Arthritis & Rheumatism (Arthritis Care & Research) Vol. 57, No. 1, February 15, 2007, pp 140 –146 DOI 10.1002/art.22462 © 2007, American College of Rheumatology
ORIGINAL ARTICLE
Barriers in the Management of Glucocorticoid-Induced Osteoporosis JENICE RIA S. GUZMAN-CLARK,1 MEIKA A. FANG,1 MARY E. SEHL,2 LAURAL TRAYLOR,1 THEODORE J. HAHN1
AND
Objective. To determine present practice for the management of glucocorticoid-induced osteoporosis (GIOP) in veterans; to characterize provider knowledge, beliefs, and practice behaviors regarding management of GIOP; and to identify potential barriers and interventions in the management of GIOP. Methods. To characterize current management of GIOP in an academic veterans administration medical center, we conducted a retrospective chart review of 100 patients who were prescribed a 90-day supply of prednisone. To assess clinicians’ knowledge of GIOP clinical guidelines and perceptions of GIOP management, primary care clinicians and subspecialists completed a questionnaire and participated in focus groups. Results. Chart review revealed that only 32 of 100 patients receiving long-term glucocorticoid treatment underwent bone mineral density testing, and only 32 patients were prescribed the recommended calcium supplements. Of the 23 providers who completed the questionnaire and participated in the focus groups, 4 correctly identified both the dose and duration of glucocorticoid use at which GIOP prevention measures should be instituted. Common GIOP management barriers cited by participants were lack of knowledge, having limited time during the clinic visit to address all problems, patient nonadherence, and system problems. The most commonly mentioned potential interventions were the use of computerized clinical reminders and patient education. Conclusion. Clinicians frequently do not follow recommended guidelines for the management of GIOP. Improving the management of GIOP will likely require a fundamental redesigning of care processes for this disorder in order to overcome provider, patient-related, and system barriers. KEY WORDS. Glucocorticoids; Osteoporosis; Veterans.
INTRODUCTION Patients treated with glucocorticoids are at risk for fractures from glucocorticoid-induced osteoporosis (GIOP). Fractures may occur even though there is minimal or no loss of bone mineral density (BMD) (1,2). Early intervention is important, even at dosages as low as 5 mg of prednisone equivalent per day for as little as 3 months (3–5). Clinical guidelines are available for the prevention and Supported by Merck & Co., Inc. and with resources and the use of facilities at the VA Greater Los Angeles Healthcare System West Los Angeles Healthcare Center. 1 Jenice Ria S. Guzman-Clark, RN, MSN, Meika A. Fang, MD, Laural Traylor, MSW, Theodore J. Hahn, MD: VA Greater Los Angeles Healthcare System, Los Angeles, CA, and the University of California, Los Angeles; 2Mary E. Sehl, MD: University of California, Los Angeles. Address correspondence to Jenice Ria S. Guzman-Clark, RN, MSN, VA Greater Los Angeles Healthcare System, West Los Angeles, GRECC 11G, 11301 Wilshire Boulevard, Los Angeles, CA 90073. E-mail:
[email protected]. Submitted for publication June 1, 2005; accepted in revised form April 14, 2006.
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management of GIOP, including those provided by the American College of Rheumatology (ACR) (6) and by Adler and Hochberg (7). Current ACR guidelines recommend that all patients beginning therapy with glucocorticoids (prednisone equivalent ⱖ5 mg/day) with a planned treatment duration of ⱖ3 months should be counseled on modification of lifestyle risk factors for osteoporosis, given calcium plus vitamin D supplementation, and started on bisphosphonate therapy. However, recent studies suggest that a relatively low percentage of patients who are prescribed continuous glucocorticoid therapy actually receive diagnostic evaluation or preventive treatment for GIOP (8 –13). In a retrospective chart review examining patients in a Veterans Administration (VA) hospital setting, Elliott and colleagues (9) noted poor adherence to guidelines for the management of GIOP. Only 8% of male veterans who were prescribed ⱖ7.5 mg/day of prednisone over a 6-month study period received any GIOP prophylaxis, and of those veterans who met the ACR criteria for antiosteoporotic therapy, only 38% received the recommended medications (9). Several studies have attempted to improve osteoporosis
Glucocorticoid-Induced Osteoporosis Barriers prevention and management with mixed results (14 –16). Developing a better understanding of provider perceptions regarding the issues that lead to the undertreatment of GIOP and utilizing provider suggestions to improve GIOP management may improve the success of future interventions. Therefore, the objective of the present study was to 1) determine present practice regarding evaluation and preventive treatment for GIOP in patients receiving longterm glucocorticoid therapy at the VA Greater Los Angeles Healthcare System (WLA) in West Los Angeles, California, a large urban academic medical center with a predominantly male patient population; 2) characterize provider knowledge, beliefs, and practice behaviors regarding the prevention and management of GIOP in veterans; and 3) identify potential barriers to and interventions for the improved management of GIOP.
PATIENTS AND METHODS This research project was approved by the Institutional Review Board at the VA Greater Los Angeles Healthcare System. Chart review. Patients who were prescribed a 90-day supply of prednisone from July 1, 2001 to June 1, 2002 were identified through the VA WLA Pharmacy Services. A retrospective chart review was performed for the first 100 patients who were prescribed on average at least 5 mg/day of prednisone. Data obtained included demographic information, medical information related to the use of glucocorticoids, prescribing providers, results of dual-energy x-ray absorptiometry (DXA) bone density studies, and treatment provided for the prevention and/or management of GIOP. If a provider noted discussion of prophylactic measures for osteoporosis or evaluation but the patient refused the recommended treatment, the patient was considered treated. Descriptive analysis was used to determine the frequency of preventive therapy and BMD measurement as well as the treatment regimen used. Provider questionnaire and focus groups. Attending physicians, internal medicine trainees (interns, residents, and fellows), and staff nurse practitioners who provide outpatient care to patients taking glucocorticoids were recruited to complete a questionnaire and participate in focus groups after obtaining informed consent. The providers answered questions regarding their medical training and knowledge, practice behaviors, and beliefs about the management of GIOP. Descriptive analysis was used to determine the frequency of responses that correctly identified measures to prevent and manage GIOP. These same clinicians attended 1 of 4 focus groups lasting 45– 60 minutes that were facilitated by a social worker trained in group dynamics. A clinical scenario was presented first to stimulate discussion. The facilitator then used scripted probes to elicit providers’ views regarding barriers to the prevention, diagnosis, and treatment of GIOP in their practice setting as well as potential strategies to overcome these barriers. Participants received dinner and a small honorarium. All sessions were audiotaped and
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Table 1. Patient and management characteristics (n ⴝ 100)* Characteristic
Value
Age, mean ⫾ SD years Male sex Glucocorticoid dose, median (range) mg/day Most common diseases requiring glucocorticoids Chronic pulmonary disease/asthma Rheumatoid arthritis Organ transplant Most common providers prescribing glucocorticoids Primary care provider Rheumatologist Pulmonologist with others Rheumatologist with others Pulmonologist Other
73 ⫾ 16.73 94 7.5 (5–60)
26 18 16
47 14 12 6 6 15
* Values are the percentage unless otherwise indicated.
transcribed verbatim. Written notes served as a secondary source of information if the audiotapes failed to adequately capture the participants’ comments. Transcripts were coded and analyzed using QSR N6 software (17). The unit of analysis for coding was in the form of a complete sentence; however, the number of respondents for specific themes is described in the text to give equal weight to each response. This was done because some respondents were able to state their idea in 1 sentence, whereas others used 2–3 sentences to convey the same idea. Two independent evaluators analyzed the transcripts for thematic content. If statements were inaudible, the evaluators referred back to the written documentation of participant statements obtained during the focus group session for clarification.
RESULTS Review of charts. The mean age of patients studied was 73 years and the median glucocorticoid dosage was 7.5 mg/day (Table 1). Chronic obstructive pulmonary disease (COPD) was the most common reason that glucocorticoid medication was prescribed. Primary care providers, followed by rheumatologists, were the most frequent prescribers of glucocorticoids. Nineteen patients were newly started on glucocorticoid therapy during the study period. Care provided to 47 of the 100 patients was comanaged with non-VA providers. Calcium was the most commonly used medication (32 patients), followed by multivitamins (19 patients) and vitamin D (12 patients) in the 100 charts reviewed. A bisphosphonate was used in only 6 of 100 patients to prevent GIOP, and another 18 patients were prescribed a bisphosphonate for treatment of GIOP after a DXA scan result showed osteopenia or osteoporosis. A total of 32 patients had DXA bone density scans documented in their medical chart, with 2 performed at non-VA facilities and 1 ordered but not yet performed during the period in which the charts were reviewed. Two
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Table 2. Characteristics of provider focus group participants (n ⴝ 23)*
Characteristic Sex Male Female Years of practice, median (range) Residency specialty Internal medicine Family medicine No response Second board certification Geriatric medicine Endocrinology Clinical genetics Rheumatology Outpatient practice location Primary care Rheumatology
Physicians (n ⴝ 19)
Nurse practitioners (n ⴝ 4)
12 7 4 (1–19)
1 3 5 (2–12)
17 1 1 1 1 1 1 3 1
* Values are the number unless otherwise indicated.
of these patients were excluded from the study because their DXA scans were performed prior to starting glucocorticoid therapy. DXA results were documented in the charts of 29 patients, with 16 patients meeting the standard criteria for osteopenia, 6 meeting the criteria for osteoporosis, and 7 having normal BMD results. Prior to bone density evaluation, one-third of these patients (9 of 29) were not taking any pharmacologic treatment to prevent GIOP and only 2 were prescribed a bisphosphonate. For the 16 patients whose DXA scans showed osteopenia, 13 were started on a bisphosphonate and either 1 or 2 of the following: calcium, vitamin D, or multivitamins. One patient was already receiving bisphosphonate therapy for preventive management and another was started only on calcium and vitamin D. Of the 6 patients whose DXA bone density measurements revealed osteoporosis, 5 patients were subsequently prescribed a bisphosphonate and the remaining patient continued on his previously instituted bisphosphonate therapy. Of the 7 patients with normal DXA results, 1 discontinued the preventive therapy he was receiving (calcium, multivitamins, and vitamin D) and the other 6 continued on their preventive therapy with calcium and vitamin D or multivitamins. Rheumatologists were the providers who most frequently ordered a BMD and changed management based on BMD results, followed by primary care providers. Provider focus groups and questionnaire. The characteristics of the focus group participants are shown in Table 2. Most of the physicians specialized in internal medicine and most of the nurse practitioners worked in primary care. The median years of practice were 4 and 5 years, respectively. Few of the health care providers (8 of 23) thought that they had adequate training and experience to manage GIOP and only 4 providers knew both the dose (5 mg/day)
of prednisone and duration of therapy (3 months) that require institution of therapy to prevent or treat GIOP according to current guidelines. Of 23 participants, 20 reported not having seen or read the ACR clinical guidelines on GIOP, and 16 of 23 reported that they usually or always institute measures to prevent GIOP in patients starting on long-term glucocorticoids; however, 9 of 23 participants did not know that bisphosphonates and BMD measurements were recommended in the prevention of GIOP. Regarding the interventions recommended for treatment of established GIOP, 21 of 23 health care providers reported that they prescribed bisphosphonates and 19 reported that they ordered calcium and vitamin D supplements. Less than half knew that lifestyle modification of risk factors, such as smoking cessation or avoidance, reduction in excessive alcohol consumption, and weightbearing exercises, is recommended to treat GIOP. All participants believed that both primary care and medicine subspecialty providers are responsible for the prevention and management of GIOP. Several themes emerged during the provider focus group sessions regarding barriers to the prevention and management of GIOP (Figure 1). The most commonly discussed barriers were provider barriers, followed by patient-related barriers as perceived by providers, and finally system barriers. The most commonly mentioned barriers are listed in Table 3. Other barriers that were mentioned included differing opinions as to who should be responsible for GIOP screening (primary care versus specialty providers), whether a DXA bone scan is necessary before starting glucocorticoid treatment, and concerns about the sensitivity of the DXA scan in measuring BMD in males. Focus group participants suggested several potential interventions that might improve the prevention and management of GIOP (Table 4, Figure 2). Participants thought that clinical reminders in the computerized medical record system would be helpful, although somewhat time
Figure 1. Most frequently identified barriers. DXA ⫽ dual-energy x-ray absorptiometry.
Glucocorticoid-Induced Osteoporosis Barriers
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Table 3. Most frequently identified barriers to glucocorticoid-induced osteoporosis prevention and treatment* Specific categories
Examples
Provider barriers Poor knowledge
“They’re probably out there [guidelines] but I don’t even know if anyone ever actually peruses them.” “You’re basically just focusing on their chief complaint.” “We don’t have sufficient time really to even address all the problems at every visit.”
Other priorities Limited time Patient barriers Attitude regarding asymptomatic disease
Nonadherence Effects of comorbid conditions System barriers Obtaining DXA Restricted drugs Computerized ordering system
“They like some treatment when things happen. They’re not so great with prevention.” “They can’t feel their osteoporosis.” “I think in our population the compliance is low to begin with . . . for something like prevention, it’s probably even lower.” “Other barriers might be . . . somebody who is taking thyroid medications. Obviously that cannot be stopped . . .” “That has to be scheduled and coordinated. . . . You order it and pray it gets done.” “. . . until pretty recently, I couldn’t order Fosamax.” “It is so time consuming . . . you really have to focus for 5 minutes on clicking the right things, that your brain can’t be free.”
* DXA ⫽ dual-energy x-ray absorptiometry.
consuming. Some barriers to the use of computerized clinical reminders included tolerance (“you get used to clicking them off and ignoring them”), being inundated with numerous other clinical reminders, and the lack of time to input all of the information required for each clinical reminder. The participants also suggested the possibility of programming the computer system to automatically order GIOP screening, with provider approval. Alternatively, it was suggested that the pharmacist could remind the clinician to screen for GIOP, depending on the dose and duration of glucocorticoid prescribed, and could alert pro-
viders about potential drug interactions and adverse reactions related to the medications used for GIOP treatment. The focus group participants also noted the importance of offering provider education through lectures and online educational opportunities, but acknowledged concerns about a lack of time to attend all of the educational opportunities available and uncertainty as to whether education would change long-term provider behavior. They also pointed out that improved access to clinical guidelines might be helpful, and suggested interventions including a pocket guide and electronic access to guidelines through
Table 4. Potential interventions to improve management of glucocorticoid-induced osteoporosis* Categories
Examples
Computerized clinical reminders
“. . . the computer adds up how many days the patient has been on steroids over the past year and it will come up with a clinical reminder that the patient has exceeded a certain number. . .” “If you had a simple 1-page reminder for the patients . . . which would tell why they are at risk and how it could be prevented . . .” “. . . if it’s [DXA] more readily available and easier, patients will be more willing to get that done if they’re at risk.” “If we had one extra person who would be willing to take the patient down [to get DXA] . . . it would be a lot easier.” “I think a medical grand rounds format would be good because it would get not just the residents but the attending staff also . . .” “Say if it were even made into a palm pilot or something like that, a little table or a card . . . in a concise format with some of the guidelines and treatment and so forth would probably be used.” “. . . probably individual counseling, just a few sentences really quick about that would probably make the most difference.” “. . . there is a superstar attached to it, they’ll say, oh yeah, that’s what so-and-so has. I see that they sort of make that connection.” “. . . the pharmacist who dispenses medication notices that this patient is on steroids for x number of months and just automatically sends you a reminder.”
Patient educational handouts System changes Ancillary staff Provider education Provider access to guidelines
Patient-provider communication Spokesperson Pharmacy alerts * DXA ⫽ dual-energy x-ray absorptiometry.
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Figure 2. Potential interventions cited by focus group participants.
the patient care computer system or a personal digital assistant program.
DISCUSSION Our retrospective chart review indicated that health care providers rarely prescribed a bisphosphonate for the prevention of GIOP, but were more willing to prescribe bisphosphonates on the basis of DXA bone density results. Our findings were similar to those of previous reports demonstrating that health care providers do a suboptimal job in preventing and treating GIOP (7–11). As in previous studies, COPD and rheumatoid arthritis were the most common diagnoses for which glucocorticoids were prescribed, and internal medicine specialists and primary care providers were the most common prescribers of glucocorticoid medications (8,10,12,13). One unsurprising finding was that the majority of the focus group participants were unfamiliar with the ACR guidelines for GIOP management and, accordingly, did not know when to screen and treat patients for this disorder. Because most clinical practice guidelines are developed by specialty-dominated organizations (ACR targets rheumatologists), providers who are not members of that specialty may not be made aware of those guidelines. In addition, previous studies have shown that issues other than providers’ lack of awareness often constitute barriers to provider adherence to clinical guidelines. These may include provider lack of self efficacy in implementing treatment guidelines, external barriers over which the provider has no control, clinical inertia, and inexperience in “treating to target” (13,14). Another important study finding is that although most of the focus group participants reported that they usually or always institute measures to prevent GIOP in patients being started on long-term glucocorticoid therapy, only onethird of patients in the retrospective chart review were prescribed preventive medications for GIOP. Therefore, the providers in the present study overestimated their compliance to the clinical guidelines for GIOP prevention,
Guzman-Clark et al similar to the reported overestimation of compliance to guidelines by health care providers managing a variety of other chronic disorders including hypertension, diabetes, and hyperlipidemia (14). In addition, although all providers initially stated that both primary and specialty providers should be responsible for the prevention and management of GIOP in the questionnaire, focus group findings revealed differing ideas as to who should actually screen and follow up patients. In this regard, there is continuing controversy in the literature as to who should be responsible for the prevention and management of GIOP, with some authors supporting the view that primary care providers should take the lead in prevention (18,19). A majority of the focus group participants in the present study placed the responsibility for screening and management of GIOP on medicine subspecialists due to the limited time available to address multiple medical problems during a primary care clinic visit and the high likelihood that subspecialists will be treating patients needing long-term or high-dose steroids. A consensus among primary care and subspecialty providers needs to be reached so that responsibilities can be better defined to improve care provided to patients (16). Of the potential solutions to provider barriers to managing GIOP, use of computerized clinical reminders appears to be a promising approach. The VA computerized patient record system has been used effectively to automatically remind providers about a number of patient care issues including annual preventive screening and potential drug interactions (20). Provider behavior, however, does not necessarily change based on treatment alerts alone. For example, in a study examining issues in osteoporosis management after the occurrence of bone fractures, Harrington and colleagues found that use of reminders and notification systems alone was not sufficient to alter provider behavior, and they recommended system and process changes to improve osteoporosis management (16). In this regard, it has been reported that providers are more likely to change medications for safety reasons if they are contacted by a pharmacist (54%) as opposed to receiving an electronic drug alert (4%) (21). Another intervention that was even more successful combined a multifaceted approach (faxed physician reminders combined with patient education), resulting in statistically significant increases in rates of BMD testing and appropriate osteoporosis treatment in older persons seen in the emergency room following a wrist fracture (22). A similar redesigning of aspects of the health care system and the addition of new management processes may be required to improve GIOP management in patient populations receiving long-term glucocorticoid therapy. Harrington and colleagues described changing the system by obtaining provider consensus and creating a direct referral program to identify osteoporosis in patients who had recently had a fracture, in combination with implementing the new processes of nurse-managed case management and followup, to ensure adherence to treatment guidelines and achievement of target clinical goals for the majority of patients (16). This population and system-based management style is rarely taught to providers and clinical administrators, but is a promising way of improving the manner
Glucocorticoid-Induced Osteoporosis Barriers in which care is provided to patients (16). The limited scope of the recommended interventions proposed by the focus group participants in the present study may reflect their lack of knowledge of the fundamental redesign of health care delivery and practitioner training that is often required to improve the care of patients with chronic disorders such as GIOP. Patient education was the second most common intervention recommended by focus group participants to attempt to improve the prevention and management of GIOP. Previous studies on patient education in osteoporosis have mainly been performed in patients who have already had fractures (15,22–26), and some of these studies enlisted the assistance of ancillary staff such as imaging center personnel (27) and pharmacies (28). Whether these interventions affect patient outcomes and future fracture incidence has not been well studied. In addition, even if osteoporosis educational materials are provided to patients at risk for osteoporosis, this is often not enough to change knowledge, attitude, and behaviors regarding prevention of osteoporosis (24,29,30). The current literature suggests that successful patient education interventions relative to osteoporosis should include techniques for better patient self-management and bone health behaviors (31) and should take into consideration differences in knowledge, attitudes, and beliefs about osteoporosis between men and women (29). Future care improvement strategies should also address comorbidity issues and help health care providers prioritize GIOP guideline recommendations in patients with complex comorbid illnesses. The focus group participants in our present study noted that they often did not have time in the clinic to deal with GIOP after addressing more life-threatening medical conditions, and that they were concerned about the ability of patients who were already taking several medications to remember to take additional medications for osteoporosis. Boyd and colleagues have pointed out that current clinical guidelines usually provide detailed guidance for managing single diseases but fail to address the needs of older patients with multiple chronic diseases (32). For example, adhering to the clinical practice guidelines for each chronic disease may potentially lead to polypharmacy, potential drug-drug and drugdisease interactions, and conflicting lifestyle recommendations. There are several limitations to the present study. First, with regard to the chart review process, it is possible that in some patients, screening and/or preventive therapy for GIOP was provided by a clinician outside the VA system and the information was not documented in the computerized medical record used in the retrospective chart review. Also, patients may not have taken the medications as prescribed or they may have self administered over-thecounter calcium and multivitamin supplements that were not recorded in the medical record. In addition, this study was performed in only 1 urban VA setting and utilized only the first 100 patients, mainly men, who met the inclusion criteria during the study period, and therefore the results may not be generalizable to other VA or non-VA settings. Furthermore, the provider focus groups were comprised of a convenience sample of providers and may
145 not reflect the views of all VA clinicians. Although COPD was the most common diagnosis associated with long-term prednisone use, only 1 physician who was board certified in pulmonary medicine participated in the focus group. Moreover, although focus group participants reported their perceptions of patient-related barriers, further research will be needed to capture actual patient perspectives and acceptance of preventive and therapeutic measures for the management of GIOP. Previous studies have shown that patient and provider perceptions about care provided or accepted may differ (33,34) and that only a small number of patients recall receiving any counseling regarding prevention of GIOP (35). In conclusion, there were a number of provider, patientrelated, and system-specific barriers identified by the clinicians in our study that contribute to suboptimal treatment of patients at risk for GIOP. To improve the quality of care for patients at risk for GIOP, interventions are needed that will change clinician knowledge, attitudes, and behavior by addressing a combination of provider, patient, and system processes and barriers similar to those identified in the present study. In our facility, we are currently examining the feasibility of several approaches to improve the prevention and management of GIOP. These include 1) developing a computerized clinical reminder with recommendations when glucocorticoids are ordered to improve provider compliance with clinical guidelines, 2) initiating a quality improvement program consisting of provider education with performance feedback and patient education (e.g., waiting room print and audiovisual materials), and 3) using the PRECEDE-PROCEED planning model designed by Green and Kreuter for health education and health promotion programs to involve patients in their own care and improve chronic disease management (36). Any future interventions to improve the prevention and treatment of GIOP will likely require a fundamental redesign of care processes to address the provider, patient, and system barriers that were identified in the present study. AUTHOR CONTRIBUTIONS Ms Guzman-Clark had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study design. Ms Guzman-Clark, and Drs. Fang and Hahn. Acquisition of data. Ms Guzman-Clark and Traylor, and Dr. Fang. Analysis and interpretation of data. Ms Guzman-Clark, and Drs. Fang, Sehl, and Hahn. Manuscript preparation. Ms Guzman-Clark and Traylor, and Drs. Fang and Sehl. Statistical analysis. Ms Guzman-Clark and Dr. Fang. Other (acquire funding support). Dr. Hahn.
ROLE OF THE STUDY SPONSOR Merck & Co. were not involved in the study design, data collection, data analysis, or writing of the manuscript. They concurred with the decision to submit the manuscript for publication and approved the content of the submitted manuscript.
REFERENCES 1. Maricic M, Gluck O. Densitometry in glucocorticoid-induced osteoporosis [review]. J Clin Densitom 2004;7:359 – 63.
146 2. Steinbuch M, Youket TE, Cohen S. Oral glucocorticoid use is associated with an increased risk of fracture. Osteoporos Int 2004;15:323– 8. 3. McIlwain HH. Glucocorticoid-induced osteoporosis: pathogenesis, diagnosis, and management. Prev Med 2003;36: 243–9. 4. Tamura Y, Okinaga H, Takami H. Glucocorticoid-induced osteoporosis. Biomed Pharmacother 2004;58:500 – 4. 5. Saag KG. Prevention of glucocorticoid-induced osteoporosis [review]. South Med J 2004;97:555– 8. 6. American College of Rheumatology Ad Hoc Committee on Glucorticoid-Induced Osteoporosis. Recommendations for the prevention and treatment of glucocorticoid-induced osteoporosis: 2001 update. Arthritis Rheum 2001;44:1496 – 503. 7. Adler RA, Hochberg MC. Suggested guidelines for evaluation and treatment of glucocorticoid-induced osteoporosis for the Department of Veterans Affairs. Arch Intern Med 2003;163: 2619 –24. 8. Aagaard EM, Lin P, Modin GW, Lane NE. Prevention of glucocorticoid-induced osteoporosis: provider practice at an urban county hospital. Am J Med 1999;107:456 – 60. 9. Elliott ME, Farrah RM, Binkley NC, Carnes ML, Gudmundsson A. Management of glucocorticoid-induced osteoporosis in male veterans. Ann Pharmacother 2004;34:1380 – 4. 10. Mudano A, Allison J, Hill J, Rothermel T, Saag K. Variations in glucocorticoid induced osteoporosis prevention in a managed care cohort. J Rheumatol 2001;28:1298 –305. 11. Solomon DH, Katz JN, Jacobs JP, la Tourette AM, Coblyn J. Management of glucocorticoid-induced osteoporosis in patients with rheumatoid arthritis: rates and predictors of care in an academic rheumatology practice. Arthritis Rheum 2002; 46:3136 – 42. 12. Yood RA, Harrold LR, Fish L, Cernieux J, Emani S, Conboy E, et al. Prevention of glucocorticoid-induced osteoporosis: experience in a managed care setting. Arch Intern Med 2001; 161:1322–7. 13. Feldstein AC, Elmer PJ, Nichols GA, Herson M. Practice patterns in patients at risk for glucocorticoid-induced osteoporosis. Osteoporos Int 2005;16:2168 –74. 14. Phillips LS, Branch WT, Cook CB, Doyle JP, El-Kebbi IM, Gallina DL, et al. Clinical inertia. Ann Intern Med 2001;135: 825–34. 15. Johnson SL, Petkov VI, Williams MI, Via PS, Adler RA. Improving osteoporosis management in patients with fractures. Osteoporos Int 2005;16:1079 – 85. 16. Harrington JT, Barash HL, Day S, Lease J. Redesigning the care of fragility fracture patients to improve osteoporosis management: a health care improvement project. Arthritis Rheum 2005;53:198 –204. 17. Richards L. Using N6 in Qualitative Research. 1st ed. Doncaster Victoria Australia: QSR International Pty Ltd; 2002. 18. Simonelli C, Killeen K, Mehle S, Swanson L. Barriers to osteoporosis identification and treatment among primary care physicians and orthopedic surgeons. Mayo Clin Proc 2002;77: 334 – 8. 19. Gourlay M. Osteoporosis management: out of subspecialty practice and into primary care [editorial]. Am Fam Physician 2004;70:1219 –20.
Guzman-Clark et al 20. Murff HJ, Kannry J. Physician satisfaction with two order entry systems. J Am Med Inform Assoc 2001;8:499 –509. 21. Glassman PA, Simon B, Belperio P, Lanto A. Improving recognition of drug interactions: benefits and barriers to using automated drug alerts. Med Care 2002;40:1161–71. 22. Majumdar SR, Rowe BH, Folk D, Johnson JA, Holroyd BH, Morris DW, et al. A controlled trial to increase detection and treatment of osteoporosis in older patients with a wrist fracture. Ann Intern Med 2004;141:366 –73. 23. Ashe M, Khan K, Guy P, Kruse K, Hughes K, O’brien P, et al. Wristwatch-distal radial fractures as marker for osteoporosis investigation: a controlled trial of patient education and a physician alerting system. J Hand Ther 2004;17:324 – 8. 24. Cuddihy MT, Amadio PC, Gabriel SE, Pankratz VS, Kurland RL, Melton LJ 3rd. A prospective clinical practice intervention to improve osteoporosis management following distal forearm fracture. Osteoporos Int 2004;15:695–700. 25. Gardner MJ, Brophy RH, Demetrakopoulos D, Koob J, Hong R, Rana A, et al. Interventions to improve osteoporosis treatment following hip fracture: a prospective, randomized trial. J Bone Joint Surg Am 2005;87:3–7. 26. Johnson SL, Petkov VI, Williams MI, Via PS, Adler RA. Improving osteoporosis management in patients with fractures. Osteoporos Int 2005;16:1079 – 85. 27. Cram P, Schlechte J, Rosenthal GE, Christensen AJ. Patient preference for being informed of their DXA scan results. J Clin Densitom 2004;7:275– 80. 28. McCormack JP, Dolovich L, Levine M, Burns S, Nair K, Cassels A, et al. Providing evidence-based information to patients in general practice and pharmacies: what is the acceptability, usefulness and impact on drug use? Health Expect 2003;6: 281–9. 29. Sedlak C, Doheny M, Estok PJ. Osteoporosis in older men: knowledge and health beliefs. Orthop Nurs 2000;19:38 – 42, 44 – 6. 30. Solomon DH, Finkelstein JS, Polinski JM, Arnold M, Licari A, Cabral D, et al. A randomized controlled trial of mailed osteoporosis education to older adults. Osteoporos Int 2006;17: 760 –7. E-pub 2006. 31. Gold DT, Silverman SL. Osteoporosis self-management: choices for better bone health. South Med J 2004;97:551– 4. 32. Boyd CM, Darer J, Boult C, Fried LP, Boult L, Wu AW. Clinical practice guidelines and quality of care for older patients with multiple comorbid diseases: implications for pay for performance. JAMA 2005;294:716 –24. 33. Unson CG, Siccion MD, Gaztambide J, Gaztambide S, Mahoney Trella P, Prestwood K. Nonadherence and osteoporosis treatment preferences of older women: a qualitative study. J Womens Health 2003;12:1037– 45. 34. Maly RC, Leake B, Frank JC, DiMatteo R, Reuben DB. Implementation of consultative geriatric recommendations: the role of patient-primary care physician concordance. J Am Geriatr Soc 2002;50:1372– 80. 35. Blalock SJ, Norton LL, Patel RA, Dooley MA. Patient knowledge, beliefs, and behavior concerning the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Rheum 2005;53:732–9. 36. Green LW, Kreuter MW. Health program planning: an educational and ecological approach. 4th ed. New York: McGrawHill; 2004.
