, Hillsdale, NJ1977
        • Czyzewski D.I.
        • Eakin M.N.
        • Lane M.M.
        • Jarrett M.
        • Shulman R.J.
        Recurrent abdominal pain in primary and tertiary care: Differences and similarities.
        Child Health Care. 2007; 36: 137-153
        • DiLorenzo C.
        • Youssef N.N.
        • Sigurdsson L.
        • Scharff L.
        • Griffiths J.
        • Wald A.
        Visceral hyperalgesia in children with functional abdominal pain.
        J Pediatr. 2001; 139: 838-843
        • Duarte M.A.
        • Goulart E.M.
        • Penna F.
        Pressure pain threshold in children with recurrent abdominal pain.
        J Pediatr Gastroenterol Nutr. 2000; 31: 280-285
        • Edwards R.R.
        • Ness T.J.
        • Weigent D.A.
        • Fillingim R.B.
        Individual differences in diffuse noxious inhibitory controls (DNIC): Association with clinical variables.
        Pain. 2003; 106: 427-437
        • El-Matary W.
        • Spray C.
        • Sandhu B.
        Irritable bowel syndrome: The commonest cause of recurrent abdominal pain in children.
        Eur J Pediatr. 2004; 163: 584-588
        • Elsenbruch S.
        • Rosenberger C.
        • Enck P.
        • Forsting M.
        • Schedlowski M.
        • Gizewski E.R.
        Affective disturbances modulate the neural processing of visceral pain stimuli in irritable bowel syndrome: An fMRI study.
        Gut. 2010; 59: 489-495
        • Faure C.
        • Wieckowska A.
        Somatic referral of visceral sensations and rectal sensory threshold for pain in children with functional gastrointestinal disorders.
        J Pediatr. 2007; 150: 66-71
        • Fields H.L.
        • Basbaum A.I.
        • Heinricher M.M.
        Central nervous system mechanisms of pain modulation.
        in: McMahon S.B. Koltzenburg M. Textbook of Pain. Elsevier/Churchill Livingstone, Philadelphia, PA2006: 125-142
        • Gaylord N.
        • Carson S.
        Assessing recurrent abdominal pain in children.
        Nurse Pract. 1983; 8: 19-24
        • Gebhart G.F.
        Descending modulation of pain.
        Neurosci Biobehav Rev. 2004; 27: 729-737
        • Ginkel R.V.
        • Voskuijl W.P.
        • Benninga M.A.
        • Taminiau J.A.
        • Boeckxstaens G.E.
        Alterations in rectal sensitivity and motility in childhood irritable bowel syndrome.
        Gastroenterology. 2001; 120: 31-38
        • Goffaux P.
        • Lafrenaye S.
        • Morin M.
        • Patural H.
        • Demers G.
        • Marchand S.
        Perterm births: Can neonatal pain alter the development of endogenous gating systems?.
        Eur J Pain. 2008; 12: 945-951
        • Goffaux P.
        • Redmond J.W.
        • Rainville P.
        • Marchand S.
        Descending analgesia—When the spine echoes what the brain expects.
        Pain. 2007; 130: 137-143
        • Goodin B.R.
        • McGuire L.
        • Allshouse M.
        • Stapleton L.
        • Haythornthwaite J.A.
        • Burns N.
        • Mayes L.A.
        • Edwards R.R.
        Associations between catastrophizing and endogenous pain-inhibitory processes: Sex differences.
        J Pain. 2009; 10: 180-190
        • Hermann C.
        • Zohsel K.
        • Hohmeister J.
        • Flor H.
        Cortical correlates of an attentional bias to painful and innocuous somatic stimuli in children with recurrent abdominal pain.
        Pain. 2008; 136: 397-406
        • Heymen S.
        • Maixner W.
        • Whitehead W.E.
        • Klatzkin R.R.
        • Mechlin B.
        • Light K.C.
        Central processing of noxious somatic stimuli in patients with irritable bowel syndrome compared with healthy controls.
        Clin J Pain. 2010; 26: 104-109
        • Jarrett M.
        • Heitkemper M.
        • Czyzewski D.I.
        • Shulman R.J.
        Recurrent abdominal pain in children: Forerunner to adult irritable bowel syndrome?.
        J Soc Pediatr Nurs. 2003; 8: 81-89
        • King C.D.
        • Wong F.
        • Currie T.
        • Mauderli A.P.
        • Fillingim R.B.
        • Riley J.L.
        Deficiency in endogenous modulation of prolonged heat pain in patients with Irritable Bowel Syndrome and Temporomandibular Disorder.
        Pain. 2009; 143: 172-178
        • Lane M.M.
        • Czyzewski D.I.
        • Chumpitazi B.P.
        • Shulman R.J.
        Reliability and validity of a modified Bristol Stool Form Scale for Children.
        J Pediatr. 2011; 159: 437-441
        • Le Bars D.
        • Villanueva L.
        Electrophysiological evidence for the activation of descending inhibitory controls by nociceptive afferent pathways.
        Prog Brain Res. 1988; 77: 275-299
        • Levine M.
        Recurrent abdominal pain in school children: The loneliness of the long-distance physician.
        Pediatr Clin North Am. 1978; 31: 969-991
        • Longstreth G.F.
        • Thompsoon W.G.
        • Chey W.D.
        • Houghton L.A.
        • Mearin F.
        • Spiller R.C.
        Functional bowel disorders.
        Gastroenterology. 2006; 130: 1480-1491
        • Maixner W.
        • Fillingim R.
        • Booker D.
        • Sigurdsson A.
        Sensitivity of patients with painful temporomandibular disorders to experimentally evoked pain.
        Pain. 1995; 63: 341-351
        • Meesters C.
        • Muris P.
        • Ghys A.
        • Reumerman T.
        • Rooijmans M.
        The Children's Somatization Inventory: Further evidence for its reliability and validity in a pediatric and a community sample of Dutch children and adolescents.
        J Pediatr Psychol. 2003; 28: 413-422
        • Michaux G.
        Comments on “Recommendations on terminology and practice of psychophysical DNIC testing” by Yarnitsky et al., 14(4), 339.
        Eur J Pain. 2010; 14: 1068-1069
        • Miro J.
        • Castarlenas E.
        • Huguet A.
        Evidence for the use of a numerical rating scale to assess the intensity of pediatric pain.
        Eur J Pain. 2009; 13: 1089-1095
        • Moshiree B.
        • Price D.D.
        • Robinson M.E.
        • Gaible R.
        • Verne G.N.
        Thermal and visceral hypersensitivity in irritable bowel syndrome patients with and without fibromyalgia.
        Clin J Pain. 2007; 23: 323-330
        • Olafsdottir E.
        • Aksnes L.
        • Fluge G.
        • Berstad A.
        Faecal calprotectin levels in infants with infantile colic, healthy infants, children with inflammatory bowel disease, children with recurrent abdominal pain and healthy children.
        Acta Paediatr. 2002; 91: 45-50
        • Pagé M.G.
        • Katz J.
        • Stinson J.
        • Isaac L.
        • Martin-Pichora A.L.
        • Campbell F.
        Validation of the numerical rating scale for pain intensity and unpleasantness in pediatric acute postoperative pain: Sensitivity to change over time.
        J Pain. 2012; 13: 359-369
        • Piche M.
        • Arsenault M.
        • Poitras P.
        • Rainville P.
        • Bouin M.
        Widespread hypersensitivity is related to altered pain inhibition processes in irritable bowel syndrome.
        Pain. 2010; 148: 49-58
        • Posserud I.
        • Syrous A.
        • Lindstrom L.
        • Tack J.
        • Abrahamsson H.
        • Simren M.
        Altered rectal perception in irritable bowel syndrome is associated with symptom severity.
        Gastroenterology. 2007; 133: 1113-1123
        • Potvin S.
        • Larouche A.
        • Normand E.
        • de Souza J.
        • Gaumond I.
        • Marchand S.
        • Grignon S.
        No relationship between the ins del polymorphism of the serotonin transporter promoter and pain perception in fibromyalgia patients and healthy controls.
        Eur J Pain. 2010; 14: 742-746
        • Price D.D.
        • Zhou Q.
        • Moshiree B.
        • Robinson M.E.
        • Verne G.N.
        Peripheral and central contributions to hyperalgesia in irritable bowel syndrome.
        J Pain. 2006; 7: 529-535
        • Rasquin A.
        • Di L.C.
        • Forbes D.
        • Guiraldes E.
        • Hyams J.S.
        • Staiano A.
        • Walker L.S.
        Childhood functional gastrointestinal disorders: Child/adolescent.
        Gastroenterology. 2006; 130: 1527-1537
        • Reynolds C.R.
        • Kamphaus R.W.
        Manual for the Behavior Assessment System for Children.
        AGS Publishing, Circle Pines, MN2004
        • Rhudy J.L.
        • Meagher M.W.
        Fear and anxiety: Divergent effects on human pain thresholds.
        Pain. 2000; 84: 65-75
        • Rhudy J.L.
        • Meagher M.W.
        The role of emotion in pain modulation.
        Curr Opin Psychiatry. 2001; 14: 241-245
        • Rhudy J.L.
        • Williams A.E.
        • McCabe K.M.
        • Nguyen M.V.
        • Rambo P.
        Affective modulation of nociception at spinal and supraspinal levels.
        Psychophysiology. 2005; 42: 579-587
        • Rhudy J.L.
        • Williams A.E.
        • McCabe K.M.
        • Russell J.L.
        • Maynard L.J.
        Emotional control of nociceptive reactions (ECON): Do affective valence and arousal play a role?.
        Pain. 2008; 136: 250-261
        • Robins P.M.
        • Schoff K.M.
        • Glutting J.J.
        • Abelkop A.S.
        Discriminative validity of the Behavioral Assessment System for Children–parent rating scales in children with recurrent abdominal pain and matched controls.
        Psychol Schools. 2003; 40: 145-154
        • Rodrigues A.C.
        • Nicholas Verne G.
        • Schmidt S.
        • Mauderli A.P.
        Hypersensitivity to cutaneous thermal nociceptive stimuli in irritable bowel syndrome.
        Pain. 2005; 115: 5-11
        • Sandrini G.
        • Rossi P.
        • Milanov I.
        • Serrao M.
        • Cecchini A.P.
        • Nappi G.
        Abnormal modulatory influence of diffuse noxious inhibitory controls in migraine and chronic tension-type headache patients.
        Cephalalgia. 2006; 26: 782-789
        • Saps M.
        • Sztainberg M.
        • Di L.C.
        A prospective community-based study of gastroenterological symptoms in school-age children.
        J Pediatr Gastroenterol Nutr. 2006; 43: 477-482
        • Serrao M.
        • Rossi P.
        • Sandrini G.
        • Parisi L.
        • Amabile G.A.
        • Nappi G.
        • Pierelli F.
        Effects of diffuse noxious inhibitory controls on temporal summation of the RIII reflex in humans.
        Pain. 2004; 112: 353-360
        • Song G.H.
        • Venkatraman V.
        • Ho K.Y.
        • Chee M.W.
        • Yeoh K.G.
        • Wilder-Smith C.H.
        Cortical effects of anticipation and endogenous modulation of visceral pain assessed by functional brain MRI in irritable bowel syndrome patients and healthy controls.
        Pain. 2006; 126: 79-90
        • Sternbach R.A.
        • Wolf S.R.
        • Murphy R.W.
        • Akeson W.H.
        Traits of pain patients: The low-back “loser”.
        Psychosomatics. 1973; 14: 226-229
        • Uc A.
        • Hyman P.E.
        • Walker L.S.
        Functional gastrointestinal disorders in African American children in primary care.
        J Pediatr Gastroenterol Nutr. 2006; 42: 270-274
        • Verne G.N.
        • Robinson M.E.
        • Price D.D.
        Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome.
        Pain. 2001; 93: 7-14
        • Villanueva L.
        • de Pommery J.
        • Menetrey D.
        • Le Bars D.
        Spinal afferent projections to subnucleus reticularis dorsalis in the rat.
        Neurosci Lett. 1991; 134: 98-102
        • Villanueva L.
        • Le Bars D.
        The activation of bulbo-spinal controls by peripheral nociceptive inputs: Diffuse noxious inhibitory controls.
        Biol Res. 1995; 28: 113-125
        • Von Baeyer C.L.
        • Spagrud L.J.
        • McCormick J.C.
        • Choo E.
        • Neville K.
        • Connelly M.A.
        Three new datasets supporting use of the Numerical Rating Scale (NRS-11) for children's self-reports of pain intensity.
        Pain. 2009; 143: 223-227
        • Walker L.S.
        • Garber J.
        Children's Somatization Inventory: Preliminary Manual.
        Vanderbilt University Medical Center, Nashville, TN1993
        • Walker L.S.
        • Garber J.
        • Greene J.W.
        Somatization symptoms in pediatric abdominal pain patients: Relation to chronicity of abdominal pain and parent somatization.
        J Abnorm Child Psychol. 1991; 19: 379-394
        • Walker L.S.
        • Garber J.
        • Greene J.W.
        Psychosocial correlates of recurrent childhood pain: A comparison of pediatric patients with recurrent abdominal pain, organic illness, and psychiatric disorders.
        J Abnorm Psychol. 1993; 102: 248-258
        • Walker L.S.
        • Guite J.W.
        • Duke M.
        • Barnard J.A.
        • Greene J.W.
        Recurrent abdominal pain: A potential precursor of irritable bowel syndrome in adolescents and young adults.
        J Pediatr. 1998; 132: 1010-1015
        • Wilder-Smith C.H.
        • Schindler D.
        • Lovblad K.
        • Redmond S.M.
        • Nirkko A.
        Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls.
        Gut. 2004; 53: 1595-1601
        • Williams A.E.
        • Rhudy J.L.
        Supraspinal modulation of trigeminal nociception and pain.
        Headache. 2009; 49: 704-720
        • Yarnitsky D.
        • Arendt-Nielsen L.
        • Bouhassira D.
        • Edwards R.R.
        • Fillingim R.B.
        • Granot M.
        • Hansson P.
        • Lautenbacher S.
        • Marchand S.
        • Wilder-Smith O.
        Recommendations on terminology and practice of psychophysical DNIC testing.
        Eur J Pain. 2010; 14: 339
        • Zohsel K.
        • Hohmeister J.
        • Flor H.
        • Hermann C.
        Somatic pain sensitivity in children with recurrent abdominal pain.
        Am J Gastroenterol. 2008; 103: 1517-1523
        • Zuckerman B.
        • Stevenson J.
        • Bailey V.
        Stomachaches and headaches in a community sample of preschool children.
        Pediatrics. 1987; 79: 677-682