|DR SC PARIJA ORATION
|Year : 2021 | Volume
| Issue : 2 | Page : 71-77
My experience on taeniasis and neurocysticercosis
Kashi Nath Prasad
Department of Microbiology, Apollomedics Super Speciality Hospital, Lucknow, Uttar Pradesh, India
|Date of Submission||25-Jan-2021|
|Date of Acceptance||25-Mar-2021|
|Date of Web Publication||20-Oct-2021|
Kashi Nath Prasad
Department of Microbiology, Apollomedics Super Speciality Hospital, LDA Colony, Kanpur Road, Lucknow - 226 012, Uttar Pradesh
| Abstract|| |
Taeniasis and neurocysticercosis (NCC) are major public health problems in developing countries. NCC is the leading cause of community-acquired active epilepsy. NCC may present as a medical emergency, especially when there is cysticercotic encephalitis or raised intracranial hypertension. Systematic community-based studies on taeniasis and NCC are lacking. We studied taeniasis and NCC-related active epilepsy disease burden in the pig farming community of Lucknow district, Uttar Pradesh, India. Based on the 30 cluster sampling approach as recommended by the World Health Organization, we estimated the prevalence of taeniasis, NCC-related active epilepsy, and silent NCC in the community. We also estimated the prevalence of swine cysticercosis. Taeniasis was detected in 18.6% of populations. Expulsions of tapeworm segments in stool, consumption of undercooked pork, age above 15 years, and handwash with clay or plain water after defecation were associated with taeniasis. On molecular analyses of positive stool samples, T. solium was identified in 40% and Taenia asiatica in 60% of cases. Active epilepsy was identified in 5.8% of subjects; 48% of them had NCC. On neuroimaging, NCC was detected in 15% of asymptomatic individuals. We observed that host genetic factors such as toll-like receptor-4, matrix metalloproteinase-9, intercellular adhesion molecule-1, and glutathione-S transferase gene polymorphisms were associated with seizure in NCC. When peripheral blood mononuclear cells (PBMCs) from NCC subjects were exposed to cysticerci fluid antigens in-vitro, PBMCs from symptomatic and asymptomatic subjects showed significantly higher Th 1 and Th 2 cytokines response respectively, symptomatic patients had significant Th-1 cytokines response, while asymptomatic individuals showed Th-2 response. Porcine cysticercosis was detected in 26% of swine; 38% of them had cysticerci in the brain. Swine with brain involvement showed clinical signs such as excessive salivation, excessive blinking and tearing, and subconjunctival nodule. On molecular analysis, 15% of cysticerci in swine were identified as T. asiatica. Infected swine when treated with albendazole plus/minus steroid, the response rate of cysticerci (either dead or resolved lesion) was 100% in albendazole-treated group and 71% in albendazole plus steroid-treated group. The above studies suggest that taeniasis and NCC are alarmingly high in the pig farming community of North India. Taeniasis in human and cysticercosis in swine due to T. asiatica call for further studies on this parasite.
Keywords: Active epilepsy, cysticercosis, neurocysticercosis, seizure, swine cysticercosis, Taenia asciatica, Taenia solium, taeniasis
|How to cite this article:|
Prasad KN. My experience on taeniasis and neurocysticercosis. Trop Parasitol 2021;11:71-7
| Introduction|| |
Cysticercosis is known since the biblical era. It has also been described in the Charak Sanhita, an ancient Indian medical book. Taenia is one of the earliest recognized helminths and currently, it has 42 valid species. The three most commonly recognized species of human importance are Taenia solium, Taenia asiatica, and Taenia saginata. T. solium and T. asiatica are known as pork tapeworms (pig being the natural intermediate host) and T. saginata as beef tapeworm (cattle being the intermediate host). Human acquires intestinal infection by the adult worm through ingestion of cysticercus (larva) in under/poorly cooked pork (in case of T. solium and T. asiatica) or beef (in case of T. saginata). All the species produce similar gastrointestinal symptoms in humans. Only T. solium is of medical importance for human because human can serve as intermediate host and the larvae liberated from the ingested eggs can enter the circulation and travel to different internal organs and can get encysted in any tissue known as cysticercosis. When the larva is lodged in the brain, the infection is called neurocysticercosis (NCC). It is the most severe form of the disease. Laboratory workers must take appropriate precautions while handling stool specimens containing eggs or proglottids to prevent accidental hand to mouth transmission. T. asiatica and T. saginata do not cause cysticercosis/neurocysticercosis (NCC) in human.
T. solium infection is highly endemic in Southeast Asia, Africa, and Latin America. The disease is increasingly reported from the developed world either due to travel to endemic regions or immigration of T. solium carriers from endemic countries. The estimated number of T. solium carriers is 2.5 million and cysticercosis cases are around 20 million. NCC is the most common cause of community-acquired active epilepsy. Worldwide data suggest that 26.3% to 53.8% of active epilepsy cases are due to NCC. The estimated death due to NCC is 50,000 per year. NCC is a preventable and potentially eradicable disease. In this review, I will share some of my personal experiences on taeniasis and NCC, based on studies in the pig farming community.
| Life Cycle of Taenia Solium|| |
Human acquires infection either by ingestion of eggs passed by T. solium carriers in their stool or by consumption of cysticerci (larvae) infested poorly cooked pork. Water, vegetables, and foods can get contaminated by eggs from Taenia carriers and can transmit the disease to human. When eggs are ingested, hexacanth embryos (larvae) are liberated in the intestine and enter the circular and get encysted in any internal organs. The encysted larva is called cysticercus and the disease is called cysticercosis. When the cysticercus is lodged in the brain, it is known as NCC. Consumption of measly (cysticercus infested) pork leads to the development of adult worm in human intestine. Pigs get infected by ingesting human feces containing eggs or proglottids passed by T. solium carriers. Human is the definitive and accidental intermediate host, while pig is the natural intermediate host. Details of life cycle with diagrams are available in our earlier publications.,
| Epidemiology|| |
Taeniasis and cysticercosis/NCC are highly endemic to all parts of the world where pigs are raised as a food source and allowed to roam freely with easy access to human feces. T. solium infection is highly endemic in Southeast Asian, sub-Saharan African, Latin American, and part of Oceanian countries. Cysticercosis is also widespread in the swine population in these countries. It is a marker of social and economic development. It is increasingly being reported in the industrialized countries either due to travel to endemic regions or immigration of T. solium carriers from endemic regions. The disease was underrecognized before the advent of newer diagnostic modalities such as computed tomography (CT), magnetic resonance imaging (MRI), and introduction of sophisticated immunological and molecular diagnostics. Before these technological advancements, NCC constituted only 2%–2.5% of all intracranial lesions with seizure disorders, which has now been reported in 25%–31% of cases.,
T. solium infection is highly endemic in many parts of India. Taeniasis ranged from 0.5% to 2% in hospitalized patients in Chandigarh, North India, and 12%–15% in labor colonies where pigs are raised. In Goa, the prevalence of taeniasis was 9.7% by stool examination. Taenia species was detected in 7.4% of schoolgoing children in Puducherry. NCC was identified in 31% of patients with seizure disorders in NIMHANS, Bangalore, India. In a community survey in South India, the prevalence of active epilepsy was 3.83/1000 populations; 28.4% of them had NCC by CT.
| Clinical Manifestations|| |
Intestinal infection by T. solium adult worm is called taeniasis. Taeniasis may remain asymptomatic with occasional expulsion of segments (proglottids) in the stool. However, it may cause gastrointestinal symptoms such as epigastric pain, vague abdominal discomforts, nausea, vomiting, and diarrhea.
It refers to encysted T. solium larva (cysticercus) in various internal organs. Brain involvement in human occurs in 70%–95% of cases and it is known as NCC. Other common sites are subcutaneous tissue, striated muscles, diaphragm, eye, and spinal cord. Ocular cysticercosis if not treated timely can lead to vision loss, and spinal cord lesion can cause cord compression, which can lead to radicular pain, weakness, and sensory deficits.
Clinical manifestations vary from completely asymptomatic to severe disease leading to death. Disease severity and clinical manifestations depend on the number, stage, and location of cysticercus and intensity of the host's immune response. In 85%–90% of cases, the cysticerci are located in the brain parenchyma (benign form). Around 10%–15% of cases of cysticerci are located in extraparenchymal sites such as subarachnoid space, ventricles, basal cistern, and aqueduct of Sylvius (malignant form). In general, parenchymal NCC presents with seizures. Other manifestations include recurrent or chronic headache (often migraine like), altered mental state/psychiatric symptoms, and focal neurological deficits. Presence of multiple degenerating parenchymal cysticerci with massive pericystic edema can cause cysticercotic encephalitis. Occlusion of small and medium intracranial arteries by cysticerci can lead to ischemic stroke. Entrapment of cranial nerves leads to paralysis of extraocular muscles, hearing loss, nerve palsy, and trigeminal neuralgia. Extraparenchymal NCC presents with sign–symptoms of raised intracranial hypertension (ICH) due to obstruction of cerebrospinal fluid (CSF) flow. Acute ICH due to NCC is a medical emergency and if untreated, it progresses rapidly with high mortality.
| Pathogenesis of Neurocysticercosis|| |
Cysticerci can survive in the brain for years, sometimes without any symptoms. Usually, the viable cysticerci disarm host defense by producing taeniaestatin and other molecules that interfere with lymphocyte proliferation and macrophage function. Moreover, they are protected from immune cells by blood–brain barrier (BBB). The cell wall of cysticerci is rich in glucan, which is immunologically inert. All these factors can lead to an asymptomatic state till the parasite starts degenerating either by natural course or following antiparasitic treatment. Once the parasite degenerates, the cyst fluid rich in immunodominant proteins is leaked which leads to inflammatory response and symptomatic disease. When numerous cysticerci are present in the parenchyma, their degeneration can lead to massive edema and cysticercotic encephalitis. Cysticerci in due course die and occasionally the lesions are resolved, but in most cases, they get calcified. Calcified lesions act as foci for seizure disorders. Extraparenchymal cysticerci can block CSF flow with raised ICH, which may present as a medical emergency.
| Treatment|| |
T. solium carriers are the only source of infection to human and swine. One T. solium carrier can infect a large number of hosts both humans and swine. Hence, T. solium carriers are the appealing target to disease control. Treatment can be individualized or can be mass population based in the endemic area. A single oral dose of either niclosamide (2 g in adults) or praziquantel (5–10 mg/kg) can cure taeniasis. Albendazole 15 mg/kg is a good alternative to praziquantel, especially in developing countries due to its low cost and easy availability.
Treatment of NCC is categorized under three headings: (1) symptomatic therapy, (2) cysticidal therapy, and (3) surgery. Symptomatic therapy constitutes antiepileptic drugs and anti-inflammatory drugs such as steroids; cysticidal therapy includes antiparasitic drugs (albendazole or praziquantel). Surgery for removal/resection of cysticercus is indicated when it is present in ventricles or in aqueduct of Sylvius obstructing the CSF flow. In case of severe ICH, emergency shunt placement or ventriculocisternostomy for CSF diversion is required.,
| My Personal Experience on Taeniasis and Neurocysticercosis|| |
While going through the village (Kalli Pashchim) just adjacent to my ex-working place, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India, in November 2000, I saw pigs were slaughtered on road slide for human consumption. I found some pigs were heavily infested with cysticerci. This observation convinced me to work on T. solium infection in this pig farming community.
We adopted a 30 cluster sampling approach as recommended by the World Health Organization to study the prevalence of taeniasis in the community. A total of 924 subjects belonging to 210 families from 30 villages provided their stool samples. Taeniasis was detected in 172 (18.6%). On multivariate analysis, history of tapeworm segments passed in the stool, consumption of undercooked pork, and hand wash after defecation with clay or plain water were associated with taeniasis. A total of 356 (38.5%) subjects in the study group had parasitic infection.
We analyzed Taenia proglottids and eggs positive human feces and cysticerci from pigs genetically based on cytochrome c oxidase subunit 1 gene (cox1). Both T. solium and T. asiatica were detected. On partial sequencing of cox1, T. solium isolates showed similarity with Asian genotype and nucleotide sequence variations ranged from 0.25% to 1.01%, whereas in T. asiatica, sequence variations ranged from 0.25% to 0.5%. Our T. solium strains formed a cluster (99% similarity) with strains of China, Indonesia, Japan, Madagascar, and Nepal, and T. asiatica with strains of China, Indonesia, Japan, Taiwan, and Thailand. Subsequently, we analyzed Taenia species based on the cytochrome B mitochondrial gene. T. solium and T. asiatica were identified in 40% and 60% of proglottids/eggs positive human feces, respectively. T. asiatica was identified in 15% of cysticerci obtained from different organs such as muscle, liver, and brain of swine (unpublished data).
Based on 30 cluster sampling, 1640 individuals of 294 families from 30 villages were enrolled for the study to estimate the NCC burden in the community. On a door-to-door survey, active epilepsy was identified in 95 (5.8%) individuals; 91 of them agreed for calf and thigh muscle ultrasound and for brain MRI. Only three (3.3%) had cysticerci (two in muscles and one in subcutaneous tissue) on ultrasound. On MRI, NCC has diagnosed in 44 (48.3%) patients with active epilepsy. Age above 15 years, epilepsy in the family and no separate place for pigs were associated with symptomatic NCC.
A total of 595 asymptomatic individuals from the same community agreed to undergo an MRI of the brain for estimation of silent NCC. Ninety (15%) of them had NCC on MRI. When the data from symptomatic and asymptomatic populations were analyzed, no statistically significant difference between the two groups in relation to number, location, and stage of the parasite was observed except that the viable cysticerci were more frequently observed in asymptomatic individuals. The next question that came to our mind was “why some individuals with the same number, stage, and location of cysticerci in the brain develop symptoms, while others with similar lesions remain asymptomatic? Do the parasite factors or the host genetic factors have a role in the development of seizure (symptom) “? To study the parasite factors, the cysticerci fluid proteins were fractionated into 12 fractions (F1 to F12) based on their molecular size. It was observed that the low molecular-weight fractions (F1 to F4) were more immunogenic when peripheral blood mononuclear cells from NCC subjects were stimulated. F2 fraction induced anti-inflammatory and regulatory cytokine response, while F1, F3, and F4 induced pro-inflammatory cytokine response. When the results were extrapolated to symptomatic and asymptomatic subjects, it was observed that symptomatic patients had significantly higher pro-inflammatory cytokine response and asymptomatic subjects had anti-inflammatory and regulatory cytokine response. The study substantiated that symptomatic patients had enhanced pro-inflammatory cytokine response, which contributed to inflammation-related tissue damage locally in the brain resulting in seizure disorders.
Host genetic factors such as toll-like receptor-4 (TLR-4), matrix metalloproteinase-9 (MMP-9), intercellular adhesion molecule-1 (ICAM-1), and glutathione S-transferase (GST) gene polymorphisms were studied. It was observed that NCC individuals with TLR-4 Asp299Gly and Thr399Ile genotypes were more frequently detected in symptomatic patients. TLR-4 Asp299Gly and Thr399Ile genotypes had 5.6 and 7.4 folds, respectively, increased risks for the development of seizure. TLR-4 Asp299Gly and Thr399Ile genotypes are known for Th-1 (pro-inflammatory cytokines) signaling. Pro-inflammatory cytokine-induced inflammation and tissue damage are likely responsible for the occurrence of seizures. When MMP-9 genotype frequencies were studied, it was observed that NCC individuals with MMP-9 R279Q genotype had 5.5-fold increased risk to develop symptomatic disease. Symptomatic NCC patients had significantly higher levels of MMP-9 compared to asymptomatic NCC subjects (344.5 vs. 165.9 pg/ml). MMP-9 plays an important role in BBB disruption through the digestion of collagen tissue of BBB. Disruption of BBB leads to an influx of leukocytes at the location of cysticerci in the parenchyma leading to the development of seizure in NCC patients.
ICAM-1 is also known as integrin expressed on vascular endothelial cells. Leukocytes bind to ICAM-1 and enter the brain by the process known as diapedesis. We observed that ICAM-1 E469E genotype had a significant association with seizure disorders. This particular ICAM-1 genotype modulates the expression of integrins that help in leukocytes infiltration in the brain leading to inflammation and symptomatic disease. Further, we studied different GST polymorphisms. It was observed that null GSTM-1 and GSTT-1 genotypes had a significant association with symptomatic disease. GST null genotype individuals are low producers of GST enzymes. These GST enzymes basically neutralize free radicals, reactive oxygen species (ROS) generated during inflammation, thus protect cells and tissues from damage. Since the symptomatic NCC patients have low GSTM-1 and GSTT-1 levels, ROS-related tissue damage appears to be a major contributor to seizure disorders. Our proposed hypothesis on the development of seizure (symptomatic disease) is shown in [Figure 1].
|Figure 1: Proposed hypothesis for the development of symptom (seizure) in neurocysticercosis. Cysticercus fluid antigens induce production of Th-1 cytokines, which enhance the TLR-4 signaling and local inflammation in the brain. TLR-4 (Thr399Ile and Asp299Gly genotypes) promotes production of Th-1 cytokines. ICAM-1 (K469E genotype) enhances the expression of integrins on vascular endothelium resulting in leukocyte adherence and infiltration in the brain. MMP-9 (R279Q genotype) enhances the production of MMP-9 that causes disruption of BBB resulting in leukocyte infiltration. Enhanced Th-1 cytokines and leukocyte infiltration induce inflammation and production of free radicals and ROS that cause local tissue damage and development of symptom (seizure). Low levels of GSTs due to null genotypes of GSTM-1 and GSTT-1 fail to neutralize free radicals and ROS and thus fail to prevent tissue damage. TLR-4: Toll-like receptor-4; MMP-9: Matrix metalloproteinase-9; ICAM-1: Intercellular adhesion molecule-1; BBB: Blood–brain barrier; ROS: Reactive oxygen species; NCC: Neurocysticercosis; GSTM-1: Glutathione S-transferase mu-1, GSTT-1: Glutathione S-transferase theta-1|
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| Porcine Cysticercosis|| |
Cysticercosis in pig (porcine cysticercosis) is a major cause of economic loss on individual farmers and on the pork industry. It is apparently a benign disease in swine despite the presence of thousands of cysticerci throughout the body. We surveyed local swine slaughterhouses to estimate the prevalence of porcine cysticercosis. We found that 26% of pigs slaughtered for human consumption had cysticerci in different organs such as muscles, brain, liver, and heart. Interestingly, around 38% of the infected swine had cysticerci in their brain. This is the first report on the MRI of swine demonstrating cysticerci in the brain and head-and-neck muscles [Figure 2]. Following health education about the preventive measures, especially among the pig farmers and mass albendazole therapy in the community, subsequent survey on 300 slaughtered pigs, the detection rate of cysticercosis decreased to 15% suggesting that preventive measures play an important role in disease control (unpublished data). Swine cysticercosis reported in other parts of India is as follows: in Chandigarh, 8%–10% of public slaughtered pigs and 0.5% of pigs reared in government farms, in Kolkata, 7% of slaughtered pigs, Bareilly (UP), 6% of free-roaming pigs and in Vellore, 11.6% of pigs were positive for antigen by ELISA and 59.8% for serum antibodies by EITB.
|Figure 2: T2-weighted magnetic resonance image of pig brain showing many cysticerci in the brain and in head-and-neck muscles|
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Further, we studied for the first time the immune response to various stages of the parasite in the brain and muscles of naturally infected swine. We observed a strong regulatory cytokine (interleukin 10) response in viable and Th-1 response in degenerating cysticerci; calcified cysticerci had a mixed Th-1, Th-2, and T-regulatory response. The study suggests that the type of immune response can influence the severity of disease. We also identified certain clinical signs of NCC in pigs and these clinical signs were excessive salivation, excessive blinking and tearing, and subconjunctival nodule.
| Antiparasitic Treatment in Swine|| |
We treated cysticerci-infected pigs with albendazole plus/minus steroid to evaluate the effects of treatment in swine. We divided the cysticerci-infected swine into two groups (10 in each group): one group was treated with albendazole alone and the other group with albendazole plus prednisolone (steroid). The details of dosing schedule are available in our earlier publication. Six weeks following treatment with albendazole alone, 100% cysticerci present in muscles and tongue responded to treatment (either killed or lesions resolved). Swine harboring ≤5 cysticerci in the brain had a 100% response to treatment; however, all 3 swine having ≥10 cysticerci in the brain died within 1 week following treatment. On autopsy, these swine had cysticercotic encephalitis with diffuse brain edema. In the albendazole plus steroid group, none of the swine irrespective of the number cysticerci in the brain died; however, the response rate both in the brain and muscle/tongue was 48% at 6 weeks and 71% at 12-weeks follow-up. We studied the immune response around the responder and nonresponder cysticerci and observed that a mixed Th-1, Th-2, and T-regulatory response associated with responder (dead) cysticerci and Th-2 and T-regulatory response with nonresponder cysticerci.
| Conclusions|| |
T. solium infection rate is a “biological indicator” of social and economic development. Poor sanitation with open-field defecation practices, poor hand hygiene, no separate place for pigs, and free roaming of pigs in the community increase the risk of infections. The high prevalence of taeniasis and swine cysticercosis suggests the continuity of transmission cycle between human and swine in the community. There is a need for further population-based studies in other parts of India to estimate the disease burden. T. solium infection is preventable and potentially eradicable. Mass anthelminthic therapy, health education, safe water, clean environment, improvement of hand hygiene, and sanitary conditions can reduce the disease burden. As a preventive measure, 1-week albendazole therapy to swine 6 weeks prior slaughter is likely to render them suitable for human consumption by killing the parasites in muscles and other organs. This can interrupt the transmission cycle from swine to human. However, further studies are required to reach a definitive conclusion. The high prevalence of T. asiatica both in human and swine in the community calls for further studies on this parasite.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]