Gereç ve Yöntem: Bu retrospektif kohort çalışmasında, İstanbul Eğitim ve Araştırma Hastanesi Kadın Hastalıkları ve Doğum Kliniği'ne başvuran 45-80 yaş arasındaki hastaların DXA sonuçlarını değerlendirdik. kemik mineral yoğunluğu (KMY) ölçümleri DXA cihazı ile anterior-posterior yönde yapıldı.

Bulgular: Dört hasta grubunda farklı bölgelerin T-skorları arasında lomber omurga (p=0.025) hariç istatistiksel anlamlı fark bulundu (p<0.005). Tüm yaş gruplarında lomber bölge T-skoru en düşük saptandı. 45-50 ve 51-60 yaşlarında femur trokanter, 61-70 ve 71-80 yaşlarında femur boynu en az osteopeniden etkilenen bölgeler olarak saptandı. Dört yaş grubunda lomber omurga kemik KMY artan yaştan etkilenmemiş saptandı. Öte yandan femur boynu ve ftrokanter bölgelerinde artan yaş ile KMY' da progresif düşüş saptandı.

Tartışma: Doğru bir KMY analizi gerçekleştirilmesi için test sınırlaması mevcut olduğunda, belirli bir lokalizasyondaki kemik yoğunluk değerlerlerinden varsayım yapılabileceğini saptadık. Farklı iskelet sistemi bölgelerinin T-skor fark aralıklarının kendi içlerinde yaş ile azalmadığını tespit ettiğimiz ve osteopeniye en duyarlı bölge olduğu için tüm yaş gruplarında öncelikle lomber KMY'nin kontrol edilmesini önermekteyiz. Bu nedenle klinisyenlere önerimiz, özellikle femur ve femur trokanter bölgelerinde yaşla artan KMY dansitesinde progresif azalmaya dikkat etmeleri ve lomber bölgedeki KMY’ nun daha genç yaşlarda azaldığını göz önüne bulundurmalarıdır.

Different skeletal sites in the same patients often differ based on the T-score values; depending on which skeletal regions are measured, individual patients have been diagnosed with osteoporosis, low BMD or normal BMD ^4-5. The World Health Organization (WHO) Osteoporosis Working Group and other international osteoporosis organizations have stated that the femoral neck is the only site that should be applied in the estimation of osteoporosis prevalence at a population level ^6-7. However, it has been hypothesized that different skeletal sites of the body, such as the spine and femur, might have different environmental and/or genetic risk factors, which may affect vertebral and femoral regions in different ways.

Studies of perimenopausal women, including dual X-ray absorptiometry (DXA) are limited in terms of identifying when and where osteopenia starts and the degree of correlation in the T-scores as reproductive women transition into menopausal status. To date studies focused on BMD changes of certain age intervals ^8-10 and a certain site. Only several studies ^11,12 have evaluated longitudinal changes in BMD over the whole adult life span and, from those studies, it has been found that in postmenopausal women, in the majority of patients BMD was overestimated from previous cross-sectional data prediction, as observed in the longitudinal reports.

The purpose of this study was to determine the differences in BMD and the lowest measured T-score of the femur neck, femur trochanter, and lumbar spine in Turkish women for the evaluation of the effect of age on different sites and their correlation with BMD with an increase in age using DXA. In order to evaluate which segment of population and site is more susceptible to loss in BMD, it is important to evaluate the pattern of bone loss by age.

In this retrospective cohort study, we evaluated the DXA results of patients between the ages of 45-80 who were admitted to the Department of Gynecology and Obstetrics of Istanbul Teaching and Research Hospital, outpatient clinics between January 2016 and January 2018 for osteoporosis evaluation. 122 perimenopausal and menopausal women were included in the study and divided into 4 groups according to ages, first group compromise of 29 patients ages between 45-50, second group compromise of 33 patients ages between 51-60, third group compromise of 30 patients ages between 61-70 and, fourth group compromise of 30 patients ages between 71-80.

The BMD measurements of the lumbar spine (L1–L4) and non-dominant hip (trochanter, femoral neck, and total hip) were performed in the anterior-posterior direction by the Hologic QDR 4500 W Elite DXA (USA) device. Protocols were applied to the measurements based on manufacturer recommendations. Measurement on the Hologic spine phantom was less than 1% on all sites for the coefficient of variation of the correct BMD measurements. Osteoporosis is defined as a BMD of 2.5 standard deviations below that of a young adult (maximum T-score of -2.5 according to the WHO ¹³. Among the patients without osteoporosis, low bone mass was defined by T-scores between -1.0 and -2.5 at either skeletal site.

The exclusion criteria were trauma, bone tumors, rheumatic diseases, avascular necrosis, infection, and hyperesthesia.

Statistical Analysis: The statistical package for the Social Sciences 15.0 software for Windows was employed for the statistical analyses (SPSS, Chicago, IL, USA). The distributions of DXA parameters are described using the mean. In the intergroup analysis for continuous variables, the Kolmogorov-Smirnov test for univariate data was used to assess the normal distribution data. The One-way ANOVA test was used for four groups when the data were suitable for normal distribution. We have provided analysis of histograms for the frequency distributions of the T-score data according to age and skeletal site to graphically demonstrate any skewness to the data distributions. The linear relationship between the variables was evaluated using Pearson’s correlation test. Variables were analyzed at a 95% confidence level and a p-value of less than 0.05 was considered significant.

As shown in Table 1, there was no statistically significant difference observed between 4 groups of patients based on BMI values. For the group of patients between 45 and 50 years of age, the T-scores of the lumbar, femoral neck region, and femur trochanter region were -1.1, -0.45 and 0.2, respectively. For the group of patients between 51 and 60 years of age, the T-scores of the lumbar region, femoral neck, femur trochanter were -1.5, -0. 5 and 0.2, respectively. For the group of patients between 61 and 70 years of age, the T-scores of the lumbar region, femoral neck, and femur trochanter were -2.4, -1.1 and -0.2, respectively. For the patients between 71 and 80 years of age, the T-scores of the lumbar region, femoral neck, and femur trochanter were -1.5, -1. 5 and -0.63, respectively.

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Table 1: Comparison of T-scores for 3 skeletal sites; there was a statistically significant difference found between T-scores of different skeletal sites between 4 age groups of patients (p<0.005) except for lumbar vertebrae (p=0.02)

As shown in Figure 1, the most concordance among all age groups occurs between the T-scores of the femur neck and trochanter followed by the lumbar vertebrae. The DXA results of the patients in the four age groups declined parallel to previous measurements, except for the 61-70 and 71-80 age groups, where the femur trochanter replaced the femur neck for the least susceptible area for osteoporosis. In the youngest (ages 45-50) group of patients, the most affected regions from low BMD were lumbar vertebrae followed by the femoral neck. The lumbar vertebrae comprise the most susceptible region of the body to osteoporosis in all age groups. The BMD measurements of lumbar vertebrae among the four age groups showed no decline with an increase in age, whereas a progressive decline in BMD occurs in the femoral neck and trochanter region with an increase in age. The degree of concordance among each skeletal site was unaffected by an increase in age.

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Figure 1: Histogram analysis of patients according to age and site of osteopenia. In all age groups lumbar region T-score was the lowest. Ages between 45-50 and 51-60 femur trochanter was found least affected by osteopenia. Ages between 61-70 and 71-80 femur neck was found least affected by osteopenia.

We observed no statistical difference between BMI values in four age groups of patients (Table 1). Low body weight causes bone loss, whereas high body weight causes high BMD ^17, which could have interfered with this study results. In a large study of American and Japanese women between 20-83 years of age, Ito et al. ¹⁸ determined that BMD began to decrease at the age of 20 in Japanese women probably due to the low BMI in their population. The peak bone mass was sustained until the age of 35 in American women, whereas in postmenopausal women, bone mass was significantly reduced in both Japanese women and American women.

In this study, the most affected region was the lumbar spine in all age groups (Table 1), which could cause progressive spinal deformities and potential neurologic sequel risk in elderly women and became a major concern of neuro-surgeons before they consider potential spinal surgery ¹⁹. Among elderly women, vertebrae fractures occur more commonly than any other region of the body in the osteoporosis group. This study shows that decline in vertebral bone density starts in the early ages starting from the mid-40s.

Although we discovered that the lumbar vertebrae are the most affected region in all age groups, we could not detect accelerated bone loss with an increase in age (Figure 1). In older women, we determined that BMD of the lumbar region, especially with an increase in age, exhibits a stable decrease in the range of approximately 35 years, instead of progressive osteopenia and/or osteoporosis compared to other regions. The lumbar vertebrae tend to begin the process of degeneration at approximately age 50, which comprises the cessation of the reproductive period of women. These findings are supported by various studies. Shao et al. ²⁰ suggested that the heights of the lumbar discs of males and females within the ages 20–69 years increased linearly with an increase in age. Koeller et al. ²¹ discovered that within the lumbar spine, the disc height seems to be almost independent of age. In line with our results, in a longitudinal Denmark study, bone loss in lumbar spine most pronounced in the first decade of menopause and, stay stable throughout women’s life ¹¹.

Similar to our findings, Choe et al. ²² showed that for the normal and low BMD group, the L3 T-scores were significantly correlated with the BMD of the femoral neck and trochanter. However, in the osteoporosis group, the L3 T-scores were not correlated with the femoral neck and femoral trochanter. In this study, we also observed a very strong correlation between the femoral neck and the trochanter in the osteopenia group and less correlation between the femoral neck and the trochanter in the osteoporosis group (Figure 1). Choi et al. ²³ discovered that the correlation between vertebral and hip joint BMD and age has an inverse relationship. We did not observe a decline in the BMD difference at different sites with an increase in age.

The discordance between the BMD results of the hip and spine had been investigated and reported in several studies ^24,25. A review of postmenopausal women revealed that the discordance between the hip BMD and the spine BMD was common and predicted different fracture patterns. Spinal osteoporosis increases the odds ratio of radiographic spine fracture 2.8-fold, whereas hip osteoporosis increases the risk of hip fracture 3.0-fold ²⁶. Parallel to our findings, osteoporosis was only detected in the hip for nearly 25% of their participants versus the spine region for nearly 40% of their participants. The regression analysis of 3000 premenopausal Scottish women revealed that the BMD change rate at the spine was almost 35% versus 19% in the hip area caused by non-genetic factors ²⁷. In a recent animal study, it has been shown that in ovariectomized rats, especially inter radicular and body areas of mandibles, were less sensitive than the femur with regard to osteoporosis ²⁸. It has been hypothesized that perimenopausal period bone mass measurements estimate the lifetime risk of fracture of a woman ²⁹.

It is important to inform patients that as they age, their DXA results decline parallel to their previous measurements, except for 61-70 and 71-80 age groups, where the trochanter is replaced by the femur neck for the least susceptible area for osteoporosis (Figure 1). To date studies that investigate femur trochanter and neck BMD distinctly are limited ^30,31, usually studies focused on the proximal femoral head. Parallel to our results in a recent study, the femoral neck fracture group was found to be statistically significantly younger than the intertrochanteric fracture group ³⁰. The clinical implications of their study suggest that low BMD in the intertrochanteric region may be protective for femoral neck fractures since the energy of direct impact on the hip might dissipate in the intertrochanteric region before the arrival of energy into the femoral neck. These findings suggest that the hat senile populations are more susceptible to intertrochanteric osteopenia and, this might be a protective factor for traumatic femoral neck fractures.

In conclusion, an assumption can be made based on the BMD values from certain locations when testing limitations exist where an accurate BMD cannot be performed. According to this study T- score concordance of different skeletal sites does not change with an increase in age. Therefore, we suggest that the lumbar BMD should be checked first, as the lumbar region was most susceptible to osteopenia in all age groups. The BMD of the subtrochanteric area of the femur can be screened by DXA without the need for further femur radiographs. Clinicians should warn patients who display osteoporotic development in the femur and who might expect to have BMD reduction in other body parts, such as the lumbar vertebrae with the same level of difference in skeletal sites from previous DXA measurements. We suggest that clinicians should pay attention to a progressive decrease in BMD density with age in the femur neck and femur trochanter regions and to consider that BMD in the lumbar region starts to decrease at younger ages so they should apply physical and therapeutic treatment methods to their patients accordingly.

Study Limitations: As we mentioned above, we excluded patients from this study with major factors that may affect bone density. However, since we could not access all the medical records of the patients, we could not take into account the situations that might little effect on the BMD of study patients, such as smoking, corticosteroid use, alcohol use, and familial history of hip fracture.

Consent for publication
The author's consent to the publication of the data.

Funding
This research received no external funding.

Conflict of interests
The authors declare that they have no conflict of interest.

List of Abbreviations
BMD, bone mineral density; DXA, dual X-ray absorptiometry; WHO, World Health Organization; BMI, body mass index.

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