Chronic Phase Shifts of the Photoperiod throughout Pregnancy Programs Glucose Intolerance and Insulin Resistance in the Rat
Open accessAbstract
Shift work during pregnancy is associated with an increased risk for preterm birth and low birth weight. However, the impact upon the long term health of the children is currently unknown. In this study, we used an animal model to determine the consequences of maternal shift work exposure on the health of the adult offspring. Pregnant rats were exposed to chronic phase shifts (CPS) in their photoperiod every 3-4 days throughout gestation and the first week after birth. Adult offspring were assessed for a range of metabolic, endocrine, circadian and neurobehavioural parameters. At 3 months of age, male pups exposed to the CPS schedule in utero had increased adiposity (+29%) and hyperleptinaemia (+99% at 0700h). By 12 months of age, both male and female rats displayed hyperleptinaemia (+26% and +41% respectively) and hyperinsulinaemia (+110% and +83% respectively). 12 month old female CPS rats displayed poor glucose tolerance (+18%) and increased insulin secretion (+29%) in response to an intraperitoneal glucose tolerance test. In CPS males the glucose response was unaltered, but the insulin response was reduced by 35%. The glucose response to an insulin tolerance test was decreased by 21% in CPS females but unaltered in males. Disruption of circadian rhythmicity during gestation resulted in gender dependent metabolic consequences for the adult offspring. These results highlight the need for a thorough analysis of shift work exposure in utero on the health of the adult offspring in humans.
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Maternal circadian disruption alters offspring metabolic functioning in adulthood, including regulation of glucocorticoids and insulin.
“Likewise, maternal circadian disruption alters offspring metabolic functioning in adulthood13, 17–19, including the regulation of glucocorticoids17 and insulin18.”
From Maternal and Early-Life Circadian Disruption Have Long-Lasting Negative Consequences on Offspring Development and Adult Behavior in Mice (2017) · cites this paper as [18]
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Cites
Health disorders of shift workers
Knutsson, A. (2003) · Occupational Medicine · doi:10.1093/occmed/kqg048 · Cited by 1,218 · see citing works
Nyirenda, M., Lindsay, R. S., Kenyon, C. J., Burchell, A. N., & Seckl, J. R. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1567 · Cited by 574 · see citing works
Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species
Holson, R. R., & Pearce, B. A. (1992) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(92)90020-b · Cited by 503 · see citing works
Clocks not winding down: unravelling circadian networks
Zhang, E. E., & Kay, S. A. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2995 · Cited by 446 · see citing works
Prenatal exposure to drugs: effects on brain development and implications for policy and education
Thompson, B. L., Levitt, P. R., & Stanwood, G. D. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2598 · Cited by 367 · see citing works
The role of prenatal stress in the etiology of developmental behavioural disorders
Kofman, O. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00015-5 · Cited by 331 · see citing works
Prenatal Stress or High-Fat Diet Increases Susceptibility to Diet-Induced Obesity in Rat Offspring
Tamashiro, K. L., Terrillion, C. E., Hyun, J., Koenig, J. I., & Moran, T. H. (2009) · Diabetes · doi:10.2337/db08-1129 · Cited by 291 · see citing works
Lésage, J., Del-Favero, F., Léonhardt, M., Louvart, H., Maccari, S., Vieau, D., & Darnaudéry, M. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1810291 · Cited by 273 · see citing works
Developmental Origins of Adult Disease
Langley‐Evans, S. C., & McMullen, S. (2010) · Medical Principles and Practice · doi:10.1159/000273066 · Cited by 261 · see citing works
Entringer, S., Buß, C., & Wadhwa, P. D. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283405921 · Cited by 236 · see citing works
O'Regan, D. J., Kenyon, C. J., Seckl, J. R., & Holmes, M. C. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00137.2004 · Cited by 228 · see citing works
Single and repetitive maternal glucocorticoid exposures reduce fetal growth in sheep.
Jobe, A. H., Wada, N., Berry, L. M., Ikegami, M., & Ervin, M. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70518-6 · Cited by 213 · see citing works
Prematurity and work in pregnancy.
McDonald, A. D., McDonald, J. C., Armstrong, B., Cherry, N., Nolin, A. D., & Robert, D. (1988) · Occupational and Environmental Medicine · doi:10.1136/oem.45.1.56 · Cited by 185 · see citing works
Profile of 24-h Light Exposure and Circadian Phase of Melatonin Secretion in Night Workers
Dumont, M., Benhaberou-Brun, D., & Paquet, J. (2001) · Journal of Biological Rhythms · doi:10.1177/074873001129002178 · Cited by 162 · see citing works
Development of metabolic systems
Grove, K. L., Grayson, B. E., Glavas, M. M., XIAO, X., & Smith, M. E. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.063 · Cited by 159 · see citing works
Abe, H., Hidaka, N., Kawagoe, C., Odagiri, K., Watanabe, Y., Ikeda, T., Ishizuka, Y., Hashiguchi, H., Takeda, R., Nishimori, T., et al. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.06.1465 · Cited by 157 · see citing works
Gender-specific programming of insulin secretion and action
Sugden, M., & Holness, M. J. (2002) · Journal of Endocrinology · doi:10.1677/joe.0.1750757 · Cited by 140 · see citing works
Shift work, Job Stress, and Late Fetal Loss: The National Birth Cohort in Denmark
Zhu, J. L., Hjøllund, N. H., Andersen, A. N., & Olsen, J. (2004) · Journal of Occupational and Environmental Medicine · doi:10.1097/01.jom.0000145168.21614.21 · Cited by 136 · see citing works
Effects of prenatal stress on maternal behavior in the rat
Patin, V., Lordi, B., Vincent, A., Thoumas, J., Vaudry, H., & Caston, J. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00491-1 · Cited by 133 · see citing works
Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress
Gerardin, D. C. C., Pereira, O. C. M., Kempinas, W. D. G., Flório, J. C., Moreira, E. G., & Bernardi, M. M. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.10.014 · Cited by 132 · see citing works
Estanislau, C. R., & Morato, S. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.04.003 · Cited by 132 · see citing works
Anxiety and increased 5-HT1A receptor response in NCAM null mutant mice
Stork, O., Welzl, H., Wotjak, C. T., Hoyer, D., Delling, M., Cremer, H., & Schachner, M. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19990905)40:3 · Cited by 127 · see citing works
Ain, R., Kent, L. N., & Soares, M. J. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.06039 · Cited by 124 · see citing works
Pregnancy-induced insulin resistance in the rat: assessment by glucose clamp technique
Leturque, A., Burnol, A., Ferré, P., & Girard, J. R. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.246.1.e25 · Cited by 116 · see citing works
Drago, F., Leo, F., & Giardina, L. (1999) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(98)00032-7 · Cited by 111 · see citing works
Inheritance of Diabetes Mellitus as Consequence of Gestational Hyperglycemia in Rats
Gauguier, D., Bihoreau, M., Ktorza, A., Berthault, M., & Picon, L. (1990) · Diabetes · doi:10.2337/diab.39.6.734 · Cited by 108 · see citing works
Shift work, duration of pregnancy, and birth weight:
Zhu, J. L., Hjøllund, N. H., & Olsen, J. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2003.12.002 · Cited by 106 · see citing works
Regulation of hepatic enzymes and insulin levels in offspring of rat dams fed a reduced-protein diet
Desai, M., Byrne, C. D., Meeran, K. M., Martenz, N. D., Bloom, S., & Hales, C. N. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.273.4.g899 · Cited by 106 · see citing works
Work Schedule During Pregnancy and Spontaneous Abortion
Whelan, E. A., Lawson, C. C., Grajewski, B. A., Hibert, E. N. L., Spiegelman, D. L., & Rich-Edwards, J. W. (2007) · Epidemiology · doi:10.1097/01.ede.0000259988.77314.a4 · Cited by 97 · see citing works
Evidence for an insulin resistance in the adult offspring of pregnant streptozotocin-diabetic rats
Holemans, K., Aerts, L., & Van Assche, F. A. (1991) · Diabetologia · doi:10.1007/bf00500377 · Cited by 97 · see citing works
Repeated light-dark shifts speed up body weight gain in male F344 rats
Tsai, L., Tsai, Y., Hwang, K., Huang, Y.-W., & Tzeng, J.-E. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00603.2004 · Cited by 92 · see citing works
Occupational factors and risk of preterm birth in nurses
Lawson, C. C., Whelan, E. A., Hibert, E. N. L., et al. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.08.006 · Cited by 90 · see citing works
Sutton, G. M., Centanni, A. V., & Butler, A. A. (2010) · Endocrinology · doi:10.1210/en.2009-1133 · Cited by 85 · see citing works
Prematurity and Work in Pregnancy
McDonald, A. D., McDonald, J. C., Armstrong, B., Cherry, N., Nolin, A. D., & ROBERT, D. (1988) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198808000-00007 · Cited by 85 · see citing works
Oh, W., Gelardi, N. L., & Cha, C. (1988) · Metabolism · doi:10.1016/0026-0495(88)90192-8 · Cited by 74 · see citing works
Animal models for clinical and gestational diabetes: maternal and fetal outcomes
Kiss, A. C. I., Lima, P. H. O., Sinzato, Y. K., Takaku, M., Takeno, M. A., Rudge, M. V. C., & Damasceno, D. C. (2009) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-1-21 · Cited by 71 · see citing works
Gender-specific programmed hepatic lipid dysregulation in intrauterine growth-restricted offspring
Choi, G. Y., Tosh, D. N., Garg, A., et al. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.02.024 · Cited by 64 · see citing works
Mokhtari-Soulimane, N. A., Guermouche, B., Yessoufou, A., Saker, M., Moutairou, K., Hichami, A., Merzouk, H., & Khan, N. A. (2005) · Clinical Science · doi:10.1042/cs20050028 · Cited by 63 · see citing works
The offspring of gestational diabetes
Carrapato, M. (2003) · Journal of Perinatal Medicine · doi:10.1515/jpm.2003.001 · Cited by 62 · see citing works
The endocrine pancreas in virgin and pregnant offspring of diabetic pregnant rats
Aerts, L., Vercruysse, L., & Van Assche, F. A. (1997) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(97)00080-6 · Cited by 55 · see citing works
Cabrera, R. J., Rodríguez-Echandía, E. L., Jatuff, A. S. G., & Fóscolo, M. R. (1999) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x1999001000009 · Cited by 53 · see citing works
Orozco-Solís, R., de Matos, R. J. B., de Souza, S. L., Grit, I., Kaeffer, B., de Castro, R. M., & Bolaños‐Jiménez, F. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.223 · Cited by 52 · see citing works
Joseph, V., Mamet, J., Lee, F., Dalmaz, Y., & Reeth, O. V. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.022236 · Cited by 40 · see citing works
Effects of maternal immobilization stress on birth weight and glucose homeostasis in the offspring
D’mello, A. P., & Liu, Y. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.10.003 · Cited by 39 · see citing works
Repercussions of mild diabetes on pregnancy in Wistar rats and on the fetal development
Saito, F. H., Damasceno, D. C., Kempinas, W. D. G., Morceli, G., Sinzato, Y. K., Taylor, K. N., & Rudge, M. V. C. (2010) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-2-26 · Cited by 39 · see citing works
The impact of fetal size and length of gestation on 6‐sulphatoxymelatonin excretion in adult life
Kennaway, D. J., Flanagan, D., Moore, V., et al. (2001) · Journal of Pineal Research · doi:10.1034/j.1600-079x.2001.300308.x · Cited by 35 · see citing works
Self-citationGlucose and Insulin Tolerance Tests in the Rat on Different Days of Gestation
Muñoz, C., López-Luna, P., & Herrera, E. (2009) · Biology of the Neonate · doi:10.1159/000244248 · Cited by 33 · see citing works
Szántóová, K., Zeman, M., Veselá, A., & Herichová, I. (2010) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-010-0636-x · Cited by 28 · see citing works
Inhibition of N-glycan processing alters axonal transport of synaptic glycoproteins in vivo.
McFarlane, I., Breen, K. C., Giamberardino, L. D., & Moya, K. L. (2000) · PubMed · Cited by 27 · see citing works
Merzouk, H., Madani, S., Boualga, A., Prost, J., Bouchenak, M., & Belleville, J. (2001) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)31606-0 · Cited by 27 · see citing works
Peters (2019) · doi:10.26481/dis.20190111vp · Cited by 23 · see citing works
Prenatal exposure to SKF-38393 alters the response to light of adult rats
Ferguson, S. A., & Kennaway, D. J. (2000) · Neuroreport · doi:10.1097/00001756-200005150-00035 · Cited by 10 · see citing works
Self-citationOccupational Factors and Risk of Preterm Birth in Nurses
Lawson, C. C., Whelan, E. A., Hibert, E. N. L., et al. (2009) · Obstetric Anesthesia Digest · doi:10.1097/01.aoa.0000358383.70015.57 · Cited by 8 · see citing works
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Reiter, R. J., Tan, D. X., Korkmaz, A., & Rosales-Corral, S. A. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmt054 · Cited by 371 · see citing works
Health Consequences of Circadian Disruption in Humans and Animal Models
Evans, J. A., & Davidson, A. J. (2013) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-396971-2.00010-5 · Cited by 291 · see citing works
Circadian rhythms in the fetus
Serón-Ferré, M., Mendez, N., Abarzua-Catalan, L., Vilches, N., Valenzuela, F. J., Reynolds, H. E., Llanos, A. J., Rojas, A., Valenzuela, G. J., & Torres-Farfan, C. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.039 · Cited by 186 · see citing works
Smarr, B. L., Grant, A. D., Perez, L., Zucker, I., & Kriegsfeld, L. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-03406-4 · Cited by 86 · see citing works
Vilches, N., Spichiger, C., Mendez, N., Abarzua-Catalan, L., Galdames, H. A., Hazlerigg, D. G., Richter, H. G., & Torres-Farfan, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091313 · Cited by 86 · see citing works
Varcoe, T. J., Boden, M. J., Voultsios, A., Salkeld, M. D., Rattanatray, L., & Kennaway, D. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053800 · Cited by 78 · see citing works
Self-citationSpichiger, C., Torres-Farfan, C., Galdames, H. A., Mendez, N., Alonso-Vazquez, P., & Richter, H. G. (2015) · Physiological Genomics · doi:10.1152/physiolgenomics.00023.2015 · Cited by 34 · see citing works
- Authors
- Varcoe, T. J., Wight, N., Voultsios, A., Salkeld, M. D., & Kennaway, D. J.
- Affiliations
- The University of Adelaide (AU)
- Corresponding author
- Varcoe, Tamara J.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-04-06
- Volume
- 6
- Issue
- 4
- Pages
- e18504
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3071829
- OpenAlex
- W1974960190
- Cited by
- 147
- References
- 53
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 6 · 2023: 10 · 2022: 11 · 2021: 11 · 2020: 26 · 2019: 9 · 2018: 7 · 2017: 11 · 2016: 7 · 2015: 10 · 2014: 5 · 2013: 9 · 2012: 8
- FWCI
- 6.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Children's Hospital Foundation
- Women's and Children's Hospital Foundation
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- shift work, prenatal exposure, adult offspring, impaired glucose tolerance, insulin resistance, hyperleptinemia, hyperinsulinemia, adiposity, circadian rhythm disruption, sex differences, metabolic programming, insulin secretion, insulin tolerance test, glucose tolerance test
- MeSH terms
- Aging, Animals, Animals, Newborn, Behavior, Animal, Body Composition, Circadian Rhythm, Female, Glucose Tolerance Test, Insulin Resistance, Male, Nervous System, Pregnancy, Pregnancy Outcome, Time Factors, Rats, Wistar, Photoperiod, Glucose Intolerance, Rats
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