Injury, Int. J. Care Injured 48S (2017) S41–S46
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Hip osteoarthritis as a predictor of the fracture pattern in proximal femur fractures Ignacio Aguado-Maestroa,b,* , Michalis Pantelic , Manuel García-Alonsob , Ignacio García-Cepedab , Peter V. Giannoudisc a b c
Academic Department of Trauma & Orthopaedics, School of Medicine, University of Leeds, Clarendon Wing, Level A, Great George Street, Leeds, UK Traumatology and Orthopaedic Surgery Department, Hospital Universitario del Río Hortega, C Dulzaina 2, Valladolid, Spain Academic Department of Trauma & Orthopaedics, School of Medicine, University of Leeds, UK
A R T I C L E I N F O
Keywords: Hip osteoarthritis Hip fracture Intracapsular Extracapsular
A B S T R A C T
Introduction: Several authors have suggested a correlation between the fracture patterns of proximal femur fractures and the degree of hip osteoarthritis (HOA), but the current evidence to support this are insufficient. The aim of our study was to demonstrate whether there is an association between the grade of HOA and fracture pattern observed, in patients presenting with a fragility fracture of the proximal femur. Materials and methods: We contacted a retrospective review of all patients presenting to our institution with fragility fractures involving the proximal femur, between March 2012 and October 2013. Pathological fractures, high-energy injuries and patients with less than one year of follow-up were excluded from further analysis. Admission radiographs and severity of HOA were assessed according to Kellgren and Lawrence scale (minimal: Grades 1–2; severe: Grades 3–4). Fractures were classified according to AO/OTA classification. Results: A total of 1003 patients (725 females; 1003 fractures) met the inclusion criteria, having a mean age of 81.5 (46–106 years). With regards to fracture classification, 417 (41.6%) fractures were classified as extracapsular and 586 (58.4%) as intracapsular. A total of 939 (93.9%) patients presented with minimal HOA, whilst 61 (6.1%) of the patients presented with severe HOA. Of the 61 patients presenting with severe HOA, 42 patients (68.9%) sustained a 31A-interthrocanteric fracture and 19 patients (31.1%) sustained a 31B-intracapsular fracture. Regarding the patients presenting with minimal HOA (832 patients in total), 323 patients (38.8%) sustained 31A-intertrochanteric fracture and 509 patients (61.2%) sustained a 31B-intracapsular fracture. Patients presenting with severe HOA were found to have a statistically significant chance to present with an extracapsular fracture (p < 0.01). Conclusions: The degree of HOA is related to the fracture pattern in patients presenting following simple mechanical falls. More specifically, higher grades of HOA are associated with extracapsular fracture patterns, whereas lower grades of HOA are associated with intracapsular fracture patterns. © 2017 Elsevier Ltd. All rights reserved.
Introduction Fragility fractures of the proximal femur are considered one of the major consequences of the aging population, mainly being associated with osteoporosis [1]. Their incidence has been estimated as high as 400/100.000 per person-years [2]. Their effects can be detrimental due to their high mortality and
* Corresponding author at: Traumatology and Orthopaedic Surgery Department, Hospital Universitario del Río Hortega, C Dulzaina SN, Valladolid, 47009, Spain. E-mail address:
[email protected] (I. Aguado-Maestro). http://dx.doi.org/10.1016/j.injury.2017.08.037 0020-1383/© 2017 Elsevier Ltd. All rights reserved.
morbidity, whilst at the same time they represent a significant economic burden to every health care system wordwide [3]. Patient’s low Bone Mineral Density (BMD) and low vitamin D serum levels, history of previous falls/fractures, vision disabilities, glucocorticoids intake, background of hyperthyroidism, hypogonadism, chronic kidney disease, increased alcohol intake and smoking are some of the factors that have been associated with an increased risk of proximal femur fragility fracture [4–7]. On the contrary, an increased body mass index (BMI) [8] and normal ranges of serum vitamin D levels [9] have been reported to reduce the risk of these fractures. Some authors have also reported that the presence of osteoarthritis (OA) is another associated with an increased risk
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of fragility fractures [5]. A possible explanation of this observation is that pain reduces physical exercise and this reduction is associated to a further BMD loss, that in turn predisposes to fragility fractures [5]. Moreover, several studies designed to assess the hypothesis that hip osteoarthritis (HOA) has a protective action against proximal femur fractures, have been inconclusive due to the difficulties of identifying a non-fractured control sample [5,10– 12]. Calderazzi et al., suggested that even though HOA could not be considered as a protective factor, there is possibly a relationship between the grade of HOA and the fracture pattern observed [13]. The same observation was also reported by Middleton and Ferris [14]. More specifically they found a tendency that patients with higher grades of HOA sustaining a proximal femur fragility fracture were more likely to sustain a pertrochanteric fracture. The potential relationship between HOA and fracture pattern has been explained according to the irregular distribution of bone mineral density throughout the proximal femur in osteoarthritic hips, where there is an increased mineral density around the neck of the femur [15,16]. Some authors have also suggested that the range of hip motion is a predictor of the fracture type, as it has been hypothesised that intracapsular fractures are secondary to impingement of the femoral neck against the acetabulum during the extremes of external rotation [17,18]. Currently, there is no evidence that the different fracture patterns are associated with short-term outcomes. Indeed, several authors report similar lengths of hospital stay, destination on discharge and in-hospital mortality [19–21]. However, there are differences with regards to the type of treatment received as different surgical procedures can be performed. Extracapsular fractures are commonly treated with osteosynthesis, in contrast to intracapsular fractures which are treated with partial or total joint replacement procedures because of their high incidence of complications with osteosynthesis [22]. Additionally, different fracture types have been associated to age [23], ABO blood group [24], parathyroid hormone (PTH) levels [25], serum calcium levels [26], steroids use [23], fall direction and mechanism of injury [22,27,28] morphology and geometry of the hip joint [29]. The aim of our study was to investigate the presence of a potential association between the grade of HOA and fracture pattern observed, in patients presenting with a fragility fracture of the proximal femur. Materials and method Following institutional board approval, all consecutive patients admitted to our institution during a 20-month period (March 2012–October 2013) presenting with a proximal femur fragility (osteoporotic) fracture were included in our study. In those patients under the age of 65, a DEXA scan with a T-score of less than 1.5 was necessary for the diagnosis of a fragility fracture. In patients older than the age of 65, fragility fractures were considered as those that occurred as a result of a minimal trauma, such as a fall from standing height or even without any identifiable trauma [30]. Exclusion criteria included high-energy injuries and pathological fractures. Data collected included patient demographics, fracture classification according to AO-OTA [31], severity of HOA if present, osteoporosis as evident on Dual Energy X-ray Absorptiometry scan (DEXA) results (T-Score of the hip where available), AMTS (Abbreviated Mental Test Score), history of previous fragility fractures and incidence of medical complications during admission. Medical complications were defined as the complications that were not related to the fracture site or surgical wound. HOA was classified according to Kellgren and Lawrence [32]. Osteophytes, periarticular ossicles, subchondral bone sclerosis, pseudocystic areas and altered shape of bone ends were assessed.
Narrowing of the joint space was not considered as a factor as it might be influenced by an intracapsular haematoma, especially in the case of intracapsular fractures. Patients were then split into two groups according to the severity of their HOA. “Minimal grade” included patients graded 1 and 2, whereas patients graded 3 and 4 were considered as “Severe grade” [13]. Fractures types were classified for analysis as extracapsular (pertrochanteric: AO-OTA 31-A and purely subtrochanteric: AO-OTA 32) and intracapsular (AO-OTA 31-B) [31]. Statistical analysis This was performed with IBM SPSS for Windows1 version 22 (SPSS inc., Chicago, IL). Results were considered statistically significant for p < 0.05. Results A total of 1003 proximal femoral fractures (1003 patients; 278 males; 490 fractures involved the right side) fulfilled the inclusion criteria and were included into the study. The mean age was 81.5 years (range: 46–106 years, SD: 11.29 years) and the median AMTS was 9 (mode: 10). DEXA scans had been performed to 151 patients and the mean T-Score of the hip was 2.55 (SD: 0.96). Length of stay (LOS) was 19.54 days (1–126 days; SD: 14.24 days). Fractures were then classified according to the AO-OTA classification. A total of 413 fractures (41.18%) were AO-31-A (intertrochanteric, extracapsular) fractures, four fractures (0.4%) were AO-32 (purely subtrochanteric, extracapsular) whereas 586 fractures (58.4%) were AO-31-B (intracapsular fractures). With regards to the degree of HOA, patients were classified as follows: Grade 0: 110 patients (11%), grade 1: 455 patients (45.4%), grade 2: 377 patients (37.6%), grade 3: 53 patients (5.3%) and grade 4: eight patients (0.8%) (Table 1).
Table 1 Patient demographics. Number of patients
1003
Age
Mean: 81.5 years Range: [46–106] SD: 11.29 Male 278 (27.7%) Female 725 (72.3%) Mean: 7.14 Range: [0–10] SD: 3.48 N: 151 Mean: 2.549 Range: [ 5.6 to 0.2] SD: 0.96 Mean: 19.5 days Range: [0–126 days] SD: 14.24 Extracapsular (31-A) 417 (41.6%) Intracapsular (31-B) 586 (58.4%) Left 514 (51.2%) Right 489 (48.8%) Grade 0: 110 (11%) Grade 1: 455 (45.4%) Grade 2: 377 (37.6%) Grade 3: 53 (5.3%) Grade 4: 8 (0.8%)
Sex
AMTS
T-Score (DEXA)
Length of Stay (LOS)
Fracture type
Fracture site
Fracture site grade of HOA
AMTS: Abbreviated Mental Test Score. DEXA: Dual Energy X-ray Absorptiometry. HOA: Hip Osteoarthritis. SD: Standard Deviation.
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Two hundred and forty-five patients (24.5%) had one or more immediate post-operative medical complications during their admission, whilst 70 patients (7%) had one or more complications involving their fracture fixation and/or healing during the follow up period. The average time of follow up was 1.08 years (range: 0– 1.42 years). When we compared the presence of a medical complication in relation to the type of fracture, we identified that 110 patients presented with an extracapsular fracture (26.4%), compared to 135 patients who presented with an intracapsular fracture (23%), (p = 0.22). Regarding fixation complications, 31 patients (7,4%) presented with extracapsular fractures and 39 patients (6.7%) presented with intracapsular fractures (p = 0.75). The degree of HOA was then analyzed according to the fracture pattern. Patients presenting with extracapsular fractures were classified as Grade I in 33.2% of the cases, as Grade II in 45.6% of the cases, as Grade III in 67.9% of the cases and as Grade IV in 75.0% of the cases (Table 2,Fig. 1). We then divided the patients into two groups. Group 1 involved minimal HOA (Grades I and II) and Group 2 involved severe HOA (Grades III and IV). When we compared the two groups, we found that Group 1 had a higher incidence of intracapsular fracture patterns (61.2%), whereas Group 2 had a higher incidence of extracapsular fracture patterns (68.9%); p < 0.01 (Table 3). In the presence of severe HOA, the risk of sustaining an extracapsular fracture was calculated to be more than 3-fold (Risk ratio: 3.19; Confidence Interval (CI): 95% 1.89–5.40). On the contrary, there was little difference in the fracture type observed in patients with minimal HOA (Risk ratio: 0.92; CI 95% 0.88–0.96). Examining for a potential relation of grade of HOA and age, it was noted that there was no association (Group 1: 81.7 years vs Group 2: 81.2 years; p = 0.74). Additionally, no association was identified between the grade of HOA and the fracture pattern observed (intracapsular: 82.09 vs extracapsular: 82.18 years; p = 0.13) (Table 4). Finally, we compared the relationship between fracture types and gender, age, T-Score (> 2.5 versus 2.5), the presence or absence of history of previous hip fractures and the prescription of Calcium/Vitamin D prior to admission time. With regards to gender, male patients presented with extracapsular fractures in 38.8% of the cases, whereas female patients presented with extracapsular fractures in 42.6% of the cases (p = 0.28). To assess the relationship between age and fracture pattern, we compared patients younger than the age of 80 years (presented with extracapsular fractures in a 37.7% of cases), to the patients older than the age of 80 years (presented with extracapsular fractures in 43.6% of the cases). There was a trend that patients older than 80 years of age presenting with an extracapsular fracture, but this did not reach statistical significance (p = 0.06). Regarding the presence or absence of osteoporosis, patients with a hip T-Score 2.5, presented with an extracapsular fracture in a 48.8% of cases, whereas patients with a T-Score above 2.5 presented with an extracapsular fracture in a 25.4% of cases, and this was statistically significant (p < 0.01). In those patients with
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Fig. 1. When the grade of hip osteoarthritis rises, so do the possibilities of sustaining an extracapsular fracture.
previous history of fragility fractures, extracapsular fractures where found in 53.3% of the cases, whereas in cases without a history of previous osteoporotic fractures, extracapsular fractures were identified in 36.8% of the cases, which again reached the level of significance (p < 0.01). Finally, patients receiving oral calcium/ vitamin D supplements prior to admission, had extracapsular fractures in 50.2% of cases, whereas those not receiving these supplements, only presented with extracapsular fractures in 38.6% of the cases (p < 0.01) (Table 5). Discussion Despite some reports investigating the potential protective effect of HOA against hip fragility fractures, little attention had been paid to the correlation between the degree of HOA and the fracture pattern observed. In our study, we attempted to shed more light into the above, by identifying and reporting any possible associations between the degree of HOA and the fracture pattern observed. When we compared our series to those of other authors, we found that the demographics were comparable. More specifically, the mean age of our cohort was 81.5 years, whereas in the literature this ranged from 80.8 years to 85.5 years [13,22,24]. Our observed male to female ratio was 3:7, also comparable to that reported by Uzoigwe et al. [24], but including more male patients as compared to reports by Calderazzi and Dinamarca-Montecinos [13,22]. Regarding the fracture pattern (31A: 41.6%; 31B: 58.4%), this was similar to the one reported by Uzoigwe et al. (31A: 44%; 31B: 56%) [24], but different than the one presented by DinamarcaMontecinos (31A: 33.7%; 31B: 66.3%) [22]. On the contrary, the grade of HOA distribution in our series was different than the one reported by Calderazzi et al. [13]. Whereas in our series we found an 11.0% of absent, 83.0% of minimal and a 6% of severe HOA, Calderazzi et al. observed absent HOA in 40%, minimal in 43.7% and severe in 16.3%. These differences, could be due to differences in the definition of HOA, as we considered narrowing of the joint space as a criterion for grade I HOA (Table 6). In our series, we identified that 24.5% of our patients had one or more medical complications, compared to 20% reported by Roche et al. [33]. Merchant et al. [34] and Folbert et al. [35] reported
Table 2 Fracture patterns according to Kellgren and Lawrence’s grades of hip HOA. Grade of HOA Fracture type
0
I
II
III
IV
Total
Extracapsular 31A Intracapsular 31B
52 (47.3%) 58 (52.7%) 110
151 (33.2%) 304 (66.8%) 455
172 (45.6%) 205 (54.4%) 377
36 (67.9%) 17 (32.1%) 53
6 (75%) 2 (25%) 8
417 (41.6%) 586 (58.4%) 1003 p < 0.01
HOA: Hip Osteoarthritis.
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Table 3 Fracture patterns according to simplified classification of hip HOA.
HOA: Hip Osteoarthritis.
Table 4 Influence of age on osteoarthritic changes present at admission time and on fracture pattern. N
Mean age (years)
Standard Deviation
Minimal grades (1–2) Severe grades (3–4)
832 61
81.2 81.7
11.44 10.94 p = 0.74
Extracapsular (31-A) Intracapsular (31-B)
417 586
82.18 81.09
11.57 11.09 p = 0.13
higher rates of medical complications (33.3% and 49.6% respectively), but such differences may account to the higher mean age of their samples or the definition of what constitutes a medical complication. No differences were noted according to the type of PFF fracture [34]. Regarding the potential association of the grade of HOA to the fracture pattern observed, we demonstrated the presence of a statistically significant relationship between these two variables. This is in line with the report by Calderazzi et al. [13]. More specifically, they reported that 63.6% of proximal femur fractures appeared in patients with minimal grades of HOA were classified as intracapsular. On the other side, when patients with severe grades
Table 5 Fracture patterns and their correlation with gender, age, BMD, History of previous fractures and calcium/vitamin D supplement use at admission time. Age
Gender Male 31A (41.6%) 31B (58.4%)
Female
108 (38.8) 309 (42.6%) 180 (61.2%) 416 (57.4%) p = 0.28
<80 y
T-Score (hip) > = 80 y
132 (37.7%) 285 (43.6%) 218 (62.3%) 368 (56.4%) p = 0.06
< = 2.5
Prev. Fracture > 2.5
39 (48.8%) 18 (25.4%) 41 (51.3%) 53 (74.6%) p < 0.01
No
Calcium/VitD intake Yes
256 (36.8%) 161 (53.3%) 439 (63.2%) 147 (47.7%) p < 0.01
No
Yes
287 (38.6%) 130 (50.2%) 457 (61.4%) 129 (49.8%) p < 0.01
BMD: Bone Mass Density. Results in bold indicate statistical significance
Table 6 Discusion. Comparison of our results with the published literature. Current study
Calderazzi et al.
Dinamarca-Montecinos et al.
Uzoigwe et al.
1003 81.5
134 85.5
647 80.8
2987 81
27.7% 72.3%
22.4% 77.6%
23.8% 76.2%
28.6% 71.4%
Fracture type Intracapsular Extracapsular
58.4% 41.6%
63.4% 36.6%
66.3% 33.7%
56% 44%
HOA Grade Absent Minimal Severe
11% 82.9% 6.1%
43.3% 41% 15.7%
Not reported
Not reported
Not reported
Not reported
52.7% 47.3%
77.6% 22.4%
61.2% 38.8%
63.6% 36.4%
31.1% 68.9%
23.8% 76.2%
N Age (years) Sex Male Female
Absent HOA Intracapsular Extracapsular Minimal HOA Intracapsular Extracapsular Severe HOA Intracapsular Extracapsular
HOA: Hip Osteoarthritis as Kellgren and Lawrence.
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of HOA sustained a proximal femur fracture, the probability of sustaining trochanteric fracture was as high as 76.2% (68.9% in our series). Calderazzi et al. found higher differences between groups, but all contrast with our results should be understood under the perspective that in our analysis, the ratio intracapsular/extracapsular was of 1.4:1 and the observed by Calderazzi et al. was 1.7:1. To explain this association, we have found theories [15,18,36] which focus on intrinsic characteristics of the osteoarthritic hips that may lead to the probability of sustaining different fracture types according to the degree of HOA. They are related to variable distribution of BMD and cortical porosity through the femoral neck in patients with HOA [15,36] and different range of motion (ROM) in osteoarthritic hips [18]. One of the most popular theories suggests that differences in BMD secondary to HOA in each zone around the hip, can lead to “weak” areas [16,29]. Subsequently, this leads to development of stress risers, which in turn predispose to fractures even following minimal trauma. More specifically, Wolf et al. reported a reduced BMD of the trochanteric area in patients affected by HOA, whilst an increased BMD was observed around the femoral neck in the same osteoarthritic hips [15]. Similarly, Greenspan et al., reported that the BMD of the trochanteric area was 11–13% lower in patients presenting with an extracapsular fracture, compared to those presenting with an intracapsular fracture [28]. Moreover, Blain et al. assessed cortical porosity in osteoporotic and HOA hip, suggesting that in osteoporosis, fragility fractures result both from the cortical thinning and the trabecular bone rarefaction associated with loss of trabecular connectivity [36]. On the contrary, cortical porosity was higher in HOA which in combination to the cortical thinning contributes to the loss of cortical strength and therefore lead to fragility fractures [36]. In our study, we have demonstrated a significance between HOA, loss of BMD and fracture pattern observed, which is in line with the above findings. Another theory supported by many authors [17,18], relates to the ROM of the osteoarthritic hips. More specifically, it supports that the mechanism of injury of intracapsular fractures is based on a forced external rotation that could lead to an impingement in the posterior wall of the acetabulum that in turn could fracture the neck of the femur. In a cadaveric study, Binns et al. [18] demonstrated that an average of 54.5 of external rotation was needed for this impingement to occur, and that hips resulting in intracapsular fractures had a higher ROM (62.1 ) compared to those resulting in extracapsular fractures (48.9 ). Even though the cause of a reduced ROM is not fully understood, it represents a characteristic feature of HOA. In a further analysis of our results, we studied other parameters such as the age, sex, BMD and history of previous fractures or prescription of calcium supplements prior to admission. Our results show a higher mean age in patients sustaining extracapsular fractures (82.18 years versus 81.09 years), but this failed to reach significance. Fox et al. observed that patients with extracapsular fractures were 1.8 years older than those presenting intracapsular fractures (p = 0.02) [23]. Similar results were reported by other authors who agree that extracapsular fractures occur in an elder population, compared to intracapsular fractures [21,26,37]. In patients younger than the age of 80 years old, extracapsular fractures only occurred in 37.7% of the cases. In patients age 80 years or more, the distribution of fracture types tends to be comparable (43.6% of extracapsular fractures; p = 0.06). The aetiology could be twofold: when population gets older, osteoarthritic changes may become more evident and this may lead to extracapsular fracture patterns. Moreover, type II of Riggs senile osteoporosis [38] is more prevalent in the elderly people and is associated with extracapsular fractures of the proximal femur. An association between lower BMD and trochanteric fractures was also found to be significant. This is in line with findings
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observed by Nakamura et al. [39] and Spencer et al. [40] who found that patients with extracapsular fractures had statistically significant lower BMD than those presenting intracapsular fractures. The authors suggested that trochanteric area has an 80 to 90% of cancellous bone and is therefore affected at a higher degree by the remodeling imbalance secondary to osteoporosis. We also found a statistically significant association with the history of previous fractures or calcium supplements prescription and the type of fracture observed. Fox et al. also reported an unexpected association between the oral intake of calcium supplements and the presence of intertrochanteric fractures [23]. They postulated the theoretical relationship between the calcium supplements prescription on patients with osteoporosis and therefore lower BMDs. The same explanation would apply to those patients presenting history of fragility fractures, as patients with history of multiple fragility injuries have lower BMDs. Conclusion We identified a relationship between the presence of severe osteoarthritic changes and the presence of an extracapsular fracture, whereas hips with low grades of HOA tend to present intracapsular patterns. Extracapsular fractures are also associated to lower T-Scores and history of previous fragility fractures. Conflict of interest All authors declare no conflict of interest in relation to this study. Acknowledgments We would like to thank González-Sagrado M, MD from the Research Support Unit and De Andrés-Loste ML at Hospital Universitario del Río Hortega from Valladolid, Spain, for the statistical and bibliographical support. References [1] Kassim Javaid M, Chana J, Cooper C. Hip fracture as the tracer condition. Best Pract Res Clin Rheumatol 2013;27:711–5, doi:http://dx.doi.org/10.1016/j. berh.2014.03.003. [2] Nieves JW, Bilezikian JP, Lane JM, Einhorn TA, Wang Y, Steinbuch M, Cosman F. Fragility fractures of the hip and femur: incidence and patient characteristics. Osteoporos Int 2010;21:399–408, doi:http://dx.doi.org/10.1007/s00198-0090962-6 Epub 2009 May 30. [3] Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res Off J Am Soc Bone Miner Res 2007;22:465–75, doi:http://dx.doi.org/10.1359/jbmr.061113. [4] Aspray TJ. Fragility fracture: recent developments in risk assessment. Ther Adv Musculoskelet Dis 2015;7:17–25, doi:http://dx.doi.org/10.1177/ 1759720X14564562. [5] Kravtsov V, Saranga D, Kidron D. Osteoarthritic changes in hip joint in patients with fractures of femoral neck. Harefuah 2013;152(335–339):368. [6] Chapurlat RD, Bauer DC, Nevitt M, Stone K, Cummings SR. Incidence and risk factors for a second hip fracture in elderly women. The Study of Osteoporotic Fractures. Osteoporos Int 2003;14:130–6, doi:http://dx.doi.org/10.1007/ s00198-002-1327-6. [7] Liu W, Yang LH, Kong XC, An LK, Wang R. Meta analysis of osteoporosis: fracture risks, medication and treatment. Minerva Med 2015. [8] Caffarelli C, Alessi C, Nuti R, Gonnelli S. Divergent effects of obesity on fragility fractures. Clin Interv Aging 2014;9:1629–36, doi:http://dx.doi.org/10.2147/ CIA.S64625. [9] Mesa-Ramos M, Caeiro-Rey JR, Etxebarría-Foronda I, Carpintero-Benítez P. Aspects of interest on vitamin D for the traumatologist and orthopaedic surgeon. Rev Esp Cir Ortopédica Traumatol 2012;56:164–73, doi:http://dx.doi. org/10.1016/j.recot.2011.11.006. [10] Weintroub S, Papo J, Ashkenazi M, Tardiman R, Weissman SL, Salama R. Osteoarthritis of the hip and fracture of the proximal end of the femur. Acta Orthop Scand 1982;53:261–4. [11] Chudyk AM, Ashe MC, Gorman E, Al Tunaiji HO, Crossley KM. Risk of hip fracture with hip or knee osteoarthritis: a systematic review. Clin Rheumatol 2012;31:749–57, doi:http://dx.doi.org/10.1007/s10067-012-1970-z.
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