American Journal of Epidemiology Advance Access originally published online on May 4, 2006
American Journal of Epidemiology 2006 164(1):32-40; doi:10.1093/aje/kwj159
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Original Contribution |
Environmental Risk Factors for Infection with Mycobacterium avium Complex
1 Department of Epidemiology, Boston University School of Public Health, Boston, MA
2 Department of Medicine, Dartmouth-Hitchcock Medical Center, Lebanon, NH
3 Glades Health Initiative, Inc., Belle Glade, FL
4 Division of HIV/AIDS Prevention, Surveillance, and Epidemiology, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Public Health Service, US Department of Health and Human Services, Atlanta, GA
5 Palm Beach County Health Department, Belle Glade, FL
Reprint requests to Carrie Reed, Department of Epidemiology, Boston University School of Public Health, 715 Albany Street, T3E, Boston, MA 02118 (e-mail: reedc{at}bu.edu).
Received for publication April 14, 2005. Accepted for publication January 19, 2006.
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ABSTRACT |
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Infection with Mycobacterium avium complex is acquired from the environment, but risk factors for M. avium complex infection and disease are poorly understood. To identify risk factors for infection, the authors performed a 1998–2000 cross-sectional study in western Palm Beach County, Florida, using a population-based random household survey. M. avium complex infection was identified by use of the M. avium sensitin skin test. Of 447 participants, 147 (32.9%) had a positive test reaction, 186 (41.6%) had a negative test reaction, and, for 114 (25.5%), test results were indeterminate. Among the 333 participants with positive or negative M. avium sensitin skin tests, age-adjusted independent predictors of M. avium complex infection in a multivariate model included Black race (odds ratio = 3.8, 95% confidence interval: 2.2, 6.6), birth outside the United States (odds ratio = 2.1, 95% confidence interval: 1.1, 3.9), and more than 6 years' cumulative occupational exposure to soil (odds ratio = 2.7, 95% confidence interval: 1.3, 6.0). Exposure to water, food, or pets was not associated with infection. Results indicate that soil is a reservoir for M. avium complex associated with human infection and that persons whose occupations involve prolonged soil exposure are at increased risk of M. avium complex infection.
HIV; Mycobacterium avium complex; opportunistic infections; risk factors
Abbreviations: HIV, human immunodeficiency virus; MAC, Mycobacterium avium complex; MaS, Mycobacterium avium sensitin; PPD, purified protein derivative
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Mycobacterium avium complex (MAC) includes two closely related organisms, M. avium and M. intracellulare. Together, these organisms account for over 70 percent of nontuberculous mycobacterial disease in the United States (1
, 2) and for more than 95 percent of nontuberculous mycobacterial disease among persons infected with human immunodeficiency virus (HIV). MAC disease can be pulmonary or disseminated and is thought to occur through either inhalation or ingestion (1, 3). MAC disease occurs directly following primary infection; disease following reactivation of a previous latent infection has not been demonstrated. Although MAC disease occurs in only 1–1.8/100,000 persons (2), asymptomatic infection with the organisms is widespread, occurring in more than 50 percent of the general population in some areas of the United States (4, 5).
Among immunocompetent persons, MAC infection can be detected by use of a number of skin test reagents. These reagents are prepared and administered in the same manner as the purified protein derivative (PPD) skin test for tuberculosis. When used in combination with the PPD skin test, MAC skin test results can indicate that a subject has been infected with MAC (5, 6). MAC skin test surveys have demonstrated that the prevalence of MAC infection increases with age to at least age 20 years and is more common among persons of Black race and male gender (7–10). Infection is found worldwide in diverse climates, although the prevalence of infection shows some geographic variation. Rural areas show higher rates of infection than urban areas (7, 9), and, in the United States, a study of military recruits found increased reactivity among recruits from southern states (7).
MAC organisms have been isolated from various environmental sources, including birds, pigs and cattle, cow's milk, water, and soil (11–20), but specific reservoirs for human infection are poorly defined. Epidemiologic studies of MAC have found associations between MAC infection and various water exposures, animals in the home, food items, and soil, but other studies have failed to confirm these associations (8, 21–25). Therefore, we performed a cross-sectional survey in western Palm Beach County, Florida, to determine risk factors for MAC infection by using a well-characterized MAC skin test reagent, Mycobacterium avium sensitin (MaS) (26).
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MATERIALS AND METHODS |
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Population-based survey
From January 1, 1998, to September 30, 2000, a population-based survey was performed in western Palm Beach County, Florida—defined as the area that includes postal zip codes 33430, 33438, 33476, and 33493. To choose study participants, a computer program randomly selected 800 addresses from the area's water meter records. These records represent all addresses in the area because the high water table makes well water nonpotable; thus, piped water is the only source of household water.
A random selection table was used to choose one resident from each selected address identified as a household. Persons with a history of blistering on prior tuberculin skin testing were excluded, as were children less than 1 year of age. Houses classified as unoccupied were visited at least six times during the study period, including at least twice in the evening and/or on weekends, before being so classified. Each participant gave informed consent, responded to a standardized questionnaire, and underwent skin testing. Human subjects committees of the Florida Department of Health, Emory University, Boston University, Dartmouth Medical School, and the Centers for Disease Control and Prevention approved the study protocol.
Self-identified HIV-infected participants
All HIV-infected residents of the community were invited to enroll in the study and were evaluated by the same protocol used in the population-based study, except that self-identified participants also received anergy skin testing. These self-identified HIV-infected participants were sought by advertising in local media and by contacting local HIV/acquired immunodeficiency syndrome service organizations and care providers. Most of these participants were referred to the study staff by the local health clinic, private practitioners, or local HIV service agencies.
Skin tests
Each participant received a skin test with PPD (5 tuberculin units; Connaught Laboratories, Swiftwater, Pennsylvania) on the right forearm and with MaS (MaS 10/2, 1 mcg/ml; Statens Seruminstitut, Copenhagen, Denmark) on the left forearm. HIV-infected participants were also skin tested with mumps (MSTA; Connaught Laboratories) and tetanus toxoid (diluted 1:10 in albumin-saline diluent; Connaught Laboratories) to assess anergy. For each antigen, 0.1 ml was injected intradermally. Trained professionals read the skin tests after 48–72 hours according to established guidelines. A single study nurse was trained in skin test planting and reading by an experienced skin test investigator (B. J. M.) and subsequently read all tests in the study. Anergy was defined as failure to demonstrate a reaction of 3 mm or greater to any of the four skin test reagents.
Interpretation of the MaS skin test followed established guidelines using both MaS and PPD reaction results (5, 6). A negative reaction to the MaS skin test was a reaction of less than 5 mm to MaS. A positive MaS skin test was a reaction of at least 5 mm and dominant to the PPD reaction—at least 3 mm larger than the PPD reaction. An indeterminate MaS reaction was defined as an MaS reaction that was at least 5 mm but was either equal in size (within 3 mm) or smaller than the PPD reaction (table 1). The MaS skin test has been shown to have a high sensitivity (73–83 percent) and high specificity (97–100 percent) for MAC infection and disease through studies in both human and animal models (5, 27–29).
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Risk factor questionnaire
A trained interviewer administered a standardized questionnaire to each participant in English, Spanish, or Haitian Creole. The survey included questions about sociodemographic information and risk factors for HIV, tuberculosis, and MAC infection. Information on Bacillus Calmette-Guérin vaccination was obtained by self-report. Exposure data collected as continuous variables were categorized for analysis. Several of these variables were classified as none, moderate, and high. For such classifications, responses greater than "none" or "never" were divided at their sample median value for each variable: "high" was defined as a response above the median and "moderate" as a median response or below. Variables using this distinction included number of baths/showers per week, frequency of swimming, and hard and soft cheese consumption. Other continuous variables were dichotomized as ever exposed and never exposed.
Questions about participation in a soil-related occupation were used to represent significant soil exposure beyond what would be normally expected in daily life. Subjects were also asked how many years they had worked in such occupations. Because of the overlap in responses between different types of soil-related occupations, a variable was created representing overall participation in a soil-related occupation. This variable was defined as the maximum time involved in any soil-related occupation. Responses greater than "never" were divided at the sample median number of years: "high" was defined as a response above the median and "moderate" as a median response or below. This overall median was also used as the division for defining "high" and "moderate" exposure to any individual soil occupation. To evaluate any further dose-response relation, the maximum number of years in a soil-related occupation was divided into three nonoverlapping ranges that created three groups of approximately equal numbers of subjects. For each group, the association with MAC infection was calculated compared with no occupational soil exposure. The median years of participation was calculated for each group, and the corresponding odds ratio was graphed at each group's median years of exposure (figure 1).
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Surveillance for MAC disease
Since MAC disease is not reportable to the health department, we monitored laboratory mycobacterial culture results at the Florida State Department of Health TB laboratory at A. G. Holley Hospital (Lantana, Florida) to identify cases of MAC disease. To minimize underdetection, a series of lectures about MAC disease was presented to physicians and other care providers in the study area, and mycobacterial blood culture tubes and processing were provided at no charge.
Analysis
Univariate statistical associations between MAC infection and categorical variables were tested by the chi-square or Fisher's exact test. Ninety-five percent confidence intervals were calculated by using a normal approximation of the binomial distribution. Because HIV infection may interfere with a subject's ability to manifest a skin test reaction to either PPD or MaS, data for the self-identified HIV-infected participants were analyzed separately. To identify risk factors for MAC infection, variables that appeared strongly associated with infection (p < 0.20 in univariate analysis) were analyzed in multivariate models adjusting for age, sex, race, and foreign birth. Variables that remained strongly associated with MAC infection were retained in the final model. Statistical analyses were performed by use of SAS version 8.0 software (SAS Institute, Inc., Cary, North Carolina).
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RESULTS |
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Subjects
Of the 800 addresses selected for the survey, 191 could not be used to select participants because 81 were businesses or vacant lots and 110 were unoccupied. For persons at the 609 remaining addresses, 447 (73 percent) were fully enrolled, 69 (11 percent) completed only the interview, 92 (15 percent) declined to participate, and one (0.2 percent) was ineligible because of a history of blistering on skin testing. The 69 who completed the interview were similar to the 447 who were fully enrolled by sex, age, employment, income, and birth in the United States. However, they were more likely to be Black but not Haitian (72 percent vs. 59 percent, p = 0.03).
Skin test reactions
Of the 447 fully enrolled participants, 147 (32.9 percent) had a positive MaS skin test reaction, 186 (41.6 percent) had a negative MaS skin test reaction, and, for 114 (25.5 percent), the MaS skin test was indeterminate. Description of skin test reactions and sizes can be found in table 1. It is unknown whether persons with an indeterminate MaS skin test were infected with MAC or whether they had cross-reactivity from infection with M. tuberculosis, so participants with this response were not included in risk factor analyses. Indeterminate MaS reactions ranged from 6 mm to 24 mm, with a median reaction size of 14 mm; positive MaS reaction sizes ranged from 5 mm to 38 mm, with a median of 12 mm. Of the 447 participants, 133 (29.8 percent) had a PPD skin test result of 10 mm or greater.
Risk factors for MAC infection
In univariate analysis, male gender, Black and Hispanic race, foreign birth, and age were all significant predictors of MAC infection (table 2). Of the environmental risk factors examined, all individual occupational exposures to soil were strong predictors of MAC infection in univariate analysis, as was the overall maximum soil exposure classification. Most of the water-related exposures, including a high level of doing dishes by hand, ever swimming, and ever swimming in a lake or pool, were slightly protective, but none of these associations were statistically significant. Cheese consumption also did not appear to be predictive of MAC infection; soft cheese showed a slight association, but consumption of hard or Cuban cheeses showed little association with MAC infection.
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We further stratified participation in soil-related occupations on the basis of years of reported participation in each occupation and maximum overall years of participation. Each soil occupational variable showed a dose-response relation, with above the median level of participation showing a stronger association with a positive skin test reaction than below the median level (table 3). In addition, the overall soil occupation variable was broken down into multiple levels of exposure, and each increase in duration of participation showed a stronger association with infection (figure 1).
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After controlling for age and sex, foreign birth, Black race, and longer duration in soil occupations remained significant predictors of MaS skin test positivity (table 4). Those who reported high levels of participation in soil-related occupations were about three times more likely to be MaS skin test positive than those who were never involved in soil-related occupations (odds ratio = 2.7, 95 percent confidence interval: 1.3, 6.0). The effect was less pronounced among those with only moderate levels of participation in soil occupations, where they had 1.3 (95 percent confidence interval: 0.7, 2.4) times the odds of being skin test positive compared with those who were never involved in soil occupations. History of Bacillus Calmette-Guérin vaccination was not associated with a positive MaS skin test reaction, and controlling for Bacillus Calmette-Guérin did not have an effect on the associations between MAC infection and other variables.
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Self-identified HIV-infected participants
Overall, 15 of the 217 HIV-infected participants (6.9 percent) had a positive MaS skin test. MaS reactions among this group ranged from 5 mm to 24 mm, with a median reaction size of 11 mm. One hundred seventy-two participants (79.2 percent) had a negative MaS skin test, and 30 (13.8 percent) had an indeterminate reaction. When we restricted the analysis to the 139 HIV-positive subjects who were not anergic, 109 (78.4 percent) had conclusive MaS skin test results—15 (10.8 percent) positive and 94 (67.6 percent) negative. Small numbers of positive skin test reactions precluded evaluation of risk factors for infection among HIV-infected participants. These subjects are described in table 5.
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MAC disease
During the 5-year period 1997–2001, intensive surveillance for MAC disease was performed in western Palm Beach County, an area with a population of 34,759 (30
). Two cases of MAC pulmonary disease were identified, both in HIV-uninfected persons, a rate of 1.2/100,000 (95 percent confidence interval: 0/100,00, 3.6/100,000). No cases of disseminated MAC disease were seen. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In this study, we found that risk of MAC infection was independently associated with Black race, birth outside the United States, and participation in a soil-related occupation. Environmental studies have isolated MAC organisms from soil on multiple occasions and in a broad range of geographic and climatic settings (11
, 12, 14, 17–20). Previous studies have suggested that soil or fertilizer might be a risk factor for infection but have not demonstrated significant associations in multivariate analysis (11, 22). The association between MAC infection and occupational exposure to soil did not appear to be specific for any single type of occupational soil exposure. Any participation in lawn and landscaping services, farming, or other occupations that would involve significant exposure to dirt or dust showed a modest association with MAC infection when these participants were compared with those reporting no participation in any soil-related occupation. When levels of exposure based on years of participation were examined, a stronger association was found for persons who reported more than 6 years of such work (the sample median) compared with those reporting no soil-related occupations. These associations also remained significant after controlling for other independent risk factors, including age, race, and foreign birth. An overall variable summarizing the maximum number of years in any soil-related occupation showed a similar dose-response trend over several increasing levels of exposure.
Skin test surveys have shown substantial geographic variation in the rates of MAC infection. Worldwide, countries near the equator seem to have higher rates of infection, with lower rates in temperate regions (31). However, an international study of MaS-dominant reactions showed remarkably similar rates of MAC infection in temperate and equatorial areas (6). In the United States, the highest rates of MAC infection are seen in the southern states and in rural areas (7, 10). Environmental sampling indicates that the organisms are present in the environments of most regions (15). Thus, geographic variation in the prevalence of MAC infection and disease is more likely the result of differences in the opportunities for exposure to environmental sources than the result of differences in the presence of MAC in the environment. The milder climate in the south provides more opportunity for exposure to soil because the ground is not frozen during the winter months and the agricultural season is longer. Likewise, urban areas have a lower prevalence of agricultural work and other soil-related exposures.
Black race was also a strong predictor of MAC infection. The association between Black race and MAC infection may represent soil exposure not captured by our study instrument. However, compared with Whites, Blacks have been shown to have an increased risk of infection with M. tuberculosis when exposures are similar (32), so the increased risk of MAC infection we observed may also be the result of increased susceptibility among Blacks. Birth outside the United States was also a significant predictor of MAC infection. These persons are very likely to have had agricultural occupations, so this association may also represent soil exposure not captured by our study instrument. In addition, persons born outside the United States who reside in western Palm Beach County are likely to have migrated there from equatorial areas, so their increased rate of positive MaS skin tests may reflect higher rates prevalent in their country of birth (31). Bacillus Calmette-Guérin vaccination was not associated with a positive MaS skin test in our study, nor did it change the associations seen between MAC infection and other predictors. This finding is consistent with the results of previous studies suggesting that Bacillus Calmette-Guérin may affect the tuberculin skin test but has little impact on the MaS skin test (32).
Epidemiologic studies have identified associations between various water sources and MAC disease in persons with advanced HIV infection (23, 24, 33). We did not find associations between water exposure and MAC infection in this study. Rather, associations with the water exposure variables were either absent or weakly protective. Previous studies have also shown an association between dairy products and MAC disease; hard cheese appeared to be a strong risk factor for disease in one study (22) but not another (25). We found a moderate association between soft cheese and MAC infection, but it did not remain significant after controlling for age, race, and foreign birth in the final model. None of the other dairy products, including hard cheese, Cuban cheese, or milk, were associated with MAC infection. A study of schoolchildren in Sweden suggested that having pet birds, dogs, or cats in the house was associated with MAC infection (8). Contact with pets was largely protective in our study and did not remain significant in multivariate models.
Although persons with HIV are at increased risk of MAC disease (1), HIV infection may interfere with a person's ability to mount a delayed hypersensitivity skin test response to either PPD or MaS, thus limiting the ability to detect MAC infection (34). Analysis of the HIV-infected participants in our survey found a lower prevalence of positive MaS skin tests than was found among HIV-uninfected patients, even after restricting the analysis to those HIV-infected subjects who were not anergic. This finding supports the conclusion that MAC disease among HIV-infected persons is more likely to result from recent acquisition of MAC than to be a reactivation of previously acquired infection. In addition, it is notable that no cases of disseminated MAC disease were seen in our HIV-infected subjects. In this regard, the high rates of tuberculosis in this area may have provided protection against MAC disease, as has been observed among HIV-infected persons in both the United States and developing countries (21, 35).
This study had several limitations. We were not able to quantify soil exposure but rather used duration of time in a soil-related occupation to represent soil exposure that would occur beyond normal activities of life. In addition, direct measurement of soil loading on skin surfaces of volunteers before and after soil-related occupational and recreational activities has shown that activities with more vigorous soil contact, such as soil-related occupations, yielded higher soil loading than other recreational activities (36). This finding indicates that our use of such soil-related occupations is an appropriate representation of significant soil-related exposure beyond what would be expected from normal activities of life. Participation in soil-related occupations has also been used as a proxy for soil exposure in the study of toxoplasmosis, a parasitic infection known to be transmitted through contact with soil (37).
On the basis of this classification of soil exposure, we were unable to distinguish which types of soil exposures may be particularly strong risk factors because we did not address other types such as gardening, yard work, or recreational exposure. Whether these other sources of soil exposure also increase risk, or whether heavy occupational exposure to soils is needed, remains unclear. In addition, the questionnaire did not distinguish whether these soil-related occupations also included water exposure (participation in irrigation, watering with a hose, etc.), and some overlap may be present. Nonetheless, this strong association between MAC infection and the several soil-related occupations supports a growing body of work indicating that soil exposure is a significant source of MAC infection.
Skin testing with MaS can present some cross-reactivity from other mycobacterial infections, notably M. tuberculosis, and can lead to misclassification of infection status. To distinguish between MAC infection and cross-reactivity, dual skin testing with MaS and PPD was used to determine the dominant reaction. This method of classifying skin test results by the dominant reaction has been shown to have high specificity and high sensitivity (5) in identifying MAC infection. We restricted our risk factor analyses to those with conclusive skin test results to ensure that we were evaluating true MAC infection. We were unable to draw conclusions about a fraction of our sample (25.5 percent, n = 114) because of inconclusive MaS skin test results. Because of imperfect sensitivity, some of these indeterminate reactions likely represent MAC infection. Although we are unable to determine which of these subjects had MAC infection, including all subjects with a MaS reaction of at least 5 mm in risk factor analyses yielded similar results (data not shown).
We found substantial rates of MAC infection in this community, although the rates were lower than have been reported previously from this area (4, 7). This difference could be due to use of a different skin test than that used in the earlier survey, or rates of MAC infection may have declined. Rates similar to those we observed have also been seen in many other areas of the southeastern United States (38), so the results of this study are likely to be generalizable to other communities where soil exposure is common and winters are mild.
MAC infection is common in many parts of the world and may provide some degree of protection from tuberculosis (39, 40). However, it also leads to disease in a proportion of infected hosts, particularly as one of the most common bacterial infections in patients with acquired immunodeficiency syndrome, accounting for increased morbidity and shortened survival. Whether the increased risk of infection with MAC requires heavy occupational exposure to soils, and whether sources of soil exposure other than those we studied are associated with increased risk, remains to be determined. Nonetheless, soil exposure should be considered a potential risk factor for MAC disease.
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ACKNOWLEDGMENTS |
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Support for this investigation was provided by the Centers for Disease Control and Prevention (cooperative agreements U64/CCU118611 and U64/CCU406791).
The authors acknowledge the staffs of the following Palm Beach County organizations: Glades Health Initiative, Inc.; the C.L. Brumback Health Center; and the Neighbors Organized for Adequate Housing for their assistance in performing the survey. They also thank Kaare Haaslov of Statens Seruminstitut for kindly donating the MaS skin test reagent.
Conflict of interest: none declared.
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