1. Introduction

The nematode Enterobius vermicularis is a parasitic helminth of great medical importance in the world due to its wide distribution, which is greater than other known parasitic helminths [1]. Its life cycle is practically restricted to humans where it invades the intestine causing the disease known as enterobiasis. Once in the intestine, gravid females migrate to the rectum during the night to deposit and attach eggs in the perianal region. This process causes an irritation that produces an itching in the region and causes the patient to scratch and contaminate his or her fingers, which facilitates their dispersal to the environment, to another individual or to the same individual (anus–hand–mouth) [2]. When the eggs are ingested, they hatch in the duodenum, and the larvae mature during migration to the large intestine to settle and continue the cycle [3]. The infection is commonly not dangerous; however, it is a cause of significant morbidity worldwide with an estimated 1 billion cases [4].

Although enterobiasis can affect any age group, it is more common in children due to inadequate sanitation and active contact with each other. Moreover, egg transmission is facilitated in children attending school due to crowded conditions and shared toilets [5]. Most cases in children are asymptomatic, but irritability and loss of appetite, nausea, insomnia, enuresis, teeth grinding, diarrhea, anal pruritus, catarrhal inflammation, and recurrent endometritis may occur [4]. Proper diagnosis of enterobiasis is relatively simple and is based on microscopic observation of typical E. vermicularis eggs in the perianal region [2]. Generally, samples are obtained by applying adhesive tape to the region immediately after waking up (Graham’s test) [6], and sometimes, it is possible to observe adult worms as well. In almost all cases, deworming treatment is successful if it is managed together with attention to hygienic measures and involvement of the whole family [7].

In the case of infection in women, some worms may become disoriented and enter the vagina, where they produce an ectopic infection with potential complications at any level of the genitourinary tract [8]. Commonly, documented cases show vaginitis, vulvar irritation, and endometritis that are not life-threatening for the patient, but the presence of other microbial agents can lead to major complications [9]. In this sense, epidemiological surveillance of enterobiasis is a valuable tool to generate information to assist in public health decision-making, especially aimed at vulnerable populations such as children.

The aim of this study was to analyze the prevalence of E. vermicularis in children from a marginalized area of the state of Oaxaca, located in southeastern Mexico, where socioeconomic and environmental conditions favor the occurrence of intestinal infectious diseases. In addition, vaginal ectopic infection was determined in girls presenting vulvovaginitis, and the presence of bacterial coinfections was documented.

2. Method

2.1. Study Area

A cross-sectional, observational study was conducted from September 2022 to February 2023 in the rural municipality of Santiago Tlazoyaltepec in the state of Oaxaca, located in southern Mexico (Figure 1). Its population is composed of 6,300 inhabitants, of which 76% speak at least one indigenous language and the highest levels of schooling are elementary (43.7%) and junior high (37.3%), with an illiteracy rate of 21%. Extreme poverty in the municipality is 58.8%, and the population in moderate poverty is 39.8% (https://www.economia.gob.mx/datamexico/es/profile/geo/santiago-tlazoyaltepec#health). The climate is temperate subhumid with summer rains, a temperature range of 14−20°C, and an altitude that ranges between 2,000 and 2,900 m above sea level [10].

3. Results

The overall prevalence of enterobiasis among children was 21% (108 girls and 85 boys), and no significant differences were observed between preschool and school children (p = X2 = 3.84, p = 3.28). However, according to sex, girls showed a significantly higher prevalence (24.16%) than boys (18.59%) (p = 0.032) (Table 2). In all positive cases, only E. vermicularis eggs were observed by Graham’s technique. On average, 190 (SD ± 60) eggs were observed per field.

Of the 108 girls positive for E. vermicularis eggs in the perianal region, 11 of them (10.19%) also showed infection in the vagina with the parasite: in six girls, only eggs were found, while in five girls, we found adults as well (Figure 2). The number of inhabitants per house and the overcrowding index in the rooms was not a determining factor for perianal and vagina infection (p = 0.321 and p = 0.213, respectively).

Visual and physical examination of the vulva of the girls positive for E. vermicularis in the vagina showed obvious lesions such as abrasions, redness, pain, and tenderness, among others (Table 3) (Figure 3). Likewise, the presence of bacterial agents was determined in the microbiological analysis, where Escherichia coli was the most common bacterium (Table 3).

4. Discussion

The overall results of our study reveal a prevalence of enterobiasis of 21.3% in preschool and school-aged children in a marginalized community in southeastern Mexico. This prevalence is similar to other rural areas of Mexico [11] and even other countries such as Venezuela and Colombia [12, 13]. Enterobiasis, like many other parasitosis, is strongly linked to poverty and even more to lack of hygiene [14]. Because of its association with hygiene, it is more common in younger children who exhibit behaviors that facilitate the transmission of E. vermicularis eggs, such as not washing their hands after playing or before eating [15]. However, we did not find significant differences between the prevalence of infection in the two age groups (school age) as suggested by some studies [16, 17].

In contrast, we observed a significantly higher prevalence in girls than in boys. Although there is no known direct association between gender and enterobiasis infection, the available literature shows higher rates in boys than in girls [3, 18], but this is not always the case [4, 19]. In this regard, Laoraksawong et al. [17] attribute this to boys engaging in more activities, being in closer contact with other children, and having worse personal hygiene than girls. Regardless of gender, when children are infected, they can easily transmit eggs to other children in schools and increase the prevalence of enterobiasis in a population. Therefore, intervention and surveillance programs in schools can help decrease enterobiasis in the child population in communities [4]. For example, in a kindergarten in Mexico where a health program against parasites was conducted, a low prevalence of enterobiasis was found [20]. However, for these actions to have a greater impact, they need to be complemented by interventions also in their homes [7].

Although we have mentioned above that the clinical picture of enterobiasis alone is not serious, untreated and prolonged infection can trigger other problems that compromise the proper development of children. In addition to problems related to height–weight, a deficit in the mental development of children with prolonged and severe infection has been observed [21]. An association with anxiety disorders, depressive disorders, and sleep disorders has also been reported [22]. Like any other parasite, E. vermicularis takes nutrients from its host to survive and perform its essential functions. In infected children in a pediatric hospital in Iran, total serum levels of protein and significant iron were found to be lower than uninfected children [1]. This highlights the importance of generating surveillance and care strategies in areas of extreme poverty such as ours, where poor nutrition can lead to complications in children infected with these parasites.

Specifically in girls, the infection can be further complicated when the worms migrate to the vagina and deposit their eggs in the vulvar region. Also, they can enter through the cervix and reach the fallopian tubes producing fertility problems [23]. Here, we found 11 girls with the presence of eggs in the vulvar region, and in five of them, adult worms were also found. None of them had serious gynecological complications, but physical examination of the girls revealed vulvovaginitis with recurrent clinical manifestations such as excoriation, itching, pruritus, and redness [24, 25]. According to the parents, none of the girls expressed any signs related to the infection. In fact, most cases of this type of ectopic infection are asymptomatic, and the lack of clinical suspicion makes diagnosis difficult [25]. Therefore, it has been suggested that the vagina may represent a potential reservoir of E. vermicularis [24]. In addition to the vagina, worms can invade the appendix [26], nasal passages, and eye orbit [27], bile ducts [28], kidney [29], and the intraluminal and intramural zone in the ileocecal segment where one death has already been reported [30]. Although enterobiasis is a common infection worldwide and has been widely studied, the mechanisms underlying ectopic infections still remain poorly understood.

On the other hand, girls with E. vermicularis infection in the vagina have a higher incidence of urinary tract infections, probably due to pathogen transfer during worm migration to this area [31]. The most frequent bacterium we found was E. coli, which has already been reported in coinfection with E. vermicularis [32]. E. coli is one of the most common bacteria in the genital tract of women; however, it sometimes leads to urinary tract infections [33]. Likewise, we found Enterococcus spp. and Staphylococcus aureus, which have been found in vaginal infections [34], but there are no previous reports of their presence together with E. vermicularis. On one hand, S. aureus is known to be an opportunistic pathogen, and increased reports of colonization in the female vaginal tract have been suggested [34]; meanwhile, some members of Enterococcus, such as E. fecalis, can invade the vagina and are an important cause of severe inflammation [35]. The presence of these bacteria in some girls in our study can be explained by the mechanical dragging of the worms when they migrate from the rectum to the vagina. Finally, no mycological agent was found in any of the girls with vulvovaginitis, where C. vaginalis is one of the most frequent [36].

5. Conclusions

Our findings show a high prevalence of enterobiasis in a child population in southeastern Mexico, with a higher occurrence in girls than in boys. The observation of eggs and adult specimens of E. vermicularis in the vagina of some girls highlights the importance of encouraging the active search for ectopic infections in order to avoid future complications. Likewise, we believe that the analysis of potential coinfections in the female genital tract can help to establish a more complete overview of the health of patients and establish appropriate treatment. For all these reasons, it is important to generate surveillance and care programs in marginalized communities that motivate the control of these parasitosis.

Conflicts of Interest

The authors declare that they have no conflicts of interest.