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Function, sarcopenia and osteoporosis 10 years after a femoral neck fracture in patients younger than 70 years

Open AccessPublished:December 21, 2021DOI:https://doi.org/10.1016/j.injury.2021.12.030

      Highlights

      • The majority of patients less than 70 years of age with a femoral neck fracture treated with CRIF had a normal muscle strength and self-assessed function 10 years later.
      • One third of patients less than 70 years of age with a femoral neck fracture are sarcopenic 10 years later indicating the importance of regular muscle preserving resistance training.

      Abstract

      Background and purpose

      A femoral neck fracture (FNF) may have long-term effects on the patient's function, also in patients younger than 70 years. These long-term effects are not well described, since most studies have short follow-ups. The aim of this study was to investigate clinical outcome by performance-based functional tests, hand grip strength, and hip function in different subgroups. The secondary aim was to study surgical complications, bone mineral density (BMD) and occurrence of sarcopenia 10 years after a FNF.

      Patients and methods

      A prospective multicenter study with a 10-year follow-up of patients aged 20–69 years with a FNF treated with internal fixation (IF). Five-times sit-to-stand test (5TSST), 4-m walking speed test, hand grip strength (HGS) and Harris Hip Score (HHS) were performed.
      A radiographic examination of the hip was performed and re-operations were registered. Bone mineral density (BMD) at the hip, spine and total body composition were assessed with dual energy x-ray absorptiometry (DXA). Present sarcopenia was determined by the combination of reduced functional performance and low fat-free mass index (FFMI).

      Results

      A total of 58 patients were included. 5TSTS was normal in 45% of the patients and old age was associated with poorer performance (p<0.001). 76% of the study population had a normal speed gait and likewise, old age (p = 0.005) and walking aids (p = 0.001) were associated with poor performance. HGS was normal in 82% of the men and 64% of the women. HHS showed that 85% had a good/excellent function. A major re-operation was performed in 34% of the patients with displaced FNF and in 20% of patients with non-displaced FNF. 74% displayed osteopenia and 12% osteoporosis. 17% of the men and 38% of the women had sarcopenia.

      Interpretation

      The majority of patients less than 70 years of age with a FNF treated with IF, had normal functional tests, muscle strength and a good hip function ten years post-operatively. However, one in ten had osteoporosis, and one third was sarcopenic which indicate the importance of encouraging regular muscle preserving resistance training after hip fracture.

      Keywords

      Introduction

      Femoral neck fractures (FNF) are uncommon in patients younger than 70 years of age, but may result in lifetime disability [
      • Robinson C.M.
      • Court-Brown C.M.
      • McQueen M.M.
      • Christie J.
      Hip fractures in adults younger than 50 years of age. Epidemiology and results.
      ,
      • Duckworth A.D.
      • Bennet S.J.
      • Aderinto J.
      • Keting J.F.
      Fixation of intracapsular fractures of the femoral neck in young patients: risk factor for failure.
      ]. Surgical or general postoperative complications have traditionally been used to evaluate the clinical results after a hip fracture [
      • Robinson C.M.
      • Court-Brown C.M.
      • McQueen M.M.
      • Christie J.
      Hip fractures in adults younger than 50 years of age. Epidemiology and results.
      ,
      • Damany D.S.
      • Parker M.J.
      • Chojnowski A.
      Complications after intracapsular hip fractures in young adults. A meta-analysis of 18 published studies involving 564 fractures.
      ]. However, to evaluate patient´s function post-operatively might be even more relevant, especially for younger patients [
      • Sprague S.
      • Slobogean G.P.
      • Scott T.
      • Chahal M.
      • Bhandari M.
      Young femoral neck fractures: are we measuring outcomes that matter?.
      ].
      Studies on patients with a hip fracture with a follow-up exceeding two years are mainly register-based, retrospective and usually includes elderly populations [
      • Do L.N.D.
      • Kruke T.M.
      • Foss O.A.
      • Basso T.
      Reoperations and mortality in 383 patients operated with parallel screws for Garden I-II femoral neck fractures with up to ten years follow-up.
      ,
      • Lie S.A.
      • Engesaeter L.B.
      • Havelin L.I.
      • Gjessing H.K.
      • Vollset S.E.
      Mortality after total hip replacement: 0-10 year follow-up of 39,543 patients in the Norwegian Arthroplasty Register.
      ]. Main focus is often surgical failures, while functional outcomes are usually not noticed [
      • Robinson C.M.
      • Court-Brown C.M.
      • McQueen M.M.
      • Christie J.
      Hip fractures in adults younger than 50 years of age. Epidemiology and results.
      ,
      • Damany D.S.
      • Parker M.J.
      • Chojnowski A.
      Complications after intracapsular hip fractures in young adults. A meta-analysis of 18 published studies involving 564 fractures.
      ,
      • Haidukewych G.J.
      • Rothwell W.S.
      • Jacofsky D.J.
      • Torchia M.E.
      • Berry D.J.
      Operative treatment of femoral neck fractures in patinets between the ages of fifteen and fifty years.
      ].
      Many elderly patients as well as patients less than 70 years of age at the time of fracture have a low bone mineral density (BMD) [
      • Emohare O.
      • Wiggin M.
      • Hemmati P.
      • Switzer J.
      Assessing Bone Mineral Density following acute hip fracture: the role of computer tomography attenuation. Ger.
      ,
      • Campenfeldt P.
      • Al-Ani A.
      • Hedström M.
      • Ekström W.
      Low BMD and high alcohol consumption predict a major re-operation in patients younger than 70 years of age with a displaced femoral neck fracture- A two-year follow up study in 120 patients.
      ] but it is unclear if this further deteriorates the following 10 years after the fracture. The prevalence of sarcopenia, i.e. the combined reduction of muscle strength and muscle mass [

      Cruz-Jentoft A., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2) and the extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.

      ], in hip fracture patients has been reported to be 17–58%, depending on population and definition of sarcopenia [
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Di Monaco R.
      • et al.
      Presarcopenia and sarcopenia in hip fracture women: prevalence and association with ability to function in activities of daily living.
      ,
      • Gonzalez-Montalvo J.I.
      • Alarcon T.
      • Gotor P.
      • Queipo R.
      • Hoyos R.
      • et al.
      Prevalence of sarcopenia in acute hip fracture patients and its influence on short-term clinical outcome.
      ]. However, no studies have examined the frequency of sarcopenia 10 years after a FNF in patients younger than 70 years of age.
      The aim of this study was to investigate clinical outcomes by functional performance tests, muscle strength and hip function as well as surgical complications, bone mineral density (BMD) and occurrence of sarcopenia 10 years after a FNF in patients 20–69 years at the time of fracture.

      Materials and methods

      This is a 10-year follow-up study of a subgroup of patients from an earlier multicenter study in patients aged 20–69 years with a FNF (Garden 1–4) [
      • Campenfeldt P.
      • Hedström M.
      • Ekström W.
      • Al-Ani A
      Good functional outcome but not regained health related quality of life in the majority of 20-69 years old patients with femoral neck fracture treated with internal fixation: a prospective 2-year follow-up study of 182 patients.
      ]. All patients were admitted to any one of the four university hospitals in Stockholm, Sweden during the years 2003–2005. Patients had an operation with a closed fracture reduction (Garden 3–4) and internal fixation (CRIF) with two cannulated screws. Only patients who were able to walk before the fracture and living independently were included. At the time of fracture, patients with psychotic disease or cognitive impairment according to Short Portable Mental Status Questionnaire (SPMSQ <3) [
      • Pfeiffer E.
      A short portable mental status questionnaire for the assessment of organic brain deficit in elderly patients.
      ] were excluded. Patients with a fracture older than 48 h before admission, previous pathology in the fractured hip, and risk factors for secondary osteoporosis (hyperparathyroidism and chronic renal failure) were also excluded.
      For the 10-year follow-up, patients from three of the participating university hospitals were contacted, whereas patients initially from the fourth university hospital were excluded due to lack of resources for a re-examination. Deceased patients were registered.
      The following variables were recorded at the 10-year follow-up: age, gender, BMI, re-operations and new fractures since index operation. Moreover, living conditions, walking ability, walking aids or not, smoking and American Society of Anesthesiologists classification (ASA) [

      American Society of Anesthesiologists- ASA Physical Status Classification System. https://www.asahq.org/standards-and-guidelines/asa-physical-status-classification-system

      ] were recorded. Functional tests were conducted and each test session started with a physical examination of the hip following a standardized protocol including Harris Hip Score (HHS) [
      • Harris W.H.
      Traumatic arthritis of the hip after dislocation and acetabular fractures: treatment by mold arthroplasty. An end-result study using a new method of result evaluation.
      ]. Performance-based functions were evaluated by five-times sit-to-stand test (5TSTS) [

      Guralnik J.M., Simonsick E.M., Ferrucci L., Glynn R.J., Berkman L.F., Blazer D.G. et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol, 49, M85–94.

      ], 4-m walking speed test [
      • Abellan van Kan G.
      • Rolland Y.
      • Andrieu S.
      • Bauer J.
      • Beauchet O.
      • Bonnefoy M.
      • et al.
      Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an International Academy on Nutrition and Aging (IANA) Task Force.
      ] and hand grip strength (HGS) measured by Jamar hand dynamometer [
      • Schmidt R.T.
      • Toews J.V.
      Grip strength as measured by the Jamar dynamometer.
      ]. Radiography of the previously fractured hip was taken and re-operations were registered. Extractions of the screws were coded as minor surgery and conversion to a total hip replacement (THR) was coded as a major re-operation. Total body, spine and hip BMD (contralateral side) and body composition were measured by dual energy x-ray absorptiometry (DXA). Presence of sarcopenia was defined by the combination of the low fat-free mass index (FFMI) and a low outcome in any of the functional performance tests and strength in accordance with European Working Group on Sarcopenia in Older People 2 (EWGSOP2) [

      Cruz-Jentoft A., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2) and the extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.

      ].

      Muscle strength

      HGS (kg) was measured in the dominant hand (JAMAR 50,301 J) with the patients in a sitting position and the highest value of three hand grip attempts was registered. Cut-off points used for low HGS indicating sarcopenia were < 16 kg in women and < 27 kg in men [

      Cruz-Jentoft A., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2) and the extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.

      ]. HGS measured with a hand dynamometer is an easy and recommended way to assess muscle strength [
      • Roberts H.C.
      • Denison H.J.
      • Martin H.J.
      • Patel H.P.
      • Syddall H.
      • Cooper C.
      • et al.
      A review of the measurement of grip strength in clinical epidemiological studies towards a standardised approach.
      ]. The Jamar hand dynamometer is the most widely used instrument with good reproducibility (r > 0.80) and reliability (r = 0.98) [
      • Roberts H.C.
      • Denison H.J.
      • Martin H.J.
      • Patel H.P.
      • Syddall H.
      • Cooper C.
      • et al.
      A review of the measurement of grip strength in clinical epidemiological studies towards a standardised approach.
      ].

      Performance based functional tests

      5TSTS was conducted by measuring the time taken to stand up from a sitting position five times as fast as possible without the use of the arms [
      • Whitney S.
      • Wrisley D.
      • Marchetti G.
      • Gee M.
      • Redfern M.
      • Furman J.
      Clinical measurement of Sit-to-Stand Performance in people with balance disorders: validity of data for the Five-Times-Sit-to-Stand Test.
      ]. The patients performed the entire test three times with at least 5-minute rest between the tests and the mean result was calculated. Cut-off points for sarcopenia according to EWGSOP2 are >15 s for five rises [

      Cruz-Jentoft A., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2) and the extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.

      ]. 5TSTS is often used in clinical practice [
      • Goldberg A.
      • Chavis M.
      • Watkins J.
      • Wilson T.
      The five-times-sit-to-stand test: validity, reliability and detectable change in older females.
      ]. The performance on this test is based upon lower limb strength, especially quadriceps strength, and has been suggested as an alternative measure for lower limb strength in older people [
      • Lord S.R.
      • Murray S.M.
      • Chapman K.
      • Munro B.
      • Tiedemann A.
      Sit-to-stand performance depends on sensation, speed, balance, and psychological status in addition to strength in older people.
      ]. Subjects who need more than 15 s to complete the test have a 74% greater risk of recurrent falls [
      • Buatois S.
      • Miljkovic D.
      • Manckoundia P.
      • Gueguen R.
      • Miget P.
      • Vançon G.
      • et al.
      Five times sit to stand test is a predictor of recurrent falls in healthy community-living subjects aged 65 and older.
      ].
      In the 4-meter walking speed test the patients were instructed to walk their normal pace with their assistive device if necessary. The patients walked down a hallway through a 1-meter zone for acceleration, a central 4-meter “testing” zone and a 1-meter zone for deceleration [
      • Sudentski S.
      • Perera S.
      • Wallace D.
      • Chandler J.M.
      • Duncan P.W.
      • Rooney E.
      • et al.
      Physical performance measures in the clinical setting.
      ]. The timer started with the first footfall after the 0-meter line and stopped with the first footfall after the 4-meter line. The patients repeated the test three times and the best score was recorded. A cutoff value of less than 0.8 m/sec could indicate sarcopenia according to EWGSOP2 [

      Cruz-Jentoft A., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2) and the extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.

      ]. Epidemiological studies of reliability and validity of gait speed assessment in elderly indicate that this parameter is an independent predictor of a wide range of poor clinical outcomes in older persons, including disability, falls, hospitalization/institutionalization and mortality [
      • Montero-Odasso M.
      • Schapira M.
      • Soriano E.R.
      • Varela M.
      • Kaplan R.
      • Camera R.A.
      • et al.
      Gait velocity as a single predictor of adverse events in healthy senior aged 75 years and older.
      ,
      • Cesari M.
      • Kritchevsky S.B.
      • Penninx B.W.
      • Nicklas B.J.
      • Simonsick E.M.
      • Newman A.B.
      • et al.
      Prognostic value of usual gait speed in well-functioning older people-results from the Health, Aging and Body Composition Study.
      ].

      Body composition and definition of sarcopenia

      Body composition, total lean body mass (LM), fat mass and bone mineral content (BMC) were also measured. The sum of BMC and LM represents fat-free mass (FFM). To normalize for body size, the fat-free mass index (FFMI, kg/m²) was calculated by dividing the FFM by height squared. Fat mass index (FMI, kg/m²) was calculated analogously [
      • Schutz Y.
      • Kyle U.U.
      • Pichard C.
      Fat-free mass index and fat mass index percentiles in Caucasians aged 18–98 y.
      ]. Cut-offs for low FFMI indicating sarcopenia for men were <17 kg/m² and <15 kg/m² for women [
      • Kyle U.G.
      • Piccoli A.
      • Pichard C.
      Body composition measurement: interpretation finally made easy for clinical use.
      ]. Sarcopenia was diagnosed if the patients displayed values below cut-off both for FFMI and for either HGS or 5TSTS in accordance with EWGSOP2 [

      Cruz-Jentoft A., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2) and the extended group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis.

      ].

      Hip function

      The postoperative hip function was measured by Harris Hip Score (HHS), a validated instrument that evaluates pain, function, range of motion and deformity of the hip [
      • Harris W.H.
      Traumatic arthritis of the hip after dislocation and acetabular fractures: treatment by mold arthroplasty. An end-result study using a new method of result evaluation.
      ]. It has a scale of 100 points in which pain constitute 44 points. Severe pain at rest gives a value of 0 and no pain gives a value of 44. Function has a maximum level of 43 points and includes evaluation of walking ability and daily activities. Maximum range of motions gives 5 points and absence of deformities gives 4 points. HHS is categorized as excellent if > 80, good between 70 and 80 and poor at < 70 points [
      • Harris W.H.
      Traumatic arthritis of the hip after dislocation and acetabular fractures: treatment by mold arthroplasty. An end-result study using a new method of result evaluation.
      ].

      Bone mineral density measurements

      BMD was measured by DXA using Hologic (Hologic corp.) or Lunar (Lunar corp.) densitometers. The BMD on the contralateral hip was evaluated when possible otherwise the values from the lumbar spine were used. The results were expressed as both areal density (g/cm²) and as standard deviation units related either to the mean value of healthy young individuals, (T-score) or to the mean value of age- and sex-matched adults (Z-score) according to recommendation by the International Society of Clinical Densitometry [
      Writing Group for the ISCD Position Development Conference
      Diagnosis of osteoporosis in men, premonopausal women, and children.
      ]. Z -score < −2 standard deviation (SD) was considered as a low BMD [
      Writing Group for the ISCD Position Development Conference
      Diagnosis of osteoporosis in men, premonopausal women, and children.
      ]. A T-score >−1 SD was considered a normal BMD, osteopenia if T-score of −1 to −2.49 SD and osteoporosis if T-score ≤−2.5 SD [
      • Kanis J.A.
      • McCloskey E.V.
      • Johansson H.
      • Cooper C.
      • Rizzoli R.
      European guidance for the diagnosis and management of osteoporosis in postmenopausal women.
      ].
      Patients were asked about history or on-going medical treatment for osteoporosis.

      Surgical complications

      Radiographics of the previously fractured hip were assessed as healed fracture and avascular necrosis was defined as segmental collapse, loss of sphere of the femoral head or subchondral fracture [
      • DeSmet A.A.
      • Dalinka M.K.
      • Alazraki N.
      • Berquist T.H.
      • Daffner R.H.
      • el-Khoury G.Y.
      • et al.
      Diagnostic imaging of vascular necrosis of the hip. American College of Radiology. ACR Appropriateness Criteria.
      ].
      A major re-operation was defined as a hip replacement and a minor re-operation if only the screws were extracted.

      Living condition, walking ability, smoking and ASA score

      Living conditions were registered as independent (i.e. own home or block of serviced flats) or as institutionalized. Walking ability was recorded as walking outdoors, walking indoors or unable to walk. Use of walking aids or not was recorded. The ASA score [

      American Society of Anesthesiologists- ASA Physical Status Classification System. https://www.asahq.org/standards-and-guidelines/asa-physical-status-classification-system

      ] was assessed at the 10-year follow-up and were divided into 5 scores (ASA 1–5) depending on the physical status of the patient. Current smokers were coded as smokers.
      All patients were treated according to identical study protocols. All assessments were carried out by physicians involved in this research project.

      Statistics

      Statistical calculations were performed using SPSS version 26 for Windows (IBM, SPSS Statistics). Mean, (SD), and percentage were used for descriptive purposes. Pearson's chi-square test was used for testing differences in contingency tables. Student T-Test and paired-sample T-test were used in continuous variables. A p-value of less than 0.05 was considered statistically significant in all analyses.

      Ethical considerations

      The study was conducted according to the Helsinki Declaration [
      • World Medical A.
      World Medical Association Declaration of Helsinki. Ethical principles for medical research involving human subjects.
      ] The local Ethics Committee (Dnr. 2001–427, Dnr. 2013–602–32) approved the protocols. STROBE guidelines were used when reporting of the study [
      • von Elm E.
      • Altman D.G.
      • Egger M.
      • Pocock S.J.
      • Gotzche P.C.
      • Vandenbroucke J.P.
      The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies.
      ]. The study was funded by grants provided by Region Stockholm (ALF project).

      Results

      General characteristics

      Baseline characteristics are displayed in Table 1. From the primary cohort of 92 patients from three university hospitals, two patients were de-registered from the public record, 22 patients were deceased and 10 patients declined participation or were not located. A total of 58 patients participated in the 10-year follow-up (Fig. 1). The average age at 10-years follow-up was 67 years (range 32–80 years, 52% women). All but one still lived independently.
      Table 1Characteristics of the study population according to gender at 10-year follow-up (n = 58) after a femoral neck fracture treated with closed reduction and internal fixation. Data presented as n (%).
      All patientsn = 58Menn = 28Womenn = 30p-value
      Mean age (SD)5866 (11.3)67 (11.0)0.67
      Independent Samples Test,.
      BMI mean (SD)
      missing 1,.
      24 (4)24.5 (3.3)22.7 (3.1)0.07
      Independent Samples Test,.
      n (%)n (%)n (%)
      Fracture type
      Non-displaced fracture

      Displaced fracture
      22 (38)

      36 (62)
      8 (29)

      20 (71)
      14 (47)

      16 (53)
      0.16
      Chi-square test.
      ASA
      1

      2

      3
      20 (35)

      25 (43)

      13 (22)
      13 (46)

      7 (25)

      8 (29)
      7 (23)

      18 (60)

      5 (17)
      0.03
      Chi-square test.
      Smoking
      Yes

      No
      13 (22)

      45 (78)
      6 (21)

      22 (79)
      7 (23)

      23 (77)
      0.86
      Chi-square test.
      Major re-operation
      Yes

      No
      17 (29)

      41 (71)
      8 (29)

      20 (71)
      9 (30)

      21 (70)
      0.91
      Chi-square test.
      a Independent Samples Test,.
      b missing 1,.
      c Chi-square test.
      Fig. 1
      Fig. 1A flowchart of the numbers of patients with completed tests at 10-year follow-up.
      Only seven patients used walking aids in form of crutches or a walker. There were 22% (n = 13) current smokers. A total of 35% (n = 20) were classified as ASA grade 1, 43% (n = 25) grade 2 and 22% (n = 13) grade 3.
      Analysis of baseline data of the 10 patients who did not want to participate revealed that the mean age at time of fracture was 59 years compared to 55 years for the included patients (p = 0.096). No significant differences were seen between “drop-outs” and participants in the FFMI (p = 0.26), BMI (p = 0.23), displaced fracture or not (p = 0.92), BMD (p = 0.134) and ASA (p = 0.613) at the time of fracture (data not shown).

      Performance based functional tests and muscle strength

      5TSTS showed that 45% (n = 26) managed to do the test within 15 s, 45% (n = 26) needed longer time and 10% (n = 6) could not perform the test at all. Age above 70 years was a significant factor associated with poor performance (Table 2).
      Table 2Results of Five times sit and stand test and 4-m walking test divided into gender, age group, re-operation, type of fracture, ASA-class and use of walking aids in patients with a femoral neck fracture at 10-year follow-up, n = 52.
      VariableNumber Total (n)Sit and stand test <15 s% (n)Sit and stand test >15 s% (n)p-value
      T-test.
      Gait speed ≥0.9 m/s% (n)Gait speed ≤0.8 m/s% (n)p-value
      T-test.
      Sex
      Male

      Female
      27

      25
      44 (12)

      56 (14)
      56 (15)

      44 (11)
      0.18585 (23)

      84 (21)
      15 (4)

      16 (4)
      0.260
      Age
      30–69 years

      70–80 years
      23

      29
      78 (18)

      28 (8)
      22 (5)

      72 (21)
      0.001100 (23)

      72 (21)
      0 (0)

      28 (8)
      0.005

      Surgery
      No or minor

      Major
      37

      15
      49 (18)

      53 (8)
      51 (19)

      47 (7)
      0.93089 (33)

      73 (11)
      11 (4)

      27 (4)
      0.351
      Fracture
      Non-displ.

      Displaced
      18

      34
      56 (10)

      47 (16)
      44 (8)

      53 (18)
      0.50978 (14)

      88 (30)
      22 (4)

      12 (4)
      0.608
      ASA
      1–2

      3–4
      47

      5
      51 (24)

      40 (2)
      49 (23)

      60 (3)
      0.78087 (41)

      60 (3)
      13 (6)

      40 (2)
      0.259
      Walking aids
      None/cane

      Walker/ two crutches
      45

      7
      58 (26)

      0 (0)
      42 (19) 100 (7)0.00287 (41)

      60 (3)
      13 (6)

      40 (2)
      0.001
      1 T-test.
      The 4-m walking speed test showed an average speed of 1,2 m/s with a range of 0.47–2.2 m/s. Walking speed of ≥ 0.9 m/s was found in 76% (n = 44) of the patients (mean age 67 years), whereas 14% (n = 8) displayed a low walking speed (≤ 0.8 m/s), and 10% (n = 6) could not perform the test. Table 2 indicates that mainly high age and need of walking aids were linked to reduced gait speed.
      HGS was normal in a majority of both men (82%) and women (64%). There was no statistical difference in HGS between gender (p = 0.22), fracture type (p = 0.92) and those who had undergone a major re-operation or not (p = 0.98) (data not shown). However, older age as a continuous variable was significantly associated with poor hand grip performance (p = 0.02).

      Body composition and occurrence of sarcopenia

      At the 10-year follow-up, mean FFMI for men was 18.2 (SD 1.3) and for women 14.8 (SD 1.2). Low FFMI values (<17 and <15 kg/m2 in men and women respectively) were seen in 17% (n = 3) of the men and 57% (n = 12) in women; p = 0.02 between gender (Fig. 2). Patients that had undergone a major re-operation had a significant lower FFMI compared to patients with no major re-operation (p = 0.01), (Fig. 2). There were no differences between patients with a displaced and non-displaced FNF (p = 0.31), (Fig. 2).
      Fig. 2
      Fig. 2Fat Free Mass Index (FFMI) presented as normal or low in% between gender, major re-operation or not and fracture type in patients with a previous femoral neck fracture 10 years ago treated with closed reduction and internal fixation. A value < 15 in women or < 17 in men are considered low and indicates sarcopenia.
      Finally, sarcopenia defined as the combined reductions in muscle strength (by HGS or 5STST) and low FFMI was observed in 17% of the men and in 38% of the women. A paired sample t-test comparing FFMI at base-line and at the 10-years follow-up, did not show a significant change (p = 0.66) over time. At baseline the FFMI was 18.0 (SD 1.3) for men and 14.9 (0.9) for women.
      The mean BMI at the follow-up for women was 22.7 (SD 3.1) and for men 24.5 (SD 3.3); p = 0.07 between genders. There was no change in BMI over the 10-year observation period (p = 0.18).

      Bone mineral density

      The BMD was measured at the contralateral femoral neck in 34 patients and at the lumbar vertebrae in eight patients due to a hip-replacement in the contralateral hip. The mean BMD (gm/cm2) for men was 0.697 (SD 0.08) and for women 0.682 (SD 0.08), (p = 0.62). The corresponding mean BMD (gm/cm2) for the same patients at the time of fracture was higher for men and women; 0.772 (SD 0.112) and 0.758 (SD 0.105) (p<0.02), respectively. A clear majority (86%) of the former young hip fracture patients displayed reduced BMD at the follow-up; i.e. osteopenia in 74% (n = 27) and 12% (n = 5) had osteoporosis (Table 3). The mean age among patients with normal BMD, osteopenia and osteoporosis was 64, 68 and 73 years respectively (p = 0.097). All patients with a low BMD had a history or on-going medical treatment for osteoporosis except for two patients with osteopenia.
      Table 3BMD at 10-years follow-up divided into normal, osteopenia and osteoporosis in patients with a femoral neck fracture, n = 42. The results are comparing gender, age, fracture type as well as BMD at the time of fracture.
      BMDNormal (T-score>1)Osteopeni (T-score −1 to −2.49)Osteoporosis (T-score≤2.5)p-value
      Chi-square test.
      All patients% (n)14 (10)74 (27)12 (5)<0.001
      Sex% (n)
      Women

      Men
      9 (2)

      42 (8)
      70 (16)

      58 (11)
      21 (5)

      0 (0)
      0.01
      Mean age6468730.097
      Type of fracture% (n)
      Non-displaced

      Displaced
      12 (2)

      31 (8)
      76 (12)

      58 (15)
      12 (2)

      11 (3)
      0.395
      Time of fracture% (n)
      Missing 4.
      10 (5)50 (21)40 (12)0.006
      1 Chi-square test.
      2 Missing 4.

      Surgical complications, radiographic examination of the hip and hip function

      Twenty-nine percent (n = 17) had a major re-operation (THR) and 34% (n = 20) had a minor re-operation (extraction of the screws) during the 10-year observation period. In patients with a displaced FNF, 34% (n = 13) had a major re-operation compared to 20% (n = 4) in those with a non-displaced FNF. A total of 22% (n = 13) had sustained another fracture during the 10 years after the FNF and 9% (n = 5) suffered a fracture in the contralateral hip.
      The radiographic examination of the previously fractured hip showed a healed fracture in 60% (n = 28), AVN in four patients and osteoarthritis in one patient.
      HHS showed good or excellent function in 85% of the patients (Table 4). The mean value for HHS was 86.0 (SD 18.2) for men and 90.5 (SD 11.5) for women (p = 0.330). For patients who had undergone a major re-operation, 67% showed a good or excellent function compared to 93% who had a minor or no re-operation (p = 0.125).
      Table 4Postoperative hip function according to Harris Hip Score in patients younger than 70 years with a femoral neck fracture at 4, 12 and 24-month and at 10-year follow-up, n = 47. A value between 80 and 100 are considered excellent, 70–80 good and <70 a poor function.
      Harris Hip Score total score4 months
      n=1,.
      12 months24 months
      n = 2.
      10 years
      Mean (SD)81.3 (19.2)85.7 (18.4)88.7 (15.8)88.3 (15.2)
      p-value
      Paired sample T-Test, data compared to 10-year follow-up.
      0.090.130.71
      All fractures% (n)
      Poor function <7022 (10)18 (8)33 (9)15 (7)
      Good function 70–8011 (5)9 (4)11 (3)13 (6)
      Excellent function >8067 (31)73 (32)56 (15)72 (34)
      Non- displaced fractures
      Poor function <705 (1)17 (3)17 (3)10 (2)
      Good function 70–8011 (2)0 (0)6 (1)16 (3)
      Excellent function >8084 (16)83 (15)78 (14)74 (14)
      Displaced fractures
      Poor function <7033 (9)19 (5)11 (3)18 (5)
      Good function 70–8011 (3)16 (4)0 (0)11 (3)
      Excellent function >8056 (15)65 (17)89 (24)71 (20)
      Data missing:.
      a n=1,.
      b n = 2.
      c Paired sample T-Test, data compared to 10-year follow-up.
      The HHS at the 10-year follow-up did not differ from that of the 2-year follow-up (p = 0.711) (Table 4).

      Discussion

      The reported findings indicate that a majority of these younger patients that sustained a FNF ten years earlier had a normal muscle strength and hip function. A third of the patients had undergone a major re-operation. Although a majority of all included patients did not display osteoporosis or sarcopenia, still a significant number had reduced BMD and muscle functionality.
      The results of 5TSTS indicate that close to half of the patients had a reduced lower extremity strength, with potential implications for mobility and general functionality. Previous studies report factors such as age, balance, sensorimotor measures and weight play important roles in the performance of this test [
      • Lord S.R.
      • Murray S.M.
      • Chapman K.
      • Munro B.
      • Tiedemann A.
      Sit-to-stand performance depends on sensation, speed, balance, and psychological status in addition to strength in older people.
      ]. To our knowledge, no previous studies have investigated 5TSTS in younger patients 10 years after a FNF. Whitney et al. [
      • Whitney S.
      • Wrisley D.
      • Marchetti G.
      • Gee M.
      • Redfern M.
      • Furman J.
      Clinical measurement of Sit-to-Stand Performance in people with balance disorders: validity of data for the Five-Times-Sit-to-Stand Test.
      ] concluded that 5TSTS is capable of identifying people with balance disorders especially in those younger than 60 years of age. Somewhat in contrast to the frequent impairment of chair-stand capacity our results show that 85% had a normal 4-m walking test. In line with some previous studies [
      • Montero-Odasso M.
      • Schapira M.
      • Soriano E.R.
      • Varela M.
      • Kaplan R.
      • Camera R.A.
      • et al.
      Gait velocity as a single predictor of adverse events in healthy senior aged 75 years and older.
      ,
      • Cesari M.
      • Kritchevsky S.B.
      • Penninx B.W.
      • Nicklas B.J.
      • Simonsick E.M.
      • Newman A.B.
      • et al.
      Prognostic value of usual gait speed in well-functioning older people-results from the Health, Aging and Body Composition Study.
      ], older age and reliance on walking aids in our patients were linked to slow gait speed, rather than factors related to previous trauma.
      Although the majority of the patients in our study performed well in HGS, up to one third displayed low HGS at the 10-year follow-up. As expected the strength declined with increasing age. More than half of the women displayed low FFMI, which was also the case for patients who had undergone a major re-operation. Still, the mean FFMI was similar 10 years after the hip fracture compared to the values at the time of inclusion, which may indicate that a FNF in this group of patients does not affect the FFMI. According to a European reference population [
      • Kyle U.G.
      • Piccoli A.
      • Pichard C.
      Body composition measurement: interpretation finally made easy for clinical use.
      ] the FFMI were similar with those found in the present study except for men with overweigh (BMI 25–29.9) who had lower values of FFMI in our study. Sarcopenia, defined as a combination of reduced strength and reduced muscle mass/FFMI, was observed in up to one third of the study population. This finding is important, since the occurrence of sarcopenia and reduced chair-stand capacity may have implications for the management of activities of daily living and the risk of falls.
      The BMI in our study did not change significantly between inclusion and follow-up. When comparing BMI at the follow-up with an age and sex matched reference group, our subjects showed a slightly lower BMI [
      • Eiben G.
      • Dey D.K.
      • Rothenberg E.
      • Steen B.
      • Björkelund C.
      • Bengtsson C.
      • et al.
      Obesity in 70 years-old Swedes: secular changes over 30 years.
      ].
      According to HHS the majority had a good or excellent hip function 10 years after the fracture, i.e., similar to the HHS score at the 24-month follow-up in the same cohort [
      • Campenfeldt P.
      • Al-Ani A.
      • Hedström M.
      • Ekström W.
      Low BMD and high alcohol consumption predict a major re-operation in patients younger than 70 years of age with a displaced femoral neck fracture- A two-year follow up study in 120 patients.
      ]. In a 12-month follow-up study of 153 patients with FNF, Frihagen et al. [
      • Frihagen F.
      • Grotle M.
      • Madsen J.E.
      • Wyller T.B.
      • Mowinckel P.
      • Nordsletten L.
      Outcome after femoral neck fractures: a comparison of Haris Hip Score, Eq-5d and Barthel Index.
      ] found a HHS that was significantly lower if re-operated. Their follow-up was much shorter and included older patients which might explain their lower values of HHS after a re-operation.
      BMD at the 10-years follow-up was as expected significantly lower when compared to baseline values. The BMD levels in this 10-year follow-up were similar to those reported in more than 7000 US inhabitants [
      • Looker A.C.
      • Wahner H.W.
      • Dunn W.L.
      • Calvo M.S.
      • Harris T.B.
      • Heyse S.P.
      • et al.
      Proximal femur bone mineral levels of US adults.
      ], where results were documented according to sex, age and ethnicity (non-Hispanic white). The majority of our patients had periods of treatment for osteoporosis, contrary to other studies showing less medical treatments for osteoporosis after a hip fracture [
      • Jennings L.A.
      • Auerbach A.D.
      • Maseli J.
      • Pekow P.S.
      • Lindenauer P.K.
      • Lee S.J.
      Missed opportunities for osteoporosis treatment in patients hospitalized for hip fracture.
      ]. A possible reason for our high level of osteoporosis treatment is that patients with osteopenia or osteoporosis at the time of inclusion in our study were referred to their GP or endocrinologist for further osteoporosis assessment and treatment according to existing guidelines.
      Studies on patients at old age sustaining a displaced FNF have shown a re-operation rate of 35–47% [
      • Lu-Yao G.L.
      • Keller R.B.
      • Littenberg B.
      • Wennberg J.E.
      Outcomes after displaced fractures of the femoral neck. A meta-analysis of one hundred and six published reports.
      ,
      • Holmberg S.
      • Mattsson P.
      • Dahlborn M.
      • Ersmark H.
      Fixation of 220 femoral neck fractures. A prospective comparison of the Rydell nail and the LIH hook pins.
      ], that are somewhat higher than in the present study. The lower re-operation rate in our study may reinforce the surgical guidelines we used for younger patients with FNF, regardless if non-displaced or not, to be treated with CRIF.
      Some of the limitations and strengths of this study should be noticed. To our knowledge, no previous study has investigated functional outcome for the younger group of patients with a FNF. The patients who were available for a follow-up after 10 years may not be representative for the whole study group. Another weakness is that some of the included patients did not participate in all examinations. A strength of the present study is the long-term follow-up after a FNF in younger patients. Moreover, we find the design with combined performance and body composition measurements important, since it allows for assessment of sarcopenia, which is an emerging condition with great relevance for patients with hip fractures.

      Conclusion

      The majority of patients less than 70 years of age with a FNF treated with CRIF had a normal muscle strength and self-assessed function 10 years after the fracture. However, one in ten had osteoporosis, close to half were limited in their chair rising capacity, and up to one third were sarcopenic. The last findings indicate a challenge for the health care system to encourage younger hip fracture patients to do regular muscle preserving resistance training, especially those patients that had undergone a major re-operation and women. Further studies are needed to assure whether such training may have any beneficial effect.

      Declaration of Competing Interest

      The authors of this article certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

      Acknowledgments

      Special thanks to RIKSHÖFT and Stockholm Hip Fracture Group for running the study during the course of years. A special thanks to Jan Tidermark who initiated the study.

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