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Abstract

Introduction:

Although measuring bone mineral density (BMD) with dual X-ray absorptiometry (DXA) represents the standard of diagnosis and management of osteoporosis, there is a significant number of fragility fractures occurring in young patients without low BMD. Recently, clinical risk tools included hip axis length (HAL), a geometric parameter derived from the hip DXA scan, as a predictor of hip fractures in older postmenopausal women. This study aims to evaluate the relationship between HAL and other cortical bone fractures in young postmenopausal, clinically healthy women.

Materials and methods:

This study is a retrospective analysis of Lunar DXA scans of 206 normal or overweight Caucasian women aged 40–60, who had less than 10 years of menopause without secondary causes of osteoporosis, no prior osteoporosis diagnosis or medication, and no history of hip or vertebral fractures.

Results:

The 15 fractured women displayed statistically greater HAL values compared to the 191 non-fractured subjects (109.43 ± 6.44 vs 104.81 ± 5.32 mm, p = 0.002), even though there were no significant differences in age, body mass index, or BMD. The difference in HAL remained significant after adjusting for lumbar spine (LS) BMD and height (108.49 ± 1.23 vs 104.88 ± 0.34 mm, p = 0.005). HAL proved to be a fair indicator of non-hip, non-vertebral cortical fractures (area under curve = 0.720, p = 0.003), with a sensitivity of 86.7% and a specificity of 55.5%.

Conclusion:

HAL was positively associated with non-hip, non-vertebral cortical bone fragility fractures in young postmenopausal, clinically healthy women and had significantly greater values in the fractured subgroup even after adjusting for LS BMD and height.

Keywords

cortical bone fragility fractures hip axis length osteoporosis postmenopause

Introduction

Bone mineral density (BMD) measurement by dual X-ray absorptiometry (DXA) on the lumbar spine (LS), hip, or distal forearm represents the gold standard for the diagnosis and management of osteoporosis. Even more, BMD is regarded as one of the main predictors of fragility fracture risk, alongside age and history of fracture.¹ According to most guidelines, osteoporosis screening is typically recommended for women aged 65 years or older or in the presence of clinical risk factors.² Despite this effort, there is a considerable number of fragility fractures that occur in younger women, under 10 years since menopause onset, and without apparent risk factors, whose BMD is not consistent with osteoporosis.^3
–5

Clinical tools were created to improve the identification of women at high risk of fractures. The University of Sheffield introduced the Fracture Risk Assessment Tool (FRAX), which considers not only BMD but also other clinical risk factors such as age, history of fracture, parental hip fracture, or glucocorticoid exposure. However, these traditional risk factors may lose their predictive accuracy in clinically healthy women during the early years of menopause. This model had been proven to be relatively successful but did not exploit all the information provided by a DXA scan and is yet to be refined with more discreet risk factors.^6,7

Research on the mechanism of cadaveric bone implies that bone density and some other traits contribute to 60%–80% of bone strength.^8,9 The pivotal determinants of bone strength include microarchitecture (cortical porosity, trabecular separation, or microdamage) and macroarchitecture (the geometrical characteristics), such as bone size, shape, and distribution. Some techniques, such as peripheral quantitative computed tomography and photon absorptiometry, provide further insight into these traits, leading to a better understanding of bone characteristics, but these methods are not widely available for clinical practice.¹⁰ Validating the assessment of three-dimensional parameters from the commonly used two-dimensional hip DXA scan was done versus in vivo computed tomography.^11,12

Through specific approved software, DXA hip measurement provides, besides BMD, a variety of biomechanical geometric parameters related to bone shape, strength, and loading adaptation. These include neck shaft angle (NSA) and hip axis length (HAL), the latter being defined as the distance between the great trochanter and inner pelvic rim.¹³ Some of the first insights about the clinical implications of HAL were provided in 1993 by Faulkner et al., who blindly determined bone geometry in 64 women with hip fracture and 134 non-fractured women aged 65 or older from the Study of Osteoporotic Fractures (SOF) cohort and suggested that a longer HAL is independently associated with hip fracture. Furthermore, when converted into standard deviations (SD), these data revealed that a one SD increase in HAL nearly doubled the risk of hip fracture.¹⁴ Subsequent papers based on cross-sectional methodology provided contradictory results. However, longitudinal studies based on both the Manitoba and SOF cohorts identified a positive association between HAL and all hip fractures,^14,15 while in the EPIDOS study, the association was proven only with femoral neck (FN) fractures, independently of BMD.¹⁶ A recent study on the same Manitoba cohort, using age and T-score stratified analysis, found that adjusting FRAX with HAL had the most significant impact for nonosteoporotic women under 70 years old (hazard ratio 1.70 per SD increase, 95% confidence interval (CI) 1.48–1.94), therefore bringing this geometric parameter into attention when assessing young, apparently healthy pre- and peri-menopausal women aged over 40 for its ability to increase hip fracture case identification independent of BMD.¹³

The 2023 International Society for Clinical Densitometry’s official position states that HAL obtained from DXA is correlated with hip fracture risk in postmenopausal women, while other geometry parameters such as cross-sectional area, buckling ratio, cross-sectional moment of inertia, or NSA should not be considered in estimating hip fracture risk.¹⁷ Recently, the beta version of the FRAX tool managed to incorporate HAL in the approximation of the 10-year probability of hip fracture, but as the input data into the FRAX beta equation was obtained mostly from Central and Northern European postmenopausal women, its results may not be superposable to Eastern Europe.¹⁸

Although many prior papers found a positive association between HAL and increased risk of various hip fractures in different ethnicities, it is yet to be seen if this parameter may be associated with non-hip fractures or other sites of cortical bone fractures at different ages.

Our study’s main objective was to evaluate the potential correlation between HAL and non-hip, non-vertebral, cortical bone fractures in young, apparently healthy, nonobese, postmenopausal women with no secondary causes of osteoporosis. Also, we aimed to establish the prevalence of osteoporosis and fragility fractures in this niche category of patients.

Materials and methods

We conducted a retrospective analysis of consecutive DXA scans of postmenopausal women aged 40–60 (N = 1271) acquired between December 2018 and July 2023 at a tertiary care center of Endocrinology—“Elias” Emergency University Hospital, Bucharest, Romania. Exclusion criteria consisted of: menopause duration exceeding 10 years (N = 146), onset of menopause before age 40 (N = 85), diagnosis of secondary osteoporosis (glucocorticoid exposure N = 60, rheumatoid arthritis N = 7, primary hyperparathyroidism N = 21, hypogonadism N = 17, untreated hyperthyroidism N = 11), prior treatment with antiresorptive or osteoanabolic medication (N = 98), underweight (body mass index (BMI) below 18.5 kg/m², N = 9) or obese patients (BMI ⩾30 kg/m², N = 133), patients with hip fractures (N = 3) or only vertebral fractures (N = 8), and insufficient data (N = 467). The patients were directed to our clinic by their primary care physicians due to prior inconclusive DXA scans performed in the outpatient setting, suspicion of other endocrine disorders, or a history of fracture.

All participants consented to provide their medical records for scientific research and signed an informed consent form. The study was approved by the hospital Ethics Board and the planning, data collection, analysis, and reporting were conducted following the Helsinki Declaration of 2013.

We gathered clinical medical data, including age, menarche, age of menopause onset, height, and weight for the computation of BMI, smoking status, high alcohol intake, detailed history of diseases and medication usage, and history of fragility fractures or parental hip fractures. The same operator performed all scans utilizing the normal quality control protocol on a single osteodensitometer (iDXA Prodigy GE Lunar, General Electric HealthCare). The patients’s BMD and T- and Z-scores for the LS, FN, and total hip (TH) were analyzed following the international standard of osteoporosis diagnosis¹⁹: normal BMD (T-score ⩾ −1 SD), low BMD, formerly known as osteopenia (T-score between −1 and −2.5 SD), and osteoporosis (T-score ⩽ −2.5 SD). The trabecular bone score (TBS), along with its T- and Z-scores, was computed using the TBS iNsight Software 1.8, Med-Imaps, a Swiss company. The DXA scans of the hips positioned supine with a 15°–30° internal rotation were evaluated through the Advanced Hip Analysis software to provide data on hip geometry parameters, such as HAL.

IBM SPSS Statistics Version 26 was used to conduct statistical analysis, with a significance threshold set at p < 0.05. The Chi-square test was used to compare the percentages of categorical variables between subgroups. The normality of the continuous variables’ distribution was assessed with the Shapiro–Wilk test and the variables were presented as mean ± SD for those with a normal distribution or median (interquartile range) for those with a non-normal distribution. For the comparison of continuous variables between subgroups, we have used the Mann–Whitney U test for skewed variables and the Independent-Samples T test for those with a normal distribution. To evaluate the association between variables, we have used Spearman’s correlation coefficients. A General Linear Model (one-way ANCOVA) was conducted to compare HAL values between fractured and non-fractured women while controlling for height and LS BMD. Levene’s test and normality checks were conducted, and the assumptions were met. The area under curve (AUC) and receiver operating characteristics (ROC) were used to compute the sensitivity and specificity for the best threshold of HAL for non-hip cortical bone fragility fractures.

Results

The study group consisted of 206 clinically healthy Caucasian postmenopausal women aged between 40 and 60 years, with a median age of 53.5 (5.3) years. The median age of menopause onset was 48 (4) years. Consequently, our patients had a median duration of 5 (4.4) years since menopause. As underweight and obese patients were excluded, the women in our study presented a median BMI of 25.7 (3.97) kg/m². Out of 206 women, 56 (27.18%) were active smokers, 3 (1.5%) admitted to consuming alcohol on a regular basis, and 15 (7.28%) mentioned a history of parental hip fracture. Furthermore, based on the self-declared medication, 10 out of 206 women (4.9%) were using calcium supplements, whereas 86 out of 206 (41.7%) were taking vitamin D. The DXA scan revealed that only 35/206 (17%) had normal values of BMD, 131/206 (63.6%) had low BMD or osteopenia, and 40/206 (19.4%) had a T-score lower than −2.5 DS, consistent with osteoporosis.

Out of the 206 patients, 15 (7.28%) had fragility fractures, totaling 16 fractures, as one woman was diagnosed with both an upper limb and vertebral fractures: 12 of the 16 fractures were of the upper limb (75%), 2 of the rib cages, 1 vertebral fracture, and 1 tibial fracture. Due to the exclusion criteria, there were no hip fractures in our study group. Out of the 15 fractured patients, most had DXA scores indicating low BMD or osteopenia. Specifically, eight patients had low BMD, two had normal BMD, and five had osteoporosis.

There was no statistical difference in the median values of age at evaluation, age of menopause onset, BMI, BMD of any bone site, or TBS between the fractured and non-fractured subgroups, as shown in Table 1.

Table 1.

Baseline characteristics of the study population.

Parameter	Fractured women (N = 15)	Non-fractured women (N = 191)	Sig.
Age at evaluation (years)	54.4 (4.9)	53.4 (5.4)	0.250
Age of menopause onset (years)	48 (4)	48 (4)	0.929
BMI (kg/m²)	25.7 (5)	25.8 (3.82)	1.000
Height (cm)	167 (10)	163 (7)	0.084
Weight	72.6 ± 9.22	67.86 ± 7.97	0.030
Smokers (%)	6/15 (40%)	50/191 (26.2%)	0.243
Parental hip fracture (%)	2/15 (13.3%)	13/191 (6.8%)	0.299
BMD values consistent with osteoporosis (%)	5/15 (33.3%)	35/191 (18.3%)	0.176
LS BMD (g/cm²)	0.982 (0.287)	1.012 (0.193)	1.000
LS T-score (SD)	−1.7 (2.4)	−1.4 (1.6)	0.320
FN BMD (g/cm²)	0.829 (0.119)	0.859 (0.137)	0.283
FN T-score (SD)	−1.5 (0.9)	−1.3 (0.92)	0.283
TH BMD (g/cm²)	0.901 (0.083)	0.922 (0.146)	0.619
TH T-score (SD)	−0.8 (0.6)	−0.6 (1.1)	0.592
TBS	1.321 ± 0.067	1.351 ± 0.092	0.225
HAL (mm)	109.43 ± 6.44	104.81 ± 5.32	0.002

BMD, bone mineral density; BMI, body mass index; FN, femoral neck; HAL, hip axis length; LS, lumbar spine; SD, standard deviation; TBS, trabecular bone score; TH, total hip. Bold values denote statistical significance at the p <.05

Besides the statistical difference in mean HAL values (p = 0.002) between the fractured women (109.43 ± 6.44 mm) and non-fractured subjects (104.81 ± 5.32 mm), in our study group, the presence of fragility fractures was correlated only with HAL (p = 0.003, r = 0.207) and not with the BMD of any bone site, nor with the TBS. HAL values showed significant positive correlations with height (p < 0.001, r = 0.478), weight (p < 0.001, r = 0.331), LS BMD (p = 0.014, r = 0.171), and LS T-score (p = 0.014, r = 0.172), but not with FN or TH BMD. LS BMD showed significant correlations with FN BMD (p < 0.001, r = 0.478), TH BMD (p < 0.001, r = 0.504), and TBS (p < 0.001, r = 0.485).

Significant differences in HAL values were seen between fractured and non-fractured women, even after adjusting for height and LS BMD, F(1, 202) = 22.159, p = 0.005, partial η² = 0.038. The adjusted means of HAL were 108.49 ± 1.23 mm for the fractured group and 104.88 ± 0.34 mm for the non-fractured group, evaluated for a height of 163.68 cm and an LS BMD value of 1.030 g/cm² (Figure 1).

Figure 1.

Estimated means of HAL for the fractured and non-fractured subgroups.

In our study, HAL was a fair indicator of non-hip cortical bone fragility fracture, with an AUC = 0.720 (p = 0.003, Std error = 0.077, 95% CI (0.578; 0.881), Figure 2). The coordinates of the ROC curve and of the Precision-Recall Curve showed a sensitivity of 86.7% and a specificity of 55.5% at a HAL cut-off value of 105.29 mm. The positive predictive power for fragility fractures of the before-mentioned HAL cut-off was 13.3%.

Figure 2.

ROC for HAL as an indicator of non-hip, non-vertebral cortical bone fragility fractures.

Discussion

Although older HAL studies included patients treated with antiosteoporotic medication, as it is known that it does not influence HAL measurements,¹³ we have decided to exclude those subjects that have received such medication. The rationale for this decision was the impact of antiosteoporotic therapy on BMD values and the correlation between HAL and BMD. Based on the same logic, we have excluded patients diagnosed with hyperparathyroidism, glucocorticoid exposure, and rheumatoid arthritis, as well as underweight patients; therefore, our study group was formed only of naïve patients. Furthermore, considering the intricate relationship between high BMI values and increased fracture risk²⁰ and recent studies that showed that an increase in BMI is also accompanied by an increase in HAL values,²¹ we decided to exclude obese patients, leaving our study group to be formed only by normal and overweight or pre-obese women. Since the relationship between HAL and hip fractures had already been proven, hip-fractured women were further excluded to prevent potentially higher HAL values from affecting the mean HAL of our fractured subgroup. Therefore, our study group included only non-hip, non-vertebral cortical bone fractures.

Although we did not compute osteoporosis prevalence for each age group, the overall percentage of this diagnosis was 19.4% in our 40–60-year-old study group, greater than what has been reported in the literature. An Austrian real-world study conducted in a specialized osteoporosis and menopause clinic during 1990–2012, involving approximately 100,000 women, revealed a lesser prevalence, despite a doubling rate every 5 years: 3.3% for the 45–49 age group, 6.4% for the 50–54 age group, and 13.5% for the 55–59-year-old women.⁵

Remarkably, only one-third of the fractured women in our study group had a T-score ⩽ −2.5 DS, while more than half of them (8/15) had a spine and/or hip BMD consistent with osteopenia. These findings mirror those of the Austrian study, which showed that most forearm and hip fragility fractures (1239/1757) happened in women under 65 with normal or low BMD.⁵ Previous studies also indicate that the percentage of fractures that occurred in patients with non-osteoporotic T-scores was higher among women 50–64 years of age than among those older.⁴

We found no significant differences in hip and spine BMD, age, or years since menopause between non-fractured women and those with prevalent non-hip and non-vertebral fractures in our relatively young study group, with a median age of 53.5 (5.3) years old. The results of our study, similar to those of other middle-aged women,⁵ dispute the effectiveness of employing conventional fracture risk factors such as age and BMD to identify young women at risk of fracture. These factors have proven to be particularly effective in older postmenopausal women.

Although we have excluded the hip-fractured patients, who are typically associated with greater HAL values, our fractured subgroup also exhibited a longer HAL. HAL was suggested to be used only as a specific marker for hip fractures and not for other osteoporotic fractures, as it was hypothesized that higher values might be associated with greater trochanter protuberance, increasing the movement arm, and predisposing the hip to impact upon a sideways fall.²² However, other studies have also initially identified HAL as a predictor for both hip and non-hip fractures.¹⁵ In the 2009 Manitoba study, after adjusting for FN BMD, HAL remained a significant predictor only for hip fractures. We point out that there are several differences: our study group is significantly younger than the Manitoba cohort, whose mean age was 66 ± 9.7 years old and whose hip BMD was correlated with HAL. Moreover, there is no evidence of acknowledging a possible history of previous fragility fracture at a younger age in the hip-fractured subgroup of the Manitoba study. In our data, within the limits of a much smaller population, we found no positive association between FN BMD and HAL; therefore, there was no adjustment for hip BMD. Despite the positive association between LS BMD and HAL in our study group, the mean values of HAL were still significantly higher in the fractured subgroup, even after controlling for height and spine BMD. These findings complement the Canadian cohort rather than contradict it.

Female twin-pair studies demonstrated that the maximum rate of growth of HAL occurred around the age of 12, reaching a peak by age 15, with one-fourth of the HAL variation being attributed to genetic factors that also influence height.²³ In our study, the strongest correlation for HAL was with height (r = 0.478), consistent with findings from the Manitoba cohort,¹³ where the same association was found, with a similar coefficient (r = 0.51). The same study showed that a greater HAL was a strong predictor of hip fractures, with a twofold increase in fractures between the highest quintile (HAL > 109.9 mm) and the lowest one (HAL < 99.5 mm). In our study, a HAL value of 105.29 mm showed a high sensitivity of 86.7% and a specificity of 55.5% for non-hip, non-vertebral cortical bone fragility fractures. This cut-off value closely aligns with the 105 mm threshold observed in earlier studies when assessing hip fracture risk.²⁴

Although we identified no apparent physiopathological mechanism of how HAL would account for non-hip fractures, other researchers have proposed that hip geometry characteristics may play a role in the dynamics and fracture risk associated with stumbling and lateral falls.²⁵ Granted that such occurrences are likely to result in hip fractures in older people, as shown by prior studies linking HAL to hip fractures,¹⁵ in younger populations, as examined in our study, the same events may result in non-hip or arm fractures.

We acknowledge that the contribution of HAL and other bone geometry parameters in fracture risk prediction seems far less important in comparison with the three main determinants of fracture: age, BMD, and prevalent fragility fractures. Still, the increased number of fractures that occur in nonosteoporotic young patients raises the need for improvement as physicians aim to identify patients who would benefit from antiosteoporotic treatment to prevent life-threatening fractures at an older age. In addition, it is important to note that the HAL is readily available information obtained from the hip DXA scan, which is already used for the diagnosis and management of osteoporosis. The introduction of HAL in the FRAX beta equation may not only further tune hip fracture prediction but also raise awareness for this parameter, setting the stage for scientific interest in bone geometry’s clinical implications.

Our study’s strength lies in the inclusion of young women in the first decade of menopause who apparently do not have clinical risk factors for osteoporosis. These individuals would often not be screened for osteoporosis based on local and most international guidelines. Moreover, our study excluded vertebral and hip-fractured women, as there is a well-known association between HAL and hip fracture. This decision aimed to enhance the comprehension of the relationship between HAL and cortical bone fractures in young postmenopausal women.

The sparse number of patients with prevalent fractures may appear deceivingly low, leading one to consider this study’s results as mere chance occurrences. However, it is important to note that these women were considered low risk according to current local and international guidelines for osteoporosis screening, as they were under 65 years old, had less than 10 years of menopause, and had no secondary osteoporosis causes. The modest addressability of patients who are considered to have a low fracture risk is an obvious impairment for better patient sampling and an important limit that alters the generalizability of the study.

Further longitudinal studies are required to assess the clinical development of future fragility fractures in this study group as they age into a more advanced decade of life that could be associated with hip fractures, while taking into consideration medical treatments and conditions, as well as lifestyle. Therefore, we aim to further evaluate the possible use of HAL as a marker for non-hip cortical fragility fracture at a younger age for the same individual who might sustain a hip fracture at an older age.

Conclusion

The HAL was the only DXA-derived parameter that positively correlated with non-hip, non-vertebral cortical bone fractures in this group of apparently healthy, young, and postmenopausal women. HAL was significantly higher in the fractured subgroup than in the non-fractured subjects, even after adjusting for height and LS BMD. We do not assume that including HAL in the routine evaluation of nonobese young middle-aged postmenopausal women could critically alter the clinical practice, but we consider that the present information could prompt further inquiry into the relationship between HAL and non-hip cortical bone fractures in this subgroup of patients, usually deemed of lesser importance when talking about the osteoporotic burden.

Supplemental Material

sj-docx-1-tae-10.1177_20420188251332082 – Supplemental material for Hip axis length and non-hip cortical fragility fractures in young postmenopausal nonobese Caucasian women

Supplemental material, sj-docx-1-tae-10.1177_20420188251332082 for Hip axis length and non-hip cortical fragility fractures in young postmenopausal nonobese Caucasian women by Irina Manuela Nistor, Simona Fica, Sorina Carmen Martin, Marius Lucian Mitrache, Theodor Eugen Oprea, Anca Elena Sirbu and Carmen Gabriela Barbu in Therapeutic Advances in Endocrinology and Metabolism

Footnotes

Appendix

Acknowledgements

The Endocrinology Department of the “Elias” Emergency University Hospital, Bucharest, Romania, for DXA equipment and scan availability.

Declarations

ORCID iDs

Irina Manuela Nistor

Anca Elena Sirbu

Supplemental material

Supplemental material for this article is available online.

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