Soil-transmitted helminth (STH) infections, due to their profound impact on human health and development, continue to be a health problem in low- and middle-income countries, particularly those located in the tropical and subtropical regions of the planet [1]. STH infections affect around 1.5 billion people worldwide [1,2]. Africa, particularly the region south of the Sahara, is the continent with the highest prevalence of helminth infections, especially those transmitted through soil and schistosomiasis [3,4]. The World Health Organization (WHO) has estimated that STH are responsible for 1.97–3.3 million disability-adjusted life years (DALYs) [5,6].

STH infections (particularly those caused by Ascaris lumbricoides, Trichuris trichiura, hookworms, and Strongyloides stercoralis) very rarely result in the death of the host. Certainly, the burden of these parasitic infections in terms of public health is less related to their mortality than to their chronic, and often imperceptible, effects on the health and nutritional status of the host [7,8].

In 2001, the 54^th World Health Assembly of the World Health Organization (WHO), recognizing the consequences of STH infections on the development of current and future generations, adopted a resolution promoting that these parasitic diseases be regarded as a public health priority by the governments of endemic countries and by the institutions of the United Nations system, and consequently calls for the development of programs for their control [9]. Since then, various STH infection control strategies have been implemented, though often discontinued, in several countries in Asia, Africa, and Latin America [10–13].

In Cuba, to determine the prevalence of infections caused by intestinal parasites and the clinical-epidemiological aspects related to them, numerous studies have been conducted in different population groups, including two national parasitological surveys [14–17]. Most of these studies have found high prevalence rates of STH infections in some areas, primarily rural regions [14,16,18]. One of these studies, conducted in San Miguel del Padrón (SMP), a semi-urban municipality located on the outskirts of Havana, reported high prevalence and intensity rates of STH infections [18].

Almost all programs for the control of STH infections implemented across Asia, Africa, and Latin America have focused on at-risk population through mass deworming, health education, and, when possible, environmental sanitation, underestimating the importance of the physician's role in these populations [13]. The physician who provides services in the communities is an opinion leader, and if equipped with the necessary cognitive tools, could be crucial in any attempt to control many entities, including STH infections. Family Doctors (FDs) are the physicians most closely linked to the diagnosis, treatment, and control of STH infections in Cuba.

The considerations contained in the preceding paragraphs highlighted the need to assess knowledge, perceptions, and practices (KPP) of FDs of SMP municipality regarding STH infection diagnosis, treatment, and control through a targeted survey. This type of tool, KPP surveys, has proven effective for similar purposes in relation to other infectious diseases in other settings [19–21]. The survey application revealed, among other aspects of interest, significant cognitive gaps, inadequate perceptions, and incorrect practices regarding the diagnosis, treatment, and control of STH infections [22]. To address the identified deficiencies and their consequences, a set of actions (which we will henceforth refer to as interventions) was carried out targeting FD’s knowledge, perceptions, and practices related to the problem. Six months after the implementation of these measures, a second application of the survey showed significant improvement among respondents in almost all of the cognitive, perceptual, and behavioral aspects evaluated.

Construction of the questionnaire

For the preparation and validation of the questionnaire on KPP regarding STH infections, which would later be applied to FDs in the municipality of SMP at two different times during the study, we proceeded in two stages:

1- Interviews with FDs: In the initial stage, open interviews were conducted with FDs (both residents and specialists). The interviews, conducted by researchers in charge of the study, covered topics related to knowledge, perceptions, and practices about STH infections. For example, the interviewee's knowledge about the biology of the different species of these parasites and their mechanisms of pathogenicity, as well as the immunology of these parasitic diseases, their different clinical forms, the most commonly used tools for their diagnosis, the available therapeutic arsenal, and the most effective control actions; the participant’s perceptions regarding the frequency of STH infections and the quality of their preparation to manage them successfully; and the physician’s practices related to the diagnosis, treatment, and control of STH infections.

2- Preparation and validation of the questionnaire: Through the analysis of the information obtained from the interviews, shared opinions, cognitive gaps, inadequate perceptions, and incorrect practices regarding the diagnosis, treatment, and control of STH infections were identified.

The questionnaire also assessed more general knowledge, perceptions, and practices, considering that the survey would serve to establish a baseline and to evaluate an intervention that would be carried out later, aimed at alleviating the deficiencies detected with the first application of the survey.

For the preparation of the instrument, it was incorporated, in addition to the aforementioned elements, the accumulated experience in the Department of Parasitology at Instituto de Medicina Tropical “Pedro Kourí” (IPK) in designing and applying such tools, and the opinions of other specialists related to both STH infections and the use of surveys as a research tool.

Once the questionnaire (26 questions) was prepared, it was submitted to expert review. Subsequently, its feasibility of use was tested through its application to a small sample of FDs that provide services outside the areas where the instrument was applied in its final form (validation trial).

After making some corrections to the texts of the statements and response options, amendments resulting from experts feedback and the validation trial, the questionnaire was ready for use. It was not deemed necessary to prepare an instruction manual for the application of the questionnaire because this activity was carried out directly by the authors.

Determination of baseline lines. First application of the survey

To explore the factors that could be affecting the quality of work of the FDs from SMP in relation to the diagnosis, treatment, and control of STH infections, the aforementioned questionnaire was applied to 104 of them. This represented 82.5% (104 out of 126) of the physicians in that specialty who were providing services in the network of polyclinics in that municipality during the period when the first phase of the research was conducted (September–October 2016). The results of this first application of the instrument would be used as baseline data for the subsequent intervention.

Components of the intervention

To contribute to mitigating the deficiencies detected with the first application of the questionnaire, and their consequences, a group of actions was executed that could improve the efficiency of the FDs´ work in SMP municipality in the diagnosis, treatment, and control of STH infections. These were: (i) delivering conferences on the topic to all the FDs of each of the polyclinics, (ii) conducting two training workshops in each of those polyclinics (led by the researchers in charge of the study, all the FDs of the municipality were summoned and a group of topics related to good knowledge, perception, and practices regarding STH infections was selected), and (iii) distributing for free to all the FDs of the municipality a book on the subject, specially prepared as part of this project [23].

Evaluation of the intervention. Second application of the survey

After 6 months of completing the implementation of the actions that were part of the intervention, a second application of the survey to FDs of SMP municipality allowed for the evaluation of the effectiveness of the measures taken. On this second occasion, the questionnaire was applied to 104 professionals. These represented 85.2% of the doctors in that specialty who provided services in the network of polyclinics of that municipality during the period in which this phase of the research was conducted.

Statistical analysis

In general, in successive stages, two types of information were processed: 1) that obtained from the open interviews conducted with a group of specialists and residents in Family Medicine during the preparation of the survey, as described in previous sections, and 2) that obtained from the application of the survey at two points in time to the universe of specialists and residents in Family Medicine in SMP municipality.

1- For the preparation of the questionnaire: For the processing of the information collected through the interviews, the qualitative content analysis procedures of Gómez, in 1999, and by Corral, in 2010, were used [24,25]. By coding the data, shared opinions, cognitive insufficiencies, inadequate perceptions, and incorrect practices related to the diagnosis, treatment, and control of STH infections were identified.

2- For the processing of the information obtained with the application of the survey at two moments: Using Microsoft Access program from the Microsoft Office 2010 package, a database was created with the information obtained from the two instances when the questionnaire was applied (baseline determination and intervention evaluation). Once the database was created, and using the statistical package Epidat 4.1, the following analyses were performed:

• Frequency analysis of the responses to each question (this analysis allowed to determine the proportion of correct answers to each of the questions measuring knowledge, the proportion of FDs who perceive differently some of the aspects investigated in the survey, and the proportion of correct and incorrect practices).

Comparison of the correct response proportions of the FDs of the municipality to the set of 19 questions that assessed cognitive aspects before and after the intervention, and comparison of the correct response proportions of those professionals to each of the questions before and after the intervention. For both types of comparisons, the Chi-squared test was used. In all cases, a p value <0.05 was considered significant.

The percentage of correct responses of FDs of SMP municipality to the 19 questions that addressed cognitive aspects about STH infections (definition, transmission, clinical aspects, diagnosis, treatment, and control) significantly improved after the intervention performed (44.7% before vs. 79.1% after) (Table 1). The improvement in cognitive aspects occurred in all the questions included in the questionnaire (information not shown).

Regarding the questions about perceptual aspects, two positive results were observed: (i) that the majority of participants believe that STH in Cuba are very common in some communities and uncommon in the rest of the national territory and (ii) that the majority of respondents now perceive that laboratory technicians performing macro and microscopic stool examinations for the detection of intestinal parasites are adequately prepared to carry out this task (Table 2).

However, the professionals' perceptions regarding the other evaluated aspects did not show significant changes after the actions taken. Thus, the majority of respondents still consider that: (i) the quality of the macroscopic and microscopic examination of feces for the detection of intestinal parasites in their health area is fair to poor, (ii) laboratory technicians lack necessary material resources to carry out this task, (iii) the knowledge and skills for the treatment of helminth infections acquired during their training are optimal or minimally necessary, and (iv) the sources of information available to maintain or increase their knowledge about these parasitic infections are sufficient (Table 2).

Regarding the inquiries about behavioral aspects, it was positive to observe that, unlike what they revealed before the intervention, the majority of respondents correctly selected the group of possible medications for treating A. lumbricoides, T. trichiura, and hookworm infections (Table 3).

Taking into account the wide geographic distribution of STH infections and their consequences in terms of health and human development, the 54^th World Health Assembly, in 2001, approved a resolution promoting that these parasitic diseases receive greater attention from the governments of endemic countries and from institutions of the United Nations system, and, consequently, the development of programs for their control by the relevant health authorities [9].

Numerous initiatives for the control of STH infections have been implemented in endemic areas across various continents [10–13,26]. Among other factors, it is believed that the insufficient integration of the strategies used, the failure to achieve an adequate intersectoriality, and the absence of a necessary multi-morbidity approach are the aspects that have most contributed to the lesser success of national and local attempts to control STH in, and as a consequence, they have not achieved adequate sustainability [13,27,28].

At a global level, the insufficient expertise of physicians providing community-level services to make an adequate manage of STH infections may have undermined some control initiatives. In general, these professionals consider that the morbidity and mortality figures for these parasitic infections are low and, consequently, do not perceive them as a major health problem. In practice, they are unaware that children infected by STH infections can develop, decades later, into physically and mentally less capable adults.

Recently, researchers from the IPK concluded a three-year study on the control of STH infections in primary schools of SMP municipality. This project included actions for mass deworming, health education, and, where feasible, environmental sanitation. The final results of this work would be used for the potential design and implementation of a national initiative for the control of STH infections in those communities of the country where these parasitic diseases constitute a health problem.

In the specific conditions of Cuba, where the figure of the FD plays a leading role in all health actions at the primary level, any initiative for the prevention and community control of STH infections must involve their active participation. Their involvement can contribute to the sustainability of such initiatives in terms of economic factors and the durability of the results. In connection with this reflection, a KPP survey was applied regarding the diagnosis, treatment, and control of STH infections to the FDs of the municipality of SMP. That questionnaire found cognitive gaps, inadequate perceptions, and incorrect practices. These results suggested that, to ensure the successful implementation of a possible national initiative for the control of STH infections in at-risk communities, actions should be taken to increase the expertise of the FDs in the diagnosis, treatment, and control of these parasitic infections.

The questionnaire applied to the FDs of SMP municipality before the intervention showed that there was a marked lack of knowledge regarding STH infections in relation to a significant part of the surveyed aspects. The success of the intervention on the professionals of SMP municipality regarding the cognitive aspects was demonstrated by the increase in the proportion of correct answers when the results of this were evaluated.

In the reviewed literature, studies like the present one regarding the knowledge of attending physicians about STH infections were not found. However, these aspects have been explored in parasitic entities produced by protozoa, such as toxoplasmosis, amoebiasis and giardiasis, in which deficiencies similar to those we describe in this document have been demonstrated [29–31]. Studies on the cognitive aspects of attending physicians concerning non-parasitic entities, such as leprosy, tuberculosis, and zoonoses have also been reported [32–34]. Those works, although on different infectious diseases and medical specialties, also demonstrated cognitive gaps, inadequate perceptions, and incorrect practices.

The analysis of the responses given to the questions that explored the perception FDs had about certain aspects of the STH infections made several facts evident to take into account:

• After the intervention, a greater percentage of participating FDs correctly perceive that STH infections in Cuba are very common in some communities and rare in the rest of the national territory and, consequently, are in better conditions to adequately characterize the communities where they work.
• Before and after the intervention, most FDs do not trust the quality of the microscopic fecal diagnosis carried out in their health units and, correspondingly, they believe that the technicians lacked necessary resources to carry it out. These perceptions, which reflect the objective conditions under which these diagnostic procedures are performed in those health units, may lead to the non-indication of this test or to an incorrect use of its results.
• After the intervention, most of the surveyed FDs believe that the knowledge and skills for the treatment of STH infections acquired during their training are optimal or minimally necessary, and that the sources of information available to keep their knowledge about STH infections updated are sufficient. This may have been aided by the distribution, as part of the intervention, of a copy per capita of a book on the subject, specially prepared as part of this project.

The analysis of the responses given to the questions that explored the practices of the surveyed FDs regarding the anthelmintic medications used for people infected with STHs showed that most of them made correct selections, which is very different from how it was before the intervention; that is to say, these professionals are now better prepared to prescribe the appropriate treatment for individuals infected by one of these parasites.

Regarding toxoplasmosis, a survey on cognitive and perceptual aspects related to its diagnosis, treatment, and control, administered to physicians from four hospitals in Nigeria, using designs and methodologies different from those employed in this study, found significant cognitive deficiencies [29]. The researchers concluded that to maintain and increase the expertise of attending physicians, continuous medical education activities were necessary. In Cuba, the application of KPP surveys on amebiasis and giardiasis to physicians of different specialties using methodologies similar to those of the present work demonstrated deficiencies similar to those addressed in this study [30,31]. In the cases of both parasite infections, subsequent academic-type interventions helped to mitigate the problem [35,36].

The shortcomings in the training of professionals related to the proper diagnosis, treatment, and control of parasitic infections do not seem to be an isolated problem. As early as the dawn of the present century, some authors critically referred to the insufficient priority given to the teaching of parasitology in Western medical schools and expressed concerns similar to those raised in this work [37–39]. Since then, data from nearly all continents show that, both in the instruction of human parasitology and veterinary parasitology, the increase of that insufficiency is a trend [41–43].

The results of this study suggest that to achieve proper expertise among doctors regarding the diagnosis, treatment, and control of STHs, it is necessary to introduce improvements in the training programs for doctors and specialists and, complementarily, create conditions that ensure the continuous education of these professionals.

The authors declare no conflict of interest.