Intestinal Predictors of Whole Blood Serotonin Levels in Children With or Without Autism.


Journal

Journal of autism and developmental disorders
ISSN: 1573-3432
Titre abrégé: J Autism Dev Disord
Pays: United States
ID NLM: 7904301

Informations de publication

Date de publication:
Sep 2022
Historique:
accepted: 27 04 2022
pubmed: 22 6 2022
medline: 6 8 2022
entrez: 21 6 2022
Statut: ppublish

Résumé

Hyperserotonemia, or elevated levels of whole blood serotonin (WB5-HT), was the first biomarker linked to autism spectrum disorder (ASD). Despite numerous studies investigating the etiology of hyperserotonemia, results have been inconsistent. Recent findings suggest a relationship between the immune system and hyperserotonemia. The current study investigated whether intestinal 5-HT levels, 5-HT gene expression, or intestinal cell types predict WB5-HT. Participants included thirty-one males aged 3-18 who were classified into one of three groups: ASD and functional GI issues, typically developing with GI issues, and typically developing without GI issues. Samples from a lower endoscopy were analyzed to examine the pathways in predicting WB-5HT. Results demonstrated an association between T-Lymphocytes and WB5-HT.

Identifiants

pubmed: 35726077
doi: 10.1007/s10803-022-05597-w
pii: 10.1007/s10803-022-05597-w
doi:

Substances chimiques

Biomarkers 0
Serotonin 333DO1RDJY

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3780-3789

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Amireault, P., et al. (2013). Serotonin is a key factor for mouse red blood cell survival. PLoS ONE, 8, e83010. https://doi.org/10.1371/journal.pone.0083010
doi: 10.1371/journal.pone.0083010 pubmed: 24358245 pmcid: 3866204
Anderson, G. M., Feibel, F. C., & Cohen, D. J. (1987a). Determination of serotonin in whole blood, platelet-rich plasma, platelet-poor plasma and plasma ultrafiltrate. Life Science, 40(11), 1063–1070. https://doi.org/10.1016/0024-3205(87)90568-6
doi: 10.1016/0024-3205(87)90568-6
Anderson, G. M., Freedman, D. X., et al. (1987b). Whole blood serotonin in autistic and normal subjects. Journal of Child Psychology and Psychiatry, 28, 885–900. https://doi.org/10.1111/j.1469-7610.1987.tb00677
doi: 10.1111/j.1469-7610.1987.tb00677 pubmed: 3436995
Anderson, G. M., Stevenson, J. M., & Cohen, D. J. (1987). Steady-state model for plasma free and platelet serotonin in man. Life Sciences, 41(15), 1777–1785. https://doi.org/10.1016/0024-3205(87)90696-5
doi: 10.1016/0024-3205(87)90696-5 pubmed: 3657383
Antoun, S., Ellul, P., Peyre, H., Rosenzwajg, M., Gressens, P., Klatzmann, D., & Delorme, R. (2021). Fever during pregnancy as a risk factor for neurodevelopmental disorders: Results from a systematic review and meta-analysis. Molecular Autism, 12(1), 60. https://doi.org/10.1186/s13229-021-00464-4
doi: 10.1186/s13229-021-00464-4 pubmed: 34537069 pmcid: 8449704
Aune, T., Golden, H. W., & McGrath, K. M. (1994). Inhibitors of serotonin synthesis and antagonists of serotonin 1A receptors inhibit T lymphocyte function in vitro and cell-mediated immunity in vivo. Journal of Immunology, 153, 1.
Baganz, N. L., & Blakely, R. D. (2013). A dialogue between the immune system and brain, spoken in the language of serotonin. ACS Chemical Neuroscience, 4(1), 48–63. https://doi.org/10.1021/cn300186b
doi: 10.1021/cn300186b pubmed: 23336044
Baganz, N. L., Lindler, K. M., Zhu, C. B., Smith, J. T., Robson, M. J., Iwamoto, H., Deneris, E. S., Hewlett, W. A., & Blakely, R. D. (2015). A requirement of serotonergic p38α mitogen-activated protein kinase for peripheral immune system activation of CNS serotonin uptake and serotonin-linked behaviors. Translational Psychiatry, 5(11), e671. https://doi.org/10.1038/tp.2015.168
doi: 10.1038/tp.2015.168 pubmed: 26529424 pmcid: 5068761
Black, C., Kaye, J. A., Jick, H.: Relation of childhood gastrointestinal disorders to autism: Nested case-control study using data from the UK General Practice Research Database. BMJ, 325, 419–421 (2202)
Chaidez, V., Hansen, R. L., & Hertz-Picciotto, I. (2014). Gastrointestinal problems in children with autism, developmental delays or typical development. Journal of Autism and Developmental Disorders, 44, 1117–1127. https://doi.org/10.1007/s10803-013-1973-x
doi: 10.1007/s10803-013-1973-x pubmed: 24193577 pmcid: 3981895
Cook, E. H., Jr., Leventhal, B. L., & Freedman, D. X. (1988). Free serotonin in plasma: Autistic children and their first-degree relatives. Biological Psychiatry, 24, 488–491. https://doi.org/10.1016/0006-3223(88)90192-8
doi: 10.1016/0006-3223(88)90192-8 pubmed: 3408767
Cross, S., et al. (2008). Molecular genetics of the platelet serotonin system in first-degree relatives of patients with autism. Neuropsychopharmacology, 33, 353–360. https://doi.org/10.1038/sj.npp.1301406
doi: 10.1038/sj.npp.1301406 pubmed: 17406648
de Magistris, L., et al. (2010). Alterations of the intestinal barrier in patients with autism spectrum disorders and in their first-degree relatives. Journal of Pediatric Gastroenterology and Nutrition, 51, 418–424. https://doi.org/10.1097/MPG.0b013e3181dcc4a5
doi: 10.1097/MPG.0b013e3181dcc4a5 pubmed: 20683204
Ferguson, B. J., et al. (2019). Lack of associations between dietary intake and gastrointestinal symptoms in autism spectrum disorder. Front Psychiatry, 10, 528. https://doi.org/10.3389/fpsyt.2019.00528
doi: 10.3389/fpsyt.2019.00528 pubmed: 31402878 pmcid: 6669230
Franke, L., Schmidtmann, M., Riedl, A., van der Voort, I., Uebelhack, R., & Mönnikes, H. (2009). Serotonin transporter activity and serotonin concentration in platelets of patients with irritable bowel syndrome: Effect of gender. Journal of Gastroenterology, 45(4), 389–398. https://doi.org/10.1007/s00535-009-0167-y
doi: 10.1007/s00535-009-0167-y pubmed: 19997855
Gabriele, S., Sacco, R., & Persico, A. M. (2014). Blood serotonin levels in autism spectrum disorder: A systematic review and meta-analysis. European Neuropsychopharmacology, 24, 919–929. https://doi.org/10.1016/j.euroneuro.2014.02.004
doi: 10.1016/j.euroneuro.2014.02.004 pubmed: 24613076
Gershon, M. D. (2013). 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Current Opinion in Endocrinology, Diabetes, and Obesity, 20, 14–21. https://doi.org/10.1097/MED.0b013e32835bc703
doi: 10.1097/MED.0b013e32835bc703 pubmed: 23222853 pmcid: 3708472
Gershon, M. D., & Tack, J. (2007). The serotonin signaling system: From basic understanding to drug development for functional GI disorders. Gastroenterology, 132, 397–414. https://doi.org/10.1053/j.gastro.2006.11.002
doi: 10.1053/j.gastro.2006.11.002 pubmed: 17241888
Heid, C. A., Stevens, J., & Livak., K. (1996). Real time quantitative PCR. Genome research. Retrieved February 3, 2022, from https://pubmed.ncbi.nlm.nih.gov/8908518/
Holingue, C., Newill, C., Lee, L. C., Pasricha, P. J., & Daniele Fallin, M. (2018). Gastrointestinal symptoms in autism spectrum disorder: A review of the literature on ascertainment and prevalence. Autism Research, 11, 24–36. https://doi.org/10.1002/aur.1854
doi: 10.1002/aur.1854 pubmed: 28856868
Hranilovic, D., Bujas-Petkovic, Z., Vragovic, R., Vuk, T., Hock, K., & Jernej, B. (2007). Hyperserotonemia in adults with autistic disorder. Journal of Autism and Developmental Disorders, 37, 1934–1940. https://doi.org/10.1007/s10803-006-0324-6
doi: 10.1007/s10803-006-0324-6 pubmed: 17165147
Hsiao, E. Y. (2014). Gastrointestinal issues in autism spectrum disorder. Harvard Review of Psychiatry, 22(2), 104–111. https://doi.org/10.1097/HRP.0000000000000029
doi: 10.1097/HRP.0000000000000029 pubmed: 24614765
Hsiao, E. Y., et al. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155, 1451–1463. https://doi.org/10.1016/j.cell.2013.11.024
doi: 10.1016/j.cell.2013.11.024 pubmed: 24315484 pmcid: 3897394
Hughes, H. K., Mills Ko, E., Rose, D., & Ashwood, P. (2018). Immune dysfunction and autoimmunity as pathological mechanisms in autism spectrum disorders. Frontiers in Cellular Neuroscience, 12, 405. https://doi.org/10.3389/fncel.2018.00405
doi: 10.3389/fncel.2018.00405 pubmed: 30483058 pmcid: 6242891
Israelyan, N., & Margolis, K. G. (2018). Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders. Pharmacological Research, 132, 1–6. https://doi.org/10.1016/j.phrs.2018.03.020
doi: 10.1016/j.phrs.2018.03.020 pubmed: 29614380 pmcid: 6368356
Jiang, H. Y., Xu, L. L., Shao, L., Xia, R. M., Yu, Z. H., Ling, Z. X., Yang, F., Deng, M., & Ruan, B. (2016). Maternal infection during pregnancy and risk of autism spectrum disorders: A systematic review and meta-analysis. Brain, Behavior, and Immunity, 58, 165–172. https://doi.org/10.1016/j.bbi.2016.06.005
doi: 10.1016/j.bbi.2016.06.005 pubmed: 27287966
Kema, I. P., de Vries, E. G., & Muskiet, F. A. (2000). Clinical chemistry of serotonin and metabolites. Journal of Chromatography B: Biomedical Sciences and Applications, 747(1–2), 33–48. https://doi.org/10.1016/s0378-4347(00)00341-8
doi: 10.1016/s0378-4347(00)00341-8 pubmed: 11103898
León-Ponte, M., Ahern, G. P., & O’Connell, P. J. (2007). Serotonin provides an accessory signal to enhance T-cell activation by signaling through the 5-HT7 receptor. Blood, 109, 3139–3146. https://doi.org/10.1182/blood-2006-10-052787
doi: 10.1182/blood-2006-10-052787 pubmed: 17158224 pmcid: 1852236
Li, Q., Han, Y., Dy, A. B. C., & Hagerman, R. J. (2017). The gut microbiota and autism spectrum disorders. Frontiers in Cellular Neuroscience, 11, 120. https://doi.org/10.3389/fncel.2017.00120
doi: 10.3389/fncel.2017.00120 pubmed: 28503135 pmcid: 5408485
Lord, C., et al. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205–223.
doi: 10.1023/A:1005592401947
Luna, R. A., et al. (2017). Distinct microbiome-neuroimmune signatures correlate with functional abdominal pain in children with autism spectrum disorder. Cellular and Molecular Gastroenterology and Hepatology, 3, 218–230. https://doi.org/10.1016/j.jcmgh.2016.11.008
doi: 10.1016/j.jcmgh.2016.11.008 pubmed: 28275689
Marler, S., Ferguson, B. J., Lee, E. B., Peters, B., Williams, K. C., McDonnell, E., Macklin, E. A., Levitt, P., Gillespie, C. H., Anderson, G. M., Margolis, K. G., Beversdorf, D. Q., & Veenstra-VanderWeele, J. (2015). Brief report: Whole blood serotonin levels and gastrointestinal symptoms in autism spectrum disorder. Journal of Autism and Developmental Disorders, 46(3), 1124–1130. https://doi.org/10.1007/s10803-015-2646-8
doi: 10.1007/s10803-015-2646-8
Masi, A., Quintana, D. S., Glozier, N., Lloyd, A. R., Hickie, I. B., & Guastella, A. J. (2015). Cytokine aberrations in autism spectrum disorder: A systematic review and meta-analysis. Molecular Psychiatry, 20(4), 440–446. https://doi.org/10.1038/mp.2014.59
doi: 10.1038/mp.2014.59 pubmed: 24934179
McBride, P. A., et al. (1998). Effects of diagnosis, race, and puberty on platelet serotonin levels in autism and mental retardation. Journal of the American Academy of Child and Adolescent Psychiatry, 37(7), 767–776. https://doi.org/10.1097/00004583-199807000-00017
doi: 10.1097/00004583-199807000-00017 pubmed: 9666633
McBride, P. A., et al. (1989). Serotonergic responsivity in male young adults with autistic disorder. Results of a pilot study. Archives of General Psychiatry, 46, 213–221. https://doi.org/10.1001/archpsyc.1989.01810030019003
doi: 10.1001/archpsyc.1989.01810030019003 pubmed: 2919950
Minderaa, R. B., Anderson, G. M., Volkmar, F. R., Akkerhuis, G. W., & Cohen, D. J. (1987). Urinary 5-hydroxyindoleacetic acid and whole blood serotonin and tryptophan in autistic and normal subjects. Biological Psychiatry, 22(8), 933–940. https://doi.org/10.1016/0006-3223(87)90002-3
doi: 10.1016/0006-3223(87)90002-3 pubmed: 2440483
Mulder, E. J., Anderson, G. M., Kema, I. P., de Bildt, A., van Lang, N. D., den Boer, J. A., & Minderaa, R. B. (2004). Platelet serotonin levels in pervasive developmental disorders and mental retardation: Diagnostic group differences, within-group distribution, and behavioral correlates. Journal of the American Academy of Child and Adolescent Psychiatry, 43(4), 491–499. https://doi.org/10.1097/00004583-200404000-00016
doi: 10.1097/00004583-200404000-00016 pubmed: 15187810
Mulder, E. J., Anderson, G. M., Kemperman, R. F., Oosterloo-Duinkerken, A., Minderaa, R. B., & Kema, I. P. (2010). Urinary excretion of 5-hydroxyindoleacetic acid, serotonin and 6-sulphatoxymelatonin in normoserotonemic and hyperserotonemic autistic individuals. Neuropsychobiology, 61(1), 27–32. https://doi.org/10.1159/000258640
doi: 10.1159/000258640 pubmed: 19923863
Muller, C. L., Anacker, A. M. J., & Veenstra-VanderWeele, J. (2016). The serotonin system in autism spectrum disorder: From biomarker to animal models. Neuroscience, 321, 24–41. https://doi.org/10.1016/j.neuroscience.2015.11.010
doi: 10.1016/j.neuroscience.2015.11.010 pubmed: 26577932
O’Mahony, S. M., Clarke, G., Borre, Y. E., Dinan, T. G., & Cryan, J. F. (2015). Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behavioural Brain Research, 277, 32–48. https://doi.org/10.1016/j.bbr.2014.07.027
doi: 10.1016/j.bbr.2014.07.027 pubmed: 25078296
Saghazadeh, A., Ataeinia, B., Keynejad, K., Abdolalizadeh, A., Hirbod-Mobarakeh, A., & Rezaei, N. (2019). A meta-analysis of pro-inflammatory cytokines in autism spectrum disorders: Effects of age, gender, and latitude. Journal of Psychiatric Research, 115, 90–102. https://doi.org/10.1016/j.jpsychires.2019.05.019
doi: 10.1016/j.jpsychires.2019.05.019 pubmed: 31125917
Schain, R. J., & Freedman, D. X. (1961). Studies on 5-hydroxyindole metabolism in autistic and other mentally retarded children. Journal of Pediatrics, 58, 315–320. https://doi.org/10.1016/s0022-3476(61)80261-8
doi: 10.1016/s0022-3476(61)80261-8 pubmed: 13747230
Shuffrey, L. C., et al. (2017). Is there sexual dimorphism of hyperserotonemia in autism spectrum disorder? Autism Research, 10, 1417–1423. https://doi.org/10.1002/aur.1791
doi: 10.1002/aur.1791 pubmed: 28401654 pmcid: 5568968
Tioleco, N., Silberman, A. E., Stratigos, K., Banerjee-Basu, S., Spann, M. N., Whitaker, A. H., & Turner, J. B. (2021). Prenatal maternal infection and risk for autism in offspring: A meta-analysis. Autism Research: Official Journal of the International Society for Autism Research, 14(6), 1296–1316. https://doi.org/10.1002/aur.2499
doi: 10.1002/aur.2499
Wikoff, W. R., et al. (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of National Academic Science of USA, 106, 3698–3703. https://doi.org/10.1073/pnas.0812874106
doi: 10.1073/pnas.0812874106
Yang, C. J., Liu, C. L., Sang, B., Zhu, X. M., & Du, Y. J. (2015). The combined role of serotonin and interleukin-6 as biomarker for autism. Neuroscience, 284, 290–296. https://doi.org/10.1016/j.neuroscience.2014.10.011
doi: 10.1016/j.neuroscience.2014.10.011 pubmed: 25453766
Zerbo, O., Qian, Y., Yoshida, C., Grether, J. K., Van de Water, J., & Croen, L. A. (2015). Maternal infection during pregnancy and autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(12), 4015–4025. https://doi.org/10.1007/s10803-013-2016-3
doi: 10.1007/s10803-013-2016-3 pubmed: 24366406 pmcid: 4108569

Auteurs

Miranda Zuniga-Kennedy (M)

Department of Psychiatry, Columbia University Medical Center, 1051 Riverside Drive, Mail Unit 78, New York, NY, 10032, USA.
New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY, 10032, USA.
Center for Autism and the Developing Brain, New York-Presbyterian Hospital, 21 Bloomingdale Road, White Plains, NY, 10605, USA.

Micah Davoren (M)

Department of Psychiatry, Columbia University Medical Center, 1051 Riverside Drive, Mail Unit 78, New York, NY, 10032, USA.
New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY, 10032, USA.
Center for Autism and the Developing Brain, New York-Presbyterian Hospital, 21 Bloomingdale Road, White Plains, NY, 10605, USA.

Lauren C Shuffrey (LC)

Department of Psychiatry, Columbia University Medical Center, 1051 Riverside Drive, Mail Unit 78, New York, NY, 10032, USA.
New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY, 10032, USA.

Ruth Ann Luna (RA)

Department of Pathology and Immunology, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Department of Pathology, Texas Children's Microbiome Center, Texas Children's Hospital, 1102 Bates Avenue, Suite 955, Houston, TX, 77030, USA.

Tor Savidge (T)

Department of Pathology and Immunology, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Department of Pathology, Texas Children's Microbiome Center, Texas Children's Hospital, 1102 Bates Avenue, Suite 955, Houston, TX, 77030, USA.

Vinay Prasad (V)

Division of Pathology, Nationwide Children's Hospital, 700 Children's Drive, Columbus, OH, 43205, USA.

George M Anderson (GM)

Departments of Child Psychiatry and Laboratory Medicine, Yale University School of Medicine, New Haven, CT, 06510, USA.

Jeremy Veenstra-VanderWeele (J)

Department of Psychiatry, Columbia University Medical Center, 1051 Riverside Drive, Mail Unit 78, New York, NY, 10032, USA. Jeremy.veenstra-vanderweele@nyspi.columbia.edu.
New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY, 10032, USA. Jeremy.veenstra-vanderweele@nyspi.columbia.edu.
Center for Autism and the Developing Brain, New York-Presbyterian Hospital, 21 Bloomingdale Road, White Plains, NY, 10605, USA. Jeremy.veenstra-vanderweele@nyspi.columbia.edu.
, 1051 Riverside Drive, Mail Unit 78, New York, NY, 10025, USA. Jeremy.veenstra-vanderweele@nyspi.columbia.edu.

Kent C Williams (KC)

Department of Pediatric Gastroenterology, Nationwide Children's Hospital, 555 S 18th Street, Columbus, OH, 43205, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH