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Case Study
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Enterobius Vermicularis: Does it Invade Central Nervous System?

Venkataramana Kandi , Ritu Vaish, Padmavali Palange, Sri Sandhya Koka, Padmajakshi Gurrapu, Mohan Rao Bhoomigari
American Journal of Infectious Diseases and Microbiology. 2019, 7(1), 8-12. DOI: 10.12691/ajidm-7-1-2
Received February 17, 2019; Revised April 04, 2019; Accepted April 24, 2019

Abstract

Enterobiasis is a common intestinal parasitic infection of humans caused by Enterobius vermicularis (E. vermicularis). Although it affects all age groups, in most instances, it causes a self-limiting illness. Infections in children may result in severe morbidity. Enterobiasis can remain as a chronic infection in cases of bad personal hygiene, and those who are not adequately treated. Dissemination of E. vermicularis larvae from the perineal and peri-anal regions into the vagina and other associated regions has been adequately documented. There are several reports of ectopic presentations of enterobiasis. This report presents a fatal case of a four-year-old child with E. vermicularis infection who presented with central nervous system (CNS) complications.

1. Introduction

Enterobius vermicularis (E. vermicularis) is a nematode residing in the large intestine of humans. It is commonly called as pinworm, threadworm, and seatworm. Enterobiasis is a common parasitic infection spread throughout the world and usually causes infection in school going children, presenting as peri-anal itching (pruritus ani), attributed to the mucoid secretions of the eggs on the skin. The adult worms although don’t contribute to the pathogenicity, are required for the continuation of the life cycle. Enterobiasis, although is not a life-threatening infection, it could lead to severe morbidity among the infected persons. Children suffering from enterobiasis suffer from sleeplessness, nausea, vomiting, abdominal pain, diarrhea and anemia. Some infected patients might also show symptoms that include nocturnal enuresis, perianal excoriations, biting of nails, nervousness, hyperactivity, and loss of weight. Infection could be symptomless or may present with mild symptoms among adults. In females, the larvae hatched out on the peri-anal skin might crawl back and enter the vagina, and wander through the fallopian tubes, uterus and might enter the peritoneum 1, 2, 3, 4, 5.

E. vermicularis does not have the buccal apparatus that helps in penetration, but it still manages to spread hematogenously, through intestinal mucosal abrasions, and may reach various organs of the body including the liver, lungs, and other organs like ovary, kidney, spleen, and are known to cause threadworm granulomas 6, 7, 8. Most infections of Enterobius have been diagnosed at sites other than the intestines, which proves its invasiveness especially in susceptible hosts 9, 10, 11, 12.

This report presents a case of a four-year-old girl child suffering from enterobiasis who died of central nervous system (CNS) complications.

2. Case Observation and Presentation

A 4-year-old school going girl child was brought to the department of pediatrics at the Prathima Institute of Medical Sciences, Karimnagar, Telangana, India. She presented with complaints of fever, and vomiting’s for 1 month, headache in the last 15 days, and abnormal movements of upper and lower limbs. The fever episodes were noted to be intense, sudden onset, and intermittent in nature. On admission, the patient was very irritated, biting the nails, and not cooperating for the treatment. There was no previous history of serious illness or hospitalization, and the child was completely normal before the start of symptoms, except that there was a history of finding tiny, live worms in the stool, and repeated episodes of abdominal pain, and diarrhea a year ago, which was treated by a local private medical practitioner. The child was second among siblings and had reached all milestones normally. The socioeconomic condition of the child appeared to be low, with both the parents being daily wage laborers, living in a poorly ventilated home.

On clinical examination, the cardiovascular system, and the respiratory systems were found to be normal. Central nervous system examination revealed positive for neck stiffness, cerebellar ataxia, and Kernig’s sign. Glasgow coma scale of 13/15 (15-best response; <8-comatose; <3-totally unresponsive) was noted, and grade I protein-energy malnutrition was observed.

Computed tomography (CT) scan of the brain revealed prominent ventricles, with slightly effaced basal cistern, and suggestive of obstructive hydrocephalus. A provisional diagnosis of subacute meningitis was made with advice to undergo magnetic resonance imaging (MRI) of the brain for further evaluation and confirmation.

MRI studies revealed T2 hyperintense regions in right thalamus with diffusion restriction and corresponding apparent diffusion coefficient (ADC) showing suppression, suggestive of acute infarction in the right thalamus. MRI also demonstrated lacunar infarct in the left lentiform nucleus, with mild dilatation of the temporal horns and lateral ventricles. An electroencephalogram was performed, which was suggestive of possible encephalitis.

The C-reactive protein (CRP) was raised (1.2 µg), with 12.5 g% haemoglobin, increased erythrocyte sedimentation rate (ESR) (30 mm), leucocytosis (19,000 cells/mm3), neutrophilia (74%), lymphopenia (20%), and hyponatremia (128 mmol/L). The parasite F test for HRP-2 antigen of Plasmodium was negative. Cerebrospinal fluid (CSF) was collected and sent to the clinical laboratory. It was clear, and colourless in appearance, with a total cell count of 6 cells/mm3 (Normal value: 0-20 cells/mm3), 90% neutrophils, 10% lymphocytes, with protein (54 mg/dl, Normal value: 20-40 mg/dL) and glucose (27 g% Normal value: 45-80 mg/dL). Gram’s stain of the CSF showed no bacteria, and it was negative for acid-fast bacilli. Wet mount of the CSF showed no fungal elements, and other parasites like the Acanthamoeba, and Naegleria.

Stool for pathology and parasites was received in the clinical laboratory. It was negative for reducing substances, and occult blood. Stool wet mount showed the presence of characteristic plano-convex, non-bile stained eggs, which were morphologically resembling E. vermicularis as shown in Figure 1. The Images of the parasite egg were sent to the Center for Disease Control and Prevention (CDC), Atlanta, USA, and was positively confirmed (dpdx@cdc.gov).

A diagnosis of possible meningoencephalitis, with cerebral infarctions, was made. The patient was managed for fever. Care was taken for the maintenance of blood pressure and was given vitamin supplements (vitamin E, vitamin B12), valproate and gabapentin. Although the patient was recommended to be under observation, they were discharged against medical advice. The patient got admitted on 30th October 2017, discharged on 8th November 2017. The condition of the patient deteriorated and was brought on 22nd November 2017, only to be declared as brought dead.

3. Discussion

E. vermicularis is previously called Oxyuris, and the disease caused by it was called as oxyuriasis 13. Human infection with E. vermicularis could be as old as 10,000 BC, as evidenced from a report, which found eggs of pinworm in the coprolites (fossilized feces) excavated from Hopug and Danger caves of western Utah 14. Report of Enterobius egg attached to an adolescent female sacral bone, dating back to 7000 AD was excavated in Iran 15. Evidence of pinworm eggs in the human coprolites, excavated in Chile, which is dated between 400-800 AD was also reported 16.

Human enterobiasis is ubiquitous, prevalent both in the tropical and temperate climate. This could be because its life cycle does not involve any developmental stage in the environment, or the soil as required by most other nematode parasites. Transmission of infection requires close association with infected patients as it does not have a soil development phase, as seen in other nematode parasites. The Human infection with E. vermicularis results from the ingestion of embryonated eggs, which hatches out larvae in the small intestine. These larvae then move into the large intestine (caecum and appendix), develops into adult male and female worms, mature, and undergo fertilization. The female gravid worm has the tendency to migrate towards the rectum, perianal region, and perineal areas to deposit the eggs. These eggs then may cause auto-infection (through nails), and retro-infection (movement of hatched out larvae back into the intestine) or be a source of infection to people living with the infected person 5. Most human infections resolve automatically without treatment. In some cases, treatment may be necessary to reduce the morbidity and re-infections.

There are fewer reports of prevalence of enterobiasis from India. In a recent study Bharti B et al. have reported that soil-transmitted helminths including the ascariasis, strongyloidiasis, trichuriasis, hookworm infection and enterobiasis account for a combined prevalence rate of 20% 17. A 2% prevalence rate of enterobiasis and a 35% combined prevalence of soil-transmitted helminthic infections (ascariasis, trichuriasis, taeniasis, infections with hookworm, and Hymenolepis nana) among school going children was reported by Ragunathan L et al. from South India 18. A report from the United States of America (USA), by Burkhart CN et al. has noted that enterobiasis is the most common helminthic infection in the USA, and Western Europe, with prevalence rates of 30-50%. The same study had also highlighted the complications of the genito-urinary tract invasion of the parasite 19. In a recent report from Iran by Moosazadeh M et al. had reported a prevalence rate of around 17% among various age groups of children 20. A study by Li H-M et al. from China (Gaozhou, Guangdong Province) reported a 50% prevalence of enterobiasis among children 21.

It was noted that in cases where the parasite develops ectopic lesions in non-habitual sites, the histopathological diagnosis becomes necessary and complicated 22, 23, 24.

Unusual presentations of human enterobiasis have been reported in the literature recently, where a 55-year-old male originating from Pakistan, had suffered from an inflammatory caecal polyp. This was initially misdiagnosed as a malignancy and was later confirmed as a case of enterobiasis. This patient gave a history of the presence of parasite worms in stool during his teenage 25. This report signifies the chronicity of the infection and the potential invasiveness of E. vermicularis.

4. Enterobiasis and CNS Involvement

A thorough search of the available literature had only identified two studies which had directly associated E. vermicularis infection with CNS invasion 26, 27. Interestingly, both reports originated from Iran. The first report had described a fatal case of a 60-year-old man who presented with meningitis. The CSF collected from the patient showed the adult worm, the larvae, and the eggs 26. The authors were not sure how the parasite had gained access to the brain. The second report describes a case of an eight-year-old boy, who presented with symptoms of severe neck pain radiating to the right shoulder. The magnetic resonance imaging of the spinal cord revealed intra-dural extra-medullary mass arising from the dura on the right anterolateral side of the spinal cord. The pathological observation of the mass-like lesion showed the presence of structures resembling E. vermicularis adult worm and the eggs. This report hypothesized the hematogenous spread of the parasite from the capillaries into the spinal cord 27.

5. Association of Other Parasitic/Nematode Infections with CNS Complications

The invasion of the parasite into the brain and the development of CNS complications was only reported in rare circumstances.

Previous research studies have noted that during various parasitic infections, which might cross the blood-brain barrier may contribute to significant pathology, which in most instances could lead to severe consequences, and even death 28, 29. As noted by the previous research, there are possibilities that the infection could prolong for a long time, and in cases of immunosuppression, and increased parasitic burden may lead to severe morbidity and mortality 30, 31.

Clinical symptoms, during CNS involvement of nematode parasites as reported previously, may be slowly progressive, and include severe headache, infection of the eyes, encephalopathy (eosinophilic meningoencephalitis), meningitis, altered mental status (restlessness), meningismus (symptoms without pathological changes in the meninges), aneurysms, vasculitis, and intracranial haemorrhages 31, 32, 33, 34, 35, 36.

It was also noted that in most cases a biopsy or CSF examination may not show the presence of the parasite, and the diagnosis is made based on the clinical, and radiological findings, along with a history of exposure 31.

Radiological features during nematode infections include hyperintense regions near the basal ganglia may be seen, along with small hemorrhages, and granulomatous changes. White matter abnormality, obstructive hydrocephalus, subarachnoid hemorrhages, and T2 hyperintense regions, and small infarctions on magnetic resonance imaging (MRI) are also reported 37, 38, 39, 40, 41, 42.

Previous research has reported the occurrence of secondary bacterial meningoencephalitis caused by Staphylococcus aureus in a squirrel monkey, which had an intestinal infestation of nematode larvae. In this case, the CSF showed no larvae, but laboratory results of stool examination, complete blood picture, biochemical profile, and urine analysis revealed systemic disease 43.

6. Other Variable Findings during Parasitic Infections

It was observed that the serum eosinophilia, which is prominent during acute infections, might be absent in chronic cases during nematode infections 44. Another significant observation is the presence of hyponatremia among the patients suffering from disseminated nematode infection (strongyloidiasis) 45.

The patient in discussion appears to have impaired immune system due to grade 1 protein-energy malnutrition and had chronic intestinal enterobiasis. This is confirmed by the history, as well as the presence of several eggs in the un-concentrated stool specimen, which indicates high parasite burden. Laboratory results revealed increased CRP, ESR, and hyponatremia. The patient was born normal, had no other underlying illness, nor was debilitated, and was going to school regularly before being admitted with CNS symptoms. The patient developed severe headache, neck stiffness, meningeal irritation, and was positive for Kernig’s sign on presentation. MRI of the brain showed the presence of T2 hyperintense regions, signs of obstructive hydrocephalus, and small infarctions in the right thalamus. With the available literature, the patient in discussion had CNS symptoms which have already been reported during other nematode infections. And It is not sure if the E. vermicularis infestation and associated pathology had caused the CNS complications and death of the patient.

7. Differential Diagnosis

There are several microbes/microbial infections, which could be associated with the central nervous system complications. These include bacterial infections (Leptospirosis, listeriosis, Meningococci, Rickettsiae, tuberculosis, and others), viruses (Enteroviruses, Arboviruses including Japanese B encephalitis virus, Measles, Epstein-Barr virus, Varicella-zoster virus, Mumps, Herpes simplex virus, Rabies, and Human immunodeficiency virus), fungi (Cryptococcosis), and parasitic infections (Cerebral amoebiasis, Naegleria, Acanthamoeba, Malaria, Trypanosomiasis, Strongyloidiasis, Schistosomiasis, Echinococcosis, Trichinosis, Onchocerciasis) 46, 47, 48, 49, 50.

8. Conclusion

Only two previous research reports had associated E. vermicularis infection with CNS complications in humans. In the present case, the infection could have persisted for a long period attributed to the impaired immunological response due to the presence of grade 1 protein-energy malnutrition, continuous re-infections (child hygiene, low socioeconomic status), and due to non-specific, or inadequate treatment. In our patient, who presented with CNS complications, the occurrence of intestinal parasitic infestation could have been an accidental finding. It can be hypothesized that the parasite larvae might have gained access into the brain, and was responsible for the CNS complications, which was, unfortunately not confirmed. Although the patient was negative for malaria, other causes of CNS complication was not completely ruled out. In view of limited data on the prevalence of human enterobiasis and, because there have been reports of ectopic enterobiasis, it is important to understand the pathophysiology of E. vermicularis infection, and its potential to invade various organs of the body including the central nervous system.

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Cite this article:

Normal Style
Venkataramana Kandi, Ritu Vaish, Padmavali Palange, Sri Sandhya Koka, Padmajakshi Gurrapu, Mohan Rao Bhoomigari. Enterobius Vermicularis: Does it Invade Central Nervous System?. American Journal of Infectious Diseases and Microbiology. Vol. 7, No. 1, 2019, pp 8-12. http://pubs.sciepub.com/ajidm/7/1/2
MLA Style
Kandi, Venkataramana, et al. "Enterobius Vermicularis: Does it Invade Central Nervous System?." American Journal of Infectious Diseases and Microbiology 7.1 (2019): 8-12.
APA Style
Kandi, V. , Vaish, R. , Palange, P. , Koka, S. S. , Gurrapu, P. , & Bhoomigari, M. R. (2019). Enterobius Vermicularis: Does it Invade Central Nervous System?. American Journal of Infectious Diseases and Microbiology, 7(1), 8-12.
Chicago Style
Kandi, Venkataramana, Ritu Vaish, Padmavali Palange, Sri Sandhya Koka, Padmajakshi Gurrapu, and Mohan Rao Bhoomigari. "Enterobius Vermicularis: Does it Invade Central Nervous System?." American Journal of Infectious Diseases and Microbiology 7, no. 1 (2019): 8-12.
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