The study included 13 healthcare providers, comprising 7 doctors and 6 nurses, from four cities in China. Participants’ ages ranged from their 20 s to 50+, with most being over 30 years old. The doctors held medical degrees (MD) and specialized primarily in infectious disease and HIV care, with their experience working with people living with HIV (PLWH) ranging from 2 to 20 years. Among the nurses, who were Registered Nurses (RN), their experience varied from 3 to 12 years in nursing, with some specializing in HIV care. The positions of the participants included both junior and senior staff, with several in leadership roles such as department chair and charge nurse, reflecting a range of expertise and perspectives in HIV care (Table 1).
Based on 13 interviews with providers from four HIV clinics across different care settings in four cities, nine subthemes emerged (Table 2) to characterize the opportunities, challenges, and aspirations by front-line HIV care providers in China for osteoporosis and fracture prevention and broader bone health promotion. Briefly, HIV care in China has been gradually shifting to a comprehensive model, with increased awareness of age-related comorbidities. Providers reported limited programming on bone health screening and prevention, but the current longitudinal patient-provider relationship model allows for program development in comprehensive comorbidity care. Providers and patients face challenges in bone care due to limited time and energy. Access to appropriate screening modalities, such as DXA, remains a major barrier, with providers considering alternative options like QUS and screening questionnaires to identify high risk patients. Additionally, program expansion for bone health is limited by financial resources, as comorbidities not directly linked to HIV infection receives less priority and funding than others. Finally, HIV providers in China hope for the development of evidence-based, population-specific clinical guidelines, accessible provider education, and improved sub-specialty collaborations and referral networks to facilitate bone health promotion for patients with HIV.
Theme 1 opportunities
Increased awareness of age-related comorbidities in overall HIV care
Clinicians from various HIV clinics across the country reported that HIV care has shifted from an acute, infectious disease-guided model to a comprehensive multi-system screening and management model. Providers agreed that this transition to a chronic disease model of care has many challenges: testing, counseling, and treatment for aging-related comorbidities often requires sub-specialty expertise. In practice, these changes were largely driven by coverage of aging-related comorbidities screening under the National Free Antiretroviral Therapy Program, which made it possible for HIV clinics to streamline comorbidity screening into regular ART follow-ups. As a result, co-morbidities that could be monitored with routine blood tests, such as those of the cardiovascular, hepatic and renal systems, receive more attention than others. While in more urban areas providers witnessed an increase in patient-initiated inquiries about some aging-related comorbidities, other providers perceived that many of their patients had limited understanding and concern regarding the screening and prevention of comorbidities. They observed that PLWH with the most pressing need for care in aging-related comorbidities were the hardest to reach due to lower health literacy, more prevalent apprehension of social judgement, and lack of resources to engage in care.
I think that cardiovascular disease is the most obvious among the comorbidities. Hypertension is easily observed because we take blood pressure every time, which can yield immediate results. Kidney-related issues are also common comorbidities, although their incidence is not as high. Additionally, we pay attention to the cognitive aspect. If patients themselves report a decline in their memory, we will be concerned. [PUMCH RN2]
With the emergence of some chronic diseases in patients, including aging, decreased bone density after medication, and the presence of hypertension and diabetes, some patients may experience cardiovascular emergencies such as stroke. The management of these chronic diseases is actually a huge challenge for us, especially with many of our patients being migrant workers. Some of them pick up their medications here but frequently go back their hometown or go to work in other places. [Shenzhen RN2]
Limited programming on bone health screening and prevention
Providers concurred that there was currently limited programming on bone loss prevention and osteoporosis screening when compared to other aging-related comorbidities. They attributed this uneven attention to the insidious onset of bone loss, described as “a double-edge sword”: while actionable items for primary and secondary prevention existed and could be extremely cost-effective, the lack of immediate life-threatening urgency meant it received less attention and thus less resources. The current standard of care for bone health varied across HIV clinics. In more resource-limited regions, clinicians reported bone health was only considered when patients presented with fractures, which were largely thought to be secondary to trauma or chronic steroid use, and oftentimes did not prompt further investigation into underlying etiology. On the other hand, providers in tertiary hospitals reported initially focusing on bone health only for patients treated with high dose steroids or other agents with known deleterious bone effects such as tenofovir disoproxil. More recently, however, a wider range of bone-related risk factors have come to their attention after bone density screening was added to routine comorbidity assessment algorithms. These clinics aspired to deliver compressive care but recognized that the lack of clear algorithms for prevention, screening, and treatment services for bone disease in HIV leads to incongruencies and inefficiencies for patients and providers.
I feel that bone density testing is out of touch with reality because we have to wait for the data to come back, have the students enter it into the system, and then the doctors can see it, which is very delayed. In terms of bone quality, I think people are more concerned about patients who have clear bone loss, [compared to] those who may have done many tests but still haven’t reached the threshold for intervention. For these patients, it’s unclear what advice to give. If [the patients] don’t need the advice, it feels like asking them to do a bone density test is just going through the motions. [PUMCH RN2]
Longitudinal patient-provider relationship allows comprehensive comorbidity care
Providers interviewed across the country described their current clinic structure. With minor variations, all clinics adopted standardized care protocols and return schedules for newly diagnosed patients to establish care. Initial visits took place weekly to biweekly to evaluate baseline CD4 count, viral load, and drug-resistance and initiate ART. Subsequently, patients with a stable ART regimen returned for follow up every three to six months with routine bloodwork. Clinics offered comorbidity screening test such as liver and kidney function test, echocardiogram, carotid ultrasound, chest X-ray, and bone density testing at varied intervals, driven by clinic protocols, insurance coverage, and research and/or local health administration funding sources.
Continuity of care was identified as the major advantage of the current clinic structure by healthcare professionals across all clinics. The same teams followed the patients over time, building trusted therapeutic relationships with patients carrying a diagnosis that remains heavily stigmatized in society. United by a common goal and commitment, physicians and nurses in these clinics collaborated closely and frequently assumed supplementary roles as social workers and care coordinators beyond delivering clinical care. They had found that this unique relationship helps them tailor care by recognizing and addressing psychological concerns (e.g. support networks, employment discrimination) and barriers to care (e.g. insurance coverage, medication access). This in turn facilitates patient engagement, particularly in patients with lower health literacy and for easily overlooked health concerns such as prevention and screening of comorbidities. Aided by electronic medical record systems that track longitudinal comorbidity screening data, most providers reported feeling well positioned to provide comprehensive comorbidity care under the current clinic structure.
One characteristic of our clinic is that the healthcare providers who prescribe the medications are the same ones who follow the patients. This is very important. Our outpatient clinic has fixed teams of doctors and nurses. Once a patient comes to a doctor’s clinic, they will continue to follow up with that same doctor for all subsequent visits. Therefore, our doctors here have abilities to see the comprehensive picture and provide consistent care. [PUMCH RN1]
Team collaboration is essential for everything. Our medical records have a colored label attached to them, serving as reminders such as if the patient has poor medication adherence. Although their viral load may not be a problem at the moment, they have adherence issues already, and this is what we need to follow up on. As soon as the medical record is reviewed and there is a colored label, we know to pay attention to this patient. Whether you or I handle the case, we always take the time to review the medical records. [Liuzhou RN1]
Theme 2 challenges
Limited time and energy of both providers and patients
Providers interviewed expressed hope to spend more time with each of their patients, as they sometimes felt their quality of care was limited by the large volume of patients scheduled on each clinic day. Physicians in one large clinic estimated their face-to-face time with each patient averaged between 1 and 5 min, making conversations on comorbidity screening and prevention difficult to fit in. A few clinics sought to mitigate this shortage by pairing clinicians with nurses or clinical assistants, who would spend additional time with patients to address barrier to care, screen for lifestyle interventions, as well as provide additional patient education. Some providers viewed this paired model as an opportunity to encourage more aging-related comorbidities care, dedicating time for targeted patient education on aging-related comorbidities and providing a window for survey- or bloodwork-based screening in the same physical space. However, most providers felt it would be challenging to incorporate any imaging-base screening into routine visits. Some clinics noted challenges in tracking, interpreting, and delivering results of comorbidity testing outside of clinic visits, as no clinician was assigned specifically for such tasks.
On the other hand, interviewed providers observed that patients had limited time and energy to dedicate to their HIV care. When routine follow-ups already posed interruptions to their daily activities, additional laboratory and imaging appointments for comorbidity screening, particularly those required traveling to off-site locations, could be perceived as nonessential and/or too onerous. One provider noted a significant portion of patients were dependent on family members to travel to appointments or accompany them for health literacy reasons, further limiting their ability to engage in complex care plans. Some clinics attempted to alleviate patient burden by integrating comorbidity surveillance and patient education into routine visits, however this resulted in lengthy visits and scheduling difficulties. Providers shared that some patients subjectively preferred to spend as little time as possible in HIV clinics to avoid being reminded of their HIV positive status, and others who preferred to keep their diagnosis private often had concerns about missing work for extended periods of time.
In fact, with our current level, it’s difficult to conduct a comprehensive assessment for patients, and we don’t have enough time and resources. For example, our cognitive assessment requires a very quiet environment and patients need to be in a very relaxed and comfortable state, but we can’t really provide that at the moment. So I think these issues are really related to the patient’s future treatment outcomes and quality of life. Nowadays, the international community also emphasizes the importance of improving patients’ quality of life, but I think there is still a long way to go to achieve this goal. It’s a difficult road ahead. [PUMCH RN1]
Barriers to DXA and openness to alternative screening modalities
With rising awareness of bone health, providers felt there was increasing clinical demand for assessment of bone mineral status to identify individuals living with HIV at increased risk of osteoporosis and fractures. For patients initiating ART, providers felt it would be particularly helpful to establish a baseline bone assessment to guide future monitoring and treatment. However, access to appropriate screening modalities remain a major barrier. Providers agreed that recommending baseline central dual-energy X-ray absorptiometry (DXA) screening at the lumbar spine and hip, the diagnostic gold standard for bone mineral density measurement, to all patients meeting criteria would be impractical. Standalone HIV clinics and clinics affiliated with infectious disease or community hospitals lacked both qualifying DXA machines as well as trained personnel to operate scanning protocols and interpret results. Traveling to an outside hospital would pose an additional barrier to care for patients oftentimes stigmatized in non-HIV care centers. Furthermore, hospital policies with regards to sharing or recognizing imaging results between institutions.
Certain sites that did not have access to central DXA had access to alternative modalities such as quantitative computed tomography, or peripheral DXA, which each have unique benefits and drawbacks. Quantitative ultrasound (QUS), a portable and noninvasive method of estimating bone mineral status at peripheral skeleton, was also introduced as part of the parent study to clinics interviewed in this study. Most providers considered ultrasound to be a safe, radiation-free, and established technique and were open to explore its use in evaluating bone health in their patients. Some providers appreciated its portability, cost-effectiveness and time-efficiency, making it a potentially feasible screening tool to integrate in routine clinic visits. At the same time, a few providers voiced concern about the operator-dependent nature of ultrasound and whether it might impact the accuracy of QUS assessment. In parallel with imaging modalities, providers expressed interest in primary prevention of bone disease. Most were open to adopting questionnaire-based assessments of modifiable behavior risk factors for fracture to guide primary prevention; however, they agreed that such survey must balance validated efficacy and ease of administration to fit into current clinic flow.
Ultrasound requires specialized training for the operator and involves some subjectivity and technical skills. However, I still think ultrasound has value as long as the data differences are not too large, and the evaluation accuracy within a certain range is acceptable. At most, there may be some differences in the accuracy of the evaluation, but it won’t classify bad evaluations as good or good evaluations as bad. [PUMCH MD1]
Program expansion limited by financial resources
Though first-line ART medications are exclusively covered by the National Free Antiretroviral Treatment Program, interviews with providers from HIV clinics in different care settings revealed vastly different financial resources available for comorbidity care. Research and program development for comorbidities in these clinics rely on funding from both national and local health agencies. Providers observed that comorbidities not directly linked to acute HIV infection receive less attention policy making and thus less funding. They reported that the patients accessed comorbidity care through a combination of national health insurance, commercial insurance, employer-provided insurance, and self-pay. When seeing patients have financial constraints, they too tended to prioritize access to antiretroviral medications over comorbidity screening. Providers in less developed areas perceived an unequal allocation of financial support between urban and rural regions, even though their patients relied more heavily on public funding in comparison to city residents. One clinic reported that recent provincial-level policy changes addressed this disparity by allowing migrant workers to access HIV care outside of their hometowns.
The national free subsidy requires everyone to use their own medical insurance, so unlike the medication, any of the [screening] tests [a patient] does may have a self-payment part. Because people living with HIV are from all walks of life, there is a substantial number of people who have financial difficulties. We have to cut back on the evaluation of comorbidities for some patients to meet their basic treatment needs. The main focus would be to monitor the viral load and T-cell subsets, and [the tests for] non-HIV related comorbidities are of relatively lower priority. Some non-HIV related comorbidities are more readily supported by [financial] resources than others. Treatment for active issues tend to be more supported than preventive care. [PUMCH RN2]
Theme 3 aspirations
Evidence-based, population-specific clinical guidelines
Providers felt access to evidence-based, population-specific clinical guidelines would lay the foundation to further program development in bone health promotion for patients with HIV in China. They reported that current national guidelines touched on osteoporosis under the broad umbrella of chronic comorbidities, however stopped short of making clinically applicable recommendations for every step along the care pathway, including prevention, screening, and treatment. Providers reported that when they encounter bone health questions in their clinical practice, they seek answers by referencing papers and guidelines from other countries, where care models and clinical scenarios could differ significantly. Thus, providers expressed a desire for guidelines that are evidence-based and population-specific, allowing them to provide high-quality bone care for patients in their clinic. Furthermore, some providers pointed out that an algorithmic approach would promote more widespread adoption of the recommendations, particularly in resource-limited settings where subspecialty expertise may not be easily accessible.
We are on the right track [to develop our own guideline], though significant gaps remain between our guidelines and those from other countries. The gaps may be due to our diagnostic technique and clinical practice differences, not because one guideline is right and the other is wrong. For example, we use different medication regimens because the medications available to us are different from first line [recommendation in foreign guidelines]. However, we still refer to their recommendations that are valuable for us, such as those for complex infections with multiple drug resistance. [Shenzhen MD1]
Accessible provider education
In addition to evidence-based, population specific clinical guidelines, providers interviewed in this study suggested that more readily accessible continuing education opportunities would constitute another foundational aspect of HIV care. Providers in tertiary hospitals/academic centers described their access to bone health-specific information in HIV was rather piecemeal, as the topic sometimes emerges in expert panels, guest speaker talks, or journal clubs. Providers from less developed areas reported more limited access to such opportunities and mostly relied on livestreamed talks or online provider forums or group chats. Topics that providers from all sites mentioned encountering frequently included ART regimen selection based upon bone health profile, interpretation of screening results, and interactions between bone health and other HIV-related non-communicable comorbidities such as cardiovascular health. When asked about preferred format for training, most providers indicated a preference for a small-group, interactive approach. They believed that in-person events would garner greater attendance and facilitate discussion and downstream action. Many providers also acknowledged that virtual events might offer logistical advantages and expressed openness to them.
For me, I would expect to receive more comprehensive and systematic training, including what medications patients can use, what adjustments in diet they should make based on their test results, whether or not they need medication, or if they need further testing, and what should the focus of their care be? All of these are step-by-step procedures. I feel that I am lacking in this area and I want to learn more about it. [Liuzhou MD1]
Sub-specialty collaborations & referral network
Finally, providers cited challenges with referrals to specialties, such as rheumatology, radiology, and orthopedic surgery, as another major barrier for facilitating bone care when their patients’ clinical needs exceeded their own expertise of infectious disease. They sometimes felt the need to be a “jack of all trades,” [Shenzhen MD1] in addition to being an infectious disease expert. Providers pointed out that current referral protocols and linkages were rather weak or nonexistent, and their clinics lacked follow-up strategies to determine whether patients completed referrals. While many clinics could attempt integration of HIV and non-communicable comorbidities screening into routine services, providers often are not equipped to provide specialized services when non-HIV related treatment is needed. As a results patients may need to be referred to specialists outside of the HIV clinic or healthcare system. Even in tertiary hospitals where patients have access to subspeciality expertise within the same healthcare system, referrals to non-infectious disease providers relied heavily on provider’s personal networks and word of mouth. They reported that other specialists frequently raised concerns about their own or their staff’s limited experience caring for patients with HIV. Less commonly, they expressed worries about the risk of HIV exposure for other patients due to inadequate universal precautions protocols. Providers described their aspirations for incorporating formalized, bidirectional referrals as part of their care pathways, which would in turn improve their capacity to screen and manage bone health.
In fact, these resources [for surgical referrals] are all obtained by our doctors through personal relationships such as our classmates or people we know socially. They might be more willing to give us the opportunity to perform surgeries [on our patients]. Most of the orthopedic doctors are willing to do surgeries for us because they have experience in providing care to HIV patients in Africa, so they are used to it and not afraid. However, the problem is that many of their assistants and nurses are unwilling to participate. Their operating rooms are available, but not everyone on the team is willing to do it. Currently, our [infectious disease] hospital is preparing to integrate an operating room for HIV patients, and when surgery is needed, we will invite outside experts to come and help us. [Fuzhou MD1]