Enterobius vermicularis in Brazil: An integrative review

ABSTRACT Enterobius vermicularis, an intestinal helminth, is transmitted through the ingestion of eggs found in food, water, dust, or other fomites, including infected individuals. This review aimed to examine the frequency and distribution of E. vermicularis infections in Brazil between 1991 and 2022. The conducted bibliographic survey revealed that the frequency of E. vermicularis infections in Brazil ranged from 0.1 to 26.1%, depending on factors such as population ethnicity, individual age group, geographic area, time frame, and diagnostic method. However, these findings were based on a limited number of publications, suggesting that the actual prevalence rates of E. vermicularis infection may still be unknown and potentially underestimated.


INTRODUCTION
Enterobiasis, also known as enterobiosis, is a globally distributed parasitic disease, not confined solely to underdeveloped countries.It is estimated that over 40 million people in the USA are infected with Enterobius vermicularis, commonly known as pinworm1 1,2 .Notably, a frequent correlation has been reported between enterobiasis and families of lower socioeconomic status 3 .
In Brazil, the proliferation of slums, coupled with the high occupancy rate per dwelling, fosters the spread of parasites, including pinworms.Similarly, settings like day care centers and schools may heighten the risk of disease transmission 3 .This review aimed to examine the distribution and frequency of E. vermicularis infection cases in Brazil from 1991 to 2022.

METHODOLOGY
An exploratory and descriptive bibliographic review was conducted between January and June 2023, focusing on the prevalence of E. vermicularis in Brazil.The research utilized the Medical Literature Analysis and Retrieval System Online (Medline) electronic database and Virtual Health Library (VHL) Regional Portal.
The search for the etiological agent, "Enterobius," was delimited using Medical Subject Headings (MeSH) terms.Additionally, the species' synonym, "pinworm," and the geographical area, "Brazil," were included in the search parameters.The Boolean operators "OR" and "AND" were utilized to combine these descriptors.Consequently, the following search strategy was formulated: 1) ((Enterobius) OR (pinworm)) AND (Brazil).

Fantinatti M and Da-Cruz AM • Enterobius vermicularis in Brazil
The inclusion criterion for manuscript selection was the full retrieval of articles.Studies were excluded if they were unavailable, utilized archaeological material, did not involve human samples, used samples known to be positive for enteroparasites, did not focus on the Enterobius worm, or were bibliographic reviews.In cases of duplicate studies across search platforms, only one was included.

Annual number of publications addressing the positivity of Enterobius vermicularis in Brazil.
A bibliographic survey of the Medline and VHL electronic libraries yielded 68 and 81 papers, respectively.Following the application of inclusion and exclusion criteria, 56 studies conducted on human samples within the Brazilian territory were selected from Medline and VHL for inclusion in this review (Table 1).
The research conducted for this review did not specify a time frame concerning the initial published study.The earliest three studies identified originated from the 1960s (two in 1965 and one in 1967); however, owing to their unavailability, they were excluded from this review.Consequently, the first study incorporated into this review dates back to 1985, involving a survey conducted using clinical stool samples from the indigenous population of Pacaas-Novos in the state of Rondônia 4 .
E. vermicularis has been detected in human feces across all regions of Brazil.However, a greater number of studies (28/56) 3, originate from the Southeast region. Despe this region boasting the highest human development indices in the country, and thus an anticipated lower frequency of enteroparasite infection, it also houses the majority of research institutes/universities and receives the most science-related investments.This fact may account for our findings.In 19 out of 27 states, including the Federal District, there were no reported instances of E. vermicularis circulation.This absence of reports could be attributed to inadequate research methods for the parasite, insufficient investment in research, or less plausibly, the absence of helminths in these states.
The methodologies employed in these studies, either individually or in combination, indicate a broad investigation into the presence of protozoa and geohelminths.Occasionally, evolutionary forms of E. vermicularis were observed.This observation underscores the apparent lack of interest in E. vermicularis research.Consequently, most of the existing data on the frequency of E. vermicularis infections are derived from studies with experimental designs that are not adequately suited for research on this particular helminth.

Prevalence of Enterobius vermicularis in Brazil
In Brazil, E. vermicularis notification is not mandatory, and no nationwide study exists to investigate this helminth.Consequently, determining the prevalence of E. vermicularis is challenging owing to the reliance on data from independent, cross-sectional research conducted by various groups with local scope and specific populations.Furthermore, the lack of standardization in diagnostic methodologies complicates this task.The highest frequency of E. vermicularis was found in samples collected in 1987 from the indigenous population of Xingu Park in Mato Grosso, with a prevalence of 26.1%.These samples were analyzed using sedimentation in water and sodium chloride solution floating techniques 32 .Despite employing similar diagnostic methods, other studies conducted in Rondônia and Mato Grosso do Sul on samples from indigenous populations reported a significantly lower frequency of E. vermicularis (2% and 3%, respectively) 4,38 .
Only a single study evaluated individuals with special needs, rendering it impossible to ascertain the frequency within this population in the country 60 .
E. vermicularis infection predominantly impacts children 5,6,7,12,24,56 .Excluding the study conducted in Sumidouro/RJ and Ituiutaba/ SP 25,29 , the infection frequency among children-only studies ranged from 0.5% in Rio de Janeiro/RJ to 72.1% in Natal/RN.The infection rates among children in Brazil fluctuate based on the region under study and the characteristics of the child population, such as family income, residential area (rural or urban), and primarily, their exposure to crowded environments.The presence of Enterobius in consumable vegetables has also been documented 20,61 , suggesting these foods may serve as a transmission route for helminths in Brazil.Among food handlers, the infection frequency varied from 0.3 to 13% depending on the region 8,37,62 , underscoring the potential role of this population in Enterobius transmission, as highlighted in the study by Fernandes et al. (2014)  37 .
The presence of infective E. vermicularis eggs in public environments, such as bathrooms and buses, is concerning because of the possibility of contamination 10,[57][58][59] .This potential for contamination elucidates the sporadic instances of E. vermicularis infection.
Anal pruritus was a common complaint (50%) among children attending a daycare center in a Rio de Janeiro/RJ community.This prompted an investigation into the prevalence of E. vermicularis infection within this demographic.In 2015, 5.9% (4/68) of the children, aged 1-4 years, were found to be infected with E. vermicularis, as determined by the Graham method.
Over the past 6 months, drugs were administered to more than 22% of these children to treat worms infection.The reported usage of antiparasitic drugs, in conjunction with the frequency of enteroparasite occurrence and its primary clinical manifestation, prompted us to question the estimated prevalence rates of helminths in Brazil.
The papers reviewed generally indicated that data on E. vermicularis infection frequency are derived from studies primarily designed to survey intestinal parasites.Therefore, the diagnostic methodologies employed exhibited lower sensitivity in detecting parasite eggs.An exception was the study by Campos et al. (2011), which aimed to ascertain pinworm prevalence and its association with enuresis cases in children from an orphanage 53 .The high infection frequency observed in this study (72.1%) resulted from three factors: 1) the age range of the population; 2) overcrowding; and 3) the diagnostic methodology, inclusive of sample collection preparation.

FINAL CONSIDERATIONS
The prevalence of E. vermicularis infections in Brazil between 1991 and 2022 ranged from 0.1-72.1%.This variation was influenced by factors such as population ethnicity, age group, geographic location, time period, and diagnostic methods.However, these statistics were derived from a limited number of publications, suggesting a potential underestimation of the actual prevalence rates of E. vermicularis infection.
E. vermicularis eggs, already infective upon release, can be transmitted directly through person-to-person contact.This makes crowded environments such as day care centers, schools, and nursing homes conducive to the spread of this helminth.Furthermore, in Brazil, favelas are home to over 17 million people, constituting 8% of the population 63 .In these settings, population agglomeration in intra-and peridomiciles is common, thereby promoting (re)infection.In such highfrequency environments, recurrent infections are anticipated.Consequently, the chronicity of E. vermicularis infection may be more prevalent than anticipated, and the issue of parasite resistance to available drugs is a subject of ongoing debate.
In Brazil, many states and municipalities lack reports of E. vermicularis infection, while others present only few reports, indicating that the geographical distribution of this infection requires further investigation.The majority of these studies are typically cross-sectional, stemming from individual research groups, and primarily focus on local parasitological surveys.However, the methodologies employed are often incomparable and may not be the most sensitive for parasite identification.The application of unsuitable techniques can result in false-negative outcomes, potentially extending the parasite-host interaction, which may cause perianal itching and gastrointestinal symptoms.Additionally, the infection has been linked to conditions such as vulvovaginitis and appendicitis.This review consolidates studies published from 1985 to 2022, showcasing the prevalence of enterobiasis across various Brazilian states and the diagnostic strategies employed.In 13% (7/54) of these studies, an E. vermicularis frequency equal to or exceeding 10% was noted.However, the absence of a national infection survey and a dearth of research targeting parasite identification precludes definitive conclusions about whether the distribution of E. vermicularis is on the rise or decline.The limited understanding of E. vermicularis transmission dynamics hampers the development of strategic control measures targeting potential transmission sources.

TABLE 1 :
Positivity of Enterobius vermicularis in Brazil up to 2022, according year in wich the samples were obtained, city and state, population studied, age, number of individuals or samples, diagnostic technique, prevalence and reference.