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Am. J. Respir. Crit. Care Med., Volume 159, Number 3, March 1999, 834-837

A Study of Tuberculosis Among Foreign-Born Hispanic Persons in the U.S. States Bordering Mexico

CHARLES D. WELLS, MIGUEL OCAÑA, KATHLEEN MOSER, DAVID BERGMIRE-SWEAT, JANET C. MOHLE-BOETANI, and NANCY J. BINKIN

Division of Tuberculosis Elimination, National Center for HIV/AIDS, Sexually Transmitted Diseases, and Tuberculosis Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia; San Diego County Department of Health, San Diego, California; Texas Department of Health, Austin, Texas; and California Department of Health Services, Berkeley, California

    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

In 1996, 10% of the 20,973 U.S. tuberculosis (TB) cases were among foreign-born (FB) Hispanic persons, with the four states bordering Mexico accounting for 83% of FBH cases. Limited information is available on this population's health care seeking and migration practices and on differences between FB Hispanic patients in border and nonborder areas. Therefore, we conducted interviews and record reviews for all consenting FB Hispanic TB patients from eight counties bordering Mexico (BC; n = 167) and seven urban nonborder counties (NBC; n = 158) in these States during 1995-1997. BC patients had resided in the U.S. longer than NBC patients (17.4 versus 10.8 yr; p < 0.01), had immigrated more often from Mexican border communities (62.4% versus 25.4%; p < 0.01), and had returned to Mexico more often in the past 12 mo (71.5% versus 47.3%; p < 0.01). TB symptoms were present for >=  6 mo in 37% of BC and 34% of NBC patients. Binational collaboration is essential for improving TB control in both countries and should extend beyond border areas of Mexico.

    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Tuberculosis (TB) is a disease without borders. This has become increasingly apparent in many developed countries, where the proportion of total TB cases occurring among immigrants continues to rise and, in countries such as Australia, Canada, and the Netherlands, exceeds 50% (1, 2). In 1996, 36.9% of the 20,973 TB cases reported in the United States (U.S.) were among foreign-born (FB) persons, representing a 50% increase over the past decade (3).

Among the 7,739 FB patients in 1996, Mexican-born persons were the largest subgroup. They accounted for 22.9% of FB patients or 8.4% of all U.S. cases; persons born in Central America comprised an additional 4.7% of FB patients or 1.7% of all U.S. cases. A relatively small number of patients were born in South America; cases from this region accounted for 2.4% of FB or 0.9% of US cases. The majority (79.2%) of the Mexican-born and Central American-born patients, who will henceforth be referred to as FB Hispanic, were cases reported in the four U.S. states that border Mexico (California, Arizona, New Mexico, and Texas) (3). In these states, 51% of FB patients and 26% of all cases are among FB Hispanic persons.

Limited information is available on the characteristics of FB Hispanic TB patients. To more effectively develop strategies for controlling and preventing TB among FB Hispanic persons and to better design and implement future collaborative efforts with Mexico, we undertook an epidemiologic study of FB Hispanic TB patients in eight border counties and seven urban counties not on the border in these four states. We also studied a small sample of FB Hispanic TB patients from two rural agricultural counties in California with migrant farm worker communities. The specific objectives of the project were to learn more about the patterns of immigration and migration of FB Hispanic persons in the two types of counties and to determine the sociodemographic, behavioral, and clinical characteristics of these patients. A previous brief report, focused on defining these patterns and characteristics, has been published on the patients from the border counties only (4). That report also examined levels of drug resistance among all patients in the border counties and revealed that FB Hispanic and U.S.-born Hispanic TB patients had similar levels of resistance to certain drugs (> 4% monoresistance to isoniazid) which were higher than levels for U.S.-born non-Hispanic patients. This study presents findings for the nonborder urban and agricultural counties in addition to the border counties and provides a more in-depth analysis of this latter group as well.

    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Participants in this study included all consenting FB Hispanic patients under treatment for TB in county public health TB clinics during October 1, 1995 through January 5, 1996 in eight border counties (San Diego and Imperial Counties, California; Yuma County, Arizona; Dona Ana County, New Mexico; and El Paso, Webb, Hidalgo, and Cameron Counties, Texas) and from six urban nonborder counties (Maricopa and Pima Counties in Arizona, and Dallas, Tarrant, Travis, and Harris Counties in Texas). Though part of Pima County, Arizona, borders Mexico, all patients participating in this county were reported in Tucson which is 60 miles from the border and is thus more characteristic of a community in a nonborder county. The counties were chosen because they contained the majority (approximately 70%) of FB Hispanic patients in the four states; urban nonborder counties as well as the border counties were included because anecdotally, clinicians and the TB programs in these states felt that the geographic origin and the experience of the two populations were different.

Additionally, 79 of 331 FB Hispanic patients (23.9%) in Los Angeles County, California, who were under treatment during August 1, 1996, through October 30, 1996, participated in the study and were considered with the other nonborder county patients for analytical purposes. These patients were selected from 10 of 11 public health jurisdictions in the county (the 11th jurisdiction was from a rural and remote part of Los Angeles County with few cases reported). This sample was identified from an initial county TB registry listing of FB Hispanic patients reported in the county for this time period. Of the 115 on the list, 79 (68.7%) patients were located and consented to participate; subsequently, an additional 253 FB Hispanic patients under treatment during the study period were reported when the TB registry was updated. The patients in the sample were similar demographically to the remaining patients with respect to age, gender, and distribution among the health districts.

Tulare and Kern Counties in California, which are rural nonborder counties that have large farm worker communities, participated in the study as well. All 24 FB Hispanic patients under treatment between November 1, 1996, through February 28, 1997 in these two counties consented to participate.

County health department staff who were bilingual in English and Spanish conducted the patient interviews using a standardized questionnaire which was available in English and Spanish; the interviewers participated in training sessions on conducting the interviews prior to beginning the study. The interviews were generally conducted in the TB clinics; however, in some situations, the staff made home visits to conduct the interviews. To assist with recall of prior treatment, patients were shown a card with photographs of TB drugs available in the U.S. and Mexico. Clinical data for participants were obtained from clinic charts, laboratory records, and data reported to the Center for Disease Control and Prevention's national TB surveillance system, SURVS-TB. Data entry and analyses, including comparisons of means, calculation of prevalence ratios, and calculation of exact binomial confidence intervals around each prevalence ratio were performed using the epidemiologic and statistical software package, Epi-Info (5). Because the number of patients from Tulare and Kern Counties was small, detailed analysis was not possible. Therefore, the main comparisons in the study were between the BC and the nonborder counties.

    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Similar proportions of patients from both the border and nonborder counties consented to participate in the study (83.5% versus 78.6%; p = 0.21). Participants from both areas were predominantly male (59.9% versus 61.0%; p = 0.87). FB Hispanic patients in border counties were older than those from nonborder counties (45.2 versus 38.8 years, p < 0.01) and had resided in the U.S. for a longer period at the time of diagnosis with TB (17.4 versus 10.8 yr, p < 0.01) (Table 1).

                              
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TABLE 1

COMPARISON OF RESULTS FROM AN EPIDEMIOLOGIC STUDY OF FOREIGN-BORN HISPANIC TB PATIENTS FROM BORDER COUNTIES AND NONBORDER URBAN COUNTIES OF THE FOUR U.S. STATES BORDERING MEXICO, 1995-1996

Similar proportions of participants age 18 to 65 yr from non-border counties and border counties were actively employed at the time of diagnosis (29.0% versus 34.1%; p = 0.4). The usual occupations for both groups were also similar, though patients in border counties were more likely to work in agriculture than those in nonborder counties (15.3% versus 4.7%; p < 0.01) (Table 1).

In terms of immigration history, more of the study participants in the border counties than in the nonborder counties were originally born in Mexico (94.0% versus 79.7%, p < 0.01). Among the Mexican-born patients, those in border counties were more likely than those in nonborder counties (62.4% versus 25.4%, p < 0.01) to have immigrated from border communities in Mexico (defined as communities within 50 miles of the U.S.-Mexico border) (Table 1). Of the Mexican-born patients who immigrated from border communities, 42/ 98 (42.9%) of those in border counties and 14/32 (43.8%) of those in nonborder counties were born in these communities (p = 0.93); the remainder moved to the border communities from areas deeper within Mexico before immigrating to the U.S. The majority of Mexican-born patients in border counties (85.7%) and in nonborder counties (83.3%) who moved to Mexican border communities prior to immigrating to the U.S. resided in those communities for 2 yr or longer (p = 0.53).

Among patients who were originally born in Central America, all of those in the border counties and the majority of those in the nonborder counties (84.4%) reported immigrating directly to the U.S. (i.e., did not reside in another country before arriving in the U.S.) from their respective countries of birth (p = 0.2). Of the 10 border county patients born in Central America, seven were from Guatemala and three were from El Salvador; of the 32 nonborder county patients born in Central America, 13 (40.6%) were from Guatemala, 12 (37.5%) were from El Salvador, four (12.5%) were from Honduras, and the remaining four (12.5%) were from the rest of Central America.

More of the Mexican-born patients from border counties ever returned to Mexico than did those from nonborder counties (83.4% versus 65.1%; p < 0.01) (Table 1). Additionally, those in border counties were more likely than those in nonborder counties to report having returned to Mexico within the 12 mo before being diagnosed with TB (71.5% versus 47.3%; p < 0.01). More than a third (37.5%) of Mexican-born patients from border counties reported returning to Mexico at least weekly, compared with 2.3% of Mexican-born patients from nonborder counties (p < 0.01). The majority of patients from both areas who ever returned to Mexico did so to visit friends and family; few did so to seek health care. Of the Central American-born patients, 60% of those from border counties and 34.4% of those from nonborder counties had ever returned to their respective countries of origin (p = 0.15). (Table 1).

The median duration of symptoms at diagnosis was 4 mo for patients from both areas; 37% of border county patients and 34% of nonborder county patients reported symptoms consistent with TB for six months or longer prior to diagnosis (Table 1). More than a quarter of patients from both border and nonborder counties reported receiving previous treatment or preventive therapy for TB prior to their current episode of TB (28.7% versus 24.7%; p = 0.7); more than a quarter of border county and nonborder county patients who had reported previous treatment or preventive therapy stated that they had received the treatment outside the United States (25.6% versus 25.0%; p = 0.95).

Many results for the 24 FB Hispanic patients from Tulare and Kern Counties in California are similar to those shared by patients from the border counties and the urban nonborder counties. As in both border and urban nonborder counties, these patients were predominantly male (66.7%); 36.8% of the 22 patients aged 18-65 yr were employed at the time of diagnosis; most of the 24 total patients (60%) had been in the United States over 10 yr; 41.0% were symptomatic with TB for 6 mo or greater prior to diagnosis; and 7 patients (29.2%) had a history of prior TB treatment. These patients were more similar to the nonborder county patients in age (37.2 years) and frequency of returning to their respective countries of origin (69.6%). However, they were more similar to the border county patients in birthplace; 95.7% originated from Mexico. This group of patients was unique in that 76.5% of patients aged 18-65 yr reported usually working in agriculture, compared to 15.3% in border counties and 4.7% in urban nonborder counties.

    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Several findings from this study have implications for efforts aimed at controlling and preventing transmission of TB among the FB Hispanic community in the U.S. border states. First, although the mean and median durations in the U.S. prior to diagnosis were shorter for patients from the urban nonborder counties than patients from the border counties, they were nonetheless substantial for both patient groups, as well as the group from the two agricultural counties. This finding suggests that TB occurring in the FB Hispanic community in the border states is not necessarily a product of recent importation of active TB, but could represent infection and transmission occurring among persons after immigration to the U.S. or reactivation of prior infection and disease.

A second finding of our study was that nearly three-quarters of Mexican-born patients in the urban nonborder counties and over one-third of Mexican-born patients in the border counties and in the two agricultural counties had immigrated to the U.S. from nonborder communities in Mexico. There are currently five binational projects, supported by the Centers for Disease Control and Prevention, in which paired cities on both sides of the U.S.-Mexico border collaborate to improve TB control and prevention efforts. These projects direct resources, such as laboratory equipment and supplies, to areas of need and develop cooperative working relations between health professionals managing TB control and prevention programs in communities of the border areas of both countries (6). Although these projects are an essential part of binational cooperative TB-control efforts between the U.S. and Mexico, our findings suggest that binational collaboration should be expanded to include nonborder regions of Mexico as well.

A third finding is that over four-fifths of patients from the border counties, nearly three-fifths of patients from the urban nonborder counties, and nearly three-quarters of patients from the two agricultural counties in the study reported returning to Mexico at least once since immigrating to the U.S.; of those ever returning, nearly three-quarters of patients from the border counties and nearly one-half of patients from the urban nonborder counties did so within the 12 mo prior to diagnosis. Among those patients from the border counties returning to Mexico within the 12 mo prior to diagnosis, over one-third did so on at least a weekly basis. This large number of periodic return visits of persons back to Mexico, where the TB rate is estimated to be fivefold that of the U.S., increases the risk for exposure to TB and thus ultimate transmission of TB within the U.S. (7). Although it is not possible to determine the relative contributions of recent importation, reactivation of prior infection, or transmission occurring after immigration to the U.S. to the TB burden among the FB Hispanic population, clearly providing technical assistance to Mexico in TB control and prevention efforts is vital and mutually beneficial to the public health of both countries.

A fourth finding of our study with implications to TB control was that the median duration of symptoms at diagnosis was 4 mo for patients from both the border counties and the urban nonborder counties as well as for the patients from the two agricultural counties, and that one-third of the patients in all three areas had been symptomatic for 6 mo or longer prior to diagnosis. Such delays of symptomatic TB patients receiving treatment increase the risk for TB transmission in the community (8, 9). Therefore, providers for this population should have a heightened awareness of the existence of TB to promote early diagnosis as well as the need to initially treat these patients with four drugs given the prevalence of INH resistance (4, 10).

In this study it is possible that a number of FB Hispanic TB patients in the border counties and the urban nonborder counties as well as the two agricultural counties who went undiagnosed were not included in the study. Because of a lack of trust of government institutions related to immigration issues, some patients may have avoided presenting to health departments in the various participating U.S. counties, opting instead to seek treatment in Mexico or from private providers in the U.S. Furthermore, because of the time frame of the study some patients who normally reside in these areas may not have been included owing to their periodic migration to other areas of these four states, to other states, or to their country of origin during the period of this study. Therefore, the results of this study could be affected by selection bias. However, among those patients who did appear in the public sector, participation rates were likely enhanced by the use of bilingual health staff to perform patient interviews in Spanish as needed or as preferred by the patient.

Another limitation of the study could include the accuracy of the clinical history data, particularly of previous TB treatment. Patients could have had difficulty with accurate recall, and in some situations, may have purposely denied prior treatment. Despite these possible limitations, we believe the results from this study are useful for planning strategies and targeting efforts to better control the burden of TB among the FB Hispanic community in the border states.

    Footnotes

Correspondence and requests for reprints should be addressed to Nancy J. Binkin, M.D., M.P.H., Division of Tuberculosis Elimination, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road (MS E-10), Atlanta, GA 30333.

(Received in original form December 30, 1997 and in revised form October 2, 1998).

Acknowledgments: The authors thank Doris Fields, Dave Espey, Paul Tribble, Karen Fleming, Gene Tamamas, and Miguel Escobedo for their assistance with this project.

Supported by the Centers for Disease Control and Prevention.

    References
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1. Raviglione, M. C., D. E. Snider Jr., and A. Kochi. 1995. Global epidemiology of tuberculosis: morbidity and mortality of a worldwide epidemic. J.A.M.A. 273: 220-226 [Abstract].

2. Rieder, H. L., J. P. Zellweger, M. C. Raviglione, S. T. Keizer, and G. B. Migliori. 1994. Tuberculosis control in Europe and international migration. Eur. Respir. J. 7: 1395-1396 [Medline].

3. U.S. Department of Health and Human Services. 1997. Reported Tuberculosis in the United States: 1996. Centers for Disease Control and Prevention, Atlanta.

4. Centers for Disease Control and Prevention. 1996. Characteristics of foreign-born Hispanic patients with tuberculosis---eight U.S. counties bordering Mexico, 1995.  M.M.W.R. 45: 1032-1036 . [Medline]

5. Epi-Info, version 6. July 1995. A Word Processing, Database, and Statistics System for Epidemiology on Microcomputers. U.S. Department of Health and Human Services/Centers for Disease Control and Prevention, Atlanta.

6. Field Office, U.S.-Mexico Border, Pan-American Health Organization. 1995. Report on the Binational Tuberculosis Activities among U.S.- Mexico Border Sister Cities 1991-1995. Prepared for International Health Affairs Office of Public Health Services, July 1995.

7. Escobedo, M. E., and F. G. de Cosio. 1997. Tuberculosis and the United States-Mexico border. J. Border Health II,1:40-48.

8. Asch, S., B. Leake, and L. Gelberg. 1994. Does fear of immigration authorities deter tuberculosis patients from seeking care?. West. J. Med. 161: 373-376 [Medline].

9. Rubel, A. J., and L. C. Garro. 1992. Social and cultural factors in the successful control of tuberculosis. Public Health Rep. 107: 626-636 [Medline].

10. Bass, J. B. Jr., L. S. Farer, P. C. Hopewell, R. O'Brien, R. F. Jacobs, F. Ruben, D. E. Snider Jr., and G. Thornton. 1994. Treatment of tuberculosis and tuberculosis infection in adults and children. Am. J. Respir. Crit. Care Med. 149: 1359-1374 [Abstract].





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