RESEARCH

Analysis of the economic impact of cystic echinococcosis in Spain

Analyse de l'impact économique de l'échinococcose kystique en Espagne

Análisis del impacto económico de la hidatidosis en España

Christine Benner^I; Hélène Carabin^I; Luisa P Sánchez-Serrano^II; Christine M Budke^III; David Carmena^IV,*

^ICollege of Public Health, Oklahoma University Health Sciences Center, Oklahoma City, OK, United States of America (USA)
^IINational Centre of Epidemiology, Instituto de Salud Carlos III, Madrid, Spain
^IIICollege of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, USA
^IVDepartment of Immunology, Microbiology and Parasitology, University of the Basque Country, PO Box 450, 01080 Vitoria-Gasteiz, Spain

ABSTRACT

OBJECTIVE: To estimate the overall economic losses due to human and animal cystic echinococcosis (CE) in Spain in 2005.
METHODS: We obtained data on annual CE incidence from surveillance and abattoir records, and on CE-related treatment and productivity losses (human and animal) from the scientific literature. Direct costs were those associated with diagnosis, surgical or chemotherapeutic treatment, medical care and hospitalization in humans, and condemnation of offal in livestock (sheep, goats, cattle and pigs). Indirect costs comprised human productivity losses and the reduction in growth, fecundity and milk production in livestock. The Latin hypercube method was used to represent the uncertainty surrounding the input parameters.
FINDINGS: The overall economic loss attributable to CE in humans and animals in 2005 was estimated at 148 964 534 euros (€) (95% credible interval, CI: 21 980 446–394 012 706). Human-associated losses were estimated at €133 416 601 (95% CI: 6 658 738–379 273 434) and animal-associated losses at €15 532 242 (95% CI: 13 447 378–17 789 491).
CONCLUSION: CE is a neglected zoonosis that remains a human and animal health concern for Spain. More accurate data on CE prevalence in humans (particularly undiagnosed or asymptomatic cases) and better methods to estimate productivity losses in animals are needed. CE continues to affect certain areas of Spain, despite several control initiatives since 1986. Given the high economic burden of CE, additional funding is needed to reduce human and animal infection rates through improved disease surveillance, regular treatment of dogs and greater cooperation between agencies.

RÉSUMÉ

OBJECTIF: Estimer les pertes économiques total dues à l'échinococcose kystique (EK) humaine et animale en Espagne en 2005.
MÉTHODES: Nous avons obtenu des données sur l'incidence annuelle de l'EK à partir de la surveillance et des dossiers d'abattoir, et sur le traitement et les pertes de productivité (humaines et animales) liés à cette maladie à partir de la littérature scientifique. Les coûts directs étaient ceux afférant au diagnostic, au traitement chirurgical ou non chirurgical, aux soins médicaux et à l'hospitalisation pour les humains et ceux afférant à la condamnation des abats pour le bétail (ovins, caprins, bovins et porcins). Les coûts indirects couvraient les pertes de productivité humaine et la diminution de la croissance, de la fécondité et de la production laitière chez le bétail. La méthode de l'hypercube latin a été appliquée pour représenter l'incertitude entourant les paramètres d'entrée.
RÉSULTATS: La perte économique total attribuable à l'EK humaine et animale en 2005 a été estimée à 148 964 534 euros (€) (intervalle de crédibilité à 95 %, IC : 21 980 446 - 394 012 706). Les pertes se rapportant aux humains ont été estimées à € 133 416 601 (IC à 95 % : 6 658 738 - 379 273 434) et celles associées aux animaux à € 15 532 242 (IC à 95 % : 13 447 378 - 17 789 491).
CONCLUSION:L'EK est une zoonose négligée, qui demeure préoccupante pour la santé humaine et animale en Espagne. Il faudrait disposer de données plus précises sur la prévalence de cette maladie chez l'homme (notamment sur les cas non diagnostiqués et les cas asymptomatiques) et de meilleures méthodes pour estimer les pertes de productivité concernant les animaux. L'EK continue de toucher certaines zones de l'Espagne, malgré plusieurs initiatives de lutte contre cette maladie depuis 1986. Compte tenu du lourd fardeau économique que représente l'EK, il faudrait aussi investir davantage dans la réduction des taux d'infection humains et animaux à travers une meilleure surveillance de la maladie, un traitement régulier des chiens et un renforcement de la coopération entre les agences ministérielles.

RESUMEN

OBJETIVO: Estimar las pérdidas económicas totales ocasionadas por la hidatidosis humana y animal en España en 2005.
MÉTODOS: Los datos sobre la incidencia anual de la hidatidosis se obtuvieron a partir de los registros de vigilancia epidemiológica y de los mataderos. Los datos sobre el tratamiento y la pérdida de productividad (humana y animal) relacionada con la enfermedad se obtuvieron a partir de la literatura científica. Los costes directos fueron los asociados al diagnóstico, el tratamiento quirúrgico o farmacológico, la atención médica y la hospitalización en humanos, y los decomisos de vísceras infectadas en animales de abasto (ganado ovino, caprino, bovino y porcino). Los costes indirectos comprendieron la pérdida de productividad en humanos y la reducción de las tasas de crecimiento, fecundidad y producción de leche en el ganado. Para representar la incertidumbre asociada a los parámetros analizados se utilizó el método del hipercubo latino.
RESULTADOS: Las pérdidas económicas totales atribuibles a la hidatidosis humana y animal fueron estimadas en 148 964 534 euros (€) (intervalo de credibilidad del 95%, IC95%: 21 980 446–394 012 706). Las pérdidas estimadas de origen humano fueron de € 133 416 601 (IC95%: 6 658 738–379 273 434), y de € 15 532 242 (IC95%: 13 447 378–17 789 491) las de origen animal.
CONCLUSIÓN: La hidatidosis es una zoonosis desatendida que en España sigue constituyendo un problema de salud humana y animal. Son necesarios datos más exactos sobre la prevalencia de la hidatidosis en humanos (sobre todo en los casos no diagnosticados o asintomáticos) y mejores métodos para calcular la pérdida de productividad en animales. La hidatidosis sigue afectando a ciertas zonas de España pese a las varias campañas de control emprendidas desde 1986. Dada la gran carga económica de la hidatidosis, es necesaria una mayor financiación para reducir las tasas de infección humana y animal mediante mejoras en la vigilancia de la enfermedad, el tratamiento periódico de los perros y la cooperación entre organismos oficiales.

Introduction

Cystic echinococcosis (CE or hydatid disease) is a zoonotic infection caused by the larval stage of the taeniid tapeworm Echinococcus granulosus. The parasite's life cycle is maintained through dogs (which harbour the adult worm in their small intestine) and a range of domestic livestock that serve as intermediate hosts. E. granulosus eggs are excreted in the faeces of infected dogs and may thus contaminate soil, grass and water. Ungulates (hoofed animals) can become infected by grazing on pasture contaminated with dog faeces. Ingested eggs hatch inside the intestine, penetrate the gut wall and are carried by the bloodstream to different organs and tissues (mainly the liver and lungs) where they develop into cysts (metacestodes) that can eventually cause severe pathological damage. Humans can become infected by ingesting eggs through consuming contaminated food or water or from handling the faeces of infected dogs.

As in other countries of the Mediterranean basin, CE is endemic in Spain.^1,2 Most affected regions are the central, north-eastern and western regions of the country, where extensive or semi-extensive farming of livestock (mostly sheep) is common. Since the mid-1980s, a number of prevention and control programmes to reduce E. granulosus infection have been implemented in these regions. These programmes have led to a considerable decrease in human and animal CE infection rates.^3–5 However, the disease remains a serious health concern in many of the affected regions. A recent survey showed human CE annual incidence rates in the range of 1.1 to 3.4 cases per 10⁵ person-years, in combination with ovine or bovine CE prevalence proportions of up to 23%.⁶

Spain is a developed country with a population of more than 43 million (77% of whom live in urban areas) and a high average income; in 2005, the gross domestic product per head was €18 677.⁷ The national public health system provides health services for an estimated 90% of the population; the remaining 10% (mainly from the autonomous regions of Madrid and Catalonia) have both public and private coverage.⁸ The national epidemiological surveillance network is based on three interdependent systems – compulsory notifiable diseases, outbreaks alerts and microbiological information. The autonomous regions where CE infection is considered endemic (Aragon, Cantabria, Castile-La Mancha, Castile-León, Catalonia, Ceuta and Melilla, Comunidad Valenciana, Extremadura, La Rioja and Navarre) report human CE to the compulsory notifiable diseases system.⁹ The proportion of symptomatic CE cases that are detected and reported to the system has been estimated at 47–57%.¹⁰ However, the completeness of case detection increases to more than 95% when the microbiological information system and computerized hospital discharge records are also considered, and the specificity is 100% (LP Sánchez-Serrano, unpublished data, 2009). Surveillance of CE in livestock is carried out through routine postmortem examination in all national slaughterhouses, with detected cases reported to the Spanish Food Safety Agency.¹¹ Official figures on human and animal CE are subsequently submitted to the European Commission as part of the Spanish Report on Trends and Sources of Zoonoses.¹²

CE affects both human and animal health and has important economic consequences.¹³ Human-associated economic losses arise through diagnostic procedures, surgical or chemotherapeutic treatment, hospitalization, convalescence, life impairment and fatalities. Animal-associated economic losses arise from decreases in carcass weight, milk production and fertility rates, and from increased condemnation of viscera. Estimation of the economic burden in humans and livestock is important and should be part of any cost–benefit programme for the control of parasitic zoonoses.^14,15 Early surveys attempting to quantify human and animal CE losses were hampered by the scarcity of reliable epidemiological and economic data.^16–18 Mathematical approaches based on decision-tree analysis and efficient sampling techniques were therefore proposed, to model the inherent uncertainty.¹⁹ Such approaches have been used successfully in various studies.^16,20,21 In Spain, the evaluation of the economic effects of CE has previously been attempted only in the autonomous regions of Extremadura⁴ and La Rioja,⁵ as part of the control programmes implemented in these regions. However, cost estimates at a national scale are lacking. The aim of this study was to estimate the overall economic losses due to human and animal CE in Spain in 2005.

Methods

Human epidemiological parameters

The human epidemiological parameters used in the analysis included diagnosed cases (in males and in females); undiagnosed or asymptomatic cases; and diagnosed cases with surgery. The number of reported CE cases by age and gender was obtained from the epidemiology surveillance network²² and was used to estimate the productivity losses in humans (see below). We assumed that the proportion of reported cases and the frequency of different types of treatment were uniform across age and gender. We also assumed that the proportion of CE cases with surgery followed a triangular distribution – with parameters of 68%, 95% and 100% – as specified in five Spanish studies of hospitalized CE cases.^23–27 Data on the type of surgical intervention undertaken among surgical cases were obtained from the same sources. The burden associated with recurrence was captured in the "per intervention cost"of each surgical case.²⁸

Surveys on the proportion of undiagnosed or asymptomatic cases in the Spanish population using mass ultrasound have not been conducted. Therefore, we assumed that the prevalence of undiagnosed or asymptomatic cases was proportional to that estimated in a study conducted in the Florida district of Uruguay. In that study, the prevalence of undiagnosed disease was estimated to be 1.64% by ultrasound, and the annual surgical incidence was 36.1 cases per 10⁵ person-years, for a ratio of 45.4.²⁹ By applying this ratio to the incidence rate of surgical cases in Spain (0.34 cases per 10⁵ person-years), we estimated the mean prevalence of undiagnosed or asymptomatic CE to be 0.0154%. However, because of the large uncertainty in this estimate, we used a triangular distribution with a mode of 0.0154% and a range of 0–0.02%.

Diagnosed reported cases, as well as undiagnosed or asymptomatic cases, were assumed to have a reduction in productivity of 2.0% (range: 0.0–4.0%), based on the only reported assumption in the literature.¹⁷ Lost-opportunity costs correspond to the productive time lost due to an infected person working less efficiently than someone who is uninfected. We assumed that the same level of lost opportunity applied to people who were asymptomatic, undiagnosed or diagnosed.

Estimation of human costs

Costs incurred because of CE in humans were divided into direct and indirect costs. Direct costs of standard care procedures, clinical tests and surgical interventions in Spain were obtained from the tariffs for health-care services in public hospitals of the autonomous regions of Aragon and Castile-León,^28,30 which are some of the most affected regions in Spain.⁶ The data obtained for the reported surgical costs comprised a composite average for all cyst resection procedures, rather than those specifically associated with CE. Direct cost estimates included separate calculations for surgical and nonsurgical patients. In both cases, a cost-per-patient estimate was calculated using the itemized prices for typical care, and the expected percentage of use for specific services, procedures and treatments.

Average wages according to sex and age were obtained from the 2005 Wage Distribution Survey of the National Statistics Institute.⁷ These data were used to calculate the direct and indirect costs associated with length of hospital stay.

Animal epidemiological parameters

The species considered in the analysis were sheep, goats, cattle and pigs. The prevalence of CE in livestock was based on the reported number of infected animals identified through inspection at abattoir.³¹ In Spain, data on the prevalence of CE in sheep and goats are reported in combination. We therefore used identical values for both species. To estimate the total number of infected animals, we extrapolated these values to the overall animal populations. Estimates of livestock life expectancy and reproductive rates were kindly provided by Professors Juan de Dios Vargas and Enrique Pérez (Faculty of Veterinary Medicine, University of Extremadura, Spain). Official figures for annual livestock meat and milk production were obtained from the country's Ministry of Agriculture, Fisheries and Food.³² Data stratified by age (young and adults) were included where available. Various livestock productivity losses associated with CE – including reduction in carcass weight, reduction in milk production and decrease in fecundity – were estimated from the scientific literature.^4,33–35

Estimation of animal costs

Direct costs (mainly the loss of revenue through offal condemnation) and indirect costs (reductions in the growth, fecundity and milk production of infected animals) were included in the estimate of the total costs associated with CE in livestock, calculated as described below.

Offal condemnation

In Spain, identification of hydatid cysts at meat inspection leads to condemnation of infected offal. We therefore assumed that the number of condemned livers and lungs equalled the total number of infected animals reported. Since only the costs of sheep offal were available, we assumed the costs of goat offal to be the same.

To estimate the total cost of condemned offal in all species for 2005, we calculated the lost revenue for each CE-infected animal, according to the average weight^36–43 and market value⁴⁴ of both liver and lung, by species and age at slaughter. Direct costs were estimated from the product of the cost per animal and the number of infected animals in each age–species stratum identified at slaughter, for all species and age groups.

Growth reduction

To calculate growth reduction, we assumed a reduced carcass weight of CE-infected animals at slaughter. We first estimated the difference in income from the sale of a healthy carcass and a CE-infected carcass (which will weigh less) for each species. We then calculated the loss in net profit to the farmer per infected animal as the difference between the estimated income and the annual farmer investment for each species.⁴⁵ It was assumed that farmers would invest equally in CE-infected or uninfected animals. For all species, the annual cost for CE-associated growth reduction was calculated from the product of the loss in net profit per infected animal and the number of infected animals identified at slaughter for each species.

Milk production

To estimate total milk not produced because of infection, we used estimates of total annual milk production and current CE prevalence in dairy species. From these data we calculated the potential percentage considered losses from unborn diary animals, as explained below.

Decreased fecundity

Animals not born because of CE infection represent losses of potential earnings from live-animal and carcass sales, and from the sale of milk in dairy species. To estimate the cost of reduced fecundity, we assumed that the prevalence of CE at slaughter would be the same in breeding and nonbreeding animals. We calculated the population birth rate given the current prevalence in each species by dividing the mean annual fecundity by the number of female animals of reproductive age.³² To simulate the birth rate in the absence of infection, we estimated the number of animals born to infected individuals and ascribed a 5.5% increase in birth rate for this proportion. We estimated the total number of "unborn"animals by calculating the difference between the potential and actual births for the infected reproductive proportion in each species.

To avoid overestimating the potential opportunity costs, we assumed an equivalent prevalence of infection in unborn animals. To estimate the potential loss at abattoir, we used the 2005 market value for meat in euros (€) and the average carcass weight, considering that a percentage of unborn individuals would also be infected and would thus have reduced carcass weights. For milk-producing species we used the respective infection rates of dairy and meat animals to estimate the proportion of dairy and meat animals unborn because of infection. For unborn dairy animals, losses related to milk production were calculated based on average annual yield and the market value of milk for each species. Because most dairy animals are eventually slaughtered for meat, losses at abattoir were also calculated with respect to the different average carcass weights for dairy animals, where applicable.

Uncertainty and sensitivity

To account for the uncertainty for parameters not available in the literature, we assigned distributions based on a likely range of values to each parameter. We generated 10 000 iterations of the final model using Latin hypercube random sampling of input parameter values based on the assigned distributions. The 50th percentile of the distribution of the 10 000 iterations represents the median, and the 2.5th and 97.5th percentiles represent the 95% credible intervals (CIs) for the total cost of CE. A stepwise linear regression of the estimated costs against the input parameter values was performed to assess the impact of each input parameter on the overall cost estimate. A separate sensitivity analysis was undertaken, excluding parameters associated with asymptomatic cases, because of the uncertain nature of the implicated parameters. The estimates from models with and without asymptomatic cases and the resulting figures illustrating the impact of input parameters were generated using @Risk^© Version 5 software (Palisades Corporation, Ithaca, New York, NY, USA), running as an add-in to Microsoft Excel^©.

Results

Table 1 and Table 2 show the epidemiological and economic parameters, respectively, used to estimate the economic losses associated with CE in humans. Table 3 (available at: http://www.who.int/bulletin/volumes/88/01/09-066795/en/index.html) and Table 4 show the epidemiological and economic parameters, respectively, used to estimate the economic losses associated with CE in livestock.

The median economic losses associated with CE in humans and animals in Spain in 2005 were estimated at €148 964 534 (Table 5). The table shows that human productivity losses constituted most (89.1%) of this total cost estimate, mainly through the potential impact of wage losses in undiagnosed or asymptomatic populations. Losses associated with CE in livestock contributed 10.4% of the total cost, mainly through indirect losses; direct losses in livestock constituted only 0.12% of the total cost. The estimated normalized regression coefficients were below 0.01, except for those for the percentage reduction in productivity in cases (0.81) and for the percentage of undiagnosed or asymptomatic cases (0.51), which suggests that these two parameters strongly influenced the overall estimate.

The sensitivity analysis excluding all undiagnosed or asymptomatic cases and their associated productivity losses resulted in a reduction of the median economic cost in 2005 to €16 442 870 (Table 5). The table shows that indirect costs associated with animal CE constituted most (93.5%) of the total cost (mainly due to reduced fecundity and reduced carcass weight in cattle). Losses associated with CE infection in humans were much smaller; they constituted only 5.3% of the total cost (mainly due to work absences associated with illness). The normalized regression coefficient values in Fig. 1 illustrate the impact of uncertain parameters on the overall costs after removing asymptomatic human cases from the model; under these conditions, several animal parameters become more important in determining the overall costs.

Discussion

This is the first study to produce a comprehensive estimate of the annual economic burden of CE in humans and animals in Spain. Studies that estimate the burden of disease at a regional level provide data that enable decision makers to prioritize allocation of limited resources. The preferred way to capture both the human and agricultural effect of a zoonosis is to estimate its economic impact.¹⁹ This has been undertaken for CE in a number of European countries, including Wales,¹⁸ and in Jordan¹⁶ and Tunisia.²¹ However, direct comparison of data is difficult due to lack of standard methods for estimating the costs of the infection and to differences among countries in human and animal population sizes, disease prevalence, inherent socioeconomic patterns and period of valuation.

The Latin hypercube method used in this study to represent the uncertainty surrounding the input parameters is particularly suitable for estimating indirect costs where accurate human and animal epidemiological data are scarce. To make the estimates more robust, we stratified rates of human CE infection and average wages by age and gender. For livestock, we used age-stratified prevalence proportions, where available.

Our results indicate that CE continues to affect human health and livelihood in Spain, especially when the indirect costs of reduced productivity and annual wages lost due to disease are taken into account. The human consequences of CE in Spain in 2005 were estimated to incur a median of €133 million when productivity losses in undiagnosed or asymptomatic cases were considered, but only €0.9 million when these losses were excluded. This large difference emphasizes the need for more accurate baseline estimates of real CE prevalence in humans (to minimize the potential impact of the uncertainty of this parameter); better methods for estimating productivity losses associated with undiagnosed or asymptomatic cases; and improved capacity for distinguishing asymptomatic cases from misdiagnosed or untreated cases (because respective productivity losses may vary considerably between groups).

Regarding the need for more accurate baseline estimates, mass screening studies of infection with E. granulosus, based on the detection of circulating antibodies to the parasite, have been undertaken in different Spanish regions to determine the infection's prevalence.^47,48 However, this approach assesses lifelong exposure to the parasite rather than the prevalence of active infection. An alternative is ultrasonography, which is a reliable and accurate diagnostic tool for reporting infection status in human asymptomatic populations.⁴⁹ Because this technique has not been used for field epidemiological surveys in Spain, we had to estimate the prevalence of undiagnosed or asymptomatic cases by extrapolating from other data.²⁹ Undiagnosed or asymptomatic cases incur productivity losses and costs due to the partial disability caused by the chronic effect of the infection.⁵⁰ A theoretical estimate of a 2% reduction in work productivity in asymptomatic cases (for estimating work productivity losses) has been proposed.¹⁷ More research on the socioeconomic effects of ill health caused by CE is needed to better quantify these parameters and generate more accurate estimates.

Another limitation of this study is that we used national-level average wages to estimate the loss-of-opportunity costs. Using wages as the sole indicator for human productivity does not capture the value of labour in localized, informal or nonregulated employment sectors (e.g. family care-giving); hence, societal burden may have been underestimated. Also, this approach does not capture any psychological burden that may be associated with the infection.

In livestock, indirect losses account for almost 99% of the total cost associated with CE, whereas the direct losses were negligible. As with humans, the scarcity of specific data on productivity losses makes accurate estimates of the economic losses of CE in livestock difficult to perform.

Another limitation of the estimated costs of surgical treatment for CE in humans is that these were based on the average cost of surgical interventions for all types of cysts (because data were not available on therapies specific to E. granulosus infections). Thus, the estimates may over or underestimate the true costs associated with the removal of cystic echinococcosis cysts. However, we do not believe that this would result in an important difference in the overall costs.

In our analysis, the prevalence of CE was assumed to be identical in sheep and goats because reported official figures do not distinguish between these species, and no relevant studies were found in the literature. Removing goats from the model had little effect on the results, since goats contributed less than €5000 of the total cost. However, in countries where goats represent a more important ruminant population, CE prevalence in sheep and goats should be considered independently.

The epidemiological parameters we used to calculate indirect animal costs were estimated averages and did not capture variations that would be expected to occur due to factors such as animal breed, type of exploitation and management, diet, neonatal and perinatal mortality rates, and comorbidity status.

Conclusion

Our findings indicate that CE imposes a significant economic burden on Spain. They also emphasize the importance of maintaining or reinforcing current control measures to consolidate the progress achieved and to reduce human and animal infection rates. Further work is required to evaluate the cost–effectiveness and cost–benefit of any control programmes implemented, and to guide decision makers and stakeholders on the best approach to take with the resources available. Better coverage and accuracy of the current surveillance systems are needed, as are improvements in the cooperation between the central and regional administrations, and the institutions responsible for collecting, providing and publishing data of epidemiological relevance. In regions of Spain where CE is epidemic, mass screening studies using ultrasonography would improve estimates of the actual prevalence of undiagnosed or asymptomatic cases.

Competing interests: None declared.

References

1. Romig T, Dinkel A, Mackenstedt U. The present situation of echinococcosis in Europe. Parasitol Int 2006;55 Suppl;S187-91. doi:10.1016/j.parint.2005.11.028 PMID:16352465        

2. Seimenis A. Overview of the epidemiological situation on echinococcosis in the Mediterranean region. Acta Trop 2003;85:191-5. doi:10.1016/S0001-706X(02)00272-3 PMID:12606096        

3. García C. Intersectorial cooperation to implement surveillance and control programmes on echinococcosis/hydatidosis. Arch Int Hidatidosis 1997;32:96-102.         

4. Gimeno-Ortiz A, Calero-Carretero R, Carmona-Carmona E, Caldera-Domínguez J. Evaluación del programa de lucha contra la hidatidosis-echinococosis en Extremadura, tras siete años de actuaciones. Rev Sanid Hig Publica 1991;65:451-61. Spanish.         

5. Jiménez S, Pérez A, Gil H, Schantz P, Ramalle E, Juste R. Progress in control of cystic echinococcosis in La Rioja, Spain: decline in infection prevalences in human and animal hosts and economic costs and benefits. Acta Trop 2002;83:213-21. doi:10.1016/S0001-706X(02)00091-8 PMID:12204394        

6. Carmena D, Sánchez-Serrano LP, Barbero-Martínez I. Echinococcus granulosus infection in Spain. Zoonoses Public Health 2008;55:156-65. doi:10.1111/j.1863-2378.2007.01100.x PMID:18331519        

7. Spain, Instituto Nacional de Estadística. [Internet site]. Available from: http://www.ine.es [accessed on 4 April 2009]          .

8. Fusté J, Séculi E, Brugulat P, Medina A, Juncá S. Población con cobertura pública o doble cobertura de aseguramiento sanitario. ¿Cuál es la diferencia? Gac Sanit 2005;19:15-21. Spanish. doi:10.1157/13071812 PMID:15745664        

9. Spanish State Official Bulletin. Real Decreto 2210/1995 por el que se crea la Red Nacional de Vigilancia Epidemiológica. BOE No. 21, 24.01. 1996. Spanish. Available from: http://www.boe.es/boe/dias/1996/01/24/index.php [accessed on 4 April 2009]          .

10. Carmena D, Benito-Pérez-de-Mendiola A, Sánchez-Serrano LP. Reporting of human cystic echinococcosis in Spain: how effective is the epidemiological surveillance system? Enferm Infecc Microbiol Clin. In press.         

11. Council Directive 64/433/EEC of the European Parliament and of the Council of 26 June 1964 on health conditions for the production and marketing of fresh meat. Available from: http://faolex.fao.org/docs/texts/eur18912.doc [accessed on 4 April 2009]          .

12. Council Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Decision 90/424/EEC and repealing Council Directive 92/117/EEC. Available from: http://www.vet.gov.ba/pdffiles/eu_leg/anheu04.pdf [accessed on 4 April 2009]          .

13. Torgerson PR. Economic effects of echinococcosis. Acta Trop 2003;85:113-8. doi:10.1016/S0001-706X(02)00228-0 PMID:12606088        

14. Budke CM, Deplazes P, Torgerson PR. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 2006;12:296-303. PMID:16494758        

15. Parasitic zoonoses. Report of a WHO Expert Committee with the participation of FAO (Technical Report Series No. 637). Geneva: World Health Organization; 1979.         

16. Torgerson PR, Dowling PM, Abo-Shehada MN. Estimating the economic effects of cystic echinococcosis. Part 3: Jordan, a developing country with lower-middle income. Ann Trop Med Parasitol 2001;95:595-603. doi:10.1080/00034980120092534 PMID:11672465        

17. Torgerson PR, Carmona C, Bonifacino R. Estimating the economic effects of cystic echinococcosis: Uruguay, a developing country with upper-middle income. Ann Trop Med Parasitol 2000;94:703-13. PMID:11144812        

18. Torgerson PR, Dowling PM. Estimating the economic effects of cystic echinococcosis. Part 2: An endemic region in the United Kingdom, a wealthy, industrialized economy. Ann Trop Med Parasitol 2001;95:177-85. doi:10.1080/00034980020030948 PMID:11299124        

19. Carabin H, Budke CM, Cowan LD, Willingham AL, Torgerson PR. Methods for assessing the burden of parasitic zoonoses: echinococcosis and cysticercosis. Trends Parasitol 2005;21:327-33. doi:10.1016/j.pt.2005.05.009 PMID:15922667        

20. Budke CM, Jiamin Q, Qian W, Torgerson PR. Economic effects of echinococcosis in a disease-endemic region of the Tibetan Plateau. Am J Trop Med Hyg 2005;73:2-10. PMID:16014823        

21. Majorowski MM, Carabin H, Kilani M, Bensalah A. Echinococcosis in Tunisia: a cost analysis. Trans R Soc Trop Med Hyg 2005;99:268-78. doi:10.1016/j.trstmh.2004.06.011 PMID:15708386        

22. National Centre of Epidemiology. [Internet site]. Available at: http://cne.isciii.es [accessed on 4 April 2009]          .

23. Burgos R, Varela A, Castedo E, Roda J, Montero CG, Serrano S, et al. Pulmonary hydatidosis: surgical treatment and follow-up of 240 cases. Eur J Cardiothorac Surg 1999;16:628-34. doi:10.1016/S1010-7940(99)00304-8 PMID:10647832        

24. Angulo JC, Sánchez-Chapado M, Diego A, Escribano J, Tamayo JC, Martín L. Renal echinococcosis: clinical study of 34 cases. J Urol 1997;157:787-94. doi:10.1016/S0022-5347(01)65041-9 PMID:9072567        

25. Moreno González E, Rico Selas P, Martínez B, García García I, Palma Carazo F, Hidalgo Pascual M. Results of surgical treatment of hepatic hydatidosis: current therapeutic modifications. World J Surg 1991;15:254-63. doi:10.1007/BF01659061 PMID:2031363        

26. Barquet N, Cayla JA, Corominas M, Bordas JM, Brau J, Trias E, et al. Hidatidosis en Catalunya: estudio en pacientes menores de 20 años (1977-1985). Med Clin (Barc) 1989;92:121-8. Spanish. PMID:2716398        

27. Hidalgo Pascual M, Barquet Esteve N. Hidatidosis hepática. Estudio de una serie de 7435 casos. Parte II: Tratamiento quirúrgico, morbimortalidad, tratamiento médico, hospitalización e implicaciones socioeconómicas. Rev Esp Enferm Apar Dig 1987b;71:103-9. Spanish. PMID:3563041        

28. Official Bulletin of Castile and Leon. Resolución de 28 de Octubre, de 2005 del Presidente de la Gerencia Regional de Salud, de revisión de las condiciones económicas aplicables en el año 2005, a la prestación de servicios de asistencia sanitaria concertada en el ámbito de la Gerencia Regional de Salud. BOCyL No. 214, 07.11.05, p. 19013. Spanish. Available from: http://bocyl.jcyl.es [accessed on 4 April 2009]          .

29. Carmona C, Perdomo R, Carbo A, Alvarez C, Monti J, Grauert R, et al. Risk factors associated with human cystic echinococcosis in Florida, Uruguay: results of a mass screening study using ultrasound and serology. Am J Trop Med Hyg 1998;58:599-605. PMID:9598448        

30. Official Bulletin of Aragon. Orden de 29 de octubre de 2004, del Departamento de Salud y Consumo, por la que se regula la acción concertada en materia de prestación de servicios sanitarios. BOA No. 135, 17.11.04, p. 10706. Spanish. Available from: http://benasque.aragob.es:443 [accessed on 4 April 2009]          .

31. The community summary report on trends and sources of zoonoses. Zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2005. The EFSA Journal 2006;94:173-82.         

32. Spain, Ministry of Agriculture, Fisheries and Food. [Internet site]. Available at: http://www.mapa.es/ [accessed on 4 April 2009]          .

33. Kenzhebaev SA. Pokazateli eckonomicheskovo ushchererba pri eckhinokokkoze karakulskikh ovets.Trudy Vsesoyuznogo Instituta Gel, mintologii-im K.L. Skryabina 1985;28:62-6. Russian.         

34. Polydorou K. Animal health and economics. Case study: echinococcosis with a reference to Cyprus. Bull Off Int Epizoot 1981;93:981-92.         

35. Ramazanov VT. Evaluation of economic losses due to echinococcosis. In: Lysenko A, ed. Vol. 2. Zoonoses control: collection of teaching aids for international training course. Moscow: Center of International Projects; 1982. pp. 283–5.         

36. Apple JK, Davis JC, Stephenson J. Influence of body condition score on by-product yield and value from cull beef cows. J Anim Sci 1999;77:2670-9. PMID:10521026        

37. McFarlane JM, Morris GL, Curtis SE, Simon J, McGlone JJ. Some indicators of welfare of crated veal calves on three dietary iron regimens. J Anim Sci 1988;66:317-25. PMID:3372377        

38. Hurtado E, González C, Vecchionacce H. Morfometría de órganos vitales de cerdos criollos en el estado Apure, Venezuela. Zootecnia Trop 2006; 24:205–11. Spanish. ISSN 0798–7269        

39. Collin A, Lebreton Y, Fillaut M, Vincent A, Thomas F, Herpin P. Effects of exposure to high temperature and feeding level on regional blood flow and oxidative capacity of tissues in piglets. Exp Physiol 2001;86:83-91. doi:10.1113/eph8602102 PMID:11429623        

40. Manso-Alonso T, Ruiz-Mantecón A, Castro-Madrigal T. Carcass yield, 5th quarter and cutting in churra lambs under different feeding strategies. Arch Zootec 1998;47:73-84.         

41. Coleman SW, Phillips WA, Chase CC, Riley DG, Morgan B, Nelson J, et al. Organ weights and internal fat of Angus or Romosinuano steers finished in the feedlot or with grain-on-pasture. J Anim Sci 2002;80 Suppl. 1;147.         

42. Kamwanja LA, Ayoade JA, Makhambera TPE. Characterisation of small ruminants in the Mitundu Area, Lilongwe, Malawi. In: Wilson RT, Bourzat D, eds. Small ruminants in African agriculture. Addis Ababa, Ethiopia: International Livestock Centre for Africa; 1985. pp. 164–72.         

43. Day JP, Boland TM, Crosby TF. The effects of plastic slatted floor or straw bedding on performance, liver weight and liver copper concentrations in intensively reared lambs. Livest Sci 2006;100:270-5. doi:10.1016/j.livprodsci.2005.09.007        

44. Ministry of Agriculture. Fisheries and Food. Agro-food statistical yearbook. Barcelona: MAFF; 2005. Available from: http://www.mapa.es/es/estadistica/pags/anuario/Anu06/indice.asp [accessed on 4 April 2009]          .

45. Anonymous. Los piensos provocan subidas de hasta un 30% en los costes de producción de los ganaderos. La Tierra 2008;207:13–4. Spanish. Available from: http://www.upa.es/_la_tierra/la_tierra_207/pag_013–014_subidas.pdf [accessed on 4 April 2009]          .

46. Spain, Ministerio de Sanidad y Política Social. Health Information System of the SNS (NHS). Available from: http://www.msc.es/en/estadEstudios/estadisticas/sisInfSanSNS/home.htm [accessed on 4 April 2009]         

47. Gutiérrez MP, Ramírez I, Zarzosa MP, Fernández JM, Dueñas AI, Mantecón MA, et al. Seroprevalencia de infección por Echinococcus granulosus en la población de Castila y León. Enferm Infecc Microbiol Clin 2003;21:563-7. Spanish. doi:10.1157/13054549 PMID:14642255        

48. Pérez-Rodríguez E, Bollo E, Navío P, Zapatero J, Flores J, Ortiz de Saracho J, et al. Estudio epidemiológico en familiares de pacientes con enfermedad hidatídica. ¿Población de alto riesgo? Rev Clin Esp 1995;195:138-40. Spanish. PMID:7754145        

49. Macpherson CNL, Bartholomot B, Frider B. Application of ultrasound in diagnosis, treatment, epidemiology, public health and control of Echinococcus granulosus and Echinococcus multilocularis. Parasitology 2003;127:S21-35. doi:10.1017/S0031182003003676 PMID:15027603        

50. Budke CM, Jiamin Q, Zinsstag J, Qian W, Torgerson PR. Utilization of disability adjusted life years in the estimation of the disease burden of echinococcosis for a high endemic region of the Tibetan Plateau. Am J Trop Med Hyg 2004;71:56-64. PMID:15238690        

(Submitted: 1 June 2009 – Revised version received: 24 September 2009 – Accepted: 2 October 2009 )

*Correspondence to David Carmena (e-mail: d.carmena@imperial.ac.uk).