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ABSTRACT |
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Helminth and protozoan infections differ importantly both in host immune response and in epidemiology. Helminths are macroparasites that reproduce sexually within the definitive host, where they can persist for many years, whereas protozoa are microparasites that are capable of direct reproduction within the host, often at high rates, and cause relatively short-lived infection.16 Helminth infections are well-known to elicit a Type 2 (Th2) noninflammatory T-cell response,17 a hallmark of which is IgE elevation with eosinophilia, and which may be strong enough to exert biasing effects on concomitant infections18,19 as well as host response to Th1-mediated chronic infections,20–22 including intracellular parasites.23 By contrast, many protozoa, like bacteria, act through manipulation of Th-1 pathways.24
These differences in host immune response have important implications in medical management of populations from different parts of the developing world. Concomitant infections are not uncommon,25 and even populations from the same regions can have different epidemiologic profiles.26 In addition, different parasitic infections may have broader implications for explaining global variations in autoimmune and atopic diseases.27 Some common protozoa, such as Giardia lamblia, Dientamoeba fragilis, and E. histolytica, may be associated with sporadic outbreaks in industrialized countries, whereas helminths have specific geographic distributions and may be rapidly extinguished with improvements in community sanitary conditions. For this reason, helminth infections are likely to be found in more recent arrivals than in long-term immigrants.12
Since the 1990s, under the auspices of the federal Immigration and Nationality Act, as amended by the Refugee Act of 1980, the United States, through the Department of Health and Human Services Office of Refugee Resettlement, in cooperation with state public health authorities, provides transitional medical care, including preventive health screening, to the approximately 70,000 refugees and asylees admitted to the United States each year (classes of immigrants who may be admitted on the basis of political persecution).28 As part of this program, the California Department of Health Services (CDHS), through its Office of County Health Services (OCHS), Refugee Health Section (RHS), administers the California Refugee Health Assessment Program (RHAP), to include health screening assessments. We here report results of parasite testing performed through the California RHAP between October 2001 and January 2004 in Santa Clara County, home to one of the largest immigrant communities in the United States. Objectives of the study were to characterize overall prevalence of helminths and protozoa in local refugees and to describe variations in prevalence in association with demographic characteristics.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Data collection. Beginning federal fiscal year (October) 2001, results of all parasite examinations conducted under the state RHAP have been entered into the state’s Refugee Health Electronic Information System (RHEIS), a standardized online database that tracks referrals as well as clinical and laboratory results. Parasite records consist of dates of stool collection, specimen number, and species identification. Only results considered pathogenic (of treatment implication) were entered. With the assistance of the state office of Refugee Health, records were extracted for all ova and parasite examinations completed between October 2001 and January 2004. In addition to results of O&P examinations, data included demographic characteristics, country of emigration, and dates of emigration and arrival in the United States. The institutional review boards of Stanford University and Santa Clara Valley Medical Center approved methods and fields targeted for extraction.
Analytic methods. We compared demographic characteristics of refugees completing O&P examinations through the Refugee Clinic with those who declined health assessments or who failed to complete an examination. For analysis of O&P results, only RHAP records with results for at least two of three possible stool specimens were considered eligible for our analysis. An examination was considered positive if intestinal parasites were identified in at least one of two (or three) stool specimens and negative if all specimens were negative. Individual test results are described by species, number of different species, and class of intestinal parasite (helminth and protozoa).
We assessed geographic and demographic (age, gender, educational attainment of adults, year of arrival) characteristics associated with helminth and protozoan infections using the 
2 test or test of medians, as appropriate. For analysis of geographic distributions, only regions with parasite results in at least five individuals were used. These regions were Africa, South Central Asia (Afghanistan, Bangladesh, Bhutan, India, Maldives, Nepal, Pakistan, and Sri Lanka), Middle East, and Eastern Europe. Because of a low representative sample, regions excluded from this analysis were Southeast Asia (N = 4), Western Europe (N = 4), and the Caribbean (N = 1). Logistic regression was used to estimate odds and 95% confidence intervals for helminth and protozoan infections univariately as well as to adjust geographic distribution for age and gender. For these analyses, Middle East and Eastern European groups were combined as the referent group due to low frequency of helminths in these regions relative to Africa and South Central Asia. Year of arrival (2001/2002 versus 2003/2004) was also assessed to look for significant variations in infection prevalence. The collapsing of years reflects the fact that relatively few records were entered in 2001, the database being initiated near the end of the year, or in 2004, which includes only one month of intakes.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Compared with those completing health assessments through RHAP, those refusing health assessments as well as those consenting to but not completing one were both younger (median ages of 24 versus 30 years, P = 0.01). Those declining health assessments, were more likely to have emigrated from East Asia (P < 0.01) or Southeast Asia (P = 0.01). Of the 534 completing health assessments, 80% were 
18 years of age (range 1 year to 80 years). Among adults completing RHAP, median years of formal education was 11, with more than 20% having no formal education. However, education was significantly lower, median level of 8 years (P < 0.01), in those refugees consenting to but not completing a health assessment. Education level was not available for those refugees refusing to initiate a health assessment. Among those completing health assessments, the largest proportion emigrated from South Central Asia (31%), followed by Africa (27%), the Middle East (25%), and Eastern Europe (16%) (Table 1).
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). Of 66 subjects with single infections, 41 (62%) were positive for the parasite on all three specimens and 52 (79%) on at least two specimens. These yields were not significantly different when comparing helminths versus protozoa.
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Different species of helminths and protozoa were found in refugees from different regions (Table 3). Hookworm and A. lumbricoides were concentrated among South Central Asian refugees (16 of 18 identifications) whereas S. stercoralis was predominantly found among African refugees (5 of 7 identifications). In addition to S. stercoralis, Africans had the greatest variety of helminth infections, including two cases of Schistosomiasis mansoni, three of Hymenolepsis nana, and one each of Taenia saginata and Trichuris trichiura. That hookworm was found exclusively in South Central Asian and Middle Eastern groups suggests Ancylostoma duodenale. By contrast, the more common pathogenic protozoa were distributed more uniformly geographically.
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). Neither age nor gender was associated with helminth infection; however, adults without a high school education were somewhat more likely to be infected (OR: 2.2 [0.93–5.1], P = 0.07). Adjusting for age and gender (Table 5) did not alter the magnitudes of association with region of emigration appreciably. In addition, Africans were not significantly different from South Central Asians in adjusted risk.
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DISCUSSION |
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Our population of refugees had somewhat lower rates of parasitic infection than has been reported in other state RHAP studies. In Minnesota,5 the overall rate of infection for eight specific pathogenic parasites was 22% among 2,129 refugees screened in 1999, with trichuriasis in 7% and giardiasis in 3%. Nearly three-quarters of this population was from sub-Saharan Africa (compared with 26% in our study population). Similarly, for a 6-year period, Massachusetts6 reported that 56% of African refugees harbored parasitic infections, including 14% with helminth infections. In a different, 3-year survey from the same jurisdiction, 21% of refugee children, 2 of 3 of whom were from Eastern Europe, were found to harbor parasitic infections, the most common species in children from this region being G. lamblia and B. hominis.30
In addition to differences in emigration mix, one explanation for the lower prevalence observed here might be the impact of predeparture albendazole programs, primarily in Saharan Africa. Detection of parasites decreased from 24% to 4% for helminths and 57% to 47% for protozoa after establishment of this program in African refugees arriving in Massachusetts.6 By comparison, 9% of Africans in this study had helminth infections. It should also be noted that albendazole does not provide complete coverage for the spectrum of parasitic infections, including schistosomiasis and protozoa. In addition, for target pathogens, efficacy can vary widely depending on species as well as course (single or three days). Notably, schistosomiasis and Strongyloides were found uniquely or primarily among Africans, and helminth prevalence was not significantly different from that observed among South Central Asians, a region where predeparture treatment is less uniformly enforced. This underscores the fact that predeparture treatment programs can vary significantly in their coverage and effectiveness.
Parasitic infections were nevertheless common in our population, and species-related geographic variations observed in this study are consistent with variations reported elsewhere. The majority of refugees are without access to empirical treatment before departure, and there remains a need for parasite screening in all incoming refugee populations. Perhaps as important as the initial screening of immigrant populations is the need for continuing surveillance in active resettlement communities. In one Canadian study of Kampuchean refugees (64% of whom had parasite infections at arrival), prevalence was still 22% six years after initial screening.31 Interestingly, while some parasites were almost completely eradicated, A. lumbricoides, G. lamblia, and hookworm, others were present at levels comparable to the initial screening (S. stercoralis decreased only slightly from 15% to 11%).31 Longitudinal studies are needed to characterize the protracted risk for overall infection as well as infection by specific parasites in communities where refugee resettlement is ongoing and to develop screening strategies beyond the initial testing.
Refugee participation in RHAP programs is often culturally driven. In this study, only 2 of 3 of refugees contacted elected to participate, and of these, about 31% did not complete their assessments. Some of those declining participation may have used other providers; however, certain geographic regions—in particular, East Asia and Southeast Asia that represented a sizeable amount of incoming refugees—were almost completely absent from the group completing health assessments through the state RHAP clinic. In addition, although protozoa were more likely to be found in children, children were underrepresented in groups completing health assessments. We also found that lower levels of educational attainment among adults were associated with lower rates of completion. Educational awareness programs targeted both to newly arriving refugees and to resettlement communities serving particular cultural groups are needed to improve participation rates.
Although refugees represent an important target screening group for parasitic infections, it is well to note that refugees represent only a fraction of the estimated 5 million persons who may have immigrated to the United States in the previous 5 years,4 a number that does not include undocumented aliens common in border states like California, or migrant laborers.32 During the 1970s and 1980s, a number of studies reported high rates of parasitic infection in nonrefugee immigrant as well as refugee groups, but current screening studies are lacking, and many of these groups do not have access to preventive health services like RHAP. With the exception of giardiasis, mandated federal reporting of intestinal parasitic infections ceased in 1994, although high-risk communities like Santa Clara County maintained reporting on seven different helminths and three different parasites until the late 1990s. It is by virtue of state RHAP programs that the epidemiology of parasitic infections in the United States is being revisited; however, the recognition of new surveillance and health care needs should not necessarily be limited to refugee groups.
The importance of recognizing parasitic infection in immigrants extends beyond the clinical diseases they specifically elicit. Although most infections are asymptomatic, increasing amounts of data indicate that harboring helminths may alter the course of other, more life-threatening and communicable infectious diseases, such as tuberculosis and HIV.33 Besides upregulating Th2 responses, many helminths also downregulate Th1 responses, affecting the ability of the host’s immune system to respond to other pathogens or vaccines.34,35 A. lumbricoides and Onchocerca volvulus, parasites commonly found in immigrant populations, have been found to impair immune response to both acute (Vibrio) and chronic (Mycobacteria) infection.36,37 High rates of latent TB infection have been noted in a number of refugee screening studies.5,8,26,30,38,39 With reactivation of latent TB often occurring within the first few years of immigration, it is conceivable that untreated helminth infections contribute to this important public health problem.
Our study has several important weaknesses. First, the low frequency of parasitic infections necessarily limited the statistical analysis. Some nonsignificant trends observed may be due to sampling error. Second, the sensitivity of microscopic stool ova and parasite testing is known to be imperfect. All subjects in this study provided at least two specimens, but other reasons for reduced sensitivity may include variations in stool sampling in concert with parasite behavior. In practice, O&P examinations are likely to be supplemented with symptom and systems reviews, as well as other laboratory tests, such as for eosinophil counts. Prevalence, therefore, may be underestimated with reliance on O&P results alone. Finally, due to limited participation rates among South and East Asians, we were unable to adequately assess patterns of infection in these two groups of refugees. We cannot be sure that these refugees did not influence the observed prevalence of infection.
Parasites comprise a very diverse group of species that have different manifestations of varying disease severity and that require different, often highly individualized, clinical approaches. In a low-incidence country, timely, cost-effective diagnosis is aided immensely by a priori clinical suspicion.3,40 Beginning to understand what classes and species of parasites are associated with recent immigrant populations can serve to better direct clinical suspicion. Under current recommendations, treatment of asymptomatic carriers in low-risk settings is optional.41 However, refugees and other immigrant populations tend to congregate, thus placing one another at increased risk of infection and facilitating the likelihood that these parasites persist within these communities. It is this public health imperative that justifies the continued screening of these populations through heightened clinical suspicion.
Received September 28, 2004. Accepted for publication March 20, 2005.
Acknowledgment: The authors would like to thank Sakchai Himathongkhan for his help in data preparation and manuscript review.
* Address correspondence to Parveen K. Garg, 8 & 281 Dunham Dr, Naperville, IL 60540. E-mail: parveen{at}md.northwestern.edu 
Authors’ addresses: Parveen K. Garg, 8 & 281 Dunham Dr., Naperville, IL 60540. Sharon Perry and Julie Parsonnet, Stanford University, Grant Building, Room S156, 5107, Stanford, CA 94305-5107. Martha Dorn, Valley Center at Lenzen, 976 Lenzen Ave., San Jose, CA 95126. Laura Hardcastle, California Department of Health Services, Office of County Health Services, Refugee Health Section, Sacramento, CA 94234-7320.
Reprint requests: Parveen K. Garg, 8 & 281 Dunham Dr., Naperville, IL 60540.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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  C. Franco-Paredes, R. Dismukes, D. Nicolls, A. Hidron, K. Workowski, A. Rodriguez-Morales, M. Wilson, D. Jones, P. Manyang, and P. Kozarsky Persistent and Untreated Tropical Infectious Diseases Among Sudanese Refugees in the United States Am J Trop Med Hyg, October 1, 2007; 77(4): 633 - 635. [Abstract] [Full Text] [PDF]
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
