r e v b r a s r e u m a t o l .

2 0 1 7;5 7(4):299–305

REVISTA BRASILEIRA DE
REUMATOLOGIA
www.reumatologia.com.br

Original article

Association between body mass index and

osteoporosis in women from northwestern Rio
Grande do Sul夽

Letícia Mazocco a , Patrícia Chagas a,b,∗

a Universidade Federal de Santa Maria (UFSM), Programa de Pós-Graduação em Gerontologia, Santa Maria, RS, Brazil
b Universidade Federal de Santa Maria (UFSM), Departamento de Alimentos e Nutricão, Palmeira das Missões, RS, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Objective: To investigate the association between body mass index (BMI) and bone mineral
Received 25 August 2014 density (BMD) in postmenopausal women.
Accepted 23 July 2016 Methods: Observational study with postmenopausal women who underwent bone densito-
Available online 9 November 2016 metry 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 crite-
Keywords: ria. The assessment of BMD was performed by dual-energy X-ray absorptiometry (DXA) and
Osteoporosis classified according to WHO. Statistical analysis was performed using prevalence ratios (PR)
Body mass index and their respective 95% confidence intervals for the factors studied. Variables associated
Women with p < 0.20 with the different outcomes (osteopenia and osteoporosis) were included in a
Bone mineral density 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 osteope-
nia 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 over-
weight women.
© 2016 Published by Elsevier Editora Ltda. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

夽
Study conducted with Fundo de Incentivo à Pesquisa (FIPE), Universidade Federal de Santa Maria (UFSM) support, Santa Maria, RS,
Brazil.
∗
Corresponding author.
E-mail: [email protected] (P. Chagas).
http://dx.doi.org/10.1016/j.rbre.2016.10.002
2255-5021/© 2016 Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
300 r e v b r a s r e u m a t o l . 2 0 1 7;5 7(4):299–305

Associação entre o índice de massa corporal e osteoporose em mulheres

da região noroeste do Rio Grande do Sul

r e s u m o

Palavras-chave: Objetivo: Verificar a associação entre o índice de massa corporal (IMC) e a densidade mineral
Osteoporose óssea (DMO) em mulheres pós-menopáusicas.
Índice de massa corporal Métodos: Estudo observacional, com mulheres pós-menopáusicas submetidas à densit-
Mulheres ometria óssea em Palmeira das Missões (RS). Dados sociodemográficos, de risco para a
Densidade mineral óssea 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.
© 2016 Publicado por Elsevier Editora Ltda. Este é um artigo Open Access sob uma
licença CC BY-NC-ND (http://creativecommons.org/licenses/by-nc-nd/4.0/).

habits, sedentary lifestyle, body composition, smoking, pro-

Introduction longed corticosteroid therapy, excessive intake of alcohol and
coffee, and low sunlight exposure.7,8
Osteoporosis is a bone metabolic disorder that is characterized Bone density is the main measurable determinant of risk
by reduced bone mineral density (BMD), with deterioration of of occurrence of a fragility fracture9 wherein lower body mass
bone microarchitecture, leading to increased skeletal fragility index (BMI) is associated with a substantially increased risk
and risk of fracture.1 Osteoporosis is the most common bone of fractures.10 This study aims to investigate the association
disease in humans and is being considered as one of the major between BMI and BMD in a sample of postmenopausal women
public health problems worldwide, due to an increase in life undergoing bone densitometry in Palmeira das Missões – RS.
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 mil- Materials and methods
lion people with osteoporosis,3 affecting individuals of both
genders and all races, and its prevalence increases as the pop- We conducted an observational study of postmenopausal
ulation ages.4 About 25% of post-menopausal women and 15% women who underwent bone densitometry in a clinic special-
of men over 50 are affected by the disease.3 izing in imaging diagnostic of the city of Palmeira das Missões
According to the Ministry of Health of Brazil, in 2012 – RS between October 2012 and December 2013.
about 1.6 million fractures from osteoporosis were registered.3 The sample consisted of 393 women who agreed to partic-
Fractures, especially in the hip, are associated with falls, ipate in the study and signed an informed consent.
regardless of bone density,5 and ultimately reduce the quality Socio-demographic data (age, marital status, education,
of life.6 Each year, the Unified Health System (SUS) in Brazil and occupation) and risk factors for low BMD (smoking, seden-
has shown increasing costs of fracture treatment in older tary lifestyle, and consumption of certain foods: milk, yogurt,
people. Only in 2009 R$57,610,000.00 were spent with admis- cheese, alcohol and coffee) were evaluated by using a stan-
sions and R$24,770,000.00 with drugs for the treatment of dardized questionnaire. In this sample, women who did not
osteoporosis.3 perform exercise were classified as sedentary subjects.
Among the determinants of BMD, one can find genetic fac- The anthropometric parameters assessed were weight,
tors (family history of fracture and osteoporosis in first-degree height, and BMI. Weight was measured using a calibrated
relatives), advanced age, white and oriental race, and chronic anthropometric scale, with the barefooted patient wearing
estrogen deprivation – and all of these variables cannot be a hospital gown for the measurement. Height was mea-
modified.7 But in fact, there are modifiable factors: eating sured using a stadiometer attached to the anthropometric
 r e v b r a s r e u m a t o l . 2 0 1 7;5 7(4):299–305 301

scale, with the woman in an upright position, with arms

Table 1 – Sociodemographic characteristics and risk
hanging along the body and with heels together. BMI was factors of 393 post-menopausal women from the
calculated by applying the Quetelét equation, that is, the northwestern area of the state of Rio Grande do Sul
division of weight (kg) by height (m) squared. For the classi- (2012–2013).
fication of nutritional status, the WHO’s reference was used11 : Variables n %
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 . Marital status
With a companion 270 68.7
The assessment of BMD was performed by dual-energy X-
No companion 123 31.3
ray absorptiometry (DXA). The densitometric measurements
of lumbar spine, femoral neck and total femur were evaluated Educational level
<4 years of study 136 34.6
with the use of a GE Lunar DPX-NT 150951 device. The values
4–8 years of study 203 51.7
found were classified according to the World Health Orga-
>8 years of study 54 13.7
nization (WHO) in T-score ≤ (−2.5): osteoporosis, and T-score
Occupation
between (−1.01) and (−2.49): osteopenia.12 The bone densito-
Unemployed 7 1.8
metry results are presented using the absolute values of BMD
Employed with a formal contract 18 4.6
(g/cm2 ). Employed unregistered 78 19.8
Data were entered in Excel and exported to the SPSS Household duties 108 27.5
software, version 18, for subsequent statistical analysis. Retired 182 46.3
Quantitative variables were described as mean ± standard Smoker 45 11.5
deviation, and categorical variables were described as fre- Sedentary lifestyle 230 58.5
quencies and percentages. Prevalence ratios (PR) and their
respective 95% confidence intervals for the factors studied
Table 2 – Consumption of alcohol, coffee and dairy
were calculated. Variables associated with p < 0.20 and with
products from 393 post-menopausal women from the
the outcomes studied (osteopenia and osteoporosis) were
northwestern area of the state of Rio Grande do Sul
included in a Poisson regression model with a robust variance (2012–2013).
to adjustment for potential confounders. A 5% significance
Variables n %
level was considered.
All participants received guidance regarding the Ten Steps Alcohol consumption 124 31.6
for a Healthy Nutrition of the Ministry of Health of Brazil. Coffee consumption 135 34.4

This study is part of a larger project that was approved by Milk consumption
the Research Ethics Committee of the Universidade Federal de Never 89 22.6
Santa Maria, under number CAEE 05494112.0.0000.5346, opin- Up to once a week 33 8.4
2–6 times/week 48 12.2
ion 119405 of October 10, 2012. All provisions of Resolution No.
Once a day 159 40.5
466/12 of the National Health Council were followed.
Two or more times/day 64 16.3

Yogurt consumption
Never 163 41.5
Results
Up to once a week 99 25.2
2–6 times/week 85 21.6
The sample consisted of 393 postmenopausal women under- Once a day 38 9.7
going bone densitometry. The mean age was 59.6 ± 8.2 years. Two or more times/day 8 2.0
The prevalence of osteopenia was 45% (n = 222) and of osteo-
Cheese consumption
porosis was 23.3% (n = 113). Never 47 12.0
Table 1 presents the socio-demographic characteristics and Up to once a week 61 15.5
risk factors for osteoporosis in our sample. Women with a part- 2–6 times/week 126 32.1
ner (68.7%), with four to eight years of education (51.7%), and Once a day 132 33.6
retirees (46.3%) were more frequent. The majority of the sam- Two or more times/day 27 6.9

ple were sedentary (58.5%) and a minority were of smokers

(11.5%). 50–59 years have 1.5 times the prevalence of osteopenia when
In Table 2, it was found that 31.6% consumed alcoholic bev- compared with women under 49; women aged 60–69 years
erages, and 34.4% were coffee drinkers. As for dairy products have 1.7 times the prevalence of osteopenia when compared
evaluated, it was found that most of the sample (40.5%) con- with women under 49, and women over 70 have 1.8 times the
sumed milk once a day, never consumed yogurt (41.5%), and prevalence of osteopenia versus women under 49, regardless
consumed cheese once a day (33.6%). of BMI.
In Table 3, PR for osteopenia versus BMI and age was Table 4 shows PR for osteoporosis related to BMI, age, mar-
checked. After the adjustments, it was found that PR for ital status and smoking status. After the adjustments, it was
osteopenia in eutrophic women is significantly higher versus found that, with respect to BMI, the PR for osteoporosis in the
obese women. Eutrophic women have 1.2 times the prevalence group of normal-weighted women is twice the PR for obese
of osteopenia of obese women, after the adjustment for age. women, being 1.7 times higher in overweight versus the obese
With regard to age, it was found that advancing age signifi- category. The PR for osteoporosis is also higher in the age
cantly increases the prevalence of osteopenia. Women aged group ≥60 years, being twice the PR for patients under 49
302 r e v b r a s r e u m a t o l . 2 0 1 7;5 7(4):299–305

years. Women without a partner also had a higher PR for osteo- confirming the findings of previous studies, in which the
porosis versus women with a partner, after the adjustment for presence of a high BMI has a positive effect on BMD.13 A cross-
potential confounders. There was no significant association in sectional study with 588 patients confirms the influence of BMI
relation to smoking and alcohol consumption. on BMD and indicates the lower prevalence of osteoporosis in
Table 5 shows the T-score values and BMD for femoral neck, the obese group.9 In a case–control study conducted in Rio
total femur and vertebral bodies in eutrophic, overweight and Grande do Sul, it was observed that the group of patients with
obese women. All values were significantly different (p < 0.001). fractures had lower BMI versus patients without fractures10 ;
furthermore, other studies indicate a protective effect of a high
BMI.14,15
Discussion The relationship between body weight and osteoporosis is
widely debated,13 but this topic has not yet been fully eluci-
This is one of the few studies evaluating the relationship dated, although several explanations have been proposed: a
between BMI versus osteopenia and osteoporosis in Brazil. PR higher body weight imposes a greater mechanical load on the
for osteopenia and osteoporosis was lower in obese women. In bone, with an increase of bone mass in order to accommodate
addition to BMI, advancing age also showed a correlation with this load,16 and body fat seems to exert a protective factor for
higher prevalence of osteopenia and osteoporosis. Women fractures.13 Furthermore, adipocytes are important estrogen
without a partner had a higher prevalence of osteoporosis. production sources, causing an increase in serum levels of
Analyzing the association of BMI with BMD, it was found this hormone and also of other hormones, such as leptin,
that obese women had lesser osteopenia and osteoporosis, insulin, preptin, and amylin, and may act directly and/or

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 pa

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 – 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 pa

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.
 r e v b r a s r e u m a t o l . 2 0 1 7;5 7(4):299–305 303

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 pa
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/cm2 )
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.

indirectly on osteoblast and osteoclast activity, resulting in loss over 5–10 years, followed by a somewhat slower phase
the development of bone mass.13 induced by age.33 In the elderly, the ultimate goal of prevention
Despite a lower prevalence of osteoporosis in obesity is to minimize bone loss and prevent falls. The exercises also
found in this study, it is important to note that not all aim to improve balance and gait pattern, with a view to a better
types of fat are beneficial for bone mass. Subcutaneous and independence status; furthermore, the exercise contributes to
visceral fat has opposite effects on the bone structure. Vis- a better quality of life.1
ceral fat promotes systemic inflammation, which can lead Menopause is also a risk factor that is associated with
to bone loss,17 besides having an association with increased an imbalance in bone metabolism, and the first five to ten
levels of proinflammatory cytokines such as TNF and IL-6, postmenopausal years constitute the period in which occurs
which increase bone resorption and promote osteoporosis.18 the largest amount of bone loss. Approximately 35% of post-
Hypercortisolism, which is associated with lower levels of menopausal women suffering from low BMD are at increased
bone mass, also displays an association with visceral fat risk of osteoporosis and of suffering fractures over the years.
accumulation.19 On the other hand, subcutaneous fat appears The decline in estrogen production is the main determinant
to be beneficial for peak bone mass, considering that proteins of this imbalance,9 coinciding with a reduced level of cal-
that are potentially protective against the development of cium absorbed by the intestine, due to the low production of
osteoporosis, for instance, adiponectin, are present at higher calcitonin, a hormone that inhibits bone demineralization,34
levels in visceral versus subcutaneous fat.18 although many other factors may contribute.9 Estrogen deficit
Obesity is also associated with many diseases, e.g., is an important determinant of bone loss during menopause,
hypertension,20 acute myocardial infarction,21 atherosclero- and in early cases, the risk is much higher.34
sis,22 diabetes mellitus type II,23 cardiovascular diseases,23 Women without partners showed more osteoporosis in
metabolic syndromes,24 and some cancers.16,20–25 Current evi- our study. There is evidence of an association between mar-
dence has shown that an excess of adipose tissue, observed riage with reduced risk of osteoporosis fractures versus living
in obesity, is responsible for the uncontrolled secretion of alone.35,36 Apparently, marriage provides “protection” against
inflammatory mediators, which leads to a chronic state of low- adverse health outcomes through a change of health behav-
intensity systemic inflammation that underlies the metabolic iors and through social networks stemmed from that union.37
and cardiovascular outcomes.26 This association can be explained by two processes: one of
The consumption of dairy products showed no significant them is that marriage provides a protective effect, composed
correlation with BMD, possibly due to the daily consumption of of a complex set of environmental, social and psychological
milk and cheese for a large number of subjects in our sample. factors; and the other process is that unmarried individuals
It is known that, in some individuals, an adequate intake of are less healthy.37,38
calcium is effective in preventing bone loss.27 The marital disruption through divorce or widowhood can
In this study, there was no significant relationship of coffee be a source of psychological stress that can influence bone
with BMD. Choi et al.,28 in a recent study that evaluated 11,064 quality. On the other hand, marriage is traditionally associ-
women and 9213 men, also found no association between BMD ated with greater economic security for the woman and can
and caffeine. Furthermore, a prospective study of 96 women lead to decreased psychological stress, which can influence
over 65 years, followed during 3 years showed that a caffeine the overall/bone health; however, marital quality is associated
intake >300 mg/day accelerated spinal bone loss.6 with better bone health for women.39
Older age proved to be a very significant factor for This study suffers from some limitations related to risk fac-
decreased bone mass, which agrees with other published tors for osteoporosis. We did not collect information about
studies.6,29–31 Peak bone mass is achieved between adoles- the presence of a previous fracture, a maternal history of
cence and the age of 35,1 and at least half of the adult bone femur fracture and/or osteoporosis, age at menarche and at
mass is acquired during adolescence.32 Henceforth, the bone menopause, treatment with corticosteroids, hormone replace-
mass remains relatively constant until the woman enters the ment therapy, sunlight exposure, and vitamin D and calcium
menopause. After menopause, there is a phase of rapid bone supplementation.
304 r e v b r a s r e u m a t o l . 2 0 1 7;5 7(4):299–305

National Heart, Lung, and Blood Institute and North

Conclusion American Association for the Study of Obesity; 2000.
12. Brandão CMA, Camargos BM, Zerbini CA, Plapler PG,
In a sample of women undergoing bone densitometry in the Mendonça LMDC, Albergarla BH, et al. Posições oficiais 2008
northwestern area of the state of Rio Grande do Sul, obese da Sociedade Brasileira de Densitometria Clínica (SBDens).
women had a lower prevalence of osteopenia compared to Arq Bras Endocrinol Metab. 2009;10:7–12.
13. Martini LA, Moura ECD, Santos LCD, Malta DC, Pinheiro MDM.
normal-weight women; moreover, this group showed a lower
Prevalência de diagnóstico autorreferido de osteoporose,
prevalence of osteoporosis as compared to normal-weight and
Brasil, 2006. Rev Saúde Pública. 2009;43:107–16.
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with advanced age, and in cases of osteoporosis, PR was higher et al. Body mass index as a predictor of fracture risk: a
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