Challenges of considering both extremities of the weight status spectrum to better understand obesity: insights from the NUTRILEAN project in constitutionally thin individuals.


Journal

International journal of obesity (2005)
ISSN: 1476-5497
Titre abrégé: Int J Obes (Lond)
Pays: England
ID NLM: 101256108

Informations de publication

Date de publication:
11 2023
Historique:
received: 04 04 2023
accepted: 27 07 2023
revised: 03 07 2023
medline: 27 10 2023
pubmed: 9 8 2023
entrez: 8 8 2023
Statut: ppublish

Résumé

While the physiology of obesity has been so extensively investigated to date, only an extremely small number of studies (less than 50) have focused on the other extremity of the weight spectrum: constitutional thinness. Yet, this important state of underweight in the absence of any eating disorders provides a mirror model of obesity that might be particularly insightful in understanding obesity. Nevertheless, important methodological and recruitment-related issues appear when it comes to this complex constitutionally thin phenotype, as experienced by our research group with the realization of the ongoing NUTRILEAN clinical trial. To face this challenge, the present paper aims at identifying, analyzing, and discussing the quality of such recruitment processes in publications about constitutional thinness. In this order, a group of experts collectively created a new grading system to assess the level of rigour and quality achieved by each study based on different criteria. The main results were that (i) metabolic-related biasing criteria were poorly observed despite being crucial, (ii) recruitment processes were not detailed enough and with sufficient explicitness, and (iii) recruiting among already identified patients would be associated with both higher sample sizes and better scores of quality. The present work encourages investigators to adopt a high level of rigour despite the complexity and duration of recruitment processes for this specific population, and readers to pay close attention to the quality of recruitment when interpreting the data. To better understand obesity and its physiological adaptations, it seems essential not only to compare it to normal-weight conditions, but also to the other extremity of the weight status spectrum represented by constitutional thinness.

Sections du résumé

BACKGROUND/OBJECTIVES
While the physiology of obesity has been so extensively investigated to date, only an extremely small number of studies (less than 50) have focused on the other extremity of the weight spectrum: constitutional thinness. Yet, this important state of underweight in the absence of any eating disorders provides a mirror model of obesity that might be particularly insightful in understanding obesity. Nevertheless, important methodological and recruitment-related issues appear when it comes to this complex constitutionally thin phenotype, as experienced by our research group with the realization of the ongoing NUTRILEAN clinical trial. To face this challenge, the present paper aims at identifying, analyzing, and discussing the quality of such recruitment processes in publications about constitutional thinness.
METHODS
In this order, a group of experts collectively created a new grading system to assess the level of rigour and quality achieved by each study based on different criteria.
RESULTS
The main results were that (i) metabolic-related biasing criteria were poorly observed despite being crucial, (ii) recruitment processes were not detailed enough and with sufficient explicitness, and (iii) recruiting among already identified patients would be associated with both higher sample sizes and better scores of quality.
CONCLUSIONS
The present work encourages investigators to adopt a high level of rigour despite the complexity and duration of recruitment processes for this specific population, and readers to pay close attention to the quality of recruitment when interpreting the data. To better understand obesity and its physiological adaptations, it seems essential not only to compare it to normal-weight conditions, but also to the other extremity of the weight status spectrum represented by constitutional thinness.

Identifiants

pubmed: 37553452
doi: 10.1038/s41366-023-01360-y
pii: 10.1038/s41366-023-01360-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1171-1177

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Griffin HJ, O’Connor HT, Rooney KB, Steinbeck KS. Effectiveness of strategies for recruiting overweight and obese Generation Y women to a clinical weight management trial. Asia Pac J Clin Nutr. 2013;22:235–40.
pubmed: 23635367
Bergmann S, Keitel-Korndörfer A, Herfurth-Majstorovic K, Wendt V, Klein AM, von Klitzing K, et al. Recruitment strategies in a prospective longitudinal family study on parents with obesity and their toddlers. BMC Public Health. 2017;17:145.
pubmed: 28143475 pmcid: 5286690 doi: 10.1186/s12889-017-4038-9
Riveros-McKay F, Mistry V, Bounds R, Hendricks A, Keogh JM, Thomas H, et al. Genetic architecture of human thinness compared to severe obesity. PLoS Genet. 2019;15:e1007603.
pubmed: 30677029 pmcid: 6345421 doi: 10.1371/journal.pgen.1007603
Diaz EO, Prentice AM, Goldberg GR, Murgatroyd PR, Coward WA. Metabolic response to experimental overfeeding in lean and overweight healthy volunteers. Am J Clin Nutr. 1992;56:641–55.
pubmed: 1414963 doi: 10.1093/ajcn/56.4.641
Schneider L, Heard I, Bréart G, Henrion R. [Maternal thinness and pregnancy]. Arch Fr Pediatr. 1979;36:1068–74.
pubmed: 547935
van Binsbergen CJ, Coelingh Bennink HJ, Odink J, Haspels AA, Koppeschaar HP. A comparative and longitudinal study on endocrine changes related to ovarian function in patients with anorexia nervosa. J Clin Endocrinol Metab. 1990;71:705–11.
pubmed: 2203799 doi: 10.1210/jcem-71-3-705
Petretta M, Bonaduce D, Scalfi L, de Filippo E, Marciano F, Migaux ML, et al. Heart rate variability as a measure of autonomic nervous system function in anorexia nervosa. Clin Cardiol. 1997;20:219–24.
pubmed: 9068906 doi: 10.1002/clc.4960200307
Hinney A, Barth N, Ziegler A, von Prittwitz S, Hamann A, Hennighausen K, et al. Serotonin transporter gene-linked polymorphic region: allele distributions in relationship to body weight and in anorexia nervosa. Life Sci. 1997;61:PL 295–303.
pubmed: 9395256 doi: 10.1016/S0024-3205(97)00888-6
Scalfi L, Coltorti A, Borrelli R, Contaldo F. Postprandial thermogenesis in leanness and anorexia nervosa. Ann Nutr Metab. 1992;36:48–54.
pubmed: 1590672 doi: 10.1159/000177698
Mazzeo SE, Slof RM, Tozzi F, Kendler KS, Bulik CM. Characteristics of men with persistent thinness. Obes Res. 2004;12:1367–9.
pubmed: 15483200 doi: 10.1038/oby.2004.172
Bosy-Westphal A, Reinecke U, Schlörke T, Illner K, Kutzner D, Heller M, et al. Effect of organ and tissue masses on resting energy expenditure in underweight, normal weight and obese adults. Int J Obes Relat Metab Disord. 2004;28:72–79.
pubmed: 14647174 doi: 10.1038/sj.ijo.0802526
Slof R, Mazzeo S, Bulik CM. Characteristics of women with persistent thinness. Obes Res. 2003;11:971–7.
pubmed: 12917502 doi: 10.1038/oby.2003.134
Miljic D, Pekic S, Djurovic M, Doknic M, Milic N, Casanueva FF, et al. Ghrelin has partial or no effect on appetite, growth hormone, prolactin, and cortisol release in patients with anorexia nervosa. J Clin Endocrinol Metab. 2006;91:1491–5.
pubmed: 16449333 doi: 10.1210/jc.2005-2304
Miljic D, Djurovic M, Pekic S, Doknic M, Stojanovic M, Milic N, et al. Glucose metabolism during ghrelin infusion in patients with anorexia nervosa. J Endocrinol Invest. 2007;30:771–5.
pubmed: 17993770 doi: 10.1007/BF03350816
Fernández-García D, Rodríguez M, García Alemán J, García-Almeida JM, Picón MJ, Fernández-Aranda F, et al. Thin healthy women have a similar low bone mass to women with anorexia nervosa. Br J Nutr. 2009;102:709–14.
pubmed: 19302720 doi: 10.1017/S0007114509274733
Tagami T, Satoh N, Usui T, Yamada K, Shimatsu A, Kuzuya H. Adiponectin in anorexia nervosa and bulimia nervosa. J Clin Endocrinol Metab. 2004;89:1833–7.
pubmed: 15070952 doi: 10.1210/jc.2003-031260
Tolle V, Kadem M, Bluet-Pajot M-T, Frere D, Foulon C, Bossu C, et al. Balance in ghrelin and leptin plasma levels in anorexia nervosa patients and constitutionally thin women. J Clin Endocrinol Metab. 2003;88:109–16.
pubmed: 12519838 doi: 10.1210/jc.2002-020645
Marra M, Pasanisi F, Montagnese C, De Filippo E, De Caprio C, de Magistris L, et al. BMR variability in women of different weight. Clin Nutr. 2007;26:567–72.
pubmed: 17517450 doi: 10.1016/j.clnu.2007.03.006
Marra M, Caldara A, Montagnese C, De Filippo E, Pasanisi F, Contaldo F, et al. Bioelectrical impedance phase angle in constitutionally lean females, ballet dancers and patients with anorexia nervosa. Eur J Clin Nutr. 2009;63:905–8.
pubmed: 19002201 doi: 10.1038/ejcn.2008.54
Germain N, Galusca B, Le Roux CW, Bossu C, Ghatei MA, Lang F, et al. Constitutional thinness and lean anorexia nervosa display opposite concentrations of peptide YY, glucagon-like peptide 1, ghrelin, and leptin. Am J Clin Nutr. 2007;85:967–71.
pubmed: 17413094 doi: 10.1093/ajcn/85.4.967
Germain N, Galusca B, Grouselle D, Frere D, Tolle V, Zizzari P, et al. Ghrelin/obestatin ratio in two populations with low bodyweight: constitutional thinness and anorexia nervosa. Psychoneuroendocrinology. 2009;34:413–9.
pubmed: 18995969 doi: 10.1016/j.psyneuen.2008.10.001
Bossu C, Galusca B, Normand S, Germain N, Collet P, Frere D, et al. Energy expenditure adjusted for body composition differentiates constitutional thinness from both normal subjects and anorexia nervosa. Am J Physiol Endocrinol Metab. 2007;292:E132–137.
pubmed: 16912058 doi: 10.1152/ajpendo.00241.2006
Galusca B, Zouch M, Germain N, Bossu C, Frere D, Lang F, et al. Constitutional thinness: unusual human phenotype of low bone quality. J Clin Endocrinol Metab. 2008;93:110–7.
pubmed: 17956951 doi: 10.1210/jc.2007-1591
Estour B, Marouani N, Sigaud T, Lang F, Fakra E, Ling Y, et al. Differentiating constitutional thinness from anorexia nervosa in DSM 5 era. Psychoneuroendocrinology. 2017;84:94–100.
pubmed: 28692876 doi: 10.1016/j.psyneuen.2017.06.015
Orthofer M, Valsesia A, Mägi R, Wang Q-P, Kaczanowska J, Kozieradzki I, et al. Identification of ALK in Thinness. Cell. 2020;181:1246–1262.e22.
pubmed: 32442405 doi: 10.1016/j.cell.2020.04.034
Bang EB, Ko JK, Kwag KH, Lee GY, Kim Y-R. A comparison of patients with anorexia nervosa and women who are constitutionally thin. Eur Eat Disord Rev. 2020;28:633–42.
pubmed: 32842173 doi: 10.1002/erv.2777
Florent V, Baroncini M, Jissendi-Tchofo P, Lopes R, Vanhoutte M, Rasika S, et al. Hypothalamic structural and functional imbalances in anorexia nervosa. Neuroendocrinology. 2019;110:552–62.
pubmed: 31484186 doi: 10.1159/000503147
Margaritelis NV, Theodorou AA, Kyparos A, Nikolaidis MG, Paschalis V. Effect of body composition on redox homeostasis at rest and in response to exercise: the case of underfat women. J Sports Sci. 2019;37:1–8.
doi: 10.1080/02640414.2019.1578450
Marra M, Sammarco R, De Filippo E, De Caprio C, Speranza E, Contaldo F, et al. Resting energy expenditure, body composition and phase angle in anorectic, ballet dancers and constitutionally lean males. Nutrients. 2019;11:502.
pubmed: 30818800 pmcid: 6471802 doi: 10.3390/nu11030502
Hasegawa A, Usui C, Kawano H, Sakamoto S, Higuchi M. Characteristics of body composition and resting energy expenditure in lean young women. J Nutr Sci Vitaminol. 2011;57:74–79.
pubmed: 21512294 doi: 10.3177/jnsv.57.74
Paschalis V, Nikolaidis MG, Theodorou AA, Deli CK, Raso V, Jamurtas AZ, et al. The effects of eccentric exercise on muscle function and proprioception of individuals being overweight and underweight. J Strength Cond Res. 2013;27:2542–51.
pubmed: 23238093 doi: 10.1519/JSC.0b013e31827fc9a6
Pasanisi F, Pace L, Fonti R, Marra M, Sgambati D, De Caprio C, et al. Evidence of brown fat activity in constitutional leanness. J Clin Endocrinol Metabol. 2013;98:1214–8.
doi: 10.1210/jc.2012-2981
Santonicola A, Siniscalchi M, Capone P, Gallotta S, Ciacci C, Iovino P. Prevalence of functional dyspepsia and its subgroups in patients with eating disorders. World J Gastroenterol. 2012;18:4379–85.
pubmed: 22969202 pmcid: 3436054 doi: 10.3748/wjg.v18.i32.4379
Galusca B, Verney J, Meugnier E, Ling Y, Edouard P, Feasson L, et al. Reduced fibre size, capillary supply and mitochondrial activity in constitutional thinness’ skeletal muscle. Acta Physiol. 2018;224:e13097.
doi: 10.1111/apha.13097
Germain N, Viltart O, Loyens A, Bruchet C, Nadin K, Wolowczuk I, et al. Interleukin-7 plasma levels in human differentiate anorexia nervosa, constitutional thinness and healthy obesity. PLoS ONE. 2016;11:e0161890.
pubmed: 27611669 pmcid: 5017702 doi: 10.1371/journal.pone.0161890
Galusca B, Jeandel L, Germain N, Alexandre D, Leprince J, Anouar Y, et al. Orexigenic neuropeptide 26RFa: new evidence for an adaptive profile of appetite regulation in anorexia nervosa. J Clin Endocrinol Metab. 2012;97:2012–8.
pubmed: 22466335 doi: 10.1210/jc.2011-3396
Gunes A, Yıldırım Bas F, Arslan B, Tok L, Tok Ö, Salman Z. Assessment of corneal parameters in patients with constitutional thinness using scheimpflug imaging. Semin Ophthalmol. 2016;33:175–8.
pubmed: 27601264
Galusca B, Prévost G, Germain N, Dubuc I, Ling Y, Anouar Y, et al. Neuropeptide Y and α-MSH circadian levels in two populations with low body weight: anorexia nervosa and constitutional thinness. PLoS ONE. 2015;10:e0122040.
pubmed: 25798605 pmcid: 4370702 doi: 10.1371/journal.pone.0122040
Ling Y, Carayol J, Galusca B, Canto C, Montaurier C, Matone A, et al. Persistent low body weight in humans is associated with higher mitochondrial activity in white adipose tissue. Am J Clin Nutr. 2019;110:605–16.
pubmed: 31374571 pmcid: 6736451 doi: 10.1093/ajcn/nqz144
Ling Y, Galusca B, Martin F-P, Bartova S, Carayol J, Moco S, et al. Resistance to lean mass gain in constitutional thinness in free-living conditions is not overpassed by overfeeding. J Cachexia Sarcopenia Muscle. 2020;11:1187–99.
pubmed: 32274897 pmcid: 7567161 doi: 10.1002/jcsm.12572
Bailly M, Germain N, Féasson L, Costes F, Estour B, Hourdé C, et al. Skeletal muscle of females and males with constitutional thinness: a low intramuscular lipid content and oxidative profile. Appl Physiol Nutr Metab. 2020;45:1287–98.
pubmed: 32479741 doi: 10.1139/apnm-2020-0068
Bailly M, Boscaro A, Thomas T, Féasson L, Costes F, Pereira B, et al. New insights on bone tissue and structural muscle-bone unit in constitutional thinness. Front Physiol. 2022;13:921351.
pubmed: 35874537 pmcid: 9305386 doi: 10.3389/fphys.2022.921351
Gabriel T, Massoubre C, Hanachi M, Doré J, Lambert C, Germain N, et al. Association of gut-specific non-inflammatory T lymphocytes with chronic anorexia nervosa and constitutional thinness. Eur Eat Disord Rev. 2022. https://doi.org/10.1002/erv.2934 .
Cominetti O, Núñez Galindo A, Corthésy J, Carayol J, Germain N, Galusca B, et al. Proteomics reveals unique plasma signatures in constitutional thinness. Proteomics Clin Appl. 2022;16:e2100114.
pubmed: 35579096 doi: 10.1002/prca.202100114
Germain N, Galusca B, Caron-Dorval D, Martin J-F, Pujos-Guillot E, Boirie Y, et al. Specific appetite, energetic and metabolomics responses to fat overfeeding in resistant-to-bodyweight-gain constitutional thinness. Nutr Diabetes. 2014;4:e126.
pubmed: 25027794 pmcid: 5189928 doi: 10.1038/nutd.2014.17
World Health Organization. Prevalence of underweight among adults. 2020. https://www.who.int/data/gho/data/indicators/indicator-details/GHO/prevalence-of-underweight-among-adults-bmi-18-(crude-estimate)-(-) . Accessed 20 Mar 2020.
Estour B, Galusca B, Germain N. Constitutional thinness and anorexia nervosa: a possible misdiagnosis? Front Endocrinol. 2014;5:175.
doi: 10.3389/fendo.2014.00175
Bailly M, Germain N, Galusca B, Courteix D, Thivel D, Verney J. Definition and diagnosis of constitutional thinness: a systematic review. Br J Nutr. 2020;124:531–47.
pubmed: 32321597 doi: 10.1017/S0007114520001440
Bailly M, Boscaro A, Pereira B, Féasson L, Boirie Y, Germain N, et al. Is constitutional thinness really different from anorexia nervosa? A systematic review and meta-analysis. Rev Endocr Metab Disord. 2021. https://doi.org/10.1007/s11154-021-09650-4 .
Bailly M, Boscaro A, Pereira B, Courteix D, Germain N, Galusca B, et al. Underweight but not underfat: is fat-free mass a key factor in constitutionally thin women? Eur J Clin Nutr. 2021;75:1764–70.
pubmed: 33772214 doi: 10.1038/s41430-021-00895-5
Estour B, Galusca B, Germain N. [Constitutional thinness]. Corresp Métab Horm Diabètes Nutr. 2012;XVI:109–14.
Estour B, Galusca B, Germain N. [Constitutional thinness]. Cah Nutr Diét. 2013;48:26–32.
doi: 10.1016/j.cnd.2012.09.002
Estour B, Galusca B, Germain N. Thinness, weight loss and constitutional thinness. Med Mal Metab. 2016;10:10–15.
Galusca B, Germain N, Estour B. Thinness, bone and fracture risk. Med Mal Metab. 2016;10:16–21.
Germain N, Galusca B, Estour B. Thinness and resistance to weight gain: a proof of concept. Med Mal Metab. 2016;10:28–33.
Galusca B, Germain N, Estour B. Maigreur et hormones de régulation de l’appétit. Méd Mal Métab. 2016;10:22–27.
Decker ST, Matias AA, Bannon ST, Madden JP, Alexandrou-Majaj N, Layec G. Effects of cigarette smoke on in situ mitochondrial substrate oxidation of slow- and fast-twitch skeletal muscles. Life Sci. 2023;315:121376.
pubmed: 36646379 doi: 10.1016/j.lfs.2023.121376
Blauw LL, Boon MR, Rosendaal FR, de Mutsert R, Gast KB, Willems van Dijk K, et al. Smoking is associated with increased resting energy expenditure in the general population: the NEO study. Metabolism. 2015;64:1548–55.
pubmed: 26363529 doi: 10.1016/j.metabol.2015.08.008
Hellerstein MK, Benowitz NL, Neese RA, Schwartz JM, Hoh R, Jacob P, et al. Effects of cigarette smoking and its cessation on lipid metabolism and energy expenditure in heavy smokers. J Clin Invest. 1994;93:265–72.
pubmed: 8282797 pmcid: 293761 doi: 10.1172/JCI116955
Seoane-Collazo P, Romero-Picó A, Rial-Pensado E, Liñares-Pose L, Estévez-Salguero Á, Fernø J, et al. κ-Opioid signaling in the lateral hypothalamic area modulates nicotine-induced negative energy balance. Int J Mol Sci. 2021;22:1515.
pubmed: 33546289 pmcid: 7913331 doi: 10.3390/ijms22041515

Auteurs

Audrey Boscaro (A)

Laboratory of the Metabolic Adaptations to Exercise under Physiological and Pathological Conditions (AME2P), UPR 3533, CRNH Auvergne, University of Clermont Auvergne, Clermont-Ferrand, France. audrey.boscaro@uca.fr.

Julien Verney (J)

Laboratory of the Metabolic Adaptations to Exercise under Physiological and Pathological Conditions (AME2P), UPR 3533, CRNH Auvergne, University of Clermont Auvergne, Clermont-Ferrand, France.

Angelo Tremblay (A)

Department of Kinesiology, Faculty of Medicine, Laval University, Quebec, QC, Canada.

James A King (JA)

National Centre for Sport and Exercise Medicine, School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough, UK.
NIHR Leicester Biomedical Research Centre, University Hospitals of Leicester NHS Trust and the University of Leicester, Leicester, UK.

Bruno Pereira (B)

Biostatistics Unit, Délégation à la Recherche Clinique et à l'Innovation (DRCI), Clermont-Ferrand, France.

Frédéric Costes (F)

Department of Sport Medicine and Functional Explorations, University Teaching Hospital of Clermont-Ferrand, Diet and Musculoskeletal Health Team, CRNH, INRA, University of Clermont Auvergne, Clermont-Ferrand, France.

Valérie Julian (V)

Department of Sport Medicine and Functional Explorations, University Teaching Hospital of Clermont-Ferrand, Diet and Musculoskeletal Health Team, CRNH, INRA, University of Clermont Auvergne, Clermont-Ferrand, France.

Martine Duclos (M)

Department of Sport Medicine and Functional Explorations, University Teaching Hospital of Clermont-Ferrand, Diet and Musculoskeletal Health Team, CRNH, INRA, University of Clermont Auvergne, Clermont-Ferrand, France.

Yves Boirie (Y)

Department of Clinical Nutrition, University Teaching Hospital of Clermont-Ferrand, Diet and Musculoskeletal Health Team, CRNH, INRA, University of Clermont Auvergne, Clermont-Ferrand, France.

David Thivel (D)

Laboratory of the Metabolic Adaptations to Exercise under Physiological and Pathological Conditions (AME2P), UPR 3533, CRNH Auvergne, University of Clermont Auvergne, Clermont-Ferrand, France.

Mélina Bailly (M)

Laboratory of the Metabolic Adaptations to Exercise under Physiological and Pathological Conditions (AME2P), UPR 3533, CRNH Auvergne, University of Clermont Auvergne, Clermont-Ferrand, France.

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