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08-12-2023 | Anorexia Nervosa | Original Article

Structure–function relationship of the pituitary gland in anorexia nervosa and intense physical activity

Authors: Manel Merabet, Natacha Germain, Jérôme Redouté, Claire Boutet, Nicolas Costes, Maurice Ptito, Bogdan Galusca, Fabien C. Schneider

Published in: Brain Structure and Function | Issue 1/2024

Abstract

Patients with Anorexia Nervosa (AN) and athletes share intense physical activity and pituitary hormonal disturbances related to absolute (AN) or relative (athletes) undernutrition. Pituitary gland (PG) structure evaluations in those conditions are scarce, and did not differentiate anterior from posterior lobe. We evaluated the structure–function relationship of anterior and posterior PG in AN and athletes, and potential reversibility of this alteration in a group of weight-recovered patients (AN_Rec). Manual delineation of anterior (AP) and posterior (PP) PG was performed on T1-weighted MR images in 17 women with AN, 15 women with AN_Rec, 18 athletes women and 25 female controls. Anthropometric, hormonal, and psychometric parameters were explored and correlated with PG volumes. AP volume (APV) was lower in AN (448 ± 82 mm³), AN_Rec (505 ± 59 mm³), and athletes (540 ± 101 mm³) vs. Controls (615 ± 61 mm³, p < 0.00001, p < 0.00001 and p = 0.02, respectively); and smaller in AN vs. AN_Rec (p = 0.007). PP volume did not show any differences between the groups. APV was positively correlated with weight (R = 0.36, p = 0.011) in AN, and luteinizing hormone (R = 0.35, p = 0.014) in total group. In AN, mean growth hormone (GH) was negatively correlated with global pituitary volume (R = 0.31, p = 0.031) and APV (R = 0.29, p = 0.037). Absolute and relative undernutrition led to a decreased anterior pituitary gland volume, which was reversible with weight gain, correlated with low bodyweight, and blockade of gonadal hypothalamic–pituitary axis. Intriguing inverse correlation between anterior pituitary gland volume and GH plasma level could suggests a low storage capacity of anterior pituitary gland and increased reactivity to low insulin-like growth factor type 1.

Allegre B, Therme P (2008) Confirmative study of a French version of the Exercise Dependence Scale-revised with a French population. Encephale 34(5):490–495. https://doi.org/10.1016/j.encep.2007.08.004CrossRefPubMed

Anastassiadis C, Jones SL, Pruessner JC (2019) Imaging the pituitary in psychopathologies: a review of in vivo magnetic resonance imaging studies. Brain Struct Funct 224:2587–2601CrossRefPubMed

Argente J, Caballo N, Barrios V, Munoz M, Pozo J, Chowen J, Morande G, Hernandez M (1997) Multiple endocrine abnormalities of the growth hormone and insulin-like growth factor axis in patients with anorexia nervosa: effect of short-and long-term weight recuperation. J Clin Endocrinol Metab 82(7):2084–2092PubMed

Baranowska B, Kochanowski J (2018) Neuroendocrine aspects of anorexia nervosa and bulimia nervosa. Neuro Endocrinol Lett 39(3):172–178PubMed

Barbarich-Marsteller NC, Foltin RW, Walsh BT (2011) Does anorexia nervosa resemble an addiction? Curr Drug Abuse Rev 4(3):197–200. https://doi.org/10.2174/1874473711104030197CrossRefPubMedPubMedCentral

Bozkurt Koseoglu S, Dinc Elibol F (2018) Does the pituitary gland volume change in polycystic ovary syndrome? Gynecol Obstet Invest 83(5):515–519CrossRefPubMed

Call C, Walsh BT, Attia E (2013) From DSM-IV to DSM-5: changes to eating disorder diagnoses. Curr Opin Psychiatry 26(6):532–536. https://doi.org/10.1097/YCO.0b013e328365a321CrossRefPubMed

Castellano AK, Powell JR, Cools MJ, Walton SR, Barnett RR, Delellis SM, Goldberg RL, Kane SF, Means GE, Zamora CA, Depenbrock PJ, Mihalik JP (2022) Relationship between anterior pituitary volume and IGF-1 serum levels in soldiers with mild traumatic brain injury history. Med Sci Sports Exerc 54(8):1364–1370. https://doi.org/10.1249/mss.0000000000002892CrossRefPubMedPubMedCentral

Delvecchio G, Mandolini GM, Perlini C, Barillari M, Marinelli V, Ruggeri M, Altamura AC, Bellani M, Brambilla P (2018) Pituitary gland shrinkage in bipolar disorder: the role of gender. Compr Psychiatry 82:95–99CrossRefPubMed

Dipla K, Kraemer RR, Constantini NW, Hackney AC (2021) Relative energy deficiency in sports (RED-S): elucidation of endocrine changes affecting the health of males and females. Hormones (athens) 20(1):35–47. https://doi.org/10.1007/s42000-020-00214-wCrossRefPubMed

Domoff SE, Meers MR, Koball AM, Musher-Eizenman DR (2014) The validity of the Dutch Eating Behavior Questionnaire: some critical remarks. Eat Weight Disord 19(2):137–144. https://doi.org/10.1007/s40519-013-0087-yCrossRefPubMed

Doraiswamy PM, Krishnan KR, Figiel GS, Husain MM, Boyko OB, Rockwell WJ, Ellinwood EH Jr (1990) A brain magnetic resonance imaging study of pituitary gland morphology in anorexia nervosa and bulimia. Biol Psychiatry 28(2):110–116. https://doi.org/10.1016/0006-3223(90)90628-fCrossRefPubMed

Estour B, Pugeat M, Lang F, Lejeune H, Broutin F, Pellet J, Rousset H, Tourniaire J (1990) Rapid escape of cortisol from suppression in response to i.v. dexamethasone in anorexia nervosa. Clin Endocrinol (oxf) 33(1):45–52CrossRefPubMed

Estour B, Germain N, Diconne E, Frere D, Cottet-Emard JM, Carrot G, Lang F, Galusca B (2010) Hormonal profile heterogeneity and short-term physical risk in restrictive anorexia nervosa. J Clin Endocrinol Metab 95(5):2203–2210CrossRefPubMed

Fehrenbach U, Jadan A, Auer TA, Kreutz K, Geisel D, Ziagaki A, Bobbert T, Wiener E (2020) Obesity and pituitary gland volume—a correlation study using three-dimensional magnetic resonance imaging. Neuroradiol J 33(5):400–409CrossRefPubMedPubMedCentral

Fink A, Vidmar S, Kumbla S, Pedreira C, Kanumakala S, Williams C, Carlin J, Cameron F (2005) Age-related pituitary volumes in prepubertal children with normal endocrine function: volumetric magnetic resonance data. J Clin Endocrinol Metab 90(6):3274–3278CrossRefPubMed

Frankel RJ, Jenkins JS (1975) Hypothalamic-pituitary function in anorexia nervosa. Acta Endocrinol (copenh) 78(2):209–221. https://doi.org/10.1530/acta.0.0780209CrossRefPubMed

Frohman LA, Kineman RD (2002) Growth hormone-releasing hormone and pituitary development, hyperplasia and tumorigenesis. Trends Endocrinol Metab 13(7):299–303CrossRefPubMed

Fujisawa I, Asato R, Nishimura K, Togashi K, Itoh K, Nakano Y, Itoh H, Hashimoto N, Takeuchi J, Torizuka K (1987) Anterior and posterior lobes of the pituitary gland: assessment by 1.5 T MR imaging. J Comput Assist Tomogr 11(2):214–220CrossRefPubMed

Galusca B, Bossu C, Germain N, Kadem M, Frere D, Lafage-Proust MH, Lang F, Estour B (2006) Age-related differences in hormonal and nutritional impact on lean anorexia nervosa bone turnover uncoupling. Osteoporos Int 17(6):888–896CrossRefPubMed

Germain N, Genteuil CD, Belleton G, Da Silva TL, Exbrayat C, Degas F, Hammour A, Gay A, Ravey B, Massoubre C (2023) Continuous glucose monitoring assessment in patients suffering from anorexia nervosa reveals chronic prolonged mild hypoglycemia all over the nycthemeron. Eur Eat Disord Rev 31(3):402–412CrossRefPubMed

Gianotti L, Lanfranco F, Ramunni J, Destefanis S, Ghigo E, Arvat E (2002) GH/IGF-I axis in anorexia nervosa. Eat Weight Disord Stud Anorexia Bulimia Obes 7:94–105CrossRef

Golden NH, Kreitzer P, Jacobson MS, Chasalow FI, Schebendach J, Freedman SM, Shenker IR (1994) Disturbances in growth hormone secretion and action in adolescents with anorexia nervosa. J Pediatr 125(4):655–660CrossRefPubMed

Grams AE, Gempt J, Stahl A, Förschler A (2010) Female pituitary size in relation to age and hormonal factors. Neuroendocrinology 92(2):128–132CrossRefPubMed

Guemmer R, Giel KE, Schag K, Resmark G, Junne FP, Becker S, Zipfel S, Teufel M (2015) High levels of physical activity in anorexia nervosa: a systematic review. Eur Eat Disord Rev 23(5):333–344CrossRef

Herholz K (1996) Neuroimaging in anorexia nervosa. Psychiatry Res 62(1):105–110. https://doi.org/10.1016/0165-1781(96)02990-3CrossRefPubMed

Isambert A, Dhermain F, Bidault F, Commowick O, Bondiau P-Y, Malandain G, Lefkopoulos D (2008) Evaluation of an atlas-based automatic segmentation software for the delineation of brain organs at risk in a radiation therapy clinical context. Radiother Oncol 87(1):93–99CrossRefPubMed

Karaca Z, Laway BA, Dokmetas HS, Atmaca H, Kelestimur F (2016) Sheehan syndrome. Nat Rev Dis Prim 2(1):1–15

Karavitaki N (2017) Diagnosis of pituitary disease. Medicine 45(8):464–469CrossRef

Karin O, Raz M, Alon U (2021) An opponent process for alcohol addiction based on changes in endocrine gland mass. iScience 24(3):102127. https://doi.org/10.1016/j.isci.2021.102127CrossRefPubMedPubMedCentral

Kornreich L, Shapira A, Horev G, Danziger Y, Tyano S, Mimouni M (1991) CT and MR evaluation of the brain in patients with anorexia nervosa. Am J Neuroradiol 12(6):1213–1216PubMedPubMedCentral

Kraemer WJ, Ratamess NA (2005) Hormonal responses and adaptations to resistance exercise and training. Sports Med 35(4):339–361. https://doi.org/10.2165/00007256-200535040-00004CrossRefPubMed

Le Tissier P, Hodson D, Lafont C, Fontanaud P, Schaeffer M, Mollard P (2012) Anterior pituitary cell networks. Front Neuroendocrinol 33(3):252–266CrossRefPubMed

Lorenzetti V, Lubman DI, Velakoulis D, Yücel M (2010) Pituitary gland volume among heroin users stabilised on substitution pharmacotherapy. Drug Alcohol Depend 110(1–2):164–166. https://doi.org/10.1016/j.drugalcdep.2010.02.012CrossRefPubMed

Machado PPP, Grilo CM, Rodrigues TF, Vaz AR, Crosby RD (2020) Eating disorder examination—questionnaire short forms: a comparison. Int J Eat Disord 53(6):937–944. https://doi.org/10.1002/eat.23275CrossRefPubMed

Malsagova KA, Kopylov AT, Sinitsyna AA, Stepanov AA, Izotov AA, Butkova TV, Chingin K, Klyuchnikov MS, Kaysheva AL (2021) Sports nutrition: diets, selection factors, recommendations. Nutrients 13(11):3771. https://doi.org/10.3390/nu13113771CrossRefPubMedPubMedCentral

Maya J, Misra M (2022) The female athlete triad: review of current literature. Curr Opin Endocrinol Diabetes Obes 29(1):44–51CrossRefPubMedPubMedCentral

Misra M, Klibanski A (2014) Endocrine consequences of anorexia nervosa. Lancet Diabetes Endocrinol 2(7):581–592. https://doi.org/10.1016/s2213-8587(13)70180-3CrossRefPubMedPubMedCentral

Monteleone P, Di Lieto A, Tortorella A, Longobardi N, Maj M (2000) Circulating leptin in patients with anorexia nervosa, bulimia nervosa or binge-eating disorder: relationship to body weight, eating patterns, psychopathology and endocrine changes. Psychiatry Res 94(2):121–129CrossRefPubMed

Moshang T Jr, Parks JS, Baker L, Vaidya V, Utiger RD, Bongiovanni AM, Snyder PJ (1975) Low serum triiodothyronine in patients with anorexia nervosa. J Clin Endocrinol Metab 40(3):470–473CrossRefPubMed

Nagel B, Palmbach M, Petersen D, Ranke M (1997) Magnetic resonance images of 91 children with different causes of short stature: pituitary size reflects growth hormone secretion. Eur J Pediatr 156:758–763CrossRefPubMed

Naruo T, Nakabeppu Y, Deguchi D, Nagai N, Tsutsui J, Nakajo M, Nozoe S-i (2001) Decreases in blood perfusion of the anterior cingulate gyri in Anorexia Nervosa Restricters assessed by SPECT image analysis. BMC Psychiatry 1(1):1–5CrossRef

Pereira MA, FitzerGerald SJ, Gregg EW, Joswiak ML, Ryan WJ, Suminski RR, Utter AC, Zmuda JM (1997) A collection of physical activity questionnaires for health-related research. Med Sci Sports Exerc 29(6 Suppl):S1-205PubMed

Raj MA, Creech JA, Rogol AD (2022) Female athlete triad. StatPearls, Treasure Island

Roeykens J, Rogers R, Meeusen R, Magnus L, Borms J, de Meirleir K (1998) Validity and reliability in a Flemish population of the WHO-MONICA optional study of physical activity questionnaire. Med Sci Sports Exerc 30(7):1071–1075CrossRefPubMed

Ryan MP (2008) The antidepressant effects of physical activity: mediating self-esteem and self-efficacy mechanisms. Psychol Health 23(3):279–307. https://doi.org/10.1080/14768320601185502CrossRefPubMed

Scheithauer BW, Kovacs KT, Jariwala LK, Randall RV, Ryan N (1988a) Anorexia nervosa: an immunohistochemical study of the pituitary gland. Mayo Clin Proc 63(1):23–28. https://doi.org/10.1016/s0025-6196(12)62660-3CrossRefPubMed

Scheithauer BW, Kovacs KT, Jariwala LK, Randall RV, Ryan N (1988b) Anorexia nervosa: an immunohistochemical study of the pituitary gland. Mayo clinic proceedings. Elsevier, pp 23–28

Segura-García C, Aloi M, Rania M, Ciambrone P, Palmieri A, Pugliese V, Ruiz Moruno AJ, De Fazio P (2015) Ability of EDI-2 and EDI-3 to correctly identify patients and subjects at risk for eating disorders. Eat Behav 19:20–23. https://doi.org/10.1016/j.eatbeh.2015.06.010CrossRefPubMed

Tanriverdi F, Unluhizarci K, Kocyigit I, Tuna IS, Karaca Z, Durak AC, Selcuklu A, Casanueva FF, Kelestimur F (2008) Brief communication: pituitary volume and function in competing and retired male boxers. Ann Intern Med 148(11):827–831. https://doi.org/10.7326/0003-4819-148-11-200806030-00005CrossRefPubMed

Torsello A, Bresciani E, Avallone R, Locatelli V (2002) Ghrelin and GH secretion. Minerva Endocrinol 27(4):257–264PubMed

Usdan LS, Khaodhiar L, Apovian CM (2008) The endocrinopathies of anorexia nervosa. Endocr Pract 14(8):1055–1063. https://doi.org/10.4158/ep.14.8.1055CrossRefPubMedPubMedCentral

Virostko J, Williams J, Hilmes M, Bowman C, Wright JJ, Du L, Kang H, Russell WE, Powers AC, Moore DJ (2019) Pancreas volume declines during the first year after diagnosis of type 1 diabetes and exhibits altered diffusion at disease onset. Diabetes Care 42(2):248–257. https://doi.org/10.2337/dc18-1507CrossRefPubMed

Wagner A, Greer P, Bailer UF, Frank GK, Henry SE, Putnam K, Meltzer CC, Ziolko SK, Hoge J, McConaha C, Kaye WH (2006) Normal brain tissue volumes after long-term recovery in anorexia and bulimia nervosa. Biol Psychiatry 59(3):291–293. https://doi.org/10.1016/j.biopsych.2005.06.014CrossRefPubMed

Weinstein A, Weinstein Y (2014) Exercise addiction- diagnosis, bio-psychological mechanisms and treatment issues. Curr Pharm Des 20(25):4062–4069. https://doi.org/10.2174/13816128113199990614CrossRefPubMed

Wong AP-Y, Pipitone J, Park MTM, Dickie EW, Leonard G, Perron M, Pike BG, Richer L, Veillette S, Chakravarty MM (2014) Estimating volumes of the pituitary gland from T1-weighted magnetic-resonance images: effects of age, puberty, testosterone, and estradiol. Neuroimage 94:216–221CrossRefPubMed

Zipursky AR, Whittle S, Yücel M, Lorenzetti V, Wood SJ, Lubman DI, Simmons JG, Allen NB (2011) Pituitary volume prospectively predicts internalizing symptoms in adolescence. J Child Psychol Psychiatry 52(3):315–323CrossRefPubMed

Title: Structure–function relationship of the pituitary gland in anorexia nervosa and intense physical activity
Authors: Manel Merabet
Natacha Germain
Jérôme Redouté
Claire Boutet
Nicolas Costes
Maurice Ptito
Bogdan Galusca
Fabien C. Schneider
Publication date: 08-12-2023
Publisher: Springer Berlin Heidelberg
Keywords: Anorexia Nervosa
Magnetic Resonance Imaging
Magnetic Resonance Imaging
Addiction
Addiction
Published in: Brain Structure and Function / Issue 1/2024
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-023-02739-3

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Structure–function relationship of the pituitary gland in anorexia nervosa and intense physical activity

Abstract

Keynote webinar | Spotlight on medication adherence

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Abstract

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