Albendazole Therapy and Enteric Parasites in United States Bound Refugees

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1 T h e n e w e ngl a nd j o u r na l o f m e dic i n e original article Albendazole Therapy and Enteric Parasites in United States Bound Refugees Stephen J. Swanson, M.D., Christina R. Phares, Ph.D., Blain Mamo, M.P.H., Kirk E. Smith, D.V.M., Ph.D., Martin S. Cetron, M.D., and William M. Stauffer, M.D. A BS TR AC T From the Epidemic Intelligence Service (S.J.S.) and the Centers for Disease Control and Prevention (C.R.P., M.S.C., W.M.S.) both in Atlanta; the Minnesota Department of Health, St. Paul (S.J.S., B.M., K.E.S.); and the Hennepin County Medical Center (S.J.S.) and the University of Minnesota (S.J.S., W.M.S.) both in Minneapolis. Address reprint requests to Dr. Swanson at the Department of Pediatrics, Hennepin County Medical Center, 701 Park Ave., G7, Minneapolis, MN 55415, or at N Engl J Med 2012;366: Copyright 2012 Massachusetts Medical Society. Background Beginning on May 1, 1999, the Centers for Disease Control and Prevention (CDC) recommended presumptive treatment of refugees for intestinal parasites with a single dose of albendazole (600 mg), administered overseas before departure for the United States. Methods We conducted a retrospective cohort study involving 26,956 African and Southeast Asian refugees who were screened by means of microscopical examination of stool specimens for intestinal parasites on resettlement in Minnesota between 1993 and Adjusted prevalence ratios for intestinal nematodes, schistosoma species, giardia, and entamoeba were calculated among refugees who migrated before versus those who migrated after the CDC recommendation of presumptive predeparture albendazole treatment. Results Among 4370 untreated refugees, 20.8% had at least one stool nematode, most commonly hookworm (in 9.2%). Among 22,586 albendazole-treated refugees, only 4.7% had one or more nematodes, most commonly trichuris (in 3.9%). After adjustment for sex, age, and region, albendazole-treated refugees were less likely than untreated refugees to have any nematodes (prevalence ratio, 0.19), ascaris (prevalence ratio, 0.06), hookworm (prevalence ratio, 0.07), or trichuris (prevalence ratio, 0.27) but were not less likely to have giardia or entamoeba. Schistosoma ova were identified exclusively among African refugees and were less prevalent among those treated with albendazole (prevalence ratio, 0.60). After implementation of the albendazole protocol, the most common pathogens among 17,011 African refugees were giardia (in 5.7%), trichuris (in 5.0%), and schistosoma (in 1.8%); among 5575 Southeast Asian refugees, only giardia remained highly prevalent (present in 17.2%). No serious adverse events associated with albendazole use were reported. Conclusions Presumptive albendazole therapy administered overseas before departure for the United States was associated with a decrease in the prevalence of intestinal nematodes among newly arrived African and Southeast Asian refugees n engl j med 366;16 nejm.org april 19, 2012

2 Albendazole and Enteric Parasites A pproximately 25% of the world s population is infected with intestinal helminths. 1 These neglected tropical infections disproportionately affect the world s least privileged and most vulnerable populations and are among the most common medical conditions in refugees. 2-4 Among resettled refugees, intestinal helminths can persist for years and are associated with increased risks of illness and death. 5-7 The United States resettles up to 80,000 refugees annually. Before resettlement, refugees undergo mandated health screenings. The Centers for Disease Control and Prevention (CDC) defines, oversees, and monitors these health screenings in accordance with the Refugee Act of ,9 In 1997, the CDC and the International Organization for Migration performed enhanced medical assessments of 390 Barawan Somali refugees awaiting resettlement in refugee camps in Kenya. 10,11 Among these refugees, 38% had a pathogenic intestinal parasite and 25% had multiple infections. The overall prevalence of intestinal parasites detected by means of stool examination among resettled African and Asian refugees has been reported to range from 14% to 64%, depending on the population and method of testing. 7,12-17 Because of the high prevalence of parasitic infections among refugee populations awaiting resettlement, on May 1, 1999, the CDC initiated presumptive predeparture treatment programs for malaria and intestinal parasites. 18,19 Presumptive mass treatment of refugees for intestinal parasites involved a single oral 600-mg dose of albendazole, administered within 3 days before departure as directly observed therapy. Pregnant women, children younger than 2 years of age, and persons with known cysticercosis or an unexplained seizure disorder were excluded. We retrospectively evaluated the effect of this overseas public health intervention on the prevalence of intestinal parasites among refugees arriving in the United States. Me thods Minnesota Screening Protocol and Reporting The Refugee Health Program of the Minnesota Department of Health has standardized guidelines for the medical examination of newly arrived refugees. Refugees are screened within 90 days after arrival, with the results documented in a centralized database. We retrospectively analyzed examination data on all 37,608 refugees who resettled in Minnesota between January 1, 1993, and December 31, The Minnesota Department of Health guidelines recommend the collection of three stool specimens on separate mornings for ova and parasite examination. 21 Three county public health clinics (in Minneapolis, St. Paul, and Olmsted) performed more than 75% of refugee health assessments. These clinics operated according to established screening protocols that did not change over time and that required a minimum of two stool samples per refugee. Two reference laboratories evaluated more than 75% of all stool specimens obtained from newly arrived refugees. Both laboratories performed ova and parasite examinations with the use of stool concentration techniques and standard light microscopy. Special stains (e.g., acid-fast and silver) were not routinely used. Since 1993, forms for refugee health assessment data have included documentation of stool tests showing intestinal infections with nematodes (Ascaris lumbricoides, hookworm [Necator americanus and Ancylostoma duodenale], whipworm [Trichuris trichiura], and Strongyloides stercoralis), giardia, entamoeba complex (Entamoeba histolytica, E. moshkovskii, and E. dispar), and schistosoma species. Exclusions and Definitions All refugees who were 2 years of age or older, were not pregnant at the time of treatment, originated in Southeast Asia or sub-saharan Africa, and submitted at least one stool specimen during the study period were included in the analysis. Children younger than 2 years of age and pregnant women were excluded because presumptive therapy initially was not recommended for these groups. The albendazole-treatment protocol excluded refugees with known cysticercosis or an unexplained seizure disorder because of the risk of adverse neurologic effects from a cysticidal agent. Because the overseas treatment recommendation was issued on May 1, 1999, refugees departing for the United States between January 1, 1993, and April 30, 1999, were categorized as untreated, and refugees departing between May 1, 1999, and December 31, 2007, were categorized as albendazole-treated. Additional health screening data (e.g., medications received overseas and body-mass in- n engl j med 366;16 nejm.org april 19,

3 T h e n e w e ngl a nd j o u r na l o f m e dic i n e dex) were not reported to the Minnesota Department of Health. Statistical Analysis Prevalence ratios and 95% confidence intervals were calculated with the use of generalized-estimating-equation log-binomial regression models with robust variance estimates to adjust for clustering according to family. Separate models were constructed for each parasite; in adjusted analyses, each model included the refugee s departure date (before vs. after the CDC recommendation for presumptive predeparture treatment a proxy for untreated vs. albendazole-treated refugees), sex, age (2 to 14 years vs. 15 years), and region or country of national origin. The model for schistosoma infection excluded all refugees from Southeast Asia, since no cases were documented in this population. Data were analyzed with the use of SAS software, version 9 (SAS Institute). R esult s Characteristics of the Study Population From 1993 through 2007, a total of 37,608 refugees from sub-saharan Africa or Southeast Asia resettled in Minnesota. Further analyses excluded as ineligible 1386 children younger than 2 years of age (3.7%) and 621 pregnant women (1.7%). Among the remaining 35,601 refugees, no health assessment data were reported to the Minnesota Department of Health for 6033 refugees (17.0%), and 2612 (7.3%) did not provide a stool sample. The proportion of refugees with complete data (i.e., those who submitted 1 stool sample) differed according to the departure period. Before the recommendation for presumptive predeparture treatment, only 4370 of 7865 untreated refugees (55.6%) submitted 1 stool specimen or more; after the recommendation, 22,586 of 27,736 albendazole-treated refugees (81.4%) did so (see Fig. 1 in the Supplementary Appendix, available with the full text of this article at NEJM.org). Among the 26,956 refugees for whom complete data were available, 14,086 were male (52.3%) and 8125 were children 2 to 14 years of age (30.1%). The median age was 19 years (interquartile range, 13 to 30). The median time between arrival and the first clinic visit was 37 days (interquartile range, 22 to 60). A total of 18,666 refugees were from sub-saharan Africa (69.2%), and 8290 refugees were from Southeast Asia (30.8%). The most common countries of origin were Somalia (43.0%), Laos (22.1%), Ethiopia (12.2%), Liberia (10.1%), Vietnam (4.5%), and Burma (Myanmar) (4.1%). The remaining 3.9% of refugees originated from the sub-saharan African countries of Benin, Burundi, Cameroon, Ivory Coast, Democratic Republic of Congo, Eritrea, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Niger, Nigeria, Rwanda, Senegal, Sierra Leone, Sudan, Togo, and Uganda. Demographic characteristics differed according to departure period; refugees who departed on or after May 1, 1999, were older and more likely to have arrived from Africa than were refugees who departed before May 1, 1999 (Table 1). Prevalence of Intestinal Infections Among the 26,956 refugees who provided a stool sample, 4897 (18.2%) had at least one intestinal parasite and 436 (1.6%) had multiple parasites (Table 2). Protozoal infections were identified in 2763 refugees (10.3%), nematodes in 1975 (7.3%), and schistosoma species in 406 (1.5%). Among the 4370 untreated refugees, 20.8% had at least one stool nematode and 3.1% had multiple nematodes (Fig. 1). The most frequent pathogen was hookworm (9.2%), followed by trichuris (8.5%), ascaris (4.1%), and strongyloides (2.6%). Among 22,586 albendazole-treated refugees, only 4.7% had one or more stool nematodes and only 0.2% had multiple nematodes. Trichuris was most common, with a prevalence of 3.9%, whereas the individual prevalences of hookworm, ascaris, and strongyloides were 0.4% or less. Giardia was detected in 10.1% of untreated refugees and 8.5% of albendazoletreated refugees. In contrast, entamoeba complex (E. histolytica, E. moshkovskii, and E. dispar) was more prevalent among albendazole-treated refugees (1.9%) than among untreated refugees (0.3%). The unadjusted prevalence of intestinal parasites differed according to region (Table 3). Schistosoma ova were detected exclusively in African refugees, with a prevalence of 5.6% among those who were untreated and 1.8% among those who were treated with albendazole. Southeast Asian refugees were more likely than African refugees to be infected with ascaris (1.5% vs. 0.6%, P<0.001), hookworm (4.0% vs. 0.9%, P<0.001), strongyloides (1.8% vs. 0.3%, P<0.001), and giardia (15.4% vs. 5.9%, P<0.001) but were less likely to have trichu n engl j med 366;16 nejm.org april 19, 2012

4 Albendazole and Enteric Parasites Table 1. Characteristics of Refugees in Minnesota, According to Departure Date (before or after the Recommendation of Empirical Treatment with Albendazole), * Characteristic Sex Age Region Included in Analysis (N = 4370) Refugees Who Departed before Recommendation (N = 7865) Excluded Because of Missing Data (N = 3495) Prevalence Ratio, Included vs. Excluded (95% CI) Included in Analysis (N = 22,586) no. (%) no. (%) Refugees Who Departed after Recommendation (N = 27,736) Excluded Because of Missing Data (N = 5150) Female 2083 (47.7) 1718 (49.2) 10,787 (47.8) 2470 (48.0) Prevalence Ratio, Included vs. Excluded (95% CI) Analysis Population (N = 26,956) Prevalence Ratio, after vs. before Recommendation (95% CI) Male 2287 (52.3) 1777 (50.8) 1.03 ( ) 11,799 (52.2) 2680 (52.0) 1.09 ( ) 0.95 ( ) 15 yr 2738 (62.7) 2311 (66.1) 16,093 (71.3) 3755 (72.9) 2 14 yr 1632 (37.3) 1184 (33.9) 1.08 ( ) 6,493 (28.7) 1395 (27.1) 1.00 ( ) 0.75 ( ) Southeast Asia 2715 (62.1) 2174 (62.2) 5,575 (24.7) 531 (10.3) Africa 1655 (37.9) 1321 (37.8) 1.00 ( ) 17,011 (75.3) 4619 (89.7) 0.98 ( ) 1.94 ( ) * On May 1, 1999, the Centers for Disease Control and Prevention issued a recommendation to provide presumptive treatment for all nonpregnant refugees 2 years of age or older before departure for the United States. The period before the recommendation was January 1, 1993, through April 30, The period after the recommendation was May 1, 1999, through December 31, Refugees were excluded from the analysis if they did not submit at least one adequate stool specimen. CI denotes confidence interval. ris (1.3% vs. 6.1%, P<0.001) or schistosoma species (0% vs. 2.2%, P not calculated). In multivariate models that included treatment status, sex, age, and country or region of origin, albendazole-treated refugees were significantly less likely than untreated refugees to have one or more nematodes (Table 4). Albendazole treatment was associated with lower adjusted prevalences of ascaris, hookworm, trichuris, strongyloides, and schistosoma. Albendazole treatment was not associated with a lower adjusted prevalence of giardia or entamoeba. No serious adverse events were reported overseas or through passive reporting by states after resettlement. Intestinal parasitosis differed according to both age and sex (Table 4). As compared with adults, children between the ages of 2 and 14 years had significantly higher adjusted prevalences of ascaris, trichuris, and giardia infection but a lower prevalence of hookworm infection. No significant differences were noted between children and adults with respect to the prevalences of strongyloides, schistosoma, and entamoeba infections. The adjusted prevalences of hookworm, strongyloides, schistosoma, and giardia infections were significantly higher among boys and men. Discussion This retrospective cohort analysis of parasitic infections detected in stool specimens from sub- Saharan African and Southeast Asian refugees on resettlement in Minnesota showed a marked decrease in intestinal parasitosis associated with the implementation of presumptive albendazole therapy before departure for the United States. A single dose of albendazole has variable efficacy against intestinal nematodes; it is highly effective against A. lumbricoides and hookworm but has only intermediate efficacy against T. trichiura and minimal efficacy against S. stercoralis A single dose of albendazole has minimal efficacy against the protozoan Giardia intestinalis and is considered ineffective against human taeniasis and Hymenolepis nana Data are lacking regarding the effectiveness of albendazole against schistosoma species trematodes. Our finding of a 77% reduction in the overall prevalence of intestinal nematodes among albendazole-treated refugees as compared with untreated refugees (from 20.8% to 4.7%) is consistent with the 83% reduction reported by Geltman et al., who conducted a retrospective evaluation of 1254 n engl j med 366;16 nejm.org april 19,

5 T h e n e w e ngl a nd j o u r na l o f m e dic i n e Table 2. Prevalence of Intestinal Parasites among Refugees Arriving in Minnesota, According to Country of Origin, Parasite* Total (N = 26,956) Somalia (N = 11,602) Ethiopia (N = 3278) Liberia (N = 2723) Other African Countries (N = 1063) Laos (N = 5959) Vietnam (N = 1215) Burma (N = 1116) number of refugees (percent) Any 4897 (18.2) 1775 (15.3) 423 (12.9) 565 (20.7) 242 (22.8) 1412 (23.7) 296 (24.4) 184 (16.5) Multiple 436 (1.6) 138 (1.2) 41 (1.3) 85 (3.1) 34 (3.2) 75 (1.3) 55 (4.5) 8 (0.7) Protozoans Any 2763 (10.3) 904 (7.8) 198 (6.0) 221 (8.1) 109 (10.3) 1119 (18.8) 57 (4.7) 155 (13.9) Multiple 52 (0.2) 25 (0.2) 5 (0.2) 2 (0.1) 7 (0.7) 12 (0.2) 0 1 (0.1) Giardia intestinalis 2368 (8.8) 629 (5.4) 179 (5.5) 204 (7.5) 80 (7.5) 1089 (18.3) 49 (4.0) 138 (12.4) Entamoeba 447 (1.7) 300 (2.6) 24 (0.7) 19 (0.7) 36 (3.4) 42 (0.7) 8 (0.7) 18 (1.6) Nematodes Any 1975 (7.3) 940 (8.1) 106 (3.2) 237 (8.7) 86 (8.1) 327 (5.5) 250 (20.6) 29 (2.6) Multiple 172 (0.6) 27 (0.2) 12 (0.4) 37 (1.4) 10 (0.9) 34 (0.6) 45 (3.7) 7 (0.6) Trichuris trichiura 1243 (4.6) 900 (7.8) 68 (2.1) 136 (5.0) 33 (3.1) 21 (0.4) 70 (5.8) 15 (1.3) Hookworm 494 (1.8) 21 (0.2) 21 (0.6) 88 (3.2) 35 (3.3) 193 (3.2) 121 (10.0) 15 (1.3) Ascaris lumbricoides 237 (0.9) 46 (0.4) 17 (0.5) 34 (1.2) 14 (1.3) 16 (0.3) 107 (8.8) 3 (0.3) Strongyloides stercoralis 205 (0.8) 3 (<0.1) 13 (0.4) 23 (0.8) 15 (1.4) 132 (2.2) 13 (1.1) 6 (0.5) Trematodes Schistosoma species 406 (1.5) 26 (0.2) 147 (4.5) 164 (6.0) 69 (6.5) * A revised form for refugee screening data permitted reporting of additional infections to the Minnesota Department of Health beginning in The following intestinal parasites detected among newly arrived refugees were excluded from the analysis of the effect of albendazole treatment: Blastocystis hominis (1529 cases), Hymenolepis nana (360), Dientamoeba fragilis (100), Clonorchis sinensis (11), fasciola species (4), taenia species (17), H. diminuta (2), and diphyllobothrium species (1). Other countries included Benin, Burundi, Cameroon, Ivory Coast, Democratic Republic of Congo, Eritrea, Gambia, Ghana, Guinea, Guinea- Bissau, Kenya, Niger, Nigeria, Rwanda, Senegal, Sierra Leone, Sudan, Togo, and Uganda. This category includes pathogenic Entamoeba histolytica and nonpathogenic E. moshkovskii and E. dispar, which cannot be morphologically differentiated by means of standard light microscopy. African refugees arriving in Massachusetts. 13 Geltman et al. determined that the group of refugees who arrived after implementation of the presumptive treatment program, as compared with the group that arrived before implementation, were less likely to have any helminth infection and had fewer infections with hookworm, trichuris, and ascaris. Shah et al., who evaluated an overseas 5-day regimen of albendazole among 815 Montagnard refugees migrating from Cambodia to North Carolina, 31 reported a 1% prevalence of intestinal helminths among treated refugees, as compared with 20% among untreated (pregnant) refugees. However, only 38 untreated refugees participated. Our study addressed limitations of previous studies by evaluating a large number of newly arrived refugees (almost 27,000) from both sub-saharan Africa and Southeast Asia. In our study, the decrease in intestinal parasitosis was greatest among refugees with the nematodes that are most susceptible to singledose albendazole namely, A. lumbricoides and hookworm. We observed a 93% reduction (from 4.1% to 0.3%) in the prevalence of ascaris infections and a 96% reduction (from 9.2% to 0.4%) in hookworm infections. Not surprisingly, single-dose albendazole was less efficacious against T. trichiura (54% reduction). This finding is consistent with studies that show lower cure rates for trichuris after single-dose albendazole (at a dose of 400 or 600 mg) The prevalence of infection with S. stercoralis decreased substantially (from 2.6% to 0.4%). However, routine microscopical examination of stool specimens (to detect ova and parasites) is an insensitive method for detecting strongyloides, which may be shed intermittently and in low numbers. 32 Thus, although 1502 n engl j med 366;16 nejm.org april 19, 2012

6 Albendazole and Enteric Parasites No albendazole treatment (before May 1, 1999) Albendazole treatment (on or after May 1, 1999) 20.8 Percent of Refugees Ascaris Hookworm Trichuris Strongyloides Any Nematode Multiple Nematodes Giardia Entamoeba Figure 1. Prevalence of Intestinal Parasites among 26,956 Refugees Arriving in Minnesota, According to Status with Respect to Albendazole Treatment before Departure for the United States. the use of albendazole before departure for the United States appeared to be protective, more definitive data based on more sensitive testing methods are needed. Regardless of treatment status, Southeast Asian refugees were more likely than African refugees to have strongyloides infection. Albendazole is not known to have any activity against trematodes. Therefore, the observed decrease among sub-saharan African refugees in the detection of schistosoma by means of microscopical examination of stool specimens after albendazole treatment was unexpected. Controlling for factors such as departure date, age, sex, or region of African origin did not account for the observed decrease. A single published study involving a mouse model showed that thiabendazole, a member of the benzimidazole class of drugs, decreased secretion of Schistosoma mansoni eggs; however, albendazole, which is also a benzimidazole, did not have a significant effect. 33 This intriguing finding suggests that some benzimidazoles might have antischistosomal activity among humans. We also found an age association for some intestinal parasitic infections in this study. Those infections transmitted through ingestion of contaminated food, water, or soil were significantly more common among children between the ages of 2 and 14 years than among older adolescents and adults. The prevalence of giardia infections was four times as high among children as among older persons. Among the soil-transmitted helminths (geohelminths), the prevalence of A. lumbricoides and T. trichiura was 30% and 70% greater, respectively, among children than among older adolescents and adults. In contrast, hookworm infections were 42% less prevalent among children, an observation supported by other studies. 34,35 A higher burden of hookworm infection in adulthood might reflect the predominant route of hookworm transmission (i.e., skin penetration) and the ongoing outdoor exposure that occurs among working adults in economically disadvantaged agrarian settings. 1,35 The higher prevalence of infections with certain types of helminths (hookworm, strongyloides, and schistosoma) and giardia among male refugees as compared with female refugees was an unexpected finding that might reflect differences in cumulative exposure on the basis of occupation. Albendazole was administered within 3 days before departure for the United States. The CDC requested that the International Organization for Migration perform monitoring for serious adverse events and report any occurrences. No serious adverse events were reported overseas or after resettlement. The incidence of side effects associated with albendazole reported in the literature remains low, with mild gastrointestinal symptoms most commonly reported at a cumulative frequency of less than 2%. 36 No significant differences in side effects were observed between single-dose n engl j med 366;16 nejm.org april 19,

7 T h e n e w e ngl a nd j o u r na l o f m e dic i n e Table 3. Unadjusted Prevalence of Intestinal Parasites among Newly Arrived Refugees in Minnesota, According to Region of Origin and Status with Respect to Albendazole Treatment before Departure for the United States, Parasite Africa (N = 18,666) Southeast Asia (N = 8,290) Unadjusted Prevalence Ratio (95% CI) P Value Treated (N = 5575) Not Treated (N = 2715) Total (N = 8290) Unadjusted Prevalence Ratio (95% CI) P Value Treated (N = 17,011) Not Treated (N = 1655) Total (N = 18,666) number (percent) number (percent) Ascaris 111 (0.6) 62 (3.7) 49 (0.3) 0.08 ( ) < (1.5) 118 (4.3) 8 (0.1) 0.03 ( ) <0.001 Hookworm 165 (0.9) 111 (6.7) 54 (0.3) 0.05 ( ) < (4.0) 291 (10.7) 38 (0.7) 0.06 ( ) <0.001 Trichuris 1137 (6.1) 285 (17.2) 852 (5.0) 0.29 ( ) < (1.3) 86 (3.2) 20 (0.4) 0.11 ( ) <0.001 Strongyloides 54 (0.3) 11 (0.7) 43 (0.3) 0.38 ( ) (1.8) 104 (3.8) 47 (0.8) 0.22 ( ) <0.001 Any nematode 1369 (7.3) 406 (24.5) 963 (5.7) 0.23 ( ) < (7.3) 504 (18.6) 102 (1.8) 0.09 ( ) <0.001 Multiple nematodes 86 (0.5) 56 (3.4) 30 (0.2) 0.05 ( ) < (1.0) 78 (2.9) 8 (0.1) 0.05 ( ) <0.001 Schistosoma species 406 (2.2) 92 (5.6) 314 (1.8) 0.33 ( ) < Giardia 1092 (5.9) 122 (7.4) 970 (5.7) 0.77 ( ) (15.4) 318 (11.7) 958 (17.2) 1.47 ( ) <0.001 Entamoeba histolytica, E. moshkovskii, 379 (2.0) 7 (0.4) 372 (2.2) 5.17 ( ) (0.8) 7 (0.3) 61 (1.1) 4.24 ( ) or E. dispar albendazole and placebo in a double-blind, multicenter study involving more than 750 schoolchildren. 37 Clinically significant adverse events were not reported among 11 randomized, controlled trials included in a meta-analysis of the efficacy of single-dose albendazole. 25 With more than 35 years of use and many hundreds of millions of patient exposures, albendazole is generally considered to have an acceptable side-effect profile and remains a mainstay of geohelminthic treatment and preventive chemotherapy programs. This study shows that presumptive therapy in refugees, like treatment programs for the control of intestinal helminthic infections in nonmigrant populations of developing countries, may substantially reduce the prevalence of intestinal parasitosis. Our data provide support for presumptive therapy with albendazole before departure for the United States as a strategy to reduce intestinal parasitosis among refugees relocating to the United States. 38,39 Revised CDC guidelines now recommend a single 400-mg dose of albendazole and include provisions for treatment of children older than 12 months of age and pregnant women in their second or third trimester. 19 We found that the prevalence of certain intestinal parasites, particularly giardia and trichuris, remained substantial despite predeparture treatment with albendazole. Geographic differences in the prevalence of these pathogens, as well as increased risks of strongyloides infection among Southeast Asian refugees and schistosomiasis among African refugees, were notable. Rates of schistosomiasis and strongyloides infection and associated morbidity remain high among refugee populations. 40,41 On the basis of these findings, the CDC has expanded its presumptive therapy recommendations to include treatment with praziquantel and ivermectin in certain refugee populations before departure for the United States. 19,42 Our study had limitations. Because albendazole treatment was not randomized, only temporal associations between presumptive therapy and the prevalence of infection can be determined. To limit the effect of confounding due to the changing composition of United States bound refugee populations over time, we controlled for critical demographic factors (i.e., country or region of origin, sex, and age) and studied a large sample to improve the precision of the statistical analysis. We were unable to control for underlying changes within countries of origin (e.g., overseas disease n engl j med 366;16 nejm.org april 19, 2012

8 Albendazole and Enteric Parasites control programs) or medical services received before entry into refugee camps that might have affected prevalence rates. It was also not possible to determine additional health interventions that may have been received within refugee camps before departure. However, data on control programs do not overlap with our intervention with respect to geography, population coverage, or time frame. National and nongovernmental organizations engaged in antihelminthic control have generally targeted schoolchildren and selected at-risk populations for mass treatment. Refugees have been excluded from such interventions and therefore would have been unlikely recipients of albendazole therapy unless it was administered within the camps by medical personnel of the International Organization for Migration following the CDC protocol during the period of study. It is possible that in the early period after initiation of the presumptive therapy program, not all refugees categorized as being treated with albendazole actually received it before departing for the United States, as a result of challenges inherent in implementing an overseas public health intervention of this magnitude across geographic regions. Internal documents of the International Organization for Migration indicate that 65 to 89% of eligible refugees received predeparture treatment with albendazole in the initial program rollout 43 ; after 2004, this proportion increased to 89 to 100%. In addition, a limited number of refugees received presumptive albendazole therapy beginning in Such misclassifications probably led to an underestimation of the effect of the albendazole intervention. Another limitation of the study was the imperfect nature of the stool ova and parasite examination as a measure of effectiveness of the intervention. The sensitivity of this test is variable, depending on the type of intestinal parasite. For example, it is reasonably sensitive for ascaris and hookworm but is insensitive for schistosomiasis and strongyloides. Stool ova and parasite analysis would not routinely detect S. haematobium. Seroprevalence rates of these infections exceed 40% in many populations, including the Sudanese lost boys and girls. 39 It remains likely that the overall rate of schistosomiasis and strongyloidiasis exceeded the rate that was detected by routine stool ova and parasite examination. Although the Minnesota Department of Health recommends three ova and parasite examinations for all newly arrived refugees, this is not uniform- Table 4. Adjusted Prevalence Ratios for Selected Parasitic Infections among Newly Arrived Refugees in Minnesota, * Multiple Nematodes Schistosoma Giardia Entamoeba Any Nematode Variable Ascaris Hookworm Trichuris Strongyloides prevalence ratio (95% CI) Departure date Referent Referent Referent Referent Referent Referent Referent Referent Referent Before recommendation for treatment, January 1, 1993 April 30, ( ) 1.13 ( ) 0.60 ( ) 0.05 ( ) 0.19 ( ) 0.26 ( ) 0.27 ( ) 0.07 ( ) 0.06 ( ) After recommendation for treatment, May 1, 1999 December 31, 2007 Sex Female Referent Referent Referent Referent Referent Referent Referent Referent Referent 1.05 ( ) 1.26 ( ) 1.44 ( ) 1.49 ( ) 1.18 ( ) 2.50 ( ) 1.03 ( ) 1.62 ( ) Male 0.94 ( ) Age 15 yr Referent Referent Referent Referent Referent Referent Referent Referent Referent 1.07 ( ) 4.22 ( ) 1.13 ( ) 1.54 ( ) 1.23 ( ) 1.13 ( ) 1.72 ( ) 0.58 ( ) 2 14 yr 1.32 ( ) * Data were calculated with the use of separate log-binomial regression models for each pathogen; all models included departure date, sex, age, and country or region of origin. This parasite was detected exclusively in sub-saharan refugees. Schistosoma species were not reported. n engl j med 366;16 nejm.org april 19,

9 T h e n e w e ngl a nd j o u r na l o f m e dic i n e ly accomplished. The actual number of submitted stool specimens may have varied among refugees and among clinics. However, no changes in this recommendation were made before or after implementation of the albendazole protocol; therefore, the number of stool specimens provided by each refugee should not have varied between untreated and treated groups and is unlikely to have affected the overall study results. In conclusion, these data provide evidence that implementation of an overseas protocol for presumptive single-dose albendazole therapy in refugees was associated with substantial decreases in infections with multiple intestinal parasites. Moderate decreases in the prevalence of strongyloides infections and an unanticipated decrease in schistosoma infections were observed. Targeting these diseases among refugees has yielded reductions in parasite burdens and may improve the health of this population. The views expressed in this article are those of the authors and do not necessarily represent the official position of the CDC. Disclosure forms provided by the authors are available with the full text of this article at NEJM.org. We thank the many health care providers and laboratory personnel in Minnesota who regularly perform medical and laboratory examinations of refugees and keep up with notification requirements of the Minnesota Department of Health; epidemiologists and health officials at the Refugee Health Program in the Minnesota Department of Health, the International Organization for Migration, the Division of Global Migration and Quarantine, and the CDC Division of Parasitic Diseases and Malaria, whose efforts made this study possible; and outside reviewers of our study, including Dr. Sue Duval of the School of Public Health, University of Minnesota. References 1. de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L. Soiltransmitted helminth infections: updating the global picture. Trends Parasitol 2003; 19: Bethony J, Brooker S, Albonico M, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006;367: Hotez PJ, Kamath A. Neglected tropical diseases in sub-saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis 2009; 3(8):e Hotez PJ, Molyneux DH, Fenwick A, et al. Control of neglected tropical diseases. N Engl J Med 2007;357: Buchwald D, Lam M, Hooton TM. Prevalence of intestinal parasites and association with symptoms in Southeast Asian refugees. J Clin Pharm Ther 1995; 20: Franco-Paredes C, Dismukes R, Nicolls D, et al. Persistent and untreated tropical infectious diseases among Sudanese refugees in the United States. Am J Trop Med Hyg 2007;77: Gyorkos TW, MacLean JD, Viens P, Chheang C, Kokoskin-Nelson E. Intestinal parasite infection in the Kampuchean refugee population 6 years after resettlement in Canada. J Infect Dis 1992;166: Library of Congress. Bill summary and status: 96th Congress ( ): S.643 ( L&summ2=m&). 9. Department of Health and Human Services, Administration for Children and Families. The Refugee Act ( 10. Enhanced medical assessment strategy for Barawan Somali refugees Kenya, MMWR Morb Mortal Wkly Rep 1998;46: Miller JM, Boyd HA, Ostrowski SR, et al. Malaria, intestinal parasites, and schistosomiasis among Barawan Somali refugees resettling to the United States: a strategy to reduce morbidity and decrease the risk of imported infections. Am J Trop Med Hyg 2000;62: Garg PK, Perry S, Dorn M, Hardcastle L, Parsonnet J. Risk of intestinal helminth and protozoan infection in a refugee population. Am J Trop Med Hyg 2005;73: Geltman PL, Cochran J, Hedgecock C. Intestinal parasites among African refugees resettled in Massachusetts and the impact of an overseas pre-departure treatment program. Am J Trop Med Hyg 2003;69: Godue CB, Gyorkos TW. Intestinal parasites in refugee claimants: a case study for selective screening? Can J Public Health 1990;81: Lifson AR, Thai D, O Fallon A, Mills WA, Hang K. Prevalence of tuberculosis, hepatitis B virus, and intestinal parasitic infections among refugees to Minnesota. Public Health Rep 2002;117: Lurio J, Verson H, Karp S. Intestinal parasites in Cambodians: comparison of diagnostic methods used in screening refugees with implications for treatment of populations with high rates of infestation. J Am Board Fam Pract 1991;4: Peterson MH, Konczyk MR, Ambrosino K, Carpenter DF, Wilhelm J, Kocka FE. Parasitic screening of a refugee population in Illinois. Diagn Microbiol Infect Dis 2001;40: Stauffer WM, Weinberg M, Newman RD, et al. Pre-departure and post-arrival management of P. falciparum malaria in refugees relocating from sub-saharan Africa to the United States. Am J Trop Med Hyg 2008;79: Centers for Disease Control and Prevention. Overseas refugee health guidelines: intestinal parasites ( overseas/intestinal-parasites-overseas.html). 20. Department of Health and Human Services, Administration for Children and Families. Refugee arrival data ( arrival_data.htm). 21. Cartwright CP. Utility of multiplestool-specimen ova and parasite examinations in a high-prevalence setting. J Clin Microbiol 1999;37: Abramowicz ME. Drugs for parasitic infections. 2nd ed. New Rochelle, NY: The Medical Letter, Bennett A, Guyatt H. Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitol Today 2000;16: Hall A, Nahar Q. Albendazole and infections with Ascaris lumbricoides and Trichuris trichiura in children in Bangladesh. Trans R Soc Trop Med Hyg 1994;88: Keiser J, Utzinger J. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 2008;299: Raccurt CP, Lambert MT, Bouloumie J, Ripert C. Evaluation of the treatment of intestinal helminthiases with albendazole in Djohong (North Cameroon). Trop Med Parasitol 1990;41: Goswami ND, Shah JJ, Corey GR, Stout JE. Persistent eosinophilia and Strongyloides infection in Montagnard refugees after presumptive albendazole therapy. Am J Trop Med Hyg 2009;81: n engl j med 366;16 nejm.org april 19, 2012

10 Albendazole and Enteric Parasites 28. Hall A, Nahar Q. Albendazole as a treatment for infections with Giardia duodenalis in children in Bangladesh. Trans R Soc Trop Med Hyg 1993;87: Pengsaa K, Sirivichayakul C, Pojjaroenanant C, Nimnual S, Wisetsing P. Albendazole treatment for Giardia intestinalis infections in school children. Southeast Asian J Trop Med Public Health 1999;30: Chung WC, Fan PC, Lin CY, Wu CC. Poor efficacy of albendazole for the treatment of human taeniasis. Int J Parasitol 1991;21: Shah JJ, Maloney SA, Liu Y, et al. Evaluation of the impact of overseas pre-departure treatment for infection with intestinal parasites among Montagnard refugees migrating from Cambodia to North Carolina. Am J Trop Med Hyg 2008;78: Dreyer G, Fernandes-Silva E, Alves S, Rocha A, Albuquerque R, Addiss D. Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. J Clin Microbiol 1996;34: Pancera CF, Alves AL, Paschoalotti MA, Chieffi PP. Effect of wide spectrum anti-helminthic drugs upon Schistosoma mansoni experimentally infected mice. Rev Inst Med Trop Sao Paulo 1997;39: Bethony J, Chen J, Lin S, et al. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People s Republic of China. Clin Infect Dis 2002;35: Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Hookworm infection. N Engl J Med 2004;351: Horton J. Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology 2000;121:Suppl:S113- S Olds GR, King C, Hewlett J, et al. Double-blind placebo-controlled study of concurrent administration of albendazole and praziquantel in schoolchildren with schistosomiasis and geohelminths. J Infect Dis 1999;179: Muennig P, Pallin D, Sell RL, Chan MS. The cost effectiveness of strategies for the treatment of intestinal parasites in immigrants. N Engl J Med 1999;340: Posey DL, Blackburn BG, Weinberg M, et al. High prevalence and presumptive treatment of schistosomiasis and strongyloidiasis among African refugees. Clin Infect Dis 2007;45: Boulware DR, Stauffer WM, Hendel- Paterson BR, et al. Maltreatment of Strongyloides infection: case series and worldwide physicians-in-training survey. Am J Med 2007;120(6):545.e1-545.e Newberry AM, Williams DN, Stauffer WM, Boulware DR, Hendel-Paterson BR, Walker PF. Strongyloides hyperinfection presenting as acute respiratory failure and gram-negative sepsis. Chest 2005; 128: Brodine SK, Thomas A, Huang R, et al. Community based parasitic screening and treatment of Sudanese refugees: application and assessment of Centers for Disease Control guidelines. Am J Trop Med Hyg 2009;80: Pre-departure anti-malarial and antiintestinal parasitosis treatment report: October 1, 2003 September 30, 2004, fiscal year 2004 report, and October 1, 2001 June 30, 2002, fiscal year 2002 report. Geneva: International Organization for Migration, Copyright 2012 Massachusetts Medical Society. an nejm app for iphone The NEJM Image Challenge app brings a popular online feature to the smartphone. Optimized for viewing on the iphone and ipod Touch, the Image Challenge app lets you test your diagnostic skills anytime, anywhere. The Image Challenge app randomly selects from 300 challenging clinical photos published in NEJM, with a new image added each week. View an image, choose your answer, get immediate feedback, and see how others answered. The Image Challenge app is available at the itunes App Store. n engl j med 366;16 nejm.org april 19,

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