Advances in the research field of osteoporosis in cold areas

Abstract

While osteoporosis is a chronic disease caused by multiple factors, it is also a risk factor for fractures. At present, numerous risk factors for osteoporosis and secondary fractures have been identified, including sunlight, physical fitness, gender, age, trauma, dietary habits, tobacco, alcohol, drugs, air quality, and genetics. Despite that factors such as long winters, short daylight hours, less daily physical activity, air pollution, low calcium and high salt diet, and sedentary lifestyle could negatively impact the bones of residents in the alpine regions of northern China, the direct effect of low-temperature stimulation on bone growth and development remains unclear. In this study, by reviewing current research progress related to osteoporosis and fracture risk in northern China, we proposed appropriate preventive measures for different risk factors to reduce the occurrence of osteoporosis and fracture in cold areas of northern China.

Keywords

osteoporosis / cold areas / cold stimulation / bone metabolism

References

[[1]] Rachner T D, Khosla S, Hofbauer L C. Osteoporosis: now and the future. Lancet, 2011; 377: 1276-1287.

[[2]] Chen P, Li Z, Hu Y. Prevalence of osteoporosis in China: a meta-analysis and systematic review. BMC Public Health, 2016; 16: 1039.

[[3]] Al-Azzani W, Mak D A M, William R, et al. Epidemic of fractures during a period of snow and ice: has anything changed 33 years on? BMJ Open, 2016; 6(9): e010582.

[[4]] Johnson N, Stirling E R, Dias J J. The effect of mean annual temperature on the incidence of distal radial fractures. Journal of Hand Surgery (European Volume), 2018; 43(9): 983-987.

[[5]] Flinkkila T, Sirnio K, Hippi M, et al. Epidemiology and seasonal variation of distal radius fractures in Oulu, Finland. Osteoporps Int, 2011; 22(8): 2307-2312.

[[6]] Cheng S Y, Levy A R, Lefaivre K A, et al. Geographic trends in incidence of hip fractures: a comprehensive literature review. Osteoporps Int, 2011; 22(10): 2575-2586.

[[7]] Eastell R, O’Neill T W, Hofbauer L C, et al. Postmenopausal osteoporosis. Nat Rev Dis Primers, 2016; 2: 16069.

[[8]] Wahl D A, Cooper C, Ebeling P R, et al. A global representation of vitamin D status in healthy populations. Arch Osteoporos, 2012; 7: 155-172.

[[9]] Balk E M, Adam G P, Langberg V N, et al. Global dietary calcium intake among adults: a systematic review. Osteoporos Int, 2017; 28: 3315-3324.

[[10]] Chevalier C, Kieser S, Colakoglu M, et al. Warmth prevents bone loss through the gut microbiota. Cell Metabolism, 2020; 32(4): 575-590.

[[11]] Lips P. Vitamin D physiology. Prog Biophys Mol Biol, 2006; 92(1): 4-8.

[[12]] Vieth R. Weaker bones and white skin as adaptions to improve anthropological “fitness” for northern environments. Osteoporosis, 2020; 31: 617-624.

[[13]] Lips P, Duong T, Oleksik A, et al. A global study of vitamin D status and parathyroid function in postmenopausal women with osteoporosis: baseline data from the multiple outcomes of raloxifene evaluation clinical trial. J Clin Endocrinol Metab, 2001; 86(3): 1212-1221.

[[14]] Grootjans-Geerts I. Hypovitaminosis D: a veiled diagnosis. Nederlands Tijdschrift Voor Geneeskunde, 2001; 145(51): 2057-2060.

[[15]] Gannage-Yared M H, Chemali R, Yaacoub N, et al. Hypovitaminosis D in a sunny country: relation to lifestyle and bone markers. J Bone Miner Res, 2000; 15(9): 1856-1862.

[[16]] Garcia-Dorta A, Medina-Vega L, Villacampa-Jimenez J J, et al. Baseline levels of vitamin D in a healthy population from a region with high solar irradiation. Nutrients, 2021; 13(5): 1647.

[[17]] Medicine I O. Dietary reference intakes for calcium and vitamin D, Washington, DC, USA: The National Academies Press, 2011.

[[18]] Souberbielle J C, Massart C, Brailly-Tabard B, et al. Prevalence and determinants of vitamin D deficiency in healthy French adults: the VARIETE study. Endocrine, 2016; 53(2): 543-550.

[[19]] Jiang W, Wu D B, Xiao G B, et al. An epidemiology survey of vitamin D deficiency and its influencing factors. Med Clin (Barc), 2020; 154(1): 7-12.

[[20]] Xie Z J, Xia W B, Zhang Z L, et al. Prevalence of vitamin D inadequacy among Chinese postmenopausal women: a nationwide, multicenter, cross-sectional study. Frontiers in Endocrinology, 2019; 9: 782.

[[21]] Wigertz K, Palacios C, Jackman L A, et al. Racial differences in calcium retention in response to dietary salt in adolescent girls. Am J Clin Nutr, 2005; 81(4): 845-850.

[[22]] Park M, Lee J S, Lee J H, et al. Prevalence and risk factors of chronic otitis media: the Korean national health and nutrition examination survey 2010-2012. PloS One, 2015; 10(5): e0125905.

[[23]] van der Wijst J, Tutakhel O A Z, Bos C, et al. Effects of a high-sodium/low-potassium diet on renal calcium, magnesium, and phosphate handling. Am J Physiol Renal physiol, 2018; 315(1): F110-F122.

[[24]] Shortt C, Madden A, Flynn A, et al. Influence of dietary sodium intake on urinary calcium excretion in selected Irish individuals. Eur J Clin Nutr, 1988; 42(7): 595-603.

[[25]] Burger H, Grobbee D E, Drueke T. Osteoporosis and salt intake. Nutr Metab Cardiovasc Dis, 2000; 10(1): 46-53.

[[26]] Tiyasatkulkovit W, Aksornthong S, Adulyaritthikul P, et al. Excessive salt consumption causes systemic calcium mishandling and worsens microarchitecture and strength of long bones in rats. Sci Rep, 2021; 11(1): 1850.

[[27]] Wu L, Luthringer B J C, Feyerabend F, et al. Increased levels of sodium chloride directly increase osteoclastic differentiation and resorption in mice and men. Osteoporos Int, 2017; 28(11): 3215-3228.

[[28]] Hanley D A, Whiting S J. Does a high dietary acid content cause bone loss, and can bone loss be prevented with an alkaline diet? J Clin Densitom, 2013; 16(4): 420-425.

[[29]] Fenton T R, Lyon A W, Eliasziw M, et al. Meta-analysis of the effect of the acid-ash hypothesis of osteoporosis on calcium balance. J Bone Miner Res, 2009; 24(11): 1835-1840.

[[30]] Nicoll R, Howard J M. The acid-ash hypothesis revisited: a reassessment of the impact of dietary acidity on bone. J Bone Miner Metab, 2014; 32(5): 469-475.

[[31]] Lombardi G, Ziemann E, Banfi G. Physical activity and bone health: what is the role of immune system? A narrative review of the third way. Front Endocrinol (Lausanne), 2019; 10: 60.

[[32]] Sheng B, Li X, Nussler A K, et al. The relationship between healthy lifestyles and bone health: A narrative review. Medicine (Baltimore), 2021; 100(8): e24684.

[[33]] Weaver C M, Gordon C M, Janz K F, et al. The national osteoporosis foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int, 2016; 27: 1281-1386.

[[34]] Serrat M A. Environmental temperature impact on bone and cartilage growth. Compr Physiol, 2014; 4(2): 621-655.

[[35]] Lazenby R A. Bone loss, traditional diet, and cold adaptation in Arctic populations. Am J Hum Biol, 1997; 9(3): 329-341.

[[36]] Fedorenko A, Lishko P V, Kirichok Y. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell, 2012; 151(2): 400-413.

[[37]] Iwaniec U T, Philbrick K A, Wong C P, et al. Room temperature housing results in premature cancellous bone loss in growing female mice: implications for the mouse as a preclinical model for age-related bone loss. Osteoporos Int, 2016; 27(10): 3091-3101.

[[38]] Motyl K J, Bishop K A, DeMambro V E, et al. Altered thermogenesis and impaired bone remodeling in misty mice. J Bone Miner Res, 2013; 28(9): 1885-1897.

[[39]] Nasoori A, Okamatsu-Ogura Y, Shimozuru M, et al. Hibernating bear serum hinders osteoclastogenesis in-vitro. PLoS ONE, 2020; 15(8): e0238132.

[[40]] Straburzynska-Lupa A, Cison T, Gomarasca M, et al. Sclerostin and bone remodeling biomarkers responses to whole-body cryotherapy (-110 degrees C) in healthy young men with different physical fitness levels. Sci Rep, 2021; 11: 16156.

[[41]] Shi X M, Blair H C, Yang X, et al. Tandem repeat of C/EBP binding sites mediates PPARgamma 2 gene transcription in glucocorticoid-induced adipocyte differentiation. J Cell Biochem, 2000; 76(3): 518-527.

[[42]] Veldhuis-Vlug A G, Rosen C J. Clinical implications of bone marrow adiposity. J Intern Med, 2018; 283(2): 121-139.

[[43]] Kovanicova Z, Karhanek M, Kurdiova T, et al. Metabolomic analysis reveals changes in plasma metabolites in response to acute cold stress and their relationships to metabolic health in cold-acclimatized humans. Metabolites, 2021; 11(9): 619.

[[44]] Lee P, Linderman J D, Smith S, et al. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab, 2014; 19(2): 302-309.

[[45]] Razzoli M, Emmett M J, Lazar M A, et al. Beta-Adrenergic receptors control brown adipose UCP-1 tone and cold response without affecting its circadian rhythmicity. Faseb J, 2018; 32(10): 5640-5646.

[[46]] Nguyen A D, Lee N J, Wee N K Y, et al. Uncoupling protein-1 is protective of bone mass under mild cold stress conditions. Bone, 2018; 106: 167-178.

[[47]] Calton E K, Soares M J, James A P, et al. The potential role of irisin in the thermoregulatory responses to mild cold exposure in adults. Am J Hum Biol, 2016; 28(5): 699-704.

[[48]] Wang F S, Wu R W, Chen Y S, et al. Biophysical modulation of the mitochondrial metabolism and redox in bone homeostasis and osteoporosis: how biophysics converts into bioenergetics. Antioxidants, 2021; 10(9): 1394.

[[49]] Kornel A, Den Hartogh D J, Klentrou P, et al. Role of the myokine irisin on bone homeostasis: review of the current evidence. International Journal of Molecular Sciences, 2021; 22(17): 9136.

[[50]] Arefanian H, Al-Khairi I, Khalaf N A, et al. Increased expression level of ANGPTL8 in white adipose tissue under acute and chronic cold treatment, 2021; 20: 117.

[[51]] Li W M, Han C L, Liu C, et al. ANGPTL2 deletion inhibits osteoclast generation by modulating NF-kappaB/MAPKs/Cyclin pathways. Biochem Biophys Res Commun, 2018; 503(3): 1471-1477.

[[52]] Kadomatsu T, Oike Y. Roles of angiopoietin-like proteins in regulation of stem cell activity. J Biochem, 2019; 165(4): 309-315.

[[53]] Lu X, Lu J, Zhang L, et al. Effect of ANGPTL7 on proliferation and differentiation of MC3T3-E1 cells. Med Sci Monit, 2019; 25: 9524-9530.

[[54]] Clapham D E. TRP channels as cellular sensors. Nature, 2003; 426: 517-524.

[[55]] Carvalho A L, Treyball A, Brooks D J, et al. TRPM8 modulates temperature regulation in a sex-dependent manner without affecting cold-induced bone loss. PLoS One, 2021; 16: e0231060.

[[56]] Yu B, Huo L, Liu Y, et al. PGC-1alpha controls skeletal stem cell fate and bone-fat balance in osteoporosis and skeletal aging by inducing TAZ. Cell Stem Cell, 2018; 23(4): 193-209.

[[57]] Labbé S M, Mouchiroud M, Caron A, et al. mTORC1 is required for brown adipose tissue recruitment and metabolic adaptation to cold. Sci Rep, 2016; 6: 37223.

[[58]] Cong P, Liu Y, Liu N, et al. Cold exposure induced oxidative stress and apoptosis in the myocardium by inhibiting the Nrf2-Keap 1 signaling pathway. BMC Cardiovascular Disorders, 2018; 18(1): 36.

[[59]] Sanchez-de-Diego C, Pedrazza L, Pimenta-Lopes C, et al. NRF2 function in osteocytes is required for bone homeostasis and drives osteocytic gene expression. Redox Biology, 2021; 40: 101845.

[[60]] Zhou H, Yang X, Wang N, et al. Tigogenin inhibits adipocytic differentiation and induces osteoblastic differentiation in mouse bone marrow stromal cells. Mol Cell Endocrinol, 2007; 270(1-2): 17-22.

[[61]] Fujiwara Y, Denlinger D L. p38 MAPK is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly Sarcophaga crassipalpis. J Exp Biol, 2007; 210(pt 18): 3295-3300.

[[62]] Nie Y, Yan Z, Yan W, et al. Cold exposure stimulates lipid metabolism, induces inflammatory response in the adipose tissue of mice and promotes the osteogenic differentiation of BMMSCs via the p 38 MAPK pathway in vitro. Int J Clin Exp Pathol, 2015; 8(9): 10875-10886.

[[63]] Moreno-Navarrete J M, Fernandez-Real J M. The gut microbiota modulates both browning of white adipose tissue and the activity of brown adipose tissue. Rev Endocr Metab Disord, 2019; 20(4): 387-397.