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Published ahead of print on October 19, 2006, doi:10.1164/rccm.200608-1092OC
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American Journal of Respiratory and Critical Care Medicine Vol 175. pp. 80-86, (2007)
© 2007 American Thoracic Society
doi: 10.1164/rccm.200608-1092OC

Original Article

Diagnostic Yield of Sputum, Induced Sputum, and Bronchoscopy after Radiologic Tuberculosis Screening

Otto D. Schoch, Philippe Rieder, Claudia Tueller, Ekkehardt Altpeter, Jean-Pierre Zellweger, Hans L. Rieder, Martin Krause and Robert Thurnheer

Pneumology, Kantonsspital St. Gallen, St. Gallen; Hospital Saint Loup, Pompaples; University Hospital Basel, Basel; Swiss Federal Office of Public Health; Swiss Lung Association, Bern; Tuberculosis Consultant Services, Kirchlindach; and Kantonsspital Münsterlingen, Münsterlingen, Switzerland

Correspondence and requests for reprints should be addressed to Otto D. Schoch, M.D., F.C.C.P., Pneumology, Kantonsspital St. Gallen, CH-9007 St. Gallen, Switzerland. E-mail: otto.schoch{at}kssg.ch


   ABSTRACT
TOP
 ABSTRACT
AT A GLANCE COMMENTARY
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Rationale: To assess feasibility and yield of diagnostic procedures after active case finding for tuberculosis with radiologic screening at the three main entry points for asylum seekers to Switzerland.

Method: Prospective multicenter study on the value of symptoms, spontaneous and induced sputum, and bronchoscopy for the confirmation of tuberculosis in radiologically selected cases.

Results: Among 101 asylum seekers examined, spontaneous sputum was collected "on the spot" in 83 and yielded 7 (54%) of 13 smear-positive and 13 (39%) of 33 culture-positive cases. Morning sputum, collected in 84, yielded 8 (62%) and 16 (49%), and the two spontaneous sputa combined 9 (69%) and 20 (61%), respectively. Two additional induced sputa, collected in 91 persons, yielded no additional smear-positive, but yielded seven culture-positive cases (yield, 82%). Bronchoscopy, performed in 87 of 92 sputum smear–negative cases, yielded four additional smear-positive and six culture-positive cases. Culture confirmation was independently and significantly predicted by obtaining a specimen using bronchoscopy (adjusted odds ratio, 11.0; 95% confidence interval, 1.9–62) and a prior decision to treat (adjusted odds ratio, 3.0; confidence interval, 1.1–8.1).

Conclusion: Radiographic anomalies compatible with tuberculosis found during screening are a poor guide to initiation of treatment. Respiratory and systemic symptoms correlated weakly with culture confirmation of tuberculosis. All radiologically selected cases must be examined with on-the-spot and early-morning sputum, regardless of symptoms. If both specimens are smear negative, the yield is increased by bronchoscopy and, to a lesser extent, by two samples of induced sputum. The examination of any single specimen has a low yield of 36 to 63% and is insufficient to exclude active tuberculosis.

Key Words: tuberculosis, pulmonary • immigrants • mass chest X-ray



   AT A GLANCE COMMENTARY
TOP
 ABSTRACT
 AT A GLANCE COMMENTARY
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Scientific Knowledge on the Subject
The examination of respiratory specimens to confirm suspected TB is standard of care. However, after radiologic TB case finding, the yields of on-the-spot spontaneous and induced sputum, morning sputum, and bronchoscopy have not been determined.

What This Study Adds to the Field
Radiographic abnormalities consistent with tuberculosis and found during screening are a poor indicator of the need for treatment. The addition of sputum testing and bronchoscopy improve diagnostic yield for tuberculosis.

 
Worldwide, tuberculosis is a major health problem, with an estimated eight million new cases and two million deaths occurring every year (1). In most industrialized countries, the control of tuberculosis has improved dramatically during the last century. The availability of effective chemotherapy, with the subsequent development of case management strategies aimed at efficiently reducing transmission of Mycobacterium tuberculosis, plays a major role (2). Today, passive case finding, based on the examination of spontaneously produced sputum samples from symptomatic patients, is the mainstay for the diagnosis of active tuberculosis (3, 4). The number of asylum seekers and immigrants to Western societies arriving from high-prevalence areas for tuberculosis has increased over the past decades and may pose a transmission risk to the resident population and to other asylum seekers (5, 6). Because the proportion of tuberculosis cases observed among foreign-born persons has been increasing in Western societies (7, 8), targeted, active case-finding programs for immigrants have been introduced, to supplement passive case-finding in the general population (9, 10). These programs are based on European recommendations endorsed by the World Health Organization (WHO) and the European Region of the International Union Against Tuberculosis and Lung Disease (8), and are aimed at diagnosing tuberculosis before or at the point of immigration, to reduce the risk of transmission within the country (11).

In Switzerland, where much higher prevalences of tuberculosis among immigrants have been reported, compared with what might be expected from the notification rates of incident cases in the resident population (12, 13), active case finding with a chest radiograph at the border point of entry has been mandated by the Swiss Federal Office of Public Health for asylum seekers, with a waiver for pregnant women and children below the age of 14 yr (14, 15). Pathologic findings on the radiographs are classified according to the likelihood of tuberculosis, and denoted with a specific code requiring an urgent need for medical examination because of suspicion of active tuberculosis (16). The aim of the present study is to ascertain the feasibility and the diagnostic yield of both spontaneous and induced sputum specimens at each of two points in time, on the spot and early morning, in the evaluation of asylum seekers with radiographs suggestive of tuberculosis requiring immediate attention. We have therefore conducted a prospective multicenter study in the three major Swiss accession centers for the registration of asylum seekers, where radiographic screening for tuberculosis is provided. Preliminary data of the study have been presented previously (17).


   METHODS
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 ABSTRACT
 AT A GLANCE COMMENTARY
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Subjects and Radiographs
During 2003 to 2005, annually, 10,000 to 15,000 asylum seekers were examined at five screening centers in Switzerland. From each center, chest radiographs were electronically transmitted to a reading facility in Lausanne. Radiographs demonstrating cavities, ill-defined infiltrates, multiple nodular infiltrates, or infiltrates with hilar or mediastinal enlargement were considered suggestive of tuberculosis. Single opacities were considered suggestive of tuberculosis if the opacity was larger than 2 cm or contained a central cavity (18). Asylum seekers with suggestive radiographs were referred to a hospital-based chest physician for further investigation.

Clinical Information
Red Cross nurses collected information on pulmonary symptoms (cough, sputum production), systemic symptoms (fever, night sweats, weight loss of > 5 kg in 6 mo), and history of tuberculosis. The specific questions were translated into 14 languages. Difficulties in communication were noted if no common language and no translation was available.

Collection of Spontaneous and Induced Sputum
At the hospital, cases with suspected tuberculosis were isolated in a well-ventilated single room, where spontaneous and induced sputum was collected. A sputum collection cup was given to the patient on arrival at the hospital, usually in the early afternoon. Patients were given verbal instructions and a leaflet with photographs explaining sputum collection. One hour was allowed for the production of spontaneous sputum, after which inhalation of 10 ml of 3% NaCl via an ultrasonic nebulizer (USV Economy U-3002-E; Schulte Elektronik, Osberg, Germany) was initiated in all patients. Induced on-the-spot sputum was collected after 15 to 30 min of inhalation. Likewise, the next morning, another set of spontaneous and induced morning sputum was collected.

Bronchoscopy
Only asylum seekers with smear-negative sputum were referred for bronchoscopy. An experienced physician performed bronchoscopy according to international standards (3). Washings of the central airways and of the involved lobes with 0.9% NaCl were performed and the fluid was collected for mycobacteriological examination.

Laboratory Workup
A laboratory certified for mycobacteriological diagnostics performed homogenization, decontamination, and cytocentrifugation according to international standards. Acid-fast bacilli were examined using bright-field (Ziehl-Neelsen) microscopy. The culture techniques used solid and liquid media for all collected specimens following standard procedures (19).

Data Collection
Data were collected and entered directly into an EpiData Entry database (20) (www.epidata.dk; EpiData Association, Odense, Denmark) at each study center. Recorded were center, age, sex, WHO region of origin, difficulty in communication, cough, sputum production, fever, weight loss, history of tuberculosis, and presence of cavity on chest radiograph. This was supplemented by subsequent results of smear and culture for on-the-spot and morning spontaneous and induced sputum, bronchial aspirate, as well as the clinicians' decision on tuberculosis treatment. The outcome could not be assessed, because asylum seekers were transferred to peripheral institutions.

Data Analysis
A positive culture in any of the collected respiratory specimens was defined as a case of confirmed tuberculosis. Univariate analysis was performed in EpiData Analysis (www.epidata.dk), comparing the characteristics of confirmed tuberculosis cases with all other cases with radiographs suggestive of active tuberculosis. To isolate independent predictor variables, a stepwise logistic regression model for the multivariate analysis was used (SYSTAT, version 10; SPSS, Inc., Chicago, IL). Odds ratios were calculated with 95% confidence intervals (CI).

Ethical Considerations
According to Swiss legislative guidelines, ethical committees of the cantons approved the study.


   RESULTS
TOP
 ABSTRACT
 AT A GLANCE COMMENTARY
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Between June 1, 2003, and May 30, 2005, all 101 asylum seekers with radiographs suggestive of active tuberculosis, referred to the three hospitals involved, were included in the study (52 in Münsterlingen, 35 in Hospital Saint Loup, Pompaples, and 14 at the University Hospital Basel). They had a mean age of 38 yr (SD ± 12.5 yr); 76 were male and 25 female. An overview of demographic characteristics, reported symptoms, and treatment decisions, comparing smear- and culture-positive (henceforth termed "smear-positive") and culture-only positive (henceforth termed "culture-positive") patients with tuberculosis, is given in Table 1. Thirty percent of the smear-positive and 35% of the culture-positive cases reported no respiratory symptoms; and in 39 and 55% of cases, respectively, no systemic manifestations of disease were recorded.


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  		TABLE 1. CHARACTERISTICS OF 13 PATIENTS WITH SMEAR-POSITIVE AND 20 PATIENTS WITH CULTURE-ONLY POSITIVE PULMONARY TUBERCULOSIS, RADIOGRAPHICALLY SCREENED WITHIN AN ACTIVE CASE-FINDING PROGRAM FOR ASYLUM SEEKERS AT THE SWISS BORDER

 
Despite considerable difficulties in communication reported for 32 of the 101 referred persons, on-the-spot sputum was collected in 83 and morning sputum in 84 persons. Induced sputum was obtained from 91 persons on both occasions. Five persons refused bronchoscopy after submitting four negative sputum samples (Table 2). Pulmonary tuberculosis was confirmed with at least one culture-positive specimen in 33 of the 101 radiologically selected cases of tuberculosis. Of these 33, 12 were also smear positive. In addition, one culture-negative patient had a positive smear of the bronchial aspirate. Of the culture-confirmed cases, nine were smear positive in sputum and three in bronchial aspirates alone. The yield of the four sputum specimens and of bronchial aspirates to detect smear- and culture-positive tuberculosis is given in Table 2. On-the-spot spontaneous sputum yielded 54% of the smear-positive and 39% of the culture-positive cases. With on-the-spot induced sputum, the yield for smear-positive cases was not increased, but the yield for culture-positive cases increased to 46%. Morning sputum was more sensitive, with a yield of 62% for smear- and 48% for culture-positive cases. With all four sputum specimens examined, 69% of the smear- and 82% of the culture-positive cases were detected. Bronchoscopy added four smear- and six culture-positive results (Table 2). Of the four individuals who tested smear positive by bronchoscopy only, one did not submit any sputum specimen, one submitted three negative sputa, and two submitted four negative sputa. Of the six individuals who were culture positive by bronchoscopy only, one did not submit any sputum specimen, one submitted only a negative on-the-spot spontaneous sputum, one submitted three, and three submitted four culture-negative specimens. Thirteen individuals (three cases with culture-confirmed tuberculosis) did not submit any spontaneous sputum; four individuals (one with smear-positive tuberculosis) submitted no sputum at all. The predictive negative values for spontaneous versus induced sputum for on-the-spot and early-morning specimens were very similar, ranging from 77 to 85%.


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  		TABLE 2. FEASABILITY AND DIAGNOSTIC YIELD OF ON-THE-SPOT SPONTANEOUS SPUTUM, ON-THE-SPOT INDUCED SPUTUM, MORNING SPONTANEOUS SPUTUM, MORNING INDUCED SPUTUM, AND BRONCHIAL WASHINGS FOR THE DETECTION OF SMEAR- AND CULTURE-POSITIVE TUBERCULOSIS IN ASYLUM SEEKERS WITH RADIOLOGICALLY SUSPECTED TRANSMISSIBLE TUBERCULOSIS, SCREENED WITHIN AN ACTIVE CASE-FINDING PROGRAM AT THE SWISS BORDER

 
Demographic characteristics, symptoms, and initial treatment decisions are reported for the 33 culture-positive and the 68 culture-negative subjects in Table 3. Asylum seekers with confirmed tuberculosis were more likely to have had bronchial excretions examined (adjusted odds ratio [OR], 11.0; 95% CI, 1.9–62), and to have been started on antituberculosis treatment (adjusted OR, 3.0; 95% CI, 1.1–8.1; Figure 1). Cavitary appearance on chest radiographs, age, sex, region of origin, history of previous tuberculosis, and communication difficulties were not significantly associated with culture confirmation.


Figure 1
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  		Figure 1. Stepwise logistic regression analysis for the prediction of culture-confirmed tuberculosis among 101 asylum seekers to Switzerland, radiographically selected because of findings suggestive of tuberculosis. Open circles: crude odds ratio; closed circles: adjusted odds ratio.

 

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  		TABLE 3. DEMOGRAPHIC CHARACTERISTICS, REPORTED SYMPTOMS, AND TREATMENT DECISION OF ASYLUM SEEKERS WITH RADIOGRAPHS SUGGESTIVE OF INFECTIOUS TUBERCULOSIS

 
Smear results, treatment decisions taken, and the final culture results for asylum seekers with and without clinical symptoms are shown in Figure 2. Nine of the 33 patients with culture-confirmed tuberculosis had treatment initiated only after the positive culture result became available, whereas in 28 persons initially placed on treatment, tuberculosis was not subsequently confirmed by culture.


Figure 2
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  		Figure 2. Flow chart for 101 asylum seekers with radiologically suspected tuberculosis with and without symptoms, smear results, treatment decisions, and final culture results. Neg, negative; Pos, positive.

 

   DISCUSSION
TOP
 ABSTRACT
 AT A GLANCE COMMENTARY
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
With this prospective multicenter study, we have systematically determined the contribution of various diagnostic steps to the confirmation of radiographically suspected pulmonary tuberculosis. In contrast to a retrospective investigation (21) and to studies evaluating diagnostic strategies in individuals with symptoms suggestive of tuberculosis presenting in passive case finding or in mixed populations (22–25), our study was conducted prospectively and in a well-defined population, selected with active radiologic case finding. This study confirms that, with the help of instructive material and interpreter services, it is possible to collect clinical information as well as spontaneous and induced sputum specimens and bronchial aspirates in the vast majority of asylum seekers, despite important language and culture barriers. Overall, tuberculosis was confirmed in a third of the persons with radiographs suggestive of tuberculosis, making radiography considerably less specific than the 66 to 82% previously reported among patients hospitalized with suspicion of active tuberculosis (10). Noteworthy is that in nearly one-third of subsequently culture-confirmed cases, no treatment was initiated based on clinical and radiographic findings alone, whereas, in contrast, nearly a third of unconfirmed cases were started on chemotherapy. Radiographic case finding alone thus represents a poor basis for initiation of antituberculosis therapy.

Symptoms
In passive case finding, it is usually the presence of symptoms that triggers the patient to seek medical care. Patients with tuberculosis often have a gradual onset of symptoms over a period of weeks, which may not be noticed (26) or are neglected by the patient for some time. This can result in delays of weeks or even months until medical advice is sought (27–30). The observed variation in the proportion of smear-positive patients not attending health care facilities is attributable to a combination of factors (31). Absence of reported symptoms is generally considered insufficient evidence to exclude infectious tuberculosis, particularly in persons identified through radiographic screening (32). Our study is in line with these observations, because one-third of patients with culture-confirmed tuberculosis reported no respiratory symptoms, whereas nearly half reported no systemic manifestations of disease. On the other hand, half of those without confirmation of tuberculosis did report symptoms, highlighting the fact that reporting symptoms is a very poor predictor in this setting. Denial of symptoms by the asylum-seeking patients for various reasons, including (unfounded) fear for personal consequences, may be contributing to the low sensitivity of clinical symptoms.

Collection of Respiratory Specimens and Diagnostic Yield
The collection of spontaneously produced sputum in symptomatic patients is standard of care in passive case finding (3, 4). It is the diagnostic tool of choice in the directly observed therapy, short course (DOTS) strategy for tuberculosis control programs all over the world (33). In clinical practice, a sensitivity of 45 to 83% has been reported for sputum smear microscopy, with a generally high specificity above 98% (4, 34–36). Serial sputum samples increase the yield, albeit with a rapidly diminishing return (37, 38). With important deviations, a common observation is that approximately 85, 10, and 5% of all cases found with three serial examinations are found on the first, second, and third sputum smear examination, respectively (38, 39). This is the largest study with data on sputum collected simultaneously by two methods (spontaneous and induced) at two time points (on the spot and in the morning). Sputum collection was successful in over 80% of the persons examined. Nevertheless, in our study, the yield of a single respiratory specimen was lower because several cases were identified only from the specimen collected by bronchoscopy. The yield for culture-positive tuberculosis from a single specimen of spontaneous or induced sputum was also relatively low, with less than half of the cases detected with a single specimen. In accordance with other studies, the yield from the morning sputa was higher than from specimens collected on the spot (40, 41). This is the rationale behind the widely recommended diagnostic standard to include the collection of at least one morning sputum in the diagnostic workup of cases of suspected tuberculosis (4, 42). In our study, the collection of two spontaneous sputa yielded only about two-thirds of the smear- and culture-positive cases. This relatively low yield is not directly comparable to other studies because the total yield of cases is partially explained by the inclusion of other than spontaneously produced specimens in the denominator.

Sputum induction, the provocation of bronchial secretions by inhalation of hypertonic saline to increase sensitivity for the detection of acid-fast bacilli, was first reported in the 1960s (43–45), but virtually no reports of its use were published during the 1980s, when bronchoscopy became widely available (46–48). In one retrospective chart review of patients able to produce sputum, no benefit for sputum induction compared with the collection of spontaneous sputum was observed (49). However, improved sensitivity and a clear benefit in patients unable to produce sputum have been reported in several other, more recent studies examining induced sputum (22–24, 50–52). Prospective studies have found equal performance for induced sputum and bronchoscopy in a mixed population of cases with clinical and radiologic findings suggestive of tuberculosis who are unable to produce spontaneous sputum (22–24). In our study, induced sputum added no smear-positive cases to those detected by two spontaneous sputa, confirming the retrospective results reported by Merrick and coworkers (49). The yield of a single specimen of induced sputum was equal to a single specimen of spontaneous sputum. However, if results are combined, the yield increased from 60 to more than 80% for culture-positive tuberculosis, with the collection of the two additional induced sputa adding 7 more to the total of 33 cases. Therefore, in settings where bronchoscopy is unavailable, the collection of induced sputum allows an increased diagnostic yield, in contrast to the examination of more than three samples of spontaneous sputum (4, 41).

Bronchial aspirates obtained during bronchoscopy considerably increased the diagnostic yield, with four additional smear-positive cases. On the other hand, the examination of bronchial aspirates alone would have missed nine cases of culture-positive tuberculosis. A single specimen has a low sensitivity, even if obtained by bronchoscopy. The combination of three specimens, examination of an on-the-spot spontaneous sputum, and a morning spontaneous sputum plus bronchial aspirates provided the best results, not missing any smear-positive and missing only three of 33 culture-positive cases, whereas the examination of two spontaneous and two induced sputum specimens, omitting bronchoscopy, would have missed four smear- and six culture-positive cases.

Recommendations to Clinicians
The diagnostic performance of symptoms and clinical findings is disappointing. Therefore, the collection of respiratory specimens in cases with radiologic findings suggestive of tuberculosis is mandatory, even if no symptoms are reported. On the basis of our findings, we recommend that all cases with radiologic findings suggestive of tuberculosis be examined with two sputum specimens, one on-the-spot sputum and one early-morning sputum. If both these specimens are smear negative, the examination of a bronchoscopically collected specimen is recommended. In settings where bronchoscopy is not easily available, the collection of induced sputum offers a valuable alternative to bronchoscopy. Collecting induced sputum is feasible and increases the yield of two spontaneous sputum specimens.

The examination of a single specimen, even if collected by bronchoscopy, is insufficient to exclude active tuberculosis, given the low yield of 36 to 63% in detecting culture-confirmed tuberculosis for any single specimen in our study. Therefore, bronchoscopy must always be supplemented by additional sputum examinations to increase diagnostic accuracy.

In conclusion, this study shows that radiographic findings suggestive of tuberculosis found during screening of asylum seekers are a poor guide to initiation of antituberculosis treatment. Similarly, respiratory symptoms and systemic disease manifestations correlated weakly with culture confirmation of tuberculosis. The results show that the yield from two spontaneous sputum samples was lower than expected and was improved with the additional collection of induced sputum and bronchial aspirates. Bronchial aspirates added more than two additional induced sputa to improve the diagnostic yield.


   Acknowledgments
 
The authors thank the Swiss Respiratory Society for funding this study; the staff of the Swiss Red Cross at the border posts in Basel, Münsterlingen, and Vallorbe for their efforts in filling out the questionnaires; the nurses and staff of the hospitals in Münsterlingen, Saint-Loup, and Basel for their efforts in collecting sputum; and the laboratory staff for processing of the specimens.


   FOOTNOTES
 
Supported by the Swiss Respiratory Society.

Originally Published in Press as DOI: 10.1164/rccm.200608-1092OC on October 19, 2006

Conflict of Interest Statement: None of the authors has a financial relationship with a commercial entity that has an interest in the subject of this manuscript.

Received in original form August 4, 2006; accepted in final form October 19, 2006


   REFERENCES
TOP
 ABSTRACT
 AT A GLANCE COMMENTARY
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. World Health Organization. Global tuberculosis control: surveillance, planning, financing. Geneva, Switzerland: World Health Organization; 2006. Publication No. WHO/HTM/TB/2006.
  2. Dye C, Watt CJ, Bleed DM, Hosseini SM, Raviglione MC. Evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally. JAMA 2005;293:2767–2775.[Abstract/Free Full Text]
  3. American Thoracic Society; Centers for Disease Control and Prevention. Diagnostic standards and classification of tuberculosis in adults and children. Am J Respir Crit Care Med 2000;161:1376–1395.[Free Full Text]
  4. Tuberculosis Coalition for Technical Assistance. International Standards for Tuberculosis Care (ISTC). The Hague. Available from: http://www.who.int/tb/publications/2006/istc_report.pdf (accessed November 8, 2006).
  5. Borgdorff MW, Nagelkerke N, Van Soolingen D, de Haas PE, Veen J, van Embden JD. Analysis of tuberculosis transmission between nationalities in the Netherlands in the period 1993–1995 using DNA fingerprinting. Am J Epidemiol 1998;147:187–195.[Abstract/Free Full Text]
  6. Lillebaek T, Andersen AB, Bauer J, Dirksen A, Glismann S, de Haas P, Kok-Jensen A. Risk of Mycobacterium tuberculosis transmission in a low-incidence country due to immigration from high-incidence areas. J Clin Microbiol 2001;39:855–861.[Abstract/Free Full Text]
  7. EuroTB; National Coordinators for Tuberculosis Surveillance in the WHO European Region. Surveillance of tuberculosis in Europe: report on tuberculosis cases notified in 2004. Available at: http://www.eurotb.org/rapports/2004/eurotb_report_2004.pdf (accessed November 8, 2006).
  8. Rieder HL, Zellweger JP, Raviglione MC, Keizer ST, Migliori GB. Tuberculosis control in Europe and international migration. Eur Respir J 1994;7:1545–1553.[Abstract]
  9. Catlos EK, Cantwell MF, Bhatia G, Gedin S, Lewis J, Mohle-Boetani JC. Public health interventions to encourage TB class A/B1/B2 immigrants to present for TB screening. Am J Respir Crit Care Med 1998; 158:1037–1041.[Abstract/Free Full Text]
  10. Dasgupta K, Menzies D. Cost-effectiveness of tuberculosis control strategies among immigrants and refugees. Eur Respir J 2005;25:1107–1116.[Abstract/Free Full Text]
  11. Bothamley GH, Rowan JP, Griffiths CJ, Beeks M, McDonald M, Beasley E, van den Both C, Feder G. Screening for tuberculosis: the port of arrival scheme compared with screening in general practice and the homeless. Thorax 2002;57:45–49.[Abstract/Free Full Text]
  12. Bonvin L, Zellweger JP. Mass miniature X-ray screening for tuberculosis among immigrants entering Switzerland. Tuber Lung Dis 1992;73:322–325.[CrossRef][Medline]
  13. Bucher H, Weinbacher M, Gyr K. Compliance von Asylbewerbern mit der erweiterten grenzsanitarischen Untersuchung im Kanton Basel-Stadt 1992–1993. Schweiz Med Wochenschr 1994;124:1660–1665.[Medline]
  14. Bundesamt für Gesundheitswesen. Grenzsanitätsdienstliche Untersuchung bei Asylbewerbern [pt. 1]. Bundesamt für Gesundheit (BAG) Bulletin 1995;4:3–5.
  15. Bundesamt für Gesundheitswesen. Grenzsanitätsdienstliche Untersuchung [pt. 2]. Bundesamt für Gesundheit (BAG) Bulletin 1995;15: 17–20.
  16. Bundesamt für Gesundheit, Lungenliga Schweiz; Zellweger JP. Vorgehen bei Verdacht auf Tuberkulose bei Asylsuchenden. Bundesamt für Gesundheit (BAG) Bulletin 2000;46:907–908.
  17. Schoch OD, Tueller C, Zellweger JP, Thurnheer R. The role of induced sputum and bronchoscopy for the assessment of asylum seekers with radiographs suggesting infectious tuberculosis. Eur Respir J 2004; 24:206s.
  18. Zellweger JP, Heinzer R, Touray M, Vidondo B, Altpeter E. Intra-observer and overall agreement in the radiological assessment of tuberculosis. Int J Tuberc Lung Dis 2006;10:1123–1126.[Medline]
  19. Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH. Manual of clinical microbiology, 7th ed. Washington, DC: ASM Press; 1999.
  20. Lauritsen JM, Bruus M. EpiData Entry (version 2.1b, 2002). A comprehensive tool for validated entry and documentation of data. EpiData Association, Odense, Denmark; 2000–2006.
  21. Bell D, Leckie V, McKendrick M. The role of induced sputum in the diagnosis of pulmonary tuberculosis. J Infect 2003;47:317–321.[CrossRef][Medline]
  22. Conde MB, Soares SL, Mello FC, Rezende VM, Almeida LL, Reingold AL, Daley CL, Kritski AL. Comparison of sputum induction with fiberoptic bronchoscopy in the diagnosis of tuberculosis: experience at an acquired immune deficiency syndrome reference center in Rio de Janeiro, Brazil. Am J Respir Crit Care Med 2000;162:2238–2240.[Abstract/Free Full Text]
  23. Al Zahrani K, Al Jahdali H, Poirier L, Rene P, Menzies D. Yield of smear, culture and amplification tests from repeated sputum induction for the diagnosis of pulmonary tuberculosis. Int J Tuberc Lung Dis 2001;5:855–860.[Medline]
  24. Anderson C, Inhaber N, Menzies D. Comparison of sputum induction with fiber-optic bronchoscopy in the diagnosis of tuberculosis. Am J Respir Crit Care Med 1995;152:1570–1574.[Abstract]
  25. Larson JL, Ridzon R, Hannan MM. Sputum induction versus fiberoptic bronchoscopy in the diagnosis of tuberculosis. Am J Respir Crit Care Med 2001;163:1279–1280.[Free Full Text]
  26. Ravessoud M, Zellweger JP. Présentation clinique de la tuberculose chez les immigrants vus au Dispensaire Antituberculeux de Lausanne. Schweiz Med Wochenschr 1992;122:1037–1043.[Medline]
  27. Wandwalo ER, Morkve O. Delay in tuberculosis case-finding and treatment in Mwanza, Tanzania. Int J Tuberc Lung Dis 2000;4:133–138.[Medline]
  28. Rajeswari R, Chandrasekaran V, Suhadev M, Sivasubramaniam S, Sudha G, Renu G. Factors associated with patient and health system delays in the diagnosis of tuberculosis in South India. Int J Tuberc Lung Dis 2002;6:789–795.[Medline]
  29. Godfrey-Faussett P, Kaunda H, Kamanga J, van Beers S, van Cleeff M, Kumwenda-Phiri R, Tihont V. Why do patients with a cough delay seeking care at Lusaka urban health centres? A health systems research approach. Int J Tuberc Lung Dis 2002;6:796–805.[Medline]
  30. Pirkis JE, Speed BR, Yung AP, Dunt DR, MacIntyre CR, Plant AJ. Time to initiation of anti-tuberculosis treatment. Tuber Lung Dis 1996;77:401–406.[CrossRef][Medline]
  31. Kimerling ME, Shakes CF, Carlisle R, Lok KH, Benjamin WH, Dunlap NE. Spot sputum screening: evaluation of an intervention in two homeless shelters. Int J Tuberc Lung Dis 1999;3:613–619.[Medline]
  32. Ministry of Health and Welfare; Korean National Tuberculosis Association. Report on the 7th Tuberculosis Prevalence Survey in Korea—1995. Seoul, Korea: The Korean Institute of Tuberculosis; 1996.
  33. Maher D, Mikulencak M. What is DOTS? A guide to understanding the WHO-recommended TB control strategy known as DOTS. Geneva, Switzerland: World Health Organization; 1999. Document No. WHO/CDS/CPC/TB/99.270.
  34. Gordin F, Slutkin G. The validity of acid-fast smears in the diagnosis of pulmonary tuberculosis. Arch Pathol Lab Med 1990;114:1025–1027.[Medline]
  35. Lipsky BA, Gates J, Tenover FC, Plorde JJ. Factors affecting the clinical value of microscopy for acid-fast bacilli. Rev Infect Dis 1984;6:214–222.[Medline]
  36. Woods GL, Pentony E, Boxley MJ, Gatson AM. Concentration of sputum by cytocentrifugation for preparation of smears for detection of acid-fast bacilli does not increase sensitivity of the fluorochrome stain. J Clin Microbiol 1995;33:1915–1916.[Abstract]
  37. Blair EB, Brown GL, Tull AH. Computer files and analyses of laboratory data from tuberculosis patients. II. Analyses of six years' data on sputum specimens. Am Rev Respir Dis 1976;113:427–432.[Medline]
  38. Mabaera B, Naranbat N, Dhliwayo P, Rieder HL. Efficiency of serial smear examinations in excluding sputum smear-positive tuberculosis. Int J Tuberc Lung Dis 2006;10:1030–1035.[Medline]
  39. Urbanczik R. Present position of microscopy and of culture in diagnostic mycobacteriology. Zentralbl Bakteriol Mikrobiol Hyg [A] 1985;260: 81–87.
  40. Gopi PG, Subramani R, Selvakumar N, Santha T, Eusuff SI, Narayanan PR. Smear examination of two specimens for diagnosis of pulmonary tuberculosis in Tiruvallur District, south India. Int J Tuberc Lung Dis 2004;8:824–828.[Medline]
  41. Van Deun A, Salim AH, Cooreman E, Hossain MA, Rema A, Chambugonj N, Hye MA, Kawria A, Declercq E. Optimal tuberculosis case detection by direct sputum smear microscopy: how much better is more? Int J Tuberc Lung Dis 2002;6:222–230.[Medline]
  42. Crofton J, Horne N, Miller F. Clinical tuberculosis, 2nd ed. Macmillan Education Ltd, London and Basingstoke; 1992.
  43. Hensler MM, Spivey CC, Dees TM. The use of hypertonic aerosol in production of sputum for diagnosis of tuberculosis. Dis Chest 1961; 40:639–642.[Medline]
  44. Yue WY, Cohen SS. Sputum induction by newer inhalation methods in patients with pulmonary tuberculosis. Dis Chest 1967;51:614–620.
  45. Betten MG, Newberry MD. A permanent sputum-induction cubicle. Am Rev Respir Dis 1968;98:711–712.[Medline]
  46. Danek SJ, Bower JS. Diagnosis of pulmonary tuberculosis by flexible fiberoptic bronchoscopy. Am Rev Respir Dis 1979;119:677–679.[Medline]
  47. Uddenfeldt M, Lundgren R. Flexible fiberoptic bronchoscopy in the diagnosis of pulmonary tuberculosis. Tubercle 1981;62:197–199.[CrossRef][Medline]
  48. de Gracia J, Curull V, Vidal R, Riba A, Orriols R, Martin N, Morell F. Diagnostic value of bronchoalveolar lavage in suspected pulmonary tuberculosis. Chest 1988;93:329–332.
  49. Merrick ST, Sepkowitz KA, Walsh J, Damson L, McKinley P, Jacobs JL. Comparison of induced versus expectorated sputum for diagnosis of pulmonary tuberculosis by acid-fast smear. Am J Infect Control 1997;25:463–466.[CrossRef][Medline]
  50. Li LM, Bai LQ, Yang HL, Xiao CF, Tang RY, Chen YF, Chen SM, Liu SS, Zhang SN, Ou YH, et al. Sputum induction to improve the diagnostic yield in patients with suspected pulmonary tuberculosis. Int J Tuberc Lung Dis 1999;3:1137–1139.[Medline]
  51. Parry CM, Kamoto O, Harries AD, Wirima JJ, Nyirenda CM, Nyangulu DS, Hart CA. The use of sputum induction for establishing a diagnosis in patients with suspected pulmonary tuberculosis in Malawi. Tuber Lung Dis 1995;76:72–76.[Medline]
  52. McWilliams T, Wells AU, Harrison AC, Lindstrom S, Cameron RJ, Foskin E. Induced sputum and bronchoscopy in the diagnosis of pulmonary tuberculosis. Thorax 2002;57:1010–1014.[Abstract/Free Full Text]



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