Integrated approaches to screening
Screening for HIV has been a key strategy for HIV programs to improve case-finding aimed at ensuring 90% of PLHIV know their status by 2020 . Case-finding has taken on many forms including facility-based, community-based, and home-based screening .
Community-based integrated HIV and noncommunicable disease screening and referral
Expanding on existing community-based screening programs, this model provides a multidisease screening package for HIV and NCDs in the general population. Human resources employed in various capacities such as community mobilization, logistics coordination, testing, and counseling is required, with the addition of screening kits for rapid testing in the field [15,17,25–31].
Case Study 1: Leveraging community-based HIV testing campaigns for noncommunicable diseases in Uganda
Chamie et al. evaluated the feasibility and diagnostic yield of integrating community-based HIV and NCD screening and referral in three well known community locations in a rural district. Local village governments were engaged prior to the campaign to plan for community mobilization, disseminate information, and maximize participation. Local healthcare workers trained and experienced in HIV counseling and testing conducted multidisease screenings for HIV, hypertension (HTN), and diabetes mellitus (DM) and held questionnaire-based interviews with community members. Patients screened positive for any disease were referred to nearby public health facilities. Most testing was done in the field using POC equipment while a central lab provided support for tuberculosis (TB) testing.
NCD screening required the addition of a point-of-care (POC) screening device for random blood glucose measurement and blood pressure machines with varying sized cuffs. The associated incremental cost of this was $2.41 per participant, onto a base cost of $26.69.
Among adults living in the catchment area, 74% participated with more of the female population (95%) reached compared with males (52%). Researchers found that 46% of patients who screened positive for HIV were newly diagnosed, while 65 and 23% of patients screened positive for HTN and DM, respectively, were newly diagnosed.
A key challenge was referral to different centers for care of HIV and NCDs because NCD care was only available at a center ∼20 km away. Overall, a quarter of the target population did not take part in the screening campaign. Despite a high-throughput design, participants spent a median of 95 min at the campaign, longer for HIV-infected participants, which may have deterred participation. Linkage to care within 3 months was higher for NCDs but still suboptimal, at 39, 43, and 61% for HIV, HTN, and DM patients respectively. A follow-up study among patients diagnosed with HTN included an intervention package (short counseling session after diagnosis, referral appointment within 30 days, and one-way transport cost facilitation) resulting in 83% linkage to care . Tracing of patients not linking within 6 months revealed that the asymptomatic nature of HTN, as well as transport cost and inconvenience were significant barriers to linkage.
Screening for noncommunicable diseases and noncommunicable disease risk factors among people living with HIV at health facilities
Leveraging established HIV clinic infrastructure, this model targets PLHIV engaged in care and screens them for NCDs and NCD risk factors, tackling the problem of dual HIV/NCD burden [16–18,32–40].
Case study 2: Screening for noncommunicable diseases and their risk factors in people living with HIV enrolled in care in Tanzania
Kagaruki et al. evaluated the magnitude and risk factors of DM and HTN among PLHIV in two Tanzania regions (one rural and one urban). They screened PLHIV in 12 HIV care and treatment centrers (CTCs) for DM, HTN, and NCD risk factors such as high low-density lipoprotein (LDL), low high-density lipoprotein (HDL), suboptimal intake of fruits and vegetables, lack of participation in vigorous activity, body mass index 25 kg/m2 at least and abnormal waist circumference. Screening utilized a structured tool adopted from the WHO STEPs survey available in both English and the local language . Qualified medical personnel were responsible for data collection, anthropometric measurements, and blood sample collection, following a 3-day training.
Of the 671 PLHIV participants, HTN and DM was prevalent in 26.0 and 4.2%, respectively. Prevalence of NCD risk factors were low HDL (72%), suboptimal fruit and vegetable consumption (70%), poor participation in vigorous activity (48%), abnormal waist circumference (47%), and high LDL (43%). All patients received health education based on their screening findings and a paper copy of their results. For patients with NCDs or NCD risk factors, study personnel communicated their information to the patient's specific CTC for further workup and management.
Key challenges were failure to return for drawing of fasting blood samples despite assurance of compensation for transport, and low participation by male PLHIV (30%) and ART-naive PLHIV (47%) in the NCD screening who cited lack of time to participate. Linkage-to-care rates and follow-up clinical outcomes for PLHIV with NCDs or NCD risk factors were unavailable as this was a research study.
Integrated approaches to care of HIV/noncommunicable disease patients
External funding for NCD care in LMICs remains low, estimated at 1.3% of total development assistance for health in 2015 . Given the large investment in HIV care in SSA, leveraging HIV infrastructure represents a key opportunity to provide NCD care to large populations without needing to replicate health service streams. We identified several examples of integrated HIV and NCD screening, treatment, and follow-up, which we divided into two distinct models: integrated HIV and NCD care within chronic disease care  and HIV care  clinics, and differentiated care for stable HIV and/or NCD patients in medication adherence clubs .
Case Study 3: Leveraging HIV platforms to work toward comprehensive primary care in Malawi
Wroe et al. described the implementation of decentralized integrated chronic care clinics (IC3) in rural Malawi where patients with HIV and/or NCDs receive care for chronic disease . The IC3 model follows the original patient flow designed for HIV care beginning with screening (both community-based and facility-based) and referral for follow-up of any and all chronic conditions. Patients receive education on common conditions before seeing clinicians trained in managing HIV and/or NCDs. Finally, patients collect their medicines and are assigned a new appointment date. Defaulter tracing occurs for patients lost to follow-up using protocols originally designed for PLHIV.
In the district where the effort was described, 7100 PLHIV received decentralized HIV care across two hospitals and 11 health centers. Prior to IC3, only two centers provided NCD care with limited success, including a high loss to follow-up rate related to patients either having to travel long distances for NCD care or requiring different clinic visits for patients with co-morbid HIV/NCD. In response, IC3 was launched and decentralized to all 13 facilities in the district. To overcome human resource constraints, existing HIV-trained personnel were converted into integrated chronic disease management providers through classroom training and continuous on-the-job mentorship and supervision on NCD screening and treatment. Patient data management was re-designed for more comprehensive and integrated data collection via creation of master files for each patient that held all information instead of having multiple files on the different disease states.
A clear patient flow system was a key element in ensuring enhanced efficiency in the IC3 without imposing significant increases in workload for the care providers. An assessment of each health worker's role in the IC3 identified a straining workload on the nurses, which was solved through task re-distribution to improve efficiency (Dr Emily Wroe, personal communication, 2017) .
As of May 2015, 6781 patients on ART and 721 patients with NCDs (HTN, DM, epilepsy, or asthma) were receiving care in IC3. Among the NCD patients, 109 (15%) were PLHIV. Medications were provided free of charge which necessitated additional funding for NCD drugs to be provided by the implementing partner. Although clinical outcomes are yet to be described, a detailed toolkit for implementers of integrated HIV/NCD care is available online [43,44].
Additional experience in integrated HIV/NCD care comes from Patel et al. who described an effort to integrate HTN management at the Lighthouse Trust HIV service delivery sites in Malawi using a health system strengthening approach  utilizing evidence-based tools and practices, and continuous training of healthcare workers to improve clinical outcomes. An HTN-specific electronic medical record module was designed for monitoring and evaluation of both clinical and programmatic outcomes. A phased approach was used to implement HTN screening to ensure that clinic wait times and staff workload were not increased. At 12 months, of 29 359 individuals screened, 11% were newly diagnosed with HTN, and 85% of those with hypertension received treatment per standardized protocols. Among persons with mild and moderate HTN, blood pressure (BP) control rates were 38 and 30% after 6 months of treatment, respectively. Notably, adherence to ART was not affected by the additional burden of antihypertensive medications. Cost-effectiveness analyses are underway. The main challenge to scale-up of this program was noted as variability in accessibility and availability of antihypertensive medications because Malawi experiences frequent stockouts.
Integration of differentiated care for HIV/noncommunicable disease
Differentiated care is care delivery that is customized to the individual patient's needs  allowing for longer periods between clinic follow-up among stable HIV patients, leading to a reduced burden on both the patient and care provider. The benefits of differentiated care for PLHIV can be extended to HIV/NCD integrated care as demonstrated by the following case study.
Case study 4: Differentiated care for HIV/noncommunicable diseases in Kenya
Khabala et al. described an integrated model encompassing principles of differentiated care for patients with HIV, HTN or DM in a low-income population in Kenya. Groups of 25–35 stable patients with HIV, HTN and/or DM were established. To be eligible to join, HTN and DM patients had to be at least 25 years of age, been on medications more than 6 months, and have a BP less than 150/100 and/or HbA1C less than 8%. PLHIV had to be at least 25 years of age, on ART for more than 1 year, have an undetectable viral load, a CD4 count more than 200, and not be in active WHO Stage 3/4 disease. Patients were informed that groups would have a mix of HIV and NCD patients but disclosure of their disease state was voluntary. The groups met quarterly in a dedicated space at the health center for a nurse-led session of approximately 2 h where they were assessed for clinical stability and received health education and drug refills. Usual clinic follow-up would occur annually, if a patient developed complications, or if they no longer met above stability criteria.
Over 1 year, 1432 patients across 47 MACs had 109 meetings and 2208 consultations (nurse-led weight and BP assessment, and ordering of routine blood tests). There was high adherence (99%) to recommended BP checks, weight checks, and blood tests by the nurse, with an overall low loss to follow-up (3.5%) or need for referral back to a clinic (2%) among members. Clinical outcomes are yet to be described.
Integrated comprehensive care for all
Early experiences with providing HIV care identified significant socioeconomic determinants of health in PLHIV in low-income settings such as food insecurity and undernutrition, and cost and logistical barriers to chronic care [47,48]. Similar determinants affect outcomes in NCDs and may be more important as few programs fully fund NCD care, often requiring user-fees for diagnostic tests, consultations, and drug purchases . A population health model that builds on the HIV care infrastructure and lessons learned potentially represents the apex of integrated care .
Case Study 5: Delivering population health in Western Kenya
In Western Kenya, care of PLHIV has provided important experiences in delivering chronic care to SSA populations [41,50]. Several principles learned from these experiences have been leveraged and adapted to deliver NCD care : home-based and community-based screening to improve NCD case-finding , task-shifting and decentralizing chronic care delivery to improve linkage and retention [50,52,53], using portable electronic medical records to streamline documentation [54,55], backing-up the Ministry of Health (MOH) medicines supply chain to ensure consistent availability , integrating income-generation and microfinance activities into care delivery to address socioeconomic barriers to health [20,52], and provision of affordable health insurance to minimize out-of-pocket costs .
A population health model grounded on the above principles has been developed to provide decentralized comprehensive care, including HIV/NCD, to the smallest administrative unit of the population (village) via community groups. These groups double both as convenient healthcare delivery points where clinical staff provide a variety of services, and as microfinance groups that provide low-interest loans and financial advice to members . Collaboration with the Kenyan National Hospital Insurance Fund (NHIF) ensures that healthcare costs remain affordable to the majority of the population as enrollees are only required to make a monthly contribution of ∼$5/month. Revolving fund pharmacies (RFPs) which utilize money collected from drug sales to cover drug re-stocking, have been established to protect against drug stock outs in government facilities , and a referral network has been built for patients who need to see higher cadres of staff. Clinical and process outcomes for the population health model are yet to be described.
Designing a responsive continuity of care model for HIV provides vital lessons that can be leveraged to address the growing NCD burden that threatens aging PLHIV and the general SSA population [7,57,58]. HIV/NCD care integration is a feasible approach to health system strengthening in SSA, and the case studies described above demonstrate a variety of HIV/NCD integration models which programs can adopt and adapt based on available resources, needs and priorities. Several common themes from the reviewed models are worth highlighting, with lessons learned and prevailing research gaps summarized in Table 2[15–22].
Leveraging existing human resources is a key strategy to address shortfalls in human resources for health (HRH)  and was a common theme across our reviewed models. Use of existing medical personnel to conduct HIV/NCD screening and referral minimized training needs [15,16], task redistribution streamlined integrated HIV/NCD care delivery [17,19], and continued training and mentorship enabled transformation of HIV care providers into integrated chronic care providers to address staff shortages . As SSA countries grapple with addressing the emerging NCD threat, a key intervention to consider is the creation of curricula to produce integrated chronic care providers instead of specific staff dedicated only to HIV or NCD roles .
Integrated HIV/NCD screening and NCD screening among PLHIV while feasible, required linkage and retention in care to reap the full benefits of early diagnosis. Linkage to care was poor following the community based integrated screening campaign described above but was noted to be higher in patients with NCDs compared to HIV . Whilst sensitization on the need for care among diagnosed patients following screening may improve linkage , decentralized, integrated HIV/NCD care, particularly in remote areas, enhances the benefits of screening programs through linkage and retention . In Kenya, integrated HIV/NCD care resulted in high retention rates  and was implemented to curb a high loss to follow-up associated with seeking care in distant facilities in Malawi . Decentralization aims to bring care closer to patients to minimize logistical barriers to access, while reducing congestion at ‘central’ health facilities .
Streamlining service delivery is an important strategy in optimizing patient-centered care  and was key to delivering decentralized integrated care. This was made possible by clarifying individual health worker roles to promote staff buy-in, identify systemic challenges, and reduce strife among workers . In addition, use of integrated files and health information technology tools minimized data management redundancies and improved efficiency, while providing a platform for monitoring patient and program progress [44,55]. Integrated MAC groups decentralized care by leveraging differentiated HIV care aspects [47,61] to provide flexible follow-up and medication refills to stable HIV and/or NCD patients, leading to improved patient satisfaction and decreasing the burden on the health system .
Public-private partnerships (PPP) between government agencies, health ministries, nongovernmental agencies (NGOs), federal programs, and academic partners were crucial to the success of integrated HIV/NCD models. Engagement with local government ensured community health needs were met to improve participation in a multidisease screening campaign in Uganda  while NGOs augmented government efforts through supplemental funding for personnel and NCD medication in Malawi and Kenya to ensure uninterrupted care [17,56]. Indeed, reviewed case studies all relied on a HIV platform established through PPP, to deliver integrated screening and/or care. Beyond ensuring interventions meet specific population health needs and facilitating implementation within existing regulatory frameworks, PPP are crucial in promoting sustainability of donor funded programs beyond funding cycles by incorporating successful programs into health policy .
Designing patient-centered quality care results in a higher likelihood of patient uptake and was a common theme in the reviewed models. Holding screening campaigns in three popular community locations improved participation in Uganda  while decentralized care and efficient clinic patient flow systems aimed to address logistical barriers for patients seeking HIV/NCD care in Malawi . Integrated MAC group meetings in Kenya utilized flexible timing to improve patient convenience , and microfinance groups were established to address economic barriers to access and incentivize retention in care [20,52]. Delivering quality chronic care to low-income populations with limited capacity to pay remains a significant global health challenge . Several programs have overcome this by providing HIV and/or NCD care free of charge to patients . However, long-term sustainability of this model of service delivery remains a concern. Imposing user-fees for care services and medicines may promote sustainability but represents a significant barrier to sustained access in low-income populations [64,65]. Microfinance groups, income-generation programs and low-cost health insurance are several programs underway in Western Kenya to minimize the economic impact of receiving NCD care, for which, unlike HIV care, patients often pay out-of-pocket [49,50,52]. Ultimately, countrywide adoption of universal healthcare coverage, which has been on the SSA agenda since the late 1970s [49,66,67], is needed.
Our review has several limitations. First, it was not systematic as we aimed to describe existing models of HIV/NCD care integration, adopting a wide search strategy that was not amenable to the narrow research question requirements of a systematic review. Second, although we attempted to make contact with author leads of the case studies, we were unable to conduct interviews with all of them, possibly missing out on recent updates regarding available models. Third, case study descriptions only highlight key components in relation to HIV/NCD integration as described in the retrieved literature and author interviews and may miss out on other key programmatic aspects. Therefore, the summary here is a reflection of current efforts and may not capture ongoing HIV and/or NCD care activities that have not been published. In addition, overlap exists across the care cascade and extends to the described case studies, description of program activities under a specific model is meant only to highlight key components of the integration model, and not to imply that these are the only components of integration within the program. Finally, our review was primarily confined to discussing different typologies of HIV/NCD integration, rather than how such models are taken to scale . Further research is warranted to determine how and where these models can be implemented successfully.
Nevertheless, our review illustrates that HIV/NCD care integration in SSA is feasible, with several models available that country programs can adopt and adapt based on available resources, needs, and priorities. Integration models are in their infancy, as exemplified by the general lack of clinical and process outcomes data, and a lack of cost-effectiveness data from the various models. These are urgently required to further inform implementers and policy makers as SSA continues to strengthen its health system in order to cope with the emerging health and economic threat posed by NCDs [58,69,70].
Leveraging the existing HIV infrastructure to provide NCD care to the SSA population is feasible. Several models of care integration have been described in SSA with important lessons that will aid context-specific replication in other SSA settings. Future efforts will need to factor in descriptions of process metrics and cost-effectiveness to further guide implementation, as well as clinical outcomes to aid decision makers.
All authors were involved in the conception and design of this review. B.N., S.V. and S.P. drafted the original manuscript. All authors critically reviewed and edited the first draft and each successive version and provided final approval for submission.
Source of support: this article as part of the Research to Guide Practice: Enhancing HIV/AIDS Platform to Address Non-Communicable Diseases in sub-Saharan Africa was supported by the U.S. National Institutes of Health Fogarty International Center.
Conflicts of interest
The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the funding agencies.
All authors have no conflicts of interest to disclose.
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Keywords:Copyright © 2018 Wolters Kluwer Health, Inc.
HIV; integration; noncommunicable; service delivery