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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 . 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 . 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 .
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 : firstname.lastname@example.org)
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 . 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 . 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 . 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 http://www.pceo.org/parasitecea.html.
# 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 . Hospitalization rates were
. 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 . 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 . 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 . 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) . 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 . 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
. 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 . 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.  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 .
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
. 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-
. 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.
Finally, we were unable to evaluate all possible
Immigrants from Eastern Europe, Asia, Africa,
screening and treatment strategies. Strategies for
Latin America, and the Middle East are all at risk of
selecting persons at risk for S. stercoralis include stool
parasitosis, but there is considerable variability even
ova and parasite screening, obtaining eosinophil
within these groups. The ideal management of para-
counts , asking patients about rural or urban
sitic infections in immigrant populations might
residence , screening for the presence of asthma-
consider the population’s risk of infection with S. ster-
like respiratory symptoms  and serological
coralis relative to other parasites. Many institutions,
screening tests . While stool screening examina-
such as most federal refugee health clinics, have these
tions  and treatment contingent on known eosino-
data. By combining our analysis with nation-speciﬁc
phil counts are more expensive and less eﬀective than
data on the prevalence of S. stercoralis infections,
presumptive treatment, there are insuﬃcient data to
providers should be able to maximize the quality and
evaluate the other options. Serological screening is
quantity of life of their immigrant populations within
much more sensitive than stool screening, however
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