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The cost-effectiveness of ivermectin vs. albendazole in the presumptive treatment of strongyloidiasis in immigrants to the united states

Epidemiol. Infect. (2004), 132, 1055–1063.
The cost-effectiveness of ivermectin vs. albendazole in thepresumptive treatment of strongyloidiasis in immigrantsto the United States P. M U E N N I G 1*, D. P A L L I N 2, C. C H A L L A H 3 A N D K. K H A N 4 1 Department of Health Policy and Management, Mailman School of Public Health, Columbia University,NY, USA2 Department of Emergency Medicine, Brigham and Women’s Hospital, Harvard Medical School, MA, USA3 Department of Community Health and Social Medicine, CUNY Medical School, NY, USA4 Inner City Health Research Unit, St. Michael’s Hospital, University of Toronto, Canada The presumptive treatment of parasitosis among immigrants with albendazole has been shown tosave both money and lives, primarily via a reduction in the burden of Strongyloides stercoralis.
Ivermectin is more effective than albendazole, but is also more expensive. This coupled withconfusion surrounding the cost-effectiveness of guiding therapy based on eosinophil counts hasled to disparate practices. We used the newly arrived year 2000 immigrant population as ahypothetical cohort in a decision analysis model to examine the cost-effectiveness of variousinterventions to reduce parasitosis among immigrants. When the prevalence of S. stercoralis isgreater than 2 %, the incremental cost-effectiveness ratios of all presumptive treatment strategieswere similar. Ivermectin is associated with an incremental cost-effectiveness ratio of $1700 perQALY gained for treatment with 12 mg ivermectin relative to 5 days of albendazole when theprevalence is 10 %. Any presumptive treatment strategy is cost-effective when compared withmost common medical interventions.
deciding among these options include the fact thatintestinal parasites are common in new immigrant The worldwide burden of intestinal parasitic disease populations, anti-parasitic agents are effective, safe, exceeds 3 billion persons [1]. In 2000, approximately and well tolerated, and stool examinations for para- 28.4 million foreign-born persons resided in the sites are labour intensive, costly, and highly insensi- United States, with most originating from countries tive at identifying infection [3, 4].
where intestinal parasites are endemic [2]. When evalu- Among intestinal parasites that are common in new ating new immigrants for parasitic infections, phys- immigrant populations, S. stercoralis results in the icians may choose watchful waiting, use eosinophilia greatest medical costs, morbidity, and loss of life [4].
as a method to identify high-risk patients, screen for This parasite is capable of autoinfection, a phenom- parasitosis using one or more stool examinations, enon in which the parasite completes its entire life- or treat presumptively. Factors to consider when cycle within the host, thus leading to multiplegenerations of new organisms and persistent infection * Author for correspondence : Dr P. A. Muennig, Assistant for decades [5, 6]. In contrast, most parasites have a Professor, Mailman School of Public Health, Columbia University, more limited lifespan or rarely result in serious illness 600 W. 168th St., 6th Floor, New York, NY 10032, USA.
(Email : or death. While the majority of persons infected with S. stercoralis either remain asymptomatic or develop the reader of the effect incorrect estimates of a vari- mild illness, those who subsequently become im- able or differences in infection rates between various munocompromised are at high risk of developing immigrant groups might have on the incremental hyperinfection syndrome, a life-threatening dissemi- cost-effectiveness ratios. For simplicity, all foreign- nated infection with a mortality rate over 50 % despite born persons are referred to as immigrants, regardless A prior cost-effectiveness analysis found that pre- sumptive treatment of immigrants with albendazolecould save lives and money ; basing treatment de- cisions on stool analysis was more expensive and less The prevalence of parasitosis among immigrants to effective than presumptive treatment [4]. This analysis the United States was obtained from the medical included various parasites, and found that both gains literature and from refugee and immigrant health in quality-adjusted life and economic benefits hinged clinics [10–16]. The prevalence data we used were on the eradication of S. stercoralis, the organism re- based on a standard single stool ova and parasite sponsible for the hyperinfection syndrome. The examination, which has an average test sensitivity analysis did not evaluate the practice of basing clinical value of approximately 25 % [17, 18]. The adjusted decisions on eosinophil counts and did not evaluate prevalence of S. stercoralis among immigrants was alternative presumptive treatment modalities.
then calculated by dividing the proportionate preva- Ivermectin, a newer anti-parasitic agent, is more lence value for a given immigrant population by the effective against S. stercoralis than albendazole and is administered as a single dose, but is narrower in itsspectrum of activity and considerably more expensivethan albendazole. Therefore, there is uncertainty sur- rounding the optimal medication for the presumptivetreatment of this parasite in immigrants, especially To calculate life expectancy for immigrants, we first among those at high risk for strongyloidiasis.
generated abridged life tables using data from the We compare the cost-effectiveness of treatment National Centre for Health Statistics for year 2000.
with single-dose ivermectin with two commonly em- Because immigrants are born outside the United ployed regimens of albendazole as well as treatment States by definition, these life tables reflect life ex- based on eosinophil counts. Immigrants are often screened for anaemia using a complete blood count (CBC) with differential. Information on a patient’s Classification of Disease, 9th Revision (ICD-9) code eosinophil count is, therefore, available to clinicians 127.2] were obtained from the 1979–1998 combined at no cost ; thus, screening for eosinophilia is intuit- mortality data file for California and New York – two ively cost-effective. We, therefore, also report the states with large immigrant populations in which S.
cost-effectiveness of treating immigrants with known stercoralis is not endemic [19]. The probability of eosinophilia (defined as an absolute eosinophil count >500 or percentage of total leukocytes >5%), andprovide a comparison to the other treatment strat- where D=deaths due to S. stercoralis, I=the 1990immigrant population of these states, and P=the overall prevalence of parasitosis in immigrants [20]. In Our study design adhered to the recommendations of this case, the 1990 immigrant population was used the Panel on Cost-Effectiveness in Health and because it fell approximately mid-point between in- Medicine [8, 9]. All relevant societal costs were in- itial and final years of the death data file.
cluded, and future costs were discounted at a rate of The number of hospitalizations due to S. stercoralis 3 %. Since there is considerable uncertainty sur- was obtained using 1996–2000 data from the State- rounding the real world value for various parameters wide Planning and Regional Cooperative System used in the analysis, we employed various sensitivity (SPARCS), a dataset containing billing, demographic, analysis techniques. The sensitivity analysis informs and diagnosis data for all civilian hospitalizations Table 1. Selected parameters included in the decision analysis model* Cost of 200 mg b.i.d albendazole (5 days) Cost of 200 mg b.i.d. albendazole (3 days) * For a full list of parameters, including age-specific mortality rates, visit
# Among infected persons.
$ Used to determine threshold cost. Medications are available overseas for less than low value.
· Annual risk among infected persons.
in New York State [21]. Hospitalization rates were [23]. Domains include sensation, mobility, cognitive function, self-care, and pain among others. Inputswere obtained by asking two infectious disease experts familiar with S. stercoralis to rate each scale.
where H is the average annual number of hospital-izations for S. stercoralis from 1996 to 2000, I is the 1998 immigrant population, and P is the prevalence ofS. stercoralis.
Most efficacy trials of anti-parasitic agents are con- The number of outpatient visits to health-care ducted overseas and are complicated by the potential providers was calculated from Medicaid claims data for re-infection and the use of insensitive tests to from 1992 to 1996 [22]. More recent data were un- identify infection. Determination of the sensitivity of available due to a 1996 federal law preventing recent eosinophilia for S. stercoralis infection is limited by immigrants from using most Medicaid services. The the lack of a gold standard comparator and a paucity mean annual number of outpatient visits was divided of studies. Finally, since eosinophilia occurs in the by the proportion of immigrants receiving Medicaid presence of many parasitic infections (as well as other medical conditions), the specificity of the test is de- Estimates of the Health-related quality of life pendent on the prevalence of other conditions in a (HRQL) scores for various health states were derived given cohort. We, therefore, used mean values for using the Health Utilities Index 2 (HUI-2), which is a sensitivity and specificity for eosinophilia and efficacy multi-attribute health status classification system used estimates for albendazole and ivermectin from the to translate dimensions of a disease into a quality medical literature and tested these in a broad sensi- adjusted life years (QALY)-compatible HRQL score tivity analyses (see Table 1) [24–31].
Table 2. Assumptions and issues in deriving parameter estimates . The 1990 immigrant population is equal to the midpoint 1979–1998 population. It was necessary to aggregate mortality data for S. stercoralis over many years to obtain a large number of deaths . Vital statistics and hospitalization data correctly tabulate mortality and hospitalization rates due to S. stercoralis. Most cases are not likely to be identified, resulting in undercounts of deaths and hospitalizations. This assumption was tested in a broad sensitivity analysis . The exclusion of parasites other than S. stercoralis will not substantially alter cost-effectiveness ratios in populations . We examined only costs and benefits associated with screening and treating S. stercoralis. Unlike albendazole, ivermectin does not treat hookworm, G. lamblia, O. vivirini, or T. solum. However, the mortality due to G. lamblia isextremely low, O. vivirini is rare, and considerable debate exists over whether albendazole would produce benefits forpersons infected with T. solum . The HRQL of uninfected immigrants is 1.0. We tested this assumption in a sensitivity analysis varying from the mean HRQL of native-born persons to 1.0. Clinicians will use 12 mg ivermectin to treat patients with eosinophilia among populations at risk for S. stercoralis. S. stercoralis is the most dangerous parasite and ivermectin is the most effective medication. Some infectious disease specialists may opt to use a higher dose and spaced dosing to maximize efficacy, which would decrease thecost-effectiveness of this option HUI-2 does not include costs due to lost productivity ;however, we chose to exclude these costs because we The cost of ivermectin was based on a single dose of felt that they would be small relative to the actual cost 12 mg (approximately 200 mg/kg for a 60 kg adult), and the cost of albendazole was based on a twice-dailydose of 200 mg for either 3 or 5 days. Each cost was obtained from the 2000 Red Book, which reportsaverage wholesale prices for medications [32]. The We developed a Markov model using DATA pro- median cost of medical visits were estimated using fessional (version 4.0, TreeAge Software, Williams- 2000 data from the Medical Care Expenditure Panel town, MA, USA) that compared : (1) treating all Survey (MEPS), an annual survey of approximately immigrants with 200 mg albendazole twice a day for 40 000 households that is representative of the US either 3 days or 5 days, (2) treating all immigrants population as a whole. We used the median cost with 12 mg ivermectin in a single dose (approxi- since data for S. stercoralis were not available and mately 200 mg/kg for a 60 kg adult), (3) treating only since a medical visit for this condition is likely those immigrants with documented eosinophilia with to fall in the middle range of duration. Details of 12 mg ivermectin, and (4) watchful waiting. In our the survey, including imputation methods, are avail- model, subjects are exposed to the annual age-specific able from the Agency for Health Research and probability of death for immigrants due to all causes ; the crude mortality rate for S. stercoralis infection The median cost of a hospitalization for S. ster- was subtracted for uninfected or successfully treated coralis was obtained using charge data from SPARCS subjects. Each surviving subject is assigned a dis- for admissions with ICD-9 code 127.2 listed as a pri- counted HRQL value or cost for each year of life.
mary diagnosis [21]. These figures were then adjusted Burial costs are incurred whenever subjects die. All using the cost-to-charge ratio for ‘ other infectious assumptions of the analysis are listed in Table 2 and and parasitic diseases ’ (Diagnosis-Related Group all parameter values are listed in Table 1.
423, which includes helmenthiasis), which was derived In the model, patients are assigned to a state of from the Centers for Medicare and Medicaid Services being either infected with S. stercoralis or uninfected.
(CMS) [34]. This cost-to-charge ratio was calculated In treatment arms, the probability of infection is by dividing the amount reimbursed by CMS by equal to the product of the parasitic prevalence and the total charges to CMS. Burial costs were added the efficacy of the medication administered. In the for all deaths, regardless of cause, since burial costs eosinophilia arm, subjects are allocated to receive associated with premature death were expected to treatment or no treatment by infection status using be relevant after discounting future costs [35]. The the prevalence, sensitivity, and specificity of the test.
Table 3. Cost, incremental cost, effectiveness, incremental effectiveness, and incremental cost-effectiveness perQALY gained of all strategies evaluated at various prevalence ratios (negative values) * Relative to watchful waiting.
# Dominated strategies are both more expensive and less effective than others.
The variables used in our analyses were subjected to This option is associated with an incremental cost- a Monte Carlo simulation and to a series of one-way effectiveness ratio of $632 relative to 3 days of alben- and two-way sensitivity analyses. In a one-way dazole and $393 relative to watchful waiting. Optimal analysis, all variables are held constant but one. In a coverage of S. stercoralis can be achieved with iver- Monte Carlo simulation, values for all variables are mectin. Presumptive treatment with 12 mg ivermectin sampled from a statistical distribution. In our Monte in a single dose was associated with a cost of $1700 Carlo simulation, we used a triangular distribution per QALY gained relative to treatment with 5 days [36]. In this distribution, the base-case estimate is of albendazole and $564 per QALY gained relative entered as the most likely value, and the likelihood to watchful waiting. Regardless of the prevalence, of values between this value and the high and low value the strategy of basing treatment on previously known eosinophil results (i.e. excluding the cost ofa complete blood count with differential) was bothmore expensive and less effective than other options Table 3 presents the results of the cost-effectiveness The Figure presents mean effectiveness and in- analysis at a 2, 10, and 20 % prevalence of S. stercor- cremental cost-effectiveness ratios of the treatment alis infection. When the prevalence of S. stercoralis is strategies at various prevalence ratios of S. stercoralis 10 % (a rate commonly seen in mixed refugee screen- infection. Presumptive treatment of immigrants with ing settings), presumptive treatment with 200 mg ivermectin increases incremental cost-effectiveness albendazole, twice a day over 3 days, was associated alongside prevalence ratios, with maximal cost-effec- with an incremental cost-effectiveness ratio of $314 tiveness when prevalence ratios are greater than per QALY gained relative to watchful waiting. The 10–12 %. Over the range of prevalence values ex- presumptive treatment of immigrants at risk of para- amined, none of the presumptive treatment strategies sitosis with 5 days of albendazole may be desired to ensure better coverage of S. stercoralis as well as All variables listed in Table 1 were tested in one- other parasitic infections such as Giardia lamblia.
way and Monte Carlo sensitivity analyses. Changes in commonly seen in immigrant groups, the cost of pre- sumptive treatment is significantly less than the cost of treatment of essential hypertension in 20-year-oldmales vs. no treatment, or the nicotine patch for 25- year-old smokers vs. no treatment [37]. While the incremental cost-effectiveness of ivermectin was de- pendent upon the underlying prevalence of S. ster- coralis infection, no one strategy clearly dominated In evaluating the use of eosinophil counts to guide presumptive treatment, we used a high estimate of test sensitivity, a generous specificity, and did not include the cost of a CBC with differential in the analysis. All of this increases the likelihood of a find- ing in favour of incorporating eosinophilia data ; nonetheless the strategy was dominated. Though the positive predictive value of eosinophilia increases with increasing parasite prevalence, this strategy becomes more costly and less effective than the other options as prevalence increases. This is attributable to increasing false-negative test results. While the test has a higher 0·02 0·12 0·22 0·32 0·42 0·52 0·62 0·72 0·82 positive predictive value when all intestinal parasitesthat cause eosinophilia are considered together, other Fig. Effectiveness and incremental cost-effectiveness of thestrategies under evaluation. Ivermectin is the most effective parasites are infrequently fatal and generate fewer strategy across the prevalence ratios of S. stercoralis (a).
costs than S. stercoralis. It is, therefore, unlikely that –&–, Ivermectin (1 day) ; ––, albendazole (5 days) ; –m–, adding other intestinal helminths to the model (with albendazole (3 days) ; –$–, eosinophil ; –––, nothing.
concomitant improvements in specificity) would However, it is more expensive than other strategies (b).
greatly improve the incremental cost-effectiveness of Dominated options are not shown in panel (b).
The prevalence of S. stercoralis varies considerably the efficacy of the regimens over plausible values by region of the world and the subpopulation sam- exerted only a moderate effect on the relative ranking pled. For example, Gyorkos et al. [38] conducted a of each regimen, and changes in other variables had serosurvey for S. stercoralis among Southeast Asians no substantive effect on strategy rankings. Notable immigrating to Canada and reported that Cambo- analyses that exerted little effect on the model include dians had a seroprevalence of 76.6 %, Laotians had a the discount rate, the cost and probability of medical seroprevalence of 55.6 %, and Vietnamese had a events, and state-specific HRQL scores. In Monte seroprevalence of 11.8 %. Serology indicates both Carlo analyses, all three presumptive treatment active and previous infections and may produce an strategies overlapped considerably. Any given strat- overestimate of the prevalence of S. stercoralis.
egy exceeded $50 000 in less than 1 % of all trials.
Nonetheless, these numbers underscore the hetero-geneity of infection rates among different groups ;predominately high-risk refugees screened with 1–3 stool ova and parasite examinations in Texas and In our analysis we found that ivermectin was a more Minnesota have an average uncorrected infection rate effective strategy, but was also an incrementally more of 1.8–4 % (or approximately 3–12 % after correction expensive (per QALY gained) than albendazole for for the sensitivity of the stool ova and parasite the treatment of S. stercoralis infections in new im- examination) [39, 40]. We demonstrate that pre- migrants to the United States. The additional expense sumptive treatment is cost-effective across a wide of ivermectin was $1700 per QALY gained, a very range of prevalence values. Clinics that treat refugees small cost relative to most other medical interven- and immigrants may wish to use our data to tailor tions in the United States. Across prevalence ratios treatment after considering the prevalence of infection in the population they treat, the mix of parasites in the the cost and positive predictive value of this option population they treat, and budgetary concerns.
render it an unlikely addition to the arsenal of cost- For instance, albendazole has a broader spectrum effective preventive modalities. One option in need of of action and includes activity against hookworm and evaluation is screening based on urban or rural resi- G. lamblia, as well as certain flatworms. Both iver- dence in the country of origin. Knowledge of the prior mectin and albendazole provide coverage of other probability of infection could greatly reduce the infections as well, including Ascaris lubricoides, number of uninfected persons who would otherwise Trichuris trichiura, and certain forms of filariasis [41].
While estimating the morbidity or costs associated Alternative treatment options exist as well. For in- with administering albendazole for some of these stance, ivermectin has been combined with albenda- organisms is limited by inadequate data, short-term zole in some international studies [47, 48]. We did not clinical and public health benefits may be realized evaluate this approach as a policy due to concerns from the presumptive treatment of immigrant and surrounding the possibility of drug interactions.
refugee populations using broad spectrum anti- It is also prudent to limit presumptive treatment to parasitic medications. However, the elimination of those for whom the drugs have demonstrated safety.
S. stercoralis should be prioritized in populations Ivermectin and albendazole are pregnancy category C in whom this parasite is prevalent given its potential for life-threatening illness and capacity for auto- The present analysis improves upon an earlier study [4]. In addition to improving mortality and hospital- Our inability to capture the costs and benefits of ization rate estimates by using multiple years of data, presumptively treating these other parasites is a limi- it uses a Markov model and includes additional pre- tation of this study. Including them would probably ventive strategies. Using a deterministic model and improve the incremental cost-effectiveness of 5 days discounted lifetime probabilities of hospitalization of albendazole relative to 3 days of albendazole and death, that study biased all variables against treatment or ivermectin. It would also slightly im- presumptive treatment, evaluated multiple parasites, prove the incremental cost-effectiveness of eosinophil and found cost savings associated with presumptive screening. Another limitation is the use of billing and treatment with 5 days of albendazole. The cost vital-statistics data to capture the morbidity and savings realized by that study were attributable to mortality associated with S. stercoralis. Contributing slightly higher hospitalization and mortality estimates to misclassification bias in datasets is clinicians’ un- for S. stercoralis (due to random error associated familiarity with the disease and the lack of a sensitive with the use of a single year of data) and the inclusion diagnostic test. Even tuberculosis, a condition that of four parasites rather than one. Though the present is probably more familiar to clinicians, is correctly analysis demonstrates that treatment may be associ- classified on death certificates just 34 % of the time ated with costs, it should be emphasized that the num- [42]. Misclassification bias probably results in an ber of deaths and hospitalizations in the real world underestimate of medical visits and deaths due to this are likely to be substantially higher than reported in parasite but would not substantially affect the rank national datasets. Therefore, the costs averted by treatment are likely to be substantially higher.
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