Bone structure and strength are enhanced in rats programmed by early overfeeding

Hormone and Metabolic Research

Volumn 46, Issue 4, 2014, Pages 259-268

  De Albuquerque Maia, L ^a   Lisboa, P C ^a   De Oliveira, E ^a   Da Conceicao E P S ^a   Lima, I C B ^b   Lopes, R T ^b   Ruffoni, L D G ^c   Nonaka, K O ^c   De Moura, E G ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

Author keywords

bone; early overfeeding; programming

Indexed keywords

CALCIUM ION; COLECALCIFEROL; COLLAGEN TYPE 1; LEPTIN; OSTEOCALCIN; COLLAGEN TYPE I TRIMERIC CROSS-LINKED PEPTIDE; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMECHANICS; BODY WEIGHT; BONE DENSITY; BONE MASS; BONE MINERAL; BONE STRENGTH; BONE STRUCTURE; BONE TISSUE; CARBOXY TERMINAL SEQUENCE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; FAT MASS; FEMUR; FEMUR HEAD; HYPERPHAGIA; INTRAABDOMINAL FAT; LACTATION; LEAN BODY WEIGHT; LITTER SIZE; LUMBAR VERTEBRA; MALE; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; OBESITY; PERINATAL STRESS; PRIORITY JOURNAL; PROGENY; RAT; VERTEBRA BODY; WEANING; ANIMAL; FEEDING BEHAVIOR; FEMALE; METABOLISM; NEWBORN; ORGAN SIZE; OVERNUTRITION; PATHOLOGY; PATHOPHYSIOLOGY; PHOTON ABSORPTIOMETRY; RADIOGRAPHY; WEIGHT BEARING; WISTAR RAT;

RATTUS;

ABSORPTIOMETRY, PHOTON; ANIMALS; ANIMALS, NEWBORN; BIOMECHANICAL PHENOMENA; BODY WEIGHT; BONE DENSITY; COLLAGEN TYPE I; FEEDING BEHAVIOR; FEMALE; FEMUR; INTRA-ABDOMINAL FAT; MALE; ORGAN SIZE; OSTEOCALCIN; OVERNUTRITION; PEPTIDES; RATS, WISTAR; WEANING; WEIGHT-BEARING; X-RAY MICROTOMOGRAPHY;

EID: 84899488595     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0034-1368728     Document Type: Article

References (82)

1. Rosen C. J., Bouxsein M. L. Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol: 2006; 2 35 43 (Pubitemid 43153647)
2. Chinn S., Rona R. R. Prevalence and trends in overweight and obesity in three cross-sectional studies of British children 1974-94. BMJ: 2001; 322 24 26 (Pubitemid 32066253)
3. de Onis M., Blössner M., Borghi E. Global prevalence and trends of overweight and obesity among preschool children. Am J Clin Nutr: 2010; 92 1257 1264
4. Whitaker R. C., Pepe M. S., Wright J. A., Seidel K. D., Dietz W. H. Early adiposity rebound and the risk of adult obesity. Pediatrics: 1998; 101 E5
5. Krassas G. E., Tzotzas T. Do obese children become obese adults: childhood predictors of adult disease. Pediatr Endocrinol Rev: 2004; 3 455 459 (Pubitemid 40204058)
6. Dörner G., Hagen N., Witthuhn W. Early postnatal overfeeding as an etiopathogenetic factor in adult obesity. Acta Biol Med Ger: 1976; 35 799 803
7. Rodrigues A. L., de Moura E. G., Passos M. C., Dutra S. C., Lisboa P. C. Postnatal early overnutrition changes the leptin signaling pathway in the hypothalamic-pituitary-thyroid axis of young and adult rats. J Physiol: 2009; 587 2647 2661
8. Rodrigues A. L., de Moura E. G., Passos M. C., Trevenzoli I. H., da Conceição E. P., Bonono I. T., Neto J. F., Lisboa P. C. Postnatal early overfeeding induces hypothalamic higher SOCS3 expression and lower STAT3 activity in adult rats. J Nutr Biochem: 2011; 22 109 117
9. Barker D. J. The developmental origins of adult disease. J Am Coll Nutr: 2003; 23 588S 595S
10. Moura E. G., Passos M. C. Neonatal programming of body weight regulation and energetic metabolism. Biosci Rep: 2005; 25 251 269 (Pubitemid 41609285)
11. de Moura E. G., Lisboa P. C., Passos M. C. Neonatal programming of neuroimmunomodulation-role of adipocytokines and neuropeptides. Neuroimmunomodulation: 2008; 15 176a 188a
12. Jones G. Early life nutrition and bone development in children. Nestle Nutr Workshop Ser Pediatr Program: 2011; 68 227 233
13. Devlin M. J., Grasemann C., Cloutier A. M., Louis L., Alm C., Palmert M. R., Bouxsein M. L. Maternal perinatal diet induces developmental programming of bone architecture. J Endocrinol: 2013; 217 69 81
14. NIH Osteoporosis prevention, diagnosis, and therapy. NIH Consensus Statement: 2000; 17 1 45
15. Eastell R., Lambert H. Diet and healthy bones. Calcif Tissue Int: 2002; 70 400 404 (Pubitemid 36935441)
16. Plagemann A., Heidrich I., Götz F., Rohde W., Dörner G. Obesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding. Exp Clin Endocrinol: 1992; 99 154 158
17. Davidowa H., Plagemann A. Hypothalamic neurons of postnatally overfed, overweight rats respond differentially to corticotropin-releasing hormones. Neurosci Lett: 2004; 371 64 68 (Pubitemid 39410516)
18. Boullu-Ciocca S., Dutour A., Guillaume V., Achard V., Oliver C., Grino M. Postnatal diet-induced obesity in rats upregulates systemic and adipose tissue glucocorticoid metabolism during development and in adulthood: its relationship with the metabolic syndrome. Diabetes: 2005; 54 197 203 (Pubitemid 40105113)
19. Conceição E. P., Moura E. G., Trevenzoli I. H., Peixoto-Silva N., Pinheiro C. R., Younes-Rapozo V., Oliveira E., Lisboa P. C. Neonatal overfeeding causes higher adrenal catecholamine content and basal secretion and liver dysfunction in adult rats. Eur J Nutr: 2013; 52 1393 1404
20. Conceição E. P., Franco J. G., Oliveira E., Resende A. C., Amaral T. A., Peixoto-Silva N., Passos M. C., Moura E. G., Lisboa P. C. Oxidative stress programming in a rat model of postnatal early overnutrition-role of insulin resistance. J Nutr Biochem: 2013; 24 81 87
21. Steppan C. M., Crawford D. T., Chidsey-Frink K. L., Ke H., Swick A. G. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept: 2000; 92 73 78
22. Thrailkill K. M., Lumpkin C. K. Jr., Bunn R. C., Kemp S. F., Fowlkes J. L. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab: 2005; 289 E735 E745 (Pubitemid 41504371)
23. Marques R. G., Morales M. M., Petroianu A. Brazilian law for scientific use of animals. Acta Cir Bras: 2009; 24 69 74
24. Lukaski H. C., Hall C. B., Marchello M. J., Sider W. A. Validation of dual X-ray absorptiometry for body-composition assessment of rats exposed to dietary stressors. Nutrition: 2001; 17 607 613 (Pubitemid 32633793)
25. Sirois I., Cheung A. M., Ward W. E. Biomechanical bone strength and bone mass in young male and female rats fed a fish oil diet. Prostaglandins Leukot Essent Fatty Acids: 2003; 68 415 442
26. Feldkamp L. A., Davis L. C., Kress J. W. Practical cone beam algorithm. J Opt Soc Am A: 1984; 1 612 619
27. Ciarelli T. E., Fyhrie D. P., Schaffler M. B., Goldstein S. A. Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res: 2000; 15 32 40 (Pubitemid 30026930)
28. Trebacz H., Zduneck A. Three-point bending and acoustic emission study of adult rat femora after immobilization and free remobilization. J Biomech: 2006; 39 237 245 (Pubitemid 41728997)
29. Haarbo J., Gotfredsen A., Hassager C., Christiansen C. Validation of body composition by dual energy X-ray absorptiometry (DEXA). Clin Physiol: 1991; 11 331 341
30. Lac G., Cavalie H., Ebal E., Michaux O. Effects of a high fat diet on bone of growing rats Correlations between visceral fat, adiponectin and bone mass density. Lipids Health Dis: 2008; 7 1 4
31. Pluijm S. M., Visser M., Smit J. H., Popp-Snijders C., Roos J. C., Lips P. Determinants of bone mineral density in older men and women: body composition as mediator. J Bone Miner Res: 2001; 16 2142 2151 (Pubitemid 32995407)
32. Reid I. R. Relationships among body mass, its components, and bone. Bone: 2002; 31 547 555 (Pubitemid 35449695)
33. Clark E. M., Ness A. R., Tobias J. H. Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab: 2006; 91 2534 2541 (Pubitemid 44024614)
34. Albala C., Yanez M., Devoto E., Sostin C., Zeballos L., Santos J. L. Obesity as a protective factor for postmenopausal osteoporosis. Int J Obes Relat Metab Disord: 1996; 20 1027 1032 (Pubitemid 26366457)
35. Klein K. O., Larmore K. A., de Lancey E., Brown J. M., Considine R. V., Hassink S. G. Effect of obesity on estradiol level, and its relationship to leptin, bone maturation, and bone mineral density in children. J Clin Endocrinol Metab: 1998; 83 3469 3475 (Pubitemid 28500873)
36. Halaas J. L., Gajiwala K. S., Maffei M., Cohen S. L., Chait B. T., Rabinowitz D., Lallone R. L., Burley S. K., Friedman J. M. Weight-reducing effects of the plasma protein encoded by the obese gene. Science: 1995; 269 543 546
37. Thomas T., Burguera B., Melton L. J. 3rd, Atkinson E. J., O'Fallon W. M., Riggs B. L., Khosla S. Role of serum leptin, insulin, and estrogen levels as potential mediators of the relationship between fat mass and bone mineral density. Bone: 2001; 29 114 120 (Pubitemid 32734491)
38. Blain H., Vuillemin A., Guillemin F., Durant R., Hanesse B., de Talance N., Doucet B., Jeandel C. Serum leptin level is a predictor of bone mineral density in postmenopausal women. J Clin Endocrinol Metab: 2002; 87 1030 1035 (Pubitemid 36121060)
39. Maor G., Rochwerger M., Segev Y., Phillip M. Leptin acts as a growth factor on the chondrocytes of skeletal growth centers. J Bone Miner Res: 2002; 17 1034 1043 (Pubitemid 34535141)
40. Plagemann A., Harder T., Rake A., Waas T., Melchior K., Ziska T., Rohde W., Dörner G. Observations on the orexigenic hypothalamic neuropeptide Y-system in neonatally overfed weanling rats. J Neuroendocrinol: 1999; 11 541 546 (Pubitemid 29312847)
41. Gogakos A. I., Duncan Bassett J. H., Williams G. R. Thyroid and bone. Arch Biochem Biophys: 2010; 503 129 136
42. Ben-Sholmo A., Hagag P., Evans S., Weiss M. Early postmenopausal bone loss in hyperthyroidism. Maturitas: 2001; 39 19 27 (Pubitemid 32635221)
43. Murphy E., Gluer C. C., Reid D. M., Felsenberg D., Roux C., Eastell R., Williams G. R. Thyroid function within the upper normal range is associated with reduced bone mineral density and an increased risk of nonvertebral fractures in healty euthyroid postmenopausal women. J Clin Endocrinol Metab: 2010; 95 3173 3181
44. Eriksen E. F., Moskelide L., Melsen F. Kinetics of trabecular bone resorption and formation in hypothyroidism: evidence for a positive balance per remodeling cycle. Bone: 1986; 7 101 108 (Pubitemid 16081132)
45. Madeira E., Mafort T. T., Madeira M., Guedes E. P., Moreira R. O., de Mendonça L. M., Lima I. C., de Pinho P. R., Lopes A. J., Farias M. L. Lean mass as a predictor of bone density and microarchitecture in adult obese individuals with metabolic syndrome. Bone: 2014; 59 89 92
46. Reid I. R., Ames R., Evans M. C., Sharpe S., Gamble G., France J. T., Lim T. M., Cundy T. F. Determinants of total body and regional bone mineral density in normal postmenopausal women-a key role for fat mass. J Clin Endocrinol Metab: 1992; 75 45 51
47. Iwaniec U. T., Dube M. G., Boghossian S., Song H., Helferich W. G., Turner R. T., Kalra S. P. Body mass influences cortical bone mass independent of leptin signaling. Bone: 2009; 44 404 412
48. Seeman E., Delmas P. D. Bone quality-the material and structural bias of bone strength and fragility. N Engl J Med: 2006; 354 2250 2261
49. Feldkamp L. A., Goldstein S. A., Parfitt A. M., Jesion G., Kleerekoper M. The direct examination of three dimensional bone architecture in vitro by computed tomography. J Bone Miner Res: 1989; 4 3 11 (Pubitemid 19079118)
50. Ma H., Turpeinen T., Silvennoinen M., Torvinen S., Rinnankoski-Tuikka R., Kainulainen H., Timonen J., Kujala U. M., Rahkila P., Suominen H. Effects of diet-induced obesity and voluntary wheel running on the microstructure of the murine distal femur. Nutr Metab (Lond): 2011; 8 1 11
51. Hildebrand T., Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc: 1997; 185 67 75 (Pubitemid 27060526)
52. Eckstein F., Matsuura M., Kuhn V., Priemel M., Müller R., Link T. M., Lochmüller E. M. Sex differences of human trabecular bone microstructure in aging are site-dependent. J Bone Miner Res: 2007; 22 817 824 (Pubitemid 351339741)
53. Xu Y., Li D., Chen Q., Fan Y. Full supervised learning for osteoporosis diagnosis using micro-CT images. Microsc Res Tech: 2013; 76 333 341
54. Saha P. K., Xu Y., Duan H., Heiner A., Liang G. Y. Volumetric topological analysis: A novel approach for trabecular bone classification on the continuum between plates and rods. IEEE Trans Med Imaging: 2010; 29 1821 1838
55. Kleerekoper M., Villanueva A. R., Stanciu J., Rao D. S., Parfitt A. M. The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tissue Int: 1985; 37 594 597 (Pubitemid 16197165)
56. Hahn M., Vogel M., Kempa M. P., Delling G. Trabecular bone pattern factor-a new parameter for simple quantification of bone microarchitecture. Bone: 1992; 13 327 330
57. Heep H., Wedemeyer C., Wegner A., Hofmeister S., von Knoch M. Differences in trabecular bone of leptin-deficient ob/ob mice in response to biomechanical loading. Int J Biol Sci: 2008; 4 169 175 (Pubitemid 351872044)
58. Brahmabhatt V., Rho J., Bernardis L., Gillespie R., Ziv I. The effects of dietary-induced obesity on the biomechanical properties of femora in male rats. Int J Obes Relat Metab Disord: 1998; 22 813 818 (Pubitemid 28359298)
59. Lee A. J., Hodges S., Eastell R. Measurement of osteocalcin. Ann Clin Biochem: 2000; 37 432 446 (Pubitemid 30426723)
60. Ip T. Y., Peterson J., Byrner R., Tou J. C. Bone responses to body weight and moderate treadmill exercising in growing male obese (fa/fa) and lean Zucker rats. J Musculoskelet Neuronal Interact: 2009; 9 155 166
61. Looker A. C., Bauer D. C., Chesnut C. H. III, Gundberg C. M., Hochberg M. C., Klee G., Kleerekoper M., Watts N. B., Bell N. H. Clinical use of biochemical markers of bone remodeling: current status and future directions. Osteoporos Int: 2000; 11 467 480
62. Egan E., Reilly T., Giacomoni M., Redmond L., Turner C. Bone mineral density among female sports participants. Bone: 2006; 38 227 233 (Pubitemid 43165789)
63. Bréban S., Chappard C., Jaffré C., Benhamou C. L. Hypoleptinaemia in extreme body mass models: the case of international rugby players. J Sci Med Sport: 2010; 13 479 484
64. Fukumoto S., Martin T. J. Bone as an endocrine organ. Trends Endocrinol Metab: 2009; 20 230 236
65. Lee N. K., Sowa H., Hinoi E., Ferron M., Ahn J. D., Confavreux C., Dacquin R., Mee P. J., McKee M. D., Jung D. Y., Zhang Z., Kim J. K., Mauvais-Jarvis F., Ducy P., Karsenty G. Endocrine regulation of energy metabolism by the skeleton. Cell: 2007; 130 456 469 (Pubitemid 47208519)
66. Lee N. K., Karsenty G. Reciprocal regulation of bone and energy metabolism. Trends Endocrinol Metab: 2008; 19 161 166 (Pubitemid 351847838)
67. Confavreux C. B., Levine R. L., Karsenty G. A paradigm of integrative physiology, the crosstalk between bone and energy metabolisms. Mol Cell Endocrinol: 2009; 310 21 29
68. Gravenstein K. S., Napora J. K., Short R. G., Ramachandran R., Carlson O. D., Metter E. J., Ferrucci L., Egan J. M., Chia C. W. Crosssectional evidence of a signaling pathway from bone homeostasis to glucose metabolism. J Clin Endocrinol Metab: 2011; 96 E884 E890
69. Kanazawa I., Yamaguchi T., Tada Y., Yamauchi M., Yano S., Sugimoto T. Serum osteocalcin level is positively associated with insulin sensitivity and secretion in patients with type 2 diabetes. Bone: 2011; 48 720 725
70. Reinehr T., de Sousa G., Alexy U., Kersting M., Andler W. Vitamin D status and parathyroid hormone in obese children before and after weight loss. Eur J Endocrinol: 2007; 157 225 232 (Pubitemid 47233129)
71. Bell N. H., Epstein S., Greene A., Shary J., Oexmann M. J., Shaw S. Evidence for alteration of the vitamin D-endocrine system in obese subjects. J Clin Invest: 1985; 76 370 373 (Pubitemid 15243466)
72. Parikh S. J., Edelman M., Uwaifo G. I., Freedman R. J., Semega-Janneh M., Reynolds J., Yanovski J. A. The relationship between obesity and serum 1,25-dihydroxyvitamin D concentrations in healthy adults. J Clin Endocrinol Metab: 2004; 89 1196 1199 (Pubitemid 38368412)
73. Lima N., da S., de Moura E. G., Passos M. C., Nogueira Neto F. J., Reis A. M., de Oliveira E., Lisboa P. C. Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr: 2011; 105 1405 1413
74. de Albuquerque Maia L., Lisboa P. C., de Oliveira E., da Silva Lima N., da Costa C. A., de Moura E. G. Two Models of Early Weaning Decreases Bone Structure by Different Changes in Hormonal Regulation of Bone Metabolism in Neonate Rat. Horm Metab Res: 2013; 45 332 337
75. Nobre J. L., Lisboa P. C., Lima Nda S., Franco J. G., Nogueira Neto J. F., de Moura E. G., de Oliveira E. Calcium supplementation prevents obesity, hyperleptinaemia and hyperglycaemia in adult rats programmed by early weaning. Br J Nutr: 2012; 107 979 988
76. Devlin M. J., Bouxsein M. L. Influence of pre-and peri-natal nutrition on skeletal acquisition and maintenance. Bone: 2012; 50 444 451
77. Paniagua M. A., Malphurs J. E., Samos L. F. BMI and low bone mass in an elderly male nursing home population. Clin Interv Aging: 2006; 1 283 287
78. Chung W., Lee J., Ryu O. H. Is the negative relationship between obesity and bone mineral content greater for older women? J Bone Miner Metab: 2013; 10.1007/s00774-013-0519-9
79. Gower B. A., Casazza K. Divergent effects of obesity on bone health. J Clin Densitom: 2013; 16 450 454
80. Pramojanee S. N., Phimphilai M., Kumphune S., Chattipakorn N., Chattipakorn S. C. Decreased jaw bone density and osteoblastic insulin signaling in a model of obesity. J Dent Res: 2013; 92 560 565
81. Hage R. E., Bachour F., Sebaaly A., Issa M., Zakhem E., Maalouf G. The Influence of Weight Status on Radial Bone Mineral Density in Lebanese Women. Calcif Tissue Int: 2013; 10.1007/s00223-013-9822-7
82. Salamat M. R., Salamat A. H., Abedi I., Janghorbani M. Relationship between Weight, Body Mass Index, and Bone Mineral Density in Men Referred for Dual-Energy X-Ray Absorptiometry Scan in Isfahan, Iran. J Osteoporos: 2013; 2013 205963