Geographic distribution, usually affected organs, and most frequent neurological forms according
The human central nervous system (CNS) may be affected by infections of several species in the
Schistosomiasis is among the parasitic diseases with the highest epidemiological importance in the world. According to the World Health Organization, schistosomiasis occurs in 76 countries and 230 million individuals require treatment annually [1,2]. Of these, about 100 million present some clinical manifestation and 20 million present severe forms of the disease [1-5]. Annually, over 200.000 people die as a consequence of schistosomiasis. In the year 2010, around 33.5 million people were treated. Despite advances in the control of the disease, with lowering of mortality and morbidity, schistosomiasis still represents a challenge to public health and has increased its area of transmission throughout the years . Since it hits the poorer regions of the world, being associated with precarious sanitary and adverse social-economical conditions, this disease has been neglected. With the increase of migratory flow and adventure tourism travels, innumerable schistosomiasis cases have been occurring, even in non-endemic countries [6-13]. Schistosomiasis is a disease caused by trematode worms, belonging to the Schistosoma genus. There are many species which affect man in different clinical manifestations, elimination methods, intermediary hosts and geographical distribution. These species share the same pattern in reproductive cycle, the transmission occurring through eggs, a proportion of which are eliminated through urine (
2. Clinical forms of schistosomiasis
2.1. Acute phase
Acute forms are basically cercarial dermatitis or summer's itch, cutaneous lesion secondary to the penetration of the skin by the cercaria, and Katayama's fever (or syndrome), which is also called acute or toxemic schistosomiasis and occurs, in genera, after three to nine weeks of cercariae penetration, when they have already become adult worms and start laying eggs. Toxemia is secondary to hypersensitivity reactions to the parasite, being characteristic to patients who do not reside in endemic areas and that are exposed to contaminated water bodies [15,16]. This form presents with fever, chills, cough, weakness, weight loss, diarrhea, vomiting, urticarial reactions, hepatosplenomegaly and eosinophilia. These manifestations last, in general, a few days but can last months and, in rare cases, be fatal. These patients present big periovular necrotic-exudative granulomas dispersed throughout the intestines, liver and other organs , and generally present spontaneous clinical improvement after a few weeks, but treatment associating schistosomicides and corticosteroids reduce the persistence time of symptoms and prevents evolution into the chronic phase.
|Sub-Saharan Africa, Brazil, Egypt, Middle-East, other regions in Africa and in the Americas||Liver, spleen and intestines||Spinal cord schistosomiasis (mainly) and cerebral schistosomiasis|
|Sub-Saharan Africa, Brazil, Egypt, Middle-East, other regions in Africa||Bladder, urethra and ureter||Spinal cord (mainly) and cerebral schistosomiasis|
|China, South-East Asia and Pacific islands||Liver, spleen and intestines||Cerebral schistosomiasis (mainly) and spinal cord schistosomiasis|
2.2. Chronic phase
Schistosomiasis' chronic phase is frequently asymptomatic. Symptoms occur with more frequency in patients who are repeatedly exposed to transmissions focuses and end up developing high worm burden. Chronic forms depend on the involved species. Schistosomiasis mansoni chronic forms are usually classified as: intestinal, hepatointestinal, hepatosplenic and decompensated hepatosplenic. In the intestinal and hepatosplenic forms patients usually do not present significant symptoms, but when present they may include abdominal discomfort, fecal urgency, episodes of diarrhea with eventual mucus or blood. Hepatic lesions are caused by egg embolism secondary to inflammatory reaction, but without significant clinical repercussions. With progression of infection and chronic inflammatory process, these patients may present significant periportal fibrosis, leading to portal hypertension. This phase is called hepatosplenic and the patient may suffer ascites and severe esophageal varices . Schistosomiasis japonica may cause the same kinds of manifestations, although liver function is usually more compromised. In schistosomiasis haematobia, oviposition may cause bladder inflammation, alongside blood in the urine and urinary urgency. Lesions in the urinary tract may cause fibrosis and urinary obstruction, leading to obstructive uropathy and increasing the risk of bladder cancer. These chronic forms depend fundamentally on high worm burdens, therefore they are diseases that affect mainly inhabitants of endemic areas. For instance, hepatosplenic forms of schistosomiasis mansoni are more frequent in areas with high endemicity and very rare in areas of low endemicity. Differently, ectopic forms of schistosomiasis occur as consequence of egg or work accumulation in any organ of the patient and, therefore, is not related to high worm burdens. Thus, it can occur in patients of endemic areas or in patients of non-endemic areas with casual exposure to the focus of transmission.
3. Spinal cord schistosomiasis
The human central nervous system (CNS) may be affected by infections of several species in the
Up until the 1980's, medullar lesion caused by
With the technological improvement in the field of immunological methods and imaging examinations, including the introduction of Computerized Tomography (CT) and, mainly, Magnetic Resonance Imaging (MRI), differential diagnosis with other causes of myelopathy has become easier. This can explain, at least in part, the great amount of articles being published in this area [22,38-44]. With the increase in interest for adventure tourism, a growing number of spinal cord schistosomiasis cases, who live in non-endemic areas and are infected in their leisure time, have been described in the literature. Spinal cord schistosomiasis, which had been considered a rare disease from the beginning of the 20th century to the early 80's, now appeared to have been, in fact, under-recognized. In the last years, it has attracted more and more the interest of researchers and is considered one of the forms of schistosomiasis that must be reevaluated from the point of view of disease burden by Public Health Organizations .
There are, in the literature, studies that allow an evaluation on the incidence or prevalence in the population with schistosomiasis or exposed to the risk of schistosomiasis. In bibliographical studies of international literature between 1930 and 1984, 64 patients were identified (12 with
The proportion of patients who go from schistosomiasis to spinal cord schistosomiasis is unknown. But a study done in Bahia with 212 patients with non-traumatic medullar lesion shows that 9.9% (21 cases) of patients had schistosomotic etiology . In another, similar study performed at the Sarah Kubitschek Hospital, in Brazil, with 231 patients, this etiology corresponded to close to 6% of the patients (13 cases) of non-traumatic medullar lesion seen in 4.5 years . There are several indications that this disease has been under-diagnosed [46-49] in endemic areas because of the difficulty of access to more sophisticated diagnostic methods and, in more developed areas, because of the lack of knowledge on the part of the doctors about this disease . This situation has been changing in the last years, particularly in Brazil, due to the improvement in diagnostic tools and better access to medical attention in the country. This may explain the increase of cases in patients of this country that are reported in the literature.
Knowledge of the epidemiological profile of the patient with spinal cord schistosomiasis can be obtained based on case reports or serial cases [26, 42, 50-52]. Spinal cord schistosomiasis occurs more frequently in male patients, with ages between 15 and 50, having low worm burden, up until then not presenting symptomatic neuroschistosomiasis, presenting intestinal and hepatointestinal forms, living in non-endemic areas (who had an eventual exposure to risk of infection) or in endemic areas.
There are several indications that a greater risk for spinal cord schistosomiasis cases in patients is present for patients with low worm burdens [53-55]. This means that spinal cord schistosomiasis can occur in patients with low risk for severe hepatosplenic forms. They are patients who do not present symptoms relating to the digestive tract, which often may lead the assisting physician not to think of schistosomiasis diagnosis. Other patients, aside from not having digestive symptoms, are not frequently exposed to the risk of transmission, making the diagnosis even harder. Examples of said patient profile are tourists who have been only sporadically exposed in areas of schistosomiasis transmission [27, 56, 57], patients who live in urban areas who, usually, have sporadic contact with transmission focuses , residents of areas that are recent focuses of transmission , and residents of areas with low prevalence for schistosomiasis .
Despite the severity of sequelae and disabilities caused by spinal cord schistosomiasis, this form of schistosomiasis is still not being considered in the development of public policies that aim to control the morbidity of schistosomiasis [1, 45, 58].
Knowledge on spinal cord schistosomiasis physiopathology has greatly improved in the last years, although some blanks still remain. It is known that periovular granulomas play a central role in medullar lesion [54, 55]. Although signs of vasculitis with immune complexes deposits close to the granulomas can be found , it is believed that these findings have a secondary role in the lesion. The mass effect produced by the granuloma and the edema that surrounds it may lead to the compression of internal structures to the spinal canal, causing secondary and definitive ischemic lesions. The eggs get to the medulla via the Batson venus plexus through embolization or through anomalous worm migration, in which case they would lay their eggs next to the medulla [54, 55]. This plexus was first described in 1940 by Batson, who intended to explain a mechanism for metastases being dispersed to the CNS . It is a network of valveless veins that connects the inferior vena cava to the veins in the vertebrae. This plexus allows the embolization of eggs without the need for collateral circulation or arteriovenous shunts, seen only in the hepatosplenic and cardiopulmonary forms of schistosomiasis. The eggs of
The greater proportion of spinal cord schistosomiasis cases in patients who present the initial form of schistosomiasis when compared to the ones who present the advanced form appears to have immunological and hemodynamic reasons. Pittella and Lana-Peixoto studied extensively the occurrence of
Patients with hepatosplenic and cardiopulmonary forms usually present discreet periovular reaction, without granulomatous response or with smaller granulomas, in non-productive stages and located in several regions of the CNS [53-55, 61, 62]. Only 10% of the patients who had eggs in the CNS in the necropsy, and presented these advanced forms also presented neurological symptoms when alive. . One of the suggested mechanisms to explain egg dispersion in cases of patients with hepatosplenic and cardiopulmonary schistosomiasis is that the eggs would get to the CNS by bypassing through collateral portal-like circulation and intrapulmonary arteriovenous shunting, secondary to hemodynamic alterations common to these advanced forms of schistosomiasis. In these cases there is major egg dispersion through the CNS through anastomoses, but few of these eggs cause symptoms given that the inflammatory response in these patients is usually discreet. In patients presenting schistosomiasis in the intestinal and hepatointestinal forms, the most viable way for the worm couples to reach the CNS is Batson's plexus and, therefore, the most common neurological forms are medullary.
5. Schistosomiasis and immune response
During the disease's evolution, immune responses change over time, there being several cytokines that participate with different responses at each moment. Immediately after infection by
With the evolution of schistosomiasis, TH2 polarized response is attenuated by suppressor T-cells, which modulate immune response, diminishing the production of cytokines, inhibiting the formation of granulomas, and diminishing the size of the granulomas that do form [63-65], a situation which has been observed in patients with hepatosplenic and cardiopulmonary schistosomiasis. This may explain the reason why there are many patients with advanced forms who present multiple eggs in the CNS, without inflammatory reaction around them and that, therefore, do not elicit any symptom [54, 55, 66].
6. Clinical manifestations
The typical clinical manifestations of spinal cord spinal cord schistosomiasis is acute or subacute and presents with lumbar pain with or without radiation to lower limbs, evolving with diminishing of muscular strength in these limbs, with the possibility of presenting, in addition, sensory alterations such as hypoaesthesia, paresthesia and dysesthesia . Clinically, there may be myeloradicular or radicular compromising of the medulla, with lesions in several segments of the medulla. Lesions which are higher in the spinal cord and in a functional section of the medulla may present signs of pyramidal liberation, such as Babinski's or hyperreflexia in the lower limbs. Lower lesions may present themselves as cauda equina syndrome with hypo- or areflexia in the lower limbs and unresponsive plantar-cutaneous reflex. Patients with spinal cord schistosomiasis usually present fecal and urinary retention, or other sphincter alterations, aside from erectile dysfunction . The amount of time between the beginning of the symptoms and the establishment of the complete manifestation normally ranges from a few days to a couple of weeks [21, 26, 66-68]. In general, these patients do no present systemic symptoms. Some patients may present cephalalgia, vomiting and other signs of meningeal irritation, such as Kernig's, Brudzinski's or nuchal rigidity . When there is radiculopathy, patient may present Lasègue's sign. Spinal cord schistosomiasis' typical triad is diminishing of muscular strength, with sensory alterations in the lower limbs associated with bladder dysfunction, this triad is found in 92,6% of the cases .
Spinal cord schistosomiasis' diagnosis it not always simple, but there is a consensus that an adequate diagnosis must include typical clinical manifestation (medullar and/or radicular symptoms), proof of exposure to
8. Imaging examinations
MRIs are very important when investigating spinal cord schistosomiasis and may show important data about the location and extension of the lesions. Although it's not a examination that can define completely the etiology, it may collaborate to differential diagnosis by showing inflammatory lesions and ruling out tumorous lesions. The affected area may present with increased volume or just an increase of paramagnetic contrast caption (Figures 3a, 3b, and 3c). The most frequently found aspect is a granulated pattern that may not be exclusive to, but is highly suggestive of, spinal cord schistosomiasis (Figures 4 and 5). A CT picture has a lower sensibility and, in some cases, may show evidence of increased volume or just high contrast caption [30, 38, 39, 41, 43, 44, 50, 68-71].
9. Laboratory examinations
Nonspecific examinations may suggest the etiology in a clinically suggestive patient. Routine CSF examination may show alterations in a high percentage of the cases, such as increase in proteins in 95% and of leukocytes in 98% of the cases, generally with predominance of lymphocytes and presence of eosinophil granulocytes in 40.8% of the cases . Despite being highly suggestive of spinal cord schistosomiasis, pelocytoses, high protein concentration and eosinophilia in CSF are not always present .
There are several immunological examination techniques to be used in the serum or CSF. The most used ones try to reveal the presence of antibodies which are specific for soluble egg antigens (SEAs), antigens from the digestive tube of adult worms, or antigens from cercariae. The most used serology techniques are ELISA (Enzyme-linked immunosorbent assay) or indirect immunofluorescence assay. Immunological blood examinations have a sensitivity varying between 80% and 97% and when tested on CSF sensitivity may vary between 56% to 97% (22, 26, 35, 68, 69, 72]. Immunological examinations must be considered as strong evidence of active
A proper investigation must be done to exclude other causes for the medullar and/or radicular lesion, such as bacterial infections (e.g. tuberculosis, syphilis, abscesses), viral infections (e.g. cytomegalovirus, poliovirus, enterovirus, HZV, HSV-1, HSV-2, HIV, HTLV-I) parasitic diseases (e.g. cysticercosis, toxoplasmosis), fungal infections or non-infectious, such as neoplasia, systemic lupus erythematosus, auto-immune vasculitis, diabetic vasculitis, B12 vitamin deficiency, multiple sclerosis, Guillan-Barré Syndrome, among others [26, 51, 68, 69, 72, 73].
Treatment is done through the use of corticosteroids and schistosomicides. The corticosteroids will diminish the inflammation and lead to regression of the granuloma, being even more important than the schistosomicide. The latter will eliminate the egg production by killing the adult worms and indirectly diminish the production of soluble egg antigens, which are important stimuli for the granulomas. In a few cases, surgical procedures may be necessary to decompress medullar structures. In other cases, treatment is clinical [26, 51, 73]. The schistosomicide may be oxamniquine (15 mg/kg dose for adults and 20 mg/kg for children with up to 5 years of age) or praziquantel (60 mg/kg for children with up to 15 years of age and 50 mg/kg for adults), both in a single dose . The corticosteroid dose is the equivalent to prednisone 1 mg/kg/day, and must be administered for 6 months, with careful suspension, given that patients may present relapses during the process.
In addition, complementary care involves adequate integral approach with psychosocial rehabilitation and motor physical therapy, intermittent bladder checking, prevention of pressure ulcers, among others. Special care must be taken regarding urodynamic aspects [26, 70, 73]. The use of laxatives or enema may be needed for patients with fecal retention.
Evolution depends, fundamentally, on early diagnosis and care, better prognosis being associated with an early introduction of the treatment, and particularly the introduction of glucocorticoids . Although symptoms and urological functional alterations do not always respond well to adequate treatment, despite its being started precociously [26, 70, 74, 75]. Patients may recover motor function, sensitivity, sphincter and erectile function control, or they may end up with any combination of absence or recovery of some of the aforementioned functions. Urodynamic alterations have not shown significant improvement in patients who underwent protocol treatment. Ferrari and colleagues (2004) found complete recovery in 31.7% (20) of the patients, 28.3% (18) of the patients presented partial recovery with no functional limitation, 25.4% (16) patients presented partial recovery with functional limitation, and 14.3% (9) of the patients did not improve at all . There were no deaths in this case series. Among the sequelae are paraplegia, paraparesis, dysfunction in the bladder or anal sphincter, sexual dysfunction, definitive sensitivity loss in the affected areas or even paraesthesia and dysesthesia [26, 30, 51]. Detailed studies on the urological aspects, done by Lima (2004) in the Hospital da Restauração in Recife, PE, show that after 9 months of treatment 52 (80%) of 65 patients, showed alterations in urodynamic examinations and 45 (69.2%) showed alterations in voiding cystourethrogram .
Several factors can actively contribute to the increase in the identification of spinal cord schistosomiasis cases, such as: improvement in diagnostic resources, increase in ecotourism activities with greater exposure of the population to risk of infection, growth of the transmission area, even in urban areas, and lowering of high parasitical loads, without diminishing of the global prevalence of schistosomiasis. There is need of investing in the study of spinal cord schistosomiasis, focusing epidemiological aspects such as: prevalence and incidence, relations between general schistosomiasis incidence and spinal cord schistosomiasis, prevalence and incidence in areas of high and low endemicity, and predisposing factors. Despite how successful controlling the hepatosplenic and cardiopulmonary forms has been throughout the years, control instruments used currently have not shown themselves as sufficient to control the spinal cord schistosomiasis problem. More studies are needed for improving the understanding on the real prevalence of the medullary forms of schistosomiasis. Changes in the Health Surveillance Systems are needed to improve control of schistosomiasis, aiming at a better understanding of the schistosomotic morbidity, particularly that of spinal cord schistosomiasis. It is not surprising that schistosomiasis control politics, based on parasitical diagnostic and treatment of the infected, have not been able to reduce the morbidity of the disease due to medullar lesions, since most patients who present this form of schistosomiasis have low worm burdens and present with negative fecal examinations. To reach effective control of spinal cord schistosomiasis, the introduction of more sensitive diagnostic methods and the development of more effective medicines for diagnosis and treatment of mild forms of schistosomiasis with low worm burdens will be needed in the basic health systems. For an initial diagnosis, the possibility of immediate introduction of serology as a diagnostic instrument in the Basic Health Units. This examination can be used as diagnostic in those patients who are still untreated. But more studies will be necessary for the development of more effective medicines and of more sensitive methods for parasitological removal. It is also important to disclose the occurrence of this form of schistosomiasis, as well as capacitating professionals for attending these patients, particularly in endemic areas and recently formed focus points. A secondary gain of disclosing information on the existence of severe forms may be the population increase in attendance to control measures for this disease.
|• Bacterial infections: tuberculosis, syphilis, abscesses, Lyme's disease.|
• Viral infections: cytomegalovirus, poliovirus, enterovirus, HZV, HSV-1, HSV-2, HIV, HTLV, EBV, HBV.
• Other infections: cysticercosis, toxoplasmosis, Chagas disease, fungal infections
• Non-infectious: neoplasia, systemic lupus erythematosus, auto-immune vasculitis, diabetic vasculitis, B12 deficiency, multiple sclerosis, polyradiculopathy, Guillan-Barré Syndrome, spinal disc herniation, syringomyelia
|• Lumbar pain with or without radiation to lower limbs|
• Paraesthesia or diminishing of lower limb sensitivity
• Paraparesis or paraplegia
• Anal and bladder sphincter dysfunction
• Evolution is generally acute or subacute (between 2 to 60 days)
|• Low thoracic or high lumbar medullar symptoms,|
• Proof of exposure to
• Exclusion of other causes for myelitis
|• Ages between 15 and 50|
• Predominantly male
• Low worm burden
• Patients thus far do not present symptomatic schistosomiasis or present intestinal and hepatointestinal forms (IS or HIS)
• Patients may reside in endemic areas or non-endemic areas, with eventual exposure to risk of infection
A special acknowledgment is dedicated to Luana Hughes Freitas for the discussion of the central ideas, inspiration and encouragement for the production of this document. The authors also acknowledge Nicole Montenegro, Marcela Montenegro Coelho e Bruno Montenegro Coelho for their dedication and support for studies in medullary neuroschistosomiasis. Acknowledgment is also due to Professor Luciano de Souza Queiroz, Department of Pathology, FCM-UNICAMP who produced the images of optical microscopy.
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