Enterobius vermicularis is the most common human helminth infecting the intestine. Due to its low pathogenicity, infection is usually asymptomatic. Extraintestinal infections of E. vermicularis are extremely rare. The commonest extraintestinal site of infection is the female genital tract [1]. The male worm dies in the bowel during copulation, and the gravid female worm can migrate from the perianal region to the vagina and can ascend and reach peritoneum through the uterine cavity and fallopian tube. Various reports are available in the literature of the worm in the vagina, myometrium, endometrium, fallopian tube, ovary and pelvic peritoneum as well as an interesting incident of invasion of a human embryo [2–4].
Enterobius vermicularis infection is rarely reported to be associated with infertility. We report the detection of uterine endometrial E. vermicularis infestation in a woman who presented with primary infertility and subsequently conceived after treatment for the infection.
A 38-year-old woman presented to our fertility clinic for evaluation of primary infertility. She was married for 15 years and had regular menstrual cycles. She had twice attempted intrauterine insemination unsuccessfully elsewhere. A hormonal assay showed normal results (FSH: 3.2 mIU/mL, LH: 5.5 mIU/mL, TSH: 1.6 mIU/mL, PRL: 7.03 ng/Ml and AMH: 1.2 ng/mL). An ultrasound evaluation revealed normal-appearing uterus and ovaries and a small right adnexal cyst. A sonohysterogram showed a normal uterine cavity, and a hysterosalpingogram confirmed the patency of both fallopian tubes. A semen analysis of her husband was also within normal limits.
An informed consent was obtained from the patient. She subsequently underwent hysterolaparoscopy. Laparoscopy revealed normal-appearing uterus and ovaries and a small fimbrial cyst which was excised. Histopathology evaluation suggested a paratubal cyst. On hysteroscopy, the uterine cavity appeared adequate. The endometrium, however, was looking irregular and polypoidal. Endometrial sampling was done and sent for histopathological evaluation which demonstrated the larvae of Enterobius vermicularis embedded within the endometrium (Figs. 1, 2). She was treated with a single dose of 400 mg of albendazole which was repeated after 2 weeks. In view of prolonged infertility and advanced age of the female, in vitro fertilization (IVF) was offered which resulted in a successful conception. She is into the sixth month of pregnancy at the moment.
Enterobiasis caused by E. vermicularis is one of the most common helminthic infestations of the cecum and adjacent gut. Ingestion of eggs present in the contaminated hands or food results in infection by this pinworm [2]. Scratching the perianal skin where the female worm has laid eggs results in hand contamination. The gravid female worm can migrate from the perianal area to the vagina and ascend through the fallopian tube to the peritoneum [3]. The worm can also pass through the intestinal wall and cause pelvic peritoneal granuloma. Such navigation by the larval and adult parasite can result in fallopian tube infiltration, tubo-ovarian abscess, salpingooophoritis or granulomata of the vulva, vagina, uterus, fallopian tubes or ovaries and rarely destruction of the human embryo [4].
Enterobius vermicularis granulomas do not usually cause clinical problems and are incidental findings. They have been reported to cause vulvovaginitis and can masquerade as cervical and endometrial carcinoma. Involvement of the pelvic peritoneum and the fallopian tube resulting in infertility has been reported [5, 6]. Ours is the first instance of uterine endometrial infection with the worm resulting in infertility. Since the patient has never undergone IVF before, the causality of this association cannot be established. The presence of unexplained infertility and its reversal after treatment of worm infestation may suggest causality. The diffuse endometrial inflammation caused by the worm could interfere with implantation and thus cause infertility. The subtle uterine irregularity was visible only on hysteroscopy.
Our case highlights the importance of ectopic enterobiasis in female reproductive ill health, especially in the tropical countries. In addition to the previously reported instances of ectopic enterobiasis-related pelvic inflammatory disease and tubal infection resulting in infertility, uterine endometrial involvement by the worm also seems to be another potential cause for infertility. Co-infection with other bacteria from the intestine and skin is another major concern as they seem to move to these sites along with the pinworm and contribute toward infection and inflammation [7]. We stress on the importance of close observation of the uterine cavity through hysteroscopy in all cases of prolonged unexplained infertility. An endometrial sampling can identify the pinworm infection and allow treatment which might restore fertility.
Conflict of interest None.
Informed consent Informed consent was obtained from the patient for inclusion in this publication.
Ethical Statement This work has not been published before; it is not under consideration for publication anywhere else; its publication has been approved by all co-authors, as well as by the responsible authorities.