Background
Despite several advances in treatment and management, syphilis remains a major public health problem worldwide. Nearly 1.5 million pregnant women are infected with syphilis each year [
1], and in Africa it was estimated that the prevalence of syphilis among antenatal care (ANC) attendees was 2.2% in 2013 [
2]. In the Democratic Republic of the Congo (DRC), the prevalence of syphilis among ANC attendees was 3.3% [
3] whereas it was 4% in Zambia [
4]. It is estimated that half of all pregnant women with untreated syphilis will experience adverse birth outcomes such as miscarriage, stillbirth, preterm delivery, low birth weight, neonatal death, and neonatal infection [
1,
5,
6].
In order to prevent these outcomes, the World Health Organization (WHO) recommends universal syphilis screening, and treatment of pregnant women testing positive, as routine practice during ANC [
7,
8]. Administering a single dose of long-acting penicillin prevents congenital syphilis. Either one (primary or secondary disease) or three (latent disease) penicillin doses are effective to treat maternal syphilis [
9].
However, several of key barriers to implementation of universal prevention of congenital syphilis screening have been identified. These barriers range from patient-level factors (e.g., late entry into ANC, costs borne by patients, and the need to return at a later time for results) to facility-level constraints (e.g., health worker absence or insufficient training; provider fears around side effects of benzathine penicillin treatment despite their rarity; and use of a diagnostic procedure that requires infrastructure that facilities may not have consistent access to such as laboratory capacity, cold storage, and electricity) and system-level issues (e.g., low prioritization of syphilis screening and treatment by health policy makers) [
10‐
12].
In accordance with theories of implementation [
13,
14], the intervention proposed by the Preventing Congenital Syphilis Trial (PCS Trial) (see Additional file
1: Appendix S1) was developed specifically to target barriers to implementing best practices identified in the literature, including those mentioned above [
15]. As such, the intervention consists of the use of point-of-care rapid syphilis diagnostic tests (RDTs) in pregnant women and same-day treatment of those who screen positive with one dose of benzathine penicillin 2.4 MU, plus a behavioral intervention based on theories of health behavior change [
16‐
18]. Specifically, the behavioral intervention consists of (1) identification and training of opinion leaders among ANC providers and (2) packaging the RDTs and pre-measured dosages of benzathine penicillin, erythromicine, anaphylaxis treatment together into ready-to-use syphilis diagnosis and treatment kits. The opinion leaders will be tasked with disseminating, implementing, and maintaining best practices among their peers using reminders, routine monitoring and feedback (Additional file
1: Appendix S1).
In addition, to ensure that the trial strategy would be effective, culturally appropriate, and acceptable to women and ANC providers, we conducted qualitative formative research to assess women’s and providers’ perspectives. The formative research aimed to identify factors that may hinder (barriers) or enable (facilitators) the syphilis screening at first ANC visit and to provide treatment to positive women at the same visit in order to identify additional, context-specific factors that may influence the implementation of PCS Trial intervention. Based on those findings we analyzed the feasibility and acceptability of the proposed intervention. In this paper, we present the results of the qualitative research and recommendations to tailor the intervention.
Methods
Study design and setting
The study used inductive inquiry consistent with the grounded theory approach [
19] and was conducted in accordance with qualitative research guidelines [
20,
21]. It included in-depth semi-structured interviews with clinic administrators, group interviews with health providers (groups were natural groups) [
22], and focus groups with pregnant women. It was performed from July to September 2015 during the preparatory phase of the PCS Trial.
Key informants were recruited in 11 of the 26 primary care clinics (PCCs) participating in the PCS trial. Clinics were purposively selected to cover all types of PCCs that will be included in the PCS Trial. In the DRC, we included 8 clinics (2 public, 2 private not-for-profit, and 4 for-profit private) located in the eastern part of Kinshasa, where seven of wich had already implemented the Prevention of Mother to Child Transmission of HIV (PMTCT) program. In Zambia, where all the clinics participating in the PCS Trial are public and have implemented the PMTCT program, we included three clinics.
Participants and sampling
Interview and focus group participants were purposively-selected to cover three target groups: clinic administrators, health care providers, and pregnant women.
Clinic administrators and health care providers
In Kinshasa, we conducted five in-depth semi-structured interviews with individuals responsible for overseeing the clinics, henceforth referred as “clinic administrators”, and eight group interviews with health care providers (henforce “providers”; 4–5 participants per group). In Lusaka, we conducted three group interviews with health care providers (4–5 participants per group). Clinic administrators were not included in Lusaka. All providers present at the moment of the clinic visit were invited and all agreed to participate. The providers ranged from physicians, nurses, midwives, lab technicians responsible for testing pregnant women, counselors (trained in Psychosocial and HIV counseling, and responsible for patient counseling on HIV and other Sexually Transmitted Infections, including Syphilis), and nutritionists (See Table
1).
Table 1
Characteristics of the participants, by country
Characteristics of study participants | • N of PCCs = 3 | • N of PCCs = 8 | • N of PCCs = 11 |
• N of authorities = 0 | • N of authorities = 5 | • N of authorities = 5 |
• N of Providers = 13 | • N of Providers = 37 | • N of Providers = 50 |
• N of Pregnant women = 13 | • N of Pregnant women = 44 | • N of Pregnant women = 57 |
PCCs Authorities (Individual Interviews) | 0 | 5 | 5 |
Female | 0 | 2 | 2 |
Male | 0 | 3 | 3 |
Health Providers | 13 | 37 | 50 |
Female | 8 (62%) | 14 (38%) | 22(44%) |
Male | 5 (38%) | 23 (62%) | 28(56%) |
Age Median | 40 (32–45) | 38 (22–65) | |
Speciallity |
Midwife and nurse | 4 (31%) | 29 (78%) | 33(66%) |
Physician | 1 (8%) | 0 | 1(2%) |
Lab Technician | 3 (23%) | 8 (22%) | 11(22%) |
Counselors | 4 (31%) | 0 | 4(8%) |
Nutritionist | 1 (8%) | 0 | 1(2%) |
Pregnant women (Group Interviews) | 13 | 44 | 57 |
Age Median | 24 (20–26) | 22 (17–41) | |
Parity: |
Primiparous | 4 (31%) | 27 (61%) | 31(54%) |
Multiparous | 9 (69%) | 17 (39%) | 26(46%) |
Education |
Elementary school incomplete | 1 (8%) | 1 (2%) | 2(4%) |
Elementary school completed | 1 (8%) | 3 (7%) | 4(7%) |
High school incomplete | 6 (46%) | 23 (52%) | 29(51%) |
High school completed | 1 (8%) | 16 (36%) | 17(30%) |
University | 4 (31%) | 1 (2%) | 5(9%) |
Questionnaires for semi-structured interviews and group interviews were developed based on the study objectives and included the following themes: (1) routine process during first ANC visit, (2) availability of resources for syphilis screening and treatment, (3) implementation of policies regarding ANC and prevention of congenital syphilis, (4) providers’ knowledge and skills to test and treat, (5) providers’ attitudes towards syphilis test and treatment, and (6) acceptability of the PCS Trial intervention. (See Additional file
2: Appendix S2 and Additional file
3: Appendix S3).
Pregnant women
In Kinshasa, we conducted eight focus groups with pregnant women (4–8 participants) in eight clinics. In Lusaka, we conducted three focus groups with pregnant women (4–5 participants) in three clinics (See Table
1). Focus group were conducted with women attending their first ANC visit. Health facility staff assisted in identifying potential study participants. Snacks and beverages were offered to participants.
The focus group questionnaire was developed based on the study objectives, and included the following themes: (1) acceptability of syphilis screening and treatment at the first ANC visit, (2) knowledge about syphilis and prevention of mother-to-child transmission, and (3) current level of participation in the decision making for clinical procedures during pregnancy including syphilis testing and treatment. (See Additional file
4: Appendix S4).
Procedure
Researchers trained in qualitative methods were appointed in Kinshasa by the DRC-based research team to conduct the data collection. In Lusaka, data collection was managed by researchers from the trial coordination institution (Institute for Clinical Effectiveness and Health Policy - IECS) and a trained local researcher. The protocol, data collection guidelines, and data analysis strategy were agreed upon by all researchers involved in data collection and analysis.
Interviews and focus groups lasted between 40 and 60 min. In Kinshasa, interviews with professionals were conducted in French and focus groups with women attending ANC were conducted in Lingala. In Lusaka, two interviews with health providers were conducted in English by a researcher from IECS, and the rest (both health providers and pregnant women) were conducted in a local language (either Nyanja or Bemba) by local researchers.
Data collection
All interviews and focus groups were audiotaped and subsequently transcribed in preparation for analysis. In the DRC, the transcripts were analyzed in French and Lingala, while in Zambia, transcripts were translated into English for the analysis.
Data analysis
The written transcripts were entered into ATLAS.ti version 7 (2013) qualitative data management software (Scientific Software Development, Berlin, Germany) and were coded according to a codebook based on themes included in the questionnaires and supplemented by a grounded theory-based approach to capture emergent themes [
19].
Thematic analysis was done for each target group. Then matrices were developed to facilitate comparisons across the transcript materials and to retain the context of the data (i.e. sites, clinic, and type of informant). Finally, data was abstracted and interpreted. As part of this analysis, direct quotations representative of the participants’ opinions were selected and are included in this manuscript to illustrate the findings. In order to protect the identity of the informants we only provide information of type of informant and city (into brackets).
Qualitative data were categorized to reflect barriers and facilitators for the implementation of universal syphilis screening at first ANC visit and same-day treatment of syphilis-positive women with benzathine penicillin. Barriers and facilitators were grouped into three categories: (1) system-level factors; (2) health providers’ knowledge, practices and skills; and (3) women’s knowledge, preferences, and behavior. Following these findings, we also described the acceptability and feasibility of implementing each intervention component of the PCS Trial and finally, we list the recommendations made to tailor the intervention.
Results
As shown in Table
1, a total of 112 individuals participated in the formative study: five clinic administrators, 50 health care providers, and 57 pregnant women. Participant characteristics varied between the two countries. While 44 % of the total health care providers were female, in Lusaka the majority were female and in Kinshasa the majority were male. Midwifes and nurses represented 78% of ANC providers in Kinshasa and 31% in Lusaka. The age of providers ranged from 22 to 65 years old in both countries. Overall, around half of the pregnant women interviewed were in their first pregnancy, while in Lusaka the majority were multiparous (69%) and in Kinshasa the majority were primiparous (61%). The median age was 24 and 22 years old, respectively (age range 17–41 in both sites). The vast majority (96%) had completed primary school.
Barriers and facilitators for testing and treating syphilis at first ANC visit
Table
2 describes factors reported by women, health providers, and clinic administrators that could be barriers and facilitators for syphilis screening and treatment to prevent congenital syphilis. To facilitate understanding, the results are organized into three main sections: first, respondents’ general comments about the current state of practice; second, their thoughts about the feasibility of the PCS Trial’s same-day screening and treatment protocol; and third, their perceptions about the utility, feasibility, and acceptability of the behavioral components of the intervention. Within these overarching categories, we have further stratified the reporting of the results into system- and facility-level factors, provider-level factors, and woman-level factors.
Table 2
Barriers and facilitators for same-day screening and treatment in antenatal care to prevent congenital syphilis
System level | • Structural constraints (beyond the health care system) • Fragmentation of the health system • Existence of ANC guidelines in conflict with proposed intervention • Poor accessibility of clinics (geographical and functional) • Staff and product shortages at the PCCs | • Existence of national guidelines for ANC best practice recommendations (including testing and counselling at first visit) • Public health initiatives to improve quality of care |
Health providers’ level | • Lack of knowledge and training about evolving best practices • Reservations regarding same-day screening and treatment | • Recognition of importance of early treatment • Willingness to improve methods for testing |
Pregnant women level | • Late enrollment in ANC • Lack of knowledge about syphilis, consequences and treatment • Stigma | • Recognized importance of ANC visits • Health education provided at the clinics • Acceptance of same-day screening and treatment at first ANC visit |
System level
This category covers factors related to the health system that may affect the success of implementing a universal ANC syphilis screening and treatment program. It also includes macro-level factors beyond the scope of the health system, such as the infrastructure and economic situation of countries.
Health care providers’ level
Feasibility of the implementation of the PCS Trial intervention components
The intervention proposed by the PCS Trial seems acceptable for clinic administrators, health providers and pregnant women at the PCCs. The implementation of the intervention is also feasible.
Supplies
Acceptability of the point of care rapid tests: In DRC, providers routinely use this kind of tests for syphilis screening in most clinics, but in Zambia the RPR test is used. That said, there are successful experiences regarding the implementation of rapid test for HIV in both countries and the tests are conducted by different providers: lab technicians, midwifes/nurses, and lay counselors. Overall, providers are familiar with rapid tests in both countries.
Acceptability of test and treatment kits: The proposal to have all the supplies needed for the day in boxes at the visit room is well accepted. Respondents are willing to have all the supplies easily accessible.
All providers said they are willing to “receive syphilis rapid test kits to enable us to work well.” (Health Provider, Kinshasa )
Tailoring the “PCS Trial” intervention
Based on the findings, we identified specific actions required to tailor each component of the intervention to the two contexts:
-
Initially, the planned intervention proposed screening and treatment supplies packed in kits for individual women (including point-of-care rapid test kits for syphilis diagnosis; treatment kits with benzathine penicillin 2.4 MU, syringe and needle, instructions, and information on side-effects; and anaphylaxis treatment kits for emergency use if needed). However, after the formative research it was chosen to use plastic boxes that contained all of the necessary supplies for the day; the boxed supplies could then be replaced the following day.
-
The process for selecting opinion leaders was changed from a discretionary selection to be completed using a peer nomination. Consequently, a Hiss questionnaire was adapted to permit peer nomination, and each clinic selected 2–3 opinion leaders.
-
Opinion leader training was tailored to address specific needs observed during the formative phase. In particular, training focused on (1) identifying priority health conditions to be screened and treated during pregnancy, (2) showing evidence about the utility of treating women at first visit even though their partner has not been treated yet, (3) reviewing how to screen and manage maternal syphilis, and (4) ensuring optimal stock management.
-
Placing Reminders: Simple messages and figures to remind prenatal health providers to conduct the screening procedures and to provide treatment for those women found positive were accepted and suggested to be developed by the selected opinion leaders during the training provided by the study coordinators.
-
Incorporation of a supportive supervision component. The initial intervention suggested that a coordinator from the local research teams would meet periodically with each facilitator team to assess the completion of activities and address unexpected problems. However, based on the formative research this was changed to a model of supportive supervision to support the opinion leader while they implement the intervention components at their clinic. A specific guideline for supportive supervision was developed, as well as a direct observation guideline. The supportive supervisor will provide monitoring information (clinic flow charts) that the facilitator can then use for feedback and academic visits.
-
Similar projects in the literature recommend including a component to empower the population for their screening and treatment. However, the findings from this study indicated that a patient empowerment component to the PCS Trial would not necessarily influence health provider behavior.
Discussion
This formative research provided useful information to tailor an intervention intended to prevent congenital syphilis in urban clinics in two African countries. Barriers for the successful implementation of same-day screening and treatment for syphilis at first ANC visit exist at system-, facility- provider- and patient-levels. Findings are similar than the reported in other studies [
23‐
25]. System-level barriers include poor geographical and functional accessibility, lack of human resources and supplies, and established norms that need to be changed in order to implement the new practice, as well as the broader economic situation in these countries. Products and supplies are provided by national programs, NGOs, or international initiatives, but they are frequently depleted. The frequent stock-outs may be due to poor managerial capacities of health workers [
26].
Among ANC providers, we identified barriers such as low awareness regarding the evidence of effectiveness of single-dose benzathine penicillin to prevent congenital syphilis, and reservations towards treating women on the first visit. Lack of training of health providers was identified as a barrier to the screening and treatment of pregnant women during ANC, confirming the findings of other authors, such as Watson et al. in Tanzania [
24].
From the woman’s perspective, we identified barriers such as late enrollment in ANC due to transportation or cost, and lack of knowledge and information about syphilis and its treatment. As highlighted by other researchers, cost of treatment can be a critical barrier for syphilis screening and treatment, especially for those women who are totally financially-dependent on their male partner [
10,
11]. Other studies have also reported that long distances to screening facilities and lack of supplies for syphilis screening and treatment are associated with delay or failure to screen [
10,
25,
26].
Given these barriers, promotion of evidence-based practices around syphilis screening and treatment presents a real challenge. However, facilitators of change exist as well. These include the existence of national guidelines currently used at clinics, which recomend syphilis screening at the first ANC visit. Overall, providers seem to have a positive attitude towards improving current practices. In addition, pregnant women understand the importance of being tested, and accept being tested and treated during the same visit if positive.
Findings confirmed that the evidence-based practice of testing for syphilis at the first ANC visit and treating with benzathine penicillin was acceptable to both providers and patients. Regarding the implementation of the PCS Trial intervention strategy, we found that the components included in the intervention were considered acceptable and feasible for implementation at the PCCs. However, the intervention was tailored to better fit the context based on the findings of this study. Specific modifications were proposed in the light of the findings of this formative research. The most substantial change was the addition of a supportive supervision component that consisted of formal support to the opinion leaders from the local intervention coordinator on a monthly basis. Other changes included use of an HISS questionnaire to select the opinion leaders by peer nomination, design of the opinion leader training, and type of reminders. Finally, the formative research indicated how to best pack the products and supplies to fit local needs.
Each of these changes was made to tailor the intervention to the local context, given that – per principles of implementation science – interventions must be right-sized for their implementation contexts in order to be effectively operationalized. Most importantly, in this study, the researchers and implementers worked in close collaboration, making joint decisions about the design of the research intervention, so that the final intervention was informed by implementers’ understanding of what would work in the field.
Study limitations
As with all qualitative research, findings helped researchers discover and explore themes, generate illuminating and illustrative personal narratives, but they may not be generalizable to the larger population of practitioners or pregnant women in these countries. We were aware about the possibility about obtaining social desirability responses (the wish to appear as a morally-worthy person to the interviewer). In order to minimize this bias in sensitive questions, as for example when asking pregnant women about the influence of their sexual partners regarding the acceptance of treatment if they test positive, we used indirect questioning – asking about what pregnant women in general feels and how they will behave – allowing respondents to project their own feelings onto others.
The study was conducted in urban settings in the capital cities of the countries participating in the study, so the findings may not be relevant for other urban or rural clinics. Findings were based on opinions and self-report rather than observation of actual practices.
Although the sample size in one country was smaller than in the other, findings are consistent across sites and we cover all type of clinics.
Conclusion
This formative research allowed us to identify factors that may hinder (barriers) or enable (facilitators) the same-day syphilis screening and treatment, and to identify additional, context-specific factors that may influence the implementation of the PCS Trial intervention. Based on those findings we tailored the intervention in order to be feasible.
Interventions that work well in controlled settings may fail during broader roll-out, in part because the controlled settings do not mimic real-world contexts. It is imperative, then, to design interventions from the start with an eye towards the constraints and assets of the context in which they will be implemented. Thus, formative research – research that occurs before an intervention designed and implemented – such as that conducted in this study, is a critical step in designing appropriate and effective interventions. In addition, including implementers and other end-users in intervention design is essential to developing interventions that will be both effective and feasible. These types of best practices are critical to help close the “know-do gap” and speed up progress on ensuring that evidence-based practices reach the populations in greatest need.
Acknowledgments
We want to thank the Zambian and Democratic Republic of Congo institutions, their health providers and patients who kindly accepted to participate in this research.
We thank Julius Mulenga for the data collection in Zambia and Prof Bruno Lapika and his qualitative research team for the data collection and thematic analysis at DRC. PCS Trial coordination teams in both countries for their help on organizing the data collection.
We thank STAG members and particularly Carl Bose for their useful inputs on the manuscript; and Rindcy Davis and Caitlin Williams editing it.
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