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Research Article

# Economic Impact of Cystic Echinococcosis in Peru

• pmoro@cdc.gov

Affiliation: Division of Healthcare Quality Promotion, Immunization Safety Office, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America

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• Affiliation: College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America

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• Affiliation: Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America

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• Affiliation: Portneuf Medical Center and Idaho State University, Pocatello, Idaho, United States of America

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• Affiliation: Instituto Peruano de Parasitologia Clinica y Experimental, Lima, Peru

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• Affiliation: Servicio Nacional de Sanidad Agraria, Ministerio de Agricultura, Lima, Peru

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• Published: May 24, 2011
• DOI: 10.1371/journal.pntd.0001179

## Abstract

### Background

Cystic echinococcosis (CE) constitutes an important public health problem in Peru. However, no studies have attempted to estimate the monetary and non-monetary impact of CE in Peruvian society.

### Methods

We used official and published sources of epidemiological and economic information to estimate direct and indirect costs associated with livestock production losses and human disease in addition to surgical CE-associated disability adjusted life years (DALYs) lost.

### Introduction

#### Application of DALYs to human surgical CE cases

The DALY formula was applied to age and gender stratified human CE surgical incidence data. The DALY is made up of two parts; years of life lost due to mortality (YLL) and years of life lost due to time lived in a disability state (YLD). The formulas for YLL and YLD are:
where N = number of deaths per age-sex group, L = remaining life expectancy at age of death
where I = age and sex specific estimates of incidence, DW = disability weight, D = average duration of disability.

Disability weight for CE was assigned a multinomial distribution based on numerous retrospective studies evaluating postoperative outcome. In accordance with previous studies, the percentage of patients projected to improve after surgery was assigned a disability weight of 0.200 for 1 year, the percentage of patients projected to have substantial postsurgical complications was assigned a disability of 0.239 for 5 years, the percentage of patients projected to have recurrent disease was assigned a disability of 0.809 for 5 years, and the percentage of patients projected to die postoperatively were assigned a disability of 1 (indicating death) for the remainder of their predicted lifespan [7]. Since malignant neoplasms of the respiratory tract (the best surrogate for CE of the lungs) have a similar disability weight at diagnosis (0.150) to that used previously for hepatic CE (0.200) and the same disability weights for sequelae, CE cases were assigned the same spectrum of disability weights regardless of lesion site. This also allows for estimates from this study to be comparable to previously published estimates for CE burden.

#### Analysis

Spreadsheet models were constructed in Excel (Microsoft, Redmond, WA) utilizing the @Risk (Palisade Corp., Ithaca, NY) statistical add-in. Values were selected across the various assigned distributions and summed using Latin Hypercube sampling techniques. A total of 10,000 simulations were performed and the mean and 95% confidence intervals (CI) obtained for annual losses. Step-wise linear regression of the estimated CE-associated costs against the input parameters was conducted to assess the impact of individual parameters on the overall cost estimate.

This study was exempted from human subjects review by the Institutional Review Board of the Centers for Disease Control and Prevention because no personal identifiers were collected.

### Results

Human health costs resulting from CE can be observed in table 5. Direct costs associated with surgical treatment of CE were estimated to account for U.S.$836,064 (95% CI:731,271–948,236) per year. Human health costs resulting from lost productivity were estimated at U.S.$1,592,764 (95% CI:310,664–3,947,315) annually. The total estimated cost of human surgical CE cases and productivity losses from non-surgically treated cases in Peru was estimated at U.S.$2,420,348 (95% CI:1,118,384–4,812,722) per year. #### Animal health costs The estimated losses resulting from liver condemnation and production losses in each animal species are detailed in table 6. Total estimated losses due to CE ranged from U.S.$196,681 (95% CI:141,641–251,629) if only direct losses (i.e., cattle and sheep liver losses) are taken into consideration to U.S.$3,846,754 (95% CI:2,676,181–4,911,383) if all production losses evaluated (liver losses, decreased carcass weight, wool losses, decreased milk production) are accounted for. #### Disability adjusted life years (DALYs) The estimated number of DALYs lost due to surgical CE in Peru was estimated at 1,139 (95% CI: 861–1,489). Table 7 shows DALYs lost for surgical cases of CE in comparison with other infectious diseases in Peru as well as estimated DALYs lost due to CE in other South American countries (Argentina, Brazil, Chile and Uruguay). #### Sensitivity analysis Sensitivity analysis for monetary losses associated with CE, indicated that human productivity losses (0.691), the estimated number of sub-clinical cases (0.447), losses due to decreased cattle carcass weight (0.339), and losses due to decreased milk production in cattle (0.281) had the largest coefficient values (in brackets) and, therefore, the greatest impact on the overall estimate on monetary losses due to CE in Peru. ### Discussion This is the first study to provide an assessment of the economic effects of CE in humans and livestock in Peru. Studies that estimate the economic burden of CE can be very important as they identify specific areas that may need to be addressed by policy makers responsible for the design and implementation of CE control programs. The economic impact of CE has been assessed in South American countries where CE is endemic [5], [19]. A recent study in Argentina, Brazil, Chile and Uruguay demonstrated total adjusted human and animal losses of US$ 108,276,378-$146,580,935 for all four countries combined [19]. However, it is difficult to make direct comparisons with other countries due to demographic and epidemiological differences. In addition, there is no standard approach recognized when estimating economic costs for CE in human and animal populations. For example, treatment costs for non-surgical CE patients were not estimated and included in the present study. Per capita GNI was also used in this study to account for human productivity losses rather than taking into account income losses for those who work outside the home versus those who are not officially employed. In addition, losses due to decreased fecundity were not included due to the lack of information on the true impact of CE on reproduction. In addition, livestock were not separated by age since CE prevalence data is not available for different age groups of domestic livestock. Finally, farmer investment was also not taken into consideration. In the present study, total estimated losses due to CE were U.S.$ 6,357,027 (95% CI: 4,422,699–8,788,182) of which two-thirds comprised human economic losses and the other third were animal production losses. This is a very conservative estimate based to a large extent on official sources of information which very likely underestimate the true extent of the problem. Nevertheless these estimates illustrate the negative economic impact of CE in Peru.

In Peru, surgery remains the treatment of choice for CE. Surgical treatment of CE is a costlier alternative than the less invasive puncture-aspiration-injection-reaspirati​on(PAIR) technique or benzimidazole use. In Argentina, a country where CE is endemic, the average cost of conventional surgery for CE of the liver was $5,936 in comparison to the cost of PAIR at$1,988 and \$1,350 for albendazole treatment [20]. PAIR is not available in Peru and use of benzimidazoles is reserved for prophylactic use prior to surgery [21]. Use of less costlier procedures in Peru such as PAIR and sole chemotherapeutic treatment could result in lower overall treatment costs. Our estimate of the cost of surgical treatment for CE is based on the cost incurred in a public hospital located in Lima city. Costs may vary in other areas of Peru, especially in endemic areas. Therefore, our estimates may not reflect the true cost of surgical treatment in the country. In addition, this estimate does not take into account an important number of patients who receive treatment at private clinics where the cost of surgical treatment can be 4 or more times higher than in public hospitals. In one study in an endemic area of Peru, 8% of patients received treatment in private clinics compared to 44% in public hospitals and 47% in hospitals of the national health care system [12]. Our estimates of treatment costs for CE underestimates the true cost of human CE as we did not include the cost of benzimidazoles given the absence of data on sole benzimidazole use against CE in Peru.

An important limitation of this study is the absence of current data on the incidence or prevalence of CE in humans and animals. Available sources of data have not been updated for the last 20–30 years. Although the Peruvian Ministry of Health has regularly collected information on outpatient consultations due to CE since 2000, it is not known how many of these cases were confirmed and the type of treatment received. Data on CE condemned livestock viscera at the national level is collected by the Peruvian Ministry of Agriculture from inspections performed in abattoirs. However, a substantial number of livestock are home slaughtered, particularly in areas endemic for CE. In addition, younger animals, which are less likely to be infected, tend to be slaughtered in abattoirs. Therefore, these official sources of information may greatly underestimate the real prevalence of infection. For example, based on official publications, the incidence of human CE in the endemic Department of Junin was 24 cases per 100,000 during 2002 [22]. However, epidemiological studies conducted in Junin have demonstrated that the surgical incidence can reach 127 cases per 100,000 [2]. Similarly, official records showed that in the coastal city of Chincha the incidence of human infection was 10 cases per 100,000 during 2005 [22], but an epidemiological investigation revealed a surgical incidence of 32 cases per 100,000 population [23]. For livestock, official sources indicated a prevalence of sheep CE of 10% for 2002 in the Department of Junin [10]. However, epidemiological studies in abattoirs in this same area showed that as many as 77% of sheep were infected [4].

We estimated that 1,139 (95% CI: 861–1,489) DALYs are lost annually in Peru due to surgical cases of CE, which is comparable to CE-associated DALYs lost for Argentina, Brazil, Chile and Uruguay combined [19]. DALYS lost due to CE were also found to be similar to other conditions such as malaria, amoebiasis, and leishmaniasis [24]. These infectious diseases are better monitored than CE and thus their DALYs estimates are likely to better capture the true impact of those diseases on the country. In the case of CE, the absence of updated information on the frequency of human CE hampers the calculation of this socio-economic indicator. However, the number of DALYs estimated to be lost in this study is very conservative since only surgical cases of CE were evaluated.

The findings of the present economic evaluation, although conservative, highlight the monetary losses caused by CE in the Peru. Control programs could potentially prevent many of these losses in a cost-effective manner. For example, a control program implemented in the highly endemic region of La Rioja, Spain based on a combination of owned dog deworming, stray dog control, and safe ruminant carcass disposal resulted in a positive cost/benefit ratio after 8 years. This ratio increased to 1.96 by the conclusion of the 14-year program [25]. Control programs have been previously implemented in Peru. For example, a pilot control program was conducted in Peru during the 1970′s which was later abandoned due largely to political instability. However, the program succeeded in reducing the number of infected dogs from 36% in 1975 to 1.6% in 1980 and the number of infected sheep from 65% in 1976 to 37% in 1980 [2], [26]. There is urgent need to implement better surveillance systems to monitor the incidence/prevalence of echinococcosis in humans and animals in Peru so that they may be used as part of new control efforts for CE. In summary, CE is an important but neglected zoonotic disease in Peru which significantly affects the economy of the country.

### Supporting Information

Alternative Language Abstract S1.

Spanish translation of the abstract by PLM.

doi:10.1371/journal.pntd.0001179.s001

(DOCX)

### Acknowledgments

We thank Ms Lilia Cabrera for her support in the execution of this study.

### Author Contributions

Conceived and designed the experiments: P. Moro. Performed the experiments: P. Moro, C. Budke, J. Vazquez, J. Villavicencio. Analyzed the data: P. Moro, C. Budke, P. Schantz, J. Vazquez, S. Santivañez, J. Villavicencio. Contributed reagents/materials/analysis tools: C. Budke, J. Vazquez, J. Villavicencio. Wrote the paper: P. Moro, C. Budke, P. Schantz, J. Vazquez, S. Santivañez, J. Villavicencio. Provided some of the databases used in study: J. Vazquez, J. Villavicencio. Provided specialized software and conducted analysis with it: C. Budke.

### References

1. 1. Moro PL, Schantz PM (2009) Echinococcosis: A review. International Journal of Infectious Diseases 13: 125–33.
2. 2. Moro PL, McDonald J, Gilman RH, Silva B, Verastegui M, et al. (1997) Epidemiology of Echinococcus granulosus infection in the central Peruvian Andes. Bulletin of the World Health Organization 75: 553–61.
3. 3. Moro PL, Bonifacio N, Gilman RH, Lopera L, Silva B, et al. (1999) Field diagnosis of Echinococcus granulosus infection among intermediate and definitive hosts in an endemic focus of human cystic echinococcosis. Trans R Soc Trop Med Hyg 93: 611–5.
4. 4. Dueger EL, Gilman RH (2001) Prevalence, intensity, and fertility of ovine cystic echinococcosis in the central Peruvian Andes. Trans R Soc Trop Med Hyg 95: 379–83.
5. 5. Torgerson PR, Carmona C, Bonifacino R (2000) Estimating the economic effects of cystic echinococcosis: Uruguay, a developing country with upper-middle income. Ann Trop Med Parasit 94: 703–13.
6. 6. Murray CJL, Lopez AD (1996) The Global Burden of Disease: Global Burden of Disease and Injury Series. Volume I. Harvard School of Public Health, Boston.
7. 7. Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12: 296–303.
8. 8. Budke CM, Jiamin Q, Zinsstag J, Qian W, Torgerson PR (2004) Use 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 71: 56–64.
9. 9. Budke CM, Jiamin Q, Qian W, Torgerson PR (2005) Economic effects of echinococcosis in a disease-endemic region of the Tibetan Plateau. Am J Trop Med Hyg 73: 2–10.
10. 10. Ministry of Health (1989) National Zoonosis Control Program Records of the National Seminar on Zoonoses and Foodborne Diseases. Lima,, Peru: Ministerio de Salud.
11. 11. Rodríguez T (1990) Epidemiological study of human hidatidosis reported during the period 1975-1986 in the principal hospitals of metropolitan Lima. Thesis. Faculty of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru, (in Spanish).
12. 12. Salgado DS, Suarez-Ognio I, Cabrera R (2007) Características clínicas y epidemiológicas de la equinococosis quística registrados en un area endémica en los Andes centrales del Perú (1991-2002). Neotrop Helminthol 1: 69–84.
13. 13. Torgerson PR, Dowling PM, Abo-Shehada MN (2001) Estimating the economic effects of cystic echinococcosis. Part 3: Jordan, a developing country with lower-middle income. Ann Trop Med Parasitol 95: 595–603.
14. 14. Vasquez JC, Montesinos E, Peralta J, Rojas L, DeLaRosa J, et al. (2009) Need for lung resection in patients with intact or ruptured hydatid cysts. Thorac Cardiovasc Surg 57: 295–302.
15. 15. World Bank. Available: http://web.worldbank.org/WBSITE/EXTERNAL​/DATASTATISTICS/0,contentMDK:20394802~pa​gePK:64133150~piPK:64133175~theSitePK:23​9419,00.html. Accessed 2010 Jun 17.
16. 16. Polydorou K (1981) Animal health and economics. Case study: echinococcosis with a reference to Cyprus. Bull Of Inter Epizooties 93: 981–992.
18. 18. Majorowski MM, Carabin H, Kilani M, Bensalah A (2005) Echinococcosis in Tunisia: a cost analysis. Trans R Soc Trop Med Hyg 99: 268–78.
19. 19. Food and Agriculture Organization of the United Nations, Regional Office for Latin America and the Caribbean (2007) Estimacion del impacto economic de la equinococosis quistica en el cono sur (Argentina, Brasil, Chile y Uruguay). June 2007. Available: http://www.paho.org/spanish/ad/dpc/vp/hi​datidosis-impacto-econ-07-fao.pdf. Accessed 2010 Jun 17.
20. 20. Larrieu E, Mercapide C, Del Carpio M, Salvitti JC, Costa MT, et al. (2000) Evaluation of the losses produced by hydatidosis and cost/benefit analysis of different strategic interventions of control in the Province of Rio Negro, Argentina. Bol Chil Parasitol55: 8–13.
21. 21. Vildósola H, Sanchéz L, Espinoza R (1989) Albendazole in the treatment of hepatic and intra-abdominal hydatidosis Rev Gastroenterol Peru 9: 17–23.
22. 22. Office of Statistics and Informatics, Ministry of Health of Peru (2008) Outpatient visits for cystic echinococcosis in public healthcare facilities of Peru, 2000-2006. Lima: Ministry of Health of Peru.
23. 23. Moro PL, Lopera L, Cabrera M, Cabrera G, Silva B, et al. (2004) Short report: endemic focus of cystic echinococcosis in a coastal city of Peru. Am J Trop Med Hyg 71: 327–9.
24. 24. Perú. Ministerio de Salud del Perú (2006) Estudio de Carga de Enfermedad en el Perú – 2004. Lima: Dirección General de Epidemiología. 41 p.
25. 25. Benner C, Carabin H, Sánchez-Serrano LP, Budke CM, Carmena D (2010) Analysis of the economic impact of cystic echinococcosis in Spain. Bull World Health Organ 88: 49–57.
26. 26. Moro P, Schantz PM (2006) Cystic echinococcosis in the Americas. Parasitol Int 55: S181–6.
27. 27. Instituto Nacional de Estadistica e Informatica. XI Censo de Población y VI de Vivienda (2007) Republica del Peru. Available: http://www.inei.gob.pe/. Accessed 2010 Jun 17.
28. 28. Gavidia CM, Gonzalez AE, Zhang W, McManus DP, Lopera L, et al. (2008) Diagnosis of cystic echinococcosis, central Peruvian Highlands. Emerg Infect Dis 14: 260–6.

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