Methods for assessing the burden of parasitic zoonoses: echinococcosis and cysticercosis

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Methods for assessing the burden of parasitic zoonoses: echinococcosis and cysticercosis He´le`ne Carabin1, Christine M. Budke2, Linda D. Cowan1, A. Lee Willingham III3,4 and Paul R. Torgerson2 1 College of Public Health, University of Oklahoma Health Sciences Center, 801 Northeast 13th Street, Room 303, Oklahoma City, OK 73104, USA 2 Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland 3 WHO/FAO Collaborating Center for Parasitic Zoonoses, Danish Center for Experimental Parasitology, Royal Veterinary and Agricultural University, Dyrelaegevej 100, DK-1870 Frederiksberg C, Denmark 4 People, Livestock and the Environment Thematic Programme, International Livestock Research Institute, PO Box 30709, 00100 Nairobi, Kenya

Cysticercosis and echinococcosis cause illness and productivity losses in human and agricultural animal populations. Recent studies suggest that these diseases have large societal impacts on endemic areas. Estimates of burden provide essential, evidence-based data for conducting cost–benefit and cost–utility analyses that will secure political will, and financial and technical resources. To evaluate the burden, the monetary and non-monetary impacts of these zoonoses on human health, agriculture and society must be considered comprehensively. In this article, we review the framework used to assess the burden of cysticercosis and echinococcosis, and the data needed to estimate the extent of the problem for societies.

The impact of cysticercosis and echinococcosis Human cysticercosis (see Glossary) and echinococcosis result in mortality, morbidity and economic losses in human and animal populations. Because the total societal impact is often unknown, several initiatives have started to assess the burden of these infections in both monetary and non-monetary terms. Human cystic echinococcosis (CE) (Figure 1) occurs when a person is infected with the larval stage of Echinococcus granulosus following ingestion of eggs and can result in a substantial lesion, most commonly in the liver or lungs [1]. Humans are aberrant intermediate hosts for Echinococcus multilocularis, which causes alveolar echinococcosis (AE): a primary infiltrative lesion in the liver, with metastases in advanced cases [1]. Human CE and, particularly, AE are difficult and expensive to treat. CE in domestic animals can result in major losses of edible offal and productivity (for review, see Ref. [2]). Humans acquire taeniosis by eating undercooked pork that is contaminated with cysticerci, the larval form of Taenia solium. In low-income countries, pigs often roam Corresponding author: Torgerson, P.R. ([email protected]). Available online 26 May 2005

where people live. They eat human faeces containing eggs that form larval cysts after migration. In humans, the metacestode can also establish itself following ingestion of eggs, and a principal site of migration is the central nervous system (CNS), resulting in neurocysticercosis (NCC). NCC has been reported to be the most common helminth disease of the CNS and the most frequent preventable cause of epilepsy in low-income countries [3]. NCC can also manifest with severe headaches, blindness, hydrocephalus, chronic meningitis, symptoms due to space-occupying CNS lesions, and dementia [4,5]. Glossary Alveolar echinococcosis: an infection or disease of humans or animals caused by the larvae of Echinococcus multilocularis. Cystic echinococcosis: an infection or disease of humans or animals caused by the larvae of Echinococcus granulosus. Cysticercosis: an infection or disease of humans or animals caused by the larvae of Taenia spp. In this article, the term refers to infection of humans or pigs with Taenia solium cysticercosis. Decision-tree analysis: a method of organizing epidemiological data into infections and the frequency of their consequences. Disability-adjusted life year: in simplest terms, this can be considered a lost healthy year of life and is a non-monetary measure of disease burden. It takes into account the severity of the syndrome and its duration, thus levelling the playing field when comparing acute and chronic conditions. A DALY also has the same value in poor and rich countries. Disability weight: a score between 0 and 1 that is assigned to a condition depending on the degree of debilitation. Direct costs: costs such as carcass condemnation or medical costs arising directly from the treatment of infection. Health-adjusted life year: an umbrella term for a family of measures of population health that includes, for example, DALYs and QALYs. Indirect costs: costs such as production deficits or wage losses arising indirectly from infection. Metacestodosis: infection with the larval stage of a cestode. Monte Carlo sampling technique: a method that can be employed in cost analysis when exact estimates are unknown. Repeated samples are taken over a probability distribution based on the known information. Neurocysticercosis: a neurological disease caused by invasion of the CNS by larvae of T. solium. Quality-adjusted life year: a population measure of health. A year of full health is equivalent to 1 QALY, whereas death corresponds to 0 QALYs. Disease conditions are graded on a continuous scale between these two extremes. Taeniosis: an infection of humans caused by the adult stages of Taenia spp. (in this article, T. solium specifically).

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Figure 1. An African child with severe abdominal echinococcosis. Photograph by Peter Schantz.

Cysticercosis–taeniosis is extremely important in smallholder farming communities [6,7] because it exacts a triple price in terms of: (i) disease of humans; (ii) loss of meat products; and (iii) substantial reduction in the household income of farmers.

Measuring morbidity and mortality rates The first step in measuring the impact of infectious agents is to assess their frequency of occurrence and any causal association with specific symptoms and/or death [8,9]. Therefore, an initial distinction must be made between the occurrence of infection and the occurrence of disease (or symptoms) or death among infected individuals. The prevalence of human and pig infection has been estimated using serology [10]. It is important to distinguish tests based on antibody detection – which measure current and past infections, or even detect maternally derived antibody – from serological tests www.sciencedirect.com

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based on antigen detection, which usually represents a good measure of current infection. In most cases, however, the exact time of infection is not known. Serum antibody tests for both CE and AE are well established for individual patient diagnosis and mass screening [11]. For animal cysticercosis and echinococcosis infection, postmortem examinations can be used for diagnosis. For porcine cysticercosis, macrolesions on the tongue can also be used but the sensitivity of this method is no more than 50–55% [12]. Human metacestodosis can be diagnosed by symptomatology or imaging techniques. However, these techniques count only cases presenting for treatment and, therefore, underestimate the true incidence of disease. Imaging methods such as ultrasound and computed tomography (CT) scan have also been used to estimate the prevalence of echinococcosis and NCC, respectively [13]. To obtain better estimates of the risk (or cumulative incidence) of infection over time or the incidence of infection per person–year at risk, a cohort study is needed. In this design, a group of individuals initially free from infection is followed for a set period and new infections are identified. Alternatively, estimates could be obtained from a nested case-control study design [14]. These studies are costly and have not, to our knowledge, been conducted in human populations to estimate the incidence of infection with echinococcosis or cysticercosis. However, if transmission is thought to be stable over a period of time, the age-specific incidence of human symptomatic cases can be used as an estimate of the cumulative incidence of disease. All measures that rely on diagnostic tests will present a degree of error that must be accounted for to estimate the real frequency of infection [15]. Bayesian techniques can be used to adjust for multiple sources of error and have been used to estimate the adjusted prevalence of porcine cysticercosis [10]. With echinococcosis in livestock, the prevalence of infection increases with age at a rate that is dependent on the prevailing infection pressure [16]. Thus, the prevalence in livestock must be stratified by age to analyse potential production losses.

Decision-tree analyses Information about population frequencies of infection types and frequencies of associated diseases can be organized with decision-tree analysis [17] (Figure 2). As more information becomes available about a disease, the decision tree becomes more complicated. The decision tree can be complemented further by information about the average costs per case of each event represented by the branches. The average cost per case of each event is multiplied by the end probability of each branch. The sum of all these values corresponds to the average cost per case of the disease of interest (Box 1). For example, the average cost per case of measles in Canada was US$254 in 2000 [18] and the cost of cysticercosis in Eastern Cape Province (South Africa) was estimated to be US$14.9 million for a population of 7.1 million in 2004*. * H. Carabin et al., abstract 179, 53rd Annual Meeting of the American Society of Tropical Medicine and Hygiene, Miami Beach, November 2004.

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Figure 2. Decision-analysis tree for estimating the monetary burden of CE in humans in Tunisia. Circles correspond to chance nodes (defined by the probability or incidence rate of the event occurring) and triangles represent end nodes. The number at the top of each branch shows the proportion of each event occurring at that point in the tree. The total proportion of cases in each group is given at the right of each branch. The values at the end of each branch represent the prevalence of this particular end-point. In this example, the annual incidence rate of surgical CE is 0.015 per 100 person–years. Of these cases, 2.3% die. Thus, the overall probability of death in human surgical CE cases in Tunisia corresponds to 0.015% multiplied by 2.3%, or 0.000345%.

Animal health costs The direct cost of CE is the loss of edible offal (mainly liver) from infected animals. The diseased parts of the organ are trimmed or the whole organ might be condemned. In the case of cysticercosis, the whole carcass will typically be condemned at slaughterhouses [19]. However, most pigs in poor countries are home slaughtered [20] and some parts of the infected animals are sold, usually at a lower price [19]. For CE, the largest costs might be the indirect costs, including reductions in live weight-gain, milk yield, fertility rates and value of wool or other products. Because some of these deficits are estimated to be R10%, they represent the most serious CE-attributable losses to agriculture. These losses might be difficult to estimate because of limited numbers of controlled studies. Nevertheless, available data (for review, see Ref. [21]) suggest that these losses are important. In Jordan, indirect losses represent up to 70% of total livestock losses that are attributable to CE [22]. AE seems to have little economic effect on livestock, although there are reports of infections in farm animals [23]. Box 1. Monetary valuation of disease in both humans and animals The overall monetary burden of zoonoses can be calculated using the following expression [26] (Equation I): " !# S X A X X X Na;s ba;s px;a;s Cx;a;s (I) sZ1 aZ1

xZ1

This corresponds to the additive societal costs for all affected species (S) across all age groups (A). For the age–species-specific population of size (Na,s), with the age–species-specific annual incidence (ba,s), there is an age–species proportion (px,a,s) of infected individuals with symptoms x. The treatment and consequences of each of these symptoms have a monetary burden of Cx,a,s. Ideally, the whole spectrum of symptoms in humans and animals is included. In reality, data about all of these elements are rarely available. A societal approach has been used to try to value each symptom of echinococcosis and cysticercosis. This means that the monetary burden will include both direct and indirect costs in humans and animals. www.sciencedirect.com

Few studies to assess the monetary burden of swine cysticercosis have been conducted. In Mexico, economic losses due to porcine cysticercosis represent more than 50% of the national investment in swine production and, in Latin America, these losses have been estimated to be US$164 million [24]. Another estimate from Mexico, which assumes a prevalence of 1.55% of cysticercosis in pigs, led to an estimated annual loss due to condemnation of carcasses (total or partial) of US$43 310 524 [25]. There are no readily available data about the effect of T. solium on swine productivity in terms of growth, fertility and/or fecundity, and the evaluation of these would require controlled experimental studies. To calculate the animal health losses, a decision tree (Figure 2) can document different types of production deficit, and Monte Carlo sampling techniques represent the uncertainty associated with these data. This approach has shown overall animal health costs per year to be US$4 million to 11 million in Tunisia [26] and US$2.3 million to 6.3 million in Jordan [22]. Human health costs Direct costs associated with the diagnosis and treatment of patients can be calculated from a representative sample of case records and by costing the range of tests and treatments those patients receive. In health care systems in which the costs of diagnosis and treatment are funded privately, there will be charges for each intervention. In a publicly funded health service, the costs can be calculated from internal auditing procedures [27]. In endemic areas, 2–4% of the population might be affected by NCC [28]. In many poor countries, 10% of acute neurological cases are patients with NCC [29]. In Mexico, 5.4% of hospitalizations were due to NCC, and 10.3% of autopsies undertaken in the National Neurosurgical Institute reported pathological evidence of NCC [30]. Furthermore, NCC was the final diagnosis for 25% of individuals presenting for brain tumours [30]. According to data collected in Peru, there would be an estimated 23 512 to 39 186 inhabitants with symptomatic NCC

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among who 18 809 to 31 349 would be associated with seizures [13]. In 1982, it was estimated that the cost per NCC patient spent by public health institutions in Mexico was US$2173 [30]. In the USA, Roberts et al. [31] suggested that the total annual costs for hospitalization (US$6539 per case) and income loss (US$1416 per case) caused by NCC in the estimated 1100 cases per year would be US$8 750 490 per year. In Mexico, estimates of wage losses associated with NCC in 1982 were US$255 million annually [30]. Treatment costs in Brazil have been estimated to be approximately US$85 million [31]. Several studies in Asia and Africa have reported the costs of epilepsy but none has been published about the specific costs associated with NCC [32–34]. Most estimates do not include the indirect costs of lost productivity, which would require case-control or, preferably, cohort studies. In humans, it has been reported that 69–96% of symptomatic NCC cases have one or more seizures, and some will develop epilepsy. Epilepsy is a syndrome with considerable social, psychological, economical and physical impact on a community, and patients with epilepsy suffer from a decreasing quality of life according to the frequency of their seizures [35]. The mean annual cost for all medical services associated with one epilepsy case, estimated from a study conducted in northeastern USA, was US$9617 [36]. Mean direct costs of treating a case of human echinococcosis have been calculated to be US$524 in Jordan and US$10 215 in the UK [22,27]. The differences reflect the different wealth of the two nations and, hence, the costs of goods and services. Indirect costs might be considerable. These include the long-term ill health of individuals who have been treated for echinococcosis or who are affected by undiagnosed disease. The mortality rate for CE is generally reported to be 1–2% in cases that undergo surgical treatment but it is much higher for AE [1]. The case fatality rate of NCC has been recorded as 5.8% in California (USA) [37] and 6.7% in Oregon (USA) [38]. Fatal cases should be costed, and the value of human life has been calculated in several ways. The capital approach is the easiest to calculate and equates the value of life with the present value of future lost output (as proxied by earnings and other labour costs). Alternatively, the ‘willingness to pay’ approach [39] looks at the maximum amount of money that an individual is willing to pay for reduction of mortality risk. Uncertainty and sensitivity analyses When estimating the national societal burden of infection, one must find estimates of the average parameters of interest. If the estimates of these parameters from field studies are biased, adding a variance around the point estimate will not correct the bias and a correction (with uncertainty) based on judgment might need to be done. For example, cross-sectional studies tend to be conducted in endemic areas in which the prevalence estimates will represent the upper limit of the national prevalence. There is also a large amount of uncertainty related to the proportion of infected cases that will develop different symptoms or experience productivity losses. This is true for animal and human cases. Finally, the monetary values attributed to the diagnosis and treatment of each symptom www.sciencedirect.com

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and, for example, the daily salary of a farmer or homemaker in a low-income country that would be lost with a reduction in productivity are virtually always uncertain. Monte Carlo or Latin Hypercube methods can be used to model uncertain parameters. The distribution of these parameters must be selected with care. When there is no knowledge about a parameter, a uniform distribution can be selected. More-informative distributions can be selected when more data become available. For example, when the prevalence is estimated, a beta distribution can be used that takes into account the sample size and the numbers affected to model the true prevalence in the population. The overall monetary impact of CE in Tunisia was estimated to be US$14.7 million per annum [95% credible interval (CI) US$10.4 million to 19.0 million] using uniform probability distributions, and US$10.7 million (95% CI US$3.4 million to 18.8 million) when defined distributions were used [26]. In Jordan, the overall annual monetary impact of CE was estimated to be US$3.8 million (95% CI US$2.6 million to 6.5 million) using this analytical technique [22]. Even when there is a high degree of uncertainty, such an approach can be useful because the lower limits of the stochastic output of the cost estimates provide an upper limit to the allowable costs for a proposed control program. Non-financial approaches for estimating the burden of disease Non-financial methods have been developed to estimate human disease burden and are often referred to under the umbrella term ‘HALYs’ (health-adjusted life years) [40]. HALYs are summary measures of population health that enable the combined impact of morbidity and death to be considered simultaneously. These methods assess the morbidity of disease states so that comparisons between different diseases can be made. They avoid costing the effects of disease financially but can be used to prioritize resources to control human disease. However, the use of HALYs has several disadvantages (Box 2) and might not always be appropriate when estimating the societal burden of zoonoses. Disability-adjusted life years (DALYs) are the preferred disease-burden measure of the World Health Organization (WHO; http://www.who.int/en/) and were first constructed for the Global Burden of Disease (GBD) study [41,42]. To quantify DALYs, disability weights (Table 1) are assigned to each morbidity adjusted for their duration. For example, a healthy individual has a disability weight of 0 and no loss of DALYs, whereas a fatal condition has a weight of 1. The number of DALYs lost is calculated for the remaining life expectancy at the age of onset of the condition. The effectiveness of intervention strategies is calculated as being the number of DALYs estimated to occur because of a given condition in the absence of intervention minus the number of DALYs expected if control measures were implemented. However, this disregards additional benefits to agriculture of disease control (e.g. anthelmintic treatment of dogs reduces echinococcosis incidence in both humans and sheep). Nevertheless, if a total societal financial analysis is undertaken, the true cost effectiveness of control, in

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Box 2. A critical review of burden-assessment methods HALYs † Non-financial approaches ignore the agricultural impact of zoonotic infections. Although cost sharing can apportion burdens between the health and agricultural sectors, it needs a total financial analysis to enable allotment of HALYs and, hence, estimate cost sharing for costeffectiveness analysis [43]. † Disability classes (used in DALYs) do not provide adequate information for evaluating the impact or true burden of disease [49]. DALYs can undervalue disability in low-income countries. For example, the differences in quality of life for paraplegics in impoverished African countries compared with those in an industrialized nation are disregarded [50]. † Different types of HALY give different results. For example, there were differences in estimates of disease burden for five common medical conditions made using both DALYs and QALYs, and in rank order of the illnesses [51]. † HALYs do not give priority to those who are worse off, they discriminate against people with limited treatment potential and they do not account for qualitative differences in outcomes (e.g. life saving versus health improving) [40]. † A proportion of non-infectious or chronic conditions due to infections might not be recognized, thus underestimating the disease burden of infectious diseases [52].

terms of DALYs saved, can be estimated by implementation of cost sharing between sectors proportional to the overall benefit of each sector [43]. Neither human cysticercosis nor echinococcosis was evaluated in the GBD study. Research to address this deficit is now underway for human echinococcosis and, in the future, the burden of disease due to cysticercosis could be calculated using similar methodology. Quality-adjusted life years (QALYs) and DALYs are similar conceptually but use different scales. For example, QALYs rank 1 as perfect health and 0 as death and, thus, have a reverse scale compared with DALYs. Therefore, interventions would aim to minimize DALYs but maximize QALYs. Echinococcosis and DALYs The potential impact of disease on afflicted individuals must be taken into consideration when constructing a DALY. Two studies suggested that patients surgically treated for CE had a significant decrease in quality of life [22,27]. Furthermore, in Kyrgyzstan, patients presenting for treatment of CE had twice the unemployment rate of the general population [44]. The SF-12v2e health survey,

† The practice of discounting future life – implying that a life saved today will be worth multiple lives saved in the future – might be interpreted as bias and/or morally inappropriate [49]. † Weighting disabilities for infections with delayed symptoms might not be straightforward if based on cross-sectional data rather than cohort data. † Other limitations of DALYs can be found in Ref. [49].

Monetary burden † The cost of treating each end-component of the decision tree (see Figure 2 in main text) can be extremely variable, difficult to obtain and confounded by the widespread practice of bartering in poor countries. † The value of labour and health costs vary between different economies, whereas DALYs are a uniform measure and, therefore, should have the same value in poor and rich countries [40]. † Productivity losses for children, homemakers and the unemployed can be difficult to estimate. However, studies of lymphatic filariasis in India have estimated working-time losses and costed them as either wage losses or opportunity losses for non-economically active workers [53,54]. From these, total costs were estimated. † Conditions such as epilepsy involve stigmatization and social isolation [55]. Assigning a monetary value to this is not straightforward and might be captured more easily with HALY measures.

which is a generic measure of general health and wellbeing, has recently been used in China to evaluate the extent of morbidity due to previously undiagnosed echinococcosis [45]. The results demonstrate significant deficits in all health categories of subjects diagnosed with echinococcosis compared with healthy gender- and agematched controls. Further studies have demonstrated that subjects with echinococcosis are also more likely to be in a lower income bracket than cross-matched healthy controls [46]. These results justify the use of DALYs to calculate human disease burden. Disability weights were constructed for AE and CE based on reported disability weights for liver cancer: a disease of similar symptomatology. DALYs were then calculated using these weights, with the likely outcomes based on several different reports. The outcomes of the disease were assigned probabilities in a multinomial distribution according to the observed outcomes in the limited numbers of trials with chemotherapy (because free albendazole treatment was the only therapy option available to this population). Disability weights were assigned using a weight of 0.200 (Dutch weight for clinically disease-free cancer) for an improved outcome [47], a

Table 1. Examples of disability weights used to calculate DALYsa Degree of morbidity Healthy Limited ability to perform at least one activity in one of the following areas: recreation, education, procreation or occupation Limited ability to perform most activities in one of the following areas: recreation, education, procreation or occupation Limited ability to perform most activities in two or more of the following areas: recreation, education, procreation or occupation Limited ability to perform most activities in all of the following areas: recreation, education, procreation or occupation Requires assistance with instrumental activities of daily living such as meal preparation, shopping or housework Requires assistance with activities of daily living such as eating, personal hygiene or toilet use Dead a

Disability weight 0 0.096 0.220 0.400 0.600 0.810 0.920 1

The societal burden of disease, in terms of DALYs, takes into account the prevalence of disease, the duration (at the disability weight defined for that condition), age distribution and gender distribution of disease, and the life expectancy at the time of diagnosis. Data from Ref. [41].

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disability weight of 0.239 (the GBD weight for preterminal liver cancer) for those with stable disease, and a disability weight of 0.809 (the GBD weight for terminal liver cancer) for disease that worsened. Fatal cases were assigned a disability weight of 1. In the calculation of DALYs lost, stochasticity was introduced because of the uncertainty of assigning disability weights and the uncertainty in the point prevalence estimates. Monte Carlo sampling techniques were used (see earlier). Using these methods, the total numbers of DALYs lost because of echinococcosis were estimated to be 50 933 (95% CIs 41 995 to 61 026) in Shiqu county (China). This consisted of w32 978 (95% CIs 25 019 to 42 422) DALYs lost because of AE and w17 955 (14 268 to 22 1238) DALYs lost because of CE, and suggests an average of w0.81 DALYs lost per person in Shiqu County [45]. By comparison, the GBD study suggested that the average number of DALYs lost per person because of infectious and non-infectious diseases was w0.18 in China as a whole. This demonstrates that, in localized highly endemic areas, echinococcosis can be among the leading causes of illness. In addition, using a cost-sharing approach for controlling echinococcosis, the cost per DALY averted in China – attributable to the public health sector – is approximately US$10–12 [46], which is within the most cost-effective band of the WHO of less than US$25 per DALY averted [48]. In addition to these DALYs averted, the costs of intervention to the livestock sector are, at most, only 25% of the potential economic benefits to animal health [46]. Concluding remarks Cysticercosis and echinococcosis contribute to high levels of human morbidity and some mortality, and livestock production losses in many parts of the world. Control of these zoonoses should be prioritized because they are preventable diseases. There are examples of effective control of these diseases; porcine cysticercosis has been eliminated from parts of the industrialized world, and echinococcosis has been eliminated from Iceland, Tasmania and New Zealand. In addition, recent studies suggest that the control of echinococcosis could be extremely cost effective in highly endemic areas such as China. In many endemic areas, a lack of accurate estimates of disease burden hampers the setting of priorities for control of infectious diseases because of finite resources. Progress in assessing the burden of echinococcosis and cysticercosis has been reviewed and some difficulties in burden measurement have been highlighted. In this article, we have also indicated where more research is needed to improve the estimates of disease burden of parasitic zoonoses in both humans and animals. Acknowledgements We thank INTAS (INTAS 01 500, 01 505 and 03 51 5661), the NIH, the US National Science Foundation (1R01TW01565–01) and the WHO for their financial support. We also thank Dirk Engels, Meghan Majorowski and Theodore Nash for helpful discussions.

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