{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T04:57:48Z","timestamp":1782968268166,"version":"3.54.5"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2021,12,9]],"date-time":"2021-12-09T00:00:00Z","timestamp":1639008000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,12,9]],"date-time":"2021-12-09T00:00:00Z","timestamp":1639008000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"the research council of norway,"},{"name":"the european research council","award":["SCARABEE"],"award-info":[{"award-number":["SCARABEE"]}]},{"name":"the european research council","award":["number 742158"],"award-info":[{"award-number":["number 742158"]}]},{"name":"united kingdom medical research council","award":["1621658"],"award-info":[{"award-number":["1621658"]}]},{"DOI":"10.13039\/501100005366","name":"University of Oslo","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100005366","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Int J Colorectal Dis"],"published-print":{"date-parts":[[2022,3]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Purpose<\/jats:title>\n                <jats:p>Children with constipation and suspected Hirschsprung\u2019s disease are referred for rectal biopsy. Since this is an invasive procedure, appropriate indications should be applied to minimize the number of \u201cunnecessary\u201d biopsies.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>We reviewed all constipated children who underwent a rectal biopsy to diagnose a possible Hirschsprung\u2019s disease at a tertiary referral hospital over a 6-year period (2013\u20132018). We registered clinical and demographic factors in these children and conducted correlation and multivariate regression analysis to evaluate the relation between these factors and a diagnosis of Hirschsprung\u2019s disease.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>We identified 225 children, aged 0\u201317\u00a0years. In total, Hirschsprung\u2019s disease was diagnosed in only 49\/225 (22%). Among the 49 children with Hirschsprung\u2019s disease, 29 (59%) were diagnosed in the neonatal period. Among girls, HD was confirmed in only 10\/101 (10%) children, and only 1 of these 10 girls was older than 6\u00a0months at the time of the biopsy. The following factors correlated significantly with Hirschsprung\u2019s disease diagnosis in children older than 1\u00a0month: \u201cmale sex\u201d, \u201cfailure to thrive\u201d, \u201cgross abdominal distention plus vomiting\u201d and \u201cfulfils the Rome 4 criteria for functional constipation\u201d.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>In children referred for rectal biopsy, the factors most indicative of Hirschsprung\u2019s disease were \u201cmale sex\u201d, \u201cfailure to thrive\u201d, \u201cgross abdominal distention plus vomiting\u201d and \u201cfulfils the Rome 4 criteria for functional constipation\u201d. Notably, the prevalence of Hirschsprung\u2019s disease decreased with the increasing age of the children. Girls referred for a biopsy rarely had Hirschsprung\u2019s disease, especially those older than 1\u00a0month.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1007\/s00384-021-04069-4","type":"journal-article","created":{"date-parts":[[2021,12,9]],"date-time":"2021-12-09T11:12:06Z","timestamp":1639048326000},"page":"597-605","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Evaluation of diagnostic factors used to refer children with constipation for rectal biopsies"],"prefix":"10.1007","volume":"37","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0860-551X","authenticated-orcid":false,"given":"Emilie G.","family":"Jaroy","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ragnhild","family":"Emblem","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henrik M.","family":"Reims","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"The Tien","family":"Mai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriel T.","family":"Risa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rune","family":"Ougland","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,12,9]]},"reference":[{"issue":"1","key":"4069_CR1","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1177\/1093526619892351","volume":"23","author":"L Ambartsumyan","year":"2020","unstructured":"Ambartsumyan L, Smith C, Kapur RP (2020) Diagnosis of Hirschsprung Disease. Pediatr Dev Pathol 23(1):8\u201322","journal-title":"Pediatr Dev Pathol"},{"key":"4069_CR2","doi-asserted-by":"crossref","unstructured":"Knowles CH, De Giorgio R, Kapur RP, Bruder E, Farrugia G, Geboes K et al (2010) The London Classification of gastrointestinal neuromuscular pathology: report on behalf of the Gastro 2009 International Working Group. Gut [Internet] 59(7):882\u2013887. Available from: https:\/\/www.gut.bmj.com\/cgi\/doi\/10.1136\/gut.2009.200444","DOI":"10.1136\/gut.2009.200444"},{"key":"4069_CR3","doi-asserted-by":"publisher","unstructured":"Stewart CL, Kulungowski AM, Tong S, Langer JC, Soden J, S\u00f8mme S (2016) Rectal biopsies for Hirschsprung disease: patient characteristics by diagnosis and attending specialty. J Pediatr Surg [Internet]. 51(4):573\u2013576. Available from: https:\/\/doi.org\/10.1016\/j.jpedsurg.2015.10.047","DOI":"10.1016\/j.jpedsurg.2015.10.047"},{"issue":"9","key":"4069_CR4","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1007\/s00383-015-3742-8","volume":"31","author":"F Friedmacher","year":"2015","unstructured":"Friedmacher F, Puri P (2015) Rectal suction biopsy for the diagnosis of Hirschsprung\u2019s disease: a systematic review of diagnostic accuracy and complications. Pediatr Surg Int 31(9):821\u2013830","journal-title":"Pediatr Surg Int"},{"key":"4069_CR5","doi-asserted-by":"crossref","unstructured":"Tabbers MM, DiLorenzo C, Berger MY, Faure C, Langendam MW, Nurko S, Staiano A, Vandenplas Y, Benninga MA\u00a0(2014)\u00a0Evaluation and treatment of functional constipation in infants and children: evidence-based recommendations from ESPGHAN and NASPGHAN. J Pediatr Gastroenterol Nutr 58(2):258\u2013274","DOI":"10.1097\/MPG.0000000000000266"},{"key":"4069_CR6","doi-asserted-by":"crossref","unstructured":"National Institute for Health and Care Excellence (NICE) (2019) The Grants Register\u00a0p 540\u2013540","DOI":"10.1007\/978-1-349-94186-5_836"},{"key":"4069_CR7","doi-asserted-by":"crossref","unstructured":"Langer JC (2013) Hirschsprung disease. Curr Opin Pediatr [Internet] [cited 2018 May 16];25(3):368\u2013374. Available from: http:\/\/content.wkhealth.com\/linkback\/openurl?sid=WKPTLP:landingpage&an=00008480-201306000-00015","DOI":"10.1097\/MOP.0b013e328360c2a0"},{"key":"4069_CR8","doi-asserted-by":"crossref","unstructured":"Lewis NA, Levitt MA, Zallen GS, Zafar MS, Iacono KL, Rossman JE, Caty MG, Glick PL (2003)\u00a0Diagnosing Hirschsprung\u2019s disease: increasing the odds of a positive rectal biopsy result. J Pediatr Surg [Internet]\u00a0[cited 2019 May 10];38(3):412\u2013416; discussion 412\u2013416. Available from: https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0022346802630787","DOI":"10.1053\/jpsu.2003.50070"},{"key":"4069_CR9","doi-asserted-by":"crossref","unstructured":"Amiel J, Sproat-Emison E, Garcia-Barcelo M, Lantieri F, Burzynski G, Borrego S et al (2008) Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet 45(1):1\u201314","DOI":"10.1136\/jmg.2007.053959"},{"key":"4069_CR10","unstructured":"Cole SZ, Lanham JS (2011) Failure to thrive: an update. Am Fam Physician 83(7):829\u2013834"},{"key":"4069_CR11","doi-asserted-by":"publisher","unstructured":"Rao SSC, Bharucha AE, Chiarioni G, Felt-Bersma R, Knowles C, Malcolm A et al (2016) Anorectal disorders. Gastroenterology [Internet] 150(6):1430\u20131442.e4. Available from: https:\/\/doi.org\/10.1053\/j.gastro.2016.02.009","DOI":"10.1053\/j.gastro.2016.02.009"},{"key":"4069_CR12","doi-asserted-by":"crossref","unstructured":"Boccia G, Manguso F, Coccorullo P, Masi P, Pensabene L, Staiano A (2007) Functional defecation disorders in children: PACCT criteria versus Rome II criteria. J Pediatr 151(4)","DOI":"10.1016\/j.jpeds.2007.04.011"},{"key":"4069_CR13","doi-asserted-by":"crossref","unstructured":"Muise ED, Hardee S, Morotti RA, Cowles RA (2016) A comparison of suction and full-thickness rectal biopsy in children. J Surg Res [Internet] 201(1):149\u2013155. Available from: https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0022480415010173","DOI":"10.1016\/j.jss.2015.10.031"},{"key":"4069_CR14","doi-asserted-by":"crossref","unstructured":"Friedmacher F, Puri P (2016) Current practice patterns of rectal suction biopsy in the diagnostic work-up of Hirschsprung\u2019s disease: results from an international survey. Pediatr Surg Int [Internet] 32(8):717\u2013722. Available from: https:\/\/www.link.springer.com\/10.1007\/s00383-016-3907-0","DOI":"10.1007\/s00383-016-3907-0"},{"key":"4069_CR15","doi-asserted-by":"publisher","unstructured":"Weber F, Knapp G (2020) Zero-cell corrections in random-effects meta-analyses. Available from: https:\/\/doi.org\/10.31219\/osf.io\/qjh5f","DOI":"10.31219\/osf.io\/qjh5f"},{"issue":"20","key":"4069_CR16","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1111\/j.1469-1809.1955.tb01285.x","volume":"1956","author":"HALDANE BJBS,","year":"1956","unstructured":"Jb H (1965) The estimation and significance of the logarithm of a ratio of frequencies. Ann Hum Genet (20):309\u2013311","journal-title":"Ann Hum Genet"},{"key":"4069_CR17","doi-asserted-by":"crossref","unstructured":"Anscombe F (1956) On Estimating Binomial Response Relations. Biometrika 43(3\/4):4","DOI":"10.2307\/2332926"},{"key":"4069_CR18","doi-asserted-by":"crossref","unstructured":"Backeljauw B, Holland SK, Altaye M, Loepke AW (2015) Cognition and brain structure following early childhood surgery with anesthesia. Pediatrics [Internet] 136(1):e1\u201312. Available from: https:\/\/www.pediatrics.aappublications.org\/cgi\/doi\/10.1542\/peds.2014-3526","DOI":"10.1542\/peds.2014-3526"},{"key":"4069_CR19","doi-asserted-by":"publisher","unstructured":"Ari A Ben, Peri T, Margalit D, Galili-Weisstub E, Udassin R, Benarroch F (2018) Surgical procedures and pediatric medical traumatic stress (PMTS) syndrome: Assessment and future directions. J Pediatr Surg [Internet] 53(8):1526\u20131531. Available from: https:\/\/doi.org\/10.1016\/j.jpedsurg.2017.10.043","DOI":"10.1016\/j.jpedsurg.2017.10.043"},{"issue":"4","key":"4069_CR20","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1093\/jpepsy\/jsj054","volume":"31","author":"AE Kazak","year":"2006","unstructured":"Kazak AE, Kassam-Adams N, Schneider S, Zelikovsky N, Alderfer MA, Rourke M (2006) An integrative model of pediatric medical traumatic stress. J Pediatr Psychol 31(4):343\u2013355","journal-title":"J Pediatr Psychol"},{"key":"4069_CR21","unstructured":"Badner JA, Sieber WK, Garver KL, Chakravarti A (1990) A genetic study of Hirschsprung disease. https:\/\/www.file\/\/\/Users\/emiliegimnesjaroy\/Desktop\/noviello.pdf. Am J Hum Genet 46(3):568\u2013580"},{"issue":"8","key":"4069_CR22","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1136\/archdischild-2016-311872","volume":"102","author":"TJ Bradnock","year":"2017","unstructured":"Bradnock TJ, Knight M, Kenny S, Nair M, Walker GM (2017) Hirschsprung\u2019s disease in the UK and Ireland: Incidence and anomalies. Arch Dis Child 102(8):722\u2013727","journal-title":"Arch Dis Child"},{"key":"4069_CR23","doi-asserted-by":"crossref","unstructured":"Tan YW, Chacon CS, Sherwood W, Haddad M, Choudhry M (2021) A critical analysis of rectal biopsy to exclude Hirschsprung\u2019s disease. Eur J Pediatr Surg","DOI":"10.1055\/s-0041-1722858"},{"issue":"4","key":"4069_CR24","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1007\/s00383-002-0842-z","volume":"19","author":"SJ Singh","year":"2003","unstructured":"Singh SJ, Croaker GDH, Manglick P, Wong CL, Athanasakos H, Elliott E et al (2003) Hirschsprung\u2019s disease: the Australian Paediatric Surveillance Unit\u2019s experience. Pediatr Surg Int 19(4):247\u2013250","journal-title":"Pediatr Surg Int"},{"issue":"2","key":"4069_CR25","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1055\/s-0029-1241820","volume":"20","author":"N Rahman","year":"2010","unstructured":"Rahman N, Chouhan J, Gould S, Joseph V, Grant H, Hitchcock R et al (2010) Rectal biopsy for Hirschsprung\u2019s disease - are we performing too many?. Eur J Pediatr Surg 20(2):95\u201397","journal-title":"Eur J Pediatr Surg"},{"issue":"1","key":"4069_CR26","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1055\/s-0038-1675771","volume":"29","author":"LAF Phillips","year":"2019","unstructured":"Phillips LAF, Darwish AA, Surana R (2019) Too many biopsies performed to rule out hirschsprung\u2019s disease: but It is worth doing them. Eur J Pediatr Surg 29(1):97\u2013101","journal-title":"Eur J Pediatr Surg"},{"issue":"10","key":"4069_CR27","doi-asserted-by":"publisher","first-page":"1044","DOI":"10.1111\/j.1463-1318.2009.01940.x","volume":"12","author":"C Noviello","year":"2010","unstructured":"Noviello C, Cobellis G, Romano M, Amici G, Martino A (2010) Diagnosis of Hirschsprung\u2019s disease: an age-related approach in children below or above one year. Colorectal Dis 12(10):1044\u20131048","journal-title":"Colorectal Dis"},{"issue":"1","key":"4069_CR28","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1186\/s13023-020-01362-3","volume":"15","author":"K Kyrklund","year":"2020","unstructured":"Kyrklund K, Sloots CEJ, de Blaauw I, Bj\u00f8rnland K, Rolle U, Cavalieri D et al (2020) ERNICA guidelines for the management of rectosigmoid Hirschsprung\u2019s disease. Orphanet J Rare Dis 15(1):164","journal-title":"Orphanet J Rare Dis"},{"key":"4069_CR29","doi-asserted-by":"publisher","unstructured":"KRAMER SN I (1955) The time of passage of the first stool and first urine by the newborn infant. J Pediatr 46(2):158\u20139. https:\/\/doi.org\/10.1016\/s0022-3476(55)80205-3. PMID: 13234010.","DOI":"10.1016\/s0022-3476(55)80205-3"},{"key":"4069_CR30","doi-asserted-by":"crossref","unstructured":"Jung PM (1995) Hirschsprung\u2019s disease: one surgeon\u2019s experience in one institution. J Pediatr Surg [Internet] 30(5):646\u201351. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/7623218","DOI":"10.1016\/0022-3468(95)90680-0"},{"key":"4069_CR31","doi-asserted-by":"publisher","unstructured":"Mugie SM, Benninga MA, Di Lorenzo C (2011) Epidemiology of constipation in children and adults: a systematic review. Best Pract Res Clin Gastroenterol [Internet] 25(1):3\u201318. Available from: https:\/\/doi.org\/10.1016\/j.bpg.2010.12.010","DOI":"10.1016\/j.bpg.2010.12.010"},{"issue":"3","key":"4069_CR32","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1097\/MPG.0000000000000209","volume":"58","author":"R Turco","year":"2014","unstructured":"Turco R, Miele E, Russo M, Mastroianni R, Lavorgna A, Paludetto R et al (2014) Early-life factors associated with pediatric functional constipation. J Pediatr Gastroenterol Nutr 58(3):307\u2013312","journal-title":"J Pediatr Gastroenterol Nutr"},{"issue":"1","key":"4069_CR33","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1016\/S0031-3955(05)70406-5","volume":"43","author":"V Loening-Baucke","year":"1996","unstructured":"Loening-Baucke V (1996) Encopresis and soiling. Pediatr Clin North Am 43(1):279\u2013298","journal-title":"Pediatr Clin North Am"},{"issue":"2","key":"4069_CR34","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1007\/s00383-006-1845-y","volume":"23","author":"A Pini-Prato","year":"2007","unstructured":"Pini-Prato A, Avanzini S, Gentilino V, Martucciello G, Mattioli G, Coccia C et al (2007) Rectal suction biopsy in the workup of childhood chronic constipation: indications and diagnostic value. Pediatr Surg Int 23(2):117\u2013122","journal-title":"Pediatr Surg Int"},{"key":"4069_CR35","doi-asserted-by":"crossref","unstructured":"Friedmacher F, Puri P (2013) Hirschsprung\u2019s disease associated with Down syndrome: a meta-analysis of incidence, functional outcomes and mortality. Pediatr Surg Int [Internet] 29(9):937\u2013946. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/23943251","DOI":"10.1007\/s00383-013-3361-1"},{"key":"4069_CR36","doi-asserted-by":"publisher","unstructured":"Jaroy EG, Acosta-Jimenez L, Hotta R, Goldstein AM, Emblem R, Klungland A et al (2019) Too much guts and not enough brains: (epi)genetic mechanisms and future therapies of Hirschsprung disease \u2014 a review. Clin Epigenetics [Internet] 11(1):135. Available from: https:\/\/doi.org\/10.1186\/s13148-019-0718-x","DOI":"10.1186\/s13148-019-0718-x"},{"issue":"1","key":"4069_CR37","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1055\/s-0035-1566099","volume":"26","author":"CMG Keyzer-Dekker","year":"2015","unstructured":"Keyzer-Dekker CMG, Sloots CE, Van Linschoten IKS, Biermann K, Meeussen C, Doukas M (2015) Effectiveness of rectal suction biopsy in diagnosing Hirschsprung disease. Eur J Pediatr Surg 26(1):100\u2013105","journal-title":"Eur J Pediatr Surg"}],"container-title":["International Journal of Colorectal Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00384-021-04069-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00384-021-04069-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00384-021-04069-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,28]],"date-time":"2022-02-28T08:10:29Z","timestamp":1646035829000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00384-021-04069-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,9]]},"references-count":37,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2022,3]]}},"alternative-id":["4069"],"URL":"https:\/\/doi.org\/10.1007\/s00384-021-04069-4","relation":{},"ISSN":["0179-1958","1432-1262"],"issn-type":[{"value":"0179-1958","type":"print"},{"value":"1432-1262","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,9]]},"assertion":[{"value":"18 November 2021","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 December 2021","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study was approved by the Oslo University Hospital\u2019s Commission for Personal Security, no 18\/21406.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}