Maternal exercise improves insulin sensitivity in mature rat offspring
Open accessAbstract
PURPOSE: Recent findings have shown that the intrauterine environment can negatively influence long-term insulin sensitivity in the offspring. Here we look at maternal voluntary exercise as an intervention to improve offspring insulin sensitivity and glucose homeostasis. METHODS: Female Sprague-Dawley rats were split into sedentary and exercise groups with the exercise cohort having voluntary access to a running wheel in the cage before and during mating, pregnancy, and nursing. Female offspring were weaned into sedentary cages. Glucose tolerance tests and hyperinsulinemic-euglycemic clamp were performed in adult offspring to evaluate glucose regulation and insulin sensitivity. RESULTS: Adult female offspring born to exercised dams had enhanced glucose disposal during glucose tolerance testing (P < 0.05) as well as increased glucose infusion rates (P < 0.01) and whole body glucose turnover rates (P < 0.05) during hyperinsulinemic-euglycemic clamp testing compared with offspring from sedentary dams. Offspring from exercised dams also had decreased insulin levels (P < 0.01) and hepatic glucose production (P < 0.05) during the clamp procedure compared with offspring born to sedentary dams. Offspring from exercised dams had increased glucose uptake in skeletal muscle (P < 0.05) and decreased heart glucose uptake (P < 0.01) compared with offspring from sedentary dams in response to insulin infusion during the clamp procedure. CONCLUSIONS: Exercise during pregnancy enhances offspring insulin sensitivity and improves offspring glucose homeostasis. This can decrease offspring susceptibility to insulin-resistant related diseases such as type 2 diabetes mellitus. Maternal exercise could be an easy, short-term, nonpharmacological method of preventing disease in future generations.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In general, the most significant effects of maternal exercise on offspring metabolic health are observed when maternal exercise begins before mating and is continued throughout pregnancy.
“In general, the most significant effects are observed when maternal exercise begins before mating and is continued throughout pregnancy.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [131]
The Methods describe exercise beginning 7–10 days before mating and continuing through pregnancy, and the Discussion reports improved insulin sensitivity in adult offspring. But the Discussion says studies comparing exercise timing are still needed; this study does not establish that this schedule produces the most significant effects. (LLM, conf=0.88)
Experimental — accuracy not yet measuredUsing voluntary wheel running, maternal exercise improved glucose tolerance in both mouse and rat offspring, compared to the offspring of sedentary controls.
“Using voluntary wheel running, maternal exercise improved glucose tolerance in both mouse and rat offspring, compared to the offspring of sedentary controls [131,132].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [131]
Several groups have shown that enforced maternal treadmill exercise or voluntary wheel running had significant effects on the metabolic health of male and female offspring.
“Several groups have shown that enforced maternal treadmill exercise or voluntary wheel running had significant effects on the metabolic health of male and female offspring [131,132,133,134,135,136].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [131]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Hales, C. N., & Barker, D. J. P. (1992) · Diabetologia · doi:10.1007/bf00400248 · Cited by 3,294 · see citing works
Persistent epigenetic differences associated with prenatal exposure to famine in humans
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E., & Lumey, L. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806560105 · Cited by 3,082 · see citing works
DeFronzo, R. A., Jacot, E., Jequier, E., Maeder, E., Wahren, J., & Felber, J. P. (1981) · Diabetes · doi:10.2337/diab.30.12.1000 · Cited by 1,770 · see citing works
Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring
Ng, S.-F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A., & Morris, M. J. (2010) · Nature · doi:10.1038/nature09491 · Cited by 1,327 · see citing works
DeFronzo, R. A., Gunnarsson, R., Björkman, O., Olsson, M., & Wahren, J. (1985) · Journal of Clinical Investigation · doi:10.1172/jci111938 · Cited by 1,167 · see citing works
Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.12.008 · Cited by 1,157 · see citing works
Birth Weight and Adult Hypertension, Diabetes Mellitus, and Obesity in US Men
Curhan, G. C., Willett, W. C., Rimm, E. B., Spiegelman, D. L., Ascherio, A., & Stampfer, M. J. (1996) · Circulation · doi:10.1161/01.cir.94.12.3246 · Cited by 917 · see citing works
The developmental origins of chronic adult disease
Barker, D. (2004) · Acta Paediatrica · doi:10.1111/j.1651-2227.2004.tb00236.x · Cited by 790 · see citing works
Magnusson, I., Rothman, D. L., Katz, L. D., Shulman, R. G., & Shulman, G. I. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115997 · Cited by 757 · see citing works
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Hales, C., & Barker, D. (2013) · International Journal of Epidemiology · doi:10.1093/ije/dyt133 · Cited by 711 · see citing works
Park, J. H., Stoffers, D. A., Nicholls, R. D., & Simmons, R. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33655 · Cited by 640 · see citing works
Intrauterine Growth Retardation Leads to the Development of Type 2 Diabetes in the Rat
Simmons, R. A., Templeton, L. J., & Gertz, S. J. (2001) · Diabetes · doi:10.2337/diabetes.50.10.2279 · Cited by 638 · see citing works
Birthweight and the Risk for Type 2 Diabetes Mellitus in Adult Women
Rich-Edwards, J. W., Colditz, G. A., Stampfer, M. J., Willett, W. C., Gillman, M. W., Hennekens, C. H., Speizer, F. E., & Manson, J. E. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-130-4_part_1-199902160-00005 · Cited by 544 · see citing works
Skeletal Muscle Fiber Type: Influence on Contractile and Metabolic Properties
Zierath, J. R., & Hawley, J. A. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020348 · Cited by 518 · see citing works
Depré, C., Vanoverschelde, J., & Taegtmeyer, H. (1999) · Circulation · doi:10.1161/01.cir.99.4.578 · Cited by 424 · see citing works
The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis.
Barker, D. J., Osmond, C., & Law, C. (1989) · Journal of Epidemiology & Community Health · doi:10.1136/jech.43.3.237 · Cited by 389 · see citing works
Insulin signaling and insulin sensitivity after exercise in human skeletal muscle
Wojtaszewski, J. F., Hansen, B. F., Gade, Kiens, B., Markuns, J. F., Goodyear, L. J., & Richter, E. A. (2000) · Diabetes · doi:10.2337/diabetes.49.3.325 · Cited by 382 · see citing works
Low birthweight is associated with specific changes in muscle insulin-signalling protein expression
Ozanne, S. E., Jensen, C. B., Tingey, K., Storgaard, H., Madsbad, S., & Vaag, A. A. (2005) · Diabetologia · doi:10.1007/s00125-005-1669-7 · Cited by 286 · see citing works
Fernandez‐Twinn, D. S., Wayman, A., Ekizoglou, S., Martin, M. S., Hales, C. N., & Ozanne, S. E. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00206.2004 · Cited by 256 · see citing works
Clapp, J. F. (1996) · The Journal of Pediatrics · doi:10.1016/s0022-3476(96)70029-x · Cited by 240 · see citing works
Raychaudhuri, N., Raychaudhuri, S., Thamotharan, M., & Devaskar, S. U. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800128200 · Cited by 227 · see citing works
The effects of maternal exercise on fetal oxygenation and feto-placental growth
Clapp, J. F. (2003) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(03)00176-3 · Cited by 208 · see citing works
Hopkins, S. A., Baldi, J. C., Cutfield, W. S., McCowan, L. M. E., & Hofman, P. L. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2255 · Cited by 199 · see citing works
Sex differences in the developmental origins of hypertension and cardiorenal disease
Gilbert, J. S., & Nijland, M. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90724.2008 · Cited by 159 · see citing works
Fiber type composition of four hindlimb muscles of adult Fisher 344 rats
Staron, R. S., Kraemer, W. J., Hikida, R. S., Fry, A. C., Murray, J. D., & Campos, G. E. R. (1999) · Histochemistry and Cell Biology · doi:10.1007/s004180050341 · Cited by 159 · see citing works
Hyperinsulinemic-euglycemic Clamps in Conscious, Unrestrained Mice
Ayala, J. E., Bracy, D. P., Malabanan, C. M., James, F. D., Ansari, T., Fueger, P. T., McGuinness, O. P., & Wasserman, D. H. (2011) · Journal of Visualized Experiments · doi:10.3791/3188 · Cited by 157 · see citing works
A microanalysis of wheel running in male and female rats
Eikelboom, R., & Mills, R. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90217-x · Cited by 155 · see citing works
Lee, H., Kim, H. K., Lee, J.-W., Kim, Y., Yang, H.-Y., Chang, H., Lee, T.-H., Shin, M.-C., Lee, M., Shin, M., et al. (2005) · Brain and Development · doi:10.1016/j.braindev.2005.05.007 · Cited by 151 · see citing works
Effect of recreational exercise on pregnancy weight gain and subcutaneous fat deposition
Clapp, J. F., & Little, K. D. (1995) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199502000-00004 · Cited by 125 · see citing works
Chen, Z., Vigueira, P. A., Chambers, K. T., Hall, A. M., Mitra, M. S., Qi, N., McDonald, W. G., Colca, J. R., Kletzien, R. F., & Finck, B. N. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.363960 · Cited by 121 · see citing works
Self-citationPerinatal exercise improves glucose homeostasis in adult offspring
Carter, L. G., Lewis, K. N., Wilkerson, D. C., Tobia, C. M., Ngo Tenlep, S. Y., Shridas, P., Garcia-Cazarin, M. L., Wolff, G., Andrade, F. H., Charnigo, R. J., et al. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00213.2012 · Cited by 118 · see citing works
Self-citationRegulation of Net Hepatic Glucose Uptake In Vivo
Pagliassotti, M. J., & Cherrington, A. D. (1992) · Annual Review of Physiology · doi:10.1146/annurev.ph.54.030192.004215 · Cited by 97 · see citing works
Neu, J. (2009) · Yearbook of Neonatal and Perinatal Medicine · doi:10.1016/s8756-5005(08)79286-2 · Cited by 90 · see citing works
Insulin action on heart and skeletal muscle glucose uptake in essential hypertension.
Nuutila, P., Mäki, M. T., Laine, H. K., Knuuti, J. M., Ruotsalainen, U., Luotolahti, M., Haaparanta‐Solin, M., Solin, O. H., Jula, A. M., & Koivisto, V. A. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118085 · Cited by 86 · see citing works
Pullen, A. (1977) · Europe PMC (PubMed Central) · Cited by 81 · see citing works
Regulation by insulin of myocardial glucose and fatty acid metabolism in the conscious dog.
Barrett, E. J., Schwartz, R. G., Francis, C. K., & Zaret, B. L. (1984) · Journal of Clinical Investigation · doi:10.1172/jci111474 · Cited by 81 · see citing works
Glucose Tolerance and Plasma Insulin of the Rat in Relation to the Oestrous Cycle and Sex Hormones
Bailey, C. J., & Matty, A. J. (2009) · Hormone and Metabolic Research · doi:10.1055/s-0028-1094063 · Cited by 79 · see citing works
Exercise signalling to glucose transport in skeletal muscle
Richter, E. A., Nielsen, J. N., Jørgensen, S. B., Frøsig, C., Birk, J. B., & Wojtaszewski, J. F. P. (2004) · Proceedings of The Nutrition Society · doi:10.1079/pns2004343 · Cited by 51 · see citing works
Sparling, J. E., Mahoney, M. M., Baker, S., & Bielajew, C. H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.041 · Cited by 35 · see citing works
Garg, M., Thamotharan, M., Oak, S. A., Pan, G., MacLaren, D. C., Lee, P. W. N., & Devaskar, S. U. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90473.2008 · Cited by 25 · see citing works
Effects of exercise in diabetic rats before and during gestation on maternal and neonatal outcomes
VanHeest, J. L., & Rodgers, C. D. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.4.e727 · Cited by 16 · see citing works
Flagged first, then by citations
1 of the 42 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Laker, R., Lillard, T. S., Okutsu, M., Zhang, M., Hoehn, K. L., Connelly, J., & Yan, Z. (2014) · Diabetes · doi:10.2337/db13-1614 · Cited by 205 · see citing works
The role of diet and exercise in the transgenerational epigenetic landscape of T2DM
Barrès, R., & Zierath, J. R. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.87 · Cited by 198 · see citing works
Stanford, K. I., Lee, M.-Y., Getchell, K. M., So, K., Hirshman, M. F., & Goodyear, L. J. (2015) · Diabetes · doi:10.2337/db13-1848 · Cited by 151 · see citing works
Effects of maternal and paternal exercise on offspring metabolism
Kusuyama, J., Alves-Wagner, A. B., Makarewicz, N., & Goodyear, L. J. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00274-7 · Cited by 122 · see citing works
Maternal Exercise Improves Glucose Tolerance in Female Offspring
Stanford, K. I., Takahashi, H., So, K., Alves-Wagner, A. B., Prince, N. B., Lehnig, A. C., Getchell, K. M., Lee, M.-Y., Hirshman, M. F., & Goodyear, L. J. (2017) · Diabetes · doi:10.2337/db17-0098 · Cited by 114 · see citing works
Placental superoxide dismutase 3 mediates benefits of maternal exercise on offspring health
Kusuyama, J., Alves-Wagner, A. B., Conlin, R. H., Makarewicz, N., Albertson, B. G., Prince, N. B., Kobayashi, S., Kozuka, C., Leth‐Møller, M., Bjerre, M., et al. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.03.004 · Cited by 114 · see citing works
McGee, S. L., & Hargreaves, M. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.06.002 · Cited by 105 · see citing works
Raipuria, M., Bahari, H., & Morris, M. J. (2015) · PLOS ONE · doi:10.1371/journal.pone.0120980 · Cited by 90 · see citing works
The epigenetic landscape of exercise in cardiac health and disease
Wu, G.-L., Zhang, X., & Gao, F. (2020) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2020.12.003 · Cited by 70 · see citing works
Harris, J. E., Pinckard, K. M., Wright, K. R., Baer, L. A., Arts, P. J., Abay, E., Shettigar, V., Lehnig, A. C., Robertson, B., Madaris, K. L., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0223-8 · Cited by 82 · see citing works
Laker, R. C., Wlodek, M. E., Connelly, J. J., & Yan, Z. (2013) · Food Science and Human Wellness · doi:10.1016/j.fshw.2013.03.002 · Cited by 75 · see citing works
Interventions to prevent adverse fetal programming due to maternal obesity during pregnancy
Nathanielsz, P. W., Ford, S. P., Long, N., Vega-García, C. C., Reyes‐Castro, L. A., & Zambrano, E. (2013) · Nutrition Reviews · doi:10.1111/nure.12062 · Cited by 74 · see citing works
Impact of Maternal Exercise during Pregnancy on Offspring Chronic Disease Susceptibility
Blaize, A. N., Pearson, K. J., & Newcomer, S. C. (2015) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000058 · Cited by 71 · see citing works
Self-citationMaternal exercise during pregnancy promotes physical activity in adult offspring
Eclarinal, J. D., Zhu, S., Baker, M. S., Piyarathna, D. W. B., Coarfa, C., Fiorotto, M. L., & Waterland, R. A. (2016) · The FASEB Journal · doi:10.1096/fj.201500018r · Cited by 70 · see citing works
Mitochondrial health, the epigenome and healthspan
Aon, M. A., Cortassa, S., Juhaszova, M., & Sollott, S. J. (2016) · Clinical Science · doi:10.1042/cs20160002 · Cited by 66 · see citing works
Gestational exercise protects adult male offspring from high-fat diet-induced hepatic steatosis
Sheldon, R. D., Blaize, A. N., Fletcher, J. A., Pearson, K. J., Donkin, S. S., Newcomer, S. C., & Rector, R. S. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.08.022 · Cited by 65 · see citing works
Self-citationMaternal Exercise Improves the Metabolic Health of Adult Offspring
Harris, J. E., Baer, L. A., & Stanford, K. I. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.01.003 · Cited by 64 · see citing works
Penfold, N., & Ozanne, S. E. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.015 · Cited by 60 · see citing works
Exercise during pregnancy protects adult mouse offspring from diet-induced obesity
Wasinski, F., Bacurau, R. F. P., Estrela, G. R., Klempin, F., Arakaki, A. M., Batista, R. O., Mafra, F. F. P., do Nascimento, L. F. R., Hiyane, M. I., Velloso, L. A., et al. (2015) · Nutrition & Metabolism · doi:10.1186/s12986-015-0052-z · Cited by 54 · see citing works
de Bessa, A. D. S. M., de Jesus, É. F., Nunes, A., Pontes, C. N. R., Lacerda, I. S., da Costa, J. M., Souza, E. J., Lino-Júnior, R. S., Biancardi, M. F., dos Santos, F. C. A., et al. (2019) · Hypertension Research · doi:10.1038/s41440-019-0321-8 · Cited by 53 · see citing works
Pereira, T. J., Gruber, B. L. M., Kereliuk, S. M., & Dolinsky, V. W. (2014) · Biochemistry and Cell Biology · doi:10.1139/bcb-2014-0141 · Cited by 51 · see citing works
Santos, M., Rodríguez-González, G. L., Ibáñez, C. A., Vega-García, C. C., Nathanielsz, P. W., & Zambrano, E. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00398.2014 · Cited by 50 · see citing works
Developmental Origins of Health Span and Life Span: A Mini-Review
Preston, J. D., Reynolds, L. J., & Pearson, K. J. (2018) · Gerontology · doi:10.1159/000485506 · Cited by 48 · see citing works
Self-citationThe effects of voluntary exercise on oocyte quality in a diet-induced obese murine model
Boudoures, A. L., Chi, M. M.-Y., Thompson, A. S., Zhang, W., & Moley, K. H. (2015) · Reproduction · doi:10.1530/rep-15-0419 · Cited by 45 · see citing works
Maternal and paternal exercise regulate offspring metabolic health and beta cell phenotype
Zheng, J., Alves-Wagner, A. B., Stanford, K. I., Prince, N. B., So, K., Mul, J. D., Dirice, E., Hirshman, M. F., Kulkarni, R., & Goodyear, L. J. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2019-000890 · Cited by 45 · see citing works
Maternal Obesity: A Focus on Maternal Interventions to Improve Health of Offspring
Shrestha, A., Prowak, M., Berlandi-Short, V.-M., Garay, J., & Ramalingam, L. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.696812 · Cited by 42 · see citing works
Castro-Rodríguez, D. C., Rodríguez-González, G. L., Menjívar, M., & Zambrano, E. (2020) · Placenta · doi:10.1016/j.placenta.2020.04.002 · Cited by 42 · see citing works
Chung, E., Joiner, H. E., Skelton, T., Looten, K. D., Mańczak, M., & Reddy, P. H. (2017) · Physiological Reports · doi:10.14814/phy2.13184 · Cited by 41 · see citing works
Inheritance of environment-induced phenotypic changes through epigenetic mechanisms
Tando, Y., & Matsui, Y. (2023) · Current Zoology · doi:10.1093/eep/dvad008 · Cited by 39 · see citing works
Risk of hypertension following perinatal adversity: IUGR and prematurity
Chatmethakul, T., & Roghair, R. D. (2019) · Journal of Endocrinology · doi:10.1530/joe-18-0687 · Cited by 37 · see citing works
Impact of parental exercise on epigenetic modifications inherited by offspring: A systematic review
Axsom, J. E., & Libonati, J. R. (2019) · Physiological Reports · doi:10.14814/phy2.14287 · Cited by 24 · see citing works
Increasing Muscle Mass Improves Vascular Function in Obese ( db/db ) Mice
Qiu, S., MINTZ, J. D., Salet, C., Han, W., Giannis, A., Chen, F., Yu, Y., Su, Y., Fulton, D. J., & Stepp, D. W. (2014) · Journal of the American Heart Association · doi:10.1161/jaha.114.000854 · Cited by 36 · see citing works
Kereliuk, S. M., & Dolinsky, V. W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084467 · Cited by 34 · see citing works
“Using voluntary wheel running, maternal exercise improved glucose tolerance in both mouse and rat offspring, compared to the offspring of sedentary controls [131,132].”
BackgroundQuiclet, C., Dubouchaud, H., Berthon, P., Sanchez, H., Vial, G., Siti, F., Fontaine, E., Batandier, C., & Couturier, K. (2017) · The Journal of Physiology · doi:10.1113/jp274739 · Cited by 31 · see citing works
Murphy, M. O., Herald, J. B., Leachman, J. R., Tezanos, A. G. V., Cohn, D. M., & Loria, A. S. (2018) · International Journal of Obesity · doi:10.1038/s41366-018-0035-z · Cited by 31 · see citing works
Homage to the ‘H’ in developmental origins of health and disease
Rosenfeld, C. S. (2016) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174416000465 · Cited by 28 · see citing works
Rosa, B. V., Blair, H. T., Vickers, M. H., Dittmer, K. E., Morel, P. C. H., Knight, C. G., & Firth, E. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082378 · Cited by 27 · see citing works
The role of DNA methylation in personalized medicine for immune-related diseases
Gupta, M. K., Peng, H., Li, Y., & Xu, C. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108508 · Cited by 25 · see citing works
Exercise Improves Glucose Disposal and Insulin Signaling in Pregnant Mice Fed a High Fat Diet
Carter, L. G., & Tenlep, S. Y. N. (2015) · Journal of Diabetes & Metabolism · doi:10.4172/2155-6156.1000634 · Cited by 23 · see citing works
Self-citationBrawerman, G. M., & Dolinsky, V. W. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.02.002 · Cited by 25 · see citing works
Elías‐López, A. L., Vázquez-Mena, Ó., & Sferruzzi-Perri, A. N. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2023.166802 · Cited by 23 · see citing works
Exercised breastmilk: a kick-start to prevent childhood obesity?
Moholdt, T. T., & Stanford, K. I. (2023) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2023.08.019 · Cited by 24 · see citing works
Falcão‐Tebas, F., Marin, E. C. S., Kuang, J., Bishop, D. J., & McConell, G. K. (2020) · The Journal of Physiology · doi:10.1113/jp279582 · Cited by 23 · see citing works
Chaves, A., Weyrauch, L. A., Zheng, D., Biagioni, E. M., Krassovskaia, P. M., Davidson, B., Broskey, N. T., Boyle, K. E., May, L. E., & Houmard, J. A. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac270 · Cited by 22 · see citing works
Musiał, B., Fernandez‐Twinn, D. S., Duque-Guimaraes, D. E., Carr, S. K., Fowden, A. L., Ozanne, S. E., & Sferruzzi-Perri, A. N. (2019) · Physiological Reports · doi:10.14814/phy2.14202 · Cited by 20 · see citing works
Klein, C. P., RODRIGUES, K. D. S., Hözer, R. M., Pereira, N. D. S. C., Saccomori, A. B., Magro, B. M. D., Crestani, M. S., Hoppe, J. B., Salbego, C. G., Dalmaz, C., et al. (2018) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2018.08.009 · Cited by 20 · see citing works
Pitchford, L. M., Ludlow, A. T., Witkowski, S., Marshall, M. R., Lima, L., Venezia, A. C., Xiao, T., Lee, M. T., Spangenburg, E. E., & Roth, S. M. (2013) · Experimental Physiology · doi:10.1113/expphysiol.2012.070300 · Cited by 19 · see citing works
Quiclet, C., Farida, S. N., Dubouchaud, H., Vial, G., Berthon, P. M., Fontaine, E. M., Batandier, C., & Couturier, K. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00126.2016 · Cited by 19 · see citing works
Impacts of maternal diet and exercise on offspring behavior and body weights
MOSER, V. C., McDaniel, K. L., Woolard, E. A., Phillips, P. M., Franklin, J. N., & Gordon, C. J. (2017) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.07.002 · Cited by 19 · see citing works
Kelly, S. A., Hua, K., Wallace, J. N., Wells, S. E., Nehrenberg, D. L., & Pomp, D. (2015) · Journal of Negative Results in BioMedicine · doi:10.1186/s12952-015-0032-x · Cited by 18 · see citing works
Exercise Epigenetics and the Fetal Origins of Disease
Chalk, T., & Brown, W. M. (2014) · Epigenomics · doi:10.2217/epi.14.38 · Cited by 18 · see citing works
Maternally expressed gene 3 in metabolic programming
Hamilton, S., de Cabo, R., & Bernier, M. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.06.007 · Cited by 16 · see citing works
Self-citationSong, L., Yan, J., Wang, N., Wei, X., Luo, X. M., Meng, K., & Sun, B. (2019) · Biology of Reproduction · doi:10.1093/biolre/ioz213 · Cited by 15 · see citing works
Klein, C. P., Hoppe, J. B., Saccomori, A. B., dos Santos, B. G., August, P. M., Klein, I. P., Crestani, M. S., Bifi, F., Hözer, R. M., Navas, P., et al. (2020) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174420000562 · Cited by 13 · see citing works
Ruebel, M. L., Borengasser, S. J., Zhong, Y., Kang, P., Faske, J. B., & Shankar, K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216441 · Cited by 14 · see citing works
Gordon, C. J., Phillips, P. M., Johnstone, A. F. M., Schmid, J. E., Schladweiler, M. C. J., Ledbetter, A. D., Snow, S. J., & Kodavanti, U. P. (2017) · Inhalation Toxicology · doi:10.1080/08958378.2017.1342719 · Cited by 14 · see citing works
Rodrigo, N., Saad, S., Pollock, C. A., & Glastras, S. J. (2022) · Nutrients · doi:10.3390/nu14102154 · Cited by 13 · see citing works
Maternal Exercise and Paternal Exercise Induce Distinct Metabolite Signatures in Offspring Tissues
Hernández‐Saavedra, D., Markunas, C. A., Takahashi, H., Baer, L. A., Harris, J. E., Hirshman, M. F., Ilkayeva, O., Newgard, C. B., Stanford, K. I., & Goodyear, L. J. (2022) · Diabetes · doi:10.2337/db22-0341 · Cited by 13 · see citing works
Muniz, G. D. S., Beserra, R., da Silva, G. D. P., Fragoso, J., Lira, A. D. O., Nascimento, E., de Castro, R. M., & Leandro, C. G. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.027 · Cited by 13 · see citing works
Farida, S. N., Dubouchaud, H., Hininger‐Favier, I., Quiclet, C., Vial, G., Galinier, A., Casteilla, L., Fontaine, E. M., Batandier, C., & Couturier, K. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.194969 · Cited by 13 · see citing works
Agarwal, M., Hoffman, J. B., Tenlep, S. Y. N., Santarossa, S., Pearson, K. J., Sitarik, A. R., Cassidy‐Bushrow, A. E., & Petriello, M. C. (2023) · Reproductive Toxicology · doi:10.1016/j.reprotox.2023.108384 · Cited by 12 · see citing works
Self-citationMaternal Exercise Does Not Significantly Alter Adult Rat Offspring Vascular Function
Blaize, A. N., Breslin, E., Donkin, S. S., Cabot, R. A., Pearson, K. J., & Newcomer, S. C. (2015) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000665 · Cited by 11 · see citing works
Self-citationInfluence of Maternal Exercise on Maternal and Offspring Metabolic Outcomes
Jevtovic, F., & May, L. E. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.106566 · Cited by 11 · see citing works
Wasinski, F., Estrela, G. R., Arakaki, A. M., Bäder, M., Alenina, N. V., Klempin, F., & Araújo, R. C. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00402 · Cited by 10 · see citing works
Transgenerational cardiology: One way to a baby's heart is through the mother
Jay, P. Y., Akhirome, E., Magnan, R. A., Zhang, M. R., Kang, L., Qin, Y., Ugwu, N., Regmi, S. D., Nogee, J. M., & Cheverud, J. M. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.029 · Cited by 10 · see citing works
Influence of gestational exercise practice and litter size reduction on maternal care
August, P. M., RODRIGUES, K. D. S., Klein, C. P., dos Santos, B. G., & Matté, C. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135454 · Cited by 9 · see citing works
Pregnancy and Lactation: A Window of Opportunity to Improve Individual Health
Rodríguez-González, G. L., Castro-Rodríguez, D. C., & Zambrano, E. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7614-0_7 · Cited by 9 · see citing works
Fit mothers for a healthy future
Stevanović‐Silva, J., Beleza, J., Coxito, P. M., da Costa, R. C. F. C., Ascensão, A. A. M. R., & Magalhães, J. (2021) · European Journal of Clinical Investigation · doi:10.1111/eci.13596 · Cited by 8 · see citing works
Purcell, A. R., & Glastras, S. J. (2023) · Nutrients · doi:10.3390/nu15092155 · Cited by 8 · see citing works
Al‐Shudiefat, A. A., Alturk, H., Al‐Ameer, H. J., Zihlif, M. A., & Alenazy, M. F. (2023) · Applied Sciences · doi:10.3390/app13105939 · Cited by 8 · see citing works
Exercise during Pregnancy: Developmental Programming Effects and Future Directions in Humans
Krassovskaia, P. M., Chaves, A., Houmard, J. A., & Broskey, N. T. (2021) · International Journal of Sports Medicine · doi:10.1055/a-1524-2278 · Cited by 7 · see citing works
Building‐up fit muscles for the future
Beleza, J., Stevanović-Silva, J., Coxito, P., Costa, R., Ascensão, A., Torrella, J. R., & Magalhães, J. (2021) · European Journal of Clinical Investigation · doi:10.1111/eci.13515 · Cited by 7 · see citing works
Dias, R. D. F., de Lima, T. I., Costa-Júnior, J. M., Gonçalves, L. M., Araújo, H. N., de Paula, F. M. M., dos Santos, G. J., Branco, R. C. S., Ou, K., Kaestner, K. H., et al. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.120239 · Cited by 7 · see citing works
Maternal exercise and its beneficial effects on glucose metabolism in offspring
Zheng, J., Zhou, L.-Y., & Xiao, X.-H. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000731 · Cited by 5 · see citing works
Song, L., Cui, J., Wang, R., Wang, N., Yan, J., & Sun, B. (2022) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.108958 · Cited by 6 · see citing works
Exercise Is Medicine: How Do We Implement It?
Khasanova, A., & Henagan, T. M. (2023) · Nutrients · doi:10.3390/nu15143164 · Cited by 6 · see citing works
Tibana, R. A., Franco, O. L., Pereira, R. W., Navalta, J. W., & Prestes, J. (2017) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0042-120538 · Cited by 6 · see citing works
Momma, H., Sawada, S., Sloan, R., Gando, Y., Kawakami, R., Terada, S., Miyachi, M., Kinugawa, C., Okamoto, T., Tsukamoto, K., et al. (2017) · Journal of Epidemiology · doi:10.2188/jea.je20160199 · Cited by 4 · see citing works
Ren, J., Zhou, L., Li, S., Zhang, Q., & Xiao, X. (2024) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00200.2024 · Cited by 6 · see citing works
Links between Exercise Capacity, Exercise Training, and Metabolism
Spagnolo, A., Klug, S., Schenkl, C., & Schwarzer, M. (2023) · Comprehensive physiology · doi:10.1002/j.2040-4603.2023.tb00283.x · Cited by 4 · see citing works
Using neonatal skin to study the developmental programming of aging
Reynolds, L. J., Dickens, B. J., Green, B. B., Marsit, C. J., & Pearson, K. J. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.12.015 · Cited by 4 · see citing works
Self-citationEffects of maternal controlled exercise on offspring adiposity and glucose tolerance
Platt, K. M., Przybylowski, J., Charnigo, R. J., Tenlep, S. Y. N., Reynolds, L. J., & Pearson, K. J. (2021) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174421000489 · Cited by 4 · see citing works
Self-citationAngiotensin-(1-7) Treatment Early in Life Prevents Cardiac Hypertrophy in Adult Hypertensive Rats
Pontes, C. N. R., de Bessa, A. D. S. M., Macedo, L. M., Ferreira-Junior, M. D., Cavalcante, K. V. N., Campos, H. M., Cruz-Leite, V. R. M., Neves, Â. R., Gomes, R. M., Ghedini, P. C., et al. (2024) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000001530 · Cited by 4 · see citing works
Quiclet, C., Armand, M., Dubouchaud, H., Vial, G., Fontaine, E. M., Batandier, C., & Couturier, K. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2022.159223 · Cited by 4 · see citing works
Laker, R., Connelly, J., & Yan, Z. (2014) · Diabetes · doi:10.2337/db14-0135 · Cited by 5 · see citing works
Jahan, H., Fatima, U., Asad, S., Zahoor, S., Tufail, P., Zainab, D., Siddiqui, N. N., Ullah, A., Pizzi, M., & Choudhary, M. (2026) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2026.01.004 · Cited by 3 · see citing works
Bansal, A., Rashid, C. S., & Simmons, R. A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-811752-1.00014-6 · Cited by 3 · see citing works
Maternal Diet and Exercise: Influences on Obesity and Insulin Resistance
Carter, L. G., Tamashiro, K. L., & Pearson, K. J. (2014) · Oxidative stress and disease · doi:10.1201/b17530-4 · Cited by 3 · see citing works
Self-citationKyere-Davies, G., Hill, K. B., Mullen, G. P., Varshney, R., Das, S., Martinez, A. E., Farriester, J. W., Kinter, M. T., Mitchell, C. M., Short, K. R., et al. (2026) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00399.2025 · Cited by 2 · see citing works
Chung, E., Looten, K. D., Lunsford, T., Skelton, T., & Grue, K. A. (2017) · Gynecology and Reproductive Endocrinology · doi:10.35841/2591-7994.1.1.7-15 · Cited by 2 · see citing works
Wibowo, J. W., Fasitasari, M., & Zulaikhah, S. T. (2021) · Jurnal Kedokteran Brawijaya · doi:10.21776/ub.jkb.2021.031.03.5 · Cited by 2 · see citing works
Alves-Wagner, A. B., Jahan, F., Kusuyama, J., Nigro, P., Hirshman, M. F., & Goodyear, L. J. (2025) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2025.101096 · Cited by 2 · see citing works
Why Do Exercise and Dietary Restriction During Pregnancy Affect Glucose Tolerance in Opposite Ways?
Borer, K. T. (2015) · Diabetes · doi:10.2337/db14-1476 · Cited by 1 · see citing works
Moosavi, S. A., Jahromi, M. K., & Jahromi, B. N. (2015) · Women’s Health Bulletin · doi:10.17795/whb-29805 · Cited by 1 · see citing works
Early life nutrition and its effect on the development of obesity and type-2 diabetes
Vickers, M. H. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-824389-3.00011-8 · Cited by 1 · see citing works
전유나, 여효성, Jeong, K. H., 김창근, 권형태, & Kim, H. J. (2014) · Exercise Science · doi:10.15857/ksep.2014.23.2.69
Gaeini, A. A., Neek, L. S., Choobineh, S., Eslaminejad, M. B., Satarifard, S., & Mousavi, S. N. (2016) · DOAJ (DOAJ: Directory of Open Access Journals)
Pregnancy, Exercise and Late Effects in the Offspring until Adult Age
Pařízková, J. (2017) · SOJ Gynecology Obstetrics and Women s Health · doi:10.15226/2381-2915/3/2/00125
Optimizing Pregnancy for Intergenerational Health Benefits
Ferraro, Z. M. (2017) · University of Ottawa Journal of Medicine · doi:10.18192/uojm.v7i2.2139
Sari, M. Y., Sari, A., Yunita, L., Mahdiyah, D., & Haryono, I. A. (2017) · Sari Mulia International Conference on Health and Sciences (SMICHS) · doi:10.2991/smichs-17.2017.21
- Authors
- CARTER, L. G., QI, N. R., CABO, R. D., & PEARSON, K. J.
- Affiliations
- University of Kentucky (US)
- University of Michigan (US)
- National Institutes of Health (US)
- Venue
- Medicine & Science in Sports & Exercise
- Published
- 2013-05
- Volume
- 45
- Issue
- 5
- Pages
- 832-840
- ISSN
- 0195-9131 (ISSN-L)
- PMC
- PMC3617068
- OpenAlex
- W2086857259
- Cited by
- 121
- References
- 42
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 2 · 2023: 12 · 2022: 9 · 2021: 9 · 2020: 12 · 2019: 9 · 2018: 6 · 2017: 11 · 2016: 10 · 2015: 11 · 2014: 11 · 2013: 4
- FWCI
- 11.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Medicine & Science in Sports & Exercise (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (T32GM008322)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK089503, T32DK007778, R01DK090460, DK-07778, P30DK020572, P30DK089503)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Keywords
- maternal physical activity, voluntary wheel running, insulin sensitivity, glucose homeostasis, offspring, pregnancy, intrauterine environment, glucose tolerance, hyperinsulinemic-euglycemic clamp, hepatic glucose production, skeletal muscle glucose uptake, type 2 diabetes prevention, non-pharmacological treatment
- MeSH terms
- Animals, Body Composition, Body Weight, Female, Fetus, Homeostasis, Insulin Resistance, Physical Conditioning, Animal, Pregnancy, Glucose Clamp Technique, Rats, Sprague-Dawley, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review