Is willingness to exercise programmed in utero? Reviewing sedentary behavior and the benefits of physical activity in intrauterine growth restricted individuals

Bischoff, Adrianne Rahde; Cunha, Fábio da Silva; Molle, Roberta Dalle; Maróstica, Paulo José Cauduro; Silveira, Patrícia Pelufo

doi:10.1016/j.jped.2017.12.015

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Review articles • J. Pediatr. (Rio J.) 94 (6) • Nov-Dec 2018 • https://doi.org/10.1016/j.jped.2017.12.015 copy

Is willingness to exercise programmed in utero? Reviewing sedentary behavior and the benefits of physical activity in intrauterine growth restricted individuals^☆ ☆ Please cite this article as: Bischoff AR, Cunha FS, Molle RD, Maróstica PJ, Silveira PP. Is willingness to exercise programmed in utero? Reviewing sedentary behavior and the benefits of physical activity in intrauterine growth restricted individuals. J Pediatr (Rio J). 2018;94:582-95.

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective:

The literature suggests that a fetus will adapt to surrounding adversities by optimizing its use of energy to improve survival, ultimately leading to the programming of the individual's energy intake and expenditure. While recent reviews focused on the fetal programming of energy intake and food preferences, there is also some evidence that fetal adversity is associated with diminished physical activity levels. Therefore, we aimed to review (a) the evidence for an association between being born with intrauterine growth restriction and sedentarism over the life-course and (b) the potential benefits of physical activity over cardiometabolic risk factors for this population.

Sources:

PubMed, Scielo, Scopus and Embase.

Summary of findings:

Most clinical studies that used objective measures found no association between intrauterine growth restriction and physical activity levels, while most studies that used self-reported questionnaires revealed such relationships, particularly leisure time physical activity. Experimental studies support the existence of fetal programming of physical activity, and show that exposure to exercise during IUGR individuals' life improves metabolic outcomes but less effect was seen on muscle architecture or function.

Conclusions:

Alterations in muscle strength and metabolism, as well as altered aerobic performance, may predispose IUGR individuals to be spontaneously less physically active, suggesting that this population may be an important target for preventive interventions. Although very heterogeneous, the different studies allow us to infer that physical activity may have beneficial effects especially for individuals that are more vulnerable to metabolic modifications such as those with IUGR.

KEYWORDS
DOHaD; IUGR; Physical activity; Sedentary behavior

Author/year (reference number)	Age in years (number of participants)	Tool	Definitions	Outcome
Objectively measured
Kehoe, 2012³⁶36 Kehoe SH, Krishnaveni GV, Veena SR, Hill JC, Osmond C, Kiran A, et al. Birth size and physical activity in a cohort of Indian children aged 6-10 years. J Dev Orig Health Dis. 2012;3:245-52.	6-10 (449)	Accelerometer for 7 days	<100 cpm: sedentary behavior 100-2291 cpm: light activity 2292-4007 cpm: moderate activity >4008 cpm: vigorous activity	No associations between body size and skinfold thickness at birth and physical activity levels
Mattocks, 2007⁴³43 Mattocks C, Ness A, Deere K, Tilling K, Leary S, Blair SN, et al. Early life determinants of physical activity in 11 to 12 year olds: cohort study. BMJ. 2008;336:26-9.	11-12 (5451)	Accelerometer for 7 days + record of swimming/cycling time	>3600 cpm: moderate to vigorous activity	BW has no influence in physical activity levels
Ridgway, 2011³²32 Ridgway CL, Brage S, Sharp SJ, Corder K, Westgate KL, van Sluijs EM, et al. Does birth weight influence physical activity in youth? A combined analysis of four studies using objectively measured physical activity. PLoS ONE. 2011;6:e16125.	9-15 (4170)	Accelerometer ≥ 3 days	<100 cpm: sedentary time >2000 cpm: moderate and vigorous activity	No association between BW and total physical activity. One cohort showed a association between higher BW and lower levels of total physical activity
Kaseva, 2015⁵¹51 Kaseva N, Martikainen S, Tammelin T, Hovi P, Jarvenpaa A-L, Andersson S, et al. Objectively measured physical activity in young adults born preterm at very low birth weight. J Pediatr. 2015;166:474-6.	22-30 (104)	Accelerometer ≥ 3 days	<320 cpm, <1.5 METs: sedentary time 1048-1624 cpm, 3-6 METs: moderate PA >1624, >6 METs: vigorous PA ≥1048 cpm, ≥3 METs: moderate-to-vigorous PA	No significant difference in physical activity levels or sedentary time in VLBW compared to term controls (same cohort as Kajantie, 2010)²⁸28 Kajantie E, Strang-Karlsson S, Hovi P, Raikkonen K, Pesonen A-K, Heinonen K, et al. Adults born at very low birth weight exercise less than their peers born at term. J Pediatr. 2010;157:610-616.e1.
Hildebrand, 2015³¹31 Hildebrand M, Kolle E, Hansen BH, Collings PJ, Wijndaele K, Kordas K, et al. Association between birth weight and objectively measured sedentary time is mediated by central adiposity: data in 10,793 youth from the International Children's Accelerometry Database. Am J Clin Nutr. 2015;101:983-90. and Ekelund, 2012⁵²52 Ekelund U, Wijndaele K, Sherar L, Cooper A. Birth weight, sedentary time and abdominal adiposity in youth: the international children's accelerometry database (ICAD). J Sci Med Sport. 2012;15:S41.	6-18 (10,793)	Accelerometer	<100 cpm: sedentary time >3000 cpm: moderate-to-vigorous PA	BW positively associated with sedentary time
van Deutekom, 2014⁵³53 van Deutekom A, Chin-A-Paw M, Vrijkotte T, Gemke R. Early programming of physical activity and sedentary behaviour at primary school age. Abcd-study. 2014;99:A90.	8-9 (183)	Accelerometer	>3000 cpm: moderate activity Minutes sedentary per day	LBW was not associated with either physical activity or sedentary time
Questionnaires
Kaseva, 2012⁴⁷47 Kaseva N, Wehkalampi K, Strang-Karlsson S, Salonen M, Pesonen A-K, Raikkonen K, et al. Lower conditioning leisure-time physical activity in young adults born preterm at very low birth weight. PLoS ONE. 2012;7:e32430.	22-30 (195)	12 month recall questionnaire	Conditioning LTPA (running, skiing, swimming), non-conditioning LTPA (household work, gardening, shoveling snow), PA from commuting to work. Frequency, duration and average intensity	VLBW undertake less leisure-time physical activity (same cohort as Kajantie, 2010)²⁸28 Kajantie E, Strang-Karlsson S, Hovi P, Raikkonen K, Pesonen A-K, Heinonen K, et al. Adults born at very low birth weight exercise less than their peers born at term. J Pediatr. 2010;157:610-616.e1.
Kajantie, 2010²⁸28 Kajantie E, Strang-Karlsson S, Hovi P, Raikkonen K, Pesonen A-K, Heinonen K, et al. Adults born at very low birth weight exercise less than their peers born at term. J Pediatr. 2010;157:610-616.e1.	18.5-27.1 (351)	Questionnaire	Occupational, commuting, and leisure-time non-conditioning physical activity. Frequency, duration and intensity.	VLBW exercise less than adults born at term (30% vs 0% were SGA in the VLBW sample)
Andersen, 2009²⁶26 Andersen LG, Angquist L, Gamborg M, Byberg L, Bengtsson C, Canoy D, et al. Birth weight in relation to leisure time physical activity in adolescence and adulthood: meta-analysis of results from 13 nordic cohorts. PLoS ONE. 2009;4:e8192.	14-74 (43,482)	LTPA Questionnaire	Duration, frequency and/or intensity	Reverse U-shaped association between BW and leisure time physical activity
Fernandes, 2010²²22 Fernandes FS, Portella AK, Barbieri MA, Bettiol H, Silva AA, Agranonik M, et al. Risk factors for sedentary behavior in young adults: similarities in the inequalities. J Dev Orig Health Dis. 2010;1:255-61.	22-23 (2057)	1 week recall questionnaire	Active: >7 days of combined activities reaching at least 3000 METs or intense activity for at least 3 days reaching a minimum of 1500 METs; Sufficiently active: ≥5 days of combined activities reaching at least 600 METs or >5 days of walking for a minimum of 30 min/day or >5 days of moderate activity for at least 30 min/day or >3 days of intense activity for at least 20 min/day; Sedentary: when the level of physical activity was below the above descriptions	LBW is a risk factor for sedentary behavior
Azevedo, 2008³⁰30 Azevedo MR, Horta BL, Gigante DP, Victora CG, Barros FC. Fatores associados ao sedentarismo no lazer de adultos na coorte de nascimentos de 1982, Pelotas, RS. Rev Saúde Pública. 2008;42:70-7.	21-23 (4297)	1 week recall questionnaire	Sedentary: <150 min/week of PA	BW inversely associated with sedentarism only in women
Hallal, 2006⁴⁹49 Hallal PC, Wells JC, Reichert FF, Anselmi L, Victora CG. Early determinants of physical activity in adolescence: prospective birth cohort study. BMJ. 2006;332:1002-7.	10-12 (4453)	Questionnaire	Sedentary lifestyle: <300 min/week of PA	Lower BW associated with increased sedentary time
Elhakeem, 2016⁵⁴54 Elhakeem A, Cooper R, Bann D, Kuh D, Hardy R. Birth weight, school sports ability, and adulthood leisure-time physical activity. Med Sci Sports Exerc. 2017;49:64-70.	13-68 (2739)	LTPA Questionnaire	Inactive: no participation in LTPA; Moderately: up to four times in LTPA; Regularly active: five or more times in LTPA (in the previous month at age 36 years, per month at age 43 years, and in the previous 4 weeks at ages 53, 60-64, and 68 years).	LBW was associated with lower ability in school sports and with nonparticipation in LTPA across adulthood.

Author/year	Age in years (number of participants)	Outcome
Aoyama, 2013⁵⁶56 Aoyama T, Tsushita K, Miyatake N, Numata T, Miyachi M, Tabata I, et al. Does cardiorespiratory fitness modify the association between birth weight and insulin resistance in adult life?. PLOS ONE. 2013;8:e73967.	20-64 (379)	BW and cardiorespiratory fitness inversely associated with HOMA-IR
Eriksson, 2004²⁹29 Eriksson JG, Ylihärsilä H, Forsen T, Osmond C, Barker DJ. Exercise protects against glucose intolerance in individuals with a small body size at birth. Prev Med. 2004;39:164-7.	65-75 (500)	Regular and moderate exercise protects against glucose intolerance in elderly people with increased risk of developing Type 2 diabetes (born with LBW)
Labayen, 2013⁵⁹59 Labayen I, Ortega FB, Moreno LA, Gonzalez-Gross M, Jimenez-Pavon D, Martinez-Gomez D, et al. Physical activity attenuates the negative effect of low birth weight on leptin levels in European adolescents; The HELENA study. Nutr Metab Cardiovasc Dis. 2013;23:344-9.	12-17 (538)	Meeting the physical activity recommendations may attenuate the negative effect of LBW on serum leptin levels
Laaksonen, 2003³⁸38 Laaksonen DE, Lakka HM, Lynch J, Lakka TA, Niskanen L, Rauramaa R, et al. Cardiorespiratory fitness and vigorous leisure-time physical activity modify the association of small size at birth with the metabolic syndrome. Diabetes Care. 2003;26:2156-64.	42-60 (462)	Regular vigorous leisure-time physical activity or good cardiorespiratory fitness seems to attenuate the association of LBW with insulin resistance and metabolic syndrome
Madsen, 2015⁵⁸58 Madsen C, Mogensen P, Thomas N, Christensen DL, Bygbjerg IC, Mohan V, et al. Effects of an outdoor bicycle-based intervention in healthy rural Indian men with normal and low birth weight. J Dev Orig Health Dis. 2015;6:27-37.	19-21 (117)	LBW benefits metabolically from exercise training to an extent comparable with NBW controls
Ortega, 2011⁶⁰60 Ortega FB, Ruiz JR, Hurtig-Wennlof A, Meirhaeghe A, Gonzalez-Gross M, Moreno LA, et al. Physical activity attenuates the effect of low birth weight on insulin resistance in adolescents findings from two observational studies. Diabetes. 2011;60:2295-9.	12-17 (846)	Higher levels of physical activity may attenuate the adverse effects of LBW on insulin sensitivity in adolescents
Redmond, 2013³⁹39 Redmond JG, Gage TB, Kiyamu M, Brutsaert TD. The effect of intra-uterine growth restriction on blood lipids and response to exercise training. Am J Hum Biol. 2013;25:844-6.	20 (36)	Low Ponderal Index have poorer lipid profile and improve values with training
Ridgway, 2011⁵⁷57 Ridgway CL, Brage S, Anderssen SA, Sardinha LB, Andersen LB, Ekelund U. Do physical activity and aerobic fitness moderate the association between birth weight and metabolic risk in youth? The European Youth Heart Study. Diabetes Care. 2011;34:187-92.	9-15 (1254)	Physical activity does not modify the association between LBW and insulin resistance

Author/year	Sex	Age	Species	Tool	Outcome
Baker, 2015⁶²62 Baker MS, Li G, Kohorst JJ, Waterland RA. Fetal growth restriction promotes physical inactivity and obesity in female mice. Int J Obes (Lond). 2015;39:98-104.	Male and female	40 days	Agouti viable yellow mice	PA measured by beam breaks: activity, ambulatory movement along the length of the cage and rearing.	IUGR female exercise less and have increased adiposity
Bellinger, 2006²⁵25 Bellinger L, Sculley DV, Langley-Evans SC. Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int J Obes (Lond). 2006;30:729-38.	Male and female	13 months	Wistar rats	Infra-red beams to monitor animal motion	Decreased locomotor activity in animals born from dams fed with a low protein diet
Corvino, 2015⁶⁹69 Corvino SB, Volpato GT, Rudge MV, Damasceno DC. Intrauterine growth restricted rats exercised before and during pregnancy: maternal and perinatal repercussions. Evid Based Complement Altern Med. 2015;2015:294850.	Female	90 days	Wistar rats	Swimming three times per week	Glucose intolerance was reversed in IUGR exposed to a swimming program
Corvino, 2017⁷⁰70 Corvino SB, Damasceno DC, Sinzato YK, Netto AO, Macedo NC, Zambrano E, et al. Comparative analysis of two different models of swimming applied to pregnant rats born small for pregnant age. An Acad Bras Cienc. 2017;89:223-30.	Female	90 days	Wistar rats	Swimming three times per week	Enhanced peripheral insulin sensitivity in exercised female rats.
Cunha, 2015²³23 Cunha FdS, Dalle Molle R, Portella AK, Benetti CdS, Noschang C, Goldani MZ, et al. Both food restriction and high-fat diet during gestation induce low birth weight and altered physical activity in adult rat offspring: the "Similarities in the Inequalities" model. PLOS ONE. 2015;10:e0118586-e118590.	Male and Female	60 days	Sprague-Dawley rats	Spontaneous activity in running wheels	Both undernutrition and overnutrition in pregnancy leads to LBW. LBW animals exercise less.
de Melo Montenegro, 2012⁶⁸68 de Melo Montenegro IH, Moita L, Dos Reis FK, de Oliveira E, Lisboa PC, de Moura EG, et al. Effects of a moderate physical training on the leptin synthesis by adipose tissue of adult rats submitted to a perinatal low-protein diet. Horm Metab Res. 2012;44:814-8.	Male	8 weeks	Wistar rats	Exercise training on a motorized treadmill	Physical activity attenuates effects of IUGR on the leptin content in visceral adipose tissue
Garg, 2009⁶⁵65 Garg M, Thamotharan M, Oak SA, Pan G, MacLaren DC, Lee PW, et al. Early exercise regimen improves insulin sensitivity in the intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab. 2009;296:E272-81.	Male and Female	60 days	Sprague-Dawley rats	Exercise training on a motorized treadmill	Exercise training in IUGR offspring improves insulin sensitivity
Huber, 2009⁸⁹89 Huber K, Miles JL, Norman AM, Thompson NM, Davison M, Breier BH. Prenatally induced changes in muscle structure and metabolic function facilitate exercise-induced obesity prevention. Endocrinology. 2009;150:4135-44.	Male and female	250 days	Wistar rats	Forced exercise in running wheels	Daily exercise decreases adiposity in IUGR offspring
Kaur, 2016⁶³63 Kaur M, Wooldridge AL, Wilkes MJ, Pitchford WS, Hynd PI, McConell GK, et al. Placental restriction in multi-fetal pregnancies increases spontaneous ambulatory activity during daylight hours in young adult female sheep. J Dev Orig Health Dis. 2016;7:525-37.	Male and female	240 days	Merino ×Border Leicester ewes	Spontaneous ambulatory activity measured with a Garmin attached to a collar	Spontaneous ambulatory activity negatively correlated with birth weight in females
Laker, 2012⁷⁵75 Laker RC, Wlodek ME, Wadley GD, Gallo LA, Meikle PJ, McConell GK. Exercise early in life in rats born small does not normalize reductions in skeletal muscle PGC-1α in adulthood. Am J Physiol Endocrinol Metab. 2012;302:E1221-30.	Male	24 weeks	Wistar rats	Exercise training on a motorized treadmill	Exercise for IUGR does not alter deficits in skeletal muscle markers of mitochondrial biogenesis in adulthood
Laker, 2011⁶⁶66 Laker RC, Gallo LA, Wlodek ME, Siebel AL, Wadley GD, McConell GK. Short-term exercise training early in life restores deficits in pancreatic beta-cell mass associated with growth restriction in adult male rats. Am J Physiol Endocrinol Metab. 2011;301:E931-40.	Male	9-24 weeks	Wistar-Kyoto rats	Exercise training on a motorized treadmill	Exercise prevents compromised pancreatic β-cell mass later in life
Leandro, 2012⁷¹71 Leandro CG, da Silva Ribeiro W, Dos Santos JA, Bento-Santos A, Lima-Coelho CH, Falcão-Tebas F, et al. Moderate physical training attenuates muscle-specific effects on fibre type composition in adult rats submitted to a perinatal maternal low-protein diet. Eur J Nutr. 2012;51:807-15.	Male	60 days	Wistar rats	Exercise training on a motorized treadmill	Physical activity reverts the effects of a perinatal low-protein diet on the proportion of fiber types in skeletal muscle
Maux, 2009⁷⁴74 Maux DA, de Araujo TN, Viana MT, Paes ST, Andrade MdA, Arruda de Moraes SR. Influence of moderate physical training on the artery wall structure of rats submitted to gestational and neonatal protein malnutrition. Rev Bras Med Esporte. 2009;15:334-7.	Male	16 weeks	Wistar rats	Exercise training on a motorized treadmill	Physical activity did not modify structural alterations on the common left carotid and horizontal aorta arteries wall
Miles, 2009⁶⁴64 Miles JL, Landon J, Davison M, Krägeloh CU, Thompson NM, Triggs CM, et al. Prenatally undernourished rats show increased preference for wheel running v. lever pressing for food in a choice task. Br J Nutr. 2009;101:902-8.	Male and female	250-365 days	Wistar rats	Running over level pressing for food	IUGR rats have greater preference for running over lever pressing for food
Miles, 2009⁶⁷67 Miles JL, Huber K, Thompson NM, Davison M, Breier BH. Moderate daily exercise activates metabolic flexibility to prevent prenatally induced obesity. Endocrinology. 2009;150:179-86.	Male and female	150 days	Wistar rats	Forced exercise in running wheels	Exercise prevents obesity in IUGR offspring.
Oliveira, 2014⁷²72 Oliveira V, Akamine EH, Carvalho MH, Michelini LC, Fortes ZB, Cunha TS, et al. Influence of aerobic training on the reduced vasoconstriction to angiotensin II in rats exposed to intrauterine growth restriction: possible role of oxidative stress and AT2 receptor of angiotensin II. PLOS ONE. 2014;9:e113035.	Male	8-18 weeks	Wistar rats	Exercise training on a motorized treadmill	Aerobic exercise promotes beneficial cardiovascular adaptations in IUGR
Reyes, 2015⁷³73 Reyes LM, Morton JS, Kirschenman R, DeLorey DS, Davidge ST. Vascular effects of aerobic exercise training in rat adult offspring exposed to hypoxia-induced intrauterine growth restriction. J Physiol. 2015;593:1913-29.	Male and female	10-16 weeks	Sprague-Dawley rats	Exercise training on a motorized treadmill	Aerobic exercise improved vasodilation in muscle arteries in IUGR males
Vickers, 2003²⁴24 Vickers MH, Breier BH, McCarthy D, Gluckman PD. Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol Regul Integr Comp Physiol. 2003;285:R271-3.	Male and female	420 days	Wistar rats	Optimax behavioral testing apparatus	IUGR offspring were significantly less active than controls. Postnatal hypercaloric diet exacerbated the sedentary behavior.

Mechanism	Author/year	Main findings
Altered cardiovascular/aerobic performance	Baraldi, 1990⁹³93 Baraldi E, Zanconato S, Zorzi C, Santuz P, Benini F, Zacchello F. Exercise performance in very-low-birth-weight children at the age of 7-12 years. Eur J Pediatr. 1991;150:713-6.	Higher energy cost of running in SGA
	Boreham, 2001⁹²92 Boreham CA, Murray L, Dedman D, Davey Smith G, Savage JM, Strain JJ. Birthweight and aerobic fitness in adolescents: the Northern Ireland Young Hearts Project. Public Health. 2001;115:373-9.	Higher birth weight, higher fitness score
	Cafiero, 2014⁹⁰90 Cafiero G, Fintini D, Brufani C, Fiori R, Giordano U, Turchetta A, et al. Cardiovascular fitness is impaired in children born small for gestational age. Acta Paediatr. 2014;103:E219-21.	Decreased cardiovascular fitness in SGA
	Lawlor, 2008⁹¹91 Lawlor DA, Cooper AR, Bain C, Davey Smith G, Irwin A, Riddoch C, et al. Associations of birth size and duration of breast feeding with cardiorespiratory fitness in childhood: findings from the Avon Longitudinal Study of Parents and Children (ALSPAC). Eur J Epidemiol. 2008;23:411-22.	Birth weight, length and ponderal index positively associated with cardiorespiratory fitness
	Reyes, 2015⁹⁴94 Reyes LM, Kirschenman R, Quon A, Morton JS, Shah A, Davidge ST. Aerobic exercise training reduces cardiac function in adult male offspring exposed to prenatal hypoxia. Am J Physiol Regul Integr Comp Physiol. 2015;309:R489-98.	Reduced baseline cardiac performance in male IUGR offspring and increased superoxide generation
Altered muscle strength	Brutsaert, 2011⁴¹41 Brutsaert TD, Tamvada KH, Kiyamu M, White DD, Gage TB. Low ponderal index is associated with decreased muscle strength and fatigue resistance in college-aged women. Early Hum Dev. 2011;87:663-9.	Low ponderal index at birth associated with lower grip strength, lower maximal isometric voluntary contraction, increased rate of fatigue and decreased training response
	Dodds, 2012⁴²42 Dodds R, Denison HJ, Ntani G, Cooper R, Cooper C, Sayer AA, et al. Birth weight and muscle strength: a systematic review and meta-analysis. J Nutr Health Aging. 2012;16:609-15.	Birth weight positively associated with greater muscle strength
	Inskip, 2007⁷⁸78 Inskip HM, Godfrey KM, Martin HJ, Simmonds SJ, Cooper C, Sayer AA, et al. Size at birth and its relation to muscle strength in young adult women. J Intern Med. 2007;262:368-74.	Increased grip strength with higher birth weight
	Kuh, 2002⁸⁰80 Kuh D, Bassey J, Hardy R, Aihie Sayer A, Wadsworth M, Cooper C. Birth weight, childhood size, and muscle strength in adult life: evidence from a birth cohort study. Am J Epidemiol. 2002;156:627-33.	Birth weight associated with adult grip strength
	Moura-Dos-Santos, 2013⁷⁷77 Moura-Dos-Santos M, Wellington-Barros J, Brito-Almeida M, Manhaes-de-Castro R, Maia J, Leandro CG. Permanent deficits in handgrip strength and running speed performance in low birth weight children. Am J Hum Biol. 2013;25:58-62.	Decreased handgrip strength and running speed performance in LBW
	Ridgway, 2009⁷⁹79 Ridgway CL, Ong KK, Tammelin T, Sharp SJ, Ekelund U, Jarvelin MR. Birth size, infant weight gain, and motor development influence adult physical performance. Med Sci Sports Exerc. 2009;41:1212-21.	Birth weight positively associated with muscle strength and aerobic fitness
	Ylihärsilä, 2007⁸¹81 Ylihärsilä H, Kajantie E, Osmond C, Forsen T, Barker DJ, Eriksson JG. Birth size, adult body composition and muscle strength in later life. Int J Obes (Lond). 2007;31:1392-9.	Birth weight associated with grip strength and increased adult lean mass
	van Deutekom, 2015⁷⁶76 van Deutekom AW, Chinapaw MJ, Vrijkotte TG, Gemke RJ. The association of birth weight and infant growth with physical fitness at 8-9 years of age-the ABCD study. Int J Obes (Lond). 2015;39:593-600.	Birth weight positively associated with handgrip strength. Impaired aerobic and neuromuscular fitness in LBW
Muscle metabolism, gene expression and histologic alterations	Brons, 2008⁸⁴84 Brons C, Jensen CB, Storgaard H, Alibegovic A, Jacobsen S, Nilsson E, et al. Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J Clin Endocrinol Metab. 2008;93:3885-92.	Normal in vivo mitochondrial function and expression of oxidative phosphorylation genes in low birth weight.
	Brutsaert, 2012⁸⁵85 Brutsaert TD, Tamvada KH, Kiyamu M, White DD, Gage TB. Response to an aerobic training intervention in young adults depends on ponderal index at birth. J Dev Orig Health Dis. 2012;3:424-32.	Plasma lactate after exercise as well as in response to training (but not aerobic capacity are dependent on ponderal index.
	Friedrichsen, 2012⁸⁶86 Friedrichsen M, Ribel-Madsen R, Mortensen B, Hansen CN, Alibegovic AC, Højbjerre L, et al. Muscle inflammatory signaling in response to 9 days of physical inactivity in young men with low compared with normal birth weight. Eur J Endocrinol. 2012;167:829-38.	CD68 expression increased in low birth weight, oxidative phosphorylation genes decreased in low birth weight and negatively correlated with CD69 expression. MPC1 and NF-κB activity unaffected. None of the inflammatory markers correlated with insulin sensitivity.
	Jensen, 2007⁸³83 Jensen CB, Storgaard H, Madsbad S, Richter EA, Vaag AA. Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab. 2007;92:1530-4.	Changes in muscle fiber composition and size
	Mortensen, 2014⁸⁷87 Mortensen B, Friedrichsen M, Andersen NR, Alibegovic AC, Højbjerre L, Sonne MP, et al. Physical inactivity affects skeletal muscle insulin signaling in a birth weight-dependent manner. J Diabetes Complicat. 2014;28:71-8.	More sensitive AMPK system
	Mortensen, 2013⁸⁸88 Mortensen B, Hingst JR, Frederiksen N, Hansen RW, Christiansen CS, Iversen N, et al. Effect of birth weight and 12 weeks of exercise training on exercise-induced AMPK signaling in human skeletal muscle. Am J Physiol Endocrinol Metab. 2013;304:E1379-90.	Bed rest is related to decreased insulin-stimulated Akt phosphorylation and to increased AMPK α1 and γ3 protein expression; insulin response of A5160 phosphorylation is decreased both pre- and post-bed rest.

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[1] * Corresponding author. E-mail:adrianne.bischoff@sickkids.ca (A.R. Bischoff).