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Proton magnetic resonance spectroscopy shows lower intramyocellular lipid accumulation in middle-aged subjects predisposed to familial longevity
Abstract
Families predisposed to longevity show enhanced glucose tolerance and skeletal muscle insulin sensitivity compared with controls, independent of body composition and physical activity. Intramyocellular lipid (IMCL) accumulation in skeletal muscle has been associated with insulin resistance. Here, we assessed whether subjects enriched for familial longevity have lower IMCL levels. We determined IMCL levels in 48 subjects from the Leiden Longevity Study, comprising 24 offspring of nonagenarian siblings and 24 partners thereof as control subjects. IMCL levels were assessed noninvasively using short echo time proton magnetic resonance spectroscopy ((1)H-MRS) of the tibialis anterior muscle with a 7 Tesla human MR scanner. IMCL levels were calculated relative to the total creatine (tCr) CH3 signal. Physical activity was assessed using the International Physical Activity Questionnaire (IPAQ). After correction for age, sex, BMI, and physical activity, offspring of long-lived nonagenarian siblings tended to show lower IMCL levels compared with controls (IMCL/tCr: 3.1 ± 0.5 vs. 4.5 ± 0.5, respectively, P = 0.051). In a pairwise comparison, this difference reached statistical significance (P = 0.038). We conclude that offspring of nonagenarian siblings predisposed to longevity show lower IMCL levels compared with environmentally matched control subjects. Future research should focus on assessing what mechanisms may explain the lower IMCL levels in familial longevity.
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Offspring of Caucasian nonagenarian siblings predisposed to longevity had lower myosteatosis compared to matched controls.
“This study revealed that offspring of Caucasian nonagenarian siblings predisposed to longevity had lower myosteatosis compared to matched controls.”
From Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging (2020) · cites this paper as Wijsman et al., 2012
Myosteatosis is a novel marker of impaired survival.
“As first suggested by the Leiden Longevity Study, myosteatosis is a novel marker of impaired survival (Wijsman et al., 2012).”
From Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging (2020) · cites this paper as Wijsman et al., 2012
Citations
Cites
Impaired Mitochondrial Activity in the Insulin-Resistant Offspring of Patients with Type 2 Diabetes
Petersen, K. F., Dufour, S., Befroy, D., Garcia, R., & Shulman, G. I. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa031314 · Cited by 2,193
Mitochondrial dysfunction in the elderly: possible role in insulin resistance
Petersen, K. F., Befroy, D., Dufour, S., Dziura, J., Ariyan, C., Rothman, D. L., DiPietro, L., Cline, G. W., & Shulman, G. I. (2003) · Science · doi:10.1126/science.1082889 · Cited by 2,107
Hagströmer, M., Oja, P., & Sjöstróm, M. (2006) · Public Health Nutrition · doi:10.1079/phn2005898 · Cited by 2,078
Improved Method for Accurate and Efficient Quantification of MRS Data with Use of Prior Knowledge
Vanhamme, L., van den Boogaart, A., & Huffel, S. V. (1997) · Journal of Magnetic Resonance · doi:10.1006/jmre.1997.1244 · Cited by 1,631
Goodpaster, B. H. (2001) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.12.5755 · Cited by 1,194
Hyperinsulinaemia: the key feature of a cardiovascular and metabolic syndrome
Ferrannini, E., Haffner, S. M., Mitchell, B. D., & Stern, M. P. (1991) · Diabetologia · doi:10.1007/bf00403180 · Cited by 898
Jacob, S., Machann, J., Rett, K., Brechtel, K., Volk, A., Renn, W., Maerker, E., Matthaei, S., Schick, F., Claussen, C. D., et al. (1999) · Diabetes · doi:10.2337/diabetes.48.5.1113 · Cited by 643
Insulin resistance as a predictor of age-related diseases
Facchini, F. S., Hua, N., Abbasi, F., & Reaven, G. M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.8.7763 · Cited by 594
Schoenmaker, M., de Craen, A. J. M., de Meijer, P. H. E. M., Beekman, M., Blauw, G. J., Slagboom, P. E., & Westendorp, R. G. J. (2005) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201508 · Cited by 363
Insulin Action and Age: European Group for the Study of Insulin Resistance (EGIR)
Ferrannini, E., Vichi, S., Beck-Nielsen, H., Laakso, M., Paolisso, L., & Smith, G. (1996) · Diabetes · doi:10.2337/diab.45.7.947 · Cited by 353
Cardiac SSFP imaging at 3 Tesla
Schär, M., Kozerke, S., Fischer, S., & Boesiger, P. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20024 · Cited by 309
Schrauwen-Hinderling, V. B., Kooi, M. E., Hesselink, M. K. C., Jeneson, J. A. L., Backes, W. H., van Echteld, C. J. A., van Engelshoven, J. M. A., Mensink, M., & Schrauwen, P. (2007) · Diabetologia · doi:10.1007/s00125-006-0475-1 · Cited by 304
Cellular mechanism of insulin resistance: potential links with inflammation
Perseghin, G., Petersen, K. F., & Shulman, G. I. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802491 · Cited by 257
Westendorp, R. G. J., van Heemst, D., Rozing, M. P., Frölich, M., Mooijaart, S. P., Blauw, G. J., Beekman, M., Heijmans, B. T., de Craen, A. J. M., Slagboom, P. E., et al. (2009) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2009.02381.x · Cited by 257
Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state
van Loon, L. J. C., & Goodpaster, B. H. (2006) · Pflügers Archiv · doi:10.1007/s00424-005-1509-0 · Cited by 232
Thamer, C., Machann, J., Bachmann, O. P., Haap, M. M., Dahl, D. B., Wietek, B., Tschritter, O., Niess, A. M., Brechtel, K., Fritsche, A., et al. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021674 · Cited by 228
Role of proton MR for the study of muscle lipid metabolism
Boesch, C., Machann, J., Vermathen, P., & Schick, F. (2006) · NMR in Biomedicine · doi:10.1002/nbm.1096 · Cited by 207
Perseghin, G., Lattuada, G., Danna, M., Sereni, L. P., Maffi, P., COBELLI, F. D., Battezzati, A., Secchi, A., Maschio, A. D., & Luzi, L. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00279.2003 · Cited by 187
Glucose tolerance and insulin action in healthy centenarians
Paolisso, G., Gambardella, A., Ammendola, S., D’Amore, A., Balbi, V., Varricchio, M., & D'Onofrio, F. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.5.e890 · Cited by 161
High-fat diet, muscular lipotoxicity and insulin resistance
Schrauwen, P. (2007) · Proceedings of the Nutrition Society · doi:10.1017/s0029665107005277 · Cited by 153
Hwang, J.-H., Pan, J. W., Heydari, S., Hetherington, H. P., & Stein, D. T. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.4.1267 · Cited by 137
Familial longevity is marked by enhanced insulin sensitivity
Wijsman, C. A., Rozing, M. P., Streefland, T. C. M., le Cessie, S., Mooijaart, S. P., Slagboom, P. E., Westendorp, R. G. J., Pijl, H., van Heemst, D., & On behalf of the Leiden Longevity Study group (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00650.x · Cited by 120
De Feyter, H. M., van den Broek, N. M. A., Praet, S. F. E., Nicolay, K., van Loon, L. J. C., & Prompers, J. J. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0756 · Cited by 116
Rozing, M. P., Westendorp, R. G. J., de Craen, A. J. M., Frölich, M., de Goeij, M. C. M., Heijmans, B. T., Beekman, M., Wijsman, C. A., Mooijaart, S. P., Blauw, G. J., et al. (2010) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2010.02725.x · Cited by 83
Vermathen, P., Kreis, R., & Boesch, C. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10721 · Cited by 78
Human insulin/IGF-1 and familial longevity at middle age
Rozing, M. P., Westendorp, R. G. J., Frölich, M., de Craen, A. J. M., Beekman, M., Heijmans, B. T., Mooijaart, S. P., Blauw, G. J., Slagboom, P. E., van Heemst, D., et al. (2009) · Aging · doi:10.18632/aging.100071 · Cited by 72
Versluis, M. J., Kan, H. E., van Buchem, M. A., & WEBB, A. G. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22195 · Cited by 57
Ren, J., Sherry, A. D., & Malloy, C. R. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22345 · Cited by 47
Creatine supplementation???Part II: in vivo magnetic resonance spectroscopy
Kreis, R., Kamber, M., KOSTER, M., Felblinger, J., Slotboom, J., Hoppeler, H. H., & Boesch, C. (1999) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199912000-00012 · Cited by 46
Some properties of different skeletal muscle fiber types: comparison of reference bases
Kelso, T. B., HODGSON, D. R., Visscher, A. R., & Gollnick, P. D. (1987) · Journal of Applied Physiology · doi:10.1152/jappl.1987.62.4.1436 · Cited by 35
Seo, Y., Shinar, H., Morita, Y., & Navon, G. (1999) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(199909)42:3 · Cited by 19
Intramyocellular triglyceride content in man, influence of sex, obesity and glycaemic control
Haugaard, S. B., Mu, H., Vaag, A. A., & Madsbad, S. (2009) · European Journal of Endocrinology · doi:10.1530/eje-08-0931 · Cited by 17
Salgin, B., Sleigh, A., Williams, R. M., Jackson, S. J., Bluck, L. J. C., Murgatroyd, P. R., Humphreys, S. M., Harding, S. G., Carpenter, T. A., & Dunger, D. B. (2008) · Clinical Science · doi:10.1042/cs20080563 · Cited by 11
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Lott, D. J., Forbes, S. C., Mathur, S., Germain, S. A., Senesac, C., Sweeney, H. L., Walter, G. A., & Vandenborne, K. (2014) · Neuromuscular Disorders · doi:10.1016/j.nmd.2014.03.013 · Cited by 41
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Ogon, I., Takebayashi, T., Takashima, H., Morita, T., Yoshimoto, M., Terashima, Y., & Yamashita, T. (2018) · Spine Surgery and Related Research · doi:10.22603/ssrr.2018-0023 · Cited by 29
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Sala, M. L., Kroft, L. J. M., Röell, B., van der Grond, J., Slagboom, P. E., Mooijaart, S. P., Roos, A., & van Heemst, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091085 · Cited by 9
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Metadata
- Authors
- Wijsman, C. A., van Opstal, A. M., Kan, H. E., Maier, A. B., Westendorp, R. G. J., Slagboom, P. E., Webb, A. G., Mooijaart, S. P., & van Heemst, D.
- Affiliations
- Department of Gerontology and Geriatrics;
- C. J. Gorter Center for High Field MRI, Department of Radiology;
- Netherlands Consortium for Healthy Ageing (NL)
- Leiden University Medical Center (NL)
- ORCID
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2012-02
- Volume
- 302
- Issue
- 3
- Pages
- E344-E348
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- OpenAlex
- W1997137435
- Cited by
- 24
- References
- 33
- Citations by year
- 2026: 1 · 2022: 1 · 2020: 4 · 2019: 1 · 2018: 3 · 2017: 2 · 2016: 4 · 2015: 2 · 2014: 3 · 2013: 2 · 2012: 1
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- VU Research Portal (submittedVersion)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- intramyocellular lipid, familial longevity, skeletal muscle, insulin sensitivity, insulin resistance, glucose tolerance, tibialis anterior, 1H NMR, physical activity, Leiden Longevity Study
- MeSH terms
- Aged, Family Health, Female, Humans, Insulin Resistance, Leg, Longevity, Male, Middle Aged, Motor Activity, Netherlands, Magnetic Resonance Spectroscopy, Surveys and Questionnaires, Cohort Studies, Body Mass Index, Matched-Pair Analysis, Muscle Fibers, Skeletal, Adult Children, Siblings, Lipid Metabolism
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