Prevalence and risk factors of radiographic vertebral fracture in Brazilian community-dwelling elderly
The prevalence and risk factors of radiographic vertebral fracture were determined among Brazilian community-dwelling elderly. Vertebral fractures were a common condition in this elderly population, and lower hip bone mineral density was a significant risk factor for vertebral fractures in both genders.
The aim of the study was to estimate the prevalence of radiographic vertebral fracture and investigate factors associated with this condition in Brazilian community-dwelling elderly.
This cross-sectional study included 943 elderly subjects (561 women and 382 men) living in São Paulo, Brazil. Thoracic and lumbar spine radiographs were obtained, and vertebral fractures were evaluated using Genant's semiquantitative method. Bone mineral density (BMD) was measured by dual X-ray absorptiometry, and bone biochemical markers were also evaluated. Female and male subjects were analyzed independently, and each gender was divided into two groups based on whether vertebral fractures were present.
The prevalence of vertebral fracture was 27.5% (95% CI 23.8–31.1) in women and 31.8% in men (95% CI 27.1–36.5) (P = 0.116). Cox regression analyses using variables that were significant in the univariate analysis showed that age (prevalence ratio = 1.03, 95% CI 1.01–1.06; p = 0.019) and total femur BMD (PR = 0.27, 95% CI 0.08–0.98; p = 0.048) were independent factors in predicting vertebral fracture for the female group. In the male group, Cox regression analyses demonstrated that femoral neck BMD (PR = 0.26, 95% CI 0.07–0.98; p = 0.046) was an independent parameter in predicting vertebral fractures.
Our results suggest that radiographic vertebral fractures are common in Brazilian community-dwelling elderly and that a low hip BMD was an important risk factor for this condition in both genders. Age was also significantly correlated with the presence of vertebral fractures in women.
KeywordsBone mineral density Elderly people Fall Femur Radiography Vertebral fracture
Underdiagnosis of vertebral fracture remains a major problem worldwide . Thus, in studies using radiographic screening of populations, the incidence of all vertebral deformities has been estimated to be three times higher than hip fracture, and only one third of vertebral fractures receive medical attention . Vertebral fractures have important clinical implications for future fracture risk. Studies have demonstrated that prevalent vertebral fracture can predict subsequent vertebral fracture , incident hip fracture , and increased mortality in the following decades , particularly if the resulting vertebral deformity is severe . As the population of the world ages, the public health impact of vertebral fractures will increase, particularly in low and middle income countries where the aging process is much faster.
The prevalence of risk factors associated with osteoporosis (OP), including bone mineral density (BMD) and bone laboratory parameters associated with vertebral fractures, have not been well characterized in healthy and asymptomatic subjects. Research has been particularly lacking in populations from low- and middle-income countries like Brazil [6, 7]. A recent study analyzed the prevalence of vertebral fractures in Latin American women . Nevertheless, this study was not specifically designed to characterize risk factors, and bone mineral density and bone laboratory parameters were not assessed .
The standard method for assessing vertebral fracture is radiographic analysis of the thoracic and lumbar spine region; however, a number of methods have been developed for interpretation of spinal X-rays, including the Genant semiquantitative method . The Genant semiquantitative method has been used to diagnose vertebral fractures in physicians’ guidelines  and has been the standard in a number of important recent osteoporosis studies [10, 11, 12, 13, 14, 15].
The aim of this study was to determine the prevalence of radiographic vertebral fracture in Brazilian community-dwelling elderly using Genant's semiquantitative (SQ) method. The study further aimed to determine the association between these fractures and OP risk factors, including BMD and bone laboratory parameters.
Materials and methods
This was a cross-sectional study nested in a population-based epidemiological study (São Paulo Ageing & Health Study). The survey was conducted from June 2005 to July 2007 on individuals 65 years old and over living in a community in the Butantã district, located on the western side of the city of São Paulo (subtropical region, latitude 23°32′51″).
This city supports a population of 10.4 million inhabitants  and is divided into 31 administrative boroughs, with territorial and population demarcations. In 2000, the Butantã district contained 377,576 residents, 6.2% of whom were over 65 years of age. The study was carried out in 66 census sectors (the smallest administrative areas) and covered a population of approximately 63,000 residents, representing 17% of the total Butantã borough population. The selection of areas was based on Family Health Program teams, but was not limited by them (i.e., they included the entire census area). This sample was representative of the age, gender, and social class demographics of the entire Brazilian elderly population .
Only well-functioning elderly were recruited to participate in this study on osteoporosis. All of the individuals were apparently healthy and showed no evidence of malabsorption, chronic diarrhea, hepatic disease, severe chronic diseases, or cancer.
All individuals answered a standardized questionnaire designed to document putative risk factors of osteoporosis and fractures [18, 19]. The questionnaire collected information regarding their health and lifestyle, including family history of hip fracture, previous fragility fracture, history of falls during the last year (two or more falls in 6 months, any fall in the last year resulting in serious injury), physical activity, alcohol use, current tobacco use, glucocorticoid use, presence of back pain, dietary calcium intake, and age at menopause.
Previous fragility fracture was determined in individuals who had experienced a fall from standing height or less after 50 years of age with a fracture occurring at sites characteristic of bone fragility (for example rib, forearm, humerus, and femur). Fractures occurring in the face, skull, ankle, elbow, and finger were not considered in this analysis . Individuals who had experienced two or more falls in the last 12 months were defined as chronic fallers . An individual was deemed to be an alcohol user when current intake exceeded three units of alcohol per day. Glucocorticoid use was defined as prednisone treatment of more than 5 mg/day for three or more consecutive months. Previous fragility fracture, family history of hip fracture, current tobacco use, glucocorticoid use, and chronic faller classification were measured as binary variables.
Back pain was assessed on scales of frequency (0, never or rarely; 1, some of the time; 2, most of the time; 3, all of the time) and severity (0, no pain; 1, mild pain; 2, moderate pain; 3, severe pain). We defined positive back pain as individuals that had experienced pain in the “most” or “all of the time” categories, or pain in the “moderate” or “severe” categories .
Physical activity was classified as (a) low, not even housework is performed; (b) moderate, performs regular housework, walks irregularly, gardening; and (c) high, performs regular physical activity aside from their daily routine at least twice a week for 30 min .
To determine calcium intake, subjects were asked whether they usually drank milk and if they ate cheese or yogurt. If dairy was consumed, individuals were asked to quantify their consumption of milk or yogurt (milliliters per day) and cheese (grams per day) during the 7 days prior to the interview.
Race was defined based on self-reported race of second-generation ancestors, an approach previously used for the Brazilian population . Individuals with four grandparents reported to be Caucasian were classified as white. Individuals with both African and Caucasian ancestors (mixed race) was classified as non-Caucasian. When racial information regarding the grandparents was unavailable, an individual’s race was determined by the race of his or her parents. Descendants of other races were not included.
Of the remaining 943 subjects, 561 were women and 382 were men. Males and females were analyzed separately, and each gender was divided into two groups based on whether vertebral fractures were present. Individuals without vertebral fracture were designated to the no fracture group; subjects presenting at least one vertebral fracture were assigned to the fracture group.
The study was approved by the Local Ethics in Research Committee of the São Paulo University School of Medicine, and all participants gave written informed consent.
The height (without shoes) of each participant was measured to the nearest 0.1 cm with a wall-mounted stadiometer. The weight of each participant (without shoes, wearing only light clothing) was measured to the nearest 0.25 kg using a double-beam balance scale. Body mass index was calculated by dividing the participants’ weight (kilograms) by their height squared (square meters).
Blood samples were collected under fasting conditions (between 8 and 10 a.m.) and stored at −70°C for later analysis.
The serum concentrations of calcium (adjusted for the albumin concentration), phosphorus, alkaline phosphatase, creatinine, and glucose were determined using standard automated laboratory methods. The estimated glomerular filtration rate (eGFR) was calculated using the Cockroft–Gault equation .
The serum concentration of 25-hydroxyvitamin D (25OHD) was measured using a radioimmunoassay technique (DiaSorin, Stillwater, MN, USA) with a lower detection limit of 5 ng/mL. The intra- and inter-assay variation coefficients in our laboratory were 10.5% and 17.8%, respectively. Intact parathyroid hormone (iPTH) serum concentrations were measured by immunoradiometric assay (ELSA-PTH, CIS bio international, France), with reference variations of 11–65 pg/mL.
Bone mineral density
BMD was measured by dual X-ray absorptiometry (DXA) using Hologic densitometry equipment (Hologic Inc. Bedford, MA, USA, Discovery model) at the following regions: lumbar spine, femoral neck, and total femur. All BMD measurements were performed by the same experienced technologist. Anatomically abnormal vertebrae were excluded from analysis of lumbar spine only if they were clearly abnormal and non-assessable within the resolution of the system or if there was more than a 1.0 T-score difference between the vertebra in question and adjacent vertebrae, as recommended by the International Society for Clinical Densitometry (ISCD) .
Precision error for BMD measurements was determined based on standard ISCD protocols . We calculated the least significant change with 95% confidence to be 0.033 g/cm2 for AP spine, 0.047 g/cm2 for femoral neck, and 0.039 g/cm2 for total femur.
Assessment of vertebral fracture
Standard lateral thoracic and lumbar spine radiographs were taken using a 40-in. tube-to-film distance centered at T7 and L2. All images provided good visibility of all vertebrae from T4 to L4, and vertebrae could be reliably identified.
The identification of vertebral fractures was performed by two concomitant readers who were each experienced in this area. The readers evaluated each T4–L4 vertebrae image to decide whether it contained a fracture. The agreement between readers (measured using a random sub-sample of 60 radiographs) was 96%, and the kappa coefficient was 0.82.
Vertebral fracture was classified using a Genant SQ approach . Each identified fractured vertebra was classified by grade based on the Genant SQ scale, where mild (grade 1) is a reduction of 20–25% of anterior, middle, and/or posterior height; moderate (grade 2) is a reduction of 26–40% in any height; and severe (grade 3) is a reduction of over 40% in any height.
Results were expressed as mean ± standard deviation or percentages. Differences between the two groups (fracture group and no fracture group) were evaluated using the Student t test, Mann–Whitney U, test or Chi-squared test. Cox regression models were used to analyze which factors were independently associated with vertebral fractures. Only variables significantly (p < 0.05) associated with vertebral fractures in the univariate analysis were included in the final proportional hazard Cox regression. Models of Cox regression were performed for each gender category. Because colinearity existed between BMD sites, sites were sequentially added to the Cox regression, and the best model was selected. A new analysis excluding subjects with mild (grade 1) fractures (n = 137) was also performed to compare the moderate/severe fracture and no fracture groups using the same statistical tests described above. These findings are presented as adjusted prevalence ratio with corresponding 95% confidence intervals (95% CI). Significance was set at p < 0.05. All analyses were performed using the Stata 9.0 software.
Anthropometric data and risk factors for osteoporosis/fractures in individuals with moderate/severe vertebral fractures (fracture group) and without fractures (no fracture group) distributed by gender category
Fracture (n = 154)
No fracture (n = 407)
Fracture (n = 123)
No fracture (n = 259)
75.2 ± 6.0
72.8 ± 5.0
72.6 ± 5.2
72.9 ± 5.1
64.5 ± 13.8
65.8 ± 13.3
71.2 ± 13.9
70.0 ± 12.0
148.6 ± 6.2
151.0 ± 6.0
163.0 ± 7.8
162.5 ± 7.3
Body mass index (kg/m2)
29.1 ± 5.6
28.8 ± 5.4
26.8 ± 4.7
26.4 ± 3.7
Caucasian, n (%)
Menopause age, years
45.4 ± 12.1
46.7 ± 9.9
Alcohol use, n (%)
Current tobacco, n (%)
Glucocorticoid use, n (%)
Fragility fracture, n (%)
Family history of hip fracture, n (%)
9 (6.7) a
Chronic faller, n (%)
Dietary calcium intake, mg/dia
431 ± 275
452 ± 310
402 ± 325
395 ± 313
High physical activity, n (%)
Back pain, n (%)
Hypertension, n (%)
Diabetes mellitus, n (%)
Laboratory parameters and bone mineral density (BMD) in individuals with moderate/severe vertebral fractures (fracture group) and without fractures (no fracture group) distributed by gender category
Fracture (n = 154)
No fracture (n = 407)
Fracture (n = 123)
No fracture (n = 259)
9.4 ± 0.4
9.4 ± 0.5
9.2 ± 0.4
9.3 ± 0.5
3.6 ± 0.5
3.5 ± 0.5
3.1 ± 0.5
3.1 ± 0.5
Alkaline phosphatase, U/L
191.5 ± 69.0
192.6 ± 57.2
181.8 ± 68.2
178.1 ± 78.1
0.93 ± 0.2
0.96 ± 0.3
1.15 ± 0.3
1.22 ± 0.5
56.4 ± 19.4
57.3 ± 18.1
59.4 ± 19.1
57.2 ± 18.1
113.1 ± 27.6
121.0 ± 55.2
114.1 ± 41.7
113.8 ± 29.7
42.9 ± 21.6
41.2 ± 21.3
39.3 ± 19.3
42.3 ± 55.2
17.0 ± 8.1
18.7 ± 9.4
21.3 ± 9.7
21.2 ± 9.3
25OHD < 30 ng/mL
25OHD <20 ng/mL
L1–L4 BMD, g/cm2
0.832 ± 0.210
0.839 ± 0.169
0.986 ± 0.183
1.010 ± 0.199
−2.2 ± 1.9
−2.2 ± 1.5
−1.2 ± 1.7
−1.0 ± 1.8
Femoral neck BMD, g/cm2
0.632 ± 0.138
0.672 ± 0.121
0.722 ± 0.125
0.760 ± 0.148
Femoral neck T-score
−2.0 ± 1.2
−1.8 ± 1.0
−1.7 ± 0.9
−1.5 ± 1.1
Total femur BMD, g/cm2
0.750 ± 0.151
0.804 ± 0.132
0.899 ± 0.135
0.935 ± 0.156
Total femur T-score
−1.6 ± 1.2
−1.3 ± 1.01
−1.1 ± 0.9
−0.9 ± 1.0
BMD and T-scores of the femoral neck were significantly lower in women within the fracture group compared to women in the no fracture group (0.632 ± 0.138 vs. 0.672 ± 0.121 g/cm2, p = 0.001 and −2.0 ± 1.2 vs. − 1.8 ± 1.0, p = 0.004, respectively). This difference was also found for the BMD (0.750 ± 0.151 vs. 0.804 ± 0.132 g/cm2, p < 0.001) and T-score of total femur (−1.6 ± 1.2 vs. −1.3 ± 1.01, p < 0.001), but no difference was observed between the two groups in the BMD and T-scores of the L1–L4 spine (p > 0.05) (Table 2).
Regarding WHO osteoporosis criteria and comparing the fracture and no fracture groups, no difference in frequency of osteoporosis (57.1% vs. 55%, p = 0.724), low bone mass (33.1% vs. 33.6%, p = 0.983), or normal BMD (9.7 vs. 11.3, p = 0.705) was observed.
Cox regression analysis for the presence of vertebral fractures in women
95% confidence interval
Total femur BMD
A new analysis excluding subjects with mild (grade 1) vertebral fracture (n = 80) demonstrated that the moderate/severe fracture group was older (77.1 ± 5.9 vs. 72.8 ± 4.9 years, p < 0.001), shorter (148.6 ± 6.1 vs. 151.0 ± 6.0 cm, p = 0.002), had a lower proportion of individuals classified as practitioners of high physical activity (9.0 ± 24.6%, p = 0.019), and had lower serum 25OHD levels (15.5 ± 7.4 vs. 18.7 ± 9.4 ng/mL, p = 0.007), femoral neck BMD (0.605 ± 0.132 vs. 0.671 ± 0.121 g/cm2, p < 0.001), femoral neck T-scores (−2.3 ± 1.1 vs. −1.8 ± 1.0, p < 0.001), total femur BMD (0.718 ± 0.146 vs. 0.804 ± 0.131 g/cm2, p < 0.001), and total femur T-scores (−1.9 ± 1.1 vs. −1.3 ± 1.0, p < 0.001) than the no fracture group. The Cox regression model included these significant variables in the univariate analysis and revealed that age, femoral neck BMD, femoral neck T-score, total femur BMD, and total femur T-score were significantly and independently associated with the presence of moderate/severe vertebral fractures in women.
Of all the measured anthropometric values and clinical risk factors associated with osteoporosis/fracture, only femoral neck BMD and T-score and total femur BMD were found to be significant in the fracture group compared to the no fracture group (p < 0.016, p = 0.042, p = 0.030, respectively) (Table 1 and 2). The Cox regression model demonstrated that only femoral neck BMD remained significant for vertebral fractures in the male population (prevalence ratio, 0.26 95% CI 0.07–0.98, p = 0.046).
Regarding WHO osteoporosis criteria and comparing the fracture and no fracture groups, no difference in frequency of osteoporosis (33.3% vs. 30.5%, p = 0.661), low bone mass (52.9 vs. 50.2%, p = 0.708), or normal BMD (13.8 vs. 19.3, p = 0.199) was observed.
The new analysis excluding subjects with mild (grade 1) vertebral fracture (n = 57), i.e., comparing the moderate and severe fracture group with no fracture, showed similar results to the previous analysis (fracture group vs. no fracture group). Cox regression analysis demonstrated that only femoral neck BMD was significant for moderate and severe fractures in the male group (prevalence ratio, 0.15 95% CI 0.02–0.93, p = 0.042).
This is the first epidemiological study in Brazil designed to characterize factors associated with vertebral fractures. We assessed a variety of clinical risk factors, bone laboratory parameters, and BMDs of both women and men aged 65 years or older. This sample was demographically similar to the age, gender, and social class distribution shown in the 2000 Brazilian census  and thus is likely representative of the bulk of the Brazilian elderly population.
Our study employed the Genant SQ method to diagnose vertebral fracture. This method is thought to be more objective and reproducible than other qualitative methods, with better interobserver agreement, and the SQ grading system method provides useful information in epidemiological and clinical study of osteoporosis . Furthermore, this method could easily be used in clinical practice, and knowledge of normal Brazilian vertebral height is not necessary for diagnosing vertebral fracture .
Vertebral fractures were present in around one third of our total sampled population. The frequency of vertebral fracture in women within our study was higher than found in Latin America and Brazil (14.7% and 14.2%, respectively; p < 0.001) in a previous LAVOS study . This discrepancy may be because we assessed a somewhat older population in our study compared to the LAVOS study (73.5 ± 5.4 vs. 68.36 ± 10.96 years, p < 0.001). Indeed, comparing age distribution, the higher prevalence of vertebral fracture seen in our study was related to the elevated frequency of fracture in individuals over the age of 80. Other possible explanations are that only the female population was assessed in our study and that a different method was used to define vertebral fracture for the LAVOS study . A European study  described a prevalence of vertebral fracture of 12% for women and 12.2% for men; however, the age group of that population (50–84 years) was also younger than our population (65–94 years).
Consistent with previous studies, our study demonstrated a positive association between age and vertebral fracture in women, with fractures more common in older individuals [6, 7]. In the previous LAVOS study, the prevalence of fracture was 6.9% in women aged 50–59 years, increasing to 27.8% in individuals over 80 years . Vertebral fracture association with older age was not observed in the male population in our study or in previous studies [6, 28, 29].
The finding that vertebral fracture was associated with hip BMD, but not lumbar spine BMD, in both women and men may be due to established effects of aging on spine site; this finding was also observed by Baddoura et al. . Although in our DXA analysis we used ISCD criteria and excluded anatomically abnormal vertebrae if they were clearly abnormal, if they were non-assessable within the resolution of the system or if there was more than a 1.0 T-score difference between the vertebra in question and adjacent vertebrae , other alterations associated with aging (extraskeletal calcification, facet joint osteoarthritis, and mild osteophytes) were not excluded and may mask the measurement of BMD at this site [29, 30, 31, 32].
Calcium intake in our population was, on average, about one third of the recommended amount for gender and age group. Calcium intake lower than the recommended amount required for good bone health has been observed around the world, including in Brazil . Similarly, low levels of vitamin D were found in all population, although lower levels were demonstrated in women with moderate and severe fracture compared to women with no fracture. The high frequency of hypovitaminosis D in apparently healthy individuals from a subtropical region observed herein is in agreement with another Brazilian study  and in studies of other places with adequate sun exposure, like Hawaii .
Even though a higher prevalence of vertebral fracture has been reported in Caucasian women compared to black women , this finding was not observed in our study.
We were not able to demonstrate differences between the fracture and no fracture group for several known clinical risk factors for osteoporosis and fractures, such as smoking and alcohol intake . These findings were probably due to a low relative risk of these factors [38, 39]. Because this population was apparently healthy, the results showed herein do not apply to frail older people.
Of note, in women excluding grade 1 fractures, the univariate analysis comparing the no fracture group to the moderate/severe fracture group showed differences in some risk factors for osteoporosis/fracture such as age, physical activity, and serum level of 25OHD, in addition to BMD. However, these factors did not remain significant in multivariate analysis. Although the multivariate analysis results were similar, the statistical models with mild fracture exclusion seem to be more accurate. This may suggest that the association with recognized risk factors is most evident with moderate and/or severe vertebral fractures, as demonstrated by others studies .
It is important to emphasize that prevalent vertebral fractures are associated with an increase in morbidity and mortality . Previous studies have shown a 20% increase in mortality 5 years after vertebral fracture . Moreover, post-menopausal women with severe vertebral fracture are at the highest risk of subsequent vertebral and nonvertebral fracture . Indeed, the severity of a previous fracture was found to be a better predictor than BMD of future nonvertebral fracture risk .
In conclusion, vertebral fractures were a common condition in the Brazilian elderly population. Moreover, femoral neck BMD was significantly correlated with vertebral fracture in both women and men. This finding strongly supports the ISCD recommendation that vertebral assessment should be utilized in individuals older than 65 years if low BMD is present .
This work was supported by grants from Fundação de Amparo e Pesquisa do Estado de São Paulo (FAPESP) #03/09313-0 and #04/12694-8, Conselho Nacional de Ciência e Tecnologia (CNPQ) #305691/2006-6 (RMRP), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (JBL).
Conflicts of interest
- 11.Harris ST, Watts NB, Genant HK, McKeever CD, Hangartner T, Keller M et al (1999) Effects of risedronate treatment on vertebral and nonvertebral fractures in women with postmenopausal osteoporosis: a randomized controlled trial. Vertebral Efficacy With Risedronate Therapy (VERT) Study Group. JAMA 13(282):1344–1352CrossRefGoogle Scholar
- 14.Reginster JY, Seeman E, De Vernejoul MC, Adami S, Compston J, Phenekos C et al (2005) Strontium ranelate reduces the risk of nonvertebral fractures in postmenopausal women with osteoporosis: Treatment of Peripheral Osteoporosis (TROPOS) Study. J Clin Endocrinol Metab 90:2816–2822CrossRefPubMedGoogle Scholar
- 16.Instituto Brasileiro de Geografia e Estatística 2006. Censo 2000: Brazil. http://www.ibge.gov.br/censo. Accessed 20 March 2007
- 17.Instituto Brasileiro de Geografia e Estatística—IBGE. Perfil dos Idosos Responsáveis pelos Domicílios no Brasil 2000. Estudos & Pesquisas. Informação Sociodemográfica e Socioeconômica 9. Rio de Janeiro: IBGE, 2002Google Scholar
- 23.Fitti JE, Kovar M (1987) The supplement on aging to the 1984 national health interview survey. Vital Health Stat 1:1–115Google Scholar