|BIOLOGICAL FACTOR AND NEURAL REGENERATION
|Year : 2020 | Volume
| Issue : 2 | Page : 90-97
Association of osteoporosis with different risk factors in a sample of Egyptian women
Nayera E Hassan1, Saneya A Wahba2, Mones M Abushady2, Samia A.W. Boseila2, Sahar A. El-Raufe El-Masry1, Enas R Abdelhamid2, Salwa R El-Batrawy1, Manal M Ali1, Aya Khalil1, Inas R El-Alameey3, Tarek S Ibrahim2
1 Department of Biological Anthropology, Medical Research Division, National Research Centre, Giza, Egypt
2 Child Health Department, Medical Research Division, National Research Centre, Giza, Egypt
3 Child Health Department, Medical Research Division, National Research Centre, Giza; Department of Clinical Nutrition, Faculty of Applied Medical Sciences, Taibah University, Medina, Saudi Arabia, Egypt
|Date of Submission||22-Oct-2020|
|Date of Decision||01-Nov-2020|
|Date of Acceptance||26-Nov-2020|
|Date of Web Publication||06-Feb-2021|
PhD Sahar A. El-Raufe El-Masry
Department of Biological Anthropology, National Research Centre, 33 El-Buhooth Street, Dokki, Giza, Cairo 12622
Source of Support: None, Conflict of Interest: None
Background/aim Both obesity and osteoporosis represent global health problems, as they are associated with major morbidity and mortality risks. The present work is aimed at assessing association of osteoporosis with different risk factors in a sample of Egyptian women.
Patients and methods The study was a cross-sectional one conducted at National Research Center, Giza. It included 90 healthy women, with age range from 21 to 60 years. Data on sociodemographic characteristics and nutritional habit were collected by a trained physician. BMI was calculated, and bone mineral density was measured by dual-energy radiograph absorptiometry.
Results Of all women, 87.8% were overweight/obese and 42.2% were osteoporotic. Women with normal BMI were more at risk of developing osteoporosis compared with obese women [odds ratio (OR)=17.86, confidence interval (CI)=2.171–146.86]. Postmenopausal women were three times more at risk of developing osteoporosis than premenopausal women (OR=2.86, CI=1.18–6.89). Women using loop and those exposed to sunray regularly were less likely to develop osteoporosis than those not using loop and those not exposed to sun (OR=0.31, CI=0.12–0.78 and OR=0.24 and CI=0.076–0.762, respectively). Women eating cheese were less likely to develop osteoporosis than those not eating cheese (OR=0.41, CI=0.166–0.966). Multiple binary logistic regression detected that women with normal BMI, postmenopausal women, women not using loop, and women not eating cheese were more at risk of developing osteoporosis.
Conclusion The current study revealed that women with normal BMI (nonobese), postmenopausal, not using loop, and not eating cheese were more at risk of developing osteoporosis. It also supports the assumption that obesity has a protective role in the development of osteoporosis in studied women population.
Keywords: bone mineral density, BMI, obesity, osteoporosis, women
|How to cite this article:|
Hassan NE, Wahba SA, Abushady MM, Boseila SA, El-Masry SE, Abdelhamid ER, El-Batrawy SR, Ali MM, Khalil A, El-Alameey IR, Ibrahim TS. Association of osteoporosis with different risk factors in a sample of Egyptian women. J Arab Soc Med Res 2020;15:90-7
|How to cite this URL:|
Hassan NE, Wahba SA, Abushady MM, Boseila SA, El-Masry SE, Abdelhamid ER, El-Batrawy SR, Ali MM, Khalil A, El-Alameey IR, Ibrahim TS. Association of osteoporosis with different risk factors in a sample of Egyptian women. J Arab Soc Med Res [serial online] 2020 [cited 2021 Jun 24];15:90-7. Available from: http://www.new.asmr.eg.net/text.asp?2020/15/2/90/308876
| Introduction|| |
Obesity, that is, excessive storage of body fat, is a disease that occurs due to chronic imbalance between energy intake and consumption . The prevalence of obesity has increased markedly in recent decades with the condition predicted to affect more than one billion people by 2030 ,. Comorbidities, including cardiovascular, metabolic disease, type II diabetes, inflammations, and some types of cancer, are usually associated with obesity ,.
Osteoporosis, the most common metabolic bone disease, characterized by decreased bone mineral density (BMD) and alterations of bone tissues, is usually associated with higher risk of low-trauma fractures . The prevalence of osteoporosis ranges between 6 and 11% worldwide; according to the National Health and Nutrition Examination Survey estimates. Because of the worldwide increase in the life expectancies, osteoporosis has become a major public health crisis. Osteoporosis affects 30% of postmenopausal women and 20% of men aged more than 50 years, and both were predicted to experience osteoporosis-related fracture throughout their lifetime. Risk of fractures, among postmenopausal women and older men, results in a significant burden of costs, disability, and mortality ,,.
Several studies view obesity as a defensive mechanism against osteoporosis, whereas others concluded that obesity had a negative effect on BMD with higher risk of fractures ,,,. Several factors including estrogen synthesis enzyme, adiponectin, leptin, and proinflammatory cytokines (secreted by adipocytes) control bone remodeling ,. Among obese postmenopausal women, adipose tissue represents the major source of estrogen synthesis, through the activity of aromatase enzyme. This adipose tissue plays a potential protective mechanism for bone. Adipose tissue also secretes leptin, which is highly correlated with body fat mass. Bone formation is modulated by leptin through enhancing bone marrow stromal cell differentiation into osteoblasts, and via inhibiting osteoclasts generation. In contrast to leptin, adiponectin concentrations, which are lower among obese individuals, are found to be associated with higher BMD loss in women ,. Bone marrow mesenchymal stem cells are common origin progenitors for adipocytes and osteoblasts. Many researchers have proved overlapping genetic susceptibility in osteoporosis and obesity ,.
Several studies revealed the endocrine regulatory role of bone-derived factors (e.g. osteocalcin and osteopontin) on body weight and glucose homeostasis. Such studies proposed that the influence of osteopontin on the adipogenic process, in the bone marrow of obese women, contributes to the development of osteoporosis. Osteoblasts produce osteocalcin (a collagen protein), which is involved in bone deposition and calcium homeostasis. It can protect against high-fat-induced obesity ,. Neuropeptide Y (NPY), the fundamental regulator of both bone mass and obesity, as well as a coordinator of interactions between them , represents a major pathway for obesity-dependent changes occurring to bone mass. Diet-induced obesity results in both leptin and insulin resistance, which in turn increase the NPY levels ,. NPY is recognizes as a key mediator driving obesity-induced cortical bone loss .
Although previous studies examined the association between BMI and BMD, yet the effect of obesity upon the skeleton remains controversial. The present work aimed to assess the association between osteoporosis and both obesity and social and nutritional status in a sample of premenopausal and postmenopausal Egyptian women.
| Patients and methods|| |
The current study included 90 healthy women recruited from the employee at the National Research Center (NRC) and their relatives with an age range between 21 and 60 years.
This was a cross-sectional study conducted between July 2016 and May 2018 at NRC at Giza. Participants fulfilling the following criteria were excluded from the current study: women having history of diseases that might affect bone metabolism, those with history of hypertension, conditions affecting inflammatory markers, thyroid diseases, diabetes mellitus, malignancies, those on drugs affecting BMD, being pregnant, women with cardiovascular disease (including heart failure), acute or chronic infections, and hepatic or renal diseases.
A written informed consent was obtained from all participants after being informed about the purpose of the study. This research paper was derived from a cross-sectional survey of a project funded by National Research Centre (NRC) Egypt, 2016–2019 entitled ‘Bone mass among overweight and obese women: mechanism and intervention’ (11th Research Plan of the NRC), with an approval obtained from Ethics Committee of NRC (Registration Number is 16/127).
Data on sociodemographic characteristics including age, smoking habit, job and education, methods of contraception, and family history of cardiovascular-related diseases were collected by a trained physician. Assessment of women’s practice was carried out by using questions to current dietary intake (e.g. milk, cheese, cake, and yoghurt) in the last month and current physical activity (e.g. walking, running, and swimming) during the last week. Participants underwent clinical examination of chest, heart, abdomen, and central nervous system, in addition to evaluation of blood pressure.
Participants’ body weight was determined to the nearest 0.01 kg, with the participant wearing minimal clothes and without shoes, using a Seca Scale Balance. In addition, body height was measured, to the nearest 0.1 cm, using Holtain Stadiometer (The Harpenden Portable Stadiometer, Wales, UK). After each measurement, scales were recalibrated following the recommendations of the International Biological Program . BMI (kg/m2) was calculated using the following formula: body weight (kg)/body height squared (m2). Then the reference BMI cutoff points recommended by WHO were applied as follows: overweight (25.00–29.99), obese (≥30.00), and normal (>18–24.9) .
Assessment of bone mineral density
Evaluation of ‘BMD’ (g/cm2), at the neck of femur, was done using dual-energy radiograph absorptiometry (Norland XR-46, version 3.9.6/2.3.1; USA) in the Medical Excellence Research Center of the NRC. Dual-energy radiograph absorptiometry scan, based on the woman’s age, weight, and height, was performed with the participant keeping the precise distance between her arms and legs according to the machine instructions manual. A well-qualified operator executed and evaluated all analyses using the same protocol for all assessments. BMD t score was calculated on the basis of the reference database. The diagnostic criteria established by the NIH Consensus Statement on Osteoporosis Prevention, Diagnosis, and Therapy  in adults were used. Based on BMD t score at neck of femur, bone density status was defined as follows: ‘osteoporotic’ when it is less than −2, ‘osteopenic’ between −2 and −1.0, and normal when it is more than −1. However, the BMD t score value of −2 was used to discriminate nonosteoporotic and osteoporotic women groups.
Statistical analyses were carried out using Statistical Package for the Social Sciences, version 21 for Windows (IBM Corp., Armonk, New York, USA). Student t test (expressed as mean±SD, minimum and maximum) was used to compare the continuous data of the two groups. Categorical data were expressed as frequencies and percentages, and were analyzed with the two-tailed χ2 test. Odds ratio (OR) and 95% confidence interval (CI) and multiple regression analysis were used to find the risk factors for osteoporosis. Statistical significance was considered when P value less than 0.05.
| Results|| |
The current study included 90 participant women with a mean age of 46.29±10.32 years and with a mean BMI of 36.43±10.33 kg/m2. Of all women, 87.8% were overweight/obese and 42.2% were osteoporotic ([Table 1]).
Women with normal BMI (18-24.9 kg/m2) were 18 times more at risk of developing osteoporosis compared with obese women (BMI ≥25 kg/m2) (OR=17.86, CI=2.171–146.86), which means obesity may have a protective effect on osteoporosis. Postmenopausal women were three times more at risk of developing osteoporosis than premenopausal women (OR=2.86, CI=1.18–6.89). Moreover, women using loop and those exposed to sunray regularly were less likely to develop osteoporosis than those not using loop and those not exposed to sun (OR=0.31, CI=0.12–0.78 and OR=0.24 and CI=0.076–0.762, respectively). Smoking, physical activity, using contraceptive pills, and ovariectomy had no significant association with osteoporosis (P>0.05) ([Table 2]).
|Table 2 Association between osteoporosis, obesity, and sociodemographic variables|
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[Table 3] shows the association between women social characteristics regarding job, education, marital status, and husband job and education and osteoporosis. No significant associations were found between osteoporosis and all the selected variables (P>0.05). No significant difference was found regarding age of menarche between osteoporotic and nonosteoporotic women (mean age of menarche: 12.73±1.80 and 13.08±1.168, respectively; P>0.05) ([Table 4]).
In [Table 5], associations between osteoporosis and different food stuff were studied. No significant associations were found regarding milk, vegetables, fruits, spinach, sesame, fish, and eggs (P>0.05). Women eating cheese were less likely to develop osteoporosis than those not eating cheese (OR=0.41, CI=0.166–0.966). Multiple binary logistic regression analysis was done to detect the predictors of osteoporosis. Women with normal BMI, postmenopausal women, women not using loop, and women not eating cheese were more at risk of developing osteoporosis (P<0.05) ([Table 6]).
|Table 6 Multiple binary logistic regression analysis for predictors of osteoporosis|
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| Discussion|| |
During the recent decades, both obesity and osteoporosis represent major global health problems with increasing prevalence and greater effect on both mortality and morbidity rates. The risk of developing both obesity and osteoporosis, which affect millions of women, increases with increased age, and with higher risk in women. Musculoskeletal degradation and increased adiposity is attributed mainly to sedentary lifestyles combined with ageing .
Recent studies have revealed that both obesity and osteoporosis are influenced by shared/common genetic and environmental factors. Although obesity is regarded as a risk factor for health, yet it has positive beneficial effect on bone formation through the mechanical loading exerted by high body mass. On the contrary, other studies that achieved no clear consensus suggested that excessive fat mass or obesity may not protect against osteoporosis, instead it could be rather damaging to bone. However, muscle functioning and soft-tissue thickness are contributory and bone protective factors ,.
In the present study, women with normal BMI were more at risk of developing osteoporosis, supporting that obesity may have a protective effect on osteoporosis. Postmenopausal women were three times more at risk of developing osteoporosis than premenopausal. Dietary habit (eating cheese) was a protective factor against osteoporosis. The beneficial effect of BMI and fat mass on BMD could be owing to the fact that increase in the fat mass leads to greater mechanical stress on bone, which in turn leads to increase in bone mass. In agreement with the current study, several previous studies demonstrated that BMI was beneficial for BMD.
In 2019, Tomlinson et al.  at UK studied 190 participants (aged 18–80 years) to assess obesity indices ‘BMD’ and concluded that higher BMI combined with ideal balanced diet (both quality and quantity) and moderate to vigorous activity represent the positive modulators of bone heath.
A study done in China by Wu et al. , concluded that obese patients have lower osteoporosis risk (OR=0.493, 95% CI=0.405–0.600, P<0.001) than normal-weight individuals, after adjusting for various conventional osteoporosis risk factors. Wang et al.  postulated that all adiposity indices, in the Chinese population, were positively correlated with BMD of all sites for both sexes, which were in agreement with the current study.
A cross-sectional investigation was done in Brazil in 2016 by Freitas et al. , assessing BMD and fat-free mass in adults and elderly people. They found an independent and protective effect of central and peripheral fat body mass on the presence of osteoporosis or osteopenia.
A hospital-based study (carried out in Changsha, China, and included 269 postmenopausal women) has concluded that the BMD of obese women was significantly higher than that of the normal weight ones .
Berg et al.  showed that all anthropometric parameters (such as BMI, waist circumference, as well as abdominal fat volume) were positively correlated to bone stiffness in the German adult population. Both visceral adipose tissue and abdominal subcutaneous adipose tissue, the potential predictors of bone stiffness, were not superior to the easily accessible anthropometric parameters such as BMI or waist circumference.
The protective association between obesity and osteoporosis was confirmed by Lloyd et al. , in USA, who concluded a positive correlation (that did not vary by sex or race) between BMI and BMD. They concluded that a 10 U increase in BMI (i.e. from normal BMI to obese) shifts an individual from an osteoporotic BMD level to a normal BMD level.
In medical practice, obesity and osteoporosis are still two major emerging challenges. In contrasts to the results of the current study, several studies revealed obesity to be associated with osteoporosis. The study carried out by Bansal and Bansal  in India in year of 2017 revealed no statistically significant relationship between BMI and BMD in women, indicating a non-protective role of obesity in the development of osteoporosis.
A total of 255 apparently healthy women were evaluated in India for BMI and BMD by Kumar et al. . Their results revealed that in premenopausal women, BMI was significantly correlated with decreased BMD at both lumbar spine and femoral neck. On the contrary, such association was missing in postmenopausal ones. Moderate to morbid obesity might not actually be a preventive factor for osteopenia.
In China at year 2015, the study carried out by Kang et al.  revealed that fat mass was positively significant with BMD in normal-weight adult men. Percentage body fat and fat mass index showed statistically negatively significant association with BMD in overweight and obesity adult men.In agreement with the current study, no consistent relationship between diet and BMD was found by Langsetmo et al.  in a study done on Canadian men and women in 2010.
A study was done to update the evidence regarding dairy intake, osteoporotic fracture risk, and prospective BMD evolution assessed by dual-energy radiograph absorptiometry in Europeans and non-Hispanic whites from North America . They concluded that the highest consumption of dairy products did not show a clear association with the total osteoporotic fracture or hip fracture risks; however, a diminished risk of vertebral fracture could be described. The results regarding BMD change were heterogeneous and did not allow for a definitive conclusion.
In contrast to the current study, a study examined links between markers of social inequality (assessed using income, marital status, and area of residence) and fracture risk in the Danish population in 2018 and demonstrated that high income and being married are associated with a significantly lower risk of bone fracture in people 50 years and more .
Strength of the present study is including social class and nutritional habit in addition to BMI in assessing the risk factors for osteoporosis. The cross-sectional study design and the relatively small sample size represented major limitations to the present study, and consequently, the causality or mechanism of the relationship between obesity and osteoporosis and reliance on a nutritional questionnaire as some answers could be falsely ideal could not be determined.
| Conclusion|| |
In conclusion, the current study revealed women with normal BMI (nonobese), postmenopausal, not using loop, and not eating cheese were more at risk of developing osteoporosis. The current study supports the assumption that obesity has a protective role in the development of osteoporosis in female population. Well-designed follow-up studies with larger sample size and careful data analysis are recommended to clearly reveal the real effect of fat mass on BMD. Moreover, studies based on genetic and molecular approaches might help recognize the regulatory pathways and hence help in developing new therapeutic interventions for both osteoporosis and obesity.
The authors acknowledge the institute ‘National Research Centre, Egypt,’ as without its fund this study could not have been done. The authors also acknowledge everybody who participated in this study; the employers of the institute who were the participants of this study, the technicians who helped in the laboratory analysis and the doctors who participated in collection of the data.’ Without their help, this study could not have been completed.
Author contributions: Nayera E. Hassan conceived and designed the study; she is the PI of the project from which these data were derived. Saneya A. Wahba and Samia A.W. Boseila designed the questionnaires about the data on sociodemographic characteristics and dietary intake. Sahar A. El-Raufe El-Masry performed analysis and interpretation of the data; she is the Co-PI of the project from which these data were derived. Moanes Shady, Enas R. Abdelhami, Inas R. El-Alameey, and Tarek S. Ibrahim participated in collection of socioeconomic and dietary intake data. Salwa R. El-Batrawy, Manal M Ali, and Aya Khalil were responsible about anthropometric assessment. All authors contributed to the collection of references, drafting of the article, and final approval of the version to be submitted. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Bosello O, Donataccio MP, Cuzzolaro M. Obesity or obesities? Controversies on the association between body mass index and premature mortality. Eat Weight Disord 2016; 21:165–174.
Hwang LC, Bai CH, Sun CA, Chen CJ. Prevalence of metabolically healthy obesity and its impacts on incidences of hypertension, diabetes and the metabolic syndrome in Taiwan. Asia Pac J Clin Nutr 2012; 21:227–233.
Mitchell NS, Catenacci VA, Wyatt HR, Hill JO. Obesity: overview of an epidemic. Psychiatr Clin North Am 2011; 34:717–732.
Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 2011; 29:415–445.
Bacha F, Gidding SS. Cardiac abnormalities in youth with obesity and type 2 diabetes. Curr Diab Rep 2016; 16:62.
Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int 2003; 14(Suppl 3):S13–S18.
Looker AC, SarafraziIsfahani N, Fan B, Shepherd JA. Trends in osteoporosis and low bone mass in older US adults, 2005-2006 through 2013-2014. Osteoporos Int 2017; 28:1979–1988.
Cauley JA. Public health impact of osteoporosis. J Gerontol A Biol Sci Med Sci 2013; 68:1243–1251.
Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, Dawson-Hughes B. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res 2014; 29:2520–2526.
Ho-Pham LT, Nguyen UD, Nguyen TV. Association between lean mass, fat mass, and bone mineral density: a meta-analysis. J Clin Endocrinol Metab 2014; 99:30–38.
Compston J. Obesity and fractures in postmenopausal women. Curr Opin Rheumatol. 2015; 27:414–419.
Dimitri P, Jacques RM, Paggiosi M, King D, Walsh J, Taylor ZA et al.
Leptin may play a role in bone microstructural alterations in obese children. J Clin Endocrinol Metab 2015; 100:594–602.
Mosca LN, Goldberg TB, da Silva VN, da Silva CC, Kurokawa CS, Bisi Rizzo AC, Corrente JE. Excess body fat negatively affects bone mass in adolescents. Nutrition 2014; 30:847–852.
Magni P, Dozio E, Galliera E, Ruscica M, Corsi MM. Molecular aspects of adipokine-bone interactions. Curr Mol Med 2010; 10:522–532.
Sharma S, Tandon VR, Mahajan S, Mahajan V, Mahajan A. Obesity: friend or foe for osteoporosis. J Midlife Health 2014; 5:6–9.
Barbour KE, Zmuda JM, Boudreau R, Strotmeyer ES, Horwitz MJ, Evans RW et al.
Health ABC Study. The effects of adiponectin and leptin on changes in bone mineral density. Osteoporos Int 2012; 23:1699–1710.
Fassio A, Idolazzi L, Rossini M, Gatti D, Adami G, Giollo A, Viapiana O. The obesity paradox and osteoporosis. Eat Weight Disord 2018; 23:293–302.
Akune T, Ohba S, Kamekura S, Yamaguchi M, Chung UI, Kubota N et al.
PPAR gamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 2004; 113:846–855.
Deng FY, Lei SF, Li MX, Jiang C, Dvornyk V, Deng HW. Genetic determination and correlation of body mass index and bone mineral density at the spine and hip in Chinese Han ethnicity. Osteoporos Int 2006; 17:119-124.
De Fusco C, Messina A, Monda V, Viggiano E, Moscatelli F, Valenzano A et al.
Osteopontin: relation between adiposetissue and bone homeostasis. Stem Cells Int 2017; 2017:4045238.
Gómez-Ambrosi J, Rodríguez A, Catalán V, Frühbeck G. The bone-adipose axis in obesity and weight loss. Obes Surg 2008; 18:1134–1143.
Wee NK, Herzog H, Baldock PA. Diet-induced obesity alters skeletal microarchitecture and the endocrine activity of bone. In: Watson RR, Mahadevan D, editors. Nutrition and diet in therapy of bone diseases. AE Wageningen. The Netherlands: Wageningen Academic 2016. pp. 375–394.
Shi YC, Lau J, Lin Z, Zhang H, Zhai L, Sperk G et al.
Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN. Cell Metab 2013; 17:236–248.
Lee SJ, Verma S, Simonds SE, Kirigiti MA, Kievit P, Lindsley SR et al.
Leptin stimulates neuropeptide Y and cocaine amphetamine-regulated transcript co-expressing neuronal activity in the dorsomedial hypothalamus in diet-induced obese mice. J Neurosci 2013; 33:15306–15317.
Wee NKY, Enriquez RF, Nguyen AD, Horsnell H, Kulkarni R, Khor EC et al.
Diet-induced obesity suppresses cortical bone accrual by a neuropeptide Y-dependent mechanism. Int J Obes (Lond) 2018; 42:1925–1938.
Tanner JM, Hiernaux J, Jarman S. Growth and physique studies. In: Weiner JS, Lourie JA, editors. Human biology: a guide to field methods. Oxford, UK: IBP. London Blackwell Publications, 1969. pp. 315–340.
Nuttall FQ. Body mass index. Obesity, BMI, and health: a critical review. Nutr Today 2015; 50:117–128.
NIH Consensus Statement. Osteoporosis prevention, diagnosis, and therapy. JAMA 2000; 17:785–795.
Pagnotti GM, Styner M, Uzer G, Patel VS, Wright LE, Ness KK et al.
Combating osteoporosis and obesity with exercise: leveraging cell mechanosensitivity. Nat Rev Endocrinol 2019; 15:339–355.
Colaianni G, Brunetti G, Faienza MF, Colucci S, Grano M. Osteoporosis and obesity: role of Wnt pathway in human and murine models. World J Orthop 2014; 5:242–246.
Singh L, Tyagi S, Myers D, Duque G. Good, bad, or ugly: the biological roles of bone marrow fat. Curr Osteoporos Rep 2018; 16:130–137.
Tomlinson DJ, Erskine RM, Morse CI, Onambélé GL. Body fat percentage, body mass index, fat mass index and the ageing bone: their singular and combined roles linked to physical activity and diet. Nutrients 2019; 11:195.
Wu DY, Qiao D, Zhang X, Zhang HQ, Luo ZC, Wang Y et al.
Lipid profiles as potential mediators linking body mass index to osteoporosis among Chinese adults: the Henan Rural Cohort Study. Osteoporos Int 2019; 30:1413–1422.
Wang J, Yan D, Hou X, Chen P, Sun Q, Bao Y et al.
Association of adiposity indices with bone density and bone turnover in the Chinese population. Osteoporos Int 2017; 28:2645–2652.
Freitas PMSS, Garcia Rosa ML, Gomes AM, Wahrlich V, Di Luca DG, da Cruz Filho RA et al.
Central and peripheral fat bodymass have a protective effect on osteopenia or osteoporosis in adults and elderly?. Osteoporos Int 2016; 27:1659–1663.
Mo J, Ouyang J. The relationship between obesity and bone mineral density in postmenopausal women. Chin J Osteoporos 2015; 21:7.
Berg RM, Wallaschofski H, Nauck M, Markus MR, Laqua R, Friedrich N, Hannemann A. Positive association between adipose tissue and bone stiffness. Calcif Tissue Int 2015; 97:40–49.
Lloyd JT, Alley DE, Hawkes WG, Hochberg MC, Waldstein SR, Orwig DL. Body mass index is positively associated with bone mineral density in US older adults. Arch Osteoporos 2014;9.
Bansal S, Bansal A. Relation between obesity and osteoporosis in women. Int J Med Dent Sci 2017; 6:1382–1385.
Kumar A, Sharma AK, Mittal S, Kumar G. The relationship between body mass index and bone mineral density in premenopausal and postmenopausal north Indian women. J Obstet Gynaecol India 2016; 66:52–56.
Kang DH, Guo LF, Guo T, Wang Y, Liu T, Feng XY, Che XQ. Association of body composition with bone mineral density in northern Chinese men by different criteria for obesity. J Endocrinol Investig 2015; 38:323–331
Langsetmo L, Poliquin S, Hanley DA, Prior JC, Barr S, Anastassiades T et al.
CaMos Research Group. Dietary patterns in Canadian men and women ages 25 and older: relationship to demographics, body mass index, and bone mineral density. BMC Musculoskelet Disord 2010; 11:20.
Matía-Martín P, Torrego-Ellacuría M, Larrad-Sainz A, Fernández-Pérez C, Cuesta-Triana F, Rubio-Herrera MÁ. Effects of milk and dairy products on the prevention of osteoporosis and osteoporotic fractures in Europeans and non-Hispanic whites from North America: a systematic review and updated meta-analysis. Adv Nutr 2019; 10(Suppl 2):S120–S143.
Hansen L, Judge A, Javaid MK, Cooper C, Vestergaard P, Abrahamsen B, Harvey NC. Social inequality and fractures-secular trends in the Danish population: a case-control study. Osteoporos Int 2018; 29:2243–2250.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]