IPIs generally constitute a significant part of Neglected Tropical Diseases (NTDs) (Hotez et al., 2009).
About two billion individuals are infected by STHs, mainly in tropical and subtropical regions, affecting vulnerable and resource-poor populations in sub-Saharan Africa, the Americas and Asia (Jourdan et al., 2018; WHO, 2020).
The global prevalence of intestinal protozoa is around 350 million infected people, considering the number of carriers of Giardia lamblia, Entamoeba histolytica and Cryptosporidium spp. (Kirk et al., 2015).
In many regions of the world, co-infection with two or more parasites is still very common in areas with poor sanitation (Abruzzi and Fried, 2011). For example, studies point to the overlapping effects of STH infections with schistosomiasis (Ezeamama et al., 2008; Campbell et al., 2016; Lo et al., 2017; Pabalan et al., 2018).
In the last 20 years, evidence has been consolidated that IPIs cause several limitations to development, particularly in children, such as malnutrition, anemia and cognitive disorders that cause educational delay, often irreversible (Stephenson et al., 2000; Ezeamama et al., 2008; Bustinduy et al., 2011; Campbell et al., 2016; Pabalan et al., 2018).
As a result of effective IPI control programs based on mass or selective chemotherapy and sanitation measures, the prevalence of these diseases has considerably decreased in the Americas and in endemic areas of Asia (Gordon et al., 2019; McManus, 2019).
In the studied sample, of the 650 patients included, 60% were female, with no predominance of age group, 96% had some degree of literacy. The study showed that 15% of the included population did not have access to drinking water and that 19.1% did not have access to treated sewage (Table 1).
In the current study, we used the strategy of combining of two parasitological methods, one semi-quantitative and the other qualitative, Kato-Katz and Hoffman, respectively, to determine the prevalence of IPIs, during a coproscopic census carried out from September 2010 to April 2011, in five neighborhoods of Barra Mansa / RJ. To improve the sensitivity of the methods, for each stool sample, three slides were prepared for microscopic analysis of each method, making a total of six slides per stool sample. The results of parasitological tests using the KK method showed low positivity for any diagnosed parasitosis (Table 2). The HH method showed a higher number of parasitic infections, with a higher frequency by Endolimax nana (17.4%), followed by Blastocystis spp (10.8%) (Table 2).
The results demonstrated that the Hoffman method showed a higher positivity for S. mansoni, when compared to Kato-Katz, including S. stercoralis, 1.5% (N = 9), for which the techniques for heavy eggs have low sensitivity (Faust et al., 1938) (Table 2).
Knowledge of the epidemiology and morbidity related to IPIs, associated with more sensitive diagnoses and more effective treatment strategies, are needed to strengthen the clinical detection and management of these conditions (Campbell et al., 2016; Ryan et al., 2017).
In this sense, the present work opted for the combination of two diagnostic methods, an option already described in other studies for areas of low endemicity of IPIs (Enk et al., 2008; Glinz et al., 2010; Caldeira et al., 2012; Meurs et al., 2017).
The current study confirmed the low prevalence of S.mansoni 0.8% (N = 5) in the city (Table 2). In the association between risk factors and the parasitological techniques used, a statistically significant difference (p = < 0.001) was observed in the variable: use of river water, confirming the need for measures to universalize basic sanitation and health education.
A systematic review and meta-analysis carried out by Gomes Casavechia et al. (2018) on the prevalence of S. mansoni infection in Brazil, identified the main risk factors associated with this endemic: gender, age, education, family income, contact with water and the presence of intermediate host snail.
The low prevalence indicated for A. lumbricoides 0.7% (N = 4) and T. trichiura 0.5% (N = 3) and absence of hookworms (Table 2), are lower than those observed by the WHO in other regions of the world, where a higher prevalence has been documented (GBD et al., 2018; Else et al., 2020). They may represent a satisfactory fact resulting from the frequent antiparasitic therapy offered to the population from this area and in several other regions of the world, during successive coproscopic censuses and annual treatments carried out since the implementation of the Schistosomiasis Control Program in the municipality (Zani et al., 2004; Enk et al., 2008; Glinz et al, 2010; Caldeira et al, 2012; Meurs et al., 2017).
On the other hand, the protist, Blastocystis sp. was observed in 10.8% (N = 66) of the stool samples (Table 2). These results are in agreement with several studies (Tan, 2008; El Safadi et al., 2014; Stensvold and Clark, 2016). Although Blastocystis sp. is highlighted as a possible causative agent of bowel disease, its pathogenic status remains controversial, with many outstanding issues (Moosavi et al., 2012; El Safadi et al., 2014; Stensvold and Clark, 2016).
Regarding giardiasis, positivity was observed in 11 samples (1.8%) by the Hoffman method (Table 2). Giardiasis is a disease of oral-faecal transmission, neglected in our environment, with a high prevalence, among other reasons because only 40% of the population in Brazil has access to properly treated sewage (Coelho et al., 2017; Gomes et al., 2020). In this study, Giardia lamblia/intestinalis was detected at a frequency of 1.5% (n = 9), only in the spontaneous sedimentation method. Sedimentation procedures are the recommended methods as being easier to perform and less prone to technical errors ().
According to Hiatt et al. (1995), the examination of a stool sample will allow the diagnosis of 60 to 80% of infections; examination of two stool samples will allow 80 to 90% detection and diagnosis will be 90% if three stool samples have been examined. Probably, the evaluation of six slides from each sample, in the current study, may have significantly increased the positivity of the diagnosis. Light microscopy of stool samples is sufficient for the diagnosis of these parasitosis in infections with a high parasite load.
The Kato-Katz method is not routinely used but has been evaluated by some researchers for detection of Giardia infection however it has limitations, particularly in its sensitivity (Carvalho et al., 2012; Engels et al., 1996).
Regarding waterborne amoebas, the results identified Entamoeba histolytica in 0.8% of the samples (n = 5), Entamoeba coli in 2.8% (N = 28) Entamoeba hartmanni in 0.2% (n = 1) and Iodamoeba butschlii in 0.2% (n = 1), but a high prevalence of Endolimax nana was observed in 17.4% (N = 106) (Table 2). The species belonging to the genera Endolimax, Iodamoeba and Entamoeba coli are considered non-pathogenic (Rey, 2008; Issa, 2014).
For E. nana, E. coli, Entamoeba hartmanni, Iodamoeba butschlii are commensalism, but they are significant because they have the same transmission mechanism as pathogenic protozoa and can serve as an indicator of poor local sanitary conditions (Rocha et al., 2000). The results for E. vermicularis 1% (n = 6) (Table 2), suggest that this prevalence may be underestimated, due to the use of non-specific methods for these parasites.
No hookworms positivity was observed, probably because the slides were not read fresh but after storage, which compromises the sensitivity of techniques for identifying these helminths (Hoffman et al., 1934; Kato and Miura, 1954; Katz et al., 1972; Willis, 1921) and the prevalence of S. stercoralis was only 1.5% (N = 9).
Deworming with albendazole and ivermectin is effective in reducing the prevalence and morbidity of soil-transmitted helminthiasis in communities with high prevalence of hookworm and strongyloidiasis (Echazú, 2017; Clark and Gilman, 2020).
Multiple parasites were identified in the studied population, a fact that can be explained by the strategy employed, where the combination of quantitative and qualitative methods resulted in the analysis of a greater quantity of feces per sample and an increase in the number of slides, resulting in better microscopic identification.
IPIs still have a significant prevalence in several regions of Brazil (Chammartin et al., 2014) and affect mainly the low-income population, without access to basic sanitation, medical care, and adequate information on prophylactic measures (Andrade et al., 2010; Bencke et al., 2006; Damazio et al., 2013).
Lodo et al. (2010) in a survey with users of a Health Unit in the city of Bom Jesus dos Perdões, São Paulo, found a prevalence of 44.7% of IPIs.
Ludwig et al. (1999) observed in a study carried out with the population of Assis, São Paulo State, that there was a correlation between the conditions of basic sanitation, expressed by the number of water and sewage connections and the frequency of parasitosis. The populations, who resided in the outskirts of the city and, with lower socioeconomic status were the most parasitized.
In this way, we highlight the need for diagnostic tools and effective control options to scale up public health interventions and improve the detection and clinical management of these infections. It must be considered that other techniques, such as serological and molecular, are more sensitive for the diagnosis of IPIs, but with reduced use by health professionals, due to their high cost and the scarcity of financial resources allocated for this purpose (Bisanzio et al., 2014; Gordon et al., 2015). The cost of serological or molecular biology tools may not be financially viable for most endemic countries.
Whereas obtain a stool sample of the subjects was not an easy process, because of cultural, aesthetic and biological issues, the preparation of six blades of each stool sample can serve as a new strategy, to be established with existing tools.
In this project, all individuals diagnosed with IPIs received test results via the Barra Mansa Municipal Health Department, being referred for outpatient treatment, if necessary.
After adequate antiparasitic treatment, studies show improvements in nutritional status and cognition, but early and long-lasting intervention would be important to prevent the irreversibility of children's cognitive and growth impairment (King, 2010; Pabalan, 2018; WHO, 2018).
IPIs are generally asymptomatic and have not shown a sensitive effect to massive deparatization with anthelmintics, except for low-income communities with the presence of children with severe conditions.
This study demonstrated the low prevalence of pathogenic IPIs in the municipality of Barra Mansa and contributed to access to adequate antiparasitic treatment.
We know that the low prevalence found may not reflect the real situation in the Brazilian population and in many other regions of the world.
Studies of enteric parasites in our country have been limited, isolated, and rare, generally reflecting the situation in small cities, requiring more comprehensive studies, and, if possible, using methods with greater sensitivity than optical microscopies, such as, for example, the use of immunological diagnostic methods such as PCR-RT (Carvalho et al., 2012; Ryan et al., 2017; Brito da Silva Alves, 2017; Faria et al., 2017; Else et al., 2020).
The reduction in the physical condition and abilities of each parasitized individual represents an obvious and avoidable loss in working days, in the capacity to learn and in the delay in physical, mental, and social development (Stephenson et al., 2000; Ezeamama et al., 2008; Bustinduy et al., 2011; Yap et al., 2012; Campbell et al., 2016; Pabalan et al., 2018).
For an effective fight against IPIs, we agree with Alum et al. (2010) who advocate that for the global and sustainable control of enteric parasites there is a need to work on several fronts, including (1) mass education on hygiene practices, (2) improvement of public and personal health conditions and (3) and where necessary large-scale deworming campaigns.
To achieve these goals, it is essential to be prioritized in all regions where the IPIs have epidemiological importance, massive investments to enable access to clean and treated sewage water, in addition to the implementation of public health systems, free, universal, and accessible with an emphasis on health promotion, education, and prevention (Gomes et al., 2020; Vlas et al., 2016).