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Original research Pan American Journal

of Public Health

Evaluation of implementation of the


protocol for managing tuberculosis/HIV
coinfection in specialized care services
in the state of Ceará, Brazil*
Silvia Helena Bastos de Paula,1 Telma Alves Martins,2 Sheila Maria Santiago
Borges,3 Christiana Maria de Oliveira Nogueira3 and Valderina Ramos Freire3

Suggested citation (Original article) Bastos de Paula SH, Martins TA, Borges SMS, de Oliveira Nogueira CM, Freire VR. Evaluación de la
implementación del protocolo de manejo de coinfección de tuberculosis y VIH en los servicios de
asistencia especializada del estado de Ceará, Brasil. Rev Panam Salud Publica. 2017;41:e48.

ABSTRACT Objectives.  Identify barriers and strategies for implementation of the protocol for managing
tuberculosis/human immunodeficiency virus (TB/HIV) coinfection in specialized care services
in Ceará state, through implementation research.
Methods.  The study followed the iPIER methodology, a new initiative to help improve the
implementation of health programs through the use of research that is conducted as a part of the
implementation process. Data were collected on the structure and processes of 22 services, and
barriers were explored in four focus groups with 28 participants, from the standpoint of the
health team, administrators, and users. The discussions were transcribed and interpreted with
regard to the objectives of the study.
Results.  The information on structure and process revealed that six services manage TB/HIV
coinfection and 16 do not. The barriers were: team members were unaware of the protocol; lack of
clinical practice guidelines in the services; specialized care services working at all three levels of
the health system; inadequate spaces for treatment of airborne diseases; and lack of communica-
tion with primary health care sectors for patient transfers. The results were discussed with teams
and administrators in seminars held in the services and with program managers for sexually
transmitted infections, human immunodeficiency virus, AIDS, hepatitis, and tuberculosis.
Conclusions.  Direct dialogue between administrators, implementers, users, and researchers gen-
erated knowledge about the services and led to joint preparation of modifications in workflow aimed
at acceptance and use of the protocol; however, users continue to resist adherence to treatment.

Keywords Tuberculosis; HIV; protocols; health services; Brazil.

Tuberculosis (TB) is related to poor factor for people with human immuno- in the 1990s with TB control policies
living conditions and is an aggravating deficiency virus (HIV) infection––one based on primary health care. The care
that has repercussions on mortality network for AIDS is relatively recent,
* Official English translation provided by the Pan from AIDS in Brazil (1) and is a reality however, and control efforts concentrate
American Health Organization. In the case of dis- throughout Latin America (2). People on the secondary and tertiary levels of
crepancy between the two versions, the Spanish
original shall prevail. with this coinfection are up to 34 times care (4). In the state of Ceará, poverty
1
Institute of Health, Secretariat of State for more prone to developing tuberculosis and low levels of schooling also contrib-
Health of São Paulo, São Paulo, Brazil. Send than the general population and HIV ute to an increased relevance of TB/HIV
­correspondence to Silvia Helena Bastos de Paula,
­silviabastos58@gmail.com. ­infection is often diagnosed as tubercu- coinfection, increased reactivation of la-
2
STDs, HIV/AIDS Technical Area, Secretariat of losis develops (3). tent infections, and problems with ad-
State for Health of Ceará, Ceará, Brazil.
3
Tuberculosis Technical Area, Secretariat of State
The public network for TB treatment in herence to treatment. The cure rate
for Health of Ceará, Ceará, Brazil. Brazil was structured and decentralized dropped from 73.2% in 2004 to 59.2% in

Rev Panam Salud Publica 41, 2017 1


Original research Bastos de Paula et al. • Protocol for managing tuberculosis/HIV coinfection

2014, and the dropout rate in 2014 (12.7%) at facilitating improvements in pro- Data collection
is above the 5% rate the World gram im­ plementation through re-
Health ­ Organization (WHO) considers search that is embedded within those Data were collected between April
acceptable (5–8). programs, conducted by the Alliance and June 2015, based on secondary
In Brazil, a Ministry of Health policy for Health Policy and Systems Re- data sources: reports from the National
on TB/HIV coinfection calls for HIV test- search (AHPSR), in collaboration with Census of Health Facilities (CNES), the
ing for all persons affected by TB, and for the Pan American Health Organiza- ­Information System for Notifiable Dis-
the tuberculin test (PPD) and treatment tion (PAHO). The iPIER model consid- eases (SINAN), and the Mortality In-
of active pulmonary TB and latent infec- ers program implementers to be key formation System (SIM). The baseline
tion by M. tuberculosis (LTBI) in people research agents in order to understand for structures and processes in the 22
infected with HIV (9). health systems deficiencies that create services was established on the basis
In 2013, a clinical protocol was adopted barriers to implementation, and to of the answers to seven sets of ques-
for managing TB/HIV coinfection, as part identify solutions. Research on pro- tions on: installed capacity and physi-
of the clinical protocol of therapeutic direc- gram execution is embedded within cal structure, human and material
tives for managing HIV infection in adults existing processes in order to support resources, investigation of diagnosed
­
(10), for implementation in specialized care the effectiveness of health policies tuberculosis cases, surveillance and in-
services for people with HIV infection. De- through research conducted as a part dicators, diagnostic methods, and in-
spite the Ministry of Health adopting the of the implementation process. A de- tervention and therapies. The
new protocol, there is still a significant lag tailed description of how the research qualitative stage used focus groups
between the national average and imple- methodology is applied can be found (service administrators, professionals,
mentation levels in the state of Ceará. In in the iPIER concept paper (12) and and users) to learn about experiences in
Brazil, 69% of subjects diagnosed with TB the study on evaluation of TB-HIV/ access, utilization, and possible barri-
were tested for HIV, with 10% coinfection AIDS treatment protocol implementa- ers that could impact implementation
in 2014. The 58.2% testing rate in Ceará is tion in specialized care services in the of the protocol.
below the national average; coinfection state of Ceará (6). To conduct the eval- Focus groups were the principal
stands at 14.6% and has been trending up- uation, the team prepared a flow chart sources of primary data. The data col-
ward in the last two years (5, 11). summarizing the stages of the study lection tools were: a set of key topics to
In Brazil’s health system, specialized (Figure 1). draw out opinions about the services
care services are the preferred location The study involved two public health from each focus group. Questions were
for managing persons with TB/HIV institutions and one nongovernmental tailored to the characteristics of the
coinfection (9). The challenge for health organization—the Rede Nacional de Pes- participants and the priority agenda
administrators in Ceará is promoting in- soas Vivendo com HIV [National Network (for users: tuberculosis, access, and
creased access to the care recommended of People Living with HIV]. The study opinion about the service; and for pro-
in the TB/HIV coinfection protocol, by team was comprised of five researchers: fessionals and administrators: knowl-
investing in the full functioning of the three from the tuberculosis program, one edge about the existence of the protocol,
state and municipal care network (6). from the HIV/AIDS program, and one availability in their service, utilization,
In the case of TB/HIV coinfection, scientific investigator. acceptance, and implementation).
there are thought to be barriers related to The research protocol was submitted
professional teams resisting responsibil- to committees on Brazil’s platform in Data analysis
ity for the health of persons with TB/ February 2015 (registration number
HIV coinfection, as well as fragmented CAAE 42719815.3.000.5469, Resolution The quantitative data were orga-
monitoring by local and regional govern- 466/2012 of the National Health Coun- nized in a database, according to the
ment AIDS and tuberculosis control cil). After it was approved in Brazil, it level of complexity of the health
programs. was sent to PAHO’s Ethics Review ­system, testing infrastructure, pharma-
Based on the aforementioned, this Committee (PAHOERCS 2015.04-0021),
­ ceutical inputs, investigation of con-
study aims to identify strategies for im- receiving final approval from both com- tacts, and treatment of LTBI data were
proving adoption of the TB/HIV man- mittees in April 2015. then entered into STATA® 11.0 software.
agement protocol through evaluation The processed data were presented to
research, with the participation of the Location of the study administrators and health profession-
network of health services, administra- als at a seminar. The qualitative data
tors, and professionals as key research The state of Ceará is located in the were obtained in the focus groups,
agents with a commitment to improving Northeastern region of Brazil and has a transcribed and submitted for content
user access. territory of 148,825 km2 and a population analysis, and a set of techniques
of 8,452,381. In all, 75% of the population was established for analyzing dia-
MATERIALS AND METHODS is concentrated in urban areas, due to cli- logues using systematic, objective pro-
matic factors, lack of water, and poverty cedures for describing the content of
Study design in the countryside. Individual and social the messages, aimed at the inference
vulnerabilities contribute to the spread of knowledge related to the conditions
This project followed the iPIER of tuberculosis and the AIDS epi- in which they were produced or re-
meth­odology, a new initiative aimed demic (11, 13). ceived (14).

2 Rev Panam Salud Publica 41, 2017


Bastos de Paula et al. • Protocol for managing tuberculosis/HIV coinfection Original research

FIGURE 1. Implementation flow of TB/HIV coinfection management in specialized care infrastructure with multidisciplinary
services in Ceará, Brazil, 2015 teams, laboratory, radiology, pharmacy,
equipment, and physical area
Health programs and policies (­Figure 4). The rest had only physicians
- State Tuberculosis Control Program / State STD/AIDS Program (Health Promotion and Protection and nurses. The majority of the profes-
Office, Secretariat of Health of Ceará, Brazil) sionals were physicians (72), followed
- TB/HIV coinfection management policy by nurses (40), pharmacists (23), social
workers (22), psychologists (22), and
biochemists (16). With regard to the
Problems and barriers to implementation
training of professionals to manage
Difficulties in terms of acceptance and utilization of the protocol for managing TB/HIV coinfections in Ceará’s
specialized care services: TB/HIV coinfection, in the period
1. Teams’ resistance to assuming responsibility for the treatment of persons with HIV/TB coinfection
2012-2014, the physician teams in 14
services (63.6%) and the nursing teams
2. User participation in co-management of the services is lacking or incipient
in 11 (50%) were found to have received
3. Insufficient structure for managing airborne diseases
training; while social workers, bio-
4. Insufficient external and internal evaluation and monitoring of service quality chemists, and psychologists, in the ma-
jority of the services, had not received
Implementation strategy (S) specific training until 2015.
S.1. Analysis and discussion of the TB/HIV coinfection policy at the local level (Ceará), identifying the The services in the capital were better
barriers to implementation of the protocol in specialized care services: organized for managing TB/HIV coin-
• Meeting to present the project and protocol fection: most (75%) conducted the PPD
• Focus group test, LTBI was treated, and treatment reg-
• Report
imens for TB and LTBI were in place.
Half of the services in the interior offered
S.2. Promote the empowerment of users and entities of HIV+ people:
the PPD test, 10% had specific drugs for
• Promotion of user participation in research coordinated with their representative entities
tuberculosis, and 30% had available
• Meeting with representatives of nongovernmental organizations on the problem of AIDS in the state of treatment for LTBI (Figure 5).
Ceará to mobilize users for the focus group.
S.3. Prepare flow of TB/HIV care including implementation of TB/HIV protocol directives in specialized
care services: Qualitative aspects of protocol
• Workshop on design of TB/HIV care flow in specialized care services implementation

Modifications in health programs and policies (M)


The focus group qualitative method
encouraged discussion and the ex-
M.1. Protocol accepted by the specialized care services in a sustainable manner
change of ideas among the participants
M.2. Integration of users and entities active in protecting the access of HIV+ people to the TB/HIV, STD, AIDS,
in each group (administrators and
and TB control programs, through programming and participatory planning with users and teams
service managers, professionals and
­
M.3. State coordination of both programs, with consideration given to the structure profile and process of
specialized care services and the current adaptation plan users).
With regard to care, the user popula-
M.4. TB/HIV care flows used in specialized care services
tion of specialized care services noted:
M.5. Monitoring guidelines integrated into routine monitoring visits.
STDs = sexually transmitted diseases; AIDS = acquired immunodeficiency syndrome; HIV = human immunodeficiency virus. “I have witnessed, heard stories, right? (...)
I am afraid to go to the post [primary care
unit for treating tuberculosis] and for some-
one to find out that I am HIV positive and
RESULTS the Unified Health System (SUS), which tell my family.”
helped determine the structure, availabil-
“Yes, the units need to get the skills to treat
Structure of the care network for ity of physical space, and teams (Figure 3).
TB patients … if people know that someone
people living with HIV/AIDS in The study found that 10% of the ser-
has tuberculosis, they already keep a cer-
the state of Ceará vices conducted imaging and 20% used tain distance, opening doors …”.
the sputum test to detect acid-fast bacilli
The care network for people infected (AFB) for patients with HIV. The services “[Tuberculosis] is a disease that still has
with HIV in the state of Ceará is com- in the interior of the state, compared much more stigma than HIV itself.”
prised of 22 specialized care services––12 with those in the capital, have deficien-
in the capital and 10 in the interior, where cies in equipment infrastructure and How the teams responded to the TB/
the epidemic has greater epidemiological team training, although half of them had HIV protocol:
importance (Figure 2). a physical structure that surpassed that
“Only nurses received the protocol.”
The distribution of specialized care ser- of services in the capital (Figure 4).
(Administrator)
vices in the state health network varied de- With respect to the teams in the
pending on their level of integration 22 specialized care services, only six “I am not familiar with the protocol (…) the
(primary, secondary, and tertiary care) in (27.2%) were found to have complex physician is always requesting the sputum

Rev Panam Salud Publica 41, 2017 3


Original research Bastos de Paula et al. • Protocol for managing tuberculosis/HIV coinfection

FIGURE 2. Location of specialized care services and their distance from the capital: “… in terms of HIV-TB, I never did any
Fortaleza, Ceará, Brazil, 2015. training; they sent me there, right? And ev-
erything that I learned was through reading
on the Internet and seeing what was hap-
Fortaleza—12 services—Capital
pening there.” (Professional)

Caucaia—1 service—20 km
Implementation of the protocol in
practice:
Maracanaú—1 service—30 km
“Tuberculosis within the specialized care
Quixadá—1 service—178 km service is a new development; before, our
HIV patients, when they were diagnosed,
Aracati—1 service—148 km were going to the basic health unit [primary
care] to be treated. And now with this new
Cascavel—1 service—60 km
system [Protocol] (…) when it opened, then
Russas—1 service—168 km
treatment started in our unit.”
(Administrator)
Sobral—1 service—230 km
In the focus groups, the implementa-
Brejo Santo—1 service—500 km tion barriers identified include (but are
not limited to): discrimination against
Juazeiro do Norte —1 service—600 km and stigmatization of tuberculosis, insuf-
ficient human resources, low level of
Crato—1 service—630 km
commitment to addressing the two dis-
eases, differences in recommendations,
and frequency of consultations for TB/
HIV, excessive demand in specialized
services and inadequate structures in the
FIGURE 3. Profile of specialized care services by level of complexity in the health services for treating communicable
system, availability of physical space, and sustainability of services, Ceará, 2015
diseases.
% Capital Interior
100
DISCUSSION
90

80 With regard to services, the organiza-


tion model was found to be mainly di-
70 rected at caring for people with HIV/
60 AIDS.; Only six (27%) of the services
have specific TB control measures and,
50 where they do exist, they are carried out
40
haphazardly, modifying the protocol’s
recommendations on managing coinfec-
30 tion, including latent tuberculosis infec-
tion. Shortcomings were identified in
20
professional training to meet the needs of
10 people with TB/HIV coinfection. This
suggests a low level of investment by the
0
Ministry and the State in the ongoing re-
Primary Secondary Tertiary
fresher training needed for the entire
health care team.
test that is done now, a fast test, indeed! But “I really do not have many complaints. It is The services do not have a complex
the issue is that I do not have a good basis very practical to read.” (Professional) physical structure suited to caring for
for testing.” (Administrator) people with TB/HIV coinfection in terms
“I think that if the team is good and you of biosafety, access to drugs and comple-
“If it does not work, it is because they are read, you are able to implement it.” mentary TB diagnostic testing (Figure 4),
‘difficult’. You can have the entire team … (Professional) and consultations with specialists.
everyone with the protocol and every-
This complicates timely diagnosis of
thing needed to function, but if the per- “Everyone has a protocol in the service.”
son does not want to, it doesn’t happen.” tuberculosis.
(Professional)
(Administrator) One implementation strategy was to
“Honestly, I did the TB training, I returned provide feedback on the infrastructure
Points in favor of implementing the to the service and received the TB-HIV pro- profile. On that occasion, there was dis-
TB/HIV protocol: tocol.” (Professional) cussion of the administrative measures

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Bastos de Paula et al. • Protocol for managing tuberculosis/HIV coinfection Original research

FIGURE 4. Specialized care service infrastructure to manage TB/HIV coinfection in the state of Ceará, Brazil, 2015

% Capital Interior
100

90

80

70

60

50

40

30

20

10

0
AFB Laboratory Radiology Pharmacy
TB = tuberculosis; HIV = human immunodeficiency virus; AFB = acid-fast bacilli

FIGURE 5. Management of TB/HIV coinfection in specialized care services in the state of Ceará, Brazil, 2015

% Capital Interior
100

90

80

70

60

50

40

30

20

10

0
Conducts PPD Investigates Treats LTBI TB medication LTBI medication
contacts
TB = tuberculosis; HIV = human immunodeficiency virus; PPD = purified protein derivative skin test; LTBI = latent tuberculosis infection.

for adapting the physical space and re- monitoring with representatives of the teams in the SINAN, demand for TB
defining internal flows to care for peo- TB and HIV/AIDS programs was es- treatment programs for users of special-
ple with TB/HIV coinfection in the tablished to promote acceptance, adop- ized care service, the interest of admin-
specialized services. According to the tion, and utilization of the protocol as a istrators and professionals in the
study’s findings, the administrators strategy for expanding the supply and demand for and supply of training, re-
will be in a position to produce ma- coverage of care for people with TB/ quests for TB diagnostic testing sup-
terial appropriate for the widest possi- HIV coinfection. plies, and inclusion of TB/HIV on the
ble dissemination of the standards to To monitor adoption of the protocol, agendas of the collegiate bodies in the
teams and users, since immediate indicators were used such as the num- Single Healthcare System (SUS).
changes in the physical structure of the ber of new cases of TB/HIV coinfection The TB management protocol requires
services are not possible. Integrated reported by the specialized care service adherence to treatment, with medication

Rev Panam Salud Publica 41, 2017 5


Original research Bastos de Paula et al. • Protocol for managing tuberculosis/HIV coinfection

taken daily under supervision—an activ- is one of the implementation strategies to Conclusion
ity suited to primary care and one that be adopted by the TB and AIDS technical
specialized care services cannot do for areas for implementing the protocol; i.e. The iPIER evaluation model allowed
lack of infrastructure and insufficient un- coordinating with the regional pharma- for direct contact among administrators,
derstanding, on the part of the team, that ceutical representatives to redefine deliv- implementers, and investigators, and for
this is a primary care function (1, 3, 8, 15). ery flows of treatments in specialized a significant number of people to immedi-
Looking at the problem from the patient’s care services. ately commit to implementing the proto-
standpoint, some users indicated they To promote the changes agreed to with col. It also improved knowledge of the
would prefer to be treated close to home the teams, monitors were embedded in barriers to implementing the protocol in
in primary care, since otherwise daily the two programs (TB and HIV), to sup- terms of tuberculosis safety, diagnostic
travel to supervised treatment is difficult port implementation of the new flow measures, and users’ information needs.
(9, 10). Another group of patients fears charts for care and to provide guidance, The changes occurred during the evalua-
their serological status will be revealed in when necessary. Changes were made to tion process, benefitting decision-making.
their community (social stigma) and processes in the monitoring tool, with The scientific evidence base of the proto-
would prefer to take the treatment on the intention of planning continuing ed- col was put into practice in the services
their own, without professional supervi- ucation for the services and reaching and adopted by at least 55% of them.
sion. The two situations suggest that coor- agreements with municipal and regional
dination is required to respect patients’ health administrators for indicator Acknowledgments. The authors are
decision-making rights (13). In the health monitoring. grateful for the support of Ludovic Rev-
system, standards and directives need to The problems identified in this research eiz, Nhan Tran, Etienne Langlois, Janaina
be tailored to users’ needs and autonomy, are useful in ongoing learning and educa- Sallas, Yurani Sandoval, Sebastián García
respecting the principles of decentraliza- tion processes for teams and administra- Martí, Ariel Bardach and the entire iPIER
tion and local capacities. tors (12, 15). The field interventions in the project team.
This fact is likely the result of the exist- services and with users produced some
ing primary care model and it is therefore signs of changes that were confirmed in Funding. This study was financed by
logical that professionals working on the the interviews, the field visits, the AHPSR (WHO). PAHO provided tech-
front line of primary care are allocated the self-evaluation instrument completed in nical cooperation for implementation
resources to increase capacity. Another September 2015, and the final seminar. of this project. In the context of the iP-
critical factor hindering implementation These included, most notably, an increase IER program, the Institute of Clinical
of the TB/HIV protocol is the limited in dissemination of the protocol among and Health Effectiveness (IECS) pro-
availability of supplies and drugs to treat administrators, professionals, and user vided technical assistance for develop-
tuberculosis in the specialized services: representatives; inclusion of the protocol ing the protocol and implementing the
only eight TB services had the appropri- in the guidelines of the routine meetings project.
ate antibiotic regimens for tuberculosis. in the services; more internal discussions
There is a systemic factor related to the on the problems and pathways for incor- Conflicts of interest. None declared
distribution flow of TB supplies and porating the protocol into the services; by the authors.
drugs, whereby the basic network has and changes in attitude among adminis-
priority. The pharmaceutical services in trators regarding implementation (dis- Declaration. The author is responsible
regional health bureaus, which are re- cerned through actions such as requests for the opinions expressed in this text,
sponsible for supplying the health net- for record books for coinfection care, cop- which do not necessarily reflect the opin-
work, are not always responsive to the ies of the protocol, and additional training ion or policy of the Revista Panameri-
need to modify distribution. This sug- on tuberculosis), as well as increased de- cana de Salud Pública/Pan American
gests that a change in the dialogue with mand from the TB services for supplies Journal of Public Health (RPSP/PAJPH)
pharmaceutical services is needed. This for TB management. and/or of PAHO.

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RESUMEN Objetivos.  Identificar barreras y estrategias para la implementación del protocolo


“Manejo de coinfección por tuberculosis y virus de inmunodeficiencia humana (TBC/
VIH)” en los servicios de asistencia especializada (SAE) de Ceará, mediante investiga-
Evaluación de la ción evaluativa.
implementación del Métodos.  Estudio desarrollado siguiendo la metodología iPIER, una nueva inicia-
tiva con el propósito de apoyar mejoras en la ejecución de programas de salud a través
protocolo de manejo de de investigaciones integradas en ellos acerca de su ejecución. Se recogieron datos de
coinfección de tuberculosis estructura y procesos de 22 servicios y se exploraron las barreras mediante cuatro
y VIH en los servicios de grupos focales, con 28 participantes, desde el punto de vista del equipo de salud, los
administradores y los usuarios. Las discusiones fueron transcritas e interpretadas
asistencia especializada del según los objetivos del estudio.
estado de Ceará, Brasil Resultados.  Los datos de estructura y procesos revelaron que seis servicios realizan
acciones de manejo de coinfección TB/VIH y 16, no lo hacen. Las barreras fueron:
desconocimiento del protocolo en los equipos, ausencia de guías de práctica clínica en
los servicios, inserción de los SAE en los tres niveles del sistema de salud, espacios
inadecuados para tratar enfermedades de transmisión aérea y falta de comunicación
con los sectores de atención primaria de salud para los traslados. Se discutieron los
resultados con equipos y administradores en seminarios en los servicios y con los
responsables de los programas de enfermedades de transmisión sexual, virus de
inmunodeficiencia humana, sida, hepatitis y tuberculosis.
Conclusiones.  El diálogo directo entre administradores, ejecutores, usuarios e inves-
tigadores generó conocimiento sobre los servicios y elaboración conjunta de modifica-
ciones de flujos para la aceptación y utilización del protocolo; sin embargo, entre los
usuarios persiste la resistencia para adherirse al tratamiento.

Palabras clave Tuberculosis; VIH; servicios de salud; protocolos; Brasil.

Rev Panam Salud Publica 41, 2017 7

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