Laranjo-González et al. Parasites & Vectors (2016) 9:81 DOI 10.1186/s13071-016-1362-3 REVIEW Open Access Epidemiology, impact and control of bovine cysticercosis in Europe: a systematic review Minerva Laranjo-González1*, Brecht Devleesschauwer2,3, Sarah Gabriël4, Pierre Dorny3,4 and Alberto Allepuz1,5 Abstract Background: Bovine cysticercosis in Europe has been known for centuries but the data showing the occurrence of this zoonosis are scarce. The aim of this paper is to review and present the current knowledge on bovine cysticercosis in Europe. Methods: We conducted a systematic review of studies published between 1990 and November 2014. Qualitative and quantitative data on prevalence, risk factors, burden and interventions were extracted and analysed. Results: Reports on prevalence were available for 23 European countries, mostly from western and central Europe; for a few of these only data before 1990 were available. Prevalence based on meat inspection was generally low (below 6.2 % in 95 % of the records) and varied between and within countries. Serology and detailed meat inspection provided a higher prevalence range (0.41–14 %). Only few studies analysing risk factors were identified. Reported factors related to access to pastures and risky waters, dairy production and uncontrolled human defecation in the proximity of the farm among others. Only one estimate of the economic impact of the disease could be identified. Recommended interventions were focused on increasing diagnostic tests sensitivity or the application of risk based surveillance strategies. Conclusions: There is a lack of complete and updated data on most countries, especially in eastern Europe. Further risk factor studies might be needed together with estimates on the burden of the disease in all European countries. Risk-based interventions are being encouraged but current data are limited to guide this approach. Keywords: Bovine cysticercosis, Taenia saginata, Prevalence, Risk factors, Burden, Cattle, Europe, Systematic review Background In cattle, natural infections are normally asymptomatic Bovine cysticercosis is a parasitic infection of cattle but they cause financial losses to the cattle industry due caused by the larval stage (cysticercus) of the cestode to downgrading, condemnation, extra handling, refriger- Taenia saginata. Humans are the definitive host and ation and transport of the infected carcasses [3]. The harbour the adult form of the parasite in their intestines. main intervention to control bovine cysticercosis in Terminal segments containing eggs are detached from Europe is meat inspection, followed by condemnation or the adult parasite and millions of eggs may be released freezing treatment when necessary, as prescribed by Euro- daily to the environment [1]. Cattle acquire the infection pean legislation [4]. However other measures such as through the ingestion of eggs [2]. The parasite migrates thorough cooking of meat and the compliance with the to metabolically active muscles where it develops into regulations on the treatment and use of wastewater and cysticerci and humans get infected by consuming raw or sludge are determinant to prevent parasite transmission. undercooked meat containing infective cysticerci. The current knowledge of the epidemiological situation of bovine cysticercosis in Europe is mainly based on the de- * Correspondence: minervalaranjo@gmail.com tection of cysticerci in the carcasses of bovine animals dur- 1 Centre de Recerca en Sanitat Animal (CReSA)-Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Campus UAB, Bellaterra, Barcelona 08193, ing meat inspection at the slaughterhouse. In the European Spain Union meat inspection is enforced through Regulation Full list of author information is available at the end of the article © 2016 Laranjo-González et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 2 of 12 (EC) No 854/2004 which prescribes a visual inspection of institutions (i.e. the European Food Safety Authority publi- specific muscles and incisions in the internal and external cations; Codex Alimentarius guidelines) and unpublished masseter muscles (not applicable to animals under six work (i.e. master’s thesis). weeks of age) and a lengthwise incision of the heart in cattle In a first screening of all retrieved records, duplicate of all ages. Carcasses and offal of heavily infected animals records were excluded. The titles and abstracts of all (generalised infections) are to be condemned. In the case of unique documents were then screened for relevance to lightly infected cattle (localised infections) the affected parts the scope of the review. If the eligibility of the document are condemned and the rest of the carcass must undergo a could not be assessed from the abstract and title only, freezing treatment that inactivates the cysticerci [4]. the full text was screened to exclude or include the Bovine cysticercosis is distributed worldwide and af- document. The exclusion criteria were: (i) publication fects developing and industrialised countries [5]. Official date before 1990; (ii) wrong agent (other than Cysticer- meat inspection reports are considered to be an under- cus bovis or T. saginata); (iii) wrong host (other than estimation of the real prevalence as meat inspection has bovine); (iv) providing epidemiological information from a low sensitivity for the detection of cysts in muscles [5]. outside Europe; (v) providing information different than The precision of the visual identification is also ques- occurrence, risk factors for T. saginata bovine infection tionable, as the cysticerci can be confused with lesions and its burden or control measures; and (vi) book chap- caused by infections with Sarcocystis spp. and Actinoba- ters. Figure 1 shows the steps applied in the search. cillus spp. or with other local alterations [6]. Papers included at this stage were selected for full text In Europe, the presence of T. saginata has been revision and assessed for eligibility. Records for which the known for centuries, yet data on the occurrence of this full text was not available were excluded. Yet, ten of these zoonosis are scarce, fragmentary and inaccurate with records provided relevant information in the abstract. This variations regarding the levels of infection in the differ- information was included in the review. Records in lan- ent countries and regions. The aim of this paper is guages other than Spanish and English were translated therefore to review and present the current knowledge with Google Translate (https://www.google.es). of bovine cysticercosis in Europe. At this step, the screening process was independently assessed by two other reviewers and disagreement about Methods eligibility was discussed among the three reviewers until Search strategy a consensus was reached. A list with the references in- We conducted a systematic review of peer-review papers cluded in the review is provided in the Additional file 2. published from 1990 to November 2014 on the occur- For each eligible study, quantitative and qualitative rence, risk factors, control measures and burden of bovine data were extracted. Quantitative data regarding preva- cysticercosis in Europe. We followed the PRISMA guide- lence and risk factors were stored in a predefined spread lines for reporting systematic reviews [7] Additional file 1. sheet document. Recorded data included information In a first step, specific review questions were defined in about the country, year of publication, year to which the order to accomplish the scope of the review. The key ele- data belonged, prevalence and 95 % confidence interval ments of these review questions were the population (i.e. (if provided), level of data collection (i.e. national or re- cattle), exposure (i.e. risk factors or burden), intervention gional) or measures of association among others. In the (i.e. control measures) and outcome (i.e. bovine cysticerco- case of prevalence, both original and non-original data sis). The search was performed in three international biblio- were collected from the included papers. If the same graphic databases: PubMed, (on 15 November 2014) and data were reported in more than one paper these were Scopus and Web of Science (on 16 November 2014). The taken into account only once to avoid duplications. If literature search was performed in English using the follow- non-original data were lacking details (e.g. collection ing set of keywords: ((cattle OR bovine OR beef) AND (cysti- date or location), the original source, although not ini- cerc* OR taeni* OR tapeworm OR tapeworms)) OR tially included in the review (e.g. study prior to 1990), “saginata”. For each bibliographic database the search strat- was consulted unless it was not available. egy was adapted as follows: in PubMed and Scopus the Data from reports such as the European Food Safety search was done in “All Fields” and in the Web of Science, Authority (EFSA) zoonoses reports were used when ori- it was done in “Topic Field” which includes Title, Abstract ginal source providing the same data (e.g. prevalence for and Author Keywords. Retrieved records were exported to a country in a specific year) had not been included in an Excel file. Other records reviewed included records ob- the review. If the year when the prevalence data were tained through citation searching (publications cited in pa- collected was not available the year of the publication of pers included in the systematic review), the proceedings of those data was considered instead. Whenever prevalence the European Network on Taeniosis/Cysticercosis (CYSTI- data corresponded to an interval of years for the purpose NET) meetings, documents published by international of representing it in bar plots only the first year was Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 3 of 12 Fig. 1 Flow diagram: search strategy steps considered. All the descriptive analyses were performed table displaying all the prevalence data identified using R 3.2.0 (https://www.r-project.org/). through the review is provided in Additional file 3. Qualitative data on occurrence, risk factors, burden In total we collected data from 50 different sources and control measures were extracted and compiled in reporting bovine cysticercosis prevalence in Europe tables along with the bibliographic reference. These based on meat inspection. The number of published re- qualitative data were classified according to the type of ports and/or personal communications per year was information given: source of infection in outbreaks, risk quite low with no more than three reports in most of factors, protective factors. Identified risk factors were the years. Reports showed that bovine cysticercosis has further classified into categories. Relevant information been present in Europe for decades and is still present on burden was extracted and summarised in a narrative today (Fig. 2). Most of the data referred to the situation form. Information on control measures was extracted after 1990, since only reports published after 1990 were and grouped into broad categories (i.e. methods to im- selected for inclusion. Nevertheless, from the included prove sensitivity, measures to destroy eggs, measures to records we identified data on prevalence from 1918 until apply to positive farms or preventive measures at farm 2013 and for some countries such as Greece, Hungary, level among others). The Netherlands, Slovenia and Serbia we could only identify reports referring to prevalence prior to 1990 Results (Fig. 3). The level of prevalence reported by routine meat Prevalence inspection was generally low across Europe as the preva- We identified bovine cysticercosis prevalence reports for lence was below 6.2 % in 95 % of the records and below 23 out of the 49 European countries. Most of the data 4.3 % in 90 % of the records. originated from routine inspection and just a few studies Few sources provided the age of the animals inspected. reported results based on other diagnostic techniques Only in a few cases prevalence was given for different such as serological tests or detailed meat inspection. A groups of age. Results showed higher rates for adult Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 4 of 12 Fig. 2 Number of sources reporting prevalence per year of publication and per year of data collection. If data are collected for an interval or years only the value for the first year is presented in the graph Fig. 3 Map of Europe representing availability of prevalence data per country Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 5 of 12 animals than for calves. In a Croatian abattoir during Netherlands). In most of the cases it was below 1.0 %, al- 2005–2010 the prevalence detected in calves (0.014 %) though the variability between and within countries was was lower than in steers (0.093 %) and much lower than very high (Fig. 4). in cows (0.69 %) [8]. In the UK, during 2008–2011 the Few studies reported results based on more sensitive prevalence detected in calves and adults was 0.008 and inspection methods such as serology or detailed meat in- 0.032 %, respectively [9]. These results are in line with spection. Studies carried out in Belgium [5] and north- the epidemiological situation observed in Belgium where eastern Spain [21] have detected, through antigen ELISA positive cattle are normally adult cattle and calves are (enzyme-linked immunosorbent assay), a prevalence generally negative at meat inspection (P. Dorny, personal level 3 to 55 times higher than the prevalence obtained communication). through meat inspection. Also, in Germany, Abuseir et Before 1990 the highest rates, based on routine meat al. [22] performed a regional epidemiological study and inspection, were reported for Turkey, Germany and detected an antibody titre level of 8.8 %, which is higher Poland. In Turkey, the prevalence detected at a regional than any prevalence level reported through meat inspec- level ranged from 0.3 to 30 % between 1957 and 1990 tion in Germany. In Turkey, a prevalence of 14 % result- [10]. In Eastern Germany and in the province of Olsztyn ing from an Indirect fluorescent antibody test (IFA) was in Poland prevalences of 3.5–6.8 % and 3.6 %, respect- reported in the area of Iç Anadolu Bölgesi, City of Konya ively, were reported during 1974–1989 [11, 12]. After [10]. Reports based on detailed meat inspection have 1990, the highest prevalence levels were reported in one been reported in Spain, Switzerland and Belgium and abattoir of Germany (i.e. 6.5 %) in 1992 [13] and in the show prevalences around 2 to 50 times higher than the Autonomous Region of Madeira (i.e. 2.0–5.8 %) during prevalence obtained by routine meat inspection [1, 23, 1993–2005 [14]. 24]. In France, in the Brittany region, in 1973 and 1974 The lowest prevalence was identified for Estonia, which the prevalence by meat inspection was less than 1 % and reported no positive cases to EFSA for 2006, 2008, 2009 increased to 9 % when the heart was cut into 2–3 mm- and 2010 [15–17]; followed by Sweden and the UK with a thick slices [25]. Finally, Eichenberger et al. [26] using range of 2*10−4-1*10−3 and 8*10−3-4*10−2%, respectively latent class analysis estimated a prevalence of 16.5 % [9, 18–20]. In the remaining countries, the prevalence was (95 % CI: 12.5–21.2 %) in dairy cows. This result below 2.0 % with few exceptions (i.e. Italy and The contrasts with the much lower prevalence estimates Fig. 4 Prevalence levels (%) based on meat inspection reported per country. Prevalences higher than 5 % are not presented in the figure. These data correspond to a few regional records reported in Turkey between 1963 and 1989 (prevalence range 9.7–30 %), one report from the Autonomous Region of Madeira in 2006 (5.8 %) and two reports from Germany (6.5 % in 1992 and 6.8 % between 1974 and 1989). Legend: BE, Belgium; BG, Bulgaria; CH, Switzerland; CZ, Czech Republic; DE, Germany; DK, Denmark; EE, Estonia; ES, Spain; FR, France; UK, United Kingdom; EL, Greece; HR, Croatia; HU, Hungary; IT, Italy; LU, Luxembourg; NL, The Netherlands; PL, Poland; PT, Portugal; SE, Sweden; SK, Slovakia; RS, Serbia; SI, Slovenia; TR, Turkey Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 6 of 12 resulting from routine meat inspection in Switzerland (Fur- and gender [5, 8, 23, 32] . Increasing age and being female ther details presented in Additional file 3). have been positively correlated with the occurrence of bo- A recent study performed in Belgium revealed a preva- vine cysticercosis. At herd level, an increased risk has also lence of 23 % and 9 % in animals negative to meat in- been associated with the number of slaughtered animals, spection by complete cutting of the predilection sites the herd size and the location of the herd. Boone et al. and by antigen ELISA, respectively. Taking into account [28] observed that the number of slaughtered animals the sensitivity and specificity of these techniques the au- was, among other factors, linked to the occurrence of bo- thors concluded that around 38.4 % of all carcasses of vine cysticercosis in a herd. Allepuz et al. [27], Kyvsgaard adult cattle were probably infected with cysticerci et al. [36] and Boone et al. [28] found that infected herds (Unpublished observations, Jansen et al., 2015). had a larger number of animals than uninfected herds. Contradictory results were found in a case–control study Risk factors conducted by Calvo-Artavia et al. [29] showing that larger In total, we have found 12 studies that analysed risk fac- herds were less at risk than smaller herds in Denmark. Ac- tors [5, 8, 23, 27–35]. These studies were conducted in 7 cording to the authors, this contradictory result could be countries, with most studies being conducted in Denmark due to the fact that in Denmark larger herds are normally (3) followed by Belgium, France and Switzerland (2 each) kept indoors. and Croatia, Italy and Spain (1 each). Some studies have investigated the existence of a Six of these studies have identified risk factors through spatial pattern in the distribution of infected herds. For the quantification of measures of association (odds ratio instance, Allepuz et al. [27] identified two statistically or relative risk) between a given factor and the occur- significant clusters in Catalonia, north-eastern Spain. In rence of cysticercosis. The risk factors at herd level iden- Belgium, one province was four times less likely to have tified in these studies and their level of association with one infected herd than the three other provinces [28]. In the occurrence of bovine cysticercosis are presented in Italy, Cassini et al. [31] identified two significant clusters Fig. 5 (95 % CI represented in most cases). The 95 % CI and Dupuy et al. [33] identified three areas in France should be interpreted with caution as small sample sizes with a higher risk of bovine cysticercosis. The reason for might produce wide CI. Further details on the identified disease cluster presence in these areas was attributed to risk factors are shown in Table 1. factors such as grazing in mountainous areas with access Eight studies identified other than previously presented to risky water sources, movement of infected animals risk factors (Fig. 5; Table 1) and for which no association from one infected herd to several herds in the same area measure was calculated. These risk factors include age or proximity to areas with a high demographic pressure. Fig. 5 Representation of the degree of association (OR and RR) per each risk factor identified. Only factors associated with a higher risk of infection are represented. The red line sets the point along the Y-axis where the degree of association equals 1. Legend: AP, Access to pastures; ARW, Access to risky water sources; CF, Access to potentially contaminated feed; Dairy, Dairy animals; Female, Being female; Organic, Organic farming; SM/C, Sharing machinery or hiring contractors; Defecation, Proximity to uncontrolled human defecation; Visits, Having visitors on farm Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 7 of 12 Table 1 Categories of risk factors for bovine cysticercosis represented in Fig. 5 Abbreviation Risk factor Subcategories included AP Access to pastures Grazing - organic Grazing - conventional (i.e. non-organic) Grazing next to streams with single outlets (without direct access to water) Grazing next to streams with sewage effluent (without direct access to water) ARW Access to risky water sources Free access to surface water (rivers, lakes, canals) Proximity of wastewater effluent (<200 m) Access to risky water with sewage treatment plant effluent in proximitya Access to risky water with no sewage treatment plant effluent in proximitya Drinking from streams with sewage outlets from single households Flooding of pastures CF Access to contaminated feed Feeding of freshly harvested grass on stable to dairy cows Purchased roughage Sewage sludge spread on own land Dairy Dairy animals Dairy as production type Female Being female Being female Organic Organic farming Organic farming SM/C Sharing machinery or hiring contractors Use of machinery (that had been used for emptying septic tanks) for spreading liquid animal manure Sharing machinery or hiring contractors Spreading of liquid manure (with machinery that had been used for emptying septic tanks) partially done by contractors Defecation Proximity to uncontrolled human defecation Car park in the proximity of grazing areas Leisure activities in the proximity of grazing areas Railway line in the proximity of grazing areas Distance to camping site ≤ 100 m Visits Having visitors on farm Having visitors on farm a Risky water sources could be streams, lakes or ponds In addition to the above mentioned studies, other pub- a larger distance) and also being closer than 100 m to a lications merely hypothesised potential risk factors for railway track. This last finding is in contrast to the find- bovine cysticercosis without performing any specific ings of a study conducted in Switzerland where the pres- study [2, 37, 38]. These factors were related to: (i) access ence of a railway track along or through farm land was of cattle to contaminated water and/or pastures; (ii) found to increase the risk of infection [34]. fertilization with potentially contaminated materials; (iii) human defecation in the proximity of grazing areas; (iv) Source of infection lack of fly and bird control; (v) persistence of eggs in Some studies have performed outbreak investigations to as- waste water after treatment; (vi) presence of tapeworm sess potential sources of infection. In Scotland, five out- carriers in the farm; and (vii) high intensification of agri- breaks (1976–1979) were traced back to the application of culture (involving high concentration of cattle and in- sludge on grazing fields [39]. However, another survey creased irrigation). (1980–1983) investigated affected farms and showed that Factors linked to a lower probability of cattle becoming only in 4.3 % of them sludge had been used, indicating the infected have also been identified in the literature. Inter- existence of other routes of infection [20]. A study con- estingly, Kyvsgaard et al. [35] observed in a case–control ducted in Denmark [40] found illegal application of sludge study in Denmark a lower risk of infection if sewage from septic tanks on pasture or crops (in some cases after sludge was spread on neighbouring land than if no spread- having been mixed with animal slurry) as the most frequent ing occurred or if the spreading was done on own land. source of infection. In Spain, by using epidemiological They also identified lower risk if the distance to a sewage questionnaires and a risk scoring system proposed by EFSA treatment plant was ≤ 100 m (in comparison with being at (2004) [24] Allepuz et al. [27] identified that water supply Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 8 of 12 was the most likely source of infection in 23 out of the 55 highlighted in different studies. Serological tests (based investigated farms. In Norway, bovine cysticercosis out- on antibody or antigen detection) provide a better sensi- breaks have been traced to foreign tourists and seasonal tivity. The main downside of antibody detection tests is farm workers, and to farm equipment used to handle sew- that they do not distinguish between animals harbouring age sludge carrying infected matter [41]. cysticerci and animals that have been exposed to eggs without establishment of cysticerci (P. Dorny, personal Burden communication). Moreover, low levels of antibodies, According to the literature review, bovine cysticercosis antigenic cross-reactivity between parasites and shortage may inflict substantial economic costs to the cattle in- of parasite material as a source of antigen [52] may also dustry [28, 42, 43] but its impact to public health seems occur. Antigen detection tests, detect animals harbour- to be less relevant. The clinical importance of T. sagi- ing infective (live) metacestodes [53] but they do not nata in humans is limited because symptoms are gener- succeed in detecting all light infections, which are the ally mild and it is easily treated [44]. However, severe most common type of infection in Europe [5]. Serology symptoms can occasionally occur and people carrying a is more time consuming than meat inspection but it tapeworm can suffer from psychological stress. The main could be a useful screening test at herd level [47]. AbE- economic losses in the cattle sector are due to extra hand- LISA kits to detect bovine cysticercosis antibodies are ling, condemnation, freezing treatment, weight loss after currently being commercialised but AgELISA kits are freezing (2–5 %) and loss of value of frozen meat of af- only available for the diagnosis of cysticercosis in fected bovines which are reported to be around 30 to humans and pigs and not for cattle. Sensitivity can also 45 % of the value of the carcasses [1]. There is a scarcity be increased, according to previous studies, through in- of studies quantifying economic burden due to cysticerco- creasing the number of incisions in the carcass or in the sis in cattle. In England the costs due to bovine cysticerco- heart (enhanced meat inspection) [1, 23]. The first would sis, including condemnation, downgrading, refrigeration, lead to carcass mutilation [21] and to a higher risk of handling, and transport have been estimated at around microbiological contamination [21]. The latter, however, £100 per carcass or £4.0 million annually [45]. would be feasible in the daily practice and useful in low cyst burden areas [23]. A recent study conducted in Interventions Belgium showed, however, that performing additional inci- In addition to general control measures described in sions to the heart did not increase the sensitivity of the Reg. (EC) No 854/2004 [4], the systematic review re- technique sufficiently to be considered profitable (Jansen vealed other measures that can be applied. Other mea- et al., 2015, unpublished observations). sures in place include sewage treatment and the Post-mortem laboratory confirmation of T. saginata is establishment of rules for the agricultural use of sewage based on macroscopic, microscopic, histological and mo- and sludge [39] and monitoring of bovine cysticercosis lecular assessment of putative lesions. If the lesion is a [46]. At farm level, the suggested interventions are to: degenerated cyst or a macroscopically similar lesion search for tapeworm carriers among the farm staff [2]; caused by other parasites (e.g. Sarcocystis spp.) incorrect conduct epidemiological studies to find the source of in- diagnosis may occur. Different improved post-mortem fection in affected farms [8, 31]; and monitor the effect- diagnostic techniques developed for this purpose identi- iveness of control measures and provide education and fied during the review include antigen ELISA in meat information to farmers. The application of pharmaco- juice [54], immunohistochemical methods [6, 55] and logical treatment to infected herds has also been described biomolecular assays [54, 56]. as a potential control measure as cattle can be efficiently The interventions to be applied on infected carcasses treated against cysticercosis [47]. However, authors ques- focus on the destruction of cysts. They include temperature tion the feasibility of applying it as the economic cost is treatment (freezing or cooking of meat) and irradiation. Ac- high and the degenerated cysticerci can still be present in cording to an EFSA Scientific Opinion it has been con- the carcasses up to two years later. Vaccination has also cluded that freezing of cattle carcasses at −10 °C for been proven as an effective tool to protect cattle [48] but 10 days kills the cysticerci [57]. It is also generally accepted vaccines are not commercially available [49] and the cost- that cooking meat properly all the way through kills the benefit is also questioned [50, 51]. Biological control using cysts [57]. Regarding irradiation, the results of a study con- antagonistic fungi to eliminate T. saginata eggs from the ducted by Geerts et al. [58] indicated that cysticerci of environment has been suggested to have potential as a T.saginata lose their infectivity after being irradiated with control tool in the future [51]. gamma rays at doses of 0.3, 0.4 and 0.6 kGy. Due to the very low sensitivity of the current meat in- On the other hand, since classical meat inspection is spection procedure the need of applying more sensitive time-consuming, costly and with low detection sensitivity, techniques to detect infected cattle has been also several authors have assessed and suggested the application Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 9 of 12 of a risk-based surveillance in order to improve meat in- degeneration of the cysts [44], the level of compliance spection sensitivity [25, 30]. This system would consist in with the officially established meat inspection proto- implementing a higher priority of surveillance resources in cols [4] and also the characteristics of the facilities those animals or areas that present higher risk of infection. where the meat inspection is carried out (i.e. speed of In this sense, it has been proposed to use more sensitive slaughter line, lighting, etc.). diagnostic procedures such as the reinforcement of meat Meat inspection sensitivity has been estimated to be be- inspection (e.g. by using antigen detection serology or in- tween 10 and 30 % [2, 5, 23]; therefore, the data collected creasing the number of incisions in the heart) in high risk underestimate the real prevalence. In order to know the areas or animals previously identified as such [33]. For ex- current epidemiological context of bovine cysticercosis ample, in Denmark, Calvo-Artavia et al. [29] proposed in- the use of more sensitive surveillance strategies is needed cluding data for the identification of low or high-risk and data collection and reporting throughout the years for animals in the Food Chain Information document, e.g. gen- all of the countries is essential. Monitoring and reporting der, age and grazing practices in the case of Denmark, to occurrence of Cysticercus bovis in the European Union is enable meat inspectors to apply a risk-based inspection. In recommended by Directive 2003/99EC (on the monitor- addition to the use of risk-based surveillance, Dupuy et al. ing of zoonoses and zoonotic agents) [46], but it is not [33] also suggested the application of specific control mea- compulsory and only very few countries annually report sures in high-risk areas depending on the risk factors iden- their data to the European Commission and European tified (e.g. increasing the control of sewage sludge in areas Food Safety Authority. identified as high-risk areas). Following this approach a Only few studies identifying risk factors have been car- Codex Alimentarius document providing guidance on the ried out and mostly in western European countries. application of risk-based measures for the control of T. Since the type of cattle production, farming management saginata in cattle has been recently developed [59]. and other factors may vary between different parts of Europe, conducting risk factors analysis in Eastern Euro- Discussion pean countries should be encouraged. Also studies based The high variability in the prevalence levels among and on more sensitive techniques would be needed in order to within countries identified through this review could be avoid possible biases due to misclassification of cases [28]. attributed to different factors. Firstly, real differences The fact that bovine cysticercosis is present in Europe might exist due to heterogeneity in the exposure to risk indicates that the transmission between cattle and factors among and within countries (e.g. differences in humans is taking place and serves also as an indicator of gender, age, herd size, breeding systems, etc.). Secondly, poor hygiene [37, 60]. Human taeniosis is not a notifiable the reported data were collected at different levels (for a disease and reported prevalences are only indicative [39]. whole country, a region, or in one or few abattoirs). For Estimates have indicated that in Europe 11 million people some countries most of the records were recorded at re- suffer from taeniosis caused by T. saginata [61]. Without gional level (e.g. Spain or Croatia) whereas in others the accurate data on the number of human cases, although the prevalence was described mainly at national level (e.g. global burden is considered to be low [42, 62], the relevance Belgium or Sweden). In the cases when the level of data of bovine cysticercosis as a public health problem is difficult collection was not specified, the approach taken was to assess [21] and has not yet been quantified [42]. Few au- assuming that data belonged to the whole country but this thors have reported estimates of the number of affected assumption could lead to inaccurate information/interpret- humans potentially infected from undetected carcasses dur- ation. Thirdly, there were differences in timeframes of data ing routine meat inspection with variable results. In the UK collection. This varied extensively between countries and it was estimated that one human case could originate from within a country. Some sources provided a mean preva- between 30–100 undetected bovine cases [9]. In France, lence for a long period (e.g. years). In other cases an annual however, it was estimated that one undetected carcass follow-up was given and therefore consecutive annual could potentially infect between eight and 20 humans [25]. prevalence data were available (e.g. Belgium). Fourthly, data Human taeniosis generally causes mild symptoms (abdom- were extracted from routine official meat inspection reports inal discomfort, mild diarrhoea, weight loss and anal prur- and from scientific studies. The accuracy of the data de- itus) and psychological distress. Only occasionally severe rived from a particular scientific study might be higher than symptoms such as appendicitis occur but no fatalities have the data obtained through official routine meat inspection been reported. Therefore it is considered that interventions procedures. Finally, factors influencing the level of detec- such as meat inspection avert very few Disability-Adjusted tion by routine meat inspection included the training, ex- Life Years (DALYs) [42]. The only direct cost of human tae- pertise, motivation of the meat inspector [2], the level of niosis is the payment of medical visits, treatment and la- infection (number of cysts), the location of cysts in other boratory tests, which are reported to be very low and muscles than those routinely inspected, the stage of reasonable in terms of cost-benefit ratio [42]. Laranjo-González et al. Parasites & Vectors (2016) 9:81 Page 10 of 12 There are almost no studies estimating the economic Additional files impact of bovine cysticercosis on the meat and cattle in- dustry and in some cases the data are outdated. Earlier Additional file 1: PRISMA 2009 Checklist. (DOC 65 kb) research estimated economic losses due to bovine cysti- Additional file 2: List of references for the records included in the review. (XLSX 20 kb) cercosis in industrialised countries at 234 US$ for a Additional file 3: Prevalence data extracted from the included whole carcass (updated to 1990 US$ prices) [63] but no records. (DOCX 98 kb) specific estimates for Europe were provided in that study. In Europe we identified only one estimate on eco- Abbreviations nomic impact in England. Therefore, in order to assess CI: Confidence interval; CYSTINET: European Network on Taeniosis/ the relevance of this animal parasitosis, studies on its Cysticercosis; EFSA: European food safety authority; ELISA: Enzyme-linked immunosorbent assay; DALYs: Disability-adjusted life years; OR: Odds ratio; economic impact in Europe are needed. RR: Relative risk. Despite these current control measures, bovine cysticer- cosis is still present in Europe, which proves that the inter- Competing interests ventions in place are not sufficient for the successful The authors declare that they have no competing interests. control of this zoonosis [37]. The current recommenda- Authors’ contributions tions are to continue performing visual meat inspection MLG conducted the systematic review of the literature, extracted and until validated serological tests are commercially available analysed data and drafted the first version of the manuscript. AA and for routine practice [37]. In order to better control this BD contributed to the screening of papers, the design of the study, interpretation of data and collaborated in the writing of the first draft. parasitosis and also to evaluate the control/prevention PD and SG contributed to the writing of the paper. All authors read and tools accurate prevalence data on animals and humans are approved the final version of the manuscript. necessary. Acknowledgements Several authors have suggested the application of risk- This work is a collaboration within the framework of CYSTINET, the European based surveillance and control systems to improve the de- network on taeniasis/cysticercosis, COST ACTION TD1302. tection sensitivity and to avoid measures that are not pro- Author details portionate to the level of risk reduction achieved [59]. In 1 Centre de Recerca en Sanitat Animal (CReSA)-Institut de Recerca i order to apply such approaches, classification of areas, Tecnologia Agroalimentàries (IRTA), Campus UAB, Bellaterra, Barcelona 08193, herds and animals at low risk, together with the epidemio- Spain. 2Department of Animal Sciences and Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA. 3Department of Virology, logical data supporting this risk classification are needed. Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent Sources of these data could be records from post-mortem University, Merelbeke, Belgium. 4Department of Biomedical Sciences, Institute inspection at the slaughterhouses and results from labora- of Tropical Medicine, Antwerp, Belgium. 5Departament de Sanitat i Anatomia Animals, Universitat Autònoma de Barcelona, Bellaterra, Barcelona 08193, tory tests, results from farm investigations, records from Spain. human health surveillance and data on human treatments. At present sufficient information to implement such sys- Received: 28 October 2015 Accepted: 5 February 2016 tems are hardly available in Europe, especially in the east- ern countries. The quality of data and data reporting of T. References saginata cysticercosis cases in Europe should be 1. Geerts S. Taenia saginata: an eternal problem? Verh K Acad Geneeskd Belg. improved. Studies identifying risk factors should be con- 1990;52:537–63. discussion 563–534. 2. 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Southeast Asian J Trop Med Public Health. 1991;22(Suppl):377–81. Submit your next manuscript to BioMed Central and we will help you at every step: • We accept pre-submission inquiries • Our selector tool helps you to find the most relevant journal • We provide round the clock customer support • Convenient online submission • Thorough peer review • Inclusion in PubMed and all major indexing services • Maximum visibility for your research Submit your manuscript at www.biomedcentral.com/submit