Assessment of the appropriate management of syphilis patients in primary health care in different regions of Brazil from 2012 to 2018

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Introduction
Cad. Saúde Pública 2022; 38(5):e00231921 In the three cycles, data were collected by previously trained interviewers using electronic forms on tablets for automated registration and submission to the central server at the Brazilian Ministry of Health. Continuous supervision of the field work was conducted to ensure the quality of the collected data and consistency checking using an electronic data validator. Each institution leading the external assessment was responsible for solving inconsistencies. More details about the PMAQ-AB methodology can be found in publications and documents from the Brazilian Ministry of Health 17,18 .
The data collection instrument contained structured questions prepared by the Brazilian Ministry of Health in partnership with the leading HEIs and was divided into three modules. The first module verified the infrastructure of the basic health units (UBS) and the second assessed the work process of the teams by interviewing health care professionals. The third module was answered by users who were present at the UBS on the day of data collection, addressing their perception of the care received.
For this study, information on the UBS infrastructure modules and the professional work process of the teams were used in the three assessment cycles. For the construction of the outcomes, available variables that were related to the infrastructure and work process for diagnosis, management, and treatment of syphilis were selected. Based on the identification of these variables, two outcomes were created: (1) Adequate infrastructure for diagnosis, management, and treatment of patients with syphilis: Affirmative answer to the presence of personal protective equipment (PPE), rapid syphilis tests, and benzylpenicillin benzathine. The affirmative answer to the three investigated items was considered as having an adequate infrastructure.
(2) Adequate work process for diagnosis, management, and treatment of patients with syphilis: Affirmative answer to the questions "Does the team request serology for syphilis?"; "Is the offer of services and referrals for pregnant women based on the assessment and classification of risk and vulnerability?"; "Does the team request HIV serology?"; "Is penicillin G benzathine applied at UBS?". An affirmative answer to the four investigated items was considered as having an adequate work process.
The adequate infrastructure outcome was assessed considering the number of UBS evaluated. For the adequate work process outcome, the number of health care teams investigated was considered. The variables of each of the outcomes for the three cycles of the PMAQ-AB were initially described. The prevalence of each outcome in each evaluation cycle was calculated. To identify the difference between cycles, weighted least square regression was done to estimate percentage annual changes in the prevalence values. A significance level of 5% was adopted. All analyses were performed using the Stata 15.0 statistical package (https://www.stata.com).
The three studies were approved by the Ethics Research Committee (CEP). Cycle I was approved by the CEP of the Medical School of UFPel via official letter (n. 38/2012); Cycle II had a favorable opinion issued by the CEP of Federal University of Goiás (opinion n. 487,055) on December 12, 2013; and Cycle III was approved by the CEP of the Medical School of UFPel with assent (n. 2,453,320). All participants signed an informed consent form. The authors declare no conflicts of interest regarding the study.

Results
On the external assessment of the PMAQ-AB, 13,842 UBS and 17,202 teams were assessed in Cycle I; 24,055 UBS and 29,778 teams in Cycle II; and 28,939 PHCCs and 37,350 teams in Cycle III. Table 1 lists the distribution of UBS and teams according to region, population size of the municipality, HDI-M, and family health coverage in each of the three cycles of the PMAQ.  In the three assessment cycles, the region with the highest prevalence of investigated PHCs was the Northeast (36.7%, 36.2%, and 41.6% in each of the cycles, respectively). In Cycle I, most teams were located in the Southeast Region (38.2%), while in Cycles II and III, most were in the Northeast Region (36.2% and 37%). Regarding size, most of the evaluated UBS and teams were located in municipalities ranging between 10,001 and 30,000 inhabitants. UBS and teams were prevalent in municipalities with high HDI-M (39.6% and 37.2%) in Cycle I and in municipalities with medium HDI-M in Cycles II and III (50.3% UBS and 43.9% teams from medium HDI-M municipalities in Cycle II and 51.3% PHC and 44.8% teams in Cycle III). In the three cycles, the number of PHC and teams investigated was greater in municipalities with 100% family health coverage (Table 1). Figure 1 shows the distribution of outcome variables. Among variables related to the infrastructure outcome, we observed that the low prevalence of rapid testing for syphilis in Cycle I (1.4%) increased in Cycle III (72.1%); in Cycle III, less than 70% of UBS had medication and PPE for the management and treatment of syphilis, especially penicillin G benzathine. From the work process outcome, we found that the use of penicillin G benzathine in the UBS increased about 26 percentage points (p.p.) between cycles, reaching 77.1% in Cycle III (Figure 1).
Regarding the prevalence of adequate infrastructure for diagnosis, management, and treatment of syphilis in Brazil, we identified that only 1.4% of UBS had minimal infrastructure in Cycle I, increasing to 17.5% in Cycle II and 42.8% in Cycle III, with an annual change of 7.0p.p. (Table 2).   Adequate infrastructure significantly increased in all regions among the three evaluations; however, the North and Northeast saw smaller increases. The presence of adequate infrastructure also progressively increased from Cycle I to Cycle III in all investigated municipality sizes -with greater annual change in p.p. in municipalities ranging between 100,001 and 300,000 inhabitants -and in the four investigated strata of HDI-M, particularly in Cycle III; the higher the HDI-M, the higher the prevalence of infrastructure. Similarly, municipalities with low HDI-M had an average 4.7p.p. annual change in adequate infrastructure whereas municipalities with high HDI-M reached 11.9p.p. In the three cycles, infrastructure prevalence was inversely proportional to FHS coverage: the lower the FHS coverage, the higher the prevalence of adequate infrastructure for diagnosis, management, and treatment of syphilis, with a difference of approximately 3.0p.p. between the annual change of municipalities with coverage up to 50% (9.5p.p.) and those with 100% coverage (6.2p.p.) ( Table 2).
The adequate work process for diagnosis, management, and treatment of syphilis, increased in about 30p.p. between Cycles I and III, with an average annual change of 5.7p.p. The Southeast Region had the lowest prevalence of adequate work process in Cycle III (69.4%) and the lowest annual change (3.8p.p.) between cycles. Larger municipalities had a higher prevalence of this research outcome in Cycle III (83.3%) and the annual change was greater in municipalities ranging between 10,001 and 30,000 inhabitants (7.3p.p.). The lower the HDI-M, the lower the prevalence of an adequate work process was in the three cycles; however, the annual change in municipalities with low, medium, and high HDI-M was two to three times higher than in those with very high HDI-M. Municipalities with up to 50% of FHS coverage had higher adequate work process prevalence in Cycle III (82.8%), but their annual change was almost twice smaller than that of municipalities with 100% FHS coverage (

Discussion
This study found that the proportion of adequate infrastructure and work process for diagnosis, management, and treatment of syphilis in Brazilian PHC significantly increased from 2012 to 2018. The studied outcomes improved in all regions, population sizes, categories of HDI-M, and FHS coverage of municipalities. Nevertheless, disparities persist, considering that the richest regions and larger municipalities with a higher HDI-M and lower FHS coverage improved the most. However, less than half of the assessed teams had adequate infrastructure to treat people with syphilis and, when considered individually, none of the items was mentioned by more than 75% of the teams. The literature often reports on the absence and the recent improvement of adequate infrastructure in PHC 15 . This reflects the recent federal government initiatives to reduce syphilis in Brazil, applied during the PMAQ-AB period, including: implementation of rapid tests in prenatal care  We emphasize the low availability of PPE in the evaluated services. Providing an adequate number of PPE in primary healthcare centers is a regulatory obligation of the employer, and the absence of equipment puts professionals at higher risk and exposure 21 . Though the literature rarely addresses absence of PPE, basic healthcare professionals, especially nurses, do not use these materials because they are insufficiently provided 22 . However, this topic has become relevant and widely studied against the backdrop of the COVID-19 pandemic, reinforcing the absence of sufficient supplies and the importance of these equipment in health care services 23 .
A proper management of syphilis requires early detection, immediate treatment of the patient and their sexual partners, and the screening and monitoring of these partners, with rapid tests and penicillin at least 24 . However, although the prevalence of these items has increased between cycles, they are not universally available. These findings corroborate the literature 26 , which suggests that deficient infrastructure, insufficient human resources, and insecurity in the patient's follow-up with the rapid reactive test and in the application of penicillin are barriers to the comprehensive care of an individual with syphilis in PHC 25 .
The Brazilian protocol for the control of STIs emphasizes the importance of, in the presence of a positive rapid test, starting treatment immediately even if the individual does not show signs and symptoms of syphilis, taking advantage of their presence at the UBS -especially if they are pregnant women, victims of sexual violence, people with a chance of loss to follow-up (who will not return to the service), people with signs and symptoms of primary or secondary syphilis, and people without a previous diagnosis of syphilis. However, treatment after the first reagent test does not exclude Cad. Saúde Pública 2022; 38(5):e00231921 the need for a second test, clinical and laboratory follow-up, and diagnosis and treatment of sexual partners 8 .
Our results also show the persistence of inequalities in the distribution of adequate UBS infrastructure in Brazil. These results corroborate other studies on this subject both in Brazil and in high-income countries such as the United States and England, emphasizing the greater fragility in caring for the poorest and most vulnerable, which strengthens the stigma and discrimination related to syphilis 26,27,28,29 .
The annual improvement pattern of adequate work process was similar to that of adequate infrastructure; however, the former reached more services in Cycle III (about 75%) since its initial situation was already more advantageous. The request for tests for HIV and syphilis and the referral of pregnant women at risk showed that these services are universally available in PHC, unlike the application of penicillin, which is still a problem despite the increasing numbers between the assessment cycles. In 2017, the Brazilian Ministry of Health published the agenda of strategic actions to reduce syphilis in the country, focusing on the training of professionals and the application of penicillin in PHC, considering that this medication can reduce the incidence of fetal and neonatal death by 80% and of congenital syphilis by 97% 30,31 . The increased proportion of penicillin application found in this study thus reveals the effectiveness of this and other public policies on the subject, reinforcing the need to maintain these strategies 31 .
We also found inequities in the adequacy of the work process, similarly to the consulted literature and other results presented 32 . Inequalities in care for syphilis go beyond context variables and are also directly related to individual socioeconomic and demographic characteristics, mostly affecting the poorest, those of lower schooling levels, and black men with less access to health care services 33 . Therefore, guaranteeing equity in PHC service in Brazil can help reduce the inequalities in the country, which have greatly increased in the last two years with the elimination and reduction of public policies for income distribution, with easier access to higher education and the acquisition of housing, and with the disqualification of the Brazilian National Primary Health Care Policy (PNAB) and the cutting of funding for health, especially for PHC 34,35 .
Although the infrastructure and the work process of health care teams for diagnosis, management, and treatment of syphilis in PHC improved, syphilis rates in Brazil showed a growing trend from 2012 to 2018, mainly in the population aged from 20 to 29 years, reaching 75.8 cases per 100,000 inhabitants in 2018 36 . Studies suggest that syphilis rates increased because of improved access to health services, diagnosis, and treatment, as well as changes in the registration of cases 36,37 . Nonetheless, the importance of tracking and monitoring cases and contacts to reduce the transmission of the bacterium is still unreported. Health surveillance is essential for the notification and epidemiological investigation of cases, and together with the PHC team, especially community health agent (ACS), it can develop strategies to break the transmission chain 38 . Actions for infected individuals and their sexual partners which seek to reduce infection and reinfection and provide early diagnosis, monitoring, completeness of drug treatment, and guidance on the subject are essential for the integral care of these individuals, possibly reducing the high number of cases.
However, this solution does not seem feasible in the current political scenario in Brazil considering: the lack of funds for the Brazilian Unified National Health System (SUS) (Constitutional Amendment n. 95, changes in Previne Brasil funding); changes in the PNAB; shortage of staff in the FHS; less ACS; focus in episodic acute complaints, disregarding work in the field and the responsibility with defined populations; and difficulty in coordinating teamwork 39,40,41 .
This study strengths include its scope, addressing three moments in time based on national PHC data, and the relevance of its subject, which still has limited literature. Regarding limitations, the relationship of adequate infrastructure and work process with the care received by users with syphilis in PHC could not be analyzed since data on these individuals is unavailable in the PMAQ-basic healthcare. Moreover, Cycle I could have had selection bias considering that, as the first cycle, only the best teams in the municipalities might have joined it.