Analysis of the economic impact of cystic echinococcosis in Spain

49Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Analysis of the economic impact of cystic echinococcosis in Spain Christine Benner,a Hélène Carabin,a Luisa P Sánchez-Serrano,b Christine M Budke c & David Carmenad 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. Une traduction en français de ce résumé figure à la fin de l’article. Al final del artículo se facilita una traducción al español. .ةلاقلما هذهل لماكلا صنلا ةياهن في ةصلاخلا هذهل ةيبرعلا ةمجترلا a College of Public Health, Oklahoma University Health Sciences Center, Oklahoma City, OK, United States of America (USA). b National Centre of Epidemiology, Instituto de Salud Carlos III, Madrid, Spain. c College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, USA. d Department of Immunology, Microbiology and Parasitology, University of the Basque Country, PO Box 450, 01080 Vitoria-Gasteiz, Spain. Correspondence to David Carmena (e-mail: d.carmena@imperial.ac.uk). (Submitted: 1 June 2009 – Revised version received: 24 September 2009 – Accepted: 2 October 2009 ) 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 in- termediate 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 ex- tensive 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 seri- ous 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 pro- vides 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 comput- erized 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 50 Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in Spain Christine Benner et al. 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 diag- nostic procedures, surgical or chemo- therapeutic 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 condemna- tion of viscera. Estimation of the eco- nomic 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 ap- proaches based on decision-tree analysis and efficient sampling techniques were therefore proposed, to model the in- herent 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 diag- nosed 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 epi- demiology surveillance network22 and was used to estimate the productivity losses in humans (see below). We as- sumed 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 stud- ies 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 un- diagnosed or asymptomatic cases in the Spanish population using mass ultrasound have not been conducted. Therefore, we assumed that the preva- lence 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 reduc- tion in productivity of 2.0% (range: 0.0–4.0%), based on the only re- ported assumption in the literature.17 Lost-opportunity costs correspond to the productive time lost due to an in- fected 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 hu- mans were divided into direct and indi- rect 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 specifi- cally associated with CE. Direct cost estimates included separate calculations for surgical and nonsurgical patients. In both cases, a cost-per-patient esti- mate 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 Na- tional 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 spe- cies. 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 produc- tion were obtained from the country’s Ministry of Agriculture, Fisheries and Food.32 Data stratified by age (young and adults) were included where avail- able. 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 in- direct 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 de- scribed below. Offal condemnation In Spain, identification of hydatid cysts at meat inspection leads to condemna- tion of infected offal. We therefore 51Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in SpainChristine Benner et al. assumed that the number of con- demned 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 con- demned offal in all species for 2005, we calculated the lost revenue for each CE-infected animal, according to the average weight36–43 and market value44 of both liver and lung, by species and age at slaughter. Direct costs were es- timated 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 calcu- lated 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 spe- cies. From these data we calculated the potential percentage considered losses from unborn diary animals, as ex- plained below. Decreased fecundity Animals not born because of CE in- fection 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 fe- male 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 po- tential opportunity costs, we assumed an equivalent prevalence of infection in unborn animals. To estimate the poten- tial 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 respec- tive 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 pa- rameters not available in the literature, we assigned distributions based on a Table 1. Epidemiological parameters used to estimate the human economic losses associated with CE in Spain, 2005 Parameter Value Distribution Reference Total no. of diagnosed cases (n = 159) in males, by age group, in years 0–19 3 Fixed 22 20–29 4 Fixed 22 30–39 14 Fixed 22 40–49 17 Fixed 22 50–59 11 Fixed 22 60–69 12 Fixed 22 70–79 22 Fixed 22 ³ 80 3 Fixed 22 in females, by age group, in years 0–19 5 Fixed 22 20–29 2 Fixed 22 30–39 10 Fixed 22 40–49 8 Fixed 22 50–59 5 Fixed 22 60–69 14 Fixed 22 70–79 18 Fixed 22 ³ 80 11 Fixed 22 Undiagnosed or asymptomatic cases 0–0.0154–0.02 Triangular see text Diagnosed cases with surgery 68–95–100 Triangular 23–27 Percentage of Radical pericystic resection among surgical cases (%) 63 Fixed 23–27 Partial pericystic resection among surgical cases (%) 18 Fixed 23–27 Cholecystectomy or coledocotomy among surgical cases (%) 18 Fixed 23–27 Length of hospital stay in days 1–14–35–136 Beta 46 Productivity loss as % per year 0–4 Uniform 17 CE, cystic echinococcosis. 52 Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in Spain Christine Benner et al. likely range of values to each parameter. We generated 10 000 iterations of the final model using Latin hypercube ran- dom sampling of input parameter val- ues 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% cred- ible intervals (CIs) for the total cost of CE. A stepwise linear regression of the estimated costs against the input parameter values was performed to as- sess 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 Table 2. Economic parameters used to estimate the economic losses associated with CE in humans, Spain, 2005 Economic parameter Value Distribution Range Reference Average yearly wage, in €, for males, by age group, in years < 25 13 758 Fixed NA 7 25–34 18 265 Fixed NA 7 35–44 23 029 Fixed NA 7 45–54 26 601 Fixed NA 7 ³ 55 26 201 Fixed NA 7 Average yearly wage, in €, for females, by age group, years < 25 11 226 Fixed NA 7 25–34 14 727 Fixed NA 7 35–44 16 383 Fixed NA 7 45–54 18 076 Fixed NA 7 ³ 55 18 416 Fixed NA 7 Direct cost and distribution of diagnostic procedures and medical treatment/care, as € per case Chest X-ray 18.8 Fixed NA 28,30 CT 84.45 Fixed NA 28,30 MRI 216.76 Fixed NA 28,30 Urography 71.67 Fixed NA 28,30 Arteriography 97.75 Fixed NA 28,30 Ultrasonography 89.76 Fixed NA 28,30 Serologic testing 15–25a Uniform 15–25 Unpublishedb Chemotherapy (Mbz/Albz) c 11.26 Fixed NA 28,30 Outpatient medical care 174.7 Fixed NA 28,30 Direct cost of surgical procedures, as € per case Radical pericystic resection 5 531.62 Fixed NA 28,30 Partial pericystic resection 2 420.02 Fixed NA 28,30 Cholecystectomy or coledocotomy 1 629.49 Fixed NA 28,30 CE, cystic echinococcosis; CT, computed tomography; €, euro; Mbz/Albz, mebendazole/albendazole; MRI, magnetic resonance imaging; NA, not applicable. a A wide range of serological tests is available for human hydatidosis. This range reflects the fact that the price depends on the particular type of test. b D Carmena, unpublished data, 2009. c Chemotherapy was measured in € per day. impact of input parameters were gener- ated 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 epi- demiological and economic param- eters, respectively, used to estimate the economic losses associated with CE in humans. Table 3 (available at: http://www.who.int/bulletin/vol- umes/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 as- sociated with CE in humans and ani- mals 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 po- tential impact of wage losses in undi- agnosed 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 53Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in SpainChristine Benner et al. Table 4. Cost parameters used to estimate the economic losses associated with CE in livestock, Spain, 2005 Parameter Average cost, in € per kga Reference Sheep Lamb carcass 6.83 32 Sheep carcass 0.60 Extrapolated from 44 Sheep liver 0.65 44 Sheep lung 0.09 44 Sheep’s milk at farm gatea 79.11 32 Farmer investment 1.59 45 Goats Kid carcass 8.40 Extrapolated from 44 Goat carcass 0.90 Extrapolated from 44 Goat liver 0.65 Extrapolated from 44 Goat lung 0.09 Extrapolated from 44 Goat’s milk at farm gatea 51.63 32 Farmer investment 1.59 45 Cattle Calf carcass 3.80 Extrapolated from 44 Bull carcass 1.72 Extrapolated from 44 Young live cow 1.76 32 Beef carcass 3.35 45 Cow liver 0.85 44 Cow lung 0.06 44 Cow’s milk at farm gatea 31.25 32 Farmer investment/kg 2.04 45 Pigs Pig liver at abattoir 0.54 44 Pig lungs at abattoir 0.06 44 Pig carcass 1.42 32 Piglet carcass 1.42 Extrapolated from 44 Farmer investment 1.06 45 CE, cystic echinococcosis; €, euro. a Average cost of milk was measured in € per 100 L. resulted in a reduction of the median economic cost in 2005 to €16 442 870 (Table 5). The table shows that indi- rect 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 as- sociated with illness). The normalized regression coefficient values in Fig. 1 illustrate the impact of uncertain pa- rameters on the overall costs after removing asymptomatic human cases from the model; under these condi- tions, several animal parameters be- come 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 mak- ers 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 stan- dard methods for estimating the costs of the infection and to differences among countries in human and animal popula- tion sizes, disease prevalence, inherent socioeconomic patterns and period of valuation. The Latin hypercube method used in this study to represent the uncer- tainty surrounding the input param- eters is particularly suitable for esti- mating indirect costs where accurate human and animal epidemiological data are scarce. To make the estimates more robust, we stratified rates of hu- man CE infection and average wages by age and gender. For livestock, we used age-stratified prevalence propor- tions, where available. Our results indicate that CE con- tinues 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 ca- pacity for distinguishing asymptomatic cases from misdiagnosed or untreated cases (because respective productivity losses may vary considerably between groups). Regarding the need for more accu- rate baseline estimates, mass screening studies of infection with E. granulosus, based on the detection of circulat- ing 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 para- site rather than the prevalence of active infection. An alternative is ultrasonog- raphy, which is a reliable and accurate diagnostic tool for reporting infection status in human asymptomatic popula- tions.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 dis- ability caused by the chronic effect of the infection.50 A theoretical estimate of a 2% reduction in work productivity 54 Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in Spain Christine Benner et al. Table 5. Median direct, indirect and total costs associated with CE in humans and livestock, including and excluding asymptomatic or undiagnosed productivity losses, Spain, 2005 Category Asymptomatic or undiagnosed productivity losses Included Excluded Median cost, in € 95% CI Median cost, in € 95% CI Human Direct 603 671 499 200–662 638 603 427 499 967–662 628 Indirect 132 795 199 5 967 994–378 695 718 274 643 59 094–717 779 Subtotal 133 416 601 6 658 738–379 273 434 872 414 630 181–1 327 733 Animal Direct 177 985 161 656–194 432 177 968 161 545–194 439 Indirect 15 353 863 13 273 648–17 610 439 15 367 200 13 287 583–17 798 384 Subtotal 15 532 242 13 447 378–17 789 491 15 546 700 13 468 193–17 798 384 Total losses 148 964 534 21 980 446–394 012 706 16 442 870 14 330 767–18 732 759 Direct 781 032 675 524–844 564 781 343 676 839–844 711 Indirect 148 189 492 22 200 164–395 747 574 15 670 240 13 543 961–17 964 120 CE, cystic echinococcosis; CI, credible interval; €, euro. Fig. 1. Estimated normalized regression coefficients showing the associations between uncertain parameters and total losses due to CE, excluding asymptomatic or undiagnosed productivity losses, Spain, 2005 Coefficient value Average number of calves per cow per year – 0.6 0.83 – 0.42 0.20 0.20 0.15 0.15 0.11 0.04 0.03 – 0.4 – 0.2 0 0.2 0.4 0.6 0.8 1 Decrease in fecundity Reduction in milk production Average weight in kg – cow carcass Percentage reduction in carcass weight for all species Average length of hospital stay, in days Average weight in kg – calf carcass Percentage diagnosed cases with surgery Average number of lambs per ewe per year CE, cystic echinococcosis. in asymptomatic cases (for estimating work productivity losses) has been proposed.17 More research on the so- cioeconomic 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 aver- age 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 psycho- logical burden that may be associated with the infection. In livestock, indirect losses ac- count 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 produc- tivity losses makes accurate estimates of the economic losses of CE in livestock difficult to perform. Another limitation of the esti- mated costs of surgical treatment for CE in humans is that these were based on the average cost of surgical interven- tions 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 re- moval 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 offi- cial 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. How- ever, in countries where goats represent a more important ruminant popula- tion, 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 comor- bidity status. 55Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in SpainChristine Benner et al. Résumé Analyse de l’impact économique de l’échinococcose kystique en Espagne 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. Conclusion Our findings indicate that CE im- poses a significant economic burden on Spain. They also emphasize the im- portance 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 coopera- tion between the central and regional administrations, and the institutions responsible for collecting, providing and publishing data of epidemiologi- cal 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. Resumen Análisis del impacto económico de la hidatidosis en España 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. 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World J Surg 1991;15:254-63. doi:10.1007/BF01659061 PMID:2031363 صخلم اينابسأ في سييكلا تاكوشلما ءادل يداصتقلاا يرثأتلا ليلحت شربلا ةباصإ نع ةمجانلا ةيلماجلإا ةيداصتقلاا رئاسخلا ريدقت :ضرغلا .2005 في اينابسأ في سييكلا تاكوشلما ءادب تاناويحلاو تاكوشلما ءادل يونسلا عوقولا لدعبم ةصاخلا تانّيبلا تعمُج :ةقيرطلا ءاد تاجلاعم تانّيبو ،تاناويحلا رزاجمو دصترلا تلاجس نم سييكلا تايشرنلا نم )ةيناويحلاو ةيشربلا( ةيجاتنلإا رئاسخلاو سييكلا تاكوشلما ،صيخشتلاب ةقلعتلما فيلاكتلا يه ةشرابلما فيلاكتلا برتعتو .ةيملعلا في ميونتلاو ،ةيبطلا ةياعرلاو ،ةئايميكلا ةجلاعلما وأ ةيحارجلا ةجلاعلماو ،منغلا( ةيناويحلا تلاضفلاب ةقلعتلما كلتو ،شربلل ةبسنلاب تايفشتسلما ةيجاتنلإا رئاسخلا ةشرابلما يرغ فيلاكتلا لمشتو .)ريزانخلاو ،رقبلاو ،زعالماو دقو .تاناويحلا في بنللا راردإ ةلقو ةبوصخلاو ومنلا ضافخناو ،ةيشربلا لخدبم طيحلما كشلا ليثمتل Latin hypercube ةقيرط تمدختسا .تاتباثتلما تاكوشلما ءاد نع ةمجانلا ةيداصتقلاا رئاسخلا ليماجإ َرِدُق :تادوجولما وروي 148964534 رادقبم 2005 ماع في تاناويحلاو شربلا في سييكلا رئاسخلا َترِدُقو .)394012706 – 21980446 :%95 CI ةقثلا ةترف( – 6658738 :%95 CI ةقثلا ةترف( وروي 133416601 رادقبم ةيشربلا CI ةقثلا ةترف( 15532242 رادقبم ةيناويحلا رئاسخلاو )379273434 .)17789491 – 13447378 :%95 يتلا ةلمهلما ةيناويحلا ضارملأا نم سييكلا تاكوشلما ءاد برتعي :جاتنتسلاا تاّنيبلل ةجاح كانهو .اينابسأ في ناويحلاو ناسنلإا نم لكل قلقلل ةيرثم لظت يتلا تلااحلا مايسلا( شربلا ينب سييكلا تاكوشلما ءاد راشتنا لوح ةقد ثركلأا ريدقتل لضفلأا قرطلاو )ضارعأب ةبوحصلما يرغ تلااحلا وأ اهصيخشت متي لم ضعب بيصي سييكلا تاكوشلما ءاد لازامو .تاناويحلا في ةيجاتنلإا رئاسخلا .1986 ماع ذنم هتحفاكلم ةددعتلما ترادابلما نم مغرلاب اينابسأ في قطانلما نإف ،سييكلا تاكوشلما ءادل ليقثلا يداصتقلاا ءبعلا نابسحلا في ذخلأا عمو نم ناويحلاو ناسنلإا في ىودعلا تلادعم ضفخل فياضإ ليومتل ةجاح كانه نواعتلا نم ديزلماو ،بلاكلل ةمظتنلما ةجلاعلماو ،ضرلما دصرت ينسحت للاخ .تائيهلا ينب 57Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in SpainChristine Benner et al. 26. 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PMID:15238690 ABull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in SpainChristine Benner et al. Table 3. Epidemiological parameters used to estimate the economic losses associated with CE in livestock, Spain, 2005 Parameter Value Distribution Range Unit Reference Sheep Total population a 22 749 000 Fixed NA Individuals 44 Lambsa 3 974 000 Fixed NA Individuals 44 Lambs for slaughter 18 497 000 Fixed NA Individuals 32 Adultsa 18 775 000 Fixed NA Individuals 44 Adults for slaughter 894 000 Fixed NA Individuals 32 No. of sheep slaughtered per year 19 390 776 Fixed NA Individuals 44 Prevalence of infection at inspectionb 0.57 Fixed NA % of infected animals at slaughter 31 Lambs 0.14 Fixed NA % of infected animals at slaughter 31 Adults 0.43 Fixed NA % of infected animals at slaughter 31 No. of dairy sheep 2 850 177 Fixed NA Individuals 32 Average weight Lamb carcass 9.80 Uniform 9.6–10.0 Kg 44 Sheep carcass 20.00 Uniform 18.0–22.0 Kg 44 Lamb liver 0.85 Uniform 0.8–0.9 Kg 40,43 Lamb lung 0.60 Uniform 0.5–0.7 Kg 40,43 Sheep liver 1.00 Uniform 0.9–1.1 Kg Extrapolated from 42 Sheep lung 0.70 Uniform 0.6–0.8 Kg Extrapolated from 42 Mean lambing per year Dairy sheep 1.5 Uniform 1.4–1.6 Lambs per ewe per year See text Meat sheep 1 Uniform 0.9–1.1 Lambs per ewe per year See text Average milk yield of dairy sheep 170 Uniform 160–170 Kg per year Extrapolated from 44 No. unborn lambs 87 089 NA Individuals Calculation Goats Total populationa 2 904 000 Fixed NA Individuals 44 Kidsa 385 000 Fixed NA Individuals 44 Kids for slaughter 1 401 000 Fixed NA Individuals 32 Adultsa 2 519 00 Fixed NA Individuals 44 Adults for slaughter 179 000 Fixed NA Individuals 32 No. goats slaughtered 1 580 549 Fixed NA Individuals 44 Prevalence of infection at inspectionb 0.57 Fixed NA % of infected animals at slaughter 31 Kids 0.14 Fixed NA % of infected animals at slaughter 31 Adults 0.43 Fixed NA % of infected animals at slaughter 31 No. of dairy goats 1 261 135 NA Individuals 32 Average weight Kid carcass 10.35 Uniform 10.0–10.7 Kg 44 Goat carcass 23.50 Uniform 21–26 Kg 44 Kid liver 0.85 Uniform 0.8–0.9 Kg Extrapolated from 40,43 Kid lung 0.60 Uniform 0.5–0.7 Kg Extrapolated from 40,43 Goat liver 1.00 Uniform 0.9–1.1 kg Extrapolated from 42 Goat lung 0.70 Uniform 0.6–0.8 Kg Extrapolated from 42 Mean kidding per year Dairy goat 1.60 Uniform 1.5–1.7 Kids born per goat per year See text Meat goat 1.30 Uniform 1.2–1.4 Kids born per goat per year See text Average milk yield of dairy goat 383 Uniform 380–386 Kg per year Extrapolated from 44 No. unborn kids 14 360 NA Individuals Calculation B Bull World Health Organ 2010;88:49–57 | doi:10.2471/BLT.09.066795 Research Economic impact of cystic echinococcosis in Spain Christine Benner et al. Parameter Value Distribution Range Unit Reference Cattle Total populationa 6 484 000 Fixed NA Individuals 44 Calves (< 1 year)a 2 254 000 Fixed NA Individuals 44 Calves for slaughter 246 944 Fixed NA Individuals 44 Young animals (> 1 but < 2 yr old)a 748 000 Fixed NA Individuals 44 Young animals for slaughter 769 645 Fixed NA Individuals 44 Adults (> 2 yr old)a 3 464 000 Fixed NA Individuals 44 For slaughtering (cows) 400 576 Fixed NA Individuals 44 For slaughtering (bulls) 1 340 393 Fixed NA Individuals 44 For milk production 1 008 000 Fixed NA Individuals 44 No. of cattle slaughtered per year 2 757 558 Fixed NA Individuals 44 No. of infected cattle slaughtered per year 19 824 Fixed NA Individuals 31 Prevalence of infection at inspection 0.7 Fixed % of infected animals at slaughter 31 Average weight Calf carcass 155.0 Uniform 150–160 Kg 44 Cow carcass 275.00 Uniform 270–280 Kg 44 Young cow carcass 242.25 Uniform 239.0–245.5 Kg 44 Bull carcass 282.50 Uniform 278–287 Kg 44 Calf liver 3.20 Uniform 2.9–3.5 Kg 36,37,41 Calf lung 3.75 Uniform 3.5–4.0 Kg 36,37,41 Cow liver 6.35 Uniform 5.4–7.3 Kg 36,37,41 Cow lung 6.15 Uniform 5.2–7.1 Kg 36,37,41 Mean calving per year Dairy cow 0.75 Uniform 0.7–0.8 Calves per cow per year See text Beef cow 0.65 Uniform 0.6–0.7 Calves per cow per year See text Annual cow milk production 6 552 700 Fixed NA Tonnes 32 Average milk yield of dairy cow 6 281 Fixed NA Kg per year 44 No. of unborn calves 19 038 Individuals Calculation Pigs Total populationa 24 884 000 Fixed NA Individuals 44 No. of pigletsa 6 762 000 Fixed NA Individuals 44 No. of pigs slaughtered 38 705 240 Fixed NA Individuals 44 No. of infected pigs slaughtered per year 10 320 Fixed NA Individuals 31 Prevalence of infection at inspection 0.03 Fixed NA % of infected animals at slaughter 31 Average weight Piglet carcass 6.70 Uniform 6.5–6.9 Kg 44 Pig carcass 85 Uniform 80–90 Kg 44 Pig lung 0.41 Uniform 0.38–0.43 Kg 38,39 Pig liver 1.01 Uniform 0.98–1.04 Kg 38,39 Piglet lung 0.075 Uniform 0.05–0.10 Kg Extrapolated from 39 Piglet liver 0.075 Uniform 0.05–0.10 Kg Extrapolated from 39 Mean no. of piglets per year 19 Uniform 18–20 Piglets/sows per year See text No. of unborn pigs 1 448 783 NA Individuals Calculated Productivity losses – all livestock Decrease in fecundity 5.5 Uniform 0.0–11.0 % decrease per year 35 Decrease in carcass weight 6.25 Uniform 2.5–10.0 % decrease per year 4,34 Decrease in milk production 2.5 Uniform 0.0–5.0 % decrease per year 4,34 CE, cystic echinococcosis; NA, not applicable. a Census at 31 December 2005. b CE prevalence rates in sheep and goats are co-reported in Spain. (Table 3, cont.)