Neurocysticercosis in Europe: still a public health concern not only for imported cases
Fabiani S., Bruschi F.*
Department of Translational Research, N.T.M.S., University of Pisa, School of Medicine, Via Roma, 55, 56126 Italy
*Corresponding Author: Prof. Fabrizio Bruschi, School of Medicine, Via Roma, 55 56126 Pisa, Italy
Tel. +39 (050) 2218547
Fax +39 (050)2218557
Neurocysticercosis in Europe is an increasing public health concern not only for imported cases. An effective surveillance system is still lacking, so the problem is certainly underestimated.
Abstract
Neurocysticercosis (NCC), a parasitic disease caused by the larvae of the cestode Taenia solium, is the most frequent parasitic disease of the Central nervous system (CNS) in the world and the leading cause of secondary epilepsy in Central and South America, East and South Asia, and sub-Saharan Africa. It is endemic in many low-and middle-income Countries of the world. Due to increased travels and immigration, NCC may be diagnosed also in non-endemic areas. In fact, tapeworm carriers from endemic zones can transmit infection to other citizens or arrive already suffering NCC. This phenomenon, occurred first in USA during the last 30 years, has been also observed in Europe, as well as in Australia, Canada, Israel, Japan and Muslin countries of the Arab World. Actually, concerning Europe, although, in some areas only few cases have been described, nevertheless the prevalence of NCC may be considered increasing, especially in Spain and Portugal. We reviewed the literature on the burden of NCC in Europe, by a search of PubMed regarding papers from 1970 to present. We only considered on PubMed published and available papers in English, French, Italian, and Spanish, the languages understood by the authors. One hundred seventy six cases of NCC have been reported in seventeen European Countries (Austria, Belgium, Denmark, Finland, France, Germany, Greece, Hungary, Ireland, Italy, Latvia, Netherlands, Sweden, United Kingdom, and Croatia, Norway, Switzerland). A particular epidemic situation is present in Spain and Portugal. In fact, we collected data that show, in Spain, an increasing incidence both in immigrated patients and in those which were born in certain Spanish geographical areas and, in Portugal, prevalence similar to that observed in endemic areas. Globally, it’s clear that as a result of increased migrations and travels from endemic regions, NCC is becoming an emerging public health problem in high-income countries, particularly affecting communities where hygiene conditions are poor and sub-sequentially the parasite can spread from human to human through eggs even in absence of a travel to the tropics. NCC is a preventable disease, it derives that it’s important to acquire a great consciousness of the epidemiology and to implement accurate surveillance systems.
Keywords
Neurocysticercosis, Europe, Epidemiology , Imported cases, Autochthonous cases
Abbreviations
1.Introduction
Neurocysticercosis (NCC) is the most frequent and widespread human neuroparasitological disease, caused by the larval form of the tapeworm Taenia solium (Hawk et al., 2005).
Cysticercosis occurs when human ingests the eggs of the adult tapeworm by a human-to-human fecal-oral transmission or possibly by an autoinfestation. In this way, humans act as the intermediate hosts in the life cycle of T. solium. Embryos are liberated from the eggs by the action of gastric juice and intestinal fluids; then, they cross the bowel wall and, entering the bloodstream, they migrate to any organ/tissue, including skeletal muscle, subcutaneous tissue, eye, liver, and preferentially brain (Flisser, 1994; White, 2000).
Inside the Central nervous system (CNS) cysticerci establish as viable cysts, and eliciting a weak inflammatory response in the surrounding tissues, they may remain for a long time in this stage. After a variable and undetermined time, depending on cyst characters and host immune regulation changes, a transition from asymptomatic to symptomatic disease can occur. In these circumstances, neurological symptoms could appear (Dixon and Lipscomb, 1961; Dixon and Hargreaves, 1944; Dixon and Smithers, 1934). Indeed, the involvement of the parenchyma, sub arachnoid space, ventricles, or spinal canal, is responsible for pleomorphic disorders, from a completely clinical silence to a broad range of clinical manifestations, including headache, seizures, hydrocephalus, coma and possibly death (Garcia and Del Brutto, 2005).
The disease is endemic in Latin America, South East Asia, India, Nepal, China, Africa and many other low- and middle income countries of the world (Flisser et al., 2003; Mafojane et al., 2003; Maguire, 2004; Pawlowski et al., 2005; Rajshekhar et al., 2003), representing, as already stated, the most frequent parasitic infection of the CNS (Carpio, 2002) and the leading cause of secondary epilepsy in Central and South America, East and South Asia, and sub-Saharan Africa (Commission on Tropical Diseases of the International League Against Epilepsy, 1994; De Bittencourt et al., 1996; Medina et al., 2005; Montano et al., 2005; Quet et al., 2010; Rajshekhar et al., 2006).
As regards other geographical areas, the first description of Taenia solium was made by Aristotle (“History of Animals”) in ancient Greece and also in ancient Egypt the parasite was circulating, as revealed by the finding of a cysticercus in the stomach wall of an Egyptian mummy of the late Ptolemaic age (second to first centuries B.C.) (Bruschi et al., 2006a). At the end of the XIX century cysticercosis was spread on all over the Europe until 1900, when the full knowledge of the entire life cycle of the parasite, including the role of pork, allowed to apply effective prevention and control measures which thus enabled human taeniasis and cysticercosis virtually to decline and in high-income countries even to disappear (Garcia and Del Brutto, 2005).
Unfortunately, these measures have not yet been completely implemented in many developing countries, and that is the reason why taeniasis and cysticercosis/NCC are still endemic in many areas, as described before.
The taeniasis-cysticercosis complex is characterized by a remarkable epidemiological stability, that is mainly due to the high biotic potential of the parasite (i.e. residual environmental contamination, average number of pigs infected by one tapeworm during a single day, time to tapeworm population renewal, etc.). Thus, complete eradication of T. solium has not been yet feasible (Gonzalez et al., 2002, 2003), and that is at the basis of the possibility of the representation of NCC in high-income countries through tapeworm carriers from endemic zones. In particular, tapeworm carriers can arrive from endemic zones, already affected by NCC or they can be a source of eggs which can be transmitted to other citizens (autochthonous cases).
During the last 30 years, due to increased travels and immigrations, this phenomenon has significantly developed (Kraft, 2007; Pradhan et al., 2003). It occurred first in USA (Más-Sesé et al., 2008; Rosenfeld et al., 1996; Schantz et al., 1992; Serpa et al., 2011, 2012; Shandera et al., 1994; Sorvillo et al., 2011; White and Atmar, 2002; White, 2000), and, after, it has been also seen in Europe, as well as in Australia, Canada, Israel, Japan and Muslin countries of the Arab World (Del Brutto, 2012 a, 2012b, 2012c, 2012d; Garcia and Del Brutto, 2005).
Concerning Europe, at present the data are not abundant. Until 1995, only few reported cases have been described, either in Western (Garcia and Del Brutto, 2005), or Eastern Europe (Adonajlo et al., 1969; Ferrante et al., 1985; Gauthier et al., 1995), and overall sporadic cases mainly occurred in immigrants from endemic regions (Wiegand et al., 1999).
Although in some European areas this parasitic disease continues to be rare, the frequency is increasing mainly due to the influx of immigrants from the endemic areas and increasing travels in these Countries (Del Brutto, 2012a).
We reviewed the literature, on the burden of NCC in Europe, detected by a search of PubMed for papers from 1970 to present). We only included on PubMed published and available papers in English, French, Italian, and Spanish, the languages understood by the authors (Fig. 1)(Tab. 1).
Over the year, from 1970 to now, decade by decade, we can appreciate a constant increasing number of publications on patients affected by NCC, which have passed from 67 during the period 1970-1994 to 109 between 1995 and 2013. (Del Brutto, 2012a); although the problem is still underestimated.
One hundred seventy six cases of NCC are collected in seventeen European Countries (Austria, Belgium, Denmark, Finland, France, Germany, Greece, Hungary, Ireland, Italy, Latvia, Netherlands, Sweden, United Kingdom, and Croatia, Norway, Switzerland) (Fig. 1). Among these patients, five were affected by spinal or medullary cysticercosis (Aghakhani et al., 1998; Bouree et al., 2006; Dietemann et al., 1985; Egberts et al., 2004; Malzacher et al., 1994), one was seropositive for HIV (Chianura et al., 2006), and one was both HIV seropositive and affected by spinal cysticercosis (Delobel et al., 2004). Moreover, one patient was a transplant recipient (Hoare et al., 2006).
Ninety five were imported cases from endemic areas (immigrants and European travelers). Only twenty cases are described as autochthonous NCC (five cases in Germany, fourteen cases in Italy, one case in United Kingdom). Other eight cases are not really autochthonous for the Countries where they have been described, but, anyway, they originate from European Countries such as former Jugoslavia (Juhl and Løgager, 2000), Turkey (Leth et al., 1992), Portugal, Spain (Raverdy et al., 1976), Greece (Sabel et al., 2001) and Croatia (Bauer et al., 1994; Gerken et al., 1986). From the analyzed published and available articles, for fifty three patients it was not possible to clarify the citizenship status (immigrants or European travelers or autochthonous cases) (Tab. 1) (Fig. 2).
A particular epidemiological situation is present in Spain and Portugal (Tab. 2) , where data, in total, show a number of cases more than fivefold the total cases reported in the seventeen European Countries analyzed. We reviewed data that show, in Spain, an increasing incidence both in immigrated patients and in patients who origin from some particular Spanish regions (Castellanos et al., 2000; Esquivel et al., 2005; Rodríguez-Sánchez et al., 2002; Ruiz et al., 2011) and, in Portugal, focusing on prevalence and distribution in the general population in the whole Country as well as in endemic areas (Monteiro et al., 1987). However, in these data, a clear identification of the geographical origin hasn’t been possible. Certainly, imported cases are the major part, but autochthonous cases exist, too (Antón Martínez et al., 2002).
2.Discussion and Conclusions
The analysis of the literature has showed unequivocally that due to increased migration and travels from endemic regions, NCC is becoming a constantly growing public health problem also in high-income Countries, particularly affecting communities where hygiene conditions are poor and consequently the parasite’s eggs can spread. Moreover, also autochthonous cases exist in Europe, particularly in Spain and Portugal, because of migration of Taenia carriers from endemic areas (Del Brutto, 2013). Analyzing published data, some categories of patients with NCC have been described. For example, in transplant recipients NCC was described rarely and they do not underlie to particular manifestations However, since these
patients are immunosuppressed, screening, prevention, and treatment are absolutely mandatory, to prevent more severe forms possibly with multiple-organ involvement (Mauad et al., 1997).
Considering another acquired immunosuppressing condition, relatively few cases of HIV and NCC co-infections have been reported in high-income Countries, even among patients from areas with a high prevalence of both diseases, separately considered (Chianura et al., 2006; Serpa et al., 2007; Soto-Hernandez et al., 1996; Thornton et al., 1992). Nevertheless, in our opinion mainly because of the improvement of diagnostic methods and the increasing number of people screened for HIV, co-infection rates are expected to rise, although at present, no systematic data are available.
NCC in HIV infection, with or without AIDS, may appear either as a life-threatening condition or as an incidental finding. In any case the identification of cysticercosis in HIV patients is very important, because other bacterial or parasitic diseases, such as tuberculous meningitis/tuberculoma and toxoplasmosis, are very common in HIV positive patients and often differential diagnosis is not so clear, and therapeutic approaches are absolutely different. Thus, just the consideration of cysticercosis in this group of patients can help an early diagnosis of an important and potentially severe comorbidity. Certainly, it is important to consider that in patients with HIV, the diagnosis of NCC can be difficult; serological assay results may be ambiguous to detect antibody in these immunosuppressed group, and the combination with radiological and clinical data is essential (Parija and Gireesh, 2009).
The effect of HIV co-infection on the natural history of NCC is not well defined (Delobel et al., 2004; Soto-Hernandez et al., 1996; Thornton et al., 1992). Moreover, it is not clear whether reconstitution of the immune system with HAART in patients with AIDS will worsen the outcome.
Symptoms of cysticercosis seem to depend on the host inflammatory response (White et al., 1997). As a matter of fact, decreased cell-mediated immunity which characterises advanced HIV infection should mantains the cysticercosis more likely asymptomatic, but no clear evidence supports these hypotheses (Delobel et al., 2004; Prasad et al., 2006; Soto-Hernandez et al., 1996; White et al., 1995).
In general, it could be postulated that the development of NCC in HIV co-infected patients may be related both to the host-parasite relationship and to the stage of progression of HIV infection. Nevertheless, further studies are necessary to clarify the pathogenesis, and the therapeutic response of NCC itself and of seizures secondary to NCC in the setting of HIV infection.
At present, NCC in HIV co-infected patients does not represent a major public health problem, especially in non endemic Countries, but this condition has to be taken into account in patients originated from endemic areas, and not only.
The accurate detection of T. solium tapeworm carriers is crucial as well as surveillance and intervention programs (Garcia et al., 1991). First of all, an epidemiological intervention to interrupt the chain of transmission is recommended both in developed and developing realities. More than one step should be considered in this route, and in particular, as indicated also by mathematical models (Gonzalez et al., 2003), only targeting both T. solium hosts (human and animal) a real effective intervention can be done.
Eight points have been demonstrated as essential:1. providing continuing health education to the population and to the healthcare personnel, mainly improving hygiene and sanitary conditions, veterinary control or surveillance systems in general; first of all avoiding use of human infected feces as agricultural fertilizer; 2. improving diagnostic techniques and notification networks, especially to increase reliable data concerning prevalence and incidence of NCC; 3. searching and reporting the sources of transmission of taeniasis/cysticercosis both in animals, including meat inspection, and humans; 4. limiting animal reservoir improving farm status and treating, and eventually vaccinating, pigs; 5. developing easy-to-use drugs, and safe and effective vaccine for pigs; 6. identifying community exposed to T. solium, carriers of adult tapeworms and closed contacts,
considering tapeworm carriers as potential sources of contagion to both themselves and to those living in their close environment; 7. targeting treatment against human taeniosis, selecting the drug of choice; 8.developing well defined protocols to clinically identify, and eventually manage, human cases.
However, in our opinion, the main epidemiological intervention is represented by the notification of the disease, which allows a true quantification of the incidence and prevalence of NCC at a regional, national, and potentially worldwide level.
Moreover, control measures should be focused to the causes of the increasing relevance of NCC in high-income countries, including Europe. In this contest, tapeworm carriers, that represent the main risk factor for acquiring cysticercosis, become the principal target. Thus, they have to be identified by a well conducted screening program (i.e. test for all “at risk patients”, such as travelers and migrants from T. solium endemic zones or their contacts, household or not; people with a history of taeniasis, positive stool examination or copro-antigen ELISA; people with late onset epilepsy of unknown origin). Once identification, the second step concerns providing treatment against intestinal tapeworms.
As previously proposed by Romàn et al. (2000), WHO Expert Consultation on Foodborne Trematode Infections and Taeniasis/Cysticercosis (2009) has emphasized the need to declare NCC an international reportable disease. The importance of the surveillance and the notification of the NCC as reportable disease have been shown in USA (Ehnert et al., 1992; Richards et al., 1985; Sorvillo et al., 1992), Mexico (García-Pedroza, 1997; Sarti et al., 1997), and Brazil (Takayanagui, 1996). At present, in Europe an effective surveillance system on NCC is lacking. The increasing on surveillance measures, together with the improvement of the diagnostic methods (Serpa and White, 2012), lead to reveal more and more new cases of NCC, although the clinical diagnosis of NCC is difficult, especially in non endemic areas, like Europe, where the disease is still rare but increasing (Del Brutto et al, 2001).
Literature searching method
The literature referenced in this review was searched by using the PubMed database for literature published from 1970 to present with keywords “Neurocysticercosis and Europe” OR “Neurocysticercosis in Europe” OR “Epidemiology of neurocysticercosis in Europe” OR “Neurocysticercosis case reports in Europe”.
Acknowlegement
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Figure legends
Fig. 1 European Countries with on PubMed published and available reported cases of neurocysticercosis (period from 1970 to present) *: only imported cases; the circle indicates the particular epidemic situation of Spain and Portugal.
Fig. 2 Collected cases in seventeen European Countries (Austria, Belgium, Denmark, Finland, France, Germany, Greece, Hungary, Ireland, Italy, Latvia, Netherlands, Sweden, United Kingdom, and Croatia, Norway, Switzerland).
Highlights
NCC in Europe is still a public health concern not only for imported cases
Over the year, from 1970 to present, decade by decade, we can appreciate a constant increasing number of publications on patients affected by NCC
At present, in Europe an effective surveillance system on NCC is still lacking
The increasing on surveillance measures, together with the improvement of the diagnostic methods, bring to reveal more and more new cases of NCC
