A comparative impact evaluation of two human resource models for community-based active tuberculosis case finding in Ho Chi Minh City, Viet Nam

Background To achieve the WHO End TB Strategy targets, it is necessary to detect and treat more people with active TB early. Scale–up of active case finding (ACF) may be one strategy to achieve that goal. Given human resource constraints in the health systems of most high TB burden countries, volunteer community health workers (CHW) have been widely used to economically scale up TB ACF. However, more evidence is needed on the most cost-effective compensation models for these CHWs and their potential impact on case finding to inform optimal scale-up policies. Methods We conducted a two-year, controlled intervention study in 12 districts of Ho Chi Minh City, Viet Nam. We engaged CHWs as salaried employees (3 districts) or incentivized volunteers (3 districts) to conduct ACF among contacts of people with TB and urban priority groups. Eligible persons were asked to attend health services for radiographic screening and rapid molecular diagnosis or smear microscopy. Individuals diagnosed with TB were linked to appropriate care. Six districts providing routine NTP care served as control area. We evaluated additional cases notified and conducted comparative interrupted time series (ITS) analyses to assess the impact of ACF by human resource model on TB case notifications. Results We verbally screened 321,020 persons in the community, of whom 70,439 were eligible for testing and 1138 of them started TB treatment. ACF activities resulted in a + 15.9% [95% CI: + 15.0%, + 16.7%] rise in All Forms TB notifications in the intervention areas compared to control areas. The ITS analyses detected significant positive post-intervention trend differences in All Forms TB notification rates between the intervention and control areas (p = 0.001), as well as between the employee and volunteer human resource models (p = 0.021). Conclusions Both salaried and volunteer CHW human resource models demonstrated additionality in case notifications compared to routine case finding by the government TB program. The salaried employee CHW model achieved a greater impact on notifications and should be prioritized for scale-up, given sufficient resources.


Background
Globally, 1.6 million people die of tuberculosis (TB) annually and an estimated 10 million people develop TB disease each year [1]. Despite concerted efforts, incidence is currently declining at less than 2% per annum [2]. If this trend continues, TB elimination will not be achieved until the year 2182 [3]. As for all infectious diseases, early detection and cure of incident cases is crucial to decrease transmission and halt the epidemic. In endemic countries, National TB Control Programs (NTP) are responsible for providing TB care and prevention to the population. However, in routine NTP operations case finding entails receiving health-seeking patients with little effort on actively searching for new TB cases. As a consequence, there are 3 million annual incident TB cases globally whom these NTPs fail to reach. This "detection gap" sustains transmission and mortality [4]. One strategy to close the detection gap is active case finding (ACF) [5]. This has led to a global surge in ACF initiatives beyond routine household contact tracing [6,7]. These initiatives range from facility-based systematic screening to community-based interventions among vulnerable populations [8,9]. These initiatives have also shown that ACF can find more people with TB at an earlier stage of disease progression [10,11]. However, better evidence on impact and cost-effectiveness is needed if they are to be sustained through national public health policies and budgets [12].
A prerequisite for ending TB entails the optimal engagement of communities. Community engagement has long been recognized as a priority in health care [13,14] and the fight against TB [15,16]. Previously defined as "paraprofessionals or lay individuals with an in-depth understanding of the community culture and language" that "have received standardized job-related training of a shorter duration than health professionals" with the primary goal of providing "culturally appropriate health services to the community," [17] community health workers (CHW) comprise a critical component of community engagement [18]. When effectively engaged, CHWs can raise health system capacity through decentralization and task-shifting [19,20]. CHW's often also reduce access barriers for vulnerable populations, so that their services are considered more patient-centric than institutionally provided care [21]. As such, CHW's comprise an ideal group to implement ACF for TB in their communities. However, there remains substantial heterogeneity in the CHW models applied and gaps in understanding regarding their optimal means of engagement [17,22].
Under most applied models, CHW receive either a salary or an incentive-driven compensation. Oftentimes performance-based incentives (PBI) are additionally offered to reward high performers [23]. While salaried CHWs have been associated with increased motivation and reduced attrition [23], volunteer CHW models are often more attractive to authorities and implementers due to their lower fixed costs. Irrespective of payment model, a consistent recommendation is that financial compensation should be commensurate with occupational demands [18]. It has further been noted that CHWs are generally poor and dependent on the remuneration for their livelihood. For this reason, the World Health Organization (WHO) recommends to limit the dominance of PBIs as part of the overall compensation package [24]. However, it remains unclear whether a higher fixed payment is associated with improved performance and greater impact. The comparative effectiveness between salaried and volunteer CHWs was therefore identified as a key knowledge gap in need of further studies [25].
Between 2014 and 2016, a community-based ACF project named PROPER CARE was piloted in Go Vap district, Ho Chi Minh City (HCMC), Viet Nam. This project employed CHWs on a full-time basis with a commensurate salary for ACF and case management. Despite positive results [26], aspirations of other district health authorities to scale up this ACF initiative were stifled by the resource demands of these salaried CHWs. In response, we devised the IMPACT-TB study (Implementing proven community-based active TB case finding interventions). Its aim was to scale up the ACF activities piloted under the PROPER CARE project, to measure changes in TB case notifications resulting from these ACF activities, and to compare the relative changes in TB case notifications between ACF implemented by incentivized volunteers and salaried employees.

Study setting
The IMPACT-TB study was conducted in 12 of the 24 districts of HCMC ( Fig. 1)

Community health workers
A cadre of CHWs was recruited in each intervention district to implement ACF activities. These individuals were identified by district authorities among current community volunteers, retired health staff, civil society members, and former TB patients. Residency in the district for over 5 years was a prerequisite to ensure geographic familiarity. CHWs were recruited by the district health authorities for the duration of the study as salaried employees or incentivized volunteers based on the study district. In our study, salaried employees were defined as full-time staff for the duration of the study, who focused solely on the ACF activities and TB patient support. These employees received a salary equivalent to USD 136/month. Volunteers had permission to engage in other livelihood generation activities. They were provided a stipend of USD 23/month to support study objectives. Both groups received the same training, core responsibilities and PBI schemes.

Intervention
CHWs targeted household and close contacts of index cases, neighbors in proximity of an index case, and urban priority groups living in slum and boarding home settings (Supplemental Information, Figure S1). Index cases were prospective TB patients notified by the DTUs of the intervention districts. Household contacts were defined as people sharing a kitchen with an index case for one or more nights in the past 3 months. Close contacts were persons that interacted with an index patient at least once per month over the past 3 months. Proximity was defined as the same administrative neighborhood or in a 50 m catchment area around the residence of the index case [27]. We used United Nations Habitat definitions for slum households [28]. Boarding homes were defined as dormitories and single-room rental facilities. District authorities further helped to identify boarding home and urban poor communities for door-to-door screening. Household contact investigations consisted of an enumeration of all contacts and verbal symptom screening of those who were present at the time of the contact investigation. Screening of close contacts was conducted either via phone or pre-arranged meeting. To screen index case neighbors and urban priority groups, CHWs conducted door-to-door visits. A verbal symptom screen was administered using a standardized questionnaire in a custom-built app installed on an Android tablet (Supplemental information, Data sources & processing). The questionnaire asked about the presence and duration of the following symptoms: cough, hemoptysis, chest pain, dyspnea, fever, night sweats, fatigue, weight loss, and history of TB.
Although all household contacts were first verbally screened for TB symptoms, they were all referred for additional chest X-ray (CXR) screening irrespective of their clinical presentation. All other persons were referred for CXR screening if they reported any one of the aforementioned symptoms. Persons with parenchymal abnormalities on CXR were tested on the Xpert MTB/ RIF assay (Cepheid; Sunnyvale, CA, USA). Individuals who did not obtain a CXR or had a normal CXR but exhibited TB-related symptoms were tested using smear microscopy. Symptomatic persons with negative sputum test results were evaluated by the DTU and PNTH for clinical diagnosis in accordance to national treatment guidelines.
Persons accessing care received a transport stipend and fully subsidized CXR at the DTU or weekend community screening events. CHWs transported sputum samples for persons unable to reach the laboratories. TB patients with rifampicin-susceptible TB were linked to treatment at the DTU. This included CHWs assisting with enrollment formalities, including support to furnish proof of residency. Rifampicin-resistant TB patients were referred to PNTH for further evaluation and treatment. CHWs followed up patients before and after enrollment for counseling and psychosocial support.

Study population
The study population included all household contacts, as well as close contacts and urban priority groups with clinical symptoms for whom CHWs completed a verbal symptom screen. Screened persons that declined to participate were referred, but their information was excluded from the analysis.

Study outcomes
The primary outcome was the additionality in All Forms TB notifications in the intervention area. The secondary outcome was the difference in All Forms TB additionality between the two human resource models. We calculated additionality using the double-difference approach [29]. This approach calculates the additive effect of the pre−/post intervention difference in case notifications, plus the concurrent notification trend difference in a control area.

Statistical analyses
We described the TB care cascade [30] bifurcated by human resource model. We presented the doubledifference additionality for All Forms TB notifications and for TB patients with bacteriologic confirmation. To assess the validity of the double-difference additionality, we conducted comparative interrupted time series (ITS) analyses of aggregate monthly TB case notification rates in two iterations. The first iteration compared the intervention and control areas. The second iteration compared the two human resource models. The ITS analyses employed segmented methods (Supplemental Information, Figure S2) applied to marginal log-linear Poisson regression models using the generalized estimating equation (GEE) approach. We tested for serial autocorrelation using the Cumby-Huizinga test with a cutoff of p < 0.1 and specified the model based on the lowest quasi-likelihood information criterion values. Statistical analyses were performed on Stata version 13 (StataCorp; College Station, TX, USA). As a large proportion of the double-difference additionality derived from a decline in notifications the control area, we conducted a post-hoc comparative ITS analysis between the study's six control districts and eight non-study districts where no ACF had been conducted in the past 3 years (from a total of 12 non-study districts in HCMC). Hypothesis tests were two-sided and point estimates included 95% confidence intervals.

Ethical considerations
Ethical approvals were granted by the Pham Ngoc Thach Hospital Institutional Review Board and the Liverpool School of Tropical Medicine Research Ethics Committee. Study implementation was approved by the Ho Chi Minh City People's Committee. We obtained written informed consent from all participants and anonymized all patient data prior to analysis.

ACF outputs
The TB care cascade is shown in Table 1  While most indicators along the TB care cascade were similar between the human resource models, there were some notable differences. The number of individuals verbally screened by salaried employees (220,995) was 121% higher compared to volunteers (100,025). Conversely, the number of patients started on TB treatment in the salaried employee districts (510) was 19% lower than those started on treatment in the volunteer districts (628). As such, the NNS in for salaried employee districts (433) was 2.7 times higher than for volunteer districts (159).

Notification impact
Changes in TB notifications for primary and secondary outcomes are shown in Table 2 The comparison between the study's control districts and eight selected non-study districts showed no statistical difference in step-change (β 6 ) or trends (β 7 ) for bacteriologically-confirmed and All Forms TB notifications (Table 4).

Discussion
Our study demonstrated that community-based ACF can generate a substantial yield of previously undetected TB, even in a setting with a well-functioning TB program. Our ITS analyses substantiated the additionality calculations of the intervention by adjusting for changes in population size and seasonality. Although the trend differences in case notification rates were modest, they were statistically significant, supporting the case for a positive intervention impact. The post-hoc comparison between the study's control and selected non-study districts further substantiated this finding by showing that the notification declines recorded in the study's control areas were experienced across the majority of all nonstudy districts in HCMC.
A key success factor of these studies was expanding screening coverage to large portions of vulnerable populations and enabling access to the more sensitive CXR-Xpert diagnostic algorithm. Another commonality was leveraging existing healthcare structures. Successful community engagement projects tended to be complementary to facility-based case finding [37]. The engagement of established networks has been shown to be effective in other health areas as well [38]. A final similarity entailed the strong community linkages. Our CHWs coordinated with neighborhood leaders and commune TB officers to conduct household contact investigations. This raised community confidence in the study and lowered access barriers [39].
In evaluating the two human resource models, we found both to be successful in improving TB detection and notification. Our analysis further showed that these yields did not displace routine activities in either model. This suggests that there is a general benefit to engaging CHWs for community-based TB service coverage expansion. We further found that despite a lower case detection yield, the increases in All Forms TB notifications in the salaried employee districts was significantly higher than the gains in the  volunteer districts. This finding was substantiated by the ITS analysis. One explanation for the dichotomy in yield and additionality was the difference in screening activities. It is well documented that to find more cases a greater number of people need to be screened [40]. The higher number of screening encounters by the employees can be a proxy for time spent on outreach. The ability of full-time CHWs to achieve higher population coverage compared to volunteers has been noted in other settings [41]. Greater population coverage and community outreach have been cited as a catalyst for increased notifications [42].
Reports from the field also suggest that volunteers placed greater reliance on public health staff and neighborhood leaders to refer persons with suspected TB. This is intuitive given the lower remuneration and time commitment to ACF activities. Consequently, a greater proportion of individuals initiated on the TB care pathway by volunteers would have potentially been notified without this ACF intervention. This displacement of passive case finding has been documented among household contacts in Viet Nam [43].
However, as evinced by the PROPER CARE pilot [26], there is limited utility in an effective community engagement model that government stakeholders deem untenable for scale-up. As such, another positive finding of our study is that the volunteer human resource model still resulted in a significant increase in TB notifications for a lower cost. However, if resource-constrained programs choose to implement a volunteer-based human resource model, it will be necessary to consider other inherent risks besides lower additionality that may offset anticipated cost savings. Volunteers tend to require greater supervisory efforts to improve performance and ensure accurate reporting [25,44]. Past studies have also found volunteerism to be associated with lower value perception and job satisfaction [45]. Concordantly, the attrition in volunteer districts was higher than in salaried employee districts. The parameters were obtained for a segmented regression model with the following structure: Here Y t is the outcome measure along time t; T t is the monthly time counter; X t indicates pre-and post-intervention periods, Z denotes the intervention cohort, and ZT t , ZX t , and ZX t T t are interaction terms. β 0 to β 3 relate to the control group as follows: β 0 , intercept; β 1 , pre-intervention trend; β 2 , post-intervention step change; β 3 , post-intervention trend. β 4 to β 7 represent differences between the control and intervention districts: β 4 , difference in baseline intercepts; β 5 , difference in preintervention trends; This was also the case among district supervisors. The attrition required continuous recruitment and capacity building, and possibly impaired quality of care. These downsides of volunteerism have been noted elsewhere [46,47]. A health economic analysis that incorporates the cost implications of the attrition and other operational challenges encountered in our study will be provided in a separate manuscript. The Viet Nam NTP has already successfully replicated the volunteer model in cities with a lower TB burden and cost of living compared to HCMC, the economic center of Viet Nam [48]. In these cities the model generated comparable notification increases to the employee model in HCMC (manuscript in preparation). This suggests that the volunteer model could be appropriate in settings, where the workload and the opportunity cost of volunteering are lower. Appropriately powering incentives for the socioeconomic context and employing a blend of monetary and non-monetary incentives are further means to optimize volunteer models [49]. Lastly, future research may seek better ways to draw on the altruistic capital of volunteer CHWs to overcome operational challenges [50].
Our study had limitations. Conducting research in a programmatic setting exposed our study to supply chain interruptions. These interruptions affected the integration of study activities into routine program operations. However, this also reflects the reality of field scale-up of an intervention. While ITS analyses aim to increase validity and interpretability of the results by compensating for secular trends, we may have missed nuanced confounders due to the non-randomized study design. A strength of our study was the length and scale of our outreach as well as integration within the existing NTP Fig. 3 Comparative ITS analysis model graphs of population-standardized monthly notification rates of 1) All Forms TB case notification rates; and 2) bacteriologically-confirmed TB case notification rates for a) intervention versus control districts; and b) employee ACF versus volunteer ACF activities. As such, we believe in the transferability of our findings that effective engagement of CHWs can produce a positive notification impact and that full-time employment of CHWs can generate superior outcomes to other high TB burden, resource-limited settings to inform local strategies to end TB.

Conclusions
Leveraging community networks to expand TB service coverage is both feasible and effective in diagnosing and treating additional persons with TB. Engaging full-time, salaried employee CHWs in TB ACF schemes can lead to greater impact, and this human resource model should be prioritized for scale up where resources permit. While further studies are needed to optimize this community engagement model, it can be a powerful and readily available tool for advancing the global End TB Strategy targets.
Additional file 1: Figure S1. Active TB case finding algorithm. Figure  S2. Visualization of the comparative interrupted time-series analysis (intervention = upper line, control = lower line).  The parameters were obtained for a segmented regression model with the following structure: Here Y t is the outcome measure along time t; T t is the monthly time counter; X t indicates pre-and post-intervention periods, Z denotes the intervention cohort, and ZT t , ZX t , and ZX t T t are interaction terms. β 0 to β 3 relate to the control group as follows: β 0 , intercept; β 1 , pre-intervention trend; β 2 , post-intervention step change; β 3 , post-intervention trend. β 4 to β 7 represent differences between the control and intervention districts: β 4 , difference in baseline intercepts; β 5 , difference in preintervention trends; β 6 , difference in post-intervention step changes; β 7 , difference in post-intervention trend b The baseline rate denotes case notification rates per quarter as monthly notification rates were unavailable for non-study districts

Availability of data and materials
The data that support the findings of this study are available from the Viet Nam National TB Control Program and Pham Ngoc Thach Provincial TB Hospital, but restrictions apply to the availability of these data. Data are can be made available from the authors upon reasonable request and with permission of the Viet Nam National TB Control Program and Pham Ngoc Thach Provincial TB Hospital.
Ethics approval and consent to participate Approvals were granted by the PNTH Institutional Review Board and the Liverpool School of Tropical Medicine Research Ethics Committee. Study implementation was approved by the HCMC People's Committee. The Pham Ngoc Thach Provincial TB Hospital approved use of the data. We obtained written informed consent from all participants and anonymized all patient data prior to analysis.

Consent for publication
Not applicable.