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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptHHS Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Arthritis Care Res (Hoboken). Author manuscript; available in PMC 2011 July 1.
Published in final edited form as:
PMCID: PMC2953549

Osteoporosis Screening, Prevention and Treatment in Systemic Lupus Erythematosus: Application of the Systemic Lupus Erythematosus Quality Indicators



Osteoporosis and fragility fractures are associated with significant morbidity for patients with systemic lupus erythematosus (SLE). New quality indicators (QI) for SLE advise bone mineral density testing, calcium and vitamin D use, and antiresorptive or anabolic treatment for specific subgroups of patients using high-dose steroids.


Subjects were participants in the University of California San Francisco Lupus Outcomes Study, an ongoing longitudinal study of patients with physician-confirmed SLE, in 2007–2008. Patients responded to an annual telephone survey and were queried regarding demographic, clinical, and other healthcare-related variables. Multiple logistic regression was used to predict receipt of care per the QIs described above.


One hundred and twenty seven patients met criteria for the formal definitions of the denominators for QI I (Screening) and QI II (Calcium and Vitamin D); 91 met formal criteria for QI III (Treatment). The proportions of patients receiving care consistent with the QIs were 74%, 58%, and 56% for QIs I, II, and III, respectively. In a sensitivity analysis of all steroid users (n=427 for QI I and II; n = 224 for QI III), rates were slightly lower. Predictors of receiving care varied by QI and by denominator; however, female sex, older age, Caucasian race, and longer disease duration were associated with higher quality care.


Bone health-related care in this community-based cohort of SLE patients is suboptimal. Quality-improvement efforts should address osteoporosis prevention and care among all SLE patients, especially those taking high-dose, prolonged steroids.

In the past50 years, SLE-related mortality has improved significantly. Lupus patients are living longer and suffering increased morbidity from complications related to chronic inflammation and long-term medication use, including coronary artery disease, malignancies, and osteoporotic fractures.1,2,3

Although estimates for the prevalence of osteopenia and osteoporosis in SLE have varied, some of the largest studies indicate that the burden of osteoporosis may be over 20%.4,5 Individuals with SLE are at particular risk for osteoporosis compared with age-matched controls because of high disease activity, vitamin D deficiency due to sun avoidance, early menopause from use of cytotoxic agents, and glucocorticoid use.6,7,8 The minimum dose of glucocorticoid that poses an increased risk of osteoporosis is debated, as many studies have found glucocorticoid use in SLE to be associated with low bone mineral density (BMD),9,10,11,12,13,14,15 while others have not confirmed this association after adjusting for disease damage and duration.16,17 Some studies suggest that SLE patients may have a baseline increased risk of low bone density that is independent of glucocorticoid use or disease duration. 18,19

Developed through a process that combined systematic literature reviews with formal expert consensus processes, the first set of quality indicators (QIs) for SLE was published in 2009. 20 As opposed to clinical guidelines, which define optimal health care practices in the context of complex clinical decision-making, QIs specify a minimally acceptable standard of care for a specific patient population.21 Three out of the 20 published QIs addressed bone health-related care and set a glucocorticoid dose of 7.5 mg of prednisone daily for at least 3 months as the threshold above which patients should be advised to use calcium, vitamin D, and to obtain screening for osteoporosis with a BMD test. As expected, guidelines regarding osteoporosis care (not specific to SLE patients)set a higher bar for screening and prevention: the American College of Rheumatology (2001) suggests that patients using more than 5 mg of prednisone daily for 3 months be screened for osteoporosis and given calcium and vitamin D prophylaxis.22 Guidelines from the National Osteoporosis Foundation (1999) go further by suggesting that patients on 5 mg of prednisone daily for an unspecified length of time or patients with any chronic condition associated with low bone mass should receive calcium, vitamin D, and screening for osteoporosis. 23

The objective of this study was to evaluate the quality of osteoporosis screening, prevention, and treatment in a community-based cohort of patients with physician-confirmed SLE. We applied the measures developed in the SLE Quality Indicator project to examine the proportion of patients who met criteria for each osteoporosis-related QI.



The University of California, San Francisco (UCSF) Lupus Outcomes Study (LOS) is an ongoing longitudinal survey of patients with confirmed SLE recruited between 2002 and 2009. Patients were originally recruited from academic rheumatology offices (22%), community rheumatology offices (11%), and other community-based sources (66%), such as SLE support groups, the Internet, and media advertisements. Two-thirds of the participants were residents of California while the remainder lived in 40 other US states. Patients were required to carry a diagnosis of SLE provided by a physician. SLE diagnoses for all LOS participants were additionally confirmed by a formal chart review to document American College of Rheumatology criteria for SLE.24

Questions regarding osteoporosis care and prevention were introduced into the LOS in 2007–2008, during the sixth wave of interviews. Seven hundred and seventy nine individuals were interviewed as part of wave 6. Thirty-seven of these patients (4.8%) were excluded because of incomplete data for the outcomes or main predictors, leaving 742 patients eligible for this analysis.


Data were collected via an annual, structured, 1-hour-long telephone survey conducted by trained interviewers. The survey included validated items covering the following domains: demographics and socioeconomic status, SLE symptoms and disease status, disability, general health and social functioning, employment, psychological and cognitive status, health care utilization, medications, and health insurance coverage.

The UCSF and Stanford Committees on Human Research approved the study protocol. All participants provided informed consent prior to the interviews.


Demographic/socioeconomic variables

Socioeconomic and demographic characteristics included age, sex, self-reported race/ethnicity (Caucasian, Hispanic, African-American, Asian, other/multiple), education level (high school or less, some college or vocational school, college graduate), and income (annual household income at or below 125% of the federal poverty threshold in the year prior to interview).

Health insurance

The insurance section of the questionnaire, derived from the Medical Expenditures Panel Survey, included items regarding the type of health plan (health maintenance organization versus fee-for-service) and source of coverage, if any (employment based, individually purchased plan, Medicare, or Medicaid).25

Clinical variables

SLE-specific variables included disease duration and disease activity, captured using the SLAQ, a validated self-report measure of SLE activity (possible range 0–44).26,27 Patients were also queried regarding their physical functioning (using the Medical Outcomes Study Short Form-36) and menopausal status.28 Presence of non-traumatic (fragility) fracture was determined by asking a series of questions (“Has a doctor told you that you broke or fractured a bone or had a spinal compression fracture?” If yes, “Which bone did you break?” If the reply included a spine or hip fracture, “Was it from a traumatic injury such as from playing a sport or a car accident?”). Self-reported diagnoses of osteoporosis were based on the following question: “Do you have or are you being treated for osteoporosis or thinning bones?”

Health care utilization

The health care utilization section of the questionnaire asked participants about their medical care over the prior12 months. It included an enumeration of all healthcare practitioner visits by specialty, including hospitalizations. Participants were asked directly about who serves as their “main SLE doctor” (rheumatologist, nephrologist, internist, general practice, other, or none).

Subjects were asked about the use of medications since the previous survey, including drugs used for common comorbid conditions, glucocorticoids (oral and intravenous), and disease modifying antirheumatic drugs (DMARDs). We created a measure of pill burden by summing the number of medications each patient reported taking (range 0–15); this sum excluded calcium or vitamin D use or drugs taken for the treatment of osteoporosis.


The primary outcome of interest was receipt of care as described in each of the 3 osteoporosis quality indicators. This was determined by calculating the proportion of patients eligible for the measure (denominator) who met criteria for care consistent with that measure (numerator). Numerators and denominators for each of the QIs are outlined in Table 1.

Table 1
Description of numerators and denominators for osteoporosis-related quality indicators in systemic lupus erythematosus

In order to define the stability of the QI’s to changes in the denominator, we measured the receipt of the QIs in 2 non-mutually exclusive groups of patients: First, we assessed the QIs as they were written, using the formal denominators listed in Table 1 (FORMAL denominator). Second, we examined patients taking glucocorticoids at any dose, for any period of time (QI I (Screening) and QI II (Calcium and Vitamin D)) or among patients taking glucocorticoids at any dose for any period of time who also had a history of osteoporosis or fragility fracture (QI III (Treatment)) (ALL STEROID denominator).

Outcomes and eligibility (i.e., numerators and denominators) were determined based on questions posed during the survey, including direct questions about BMD testing, calcium, vitamin D, and antiresorptive and anabolic use. Qualifying antiresorptives/anabolics included alendronate, residronate, ibandronate, etidronate, pamidronate, zolendronic acid, calcitonin nasal spray, raloxifene, and teriparatide.

Because questions about BMD testing were posed in all waves of the LOS, we were able to determine whether patients had received BMD testing at any time within the past 24 months. We chose a 24-month window because (1) the QIs do not provide a specific timeframe for BMD testing and (2) the majority of insurance companies, including Medicare, cover the cost of BMD testing for qualifying patients at least once every 24 months.29

Statistical analysis

We calculated the percent of patients who received the individual outcomes of BMD testing, calcium, vitamin D, and antiresorptives or anabolics. We determined the proportions of patients in each denominator (FORMAL and ALL STEROID) who received care consistent with each QI. We used bivariate analyses and multiple logistic regression to assess the association between baseline characteristics and the QI outcomes. Variables in the multivariate models were determined a-priori based on prior studies of osteoporosis care and included age, ethnicity, income, education, health insurance, disease duration, disease activity, daily pill burden, and the specialty of the main SLE physician.30,31 All covariates were tested to ensure non-collinearity. In the models for the FORMAL denominator, some of the covariate categories were collapsed because of the small number of events. SAS 9.2 (Cary, NC) was used for all analyses.


We analyzed data from 742 subjects from wave 6 of the LOS. Of these, 127 met eligibility criteria for the FORMAL denominator for QIs I (Screening) and II (Calcium and Vitamin D), and 91 for the FORMAL denominator for QI III (Treatment). Four hundred and twenty seven met criteria for the ALL STEROID denominator for QIs I (Screening) and II (Calcium and Vitamin D), and 224 for the ALL STEROID denominator for QI III (Treatment). Baseline characteristics of individuals meeting eligibility criteria for each denominator are listed in Table 2.

Table 2
Baseline characteristics of individuals from the UCSF Lupus Outcomes Study in the FORMAL and ALL STEROID denominators for quality indicators I, II, and III.

Figure 1 shows the proportion of eligible patients receiving care consistent with each of the quality indicators for the 2 denominators of interest (FORMAL and ALL STEROID, see Table 1). The proportion of patients receiving the care described in the QIs ranged from 54 to 74% and was slightly higher in the FORMAL group compared with the ALL STEROID group. Of note, when we assessed QI III (Treatment) among men and post-menopausal women only, the proportions of patients receiving care per the QI were essentially unchanged at 57% for the FORMAL denominator (n = 56) and 54% in the ALL STEROID denominator(n = 137).

Figure 1
The x-axis is marked by the quality indicators I, II, and III for the FORMAL and ALL STEROID denominators. a: Patients taking at least 7.5 mg of prednisone per day for at least 3 months. b: Patients taking at least 7.5 mg of prednisone per day for at ...

In the bivariate analyses (unadjusted) of the FORMAL denominator patients, receipt of QI I (Screening) was predicted by age, Caucasian race, and disease duration (see Table 3). The multivariate (adjusted) model showed only older age as predicting QI I (Screening) receipt (per 10 years OR 1.9, 95% CI 1.2, 3.1). Multivariate analysis for QI II (Calcium and Vitamin D) in the FORMAL denominator showed a significant predictor to be Caucasian race (OR 4.3, 95% CI 1.9, 9.6). The multivariate model for QI III (Treatment) did not reveal any significant predictors.

Table 3
Logistic regression model predicting receipt of care consistent with osteoporosis-related quality indicators for patients in the UCSF Lupus Outcomes Study (FORMAL denominator)

The sensitivity analysis using the ALL STEROID denominator revealed slightly different predictors of receiving care as per the QIs. Multivariate (adjusted) analysis showed female sex (OR 2.8, 95% CI 1.3, 5.9), older age (per 10 years OR 1.3, 95% CI 1.1, 1.6), longer disease duration (per 10 years OR 1.5, 95% CI 1.1, 2.1), and rheumatologist subspecialty care (OR 1.8, 95% CI 1.1, 3.1) to be significant predictors for the receipt of QI I (Screening) (see Table 4). Female sex predicted the receipt of QI II (Calcium and Vitamin D) (OR 2.6, 95% CI 1.2, 5.5). Having a rheumatologist as the main SLE physician predicted receipt of QI III (Treatment) (OR 2.3, 95% CI 1.3, 4.6).

Table 4
Logistic regression model predicting receipt of care consistent with osteoporosis-related quality indicators for patients in the UCSF Lupus Outcomes Study taking any dose of glucocorticoid (ALL STEROID denominator)


This study examined the screening, prophylaxis, and treatment of osteoporosis in a large, community-based cohort of patients with physician-confirmed SLE. Regardless of whether we used lenient or strict definitions to delineate the patient populations eligible for relevant processes of care, the proportion of patients receiving these interventions was similar. Screening for osteoporosis with a BMD test occurred more frequently (69–74%) than calcium and vitamin D use (56–58%), or antiresorptive or anabolic use (54–56%), even when the QI III (Treatment) analysis was restricted to men and post-menopausal women (54–57%). We conclude that osteoporosis screening, prophylaxis, and treatment for SLE patients is suboptimal.

Our results show slightly higher proportions of patients receiving bone health-related care compared with prior estimates. Lee et al. surveyed US women with SLE seen in an academic rheumatology practice. In that study of 204 women, 50% reported calcium use and approximately 45% reported vitamin D use; 62% were post-menopausal, and 50% were currently using glucocorticoids. 32 In our sample, with a comparable fraction of post-menopausal women and patients on glucocorticoids, 62% of patients reported calcium use and 55% reported vitamin D use. Almehed et al. studied 163 women with SLE in Sweden, again with similar fractions of post-menopausal patients and steroid users: 53% of these patients reported taking calcium and vitamin D.4 Only 35% of patients with documented osteoporosis were taking bisphosphonates. In our sample, 47% of patients with documented osteoporosis were taking antiresorptive or anabolic agents. Pineau et al. examined a clinical database to show that that 40% of female SLE patients from the University of Toronto Lupus Clinic received a BMD test over a 5 year period. 33 Our sample showed that 51% of patients reported receiving a BMD test within 2 years. Self-reported use of DXA scans has been shown to have a very high positive predictive value when compared with medical chart review.34 One possible explanation for these discrepancies is that over time, awareness of osteoporosis has increased, and patients and their physicians are taking more care to perform screening, prevention, and treatment. Alternately, these differences may be a result of dissimilarities in health care system factors or the demographics of the populations studied.

We found that the major predictors of receipt of care varied by quality indicator and by denominator. Important factors predicting higher quality care included female sex, older age, Caucasian race, and longer disease duration, although these were not predictive for the receipt of all QIs. Notably, in the model that examined the FORMAL denominator, the only predictive factors were older age (QI I (Screening) only) and Caucasian race (QI II (Calcium and Vitamin D) only).

Our findings regarding predictors of care are not surprising: post-menopausal women without SLE have an indication for BMD testing and osteoporosis prophylaxis.35 In addition, our results are consistent with previous studies: Pineau et al. report that SLE patients who were referred for BMD testing had a greater number of traditional risk factors for osteoporosis, higher SLE activity, renal involvement, increased damage, higher mean glucocorticoid dose, increased use of immunosuppressants, and presence of avascular necrosis.33 In studies of osteoporosis care in patients with rheumatoid arthritis (RA), predictors have been similar. Aizer et al. assessed predictors of BMD testing among 2717 RA patients entering the CORRONA database without a prior dual energyX-ray absorptiometry (DXA) scan: older age, female sex, history of fracture, and history of steroid use predicted BMD testing within 12 months of entering the study.36 Solomon et al. evaluated osteoporosis care in 236 RA patients taking oral glucocorticoids: rates of BMD testing were low (23%), as were calcium and vitamin D use (42%). 37 Predictors of care included female sex, post-menopausal status, and having no additional comorbidities. Although these studies did not find as association of racial/ethnic groups with quality care, studies of quality indicators for cardiovascular disease, stroke and TIA, and diabetes have found such racial disparities.38,39 The fact that we found few predictors of care may indicate that we were limited in our power to detect differences; however, it is important to note that receipt of the QIs was low overall.

Our results must be interpreted with several caveats. First, data for the LOS, including data used for definitions of the numerators and denominators for the quality indicators, were collected by self-report. There is support in the literature for the validity of self-report for fragility fractures and osteoporosis diagnoses, as well as for BMD testing and medication use, including calcium and vitamin D: The sensitivity and specificity of self-report for documented hip fracture has been found to be very high.40,41 Agreement between self-report and medical record for the diagnosis of osteoporosis appears to be lower, but “false positive” self-reported diagnoses of osteoporosis arerare.42 Self-reported use of DXA scans has a 93% positive predictive value for DXA documented in the medical record. 34 The concordance of self-report for medication use (including calcium and vitamin D use) with medical record or administrative claims data is variable.43,44,45 However, several studies have shown substantial agreement between patient interview and medical records as sources of information regarding medication use and suggest that the impact of possible misclassification on models that predict medication use is minimal.,46,47 Overall, these studies show that the validity self-report for bone-health related care is reasonable, and therefore our results are likely reliable.

Second, few (127) patients met criteria for the formal QI denominators. We may have been underpowered to detect differences in rates of QI receipt among different subgroups of patients in this group. Third, quality indicators are process measures designed to be assessed on physicians or health-care systems and are intended to account for patient refusal of a measure or contraindications to a drug. We do not have information on reasons for drug non-use or contraindications (other than pre-menopausal status) available in this study, so it is possible that some patients were intolerant or otherwise ineligible to take calcium, vitamin D, or antiresorptives/anabolics. In this case, we may be underestimating the proportion of patients receiving care consistent with the quality indicators.

Based on the low receipt of the 3 bone-health-related SLE quality indicators, we have established that there exists a gap between actual and minimally-acceptable care. Quality-improvement efforts should address osteoporosis prevention and treatment among all SLE patients, especially in those taking high-dose, prolonged steroids. Educational initiatives highlighting the SLE quality indicators to SLE patients and their providers will likely improve the rates of quality bone health-related care in these populations.


Funding: ACR/REF Physician-Scientist Development Award, National Center for Research Resources, Grant Number: 5-M01-RR-00079, Rosalind Russell Medical Research Center for Arthritis, NIH (Grant Number: R01-AR-44804), State of California Lupus Fund, Arthritis Foundation, Agency for Healthcare Research and Quality, National Institute of Arthritis and Musculoskeletal and Skin Diseases (Grant Number: 1-R01-HS-013893, P60-AR-053308)


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