ORIGINAL RESEARCH published: 26 November 2019 doi: 10.3389/fmed.2019.00273 Specific Interventions for Implementing a Patient-Centered Approach to TB Care in Low-Incidence Cities Adrià Pujol-Cruells 1 and Cristina Vilaplana 1,2* 1 Experimental Tuberculosis Unit, Fundació Institut Germans Trias i Pujol, Universitat Autònoma de Barcelona, Badalona, Spain, 2 Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (CIBERES), Madrid, Spain Background: According to the latest Guidelines from the World Health Organization, there is an increasing need for patient-centered tuberculosis disease management given the socio-economic factors influencing the tuberculosis epidemic. In the present study, we aimed to study TB in Barcelona city from an anthropological point of view and to devise a series of specific proposals to implement a patient-centered approach in our setting. Edited by: Delia Goletti, Methods: We carried out a qualitative study using an anthropological approach in Istituto Nazionale per le Malattie Barcelona in the period between November 2017 and November 2018 and proposed Infettive Lazzaro Spallanzani specific interventions based on our observations. (IRCCS), Italy Reviewed by: Results: In practice, in our environment (a low-incidence European country where Leonel Lagunes, tuberculosis tends to present in patients with multiple social problems), and despite the Vall d’Hebron University Hospital, Spain goodwill of the care teams, there are no established and stable circuits, or specific tools Frédéric Méchaï, to ensure that this is done routinely. Based on our observations, we have devised a series Hôpital Avicenne, France of specific proposals to implement a patient-centered approach. With these interventions *Correspondence: we aim to (a) directly ameliorate TB patients well-being in any diagnostic/healthcare Cristina Vilaplana cvilaplana@igtp.cat; management center and (b) at more general level, to increase TB detection and cvilaplana@gmail.com treatment adherence. Specialty section: Conclusions: The patient-centered TB management recommended by the WHO might This article was submitted to be essential for patients’ well-being, but there is a lack of circuits or working protocols that Infectious Diseases - Surveillance, ensure its implementation in a regulated manner. In the present manuscript we explain Prevention and Treatment, a section of the journal the various concrete measures that we propose in our region and which could be put into Frontiers in Medicine practice in other cities or geographic regions with similar epidemiological characteristics. Received: 11 June 2019 Keywords: tuberculosis, patient-centered approach, care management, interventions, socio-economic factors, Accepted: 11 November 2019 anthropology Published: 26 November 2019 Citation: Pujol-Cruells A and Vilaplana C (2019) Specific Interventions for INTRODUCTION Implementing a Patient-Centered Approach to TB Care in According to the latest global report on tuberculosis (TB) published by the World Health Low-Incidence Cities. Organization (WHO), there were up to 10 million cases of TB and 1.3 million TB-related deaths Front. Med. 6:273. in 2017 (1). Following the global trend, the incidence rate in Europe is decreasing. In Spain, after doi: 10.3389/fmed.2019.00273 two epidemic peaks, coinciding first with the abundance of parenteral drug users among people Frontiers in Medicine | www.frontiersin.org 1 November 2019 | Volume 6 | Article 273 Pujol-Cruells and Vilaplana Patient-Centered TB Care Interventions infected with HIV (in the late 1980s and 1990s), and then with The second phase was participatory observation: real follow-up the large-scale migration from countries with a high incidence of including informal conversations and unstructured interviews TB found in the early 2000s, TB is relatively well-controlled and with patients diagnosed with TB (n = 22), and health is also decreasing in incidence (2). As such, the main problems professionals including medical and nursing staff, social workers in epidemiological terms are the high incidence in large cities and health agents (n = 29). No data from the participants and delays in diagnosis (an average of 60 days from the onset was recorded, only the anthropologist impressions. The third of symptoms according to the latest data available) (3). In the phase was collaborative observation: proposing strategies for case of Barcelona, a model TB control program established by intervention in the community. the city’s Public Health Agency, which allows an interchange of The study was conducted within the STAGE-TB project information between clinical TB units, case managers and public (registered at ClinicalTrials.gov, identifier: NCT03691883), health nurses, as well as healthcare agents (4), thereby facilitating coordinated by the Experimental Tuberculosis Unit; and its the active monitoring, detection and follow-up of patients and protocol and procedures were reviewed and approved by the access to the complete data for all cases, has been operating for correspondent responsible institutional review committees. more than 30 years. This has led Barcelona to be considered a laboratory in which the problems and challenges of TB control programs in Western Europe, especially in large cities, can be RESULTS studied. In the latest report (with data from 2016), the incidence rate was 16.2/100,000 inhabitants, distributed unevenly in the Our qualitative study confirmed the high prevalence of social various districts depending on their levels of income (up to exclusion associated with this disease. In Barcelona, the 43.8/100,000 in the Ciutat Vella district, for example). About paradigmatic patient is an immigrant with difficulties entering half of these patients were born outside Spain, the percentage the social and working environment of the region and with of patients with socio-economic vulnerability was estimated at language-related communication problems. The social exclusion 7.3% and there was an increase in homelessness and alcoholism. associated with TB is determined by both the personal, family The percentage of patients with completed treatment was lower and legal status of the individual (whether native or migrant) as in the elderly, the homeless, those addicted to parenteral drugs well as by the added problem of the disease itself, which given and those with a history of imprisonment, partly due to the high the resulting chronicity, associated disability and hospitalization mortality in these groups (3). (when required) acts as a barrier (not always symbolic) that One of the aspects that the latest WHO report highlighted is hinders or prevents the patient from finding work, having a that, in order to achieve the reductions in incidence necessary place to live and establishing social relationships. Healthcare to meet the milestones set for 2030, the socio-economic workers recognize well-situations of poverty, malnutrition, social factors influencing the TB epidemic must be addressed (1). exclusion, and fragility at a mental health level; but there Unfortunately, this is not the only problem, as the latest are no established circuits or protocols that allow addressing WHO publication regarding TB treatment guidelines (5) clearly appropriately these situations. suggests that a patient-centered approach is required in the Moreover, hospitalization or the termination of any activity treatment of TB patients. Such an approach considers that it is considered normal for the individual causes the patient to insufficient to cure only the illness and that the patient must feel trapped in limbo, which can hinder their reintegration also be cured. For this: (1) the patient must participate actively into the environment, especially the working environment. In in the process, (2) their preferences, needs and values must addition, there are two cultural perceptions around the disease: be taken into account, and (3) a complete approach, including in stabilized environments, TB is associated with pathological both mental health and social aspects, must be used. There is social states and is therefore seen as an anomaly, whereas in less sufficient evidence to support this more holistic-type approach in structured social environments, TB is perceived as a consequence TB has been shown to have an important impact on both patient of the pervading conditions. The social exclusion (and socio- well-being and treatment outcomes (6). economic factors in general) associated with the illness, as well In the present manuscript we aimed to study TB in Barcelona as the duration of medical treatments, also has an impact on the city from an anthropological point of view and to devise a series institutions and health personnel that these patients attend, and of specific proposals to implement a patient-centered approach; they are often not aware of the quality of the service they receive. applicable to our setting but which could be extrapolated to other Depending on the different geographical origins of the cities with similar epidemiological situations. patients, there is also a cultural shock between the patients and their new social framework (which also includes the area of healthcare), since the disease brings individuals into contact METHODS with cultural realities to which they are not accustomed, mainly due to differences in customs and gender perspectives. This We carried out a qualitative study using an anthropological generates isolation in these patients and means that, although approach in Barcelona in the period between November 2017 and they tend to recognize the seriousness of the illness (and its November 2018. The field work was divided into three phases. associated medical problems), this perception does not always First phase was floating observation of 40 patients and 8 health translate into healthy behaviors. In order to minimize this professionals: initial phase of prospecting, without intervention. cultural shock and its impact on individuals, the design of Frontiers in Medicine | www.frontiersin.org 2 November 2019 | Volume 6 | Article 273 Pujol-Cruells and Vilaplana Patient-Centered TB Care Interventions activities in which patients can participate is often necessary. when budgeting the different proposed interventions. We have However, the offer is limited and must take into account the included this information as Table 2, which could be used to cultural point of view. calculate the amount of funding needed once applied to the cost Based on our observations, we have devised a series of specific of living, cost of salaries, and other cost measures of the specific proposals to implement a patient-centered approach, applicable country/region where to implement the intervention. to Barcelona and which could be extrapolated to other cities with similar epidemiological situations. With these interventions we aim to a) directly ameliorate TB patients well-being in DISCUSSION any diagnostic/healthcare management center and b) at more general level, to increase TB detection and treatment adherence. One of the limitations of the study is that we focused on These proposals are set out in Table 1 and can be divided the anthropological approach and didn’t conduct an associated depending on the level at which they are to be applied: (a) at epidemiological study to perform a precise description of the diagnostic and/or treatment center, which can improve the the studied population (including their geographical origin, conditions of the patients directly, and (b) at the population spoken language and detailed social condition). However, our level in general, affecting neighborhoods with the highest risk observations were in line with results of the quantitative studies of TB. carried out in this city (2, 3, 7) and similar to findings from At the level of the diagnostic and/or treatment center (Table 1 other major European cities (8, 9). The treatment management and Figure 1), it is essential to carry out activities that mitigate options recommended by the WHO in its guidelines are currently unemployment or the illegal behavior, stigma and uprooting of applied well in Spain [in Barcelona, for example, the percentage patients, especially if they are admitted. These activities must of cured bacillary pulmonary cases or those who have completed include leisure activities, health, training, and psychological treatment is as high as 92.5% (3)], except for the administration support (programmed; compulsory or voluntary) and be adapted of DOTS (performed in 30.4% of patients, reaching 71% in to the patients’ cultural context (gender, age, religion, customs, users of injected drugs (UDI) and 90% in homeless people, etc.). Moreover, the centers must be equipped with suitable although rarely via telematics) and the lack of uniformity in terms facilities and spaces to carry them out and there must be a of supply. network of agreements and collaborations between the centers The main problem arises, however, when it comes and the facilities in the city, and particularly in the patients’ to treatment-adherence interventions. The WHO neighborhood. At an internal level, we believe that both the recommendations (5) regarding the provision of health presence of a regularly scheduled institutional therapy in the education and advice to patients are met relatively well in Spain form of group sessions attended by both patients and healthcare by all persons involved (patients and healthcare personnel). staff and social mentoring program (in-house or outsourced However, there are no guidelines or recommendations through contracts or collaborations with mentoring associations) for activities to ensure the uniformity of actions and their should be implemented. fulfillment. This situation worsens when it comes to recognizing With regard to the interventions of a more general and addressing situations of poverty, malnutrition, social nature proposed for application in neighborhoods with the exclusion and fragility at a mental health level. Thus, although highest incidence of TB (Table 1), it would be important to these problems are usually correctly identified at a healthcare have information tools (i.e., leaflets, infographics, videos) level, it is often logistically difficult to resolve them and, if in different languages (in Barcelona: in Catalan, Spanish, this is achieved, it is often solely due to the goodwill of all French, English, Arabic, Urdu, Chinese) and universal access, those involved (medical and nursing staff, health agents, social with the participation of patients during their design; to workers at the centers and associations). Moreover, there is organize talks and conferences on the disease in which currently little or no coordination or uniformity, and there are patients or ex-patients also participate, thereby taking full no established circuits or protocols that allow comprehensive advantage of the figure of the “expert patient”; and to care to be provided. Thus, although there are links to other ensure the continuing specialized training of professionals. public-health programs and sufficient resources to properly Given the profile of an individual potentially affected address patients with co-morbidities (such as HIV co-infection), with TB (with the concomitant social pathology that other problems, such as those from the mental health sphere, are affects detection, diagnosis and treatment adherence), we often under-diagnosed and, therefore, under-treated. believe that the creation of interdisciplinary teams from Another of the main problems of TB in our region is that, professionals already working on the ground would be despite being aware of the precarious socio-economic factors essential (Figure 2). present in some patients, it is difficult to include these patients, The holistic and multidisciplinary approach proposed as requested by the WHO, in publicly offered services and requires substantial human and financial resources. community-based resources and support, mainly due to the lack Unfortunately, a concrete estimation of its cost is very of established protocols and circuits. difficult to be calculated, as it depends on the setting where Given this situation at the local level of a large city (Barcelona), to be implemented and the resources available (including the as seen from our anthropological work, and taking into account type of Healthcare System). However, we made the exercise of the recommendations of the WHO (5) and those of “The working detailing the items which in our opinion should be considered group for TB control in big cities and urban risk groups in the Frontiers in Medicine | www.frontiersin.org 3 November 2019 | Volume 6 | Article 273 Pujol-Cruells and Vilaplana Patient-Centered TB Care Interventions TABLE 1 | Specific interventions proposed to implement the patient-centered approach to TB care. Level of Proposals Expected impacts intervention In diagnostic or Scheduled activities (leisure, health, training, psychological For patients: To increase patient well-being and mental balance, treatment centers support) available to TB patients, adapted from a cultural point of favor their integration into society, establish a bond with the city, view (gender, age, religion, customs, etc.), performed in suitable minimize culture shock, decrease para/illegal behaviors. spaces, in-house or in neighborhood, or city facilities (libraries, For society in general: increase awareness. museums, swimming pools, gyms) thanks to collaboration For centers: to offer a more complete portfolio covering the agreements. patient-centered approach. Regularly scheduled institutional group sessions with both patients Two-way flow of information; to reveal problems, doubts and and staff attending. fears; increase treatment adherence. Social mentoring activities, in-house or outsourced, thanks to To accelerate and increase reinsertion, emancipation and collaboration agreements with other institutions or NGOs. adherence to treatment, while reducing isolation and unhealthy habits, in the framework of interventions to generate, reconnect or strengthen the bonds of the individual with society. In high TB incidence Information tools (i.e., leaflets, infographics, videos), in different For patients: to increase treatment adherence, bond with neighborhoods languages, of universal access, patients coauthoring. Two healthcare staff and increase patient confidence. versions: one for patients and their relatives, another one for the For relatives: to resolve doubts and give them tools to handle general population. day-to-day problems. For the general population: to increase awareness, to promote early diagnosis. Conferences, seminars, informal talks on the disease, its To increase awareness of the presence of the disease in the management and its impact; patients involved; conducted using environment; increase health literacy; reduce fears and resolve community infrastructures and spaces: schools, civic centers, doubts. libraries, museums, places of worship, leisure and health facilities (gymnasia, swimming pools, shopping centers). Continuing education for healthcare professionals on TB To increase awareness of the presence of the disease and reduce screening, diagnosis, management and treatment; carried out diagnostic delay; to refresh and update information on TB periodically; i.e., refresher courses, infographics, etc. management. Creating interdisciplinary teams; at city, regional or national level; To generate documents, protocol circuits, and guidelines that recommended to include healthcare workers, mental health ensure the implementation of a global approach to the therapists, social science workers, nutritionists, and patients management of TB patients. (expert patient). FIGURE 1 | Interventions proposed at the level of the diagnostic and/or treatment center. EU” (9), we have devised a series of specific proposals applicable Interventions proposed at the level of the diagnostic and/or to Barcelona that could be extrapolated to other cities with similar treatment center, apart from facilitating the leisure options and epidemiological situations. training available at the centers, and working on how to stop Frontiers in Medicine | www.frontiersin.org 4 November 2019 | Volume 6 | Article 273 Pujol-Cruells and Vilaplana Patient-Centered TB Care Interventions FIGURE 2 | Creation of interdisciplinary teams: phases. transmission and spread of the disease, ensure that there is no in order to optimize resources, it would be advisable to use discontinuity between the hospital/residential world and that of existing resources that have proven useful in other regions the general population outside this institutional context. It also or countries with a similar TB incidence and characteristics. adds value to those centers that offer it, since the quality of the All these initiatives need to be carried out using community services provided increases beyond strictly medical care (which infrastructures and space in order to link them to society itself, is already covered nowadays). At an internal level, regularly especially schools, civic centers, libraries, places of worship, scheduled institutional therapy help strengthen messages related and leisure and health facilities (gymnasia, municipal swimming to the disease, encourage a two-way flow of information and pools, shopping centers). The continuing specialized training can be used to carry out training. They also have an important of professionals is also indispensable (5), especially in low- impact on the outcomes of the disease (10). This type of activity impact countries (such as those in Western Europe), and can could form part of the group of interventions that favor treatment be done by way of refresher courses or much simpler tools to adherence and the psychological support defined by the WHO encourage professionals to take into account the illness in these (5). Finally, we propose that a social mentoring program environments, such as infographics and reminders in the clinic. should be implemented, to accelerate and increase reintegration, On the creation of interdisciplinary teams from professionals emancipation and treatment adherence, while reducing both already working on the ground, we do believe it would represent a isolation and unhealthy habits, in the framework of interventions significant step toward tackling the illness and increasing patient to generate, reconnect or strengthen the ties of individuals with wellbeing. These teams could be created at a city, regional or society (11). national level, and it may be advisable for them to be led by local With regard to the interventions of a more general nature Public Health Agencies. Although this approach has not been proposed for application in neighborhoods with the highest tested in tuberculosis in our setting, similar initiatives, such as incidence of TB, we must make an effort to intensify the presence the management of care for people with complex needs, which and implementation of tools that enhance visibility of the disease involves the coordination of health services (including mental given the fact that poor population information and inadequate health) at both the primary care and hospital levels, social services training of professionals result in a delay in diagnosis. In this (both at a community and an individual level), and a specialized sense, it would be important to ensure the participation of community support team (formed by geriatricians, pharmacists, patients during their design. Similar experiences have shown occupational therapists, dieticians), have been implemented (14). that joint development (by professionals and patients working To accomplish this goal, the following sequence of steps together) of the information (the story) plays a key role in the would be required: (1) a call to all agents, including the main solution to the problem (12, 13). actors involved in TB care (professionals in the fields of social All these communication tools and activities should applied sciences, public administration, politics, and communication, twice: once for patients and their friends and families, and the from the legislative world, criminologists, teachers from all walks second time for the general population (distributed in geographic of life (especially adults), nutritionists, therapists and others). regions at higher risk). In this regard, it should be noted that, In this first session, all these agents would be summoned and Frontiers in Medicine | www.frontiersin.org 5 November 2019 | Volume 6 | Article 273 Pujol-Cruells and Vilaplana Patient-Centered TB Care Interventions TABLE 2 | Suggested items to be considered when budgeting the specific interventions proposed. Interventions proposed Items to be considered when budgeting Scheduled activities available to TB patients If done in-house: • costs of adapting/transforming the in-house spaces to make them suitable for the purposes. • salary of professionals organizing and/or conducting the activities or effort cost. Costs can be diminished/suppressed by establishing collaboration agreements with neighborhood or city facilities (libraries, museums, swimming pools, gyms). Regularly scheduled institutional group sessions with • Salary for a psychologist/therapist. both patients and staff attending. Social mentoring activities, in-house or outsourced, • Salary for a program supervisor (administrative management of the team, formative supervision, thanks to collaboration agreements with other monitoring performance). institutions or NGOs. • Salary for mentors. • Mentors’ travel expenses (including per diem). • Communication support (i.e., Mobile phones, internet connection). • Cost of training the mentors. These costs could be decreased/ suppressed by establishing collaboration agreements with local associations and NGO to partially cover the activity. Information tools for patients and relatives and for the • Costs of designing the information material (payment-as-a-service or effort cost of professionals). general population. • Costs of translations. • Costs of publishing the material. • Costs of distributing the material (salary or effort cost of distributor/s). Communication activities • Effort cost of professionals giving the communication activities. This cost can be diminished/suppressed if the professionals agree to voluntary work. • Cost of renting community infrastructures and spaces. This cost can be diminished/suppressed by establishing collaboration agreements with city council or similar local institutional bodies. Continuing education for healthcare professionals on TB • Costs of performing an educational course. It will depend on the format and channel: webinar, videos, tutorials, classroom course. Can include effort cost of professionals involved (including professors), internet domain, editing. Costs can be diminished by establishing collaboration agreements with universities, foundations and NGO which can contribute to the activity. • Costs of designing educational material (payment-as-a-service or effort cost of professionals) and publishing educational material. Creating interdisciplinary teams Minimal team: • Effort cost of 1 MD to coordinate the program and to act as the interlocutor with the physicians of hospitals and other institutions feeding the program with patients. • Effort cost for 1 nurse to act as the interlocutor with the MD in charge of the program and the nurse team at territorial level about the specific cases. • Salary of 1 healthcare manager/administrative to manage the team and to coordinate the collaboration agreements with the institutions and facilities. • Effort cost for 1 healthcare worker. • Effort cost for 1 social assistant. • Effort cost for 1 expert patient and/or costs of meetings with expert patients. Minimal team needs coordination with mental health therapists and nutritionists, that in case of being included in the team their effort cost or salary would need to be also included. trained, and they would be invited to put forward their reflections Finally, under the tutelage of the Multidisciplinary Teams and proposals at a second meeting. A Multidisciplinary Teams Committee, and once all proposals have been analyzed, the Committee, in other words a group of people from all the interdisciplinary pilot team should be appointed, its ideal test different levels that would lead the initiative and ensure its good performance and main lines of work (areas, agents) defined, performance, would also be created. The second step would and the proposals implemented in the territory during a trial be the pooling of new approaches and points of view from all period. Although initially there may be multiple solutions for these other disciplines in order to create a pilot team that can financing these teams (including the association of this initiative work on the search for improvements and solutions for patients, with a research project), it is important that the local public reaching a consensus and generating documents, along with administration assumes responsibility for the economic viability protocol circuits and guidelines that ensure a global approach of these teams beyond the pilot stage. to the disease. Again, we emphasize that both the screening for From an economic point of view, we have envisaged several mental disorders and counseling and psychological support for interventions with a potential wide range of feasibility depending patients are very important for the entire duration of disease on the available resources at local or governmental level. As the follow-up and treatment, especially in those most vulnerable at funds for the implementation of actions might be unassumable by the social level [such as refugees or immigrants (15) or in cases of the diagnostic/healthcare management centers and the National multi-drug resistance (16, 17)], and these need to be both offered Health System (which can vary a lot between different countries and provided, then routinely scheduled in a regulated manner. sharing the same epidemiology in terms of TB), collaboration Frontiers in Medicine | www.frontiersin.org 6 November 2019 | Volume 6 | Article 273 Pujol-Cruells and Vilaplana Patient-Centered TB Care Interventions agreements with local associations, NGO, city council or similar Committee (study approval code: PI-17-064) and the Vall local institutional bodies need to be established, in order to d’Hebron Hospital Clinical Research Ethics Committee (code partially cover or contribute to the activity, and thus to decrease PR(AG)101/2017). Verbal informed consent was obtained from or even suppress part of the costs. Further studies should be all participants because the study was based on informal conducted in order to elucidate at which extent some of the conversations, no questionnaires, or structured interviews were actions proposed here could also be implemented in low-income conducted and no personal data from the participants were countries, which due to their high-TB prevalence could benefit recorded. Written informed consent for participation was not even more of their impact if proven successful. required for this study in accordance with the national legislation and the institutional requirements. CONCLUSION AUTHOR’S NOTE The WHO recommendations in terms of tackling TB are very meaningful from the point of view of addressing the suffering We would like to emphasize that all the reflections presented of patients beyond the disease itself, and although care teams have been possible thanks to TB patients, all healthcare staff are usually aware of this, there are currently still no circuits involved, Servicios Clínicos SLU, the Barcelona Public Health or working protocols that define the necessary interventions Agency, and the health agents of Barcelona. Preliminary results or circuits that ensure their implementation in a regulated of the study were presented at the XXII International Workshop manner. With this publication, we hope to highlight this on TB conducted in Barcelona on the 26–27 November shortcoming while explaining the various concrete measures 2018, and published as a conference abstract in Rev Enf that we propose in our region and which could be put into Emerg 2018;17:159–160. practice in other cities or geographic regions with similar epidemiological characteristics, once adapted to the limitations AUTHOR CONTRIBUTIONS of the new setting. AP-C conducted the floating and participatory observation TAKE HOME MESSAGE phases of the field work. Both AP-C and CV contributed in the design of the study, worked in the analysis and interpretation There is an increasing need for patient-centered tuberculosis together, and in the collaborative observation by proposing disease management, but this is not done routinely. In this article strategies for intervention in the community. The authors we propose a series of specific interventions that could be easily worked together to draft the manuscript and approved its implemented in low-incidence cities during care management. final version. DATA AVAILABILITY STATEMENT FUNDING All datasets generated for this study are included in the This work was supported solely by the Experimental Tuberculosis article/supplementary material. Unit funds. CVM has a Miguel Servet II contract funded by the Instituto Carlos III (ISCIII, CPII18/00031). Funds were ETHICS STATEMENT received from the Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (CIBERES) to cover the open The studies involving human participants were reviewed and access publication fees. 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