Outbreak of Tuberculosis Associated with a Floating Card Game in the Rural South: Lessons for Tuberculosis Contact Investigations

Transcription

1 1221 Outbreak of Tuberculosis Associated with a Floating Card Game in the Rural South: Lessons for Tuberculosis Contact Investigations Naomi N. Bock, John P. Mallory, Nell Mobley, Beverly DeVoe, and B. Brooks Taylor From the Department of Medicine, Emory University School of Medicine, and the Coastal Health District and the Epidemiology and Prevention Branch, Division of Public Health, Georgia Department of Human Resources, Atlanta, Georgia We investigated an outbreak of tuberculosis disease and infection in a rural southern county in which an average of less than one case per year had occurred in the previous 10 years. Nine cases of tuberculosis developed. Reinterview 19 months after the patient with the initial case presented revealed that he had participated in an illegal floating card game with two of the other patients; numerous other unacknowledged social connections among the patients existed. Restriction fragment length polymorphism typing revealed that mycobacteria isolated from five of six available specimens matched; the patient from whom the nonmatched mycobacterium was isolated had a coincident relapsed case. The infection rate among contacts decreased as the investigation expanded to include more than one-third of the county residents: from 51% of those named initially to 2% of those at a school screening and from 68% of those named by more than one patient to 20% of those named by only one patient. Maintaining effective tuberculosis control programs in areas in which the incidence is low will be a challenge as rates of tuberculosis continue to decline nationwide. The resurgence of tuberculosis in the United States more previously named contacts were also interviewed to elicit any than a decade ago was fueled in part by the epidemic of HIV social connections among them and to identify additional per- infection, immigration from areas in which tuberculosis is en- sons for an expanded contact evaluation. demic, and intrainstitutional transmission of Mycobacterium Contacts were evaluated with symptom screening for tuber- tuberculosis in hospitals and correctional facilities [1]. Tremenmethod culosis and a tuberculin skin test administered by the Mantoux dous efforts at rebuilding the tuberculosis control infrastructure that used 5 TU of PPD, and the results were read by and at targeting tuberculosis control programs to specific risk trained public health nurses and field staff. An induration of groups have contained the tuberculosis epidemic nationally, 5 mm at 48 to 72 hours was considered positive [3]. Contacts and rates of tuberculosis in 1997 were the lowest ever [2]. We with symptoms of tuberculosis or a positive tuberculin skin describe an outbreak of tuberculous disease and infection in a test underwent chest radiography and counseling on risk factors rural southern county in which there had been only seven cases for HIV infection and were offered HIV testing if indicated. of tuberculosis in the prior decade. This outbreak illustrates Contacts were evaluated for preventive isoniazid therapy ac- important issues confronting tuberculosis control programs as cording to current guidelines of the Centers for Disease Control rates of tuberculosis decline nationally. and Prevention [3]. M. tuberculosis isolates were available from six cases and Methods were sent to the Alabama Department of Public Health Bureau of Clinical Laboratories (Montgomery, AL) for analysis of In May 1996, the eighth case of tuberculosis diagnosed in restriction fragment length polymorphisms (RFLPs). DNA was one Georgia county within an 18-month period alerted local extracted, digested, and subjected to electrophoresis. The mempublic health officials to a possible outbreak. This rural county branes were hybridized with a fragment of the insertion se- (size, Ç400 square miles, population, õ10,000 people) has quence IS6110 to provide a characteristic DNA fingerprint esone of the lowest incomes per capita in the state. With concern tablished by the frequency and location of repeats of the about an outbreak, state, regional, and county public health insertion sequence [4]. The secondary probe ptbn12, a recom- personnel collaborated on an intervention. Patients with tubersequence binant plasmid containing a polymorphic GC-rich repetitive culosis were reinterviewed, and their family members and some insert, was employed for further discrimination of isolates with five or fewer copies of IS6110 [5]. The x 2 test or Fisher s exact test was used for statistical analysis of comparisons between group frequencies, and relative Received 25 February 1998; revised 24 June risks and 95% confidence intervals are reported. Analysis Reprints or correspondence: Dr. Naomi Bock, Division of Infectious Diseases, Emory University School of Medicine, 69 Butler Street, Atlanta, Georgia was done by using Epi-Info Version 6.0 [6] Case Reports Clinical Infectious Diseases 1998;27: Case 1. A 41-year-old African American man (index case) 1998 by the Infectious Diseases Society of America. All rights reserved /98/ $03.00 was suspected of having tuberculosis in November 1993; how-

2 1222 Bock et al. CID 1998;27 (November) ever, when initial cultures of sputum were negative for for acid-fast bacilli and a positive sputum culture 18.5 months M. tuberculosis, his physician decided that he did not have after case 1 was diagnosed. Although she did not reveal it tuberculosis and prescribed isoniazid as preventive therapy. during the initial contact interview, her brother lived in the The patient refused to take it. The patient then presented for household of patient 5, and she had visited there and socialized medical evaluation again in September 1994; examination of with patient 1 there. She was HIV-seronegative. sputum smears revealed acid-fast bacilli, and cultures of sputum Case 7. A 36-year-old African American man (who played were positive for M. tuberculosis. At the initial interview cards with patient 1, frequented the same nightclub as patient for contact investigation, he identified family and friends but 1, and coached at the county recreation department s after- did not disclose his participation in an ongoing illegal card school program that patients 2 and 4 attended) had pleural game, part-time work in a nightclub known as a site of illegal tuberculosis diagnosed on the basis of a positive pleural fluid drug selling, or a liaison with a woman of whom his wife was culture 18.5 months after case 1 was diagnosed. He was HIVseronegative. unaware. He was HIV-seronegative. Case 2. A 14-year-old African American boy had lym- Case 8. A 56-year-old African American man had had phatic tuberculosis diagnosed on the basis of a positive tuberculin tuberculosis in Pulmonary tuberculosis was diagnosed skin test and chest radiograph revealing abnormalities 6 on the basis of a sputum smear positive for acid-fast bacilli weeks after case 1 was diagnosed. More than 50% of the contacts and a positive sputum culture 19 months after case 1 was named initially by this patient were the same as those diagnosed. He had participated in a car pool with patient 1 but named by patient 1, but this occurrence was not considered as had not been named as a contact. He was HIV-seronegative. an indicator of a possible outbreak at the time. He denied risk Case 9. A 46-year-old African American man was found factors for HIV infection and refused testing. during neighborhood screening as part of an expanded contact Case 3. A 33-year-old African American man had pulmo- investigation (see below). He had pulmonary tuberculosis diagnosed nary tuberculosis diagnosed on the basis of a positive sputum on the basis of a sputum smear positive for acid-fast culture 7 months after case 1 was diagnosed. He played cards bacilli and a positive sputum culture. He denied any social with patient 1 but did not identify him as a contact. He was contact with the other patients, but his stepfather owned the HIV-seronegative. building in which the nightclub frequented by patients 1 and Case 4. A 16-year-old African American girl was named 7 operated. He was HIV-seronegative. as a contact by patient 3, her uncle. She had multiple connections to other patients that were not revealed until a follow-up investigation 6 months later: she lived next door to patient 1, Results attended school with patient 2, and participated in after-school activities at the recreation center with patient 7 (see below). Bacteriology She became pregnant shortly after starting preventive therapy The M. tuberculosis isolates from eight cases were susceptible with isoniazid, and therapy was discontinued, although isoniato all antituberculosis medications tested. No isolate was recovzid preventive therapy is recommended for pregnant women ered from patient 2, but he responded to treatment with firstwith recently acquired infection [3]. She developed symptoms line medications. Isolates from positive cultures of sputum from of tuberculosis during her eighth month of pregnancy, and patients 3 and 5 could not be obtained for RFLP typing. The cultures of sputum and amniotic fluid obtained at the time of characteristics of the nine cases are summarized in table 1. delivery yielded M. tuberculosis 12.5 months after case 1 was diagnosed. Her contacts were the same as those of patient 3 except for her boyfriend and infant. She was HIV-seronegative. Her infant had no signs of tuberculosis disease and was treated Contact Investigation with isoniazid preventive therapy. The contact investigation occurred in three stages. During Case 5. A 34-year-old African American HIV-seropositive initial interviews with the patients at the time of each diagnosis, woman had pulmonary tuberculosis diagnosed on the basis a 61 contacts were named, of whom 31 (51%) had positive tuberculin sputum smear positive for acid-fast bacilli and a positive sputum skin tests (figure 1). Nineteen months after the first patient culture 15.5 months after case 1 was diagnosed. She had presented, when it was recognized that there was an outbreak, a liaison with patient 1 that was not revealed to public health the patients were reinterviewed to determine missed intercon- personnel initially by either of them. She was noncompliant nections among them and to identify other contacts. More experienced with her antituberculosis treatment, and cultures of her sputum interviewers were used, and not only patients but also never became negative; she died 3 months after beginning their families and some of the previously named contacts were antituberculosis treatment. The treating physician listed tuberculosis interviewed. Two hundred eighty-two additional persons were and AIDS as causes of death. named and underwent tuberculin skin testing; 53 (19%) had Case 6. A 42-year-old African American woman had pulmonary positive skin tests. Twenty-one (68%) of 31 contacts named tuberculosis on the basis of a sputum smear positive by more than one patient had positive tests, compared with 63

3 CID 1998;27 (November) Tuberculosis Outbreak and Contact Investigations 1223 Table 1. Characteristics of patients with tuberculosis in an outbreak associated with a floating card game. Status of AFB sputum Other patients named smear at diagnosis of Time of as contacts during Case no.,* culture-positive HIV diagnosis Card game Matching follow-up contact age (y)/sex pulmonary tuberculosis serostatus (mo) player RFLP investigation 1, 41/M Positive Negative Yes Yes 3 8 2, 14/M ND Not tested 1.5 No NA 7 3, 33/M Negative Negative 7 Yes NA 1 and 7 4, 16/F Negative Negative 12.5 No Yes 1 and 7 5, 34/F Positive Positive 15.5 No NA 1 6, 42/F Positive Negative 18.5 No Yes 1 and 7 7, 36/M ND x Negative 18.5 Yes Yes 1 4 and 6 8, 56/M Positive Negative 19 No No 1 9, 46/M Positive Negative 20 No Yes None NOTE. AFB Å acid-fast bacillus; NA Å isolate not available for RFLP typing; ND Å not done; RFLP Å restriction fragment length polymorphism. * Cases are listed in order of diagnosis. Number of months after diagnosis of first case. Follow-up contact investigation conducted 19 months after the first case was diagnosed. Lymphatic tuberculosis. x Pleural tuberculosis. (20%) of 312 named by only one patient (RR, 6.47; 95% CI, contacts was high (19%), the contact investigation was expanded to persons from the identified community sites ). Reinterview of the patients, their families, and some of the A public health team went door to door in the four-block area contacts revealed the existence of a floating card game attended surrounding the home of each of the five patients who lived in by three of the patients. The card game, which involved illegal town, explaining the outbreak and offering tuberculin skin testing gambling, rotated every few weeks to a different home or back at that time. The neighborhoods consisted of unpaved roads room of a work site. Three other sites where transmission of where most of the residents lived in trailers. One hundred sixtytwo persons (94% of those approached in the neighborhood M. tuberculosis might have occurred were identified: a neighborhood where five of the patients lived, a nightclub where screening) agreed to tuberculin skin testing; 27 (17%) had positive tuberculin skin tests. One case of active tuberculosis (case patient 1 tended bar occasionally and patient 7 socialized, and the county school where patients 2 and 4 were students. Be- 9) was found during the neighborhood screening. cause the proportion of infected persons among the named The nightclub was known as a site of various illegal activi- ties, and public health officials believed that on-site contact evaluation would not be well received. Instead, posters were placed there encouraging patrons to come to the health department for tuberculin skin testing. Tuberculin skin testing was also made available to anyone in the county who requested it after media reports about the outbreak. Four hundred seven persons presented for tuberculin skin testing; 36 (9%) had positive skin tests. Compared with the named contacts, those persons who presented for tuberculin skin testing after communitywide media coverage were less likely to have positive tuberculin skin tests (RR, 0.51; 95% CI, ). Although the smear of sputum from the high school student with culture-positive pulmonary tuberculosis (case 4) was negative for acid-fast bacilli (making the patient less infectious), public health investigators decided to perform screening at the school to assuage the community s concern and to obtain epidemiological data on the prevalence of tuberculosis infection in the county. Fifteen hundred students, faculty, and employees Figure 1. Proportion of infected contacts detected by an expanding contact investigation of an outbreak of tuberculosis associated with of the school underwent tuberculin skin testing. Thirty-four a floating card game. * Å Reinterview of patients with tuberculosis persons (2%) had positive skin tests: three adults and 31 chil- that was conducted 19 months after the first case was diagnosed. dren between 6 and 18 years of age.

4 1224 Bock et al. CID 1998;27 (November) Ninety-seven of the 181 persons with positive tuberculin skin ities to participate in the contact investigation. Unlike a more tests were treated with isoniazid preventive therapy. Directly transient urban population, the stable population in this rural observed preventive therapy was used for the 42 children setting allowed the missed contacts to be detected when they treated, who made up 43% of the total treatment group. Of the developed active tuberculosis or to be identified during a fol- 84 adults who were not treated with preventive therapy, 5 low-up contact investigation when the outbreak was recognized had preexisting liver disease, 7 refused treatment, and 72 had 19 months after the index case was diagnosed. In addition, presented to the health department for screening but had no since the index patient had been prescribed isoniazid preventive identified exposure to any of the patients, were older than 35 therapy before developing acid-fast bacillus smear positive, years of age, and had no medical conditions putting them at culture-positive pulmonary tuberculosis but had refused to take increased risk for developing active tuberculosis [3]. Seventysix it, the subsequent outbreak demonstrates the high cost of misstherapy (78%) of those persons who started isoniazid preventive ing an opportunity for tuberculosis prevention. completed the prescribed course, including all of the Outbreaks of tuberculous disease and infection in low-inci- children. dence areas demonstrate the challenge of maintaining tuberculosis control expertise among staff who see few cases. Recent RFLP Analysis experience in high-incidence urban areas has shown the effectiveness of an army of specialist physicians, nurses, outreach Isolates recovered from six of the patients were available workers, peer counselors, and program staff in turning the tide for RFLP analysis. Five isolates had the same two-band chro- of a tuberculosis epidemic [9]. However, this highly successful mosomal DNA restriction pattern, with the secondary probe model is not directly transferable to areas in which fewer cases ptbn12 confirming that they were the same pattern (table 1). occur. Many rural counties have only one nurse to perform Four of the five patients for whom matching patterns were clinical and contact tracing roles. Even in more populous countfound acknowledged social interactions with the other patients ies, a few staff may manage not just tuberculosis but also child during the reinterview. The fifth patient (case 9) denied interactions immunization, sexually transmitted diseases, prevention of HIV with the other patients. However, 25% of his named infection, and other programs. Public health providers in this contacts were the same people named as contacts by the other setting must maintain expertise in multiple program areas, and patients. Another patient (case 8), for whom a nonmatching their training and supervision requirements differ from those eight-band chromosomal DNA restriction pattern was found, of providers who work full-time in tuberculosis programs. had had tuberculosis in 1988, and his case was considered a For instance, the rate of tuberculosis in Georgia has been relapse. higher than the national average for the last 25 years. In 1997, only 41% of the 696 cases in Georgia occurred in the two Discussion urban counties that make up the city of Atlanta. The other 407 cases occurred in the remaining 157 counties; the number of This outbreak of tuberculosis in the rural South, which resulted cases per county ranged from zero to 40 (average, 2.6) (Georgia in a rate of tuberculosis in the affected county of 86 Tuberculosis Control Program, unpublished data). Maintaining cases per 100,000 persons in 1996, demonstrates both known categorical tuberculosis programs (i.e., programs that are and new challenges for tuberculosis control programs. Delays funded and provide care by experienced medical personnel and in diagnosis and initiation of effective treatment in infectious social workers) is absolutely necessary, but outside of large cases, as occurred in case 1, are well documented to increase urban areas with high tuberculosis case loads, these programs transmission of M. tuberculosis [7, 8]. Less well documented may have to be reformatted to fit the changing epidemiology. are delays in recognizing contacts, as occurred in this outbreak. A new model for tuberculosis control programs could plan The follow-up investigation conducted 19 months after the for incremental increases in skills, with local public health staff index patient s case was diagnosed revealed that he could have having adequate expertise for initiating case management while identified his two card-playing associates (cases 3 and 7), his working within a network of more experienced supervisors and extramarital liaison (case 5), and another social contact (case consultants. In this type of network, direction of local public 6) at his initial contact interviews. All four patients presented health providers by regional supervisors would be standard, with tuberculosis disease 7 to 18.5 months later; isoniazid ther- timely, and effective. For example, a county nurse who might apy potentially could have prevented the progression of their manage four or five cases of tuberculosis a year would be infections to active disease. expected to report to and get feedback from a regional tuberculosis Three possible reasons for the delays include the following: supervisor within 1 week of encountering a new or sus- failure of local public health workers with limited previous pected case. The regional supervisor might thus indirectly manage tuberculosis control experience to recognize the extent of the 100 cases from multiple counties. The supervisors in exposure and to extend the investigation when a high propor- turn would be supported by state level specialists in medicine, tion of contacts were infected, failure of patients to disclose epidemiology, and behavioral and social aspects of tuberculosis illegal and illicit social contacts, and reluctance of racial minor- case management. Supervisors would have the expertise to

5 CID 1998;27 (November) Tuberculosis Outbreak and Contact Investigations 1225 recognize problems early, on the basis of ongoing epidemiolog- cases occur in racial and ethnic minorities [2]; all the cases in ical surveillance and case reviews; they would also have a this outbreak occurred in African Americans. Recent medical response plan ready to implement once a problem was detected, literature has recognized racial barriers to participation in clinical including access to trained personnel to constitute a response trials for both cancer and HIV infection or AIDS [13, 14], team. Challenges for tuberculosis control programs include and similar issues may discourage minority participation in maintaining the appropriate skill level for local public health contact investigations. Reported barriers to minority participa- providers who do not work exclusively in tuberculosis pro- tion in clinical trials include economic barriers such as lost grams as well as structuring reliable links to effective networks wages, transportation problems, fear and mistrust of health care of supervision and consultation. professionals and the system, and cultural beliefs or myths Illegal and illicit social connections, including gambling and about specific diseases. Strategies reported to be effective for drug-using partners and a woman with whom an extramarital recruiting minority populations into clinical trials might be liaison occurred, were not initially identified by the index patient useful for tuberculosis control programs to improve participapersons as contacts, nor did the subsequent patients among these tion in contact investigations. Such strategies include, but are identify the index patient as a contact. Mangura et not limited to, developing long-term relationships with commu- al. [10] recently described a tuberculosis miniepidemic that nities in which cases occur, employing community residents occurred after routine contact investigation failed to identify as health department staff, incorporating evening and weekend social contacts in a church choir. In the tuberculosis outbreak hours into the health department schedule to avoid disrupting associated with a floating card game, three cases and one death work schedules, and incorporating individuals cultures, tradi- might have been prevented had public health interviewers been tions, beliefs, and life-styles into educational materials [14]. able to encourage patients to reveal these contacts while assuring Some investigators have argued that tuberculosis transmisfor the confidentiality of the relationship. Invoking the model sion networks have become too complex to be recognized by incremental skills, an initial contact interview could be routine public health activities and that systematic RFLP analy- conducted by a multipurpose county public health nurse, which sis of strains within a population would more effectively elucidate would be followed by a second interview with a more highly transmission [15, 16]. Routine RFLP analysis of all speciwould trained investigator who could use language- and culture- mens would ultimately have revealed the tuberculosis outbreak appropriate communication methods to increase both the patient s associated with a floating card game, although probably not understanding of tuberculosis and his or her cooperation any earlier than it finally became apparent to local public health with the contact investigation. personnel. More importantly, systematic RFLP analysis would In fact, in this outbreak, some contacts were missed, not not have prevented this outbreak. because of the taboo of the social relationships, but because This tuberculosis outbreak in the rural South demonstrates the normal daily interconnections between them and the pa- new challenges for tuberculosis control programs in the United tients were not recognized by public health investigators. The States. As rates of tuberculosis continue to decline, fewer spe- extent to which people were in and out of one another s homes, cialists will be available, and arguments against retaining categorical cars, clubs, and overall environments was not revealed by the services for tuberculosis may resurface [17]. In the initial interviews. That transmission of M. tuberculosis was past, declining rates led to a loss of categorical funding and enhanced by the social dynamics of the community is shown deterioration of the tuberculosis control infrastructure, engen- by the results of the expanded contact investigation. First, there dering the resurgence of disease in the 1980s [18]. The expertise was a markedly increased risk of tuberculosis infection in contacts that has developed over the last 10 years should not be named by two or more patients compared with those lost but should be adapted to the changing epidemiology. named by only one patient (RR, 6.47; P õ.001). Second, the infection rate among those persons who presented to the health department for screening after a community outreach campaign References was significantly lower than that among those persons named 1. Cantwell MF, Snider DE Jr, Cauthen GM, Onorato IM. Epidemiology of when the patients were asked to identify anyone with whom tuberculosis in the United States, 1985 through JAMA 1994;272: they might have interacted (RR, 0.51; P õ.001). Behavioral Centers for Disease Control and Prevention. Tuberculosis morbidity research has stressed the need for health care providers to United States, MMWR Morb Mortal Wkly Rep 1998;47: understand the patient s social setting to improve adherence 3. American Thoracic Society. Treatment of tuberculosis and tuberculosis with antituberculosis treatment [11]. A similar understanding infection in adults and children. Am J Respir Crit Care Med 1994;149: may be necessary to increase cooperation with contact tracing, and both ethnography and social network analysis have been 4. Ross BC, Raios K, Jackson K, Dwyer B. Molecular cloning of a highly repeated DNA element from Mycobacterium tuberculosis and its uses recommended as tools to enhance contact investigations [12]. as an epidemiological tool. J Clin Microbiol 1992;30: Race may have played a role in the delayed recognition of 5. Chaves F, Yang Z, el Hajj H, et al. Usefulness of the secondary probe the extent of the tuberculosis exposure in this rural county. In ptbn12 in DNA fingerprinting of Mycobacterium tuberculosis. J Clin Georgia, as in the rest of the United States, most tuberculosis Microbiol 1996;34:

6 1226 Bock et al. CID 1998;27 (November) 6. Dean AG, Dean JA, Coulombier D, et al. Epi-info, version 6: a word 12. Rothenberg R, Narramore J. The relevance of social network concepts to processing, database, and statistics program for epidemiology on micro- sexually transmitted disease control. Sex Transm Dis 1996;23:24 9. computers. Atlanta: Centers for Disease Control and Prevention, el-sadr W, Capps L. The challenge of minority recruitment in clinical 7. MacIntyre CR, Plant AJ, Hulls J, Streeton JA, Graham NMH, Rouch GJ. trials for AIDS. JAMA 1992;267: High rate of transmission of tuberculosis in an office: impact of delayed 14. Swanson GM, Ward AJ. Recruiting minorities into clinical trials: toward diagnosis. Clin Infect Dis 1995;21: a participant-friendly system. J Natl Cancer Inst 1995;87: Allos BM, Gensheimer KF, Bloch AB, et al. Management of an outbreak 15. Genewein A, Telenti A, Bernasconi C, et al. Molecular approach to identiof tuberculosis in a small community. Ann Intern Med 1996;125: fying route of transmission of tuberculosis in the community. Lancet ;342: Small PM, Hopewell PC, Singh SP, et al. The epidemiology of tuberculosis 9. Frieden TR, Fujiwara PI, Washko RM, Hamburg MA. Tuberculosis in in San Francisco: a population-based study using conventional and mo- New York City turning the tide. N Engl J Med 1995;333: lecular methods. N Engl J Med 1994;330: Mangura BT, Napolitano EC, Passannante MR, McDonald RJ, Reichman 17. Hopewell PC. The baby and the bath water the case for retaining categor- LB. Mycobacterium tuberculosis miniepidemic in a church gospel choir. ical services for tuberculosis control in a reformed health care system. Chest 1998;113: Am J Respir Crit Care Med 1994;150: Sumartojo E. When tuberculosis fails: a social behavioral account of pa- 18. Reichman L. The U-shaped curve of concern. Am Rev Respir Dis 1991; tient adherence. Am Rev Respir Dis 1993;147: :741 2.