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Undertreatment of osteoporosis following hip fracture in the elderly
Archives of Gerontology and Geriatrics 49 (2009) 153–157
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Undertreatment of osteoporosis following hip fracture in the elderly Peter Lu¨thje a,*, Ilona Nurmi-Lu¨thje b,c, Juha-Pekka Kaukonen d, Salla Kuurne a, Helena Naboulsi d, Matti Kataja e a
Kuusankoski Regional Hospital, Sairaalankuja 2, FI-45750 Kuusankoski, Finland Department of Public Health, University of Helsinki, Mannerheimintie 172, P.O. Box 41, FI-00014 Helsinki University, Finland c Health Centre of Kouvola Region, P.O. Box 84, FI-45101 Kouvola, Finland d Pa¨ija¨t-Ha¨me Central Hospital, Keskussairaalankatu 7, FI-15850 Lahti, Finland e National Public Health Institute, Mannerheimintie 166, FI-00300 Helsinki, Finland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 February 2008 Received in revised form 12 June 2008 Accepted 17 June 2008 Available online 15 August 2008
The national Finnish guidelines for medical treatment of hip fracture patients are: osteoporosis medication and the daily concomitant use of vitamin D and calcium supplements. We investigated the post-fracture medical therapy for osteoporosis and the calcium and vitamin D therapy among hip fracture patients in two Finnish hospitals. The pre-fracture osteoporosis medication and use of calcium and vitamin D supplements of the patients were inquired on admission. The patient-specific use of osteoporosis medication and of prescribed calcium and vitamin D therapy during the follow-up time were checked from The Finnish Social Insurance Institution. At the end of the follow-up, those who were alive were inquired about the use of medication at the time. Eight percent of the 223 patients used osteoporosis medication and 8% used prescribed calcium and vitamin D supplements before the fracture. During the follow-up, the figures were 39% (52/133) and 53% (70/133), respectively, and at the end of the follow-up, correspondingly, 25% (29/114) and 44% (50/114). The follow-up time was 19.5–35 months. The post-fracture medical therapy for osteoporosis was insufficient. More effort should be focused on the secondary prevention following hip fracture in order to ensure the recommended treatment of osteoporosis. ß 2008 Elsevier Ireland Ltd. All rights reserved.
Keywords: Hip fracture Osteoporosis Anti-osteoporotic treatment Adherence for prescribed osteoporosis treatment
1. Introduction Hip fracture is the most severe and economically most important complication of osteoporosis in aged people. More than 4% of these patients die during hospitalization (AAOS, 1999) and one-third die within 1 year (Nurmi et al., 2004). Many hip fracture patients lose the ability to live independently, and approximately 10% of those who are alive after the first post-fracture year are permanently bedridden (Nurmi et al., 2004). In addition to the operative treatment of the fracture, the patients need anti-osteoporotic treatment to prevent further fractures. However, according to literature, secondary prevention of osteoporosis, especially following hip fracture is not very successful (Kamel et al., 2000; Gardner et al., 2002; Juby and Degeus-Wenceslau, 2002; Cadarette et al., 2008). The subjects of the studies as regards the efficacy of osteoporosis medication have been 70 years old, on average, and among this age group the anti-osteoporotic medication with anti-resorptive or other bone specific drugs have proved to be
* Corresponding author. Tel.: +358 400 753 464; fax: +358 5 220 2255. E-mail address: [email protected].fi (P. Lu¨thje). 0167-4943/$ – see front matter ß 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.archger.2008.06.007
efficient, in order to prevent osteoporotic fractures (Black et al., 2001; NIH, 2001; Poole and Compston, 2006). This is the case among the 80-year-olds as well (Boonen et al., 2004). In addition to the anti-osteoporotic therapy, sufficient amount of vitamin D and calcium supplement is necessary. The purpose of this study was to investigate the post-fracture pharmacological treatment of osteoporosis, that is, anti-osteoporotic drugs and vitamin D and calcium supplements, among hip fracture patients. 2. Materials and methods We registered prospectively all consecutive patients with a fresh hip fracture at the Pa¨ija¨t-Ha¨me Central Hospital (Hospital A), and at the Regional Hospital Kuusankoski (Hospital B), in Southeastern Finland (618N). Hospital A is responsible for an area of 203,000 inhabitants and Hospital B, correspondingly, for an area of 100,000 inhabitants. In order to ensure that at least 100 patients per hospital to enrol in the study, the study period in Hospital A was from February 1, 2003, to January 31, 2004 (12 months), and in Hospital B from February 1, 2003, to April 30, 2004 (15 months). The primary data from the time of the fracture have been analyzed and published previously (Nurmi et al., 2005). For this paper, the patients who were still alive were identified in the patient record system to whom a questionnaire was sent in November–December, 2005 at an average 28 months after the fracture. In the questionnaire, the following information was inquired: present place of residence
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P. Lu¨thje et al. / Archives of Gerontology and Geriatrics 49 (2009) 153–157 Table 1 The background parameters (Nurmi et al., 2005), n (%), except the age given as mean S.D.
Fig. 1. The use of anti-osteoporotic medication and of prescribed vitamin D plus calcium supplements (*bedridden patients are not included). (actual home; residential home; institution), locomotor ability, has the patient sustained new fractures after the hip fracture (if yes, which fractures; if the answer remained unclear, the patient records were checked), has the patient undergone a BMD testing (spine and/or hip), and what is the regular medication of the patient. More specifically, the use of anti-osteoporotic medication, prescribed vitamin D plus calcium supplements, non-prescribed vitamin D and calcium preparations and multivitamin preparations were inquired. The study nurses interviewed patients, who did not respond to the questionnaire, by phone (SK, HN). Additionally, the anti-osteoporotic medication and prescribed calcium and vitamin D supplements of the patients during the period from February 1, 2003, to December 31, 2005, were checked from the Finnish Social Insurance Institution. The length of prescription was determined from the last date the medication was redeemed in the pharmacy. In Finland, the pharmacies are allowed to sell prescribed drugs for a 3-month period only. The drugs were classified according to the Anatomical Therapeutic Chemical classification system (ATC codes) (Classification of Drugs, 2006). During the study period following anti-osteoporotic drugs were available in Finland: hormones, bisphosphonates, calcitonin, selective estrogen receptor modulators (SERMs), and teriparatide. In analyzing the use of vitamin D, calcium and anti-osteoporotic drugs, patients who were bedridden were not taken into account (National Guidelines, 2006a,b). Further, if the patient had undergone a BMD testing, the results were checked. The study protocol was approved by the ethic committees of the Pa¨ija¨t-Ha¨me Central Hospital and Kymenlaakso Health Care Districts.
Variables (n of subjects)
Hospital A
Hospital B
Total
Females Males Total
89 (74) 31 (26) 120 (100)
69 (67) 34 (33) 103 (100)
158 (71) 65 (29) 223 (100)
Age (years) Females (range 47–96) Males (range 38–91)
81.2 10 74.4 10
79.6 11 71.5 13
Place of residence (n = 223) Actual home Residential home Institution
85 (71) 14 (12) 21 (17)
61 (60) 22 (21) 20 (19)
146 (66) 36 (16) 41 (18)
Previous fractures (n = 222) No One fracture Several fractures
81 (68) 35 (29) 4 (3)
66 (65) 24 (24) 12 (12)
147 (66) 59 (27) 16 (7)
Type of hip fracture (n = 222) Cervical Trochanteric Subtrochanteric
68 (57) 44 (37) 7 (6)
44 (43) 47 (46) 12 (12)
112 (50) 91 (41) 19 (9)
Daily pre-fracture use of non-prescribed calcium (n = 223) Yes 23 (19) 21 (20) No 93 (78) 80 (78) Unknown 4 (3) 2 (2)
44 (20) 169 (77) 6 (3)
Daily pre-fracture use of non-prescribed vitamin D (n = 223) Yes 23 (19) 11 (10) No 91 (71) 86 (84) Unknown 4 (5) 6 (6)
34 (15) 177 (78) 12 (5)
80.5 10 72.9 12
Daily pre-fracture use of prescribed calcium and vitamin D (n = 223) 11 (9) 7 (7)
18 (8)
Pre-fracture use of osteoporosis drug (n = 223) 10 (8)
17 (8)
S-25(OH)D (nmol/l) (n = 223) <20 20–37.4 37.5–74 >74
15 47 56 2
(13) (39) (47) (2)
7 (7)
6 50 42 5
(6) (49) (41) (5)
21 97 98 7
(9) (44) (44) (3)
Note: All comparisons between Hospitals A and B were insignificant. 2.1. Statistical analysis Differences between two groups were tested with the x2-test and the Wilcoxon rank test, and in case of more than two groups with the Kruskall–Wallis test. The Fisher’s exact test was used when appropriate. Differences in the mean values between two groups were tested with the t-test, and in case of more than two groups the two-way analysis of variance was used.
3. Results
had died. The questionnaire was sent to the 137 patients (93 women and 44 men) who were still alive. The mean age of the surviving women was 79 10 (S.D.) years and of men 72 12 years. Two-thirds (68%) of the patients answered the questionnaire by mail, 28% by phone and 4% (6/137) did not respond. Thus, the final response rate was 96% (131/137).
3.1. Background
3.3. Place of residence and locomotor ability
A total of 223 patients with an acute hip fracture were primarily enrolled in the study in two hospitals. No significant differences were in the baseline between the hospitals (Table 1). Two patients sustained a second hip fracture on the opposite hip during the primary study period. Prior to the hip fracture, 8% used prescribed calcium (500 mg) plus vitamin D (400 IU) supplements (once or twice/day) and 8% (15 women and 3 men) used anti-osteoporotic therapy (bisphosphonates, calcitonin, or oestrogen; Nurmi et al., 2005).
The place of residence of the patients was found out from the questionnaire and patient records in a total of 135 cases. Of those, 62% (83/135) were living in their actual home, 27% (37/135) in a residential home and 11% (15/135) were in institutional care. Thirteen out of 131 patients (10%) who responded the questionnaire, were permanently bedridden.
3.2. The present results After an average of 28 months from the hip fracture (median 27.5 months, range 19.5–35 months) 39% of the patients (86/221)
3.4. New osteoporotic fractures Information about new fractures was available in 129/131 patients. Fourteen of them (11%) had sustained new osteoporotic fractures. Two patients had sustained two new fractures. Three patients (2%) had sustained a second hip fracture to the opposite hip. Of the fourteen patients with new fractures, two used
P. Lu¨thje et al. / Archives of Gerontology and Geriatrics 49 (2009) 153–157
recommended medication (oral bisphosphonates, prescribed vitamin D plus calcium), two used prescribed vitamin D plus calcium during the entire follow-up, and four patients used oral bisphosphonates, prescribed vitamin D plus calcium for some time. 3.5. Bone mineral density (BMD) BMD was measured in 16 out of 221 patients (7%), who were all relatively young: the mean age in women was 64 16 years and in men 63 14 years. The examinations were performed in four different places, all of them using LunarR densitometers. Osteoporosis was found in six women and four men (mean T score 2.8), osteopenia in five women and one man (mean T score 1.8). 3.6. Anti-osteoporotic therapy, vitamin D and calcium (Fig. 1) The medication remained unknown in four out of 137 patients. Of the remaining 133 patients, 39% (52/133) used anti-osteoporotic therapy during the follow-up. Women used anti-osteoporotic medication more than men (43/92; 47% vs. 9/41; 22%) (x2 = 7.32, d.f. = 1, p < 0.01). The median duration of the anti-osteoporotic therapy was 25 months. Furthermore, 53% (70/133) of the patients used prescribed vitamin D plus calcium supplements (vitamin D 400 IU calcium 500 mg) either once or twice a day (women 53/92; 58% and men 17/41; 41%, n.s.). The median duration of the use of vitamin D plus calcium supplements was 22 months. At the end of the follow-up, 13 patients were permanently bedridden and their medication was not considered. In addition, four patients did not answer the question on daily medication. Thus, at the end of the follow-up our material included 114 out of 131 patients as regards the use of medication. One-fourth (25%) (29/114) used anti-osteoporotic treatment (oral bisphosphonates and intranasal calcitonin); 31% (24/78) of women and 14% (5/36) of men. Six patients used only intranasal calcitonin and four patients used oral bisphosphonates plus intranasal calcitonin. Further, 44% (50/114) (women 38/78; 49% and men 12/36; 33%) used prescribed vitamin D and calcium, 38% (43/114) of patients told that they did not use any non-prescribed calcium or vitamin D drugs. However, 6% (7/114) told they used both non-prescribed supplements, 5% (6/ 114) used calcium only and 7% (8/114) used vitamin D only. The daily doses of non-prescribed vitamin D were approximately 300 IU and of calcium, correspondingly, 520 mg. 4. Discussion The results of this study indicate that 39% of patients who had sustained a hip fracture used post-fracture anti-osteoporotic medication (oral bisphosphonates and intranasal calcitonin) and 53% used prescribed vitamin D plus calcium supplements. The median duration of use of these drugs were 25 and 22 months, respectively. At the end of the follow-up (median 27.5 months), the corresponding figures were 24% and 44%. Our results are in concordance with previous studies. According to the literature, an undertreatment of osteoporosis in patients with hip fractures is common (Kamet et al., 2000; Gardner et al., 2002; Juby and Degeus-Wenceslau, 2002; Panneman et al., 2004; Kamel, 2005; Khandwala et al., 2005; Petrella and Jones, 2006; Cadarette et al., 2008). A hip fracture is associated with a 2.5-fold increased risk of subsequent fracture. Such fractures occur at a rate of 10.4 per 100 patients per year, which is 2.5 times as high as the rate in aged-matched persons without previous hip fracture (Colo´n-Emeric et al., 2003). The use of anti-osteoporosis medication, however, is very important in preventing bone loss. The post-operative period following a hip fracture is the most critical. Minimal exercise due to
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the fracture further increases the loss of BMD, especially in the contralateral proximal femur: Two percent during the first 2 months and from 4% to 7% during the first post-fracture year (Karlsson et al., 1996; Dirschl et al., 1997; Fox et al., 2000). Hence, the post-fracture anti-osteoporotic medication should be started as soon as possible (Van Helden et al., 2006) in order to prevent the decrease of the BMD. A new alternative for hip fracture patients is the annual use of intravenous zoledronic acid, which has shown a significant reduction in the rate of new clinical fractures (Lyles et al., 2007). Our results show that the national Finnish guidelines for treatment of osteoporosis are not sufficiently followed (National Guidelines, 2006b). Both the Finnish guidelines for hip fracture treatment and the Finnish guidelines for treatment of osteoporosis clearly indicate that if the patient is not permanently bedridden, anti-osteoporotic medication and daily use of vitamin D plus calcium supplements are to be started (National Guidelines, 2006a,b). In the present study, 11% (14/129) of the patients sustained new fractures. Two of these patients used recommended anti-osteoporotic medication, four patients used recommended antiosteoporotic medication for some time, and two patients used only prescribed calcium plus vitamin D. In spite of adequate medication there is still a risk for further fractures. According to a Dutch study, the cumulative incidence of patients with new clinical fractures over 2 years was 11% (Van Helden et al., 2006). The incidence of further fractures was increased with the patient’s age. The new fracture incidence in women was 12.2% as compared to 7.4% in men (Van Helden et al., 2006). Furthermore, a study from Sweden indicate that the risk of a subsequent fracture after an osteoporotic fracture is the highest immediately after the event (Johnell et al., 2004). In our study, a few patients used oral bisphosphonate and intranasal calcitonin (200 IU/day) simultaneously, whereas some of the patients used only intranasal calcitonin (200 IU/day). The reason for using calcitonin was the gastrointestinal side-effect of oral bisphosphonate. The reason for using both drugs simultaneously was probably the effect of intranasal calcitonin in reducing the bone pain (Woo and Adachi, 2001; Knopp et al., 2005). The current analgesic dose of the intranasal route is 200 IU/day (Lussier et al., 2004). It is similar to that used in anti-osteoporotic therapy in Finland. However, it has been shown that intranasal calcitonin has no effect on chronic pain (Papadokostakis et al., 2006). In addition, prior to the hip fracture, every third patient (75/ 221) in this material had already sustained a fracture, most of them being fractures of the wrist (27%), ankle (12%) or hip (11%) (Nurmi et al., 2005). According to previous studies, 6–15% of hip fracture patients sustain a second hip fracture on the opposite hip (Dretakis et al., 1998; Dinah, 2002; Rodaro et al., 2004; Yamanashi et al., 2005; Fukushima et al., 2006; Berry et al., 2007; Lo¨nnroos et al., 2007). In a recent Japanese retrospective study, 11% of the hip fracture patients (n = 835) sustained a second hip fracture at an average 4.3 years from the first hip fracture (Fukushima et al., 2006). In the Framingham study, 15% of the subjects experienced a second hip fracture during a median of 4.2 years of follow-up (Berry et al., 2007). In our data, 2% of the patients who were still alive sustained a second fracture. The follow-up time, however, was quite short in this respect (median 27.5 months). Together with the anti-osteoporotic therapy, receiving sufficient doses of vitamin D plus calcium supplements should be ensured. In the beginning of this study series, the serum 25(OH) Dconcentration of the patients was analyzed (Nurmi et al., 2005) (Table 1). About half of the patients suffered from hypovitaminosis D, S-25(OH) D being on admission less than 37.5 nmol/l. In 9% of the patients, the vitamin D deficiency was severe (S-25(OH) D less
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than 20 nmol/l) and only 2% had S-25(OH) D concentration over 76 nmo/l, which is sufficient for maximum bone health according to bone researchers (Chapuy et al., 1997; Holick, 2004). At the end of the study, 38% of the patients told that they did not use prescribed vitamin D plus calcium supplements. The daily doses of those patients who used non-prescribed supplements were insufficient. What should be done to ensure the optimal treatment for osteoporosis in patients with an acute hip fracture? Most aged patients who sustain low-trauma fractures do not receive evaluation and remain at an increased risk for further fractures. These patients need a routine assessment, and, when necessary, treatment for osteoporosis after their fracture (McLellan et al., 2003). Secondary prevention of osteoporotic fractures should be part of the primary treatment. Osteoporosis specialist nurses play an important role in identifying the patients who should be assessed. Co-operation in multidisciplinary teams (staffs of the emergency room, of the orthopedic ward, and of the rehabilitation unit, and the primary care physicians) is important as well, in order to succeed in secondary prevention. It is important, as well to decrease the risk of falling (Ja¨rvinen et al., 2008). Previous studies have shown that among older people who fall osteoporosis is not the strongest risk factor for fracture (Kannus et al., 2002, 2005; Robinovitch et al., 2003). Evidence from systematic reviews and meta-analyses of RCTs have shown that at least 15% of falls in aged people can be prevented, with individual trials reporting reductions of even 50% (Kannus et al., 2005; Oliver et al., 2007). A recent Dutch cohort study (n = 568) of patients over 50 years of age, who had been admitted due to an acute clinical fracture, showed that osteoporosis was present in one-third of the patients, and half of the patients had at least one fall-related risk factor before the current fracture (Van Helden et al., 2008). The mean age was 67 years, and the material included 15% patients with a hip fracture (Van Helden et al., 2008). For the present, however, there is no RCT-study on preventing falling with the primary end point a new fracture. Our study had some limitations. The mortality was high (39%), and we could not find out the use of anti-osteoporotic medication or prescribed use of vitamin D plus calcium supplements of those who were not alive. The mortality of hip fracture patients is mostly studied at 1 year after the injury. According to previous Finnish studies the mortality rate at 1 year ranged from 26% to 33% (Heikkinen et al., 2004; Nurmi et al., 2004). Thus, our 39% mortality rate at on average 28 months after the fracture was not high after all. Of the patients who died during the follow-up, a notable number were institutionalized for shorter or longer periods after the operation. The Social Insurance Institution has no data of the medication of those in institutional care. Improving the adherence for prescribed osteoporosis treatment is crucial. According to previous studies adherence to oral antiosteoporotic treatment is low: after 6 months 20% of the patients have discontinued the medication, after 1 year the figure is 50% and after 2 years over 75% (Papaioannou et al., 2003; Cramer et al., 2004; Reginster and Rabenda, 2006). In a recent Cochrane review following interventions for enhancing medication adherence were considered effective: more thorough patient instruction and counselling, reminders, close follow-up, supervised self-monitoring, rewards for success, and manual telephone follow-up (Haynes et al., 2006). However, these interventions are more cost-effective in short-term treatments (Haynes et al., 2006). According to Finnish experience, the professional expertise of osteoporosis specialist nurses could be a solution. In addition, telephone followups carried out by nurses could improve the adherence for oral anti-osteoporotic treatment. One further alternative could be the use of intravenous administration of zoledronic acid once a year,
which ensures that patients will have a full treatment effect for at least 12 months (Black et al., 2007). Treatment of osteoporosis at the time of a fracture is a highly cost-effective intervention (Johnell et al., 2003; Kanis et al., 2004, 2008; Schousboe et al., 2005a,b). 5. Conclusions Summing up, the proportion of hip fracture patients treated with prescribed calcium and vitamin D supplements and antiosteoporotic drugs is low. This places them at increased risk of other osteoporotic fractures. Health care professionals need to be actively educated about the guidelines by the International Osteoporosis Foundation (IOF) (Kanis et al., 1997) and the national guidelines. Conflict of interest statement None. Acknowledgments This study was supported by grants from the EVO foundations of Kymenlaakso and Pa¨ija¨t-Ha¨me health care districts and the Kymi Ltd. 100-years Foundation. References AAOS (American Academy of Orthopedic Surgeon), 1999. Position Statement. Hip Fracture in Seniors: A Call for Health System Reform. American Academy of Orthopedic Surgeons, Rosemont. Berry, S.D., Samelson, E.J., Hannan, M.T., McLellan, R.R., Lu, M., Cupples, L.A., Shaffer, M.L., Beiser, A.L., Kelly-Hayes, M., Kiel, D.P., 2007. Second hip fracture in older men and women. Arch. Int. Med. 167, 1971–1976. Black, D.M., Steinbuch, M., Palermo, L., Dargent-Molina, P., Lindsay, R., Hoseyni, M.S., Johnell, O., 2001. An assessment tool for predicting fracture risk in postmenopausal women. Osteoporosis Int. 12, 519–528. Black, D.M., Delmas, P.D., Eastell, R., Reid, I.R., Boonen, S., Cauley, J.A., Cosman, F., Lakatos, P., Leung, P.C., Man, Z., Mautalen, C., Mesenbrink, P., Hu, H., Caminis, J., Tong, K., Rosario-Jansen, T., Krasnow, J., Hue, T.F., Sellmeyer, D., Eriksen, E.F., Cummings, S.R., 2007. Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N. Engl. J. Med. 356, 1809–1822. Boonen, S., McClung, M.R., Eastell, R., El-Hajj Fuleihan, G., Barton, I.P., Delmas, P., 2004. Safety and efficacy of risedronate in reducing fracture risk in osteoporotic women aged 80 and older: implications for the use of antiresorptive agents in the old and oldest old. J. Am. Geriatr. Soc. 52, 1832–1839. Cadarette, S.M., Katz, J.N., Brookhart, M.A., Levin, R., Stedman, M.R., Choudhry, N.K., Solomon, D.H., 2008. Trends in drug prescribing for osteoporosis after hip fracture, 1995–2004. J. Rheumatol. 35, 319–326. Chapuy, M.C., Preziosi, P., Maamer, M., Arnaud, S., Galan, P., Hercberg, S., Meunier, P.J., 1997. Prevalence of vitamin D insufficiency in adult normal population. Osteoporosis Int. 7, 439–443. Classification of Drugs, 2006. La¨a¨kkeiden luokitus (ATC) ja ma¨a¨ritellyt vuorokausiannokset (DDD). La¨a¨kelaitos, Edita Prima Oy (in Finnish). Colo´n-Emeric, C., Kuchibhatla, M., Pieper, C., Hawkes, W., Fredman, L., Magaziner, J., Zimmerman, S., Lyles, K.W., 2003. The contribution of hip fracture to risk of subsequent fracture: data from two longitudinal studies. Osteoporosis Int. 14, 879–883. Cramer, J., Amonkar, M.M., Hebborn, A., Suppapanya, N., 2004. Does dosing regimen impact persistence with bisphosphonate therapy among postmeno-pausal osteoporotic women? J. Bone Miner. Res. 19 (Suppl. 1), S448. Dinah, A.F., 2002. Sequential hip fractures in elderly patients. Injury 33, 393–394. Dirschl, D.R., Henderson, R.C., Oakley, W.C., 1997. Accelerated bone mineral loss following a hip fracture: a prospective longitudinal study. Bone 21, 79–82. Dretakis, K.E., Dretakis, E.K., Papakitsou, E.F., Psarakis, S., Steriopoulus, K., 1998. Possible predisposing factors for the second hip fracture. Calcif. Tissue Int. 62, 366–369. Fox, K.M., Magaziner, J., Hawkes, W.G., Yo-Yahiro, J., Zimmerman, S.I., Holder, L., Michael, R., 2000. Loss of bone density and lean body mass after hip fracture. Osteoporosis Int. 11, 31–35. Fukushima, T., Sudo, A., Uchida, A., 2006. Bilateral hip fractures. J. Orthop. Sci. 11, 435–438. Gardner, M.J., Flik, K.R., Moor, P., Lane, J.M., 2002. Improvement in the undertreatment of osteoporosis following hip fracture. J. Bone Joint Surg. Am. 84, 1342–1348. Haynes, R.B., Yao, X., Degani, A., Kripalani, S., Garg, A., McDonald, H.P., 2006. Interventions for enhancing medication adherence (review). Cochrane Libr. 4.
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Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Undertreatment of osteoporosis following hip fracture in the elderly Peter Lu¨thje a,*, Ilona Nurmi-Lu¨thje b,c, Juha-Pekka Kaukonen d, Salla Kuurne a, Helena Naboulsi d, Matti Kataja e a
Kuusankoski Regional Hospital, Sairaalankuja 2, FI-45750 Kuusankoski, Finland Department of Public Health, University of Helsinki, Mannerheimintie 172, P.O. Box 41, FI-00014 Helsinki University, Finland c Health Centre of Kouvola Region, P.O. Box 84, FI-45101 Kouvola, Finland d Pa¨ija¨t-Ha¨me Central Hospital, Keskussairaalankatu 7, FI-15850 Lahti, Finland e National Public Health Institute, Mannerheimintie 166, FI-00300 Helsinki, Finland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 February 2008 Received in revised form 12 June 2008 Accepted 17 June 2008 Available online 15 August 2008
The national Finnish guidelines for medical treatment of hip fracture patients are: osteoporosis medication and the daily concomitant use of vitamin D and calcium supplements. We investigated the post-fracture medical therapy for osteoporosis and the calcium and vitamin D therapy among hip fracture patients in two Finnish hospitals. The pre-fracture osteoporosis medication and use of calcium and vitamin D supplements of the patients were inquired on admission. The patient-specific use of osteoporosis medication and of prescribed calcium and vitamin D therapy during the follow-up time were checked from The Finnish Social Insurance Institution. At the end of the follow-up, those who were alive were inquired about the use of medication at the time. Eight percent of the 223 patients used osteoporosis medication and 8% used prescribed calcium and vitamin D supplements before the fracture. During the follow-up, the figures were 39% (52/133) and 53% (70/133), respectively, and at the end of the follow-up, correspondingly, 25% (29/114) and 44% (50/114). The follow-up time was 19.5–35 months. The post-fracture medical therapy for osteoporosis was insufficient. More effort should be focused on the secondary prevention following hip fracture in order to ensure the recommended treatment of osteoporosis. ß 2008 Elsevier Ireland Ltd. All rights reserved.
Keywords: Hip fracture Osteoporosis Anti-osteoporotic treatment Adherence for prescribed osteoporosis treatment
1. Introduction Hip fracture is the most severe and economically most important complication of osteoporosis in aged people. More than 4% of these patients die during hospitalization (AAOS, 1999) and one-third die within 1 year (Nurmi et al., 2004). Many hip fracture patients lose the ability to live independently, and approximately 10% of those who are alive after the first post-fracture year are permanently bedridden (Nurmi et al., 2004). In addition to the operative treatment of the fracture, the patients need anti-osteoporotic treatment to prevent further fractures. However, according to literature, secondary prevention of osteoporosis, especially following hip fracture is not very successful (Kamel et al., 2000; Gardner et al., 2002; Juby and Degeus-Wenceslau, 2002; Cadarette et al., 2008). The subjects of the studies as regards the efficacy of osteoporosis medication have been 70 years old, on average, and among this age group the anti-osteoporotic medication with anti-resorptive or other bone specific drugs have proved to be
* Corresponding author. Tel.: +358 400 753 464; fax: +358 5 220 2255. E-mail address: [email protected].fi (P. Lu¨thje). 0167-4943/$ – see front matter ß 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.archger.2008.06.007
efficient, in order to prevent osteoporotic fractures (Black et al., 2001; NIH, 2001; Poole and Compston, 2006). This is the case among the 80-year-olds as well (Boonen et al., 2004). In addition to the anti-osteoporotic therapy, sufficient amount of vitamin D and calcium supplement is necessary. The purpose of this study was to investigate the post-fracture pharmacological treatment of osteoporosis, that is, anti-osteoporotic drugs and vitamin D and calcium supplements, among hip fracture patients. 2. Materials and methods We registered prospectively all consecutive patients with a fresh hip fracture at the Pa¨ija¨t-Ha¨me Central Hospital (Hospital A), and at the Regional Hospital Kuusankoski (Hospital B), in Southeastern Finland (618N). Hospital A is responsible for an area of 203,000 inhabitants and Hospital B, correspondingly, for an area of 100,000 inhabitants. In order to ensure that at least 100 patients per hospital to enrol in the study, the study period in Hospital A was from February 1, 2003, to January 31, 2004 (12 months), and in Hospital B from February 1, 2003, to April 30, 2004 (15 months). The primary data from the time of the fracture have been analyzed and published previously (Nurmi et al., 2005). For this paper, the patients who were still alive were identified in the patient record system to whom a questionnaire was sent in November–December, 2005 at an average 28 months after the fracture. In the questionnaire, the following information was inquired: present place of residence
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P. Lu¨thje et al. / Archives of Gerontology and Geriatrics 49 (2009) 153–157 Table 1 The background parameters (Nurmi et al., 2005), n (%), except the age given as mean S.D.
Fig. 1. The use of anti-osteoporotic medication and of prescribed vitamin D plus calcium supplements (*bedridden patients are not included). (actual home; residential home; institution), locomotor ability, has the patient sustained new fractures after the hip fracture (if yes, which fractures; if the answer remained unclear, the patient records were checked), has the patient undergone a BMD testing (spine and/or hip), and what is the regular medication of the patient. More specifically, the use of anti-osteoporotic medication, prescribed vitamin D plus calcium supplements, non-prescribed vitamin D and calcium preparations and multivitamin preparations were inquired. The study nurses interviewed patients, who did not respond to the questionnaire, by phone (SK, HN). Additionally, the anti-osteoporotic medication and prescribed calcium and vitamin D supplements of the patients during the period from February 1, 2003, to December 31, 2005, were checked from the Finnish Social Insurance Institution. The length of prescription was determined from the last date the medication was redeemed in the pharmacy. In Finland, the pharmacies are allowed to sell prescribed drugs for a 3-month period only. The drugs were classified according to the Anatomical Therapeutic Chemical classification system (ATC codes) (Classification of Drugs, 2006). During the study period following anti-osteoporotic drugs were available in Finland: hormones, bisphosphonates, calcitonin, selective estrogen receptor modulators (SERMs), and teriparatide. In analyzing the use of vitamin D, calcium and anti-osteoporotic drugs, patients who were bedridden were not taken into account (National Guidelines, 2006a,b). Further, if the patient had undergone a BMD testing, the results were checked. The study protocol was approved by the ethic committees of the Pa¨ija¨t-Ha¨me Central Hospital and Kymenlaakso Health Care Districts.
Variables (n of subjects)
Hospital A
Hospital B
Total
Females Males Total
89 (74) 31 (26) 120 (100)
69 (67) 34 (33) 103 (100)
158 (71) 65 (29) 223 (100)
Age (years) Females (range 47–96) Males (range 38–91)
81.2 10 74.4 10
79.6 11 71.5 13
Place of residence (n = 223) Actual home Residential home Institution
85 (71) 14 (12) 21 (17)
61 (60) 22 (21) 20 (19)
146 (66) 36 (16) 41 (18)
Previous fractures (n = 222) No One fracture Several fractures
81 (68) 35 (29) 4 (3)
66 (65) 24 (24) 12 (12)
147 (66) 59 (27) 16 (7)
Type of hip fracture (n = 222) Cervical Trochanteric Subtrochanteric
68 (57) 44 (37) 7 (6)
44 (43) 47 (46) 12 (12)
112 (50) 91 (41) 19 (9)
Daily pre-fracture use of non-prescribed calcium (n = 223) Yes 23 (19) 21 (20) No 93 (78) 80 (78) Unknown 4 (3) 2 (2)
44 (20) 169 (77) 6 (3)
Daily pre-fracture use of non-prescribed vitamin D (n = 223) Yes 23 (19) 11 (10) No 91 (71) 86 (84) Unknown 4 (5) 6 (6)
34 (15) 177 (78) 12 (5)
80.5 10 72.9 12
Daily pre-fracture use of prescribed calcium and vitamin D (n = 223) 11 (9) 7 (7)
18 (8)
Pre-fracture use of osteoporosis drug (n = 223) 10 (8)
17 (8)
S-25(OH)D (nmol/l) (n = 223) <20 20–37.4 37.5–74 >74
15 47 56 2
(13) (39) (47) (2)
7 (7)
6 50 42 5
(6) (49) (41) (5)
21 97 98 7
(9) (44) (44) (3)
Note: All comparisons between Hospitals A and B were insignificant. 2.1. Statistical analysis Differences between two groups were tested with the x2-test and the Wilcoxon rank test, and in case of more than two groups with the Kruskall–Wallis test. The Fisher’s exact test was used when appropriate. Differences in the mean values between two groups were tested with the t-test, and in case of more than two groups the two-way analysis of variance was used.
3. Results
had died. The questionnaire was sent to the 137 patients (93 women and 44 men) who were still alive. The mean age of the surviving women was 79 10 (S.D.) years and of men 72 12 years. Two-thirds (68%) of the patients answered the questionnaire by mail, 28% by phone and 4% (6/137) did not respond. Thus, the final response rate was 96% (131/137).
3.1. Background
3.3. Place of residence and locomotor ability
A total of 223 patients with an acute hip fracture were primarily enrolled in the study in two hospitals. No significant differences were in the baseline between the hospitals (Table 1). Two patients sustained a second hip fracture on the opposite hip during the primary study period. Prior to the hip fracture, 8% used prescribed calcium (500 mg) plus vitamin D (400 IU) supplements (once or twice/day) and 8% (15 women and 3 men) used anti-osteoporotic therapy (bisphosphonates, calcitonin, or oestrogen; Nurmi et al., 2005).
The place of residence of the patients was found out from the questionnaire and patient records in a total of 135 cases. Of those, 62% (83/135) were living in their actual home, 27% (37/135) in a residential home and 11% (15/135) were in institutional care. Thirteen out of 131 patients (10%) who responded the questionnaire, were permanently bedridden.
3.2. The present results After an average of 28 months from the hip fracture (median 27.5 months, range 19.5–35 months) 39% of the patients (86/221)
3.4. New osteoporotic fractures Information about new fractures was available in 129/131 patients. Fourteen of them (11%) had sustained new osteoporotic fractures. Two patients had sustained two new fractures. Three patients (2%) had sustained a second hip fracture to the opposite hip. Of the fourteen patients with new fractures, two used
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recommended medication (oral bisphosphonates, prescribed vitamin D plus calcium), two used prescribed vitamin D plus calcium during the entire follow-up, and four patients used oral bisphosphonates, prescribed vitamin D plus calcium for some time. 3.5. Bone mineral density (BMD) BMD was measured in 16 out of 221 patients (7%), who were all relatively young: the mean age in women was 64 16 years and in men 63 14 years. The examinations were performed in four different places, all of them using LunarR densitometers. Osteoporosis was found in six women and four men (mean T score 2.8), osteopenia in five women and one man (mean T score 1.8). 3.6. Anti-osteoporotic therapy, vitamin D and calcium (Fig. 1) The medication remained unknown in four out of 137 patients. Of the remaining 133 patients, 39% (52/133) used anti-osteoporotic therapy during the follow-up. Women used anti-osteoporotic medication more than men (43/92; 47% vs. 9/41; 22%) (x2 = 7.32, d.f. = 1, p < 0.01). The median duration of the anti-osteoporotic therapy was 25 months. Furthermore, 53% (70/133) of the patients used prescribed vitamin D plus calcium supplements (vitamin D 400 IU calcium 500 mg) either once or twice a day (women 53/92; 58% and men 17/41; 41%, n.s.). The median duration of the use of vitamin D plus calcium supplements was 22 months. At the end of the follow-up, 13 patients were permanently bedridden and their medication was not considered. In addition, four patients did not answer the question on daily medication. Thus, at the end of the follow-up our material included 114 out of 131 patients as regards the use of medication. One-fourth (25%) (29/114) used anti-osteoporotic treatment (oral bisphosphonates and intranasal calcitonin); 31% (24/78) of women and 14% (5/36) of men. Six patients used only intranasal calcitonin and four patients used oral bisphosphonates plus intranasal calcitonin. Further, 44% (50/114) (women 38/78; 49% and men 12/36; 33%) used prescribed vitamin D and calcium, 38% (43/114) of patients told that they did not use any non-prescribed calcium or vitamin D drugs. However, 6% (7/114) told they used both non-prescribed supplements, 5% (6/ 114) used calcium only and 7% (8/114) used vitamin D only. The daily doses of non-prescribed vitamin D were approximately 300 IU and of calcium, correspondingly, 520 mg. 4. Discussion The results of this study indicate that 39% of patients who had sustained a hip fracture used post-fracture anti-osteoporotic medication (oral bisphosphonates and intranasal calcitonin) and 53% used prescribed vitamin D plus calcium supplements. The median duration of use of these drugs were 25 and 22 months, respectively. At the end of the follow-up (median 27.5 months), the corresponding figures were 24% and 44%. Our results are in concordance with previous studies. According to the literature, an undertreatment of osteoporosis in patients with hip fractures is common (Kamet et al., 2000; Gardner et al., 2002; Juby and Degeus-Wenceslau, 2002; Panneman et al., 2004; Kamel, 2005; Khandwala et al., 2005; Petrella and Jones, 2006; Cadarette et al., 2008). A hip fracture is associated with a 2.5-fold increased risk of subsequent fracture. Such fractures occur at a rate of 10.4 per 100 patients per year, which is 2.5 times as high as the rate in aged-matched persons without previous hip fracture (Colo´n-Emeric et al., 2003). The use of anti-osteoporosis medication, however, is very important in preventing bone loss. The post-operative period following a hip fracture is the most critical. Minimal exercise due to
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the fracture further increases the loss of BMD, especially in the contralateral proximal femur: Two percent during the first 2 months and from 4% to 7% during the first post-fracture year (Karlsson et al., 1996; Dirschl et al., 1997; Fox et al., 2000). Hence, the post-fracture anti-osteoporotic medication should be started as soon as possible (Van Helden et al., 2006) in order to prevent the decrease of the BMD. A new alternative for hip fracture patients is the annual use of intravenous zoledronic acid, which has shown a significant reduction in the rate of new clinical fractures (Lyles et al., 2007). Our results show that the national Finnish guidelines for treatment of osteoporosis are not sufficiently followed (National Guidelines, 2006b). Both the Finnish guidelines for hip fracture treatment and the Finnish guidelines for treatment of osteoporosis clearly indicate that if the patient is not permanently bedridden, anti-osteoporotic medication and daily use of vitamin D plus calcium supplements are to be started (National Guidelines, 2006a,b). In the present study, 11% (14/129) of the patients sustained new fractures. Two of these patients used recommended anti-osteoporotic medication, four patients used recommended antiosteoporotic medication for some time, and two patients used only prescribed calcium plus vitamin D. In spite of adequate medication there is still a risk for further fractures. According to a Dutch study, the cumulative incidence of patients with new clinical fractures over 2 years was 11% (Van Helden et al., 2006). The incidence of further fractures was increased with the patient’s age. The new fracture incidence in women was 12.2% as compared to 7.4% in men (Van Helden et al., 2006). Furthermore, a study from Sweden indicate that the risk of a subsequent fracture after an osteoporotic fracture is the highest immediately after the event (Johnell et al., 2004). In our study, a few patients used oral bisphosphonate and intranasal calcitonin (200 IU/day) simultaneously, whereas some of the patients used only intranasal calcitonin (200 IU/day). The reason for using calcitonin was the gastrointestinal side-effect of oral bisphosphonate. The reason for using both drugs simultaneously was probably the effect of intranasal calcitonin in reducing the bone pain (Woo and Adachi, 2001; Knopp et al., 2005). The current analgesic dose of the intranasal route is 200 IU/day (Lussier et al., 2004). It is similar to that used in anti-osteoporotic therapy in Finland. However, it has been shown that intranasal calcitonin has no effect on chronic pain (Papadokostakis et al., 2006). In addition, prior to the hip fracture, every third patient (75/ 221) in this material had already sustained a fracture, most of them being fractures of the wrist (27%), ankle (12%) or hip (11%) (Nurmi et al., 2005). According to previous studies, 6–15% of hip fracture patients sustain a second hip fracture on the opposite hip (Dretakis et al., 1998; Dinah, 2002; Rodaro et al., 2004; Yamanashi et al., 2005; Fukushima et al., 2006; Berry et al., 2007; Lo¨nnroos et al., 2007). In a recent Japanese retrospective study, 11% of the hip fracture patients (n = 835) sustained a second hip fracture at an average 4.3 years from the first hip fracture (Fukushima et al., 2006). In the Framingham study, 15% of the subjects experienced a second hip fracture during a median of 4.2 years of follow-up (Berry et al., 2007). In our data, 2% of the patients who were still alive sustained a second fracture. The follow-up time, however, was quite short in this respect (median 27.5 months). Together with the anti-osteoporotic therapy, receiving sufficient doses of vitamin D plus calcium supplements should be ensured. In the beginning of this study series, the serum 25(OH) Dconcentration of the patients was analyzed (Nurmi et al., 2005) (Table 1). About half of the patients suffered from hypovitaminosis D, S-25(OH) D being on admission less than 37.5 nmol/l. In 9% of the patients, the vitamin D deficiency was severe (S-25(OH) D less
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than 20 nmol/l) and only 2% had S-25(OH) D concentration over 76 nmo/l, which is sufficient for maximum bone health according to bone researchers (Chapuy et al., 1997; Holick, 2004). At the end of the study, 38% of the patients told that they did not use prescribed vitamin D plus calcium supplements. The daily doses of those patients who used non-prescribed supplements were insufficient. What should be done to ensure the optimal treatment for osteoporosis in patients with an acute hip fracture? Most aged patients who sustain low-trauma fractures do not receive evaluation and remain at an increased risk for further fractures. These patients need a routine assessment, and, when necessary, treatment for osteoporosis after their fracture (McLellan et al., 2003). Secondary prevention of osteoporotic fractures should be part of the primary treatment. Osteoporosis specialist nurses play an important role in identifying the patients who should be assessed. Co-operation in multidisciplinary teams (staffs of the emergency room, of the orthopedic ward, and of the rehabilitation unit, and the primary care physicians) is important as well, in order to succeed in secondary prevention. It is important, as well to decrease the risk of falling (Ja¨rvinen et al., 2008). Previous studies have shown that among older people who fall osteoporosis is not the strongest risk factor for fracture (Kannus et al., 2002, 2005; Robinovitch et al., 2003). Evidence from systematic reviews and meta-analyses of RCTs have shown that at least 15% of falls in aged people can be prevented, with individual trials reporting reductions of even 50% (Kannus et al., 2005; Oliver et al., 2007). A recent Dutch cohort study (n = 568) of patients over 50 years of age, who had been admitted due to an acute clinical fracture, showed that osteoporosis was present in one-third of the patients, and half of the patients had at least one fall-related risk factor before the current fracture (Van Helden et al., 2008). The mean age was 67 years, and the material included 15% patients with a hip fracture (Van Helden et al., 2008). For the present, however, there is no RCT-study on preventing falling with the primary end point a new fracture. Our study had some limitations. The mortality was high (39%), and we could not find out the use of anti-osteoporotic medication or prescribed use of vitamin D plus calcium supplements of those who were not alive. The mortality of hip fracture patients is mostly studied at 1 year after the injury. According to previous Finnish studies the mortality rate at 1 year ranged from 26% to 33% (Heikkinen et al., 2004; Nurmi et al., 2004). Thus, our 39% mortality rate at on average 28 months after the fracture was not high after all. Of the patients who died during the follow-up, a notable number were institutionalized for shorter or longer periods after the operation. The Social Insurance Institution has no data of the medication of those in institutional care. Improving the adherence for prescribed osteoporosis treatment is crucial. According to previous studies adherence to oral antiosteoporotic treatment is low: after 6 months 20% of the patients have discontinued the medication, after 1 year the figure is 50% and after 2 years over 75% (Papaioannou et al., 2003; Cramer et al., 2004; Reginster and Rabenda, 2006). In a recent Cochrane review following interventions for enhancing medication adherence were considered effective: more thorough patient instruction and counselling, reminders, close follow-up, supervised self-monitoring, rewards for success, and manual telephone follow-up (Haynes et al., 2006). However, these interventions are more cost-effective in short-term treatments (Haynes et al., 2006). According to Finnish experience, the professional expertise of osteoporosis specialist nurses could be a solution. In addition, telephone followups carried out by nurses could improve the adherence for oral anti-osteoporotic treatment. One further alternative could be the use of intravenous administration of zoledronic acid once a year,
which ensures that patients will have a full treatment effect for at least 12 months (Black et al., 2007). Treatment of osteoporosis at the time of a fracture is a highly cost-effective intervention (Johnell et al., 2003; Kanis et al., 2004, 2008; Schousboe et al., 2005a,b). 5. Conclusions Summing up, the proportion of hip fracture patients treated with prescribed calcium and vitamin D supplements and antiosteoporotic drugs is low. This places them at increased risk of other osteoporotic fractures. Health care professionals need to be actively educated about the guidelines by the International Osteoporosis Foundation (IOF) (Kanis et al., 1997) and the national guidelines. Conflict of interest statement None. Acknowledgments This study was supported by grants from the EVO foundations of Kymenlaakso and Pa¨ija¨t-Ha¨me health care districts and the Kymi Ltd. 100-years Foundation. References AAOS (American Academy of Orthopedic Surgeon), 1999. Position Statement. Hip Fracture in Seniors: A Call for Health System Reform. American Academy of Orthopedic Surgeons, Rosemont. Berry, S.D., Samelson, E.J., Hannan, M.T., McLellan, R.R., Lu, M., Cupples, L.A., Shaffer, M.L., Beiser, A.L., Kelly-Hayes, M., Kiel, D.P., 2007. Second hip fracture in older men and women. Arch. Int. Med. 167, 1971–1976. Black, D.M., Steinbuch, M., Palermo, L., Dargent-Molina, P., Lindsay, R., Hoseyni, M.S., Johnell, O., 2001. An assessment tool for predicting fracture risk in postmenopausal women. Osteoporosis Int. 12, 519–528. Black, D.M., Delmas, P.D., Eastell, R., Reid, I.R., Boonen, S., Cauley, J.A., Cosman, F., Lakatos, P., Leung, P.C., Man, Z., Mautalen, C., Mesenbrink, P., Hu, H., Caminis, J., Tong, K., Rosario-Jansen, T., Krasnow, J., Hue, T.F., Sellmeyer, D., Eriksen, E.F., Cummings, S.R., 2007. Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N. Engl. J. Med. 356, 1809–1822. Boonen, S., McClung, M.R., Eastell, R., El-Hajj Fuleihan, G., Barton, I.P., Delmas, P., 2004. Safety and efficacy of risedronate in reducing fracture risk in osteoporotic women aged 80 and older: implications for the use of antiresorptive agents in the old and oldest old. J. Am. Geriatr. Soc. 52, 1832–1839. Cadarette, S.M., Katz, J.N., Brookhart, M.A., Levin, R., Stedman, M.R., Choudhry, N.K., Solomon, D.H., 2008. Trends in drug prescribing for osteoporosis after hip fracture, 1995–2004. J. Rheumatol. 35, 319–326. Chapuy, M.C., Preziosi, P., Maamer, M., Arnaud, S., Galan, P., Hercberg, S., Meunier, P.J., 1997. Prevalence of vitamin D insufficiency in adult normal population. Osteoporosis Int. 7, 439–443. Classification of Drugs, 2006. La¨a¨kkeiden luokitus (ATC) ja ma¨a¨ritellyt vuorokausiannokset (DDD). La¨a¨kelaitos, Edita Prima Oy (in Finnish). Colo´n-Emeric, C., Kuchibhatla, M., Pieper, C., Hawkes, W., Fredman, L., Magaziner, J., Zimmerman, S., Lyles, K.W., 2003. The contribution of hip fracture to risk of subsequent fracture: data from two longitudinal studies. Osteoporosis Int. 14, 879–883. Cramer, J., Amonkar, M.M., Hebborn, A., Suppapanya, N., 2004. Does dosing regimen impact persistence with bisphosphonate therapy among postmeno-pausal osteoporotic women? J. Bone Miner. Res. 19 (Suppl. 1), S448. Dinah, A.F., 2002. Sequential hip fractures in elderly patients. Injury 33, 393–394. Dirschl, D.R., Henderson, R.C., Oakley, W.C., 1997. Accelerated bone mineral loss following a hip fracture: a prospective longitudinal study. Bone 21, 79–82. Dretakis, K.E., Dretakis, E.K., Papakitsou, E.F., Psarakis, S., Steriopoulus, K., 1998. Possible predisposing factors for the second hip fracture. Calcif. Tissue Int. 62, 366–369. Fox, K.M., Magaziner, J., Hawkes, W.G., Yo-Yahiro, J., Zimmerman, S.I., Holder, L., Michael, R., 2000. Loss of bone density and lean body mass after hip fracture. Osteoporosis Int. 11, 31–35. Fukushima, T., Sudo, A., Uchida, A., 2006. Bilateral hip fractures. J. Orthop. Sci. 11, 435–438. Gardner, M.J., Flik, K.R., Moor, P., Lane, J.M., 2002. Improvement in the undertreatment of osteoporosis following hip fracture. J. Bone Joint Surg. Am. 84, 1342–1348. Haynes, R.B., Yao, X., Degani, A., Kripalani, S., Garg, A., McDonald, H.P., 2006. Interventions for enhancing medication adherence (review). Cochrane Libr. 4.
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