Abstract
objective For a cohort of patients with tuberculosis in Carabayllo, Peru, we describe the prevalence of medical comorbidities and socio-economic needs, the efforts required by a comprehensive support programme ('TB Cero') to address them and the success of this programme in linking patients to care.
methods Patients diagnosed with tuberculosis in Carabayllo underwent evaluations for HIV, diabetes, mental health and unmet basic needs. For patients initiating treatment during 14 September, 2015-15 May, 2016, we abstracted data from evaluation forms and a support request system. We calculated the prevalence of medical comorbidities and the need for socio-economic support at the time of tuberculosis diagnosis, as well as the proportion of patients successfully linked to care or support.
results Of 192 patients, 83 (43%) had at least one medical comorbidity other than tuberculosis. These included eight (4%) patients with HIV, 12 (6%) with diabetes and 62 (32%) deemed at risk for a mental health condition. Of patients who required follow-up for a comorbidity, 100% initiated antiretroviral therapy, 71% attended endocrinology consultations and 66% attended psychology consultations. Of 126 (65%) patients who completed the socio-economic evaluation, 58 (46%) reported already receiving food baskets from the municipality, and 79 (63%) were given additional support, most commonly food vouchers and assistance in accessing health care.
conclusion Carabayllo tuberculosis patients face many challenges in addition to tuberculosis. A collaborative, comprehensive treatment support programme can achieve high rates of linkage to care for these needs.
Introduction
Globally, an estimated 10 million people fell sick with tuberculosis and 1.4 million died from it in 2015 [1] . Tuberculosis (TB) frequently occurs alongside other medical conditions, such as HIV and diabetes, and it is a disease associated with poverty and stigma. Many of the conditions that accompany TB are associated with poor TB treatment outcomes. However, TB treatment programmes often focus narrowly on ensuring that patients are diagnosed and receive anti-TB medications. As a result, patients with TB face various challenges that fall outside the scope of focus of conventional TB programmes, but which can negatively impact their treatment outcomes. While it would require increased efforts by health systems to simultaneously and comprehensively address the medical and social challenges faced by patients with TB in addition to curing their TB, these efforts are likely to pay off in the form of improved TB treatment outcomes.
The Zero TB Initiative is a network of local coalitions -in cities, districts and counties -that are committed to achieving a rapid reduction in the number of people suffering from TB by applying a comprehensive strategy [2, 3] . The District of Carabayllo in northern Lima, Peru, launched the first coalition in 2015. The 'TB Cero' programme in Carabayllo seeks to avoid TB deaths through active case-finding, comprehensive support for patients with TB and their families, and preventive therapy to avert future cases. This article focuses on the treatment support component, describing the prevalence of medical comorbidities and socio-economic needs among the initial cohort of TB Cero patients at the time of TB diagnosis, the efforts required to address their various needs and the success achieved by the programme in linking patients to care.
Methods

Study population
All patients initiating treatment for TB in Carabayllo since 14 September 2015 were offered support through TB Cero. This analysis includes patients initiating treatment during 14 September 2015-15 May, 2016. Evaluation results reflect data available as of 15 June 2016.
Carabayllo is a peri-urban district in the north of the metropolitan Lima area; 78% of its area are classified as rural. In 2014, its population was approximately 250 000. According to a 2013 survey, 24% were living in poverty, reflecting one of the highest poverty rates in Lima. The reported TB incidence is roughly 100 cases per 100 000 residents.
The TB Cero programme TB Cero is a collaboration between the non-governmental organisation Socios En Salud (SES), the Ministry of Health of Peru and the Municipality of Carabayllo. The objective of TB Cero is to avert TB deaths through active case-finding, comprehensive patient support, and preventive therapy for household contacts. This analysis focuses on the patient support component.
For TB Cero's patient support component, all patients diagnosed with TB in any of the nine public health facilities in Carabayllo were referred to TB Cero upon diagnosis. As part of routine practice, patients were started on TB treatment immediately and offered an HIV test and a glucose test for diabetes. Through a field team comprising SES nurses, nurse technicians, psychologists and social workers, TB Cero offered additional evaluations to supplement those covered by the TB services at the health facilities. Patients were interviewed about existing medical conditions and were offered diabetes testing using a haemoglobin A1C test (performed at a private laboratory with costs covered by SES), a mental health evaluation and an assessment for unmet basic needs. If health issues were identified during the interview or screenings, the TB Cero field team helped the patient engage the appropriate health service at a health facility or a referral-level facility. The field team facilitated linkage to existing publicsector health services by identifying the services that patients required, making appointments and sometimes accompanying patients to these appointments, coordinating with care providers in the health facilities and advocating for patients. Patients were also eligible for services provided by the municipality such as quarterly food baskets for patients with TB. If patients reported unmet basic needs within their households, SES provided socioeconomic assistance, including food vouchers or nutritional supplements, subsidies for transportation to health centres, assistance with paperwork for applying for access to health insurance or other available social services, services to improve living conditions, and healthcare supplies. We considered multiple factors to determine whether families required help with food, including the poverty score, the number of dependents, household income and expenses, and other sources of support.
TB Cero supported patients through TB treatment in collaboration with the public health facilities. In Peru, patients are asked to go to a health facility each day to receive treatment under the observation of healthcare worker. Health facility staff notified TB Cero about any patients who were not able to receive their medications regularly, and TB Cero provided a community health worker to bring these patients their medications in their homes, foster treatment literacy and provide emotional support.
Evaluation tools used for TB Cero
Haemoglobin A1C values >6.4% were considered indicative of diabetes, and values between 4.7 and 6.4% indicative of pre-diabetes (pre-diabetes was not defined as a medical comorbidity in analysis). For the mental health evaluation, the Self-Reporting Questionnaire (SRQ-18) was used to identify persons at high risk of depression, psychotic disorders or alcoholism; in February 2016, depression screening was performed using the Patient Health Questionnaire (PHQ-9) instead. Both of these instruments have been validated in Peru [4, 5] . Standardised forms were also used to identify persons who used substances or who had been victims of domestic violence. Patients were referred for mental health attention if they had a score of ≥1 on the psychotic disorder or alcoholism section of the SRQ-18, if they reported substance use or having experienced domestic violence or if they had a score of ≥10 on the PHQ-9. Patients not screened with the PHQ-9 were referred if they had a score of ≥9 on the neurotic disorder section of the SRQ-18 or a score of 7-8 with signs of depression. Patients and/or heads of households were interviewed using standardised forms to evaluate poverty level and identify unmet basic needs (Appendix S1).
Data collection and analysis
Data recorded on the evaluation forms and in the support request system were abstracted into an analytic data set. We calculated the prevalence of medical comorbidities and the need for socio-economic support at the time of TB disease diagnosis, as all evaluations were performed shortly after patients were diagnosed with TB.
Ethical considerations
This analysis relied on data collected for administration of the TB Cero programme and required no additional data collection or interaction with participants. It was determined not to comprise Human Subjects Research by the Partners Healthcare Institutional Review Board.
Results
A total of 192 patients were diagnosed with TB in Carabayllo between 14 September 2015 and 15 May 2016 (Table 1) . Of these, 29 (15%) had a history of prior TB treatment, and 23 (12%) had multidrug-resistant (MDR) TB. Patients had a median age of 32 years (interquartile range 22-48), and nine (4%) of the patients were children <15 years old.
Linkage to care for medical comorbidities
In total, 83 (43%) patients had at least one medical condition other than TB. Eight (4%) patients had HIV infection, which all of them knew about prior to their TB diagnosis. However, only two (25%) were receiving antiretroviral therapy at the time of TB diagnosis. TB Cero helped the remaining patients through the evaluation and registration process for antiretroviral therapy (Table 2) .
In total, 12 (6%) patients either knew that they had diabetes (n = 10) or were newly diagnosed with it (n = 2). Of those who reported knowing they had diabetes at the baseline interview, eight (80%) were receiving some sort of medical treatment for diabetes. Of the 114 (59%) patients who accepted the offered haemoglobin A1C test, eight (7%) had a result indicating diabetes (including six patients who already knew about their condition) and 12 (11%) had a result indicating pre-diabetes. The prevalence of diabetes among those tested was higher in older age groups (Table 3 ; Cochran-Armitage trend test exact P = 0.047). None of the pre-diabetic patients knew about their condition. Of the 14 patients newly diagnosed with diabetes or pre-diabetes, 10 (71%) attended a follow-up medical consultation, two (14%) declined the consultation, and two (14%) moved to another jurisdiction (Table 2) .
Of the 135 (70%) patients who underwent mental health screening, 62 (46%) were considered to be at risk for a mental health condition based on the questionnaire results ( Table 4 ). The conditions most frequently identified during the screening were alcohol dependence and depression. Of the patients at risk, 47 (76%) accepted a referral to a health facility for further attention, and 41 (87%) attended the appointment ( Table 2 ). The psychologist at the health facility recommended psychiatric care for nine (22%) of these patients, psychotherapy for two (5%) and counselling for 28 (68%).
When asked about any other medical conditions, 20 (10%) patients reported at least one; four (2%) patients reported two conditions. Reported conditions were cancer (n = 3), gastritis (n = 7), hernia (n = 2) and one report each of acromegaly, Alzheimer's disease, asthma, cardiovascular disease, cellulitis, fatty liver disease, glaucoma, hypertension, hypothyroidism, post-trauma spleen surgery and stroke.
Socio-economic assistance
A total of 126 (65%) patients were evaluated to determine their need for socio-economic assistance (Table 5) . Of the 66 (34%) patients who were not evaluated, 30 (45%) explicitly declined the evaluation. Of evaluated patient households, 62 (49%) reported receiving support from one or more municipal services such as monthly food baskets (n = 58), a soup kitchen (n = 3) and a rehabilitation centre (n = 2). We were unable to assess the municipal services accessed by patients who did not undergo the evaluation.
After evaluation, 79 (63%) households were determined to require additional socio-economic assistance from SES. Assistance was given to address the needs of the TB patient him or herself (e.g. nutritional supplements or transport to health facilities), the needs of family members (e.g. reimbursement for chest radiographs used to evaluate family members for TB) and needs of the household as a whole (e.g. assistance with rent or utility payments). Of the households that received any form of assistance, 33 (41%) required only one form of assistance, 27 (34%) required two, and 20 (25%) required more than two. The most common form of assistance provided was food vouchers; of the 40 families requiring food vouchers, 18 (45%) also reported receiving food baskets from the municipality.
Home-based treatment support
Nurses at the nine health facilities identified 36 (19%) patients who had demonstrated or anticipated difficulty in coming to the health facility daily for treatment. The most common reasons for this were that medical complications rendered them too ill to travel and lack of money for transport. All of these patients were provided with a community health worker to deliver their treatment at home ( Table 2) .
Discussion
Among patients with TB in Carabayllo, we observed that four in 10 patients had medical issues other than TB, and that four in 10 patient households required assistance to meet their basic needs. The TB Cero programme provides an example of how these issues can be addressed through effective partnerships.
Helping patients to address concomitant health concerns is an important component of stopping the TB epidemic, as medical comorbidities and poverty can affect TB treatment outcomes and transmission. For example, most of the patients with HIV in this cohort 76 (100) †Eight patients knew they had HIV prior to their TB diagnosis, and there were no new HIV diagnoses. The six patients requiring follow-up were those who were not receiving antiretroviral therapy.
‡Ten patients knew they had diabetes prior to their TB diagnoses. The 14 patients requiring follow-up were those who were newly diagnosed with diabetes (two patients) or pre-diabetes (12 patients) based on the haemoglobin A1C test result. Diabetes was defined as an HbA1C result of >6.4%; pre-diabetes was defined as an HbA1C result of 5.7-6.4%. were not receiving antiretroviral therapy at the time of their TB diagnosis, a situation associated with substantial mortality risk [6] . Diabetes, which was diagnosed in 7% of tested patients in this cohort, is associated with increased risk of death, treatment failure and relapse among patients with TB [7] . Alcohol dependence, reported by 16% of this cohort, can lead to irregular or incomplete treatment, increasing the risks of death, relapse and development of additional drug resistance [8] . Finally, although we did not measure malnutrition, we found that one in five households in this cohort required food vouchers because of food insecurity. Malnourished TB patients are at higher risk of death from TB [9] , and malnourished household members have a higher risk of developing it themselves [10] . Importantly, it is possible to mitigate the risks of poor outcomes associated with many of these conditions. Antiretroviral therapy lowers the risk of death in TB patients with HIV by nearly 60% [11] . Better diabetes management improves TB treatment outcomes [12, 13] . While data are sparse, several studies suggest a positive effect of nutritional or caloric supplementation on TB treatment outcomes [14] . In Lima, Peru, all of these interventions are available and supported by local or national policy. Thus, it is feasible to implement a comprehensive approach to managing the health issues that patients with TB face, with the goal of improving their treatment outcomes.
Interventions that alleviate poverty can also improve health outcomes. This is a particularly relevant observation for TB, as it is both a cause and an effect of poverty. Children and adults who live in poverty face an increased risk for TB because malnutrition, overcrowding and poor access to health care all contribute to TB risk [15] . Conversely, TB fuels poverty; across different settings worldwide, the process of being diagnosed and treated for TB costs patients the equivalent of half their yearly income on average, even when the drugs themselves are free [16] . Cash transfer and microfinance interventions have been shown to improve healthcare access and household food security [17] as well as TB treatment completion rates [18] , suggesting a role for such socio-economic interventions in comprehensive TB programmes [15] .
It has been argued health systems could gain efficiency as well as effectiveness by integrating care for conditions that affect the same patients [19] . Indeed, efforts to integrate care for TB and HIV in sub-Saharan Africa have improved diagnosis and treatment of both [20] , although the practical challenges of integration have been substantial [21] . In many healthcare systems, including Peru's, different conditions (e.g. TB, diabetes, mental health issues) are currently managed by different providers. While integrating care for these different conditions would likely be beneficial for patients, it would require significant changes to the organisation of the healthcare system. TB Cero's strategy of having a field team who function as case managers and patient advocates is one method for offering coordinated care in a system where care is not integrated at the provider level.
TB Cero was implemented through a partnership between a non-profit organisation (SES), the public health system and the municipal government. Its initial strategy has been to help patients fully take advantage of the services available in the public sector and then for SES to fill in gaps where the public sector did not provide support. Many patient needs could effectively be addressed by services available at public health facilities, but advocacy on behalf of patients, accompaniment, and financial assistance were often required to help patients access these services. While public programmes such as food baskets for patients with TB and soup kitchens helped many patients suffering from food insecurity, a substantial number of patients still required additional food assistance from SES. Improved coordination among the public and private partners in this initiative can lead to more efficiencies. This analysis is limited to the description of conditions experienced by patients with TB and their families at the time of TB diagnosis, and what the TB Cero programme did to help them address these conditions. We do not have data on how these conditions may have changed over the course of treatment. In addition, this baseline analysis does not speak to the impact of the TB Cero programme on TB treatment outcomes; a complete evaluation is planned for when the cohort is anticipated to complete TB treatment.
In conclusion, patients with TB in Carabayllo face many challenges, both medical and socio-economic, all of which may affect their ability to successfully complete TB treatment. However, it is possible to understand and systematically address these myriad needs through effective collaboration between the public healthcare system, partners, who work in the community, and other stakeholders.

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