Association between body mass index and osteoporosis in women from northwestern Rio Grande do Sul^☆

ABSTRACT

Objective:

To investigate the association between body mass index (BMI) and bone mineral density (BMD) in postmenopausal women.

Methods:

Observational study with postmenopausal women who underwent bone densitometry in Palmeira das Missões - RS. Sociodemographic data, risk for osteoporosis and food intake were assessed through a specific form. BMI was calculated according to WHO criteria. The assessment of BMD was performed by dual-energy X-ray absorptiometry (DXA) and classified according to WHO. Statistical analysis was performed using prevalence ratios (PR) and their respective 95% confidence intervals for the factors studied. Variables associated with p < 0.20 with the different outcomes (osteopenia and osteoporosis) were included in a Poisson regression model with robust variance to adjust for potential confounding factors. A 5% significance level was considered.

Results:

393 postmenopausal women with a mean age of 59.6 ± 8.2 years participated.After the adjustments, the normal weight women had 1.2 times the prevalence of osteopenia of obese women (PR = 1.2; CI 95% 1.3-1.5). Considering osteoporosis, the PR of euthophic women was twice the PR of obese women (PR = 2; CI 95% 1.4-2.9) and was 1.7 times greater for overweight group compared to obese category (PR = 1.7; CI 95% 1.2-2.5).

Conclusion:

Obese women had lower prevalence of osteopenia compared with normal weight subjects and also with lower prevalence of osteoporosis as compared to normal- and overweight women.

Keywords:
Osteoporosis; Body mass index; Women; Bone mineral density

RESUMO

Objetivo:

Verificar a associação entre o índice de massa corporal (IMC) e a densidade mineral óssea (DMO) em mulheres pós-menopáusicas.

Métodos:

Estudo observacional, com mulheres pós-menopáusicas submetidas à densitometria óssea em Palmeira das Missões (RS). Dados sociodemográficos, de risco para a osteoporose e do consumo alimentar foram avaliados por meio de formulário específico. O IMC foi calculado de acordo com a Organização Mundial de Saúde (OMS). A avaliação da DMO foi feita por meio de absorciometria por dupla emissão de raios-X (DXA) e classificada de acordo com a OMS. A análise estatística foi feita por meio de razões de prevalência (RP) e os seus respectivos intervalos de 95% de confiança para os fatores em estudo. Variáveis que se associaram com p < 0,20 com os diferentes desfechos (osteopenia e osteoporose) foram incluídas em um modelo de regressão de Poisson com variância robusta para ajuste para potenciais fatores de confusão. Foi considerado um nível de significância de 5%.

Resultados:

Participaram 393 mulheres pós-menopáusicas, com média de 59,6 ± 8,2 anos.Após os ajustes, as mulheres eutróficas apresentaram 1,2 vez a prevalência de osteopenia das mulheres obesas (RP = 1,2; IC 95% 1,3-1,5). E em relação à osteoporose, no grupo das eutróficas a RP foi duas vezes a RP das obesas (RP = 2; IC 95% 1,4-2,9) e 1,7 no grupo com sobrepeso em relação à categoria obesidade (RP = 1,7; IC 95% 1,2-2,5).

Conclusões:

As mulheres obesas apresentaram menor prevalência de osteopenia em comparação com as eutróficas, bem como tiveram menor prevalência de osteoporose em comparação com as mulheres eutróficas e com sobrepeso.

Palavras-chave:
Osteoporose; Índice de massa corporal; Mulheres; Densidade mineral óssea

Introduction

Osteoporosis is a bone metabolic disorder that is characterized by reduced bone mineral density (BMD), with deterioration of bone microarchitecture, leading to increased skeletal fragility and risk of fracture.¹ Osteoporosis is the most common bone disease in humans and is being considered as one of the major public health problems worldwide, due to an increase in life expectancy of the population and to the high rate of morbidity and mortality related to fractures, especially those in the hip.² In Brazil, it is estimated that there are approximately 10 million people with osteoporosis,³ affecting individuals of both genders and all races, and its prevalence increases as the population ages.⁴ About 25% of post-menopausal women and 15% of men over 50 are affected by the disease.³

According to the Ministry of Health of Brazil, in 2012 about 1.6 million fractures from osteoporosis were registered.³ Fractures, especially in the hip, are associated with falls, regardless of bone density,⁵ and ultimately reduce the quality of life.⁶ Each year, the Unified Health System (SUS) in Brazil has shown increasing costs of fracture treatment in older people. Only in 2009 R$57,610,000.00 were spent with admissions and R$24,770,000.00 with drugs for the treatment of osteoporosis.³

Among the determinants of BMD, one can find genetic factors (family history of fracture and osteoporosis in first-degree relatives), advanced age, white and oriental race, and chronic estrogen deprivation - and all of these variables cannot be modified.⁷ But in fact, there are modifiable factors: eating habits, sedentary lifestyle, body composition, smoking, prolonged corticosteroid therapy, excessive intake of alcohol and coffee, and low sunlight exposure.^7,8

Bone density is the main measurable determinant of risk of occurrence of a fragility fracture⁹ wherein lower body mass index (BMI) is associated with a substantially increased risk of fractures.¹⁰ This study aims to investigate the association between BMI and BMD in a sample of postmenopausal women undergoing bone densitometry in Palmeira das Missões - RS.

Materials and methods

We conducted an observational study of postmenopausal women who underwent bone densitometry in a clinic specializing in imaging diagnostic of the city of Palmeira das Missões - RS between October 2012 and December 2013.

The sample consisted of 393 women who agreed to participate in the study and signed an informed consent.

Socio-demographic data (age, marital status, education, and occupation) and risk factors for low BMD (smoking, sedentary lifestyle, and consumption of certain foods: milk, yogurt, cheese, alcohol and coffee) were evaluated by using a standardized questionnaire. In this sample, women who did not perform exercise were classified as sedentary subjects.

The anthropometric parameters assessed were weight, height, and BMI. Weight was measured using a calibrated anthropometric scale, with the barefooted patient wearing a hospital gown for the measurement. Height was measured using a stadiometer attached to the anthropometric scale, with the woman in an upright position, with arms hanging along the body and with heels together. BMI was calculated by applying the Quetelét equation, that is, the division of weight (kg) by height (m) squared. For the classification of nutritional status, the WHO's reference was used¹¹: underweight: ≤18.5 kg/m², normal weight: 18.5-24.9 kg/m², overweight: 25.0-29.9 kg/m², obesity: ≥30.0 kg/m².

The assessment of BMD was performed by dual-energy X-ray absorptiometry (DXA). The densitometric measurements of lumbar spine, femoral neck and total femur were evaluated with the use of a GE Lunar DPX-NT 150951 device. The values found were classified according to the World Health Organization (WHO) in T-score ≤ (−2.5): osteoporosis, and T-score between (−1.01) and (−2.49): osteopenia.¹² The bone densitometry results are presented using the absolute values of BMD (g/cm²).

Data were entered in Excel and exported to the SPSS software, version 18, for subsequent statistical analysis. Quantitative variables were described as mean ± standard deviation, and categorical variables were described as frequencies and percentages. Prevalence ratios (PR) and their respective 95% confidence intervals for the factors studied were calculated. Variables associated with p < 0.20 and with the outcomes studied (osteopenia and osteoporosis) were included in a Poisson regression model with a robust variance to adjustment for potential confounders. A 5% significance level was considered.

All participants received guidance regarding the Ten Steps for a Healthy Nutrition of the Ministry of Health of Brazil.

This study is part of a larger project that was approved by the Research Ethics Committee of the Universidade Federal de Santa Maria, under number CAEE 05494112.0.0000.5346, opinion 119405 of October 10, 2012. All provisions of Resolution No. 466/12 of the National Health Council were followed.

Results

The sample consisted of 393 postmenopausal women undergoing bone densitometry. The mean age was 59.6 ± 8.2 years. The prevalence of osteopenia was 45% (n = 222) and of osteoporosis was 23.3% (n = 113).

Table 1 presents the socio-demographic characteristics and risk factors for osteoporosis in our sample. Women with a partner (68.7%), with four to eight years of education (51.7%), and retirees (46.3%) were more frequent. The majority of the sample were sedentary (58.5%) and a minority were of smokers (11.5%).

Table 1
Sociodemographic characteristics and risk factors of 393 post-menopausal women from the northwestern area of the state of Rio Grande do Sul (2012-2013).

Variables	n	%
Marital status
With a companion	270	68.7
No companion	123	31.3
Educational level
<4 years of study	136	34.6
4-8 years of study	203	51.7
>8 years of study	54	13.7
Occupation
Unemployed	7	1.8
Employed with a formal contract	18	4.6
Employed unregistered	78	19.8
Household duties	108	27.5
Retired	182	46.3
Smoker	45	11.5
Sedentary lifestyle	230	58.5

In Table 2, it was found that 31.6% consumed alcoholic beverages, and 34.4% were coffee drinkers. As for dairy products evaluated, it was found that most of the sample (40.5%) consumed milk once a day, never consumed yogurt (41.5%), and consumed cheese once a day (33.6%).

Table 2
Consumption of alcohol, coffee and dairy products from 393 post-menopausal women from the northwestern area of the state of Rio Grande do Sul (2012-2013).

Variables	n	%
Alcohol consumption	124	31.6
Coffee consumption	135	34.4
Milk consumption
Never	89	22.6
Up to once a week	33	8.4
2-6 times/week	48	12.2
Once a day	159	40.5
Two or more times/day	64	16.3
Yogurt consumption
Never	163	41.5
Up to once a week	99	25.2
2-6 times/week	85	21.6
Once a day	38	9.7
Two or more times/day	8	2.0
Cheese consumption
Never	47	12.0
Up to once a week	61	15.5
2-6 times/week	126	32.1
Once a day	132	33.6
Two or more times/day	27	6.9

In Table 3, PR for osteopenia versus BMI and age was checked. After the adjustments, it was found that PR for osteopenia in eutrophic women is significantly higher versus obese women. Eutrophic women have 1.2 times the prevalence of osteopenia of obese women, after the adjustment for age. With regard to age, it was found that advancing age significantly increases the prevalence of osteopenia. Women aged 50-59 years have 1.5 times the prevalence of osteopenia when compared with women under 49; women aged 60-69 years have 1.7 times the prevalence of osteopenia when compared with women under 49, and women over 70 have 1.8 times the prevalence of osteopenia versus women under 49, regardless of BMI.

Table 3
Crude and adjusted prevalence ratio (PR) of osteopenia in body mass index (BMI) and age group categories of 393 post-menopausal women from the northwestern area of the state of Rio Grande do Sul (2012-2013).

Variable	Osteopenia (%)	Crude PR	p	Adjusted PR	p a
BMI
Obesity	67.0	1		1
Eutrophia	77.8	1.2 (1.0-1.4)	0.126	1.2 (1.1-1.5)	0.048
Overweight	79.0	1.2 (1.1-1.4)	0.041	1.2 (1.0-1.3)	0.096
Age
<49 years	48.1	1		1
50-59 years	71.4	1.5 (1.0-2.2)	0.056	1.5 (1.0-2.2)	0.046
60-69 years	82.4	1.7 (1.1-2.6)	0.009	1.7 (1.2-2.5)	0.008
>70 years	86.2	1.8 (1.2-2.7)	0.006	1.8 (1.2-2.7)	0.004

• ^a
  Adjusted for BMI and age.

Table 4 shows PR for osteoporosis related to BMI, age, marital status and smoking status. After the adjustments, it was found that, with respect to BMI, the PR for osteoporosis in the group of normal-weighted women is twice the PR for obese women, being 1.7 times higher in overweight versus the obese category. The PR for osteoporosis is also higher in the age group ≥60 years, being twice the PR for patients under 49 years. Women without a partner also had a higher PR for osteoporosis versus women with a partner, after the adjustment for potential confounders. There was no significant association in relation to smoking and alcohol consumption.

Table 4
Prevalence ratio (PR) of osteoporosis in body mass index (BMI), age, marital status, smoking and alcohol categories of 393 post-menopausal women from the northwestern area of the state of Rio Grande do Sul (2012-2013).

Variable	Osteoporosis (%)	Crude PR	p	Adjusted PR	p a
BMI
Obesity	34.5	1		1
Eutrophia	76.9	2.2 (1.5-3.3)	<0.001	2.0 (1.4-2.9)	<0.001
Overweight	64.3	1.9 (1.3-2.8)	0.002	1.7 (1.2-2.5)	0.003
Age
<49 years	30.0	1		1
50-59 years	48.1	1.6 (0.8-3.3)	0.189	1.4 (0.7-2.6)	0.293
60-69 years	71.2	2.4 (1.2-4.7)	0.014	2.0 (1.1-3.7)	0.029
>70 years	85.2	2.8 (1.4-5.6)	0.003	2.2 (1.2-4.0)	0.015
Marital status
With a partner	49.1	1		1
Without a partner	74.2	1.5 (1.2-1.9)	0.001	1.3 (1.0-1.6)	0.028
Smoking
Stopped	51.7	1		1
Smoker	74.1	1.4 (0.9-2.2)	0.091	1.2 (0.8-1.8)	0.372
Nonsmoker	56.5	1.1 (0.7-1.6)	0.655	1.1 (0.7-1.6)	0.724
Alcohol
Yes	48.0	1		1
No	62.3	1.3 (1.0-1.8)	0.108	1.2 (0.9-1.6)	0.157

• ^a
  Adjusted for BMI, age, marital status, smoking and alcohol.

Table 5 shows the T-score values and BMD for femoral neck, total femur and vertebral bodies in eutrophic, overweight and obese women. All values were significantly different (p < 0.001).

Table 5
T-score and bone mineral density (BMD) values in body mass index categories of 393 postmenopausal women from the northwestern area of the state of Rio Grande do Sul (2012-2013).

Variable	Eutrophia	Overweight	Obesity	p a
	n = 94	n = 164	n = 135
T-score
T-score, femoral neck	-1.6 ± 1.0	-1.3 ± 0.9	-0.9 ± 1.0	<0.001
T-score, total femur	-1.4 ± 1.1	-0.8 ± 0.9	-0.3 ± 1.0	<0.001
T-score, vertebral bodies	-1.9 ± 1.4	-1.4 ± 1.3	-0.9 ± 1.4	<0.001
BMD (g/cm 2 )
BMD, femoral neck	0.815 ± 0.146	0.857 ± 0.124	0.906 ± 0.140	<0.001
BMD, total femur	0.830 ± 0.138	0.899 ± 0.124	0.973 ± 0.136	<0.001
BMD, vertebral bodies	0.947 ± 0.171	1.005 ± 0.167	1.061 ± 0.188	<0.001

• ^a
  ANOVA.

Discussion

This is one of the few studies evaluating the relationship between BMI versus osteopenia and osteoporosis in Brazil. PR for osteopenia and osteoporosis was lower in obese women. In addition to BMI, advancing age also showed a correlation with higher prevalence of osteopenia and osteoporosis. Women without a partner had a higher prevalence of osteoporosis.

Analyzing the association of BMI with BMD, it was found that obese women had lesser osteopenia and osteoporosis, confirming the findings of previous studies, in which the presence of a high BMI has a positive effect on BMD.¹³ A cross-sectional study with 588 patients confirms the influence of BMI on BMD and indicates the lower prevalence of osteoporosis in the obese group.⁹ In a case-control study conducted in Rio Grande do Sul, it was observed that the group of patients with fractures had lower BMI versus patients without fractures¹⁰; furthermore, other studies indicate a protective effect of a high BMI.^14,15

The relationship between body weight and osteoporosis is widely debated,¹³ but this topic has not yet been fully elucidated, although several explanations have been proposed: a higher body weight imposes a greater mechanical load on the bone, with an increase of bone mass in order to accommodate this load,¹⁶ and body fat seems to exert a protective factor for fractures.¹³ Furthermore, adipocytes are important estrogen production sources, causing an increase in serum levels of this hormone and also of other hormones, such as leptin, insulin, preptin, and amylin, and may act directly and/or indirectly on osteoblast and osteoclast activity, resulting in the development of bone mass.¹³

Despite a lower prevalence of osteoporosis in obesity found in this study, it is important to note that not all types of fat are beneficial for bone mass. Subcutaneous and visceral fat has opposite effects on the bone structure. Visceral fat promotes systemic inflammation, which can lead to bone loss,¹⁷ besides having an association with increased levels of proinflammatory cytokines such as TNF and IL-6, which increase bone resorption and promote osteoporosis.¹⁸ Hypercortisolism, which is associated with lower levels of bone mass, also displays an association with visceral fat accumulation.¹⁹ On the other hand, subcutaneous fat appears to be beneficial for peak bone mass, considering that proteins that are potentially protective against the development of osteoporosis, for instance, adiponectin, are present at higher levels in visceral versus subcutaneous fat.¹⁸

Obesity is also associated with many diseases, e.g., hypertension,²⁰ acute myocardial infarction,²¹ atherosclerosis,²² diabetes mellitus type II,²³ cardiovascular diseases,²³ metabolic syndromes,²⁴ and some cancers.^16,20-25 Current evidence has shown that an excess of adipose tissue, observed in obesity, is responsible for the uncontrolled secretion of inflammatory mediators, which leads to a chronic state of low-intensity systemic inflammation that underlies the metabolic and cardiovascular outcomes.²⁶

The consumption of dairy products showed no significant correlation with BMD, possibly due to the daily consumption of milk and cheese for a large number of subjects in our sample. It is known that, in some individuals, an adequate intake of calcium is effective in preventing bone loss.²⁷

In this study, there was no significant relationship of coffee with BMD. Choi et al.,²⁸ in a recent study that evaluated 11,064 women and 9213 men, also found no association between BMD and caffeine. Furthermore, a prospective study of 96 women over 65 years, followed during 3 years showed that a caffeine intake >300 mg/day accelerated spinal bone loss.⁶

Older age proved to be a very significant factor for decreased bone mass, which agrees with other published studies.^6,29-31 Peak bone mass is achieved between adolescence and the age of 35,¹ and at least half of the adult bone mass is acquired during adolescence.³² Henceforth, the bone mass remains relatively constant until the woman enters the menopause. After menopause, there is a phase of rapid bone loss over 5-10 years, followed by a somewhat slower phase induced by age.³³ In the elderly, the ultimate goal of prevention is to minimize bone loss and prevent falls. The exercises also aim to improve balance and gait pattern, with a view to a better independence status; furthermore, the exercise contributes to a better quality of life.¹

Menopause is also a risk factor that is associated with an imbalance in bone metabolism, and the first five to ten postmenopausal years constitute the period in which occurs the largest amount of bone loss. Approximately 35% of postmenopausal women suffering from low BMD are at increased risk of osteoporosis and of suffering fractures over the years. The decline in estrogen production is the main determinant of this imbalance,⁹ coinciding with a reduced level of calcium absorbed by the intestine, due to the low production of calcitonin, a hormone that inhibits bone demineralization,³⁴ although many other factors may contribute.⁹ Estrogen deficit is an important determinant of bone loss during menopause, and in early cases, the risk is much higher.³⁴

Women without partners showed more osteoporosis in our study. There is evidence of an association between marriage with reduced risk of osteoporosis fractures versus living alone.^35,36 Apparently, marriage provides “protection” against adverse health outcomes through a change of health behaviors and through social networks stemmed from that union.³⁷ This association can be explained by two processes: one of them is that marriage provides a protective effect, composed of a complex set of environmental, social and psychological factors; and the other process is that unmarried individuals are less healthy.^37,38

The marital disruption through divorce or widowhood can be a source of psychological stress that can influence bone quality. On the other hand, marriage is traditionally associated with greater economic security for the woman and can lead to decreased psychological stress, which can influence the overall/bone health; however, marital quality is associated with better bone health for women.³⁹

This study suffers from some limitations related to risk factors for osteoporosis. We did not collect information about the presence of a previous fracture, a maternal history of femur fracture and/or osteoporosis, age at menarche and at menopause, treatment with corticosteroids, hormone replacement therapy, sunlight exposure, and vitamin D and calcium supplementation.

Conclusion

In a sample of women undergoing bone densitometry in the northwestern area of the state of Rio Grande do Sul, obese women had a lower prevalence of osteopenia compared to normal-weight women; moreover, this group showed a lower prevalence of osteoporosis as compared to normal-weight and overweight women. The prevalence of osteopenia increased with advanced age, and in cases of osteoporosis, PR was higher in those aged over 60 years. PR for osteoporosis was significantly higher in women without a partner.

• ☆
  Study conducted with Fundo de Incentivo à Pesquisa (FIPE), Universidade Federal de Santa Maria (UFSM) support, Santa Maria, RS, Brazil.

Acknowledgements

We thank Clinica Diag image, especially to Dr. Sérgio Danilo Aragonez, by encouraging this clinical research. We also appreciate the assistance received from AEX-CAPES and FIPE-UFSM.

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Publication Dates

• Publication in this collection
  Jul-Aug 2017

History

• Received
  25 Aug 2014
• Accepted
  23 July 2016