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Exposure of dentists to Mycobacterium tuberculosis, Ibadan, Nigeria.

Tuberculosis (TB) is a serious public health concern globally, and almost half of new infections are undetected (1). The infection is spread by airborne droplet nuclei that contain Mycobacterium tuberculosis, which remain airborne for minutes to hours after expectoration through coughing, sneezing, or talking by persons with pulmonary TB (2).

Acquisition of TB in healthcare facilities is a well-recognized hazard for healthcare workers and patients. Dental practitioners may be at increased risk because they work in close proximity to potentially infectious secretions (3). The risk is higher in areas like Nigeria, where TB is endemic; control practices are poor; and compliance with guidelines for preventing TB in healthcare facilities, such as those issued by the US Centers for Disease Control and Prevention (4), is limited.

We initiated this study to assess the risk for exposure of dentists to M. tuberculosis infection and to determine its prevalence among dental patients. Participants were patients in the dental clinic of University College Hospital, Ibadan, Nigeria, the largest hospital in the country.

The Study

This study was conducted in the dental center of University College Hospital, a tertiary hospital located in Ibadan, Oyo State, southwestern Nigeria. Nigeria, which has a population of >140 million, is rated as fourth among TB-endemic nations, with a prevalence of 521 cases per 100,000 population during 2007 (5). Ethical clearance for the study was obtained from the Oyo State Ethical Review Board as part of a multifocused study of TB in the state.

The dental center comprises 7 units that provide care to [approximately equal to]1,800 patients annually. This study was carried out in the Oral Surgery Clinic, one of the units in the center where a member of the study team is a consultant. Patients were recruited during February 2006 through July 2007. A total of 312 consecutive patients who came to the clinic for treatment were invited to participate; 101 gave consent (23/101 patients were excluded because they could not produce a sputum sample). Thus, 78 patients were evaluated.

Each participant completed a structured questionnaire that requested information about age, sex, occupation, bacille Calmette-Guerin (BCG) vaccination, history of chronic cough or TB, HIV status, and contact with a patient who had chronic cough or TB. A single expectorated sputum sample was collected from each participant and placed in a sterile universal container. Collection was done through the support of medical house officers/registrars posted to the unit; a consultant (1 of the study group members) was responsible for overall supervision.

The sputum specimen and culture were processed by using a standard procedure as described by Cadmus et al. (6). Using the Ziehl-Neelsen technique, we performed smear microscopy. Isolates were harvested for molecular typing analysis by scraping the growth from a slope into 200 [micro]L of distilled water and heating the product at 80[degrees]C for 1 h.

Molecular identification of isolates was conducted in the Veterinary Laboratories Agency, Addlestone, Surrey, UK, by spoligotyping as described by Kamerbeek et al. (7) with minor modifications and repeated at the Center for Infectious Disease Control (RIVM) in the Netherlands. Furthermore, the Hain Genotype Mycobacterium tuberculosis complex (MTBC) test (Hain Lifescience, Nehren, Germany) was applied to determine whether an isolate was a member of the MTBC, after which the Hain line probe assay identification kit for subspecies of MTBC was applied (Hain Lifescience).

Seventy-eight dental patients who could give a sputum sample consented to participate in the study. Forty-one (52%) participants were women; median age was 32 years. A total of 20 participants (26%) reported having received BCG vaccine, and 10 reported prior exposure to a person with chronic cough or with TB. None of the participants reported a personal history of chronic cough or TB. Ten (13%) of the 78 participants had culture-confirmed TB, 7 of whom had initial positive acid-fast bacilli (AFB) smears through concentrated sputum samples. The HIV status of 70 respondents (including those with TB) was unavailable, and 1 of the remaining 8 respondents reported being positive for HIV during questionnaire/ sample collection. The demographic characteristics, AFB smear results, BCG vaccination history, and known TB exposure of the participants with mycobacterial growth are presented in the Table.

Spoligotyping in the United Kingdom and repeated molecular identification in the Netherlands identified the strains as M. tuberculosis. In spoligotyping, different genotypic patterns were visualized (8), which limited the possibility of laboratory cross-contamination.


In patients who sought treatment at the dental clinic of a tertiary hospital in Nigeria, we found an unexpectedly high rate of unrecognized infection with pathogenic mycobacteria. Ten (13%) of 78 study participants who provided sputum samples were infected with M. tuberculosis. Our findings corroborate other studies of TB cases and show that AFB smears alone would miss some infected patients. M. tuberculosis is transmitted with high efficiency to household contacts (9), and transmission of mycobacteria, including multidrug-resistant M. tuberculosis strains, from dental patients to dental practitioners, probably occurs (10). Accordingly, infected participants in this study, especially those who had positive AFB smears, were, in principle, capable of infecting dental practitioners and other patients. Reports from other settings suggest that the threat of TB transmission from clients to dentists is not only theoretical (11). This extremely high percentage of undiagnosed AFB positivity is of public health concern because dental clinics in TB-endemic areas are not usually considered a place of high risk for TB transmission; therefore, preventive measures are not routinely implemented.

This study has several limitations. First, patients were recruited from only 1 of the 7 units in the dental center, constricting the pool of patients invited to participate. However, all patients visiting the center were exposed to similar conditions, and the patients who came to the oral surgery clinic had often been referred from other units in the dental center. Second, only 1 sputum sample was collected from each participant. The yield possibly would have been higher if we had collected more samples. Third, dental problems (12) and TB (13) are major comorbidities among persons infected with the HIV, and the synergism between M. tuberculosis and HIV is well documented. Because we did not collect complete histories on the HIV status of participants, we are unable to delineate the role of HIV with respect to our observations. However, in 2003, the same clinic recorded a 2.3% HIV prevalence among 300 patients screened for oral surgery (14); the 2008 prevalence data for the state was 2.2% (15). Fourth, our study was conducted in the dental clinic of the major tertiary hospital in 1 of the largest cities in Nigeria; thus, the findings may not be generalizable to all facilities where dental care is provided. Nevertheless, a surprisingly high proportion of dental patients in this study had potentially infectious TB. Therefore, evidence-based strategies should be implemented to quickly diagnose TB and prevent its transmission in dental clinics. Of particular importance in preventing nosocomial TB in dental clinics will be the adoption of infection control measures that may include the use of appropriate masks. Finally, our study also emphasizes the view that active case finding in high prevalence settings could be beneficial.


We thank Kehinde Adesokan and Melissa Okker for technical assistance.

This work was funded by the authors.

Dr Cadmus is the coordinator of the Tuberculosis Research Laboratory of the Department of Veterinary Public Health and Preventive Medicine, University of Ibadan. His research interests include the epidemiology of TB in humans and animals and TB diagnostics, as well as other diseases of public health importance.


(1.) World Health Organization. Global tuberculosis control: surveillance, planning, financing. Geneva: The Organization. 2008 [cited 2008 Dec 14]. WHO_2008_global_TB_report.pdf

(2.) Louden RG, Roberts RM. Droplet expulsion from the respiratory tract. Am Rev Respir Dis. 1966;95:435-42.

(3.) Harlow RF and Rutkauskas, JS. Tuberculosis risk in the hospital dental practice. Spec Care Dentist. 1995;15:50-5. DOI: 10.1111/j.1754-4505.1995.tb00476.x

(4.) Centers for Disease Control and Prevention. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care facilities. MMWR Recomm Rep. 2005;54(RR-17):1-141.

(5.) World Health Organization. Global tuberculosis control: epidemiology, strategy, financing. WHO report 2009 [cited 2010 May 13].

(6.) Cadmus S, Palmer S, Okker M, Dale J, Gover K, Smith N, et al. Molecular analysis of human and bovine tubercle bacilli from a local setting in Nigeria. J Clin Microbiol. 2006;44:29-34. DOI: 10.1128/ JCM.44.1.29-34.2006

(7.) Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35:907-14.

(8.) Vitol I, Driscoll J, Kreiswirth B, Kurepina N, Bennett KP. Identifying Mycobacterium tuberculosis complex strain families using spoligotypes. Infect Genet Evol. 2006;6:491-504. DOI: 10.1016/j. meegid.2006.03.003

(9.) de Jong BC, Hill PC, Aiken A, Awine T, Antonio M, Adetifa IM, et al. Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in The Gambia. J Infect Dis. 2008;198:1037-43. DOI: 10.1086/591504

(10.) Harlow RF, Rutkauskas JS. Tuberculosis risk in the hospital dental practice. Spec Care Dentist. 1995;15:50-5. DOI: 10.1111/j.17544505.1995.tb00476.x

(11.) Cleveland J, Kent J, Gooch B, Valway S, Marianos, D, Onorato I. Multidrug-resistant tuberculosis (MDRTB) in an HIV dental clinic. In: Abstracts of the International Conference on AIDS; Atlanta; 1993 Jun 6-11; Abstract Ws-C12-5. Atlanta: Centers for Disease Control and Prevention; 1993.

(12.) Patton LL, van der Horst C. Oral infections and other manifestations of HIV disease. Infect Dis Clin North Am. 1999;13:879-900. DOI: 10.1016/S0891-5520(05)70114-8

(13.) Havlir DV, Getahun H, Sanne I, Nunn P. Opportunities and challenges for HIV care in overlapping HIV and TB epidemics. JAMA. 2008;300:423-3x. DOI: 10.1001/jama.300.4.423

(14.) Arotiba JT, Odaibo GN, Fasola AO, Obiechina AE, Ajagbe HA, Olaleye OD. Human immunodeficiency virus (HIV) infection among oral surgery patients at the University College Hospital, Ibadan, Nigeria. Afr J Med Med Sci. 2003;32:253-5.

(15.) Federal Ministry of Health (Nigeria). Technical report on the 2008 National HIV/Syphilis sentinel survey among pregnant women attending antenatal clinics in Nigeria, Abuja (Nigeria): The Ministry. p. 1-86.

Address for correspondence: Simeon I. Cadmus, Department of Veterinary Public Health and Preventive Medicine, University of Ibadan, PO Box 21452, U.I. Post Office, Ibadan 20005, Nigeria; email:

All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is required.

Author affiliations: University of Ibadan, Ibadan, Nigeria (S.I. Cadmus, V.N. Okoje); Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA (B.O. Taiwo); Radboud University Nijmegen, Nijmegen, the Netherlands (D. van Soolingen); and National Institute for Public Health and the Environment, Bilthoven, the Netherlands (D. van Soolingen)

DOI: 10.3201/eid1609.100447
Table. Demographic characteristics, BCG vaccination status, and TB
exposure history of participants with positive sputum culture
results, University College Hospital, Ibadan, Nigeria, 2006-2007 *

Participant   Age,                    BCG           Exposure to
ID            y/sex   Occupation      vaccination   TB patients

1             49/F    Hairdresser     No            No
2             60/M    Trader          Yes           No
3             24/F    None            Yes           No
4             30/F    Student         No            No
5             45/M    Businessman     Yes           No
6             77/M    Retired         Yes           No
7             44/M    Clergyman       Yes           No
8             40/F    Trader          No            Yes
9             63/M    Retired         Yes           No
10            54/F    Civil servant   Yes           No

Participant   Age,                    Positive
ID            y/sex   Occupation      AFB smear

1             49/F    Hairdresser     Yes
2             60/M    Trader          Yes
3             24/F    None            No
4             30/F    Student         Yes
5             45/M    Businessman     Yes
6             77/M    Retired         No
7             44/M    Clergyman       No
8             40/F    Trader          Yes
9             63/M    Retired         Yes
10            54/F    Civil servant   Yes

* BCG, bacille Calmette-Guerin; TB, tuberculosis; ID, identification;
AFB, acid-fast bacilli.
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Article Details
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Title Annotation:DISPATCHES
Author:Cadmus, Simeon I.; Okoje, Victoria N.; Taiwo, Babafemi O.; van Soolingen, Dick
Publication:Emerging Infectious Diseases
Geographic Code:6NIGR
Date:Sep 1, 2010
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