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ORIGINAL ARTICLE Table of Contents   
Year : 2010  |  Volume : 53  |  Issue : 2  |  Page : 227-231
Extra-pulmonary tuberculosis in Saudi Arabia


Department of Pathology (Microbiology), King Khalid University Hospital, Riyadh, Saudi Arabia

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Date of Web Publication12-Jun-2010
 

   Abstract 

Studies from developed countries have reported that extra-pulmonary tuberculosis (EPTB) is on the rise due to the human immunodeficiency virus (HIV) epidemic. However, similar studies from high-burden countries with low prevalence of HIV like Saudi Arabia are lacking. Therefore, we conducted this study to investigate demographic and clinical characteristics of patients with pulmonary and extra-pulmonary tuberculosis. A retrospective analysis was carried out on all patients (n=431) with a culture - proven diagnosis of tuberculosis seen at University teaching hospital, Riyadh, Saudi Arabia from January 2001 to December 2007. A total of 183 (42.5%) pulmonary tuberculosis (PTB) and 248 (57.5%) extra-pulmonary TB (EPTB) cases were compared in terms of age, sex, and nationality. There were 372 Saudis (SA) (86.3%) and the remaining non-Saudis (NSA) 59 (13.7%). The age distribution of the PTB patients had a bimodal distribution. EPTB was more common at young age (20-29 years). The proportion of EPTB cases was significantly higher among NSA patients (72.9%) compared to SA patients (55.1%). Females had higher proportion (59.5%) of EPTB than males (55.6%). The most common site was lymph node tuberculosis (42%). In conclusion, our data suggest that EPTB was relatively common in younger age, female gender and NSA. Tuberculosis (TB) control program may target those populations for EPTB case-finding.

Keywords: Extra-Pulmonary Tuberculosis, M. tuberculosis, pulmonary tuberculosis

How to cite this article:
Al-Otaibi F, El Hazmi MM. Extra-pulmonary tuberculosis in Saudi Arabia. Indian J Pathol Microbiol 2010;53:227-31

How to cite this URL:
Al-Otaibi F, El Hazmi MM. Extra-pulmonary tuberculosis in Saudi Arabia. Indian J Pathol Microbiol [serial online] 2010 [cited 2019 Nov 13];53:227-31. Available from: http://www.ijpmonline.org/text.asp?2010/53/2/227/64327



   Introduction Top


Tuberculosis (TB) remains a major global public health problem. [1] It is estimated that about one-third of the world's population is infected with Mycobacterium tuberculosis. [2] Despite improved living standards, the availability of free anti-tuberculosis medications, and the implementation of mass bacillus Calmette-Guerin (BCG) vaccination at birth, tuberculosis remains an endemic disease in the Kingdom of Saudi Arabia (KSA). Epidemiologic studies have demonstrated that the prevalence of TB in Saudi Arabia is high. [3],[4] The World Health Organization (WHO) reported that the annual incidence rate of reported TB cases per 100,000 population in Saudi Arabia in 2006 was 44%.

Extra-Pulmonary Tuberculosis (EPTB) has the reverse epidemiological trend of pulmonary tuberculosis (PTB). Over the last several years, reported EPTB was increasing in absolute numbers and proportion of all reported TB cases. [5] This proportion varied widely between hospitals and at different time period in KSA reflecting variation in referral patterns. In 1998, 37% of reported tuberculosis cases from King Khalid National Guard Hospital (KKNGH), Jeddah [6] had extra-pulmonary involvement. More recently in 2003, EPTB was diagnosed in 51% of TB cases from the Saudi Aramco Medical-Services Organization. [7] Our study aims to investigate demographic and clinical characteristic of patients with Extra-Pulmonary Tuberculosis at, Riyadh, Saudi Arabia.


   Materials and Methods Top


Our hospital is a tertiary care teaching hospital serving the population of Riyadh, the capital city in the central area of Saudi Arabia. The total population served by the hospital is about 1.5 million inhabitants. This study included 431 patients with tuberculosis, who represent 98% of the culture-proven TB cases diagnosed in our microbiology laboratory from January 2001 through December 2007. In addition, we reviewed TB surveillance data from the annual reports of the TB control unit. All smear-positive cases are referred and admitted to designate TB wards attached to the TB control unit. The majority of extra-pulmonary cases of tuberculosis are also referred to the TB control unit for treatment. Some extra-pulmonary TB cases, e.g., gastrointestinal or skeletal TB, may be treated in the general hospitals. Doctors and laboratories are required by law to notify newly diagnosed TB cases to the TB control department. The medical records of cases were reviewed retrospectively. From each medical case file, the patient's history, physical findings, chest radiographs and reports of laboratory investigations were reviewed to obtain the necessary information about diagnosis of TB. Testing for HIV infection is carried out based on epidemiological and / or clinical suspicion, therefore only a fraction of our cases were tested. The patients were divided into two groups as EPTB (including intrathoracic and pleural TB) and PTB according to the European consensus on surveillance of tuberculosis. [8] The two groups were compared by age, sex and nationality.

Statistical Analysis

Differences in categorical variables between EPTB and PTB were compared and analyzed using the chi-square test. A two-sided P-value < 0.05 was considered statistically significant.


   Results Top


Between January 2001 and December 2007, a total of 431 patients with a positive culture for M. tuberculosis were identified. One hundred and eighty three patients (42.5%) were classified as PTB and 248 (57.5%) as EPTB. Of the 248 cases of EPTB, 35(14.1%) had concurrent PTB.

Demographic Features

The overall male to female ratio of TB cases was 1.01 (216/215). For PTB patients, the male to female ratio was 1.1 (96/87), but 0.94 (120/128) for EPTB patients. Of the 215 female patients, 128 (59.5%) had EPTB disease, whereas 120 (55.6%) of 216 male Patients did. The difference was statistically not significant (P=0.4604) [Table 1].

[Figure 1] shows the age distributions of EPTB and PTB confirming the tendency for EPTB to occur at younger ages 20-29 years. The proportion of EPTB cases decreased significantly with increasing age being 21.4%, 10-14% and 4.8% for the age groups 20-29 years, 40-69 years and >80 years respectively (P=0.0018) . The age at incidence of PTB showed evidence of a bimodal pattern, with peaks at 20-29years and 70-80 years.

[Figure 2] shows the age distribution of EPTB and PTB among the 431 TB patients stratified by gender. Of the 105 patients tested for HIV; all were seronegative except 2 (1.9%).

Population Studied

This study was carried out on a relatively wide section of the Riyadh population attending and referred to KKUH. The incidence of the disease was investigated in both Saudi (SA) and non-Saudi (NSA) patients. Of the total patients, there were 372 Saudis (86.3%), and the remaining 59 patients (13.7%) were non-Saudis. The proportion of EPTB cases was significantly higher among NSA patients 34 (72.9%) of 59 compared to SA patients 205 (55.1%) of 372 (P=0.0153). In contrast, PTB was more prevalent among SA (44.9%) than NSA (27.1%) patients (P=0.015) [Table 1]. The NSA population included 18 nationalities. Amongst patients with EPTB, eight patients (18.6%) were from Philippines, 5 (11.6%) were Somali, Yemeni and Sudanese for each. 4(9.3%) were Indonesian and Pakistani. The remaining patients were from India, Erithrea, Bangladesh, Nepal, Kenya, Sri Lanka and Qatar. [Figure 3] shows the age distribution of EPTB in the SA and NSA populations. NSA patients were more likely to have EPTB at a younger age with peak at 30-39 years.

Sites of EPTB

The most common site of EPTB was the lymph nodes (42%) followed by osteoarticular (13.7%), abdominal (13.3%) and pleural (12.1%) tuberculosis. Other sites were CNS (4.4%), urogenital (3.6%), military (2.1%) and Para-vertebral abscess (1.2%). Eighteen EPTB patients (7.3%) had TB at other sites. Amongst them 15 patients had soft tissue abscess at different sites, namely, the gluteus (4), breast (4), back (2), chest wall (2), big toe (1) and inguinal area (2). The remaining three patients had retropharyngeal (2) and skin TB (1).

Sites of EPTB according to gender are illustrated in [Figure 4]. Lymphatic TB was the most frequent form in both genders. More particularly, extra-thoracic (superficial) lymph node involvement had a strong female predominance [Table 2]. Pleurisy was the third leading site in male patients after osteoarticular TB.


   Discussion Top


Our study reports epidemiology of EPTB from a high-burden country with low prevalence of HIV. [9],[10],[11],[12] To our knowledge, no similar study characterizing and comparing EPTB with PTB has been reported from the Middle East region. EPTB is increasingly common in our community, accounting for 28.2 % of all reported TB cases in 1997 [13] compared with only 11.7 % in 1991. [14] In this study EPTB accounted for 57.5% of TB cases seen at KKUH. This proportion is in concordance with earlier studies from Dhahran, [7] Jeddah [15] and Riyadh [16] cities confirming that the incidence of EPTB is increasing generally in KSA. The increasing rate of reported EPTB may have resulted from better diagnostic facilities identifying more cases and better reporting system. Being an area of low prevalence of HIV, it is unlikely that HIV accounts for this increase. However, it must be emphasized that immigrants play a major role in the epidemiology of tuberculosis. The contribution of foreign-born to the changing rate of tuberculosis has been observed in other regions of the World, such as Germany, Denmark and USA. [8],[17],[18]

Differences in the likelihood of EPTB have been observed in various studies among tuberculosis patients by demographic characteristic. In this study although not statistically significant, the proportion of EPTB among females is higher than males. As observed in other studies, female tuberculosis patients were considerably more likely to present with an extra pulmonary manifestations than male patients. [8],[18],[19] In this context, the increased likelihood of females with tuberculosis presenting with an extra-pulmonary disease manifestation was particularly pronounced among those aged (40-49 years). On the contrary, male patients showed high prevalence of EPTB in the younger age group (20-29 years). An explanation for this finding remains unclear, but it suggests that endocrine factors might play a role. An important finding in this investigation was the predominance of EPTB among the young age group (20-29 years). This is consistent with studies from the USA and Europe [20],[21] which have found that young age was independent risk factor for EPTB. A recent case-controlled study from Nepal has reported a strong association between younger age and female gender with EPTB. [22] This raises the possibility that after primary infection in the lungs the probability of reactivation at an extra-pulmonary site may be higher at younger age. Our results suggest that at older ages reactivation of TB was common in the lungs. This may be due to decreased local immunity in the lungs in the elderly as a result of associated life-style factors (smoking) or diseases such as emphysema and bronchitis.

The overall SA to NSA ratio of TB cases was 6.3 (372/59). Compared with earlier reports from Jeddah and Dammam [15],[23] cities, the proportion of NSA in this study is considerably low and in addition, we noted that, NSA nationals tended to have EPTB more than PTB. This difference can be explained by the variation in the geographical distribution of immigrants in KSA and by pre-employment screening at entry, which prominently targets pulmonary tuberculosis. In addition, EPTB manifests after a longer interval following acquisition of infection than PTB. [24] Demographic variations among the SA and NSA nationals were observed. In SA patients, EPTB was prevalent over a wider age span with a peak in the younger age group (20-29 years). In the NSA population the greatest number of patients was in the 30-39 years group [Figure 3]. The distribution in SA patients differs, with a plateau rather than a sharp decline after 30 in NSA. This difference can be explained by the larger number of young NSA nationals in the expatriate work force. This finding was observed in a previous study reported from Jeddah. [15]

In our study, the lymph nodes were the most common site of EPTB. Our results are comparable to earlier studies from Nepal and Turkey, [22],[25],[26] which have reported that lymph nodes accounted for nearly half the cases of EPTB. In Hong Kong, the genitourinary system and the skin were the common sites, whereas in the USA, bones and/or joints were the most common sites. In this series, in particular, isolated intrathoracic and extra-thoracic lymph node TB was the most common form of EPTB in females (63% of all cases of EPTB). [27],[28] On the other hand, pleural, urogenital, and osteoarticular TB were more common among males. Majority of the patients with extra thoracic lymph node TB were within the age range of 20 to 49 years, i.e., they were young adults. Other forms of EPTB, such as TB of the skin, CNS, military TB were rare and diagnosed mostly in adults. This is consistent with other studies from Saudi Arabia which have reported that CNS and TB meningitis were rare in children. [29],[30] However, a study from Turkey found that, the most commonly involved site among 64 children with EPTB was the CNS (25%). [31] It is known that bacilli Calmette-Guerin (BCG) vaccinations had a protective effect against TB forms such as meningeal TB in children. In KSA BCG vaccination is mandatory to be given at birth. Several studies have reported an increasing trend of EPTB among HIV infected persons. [31],[32],[33] However, it has been demonstrated that EPTB was associated with a poor immune status even in the absence of HIV infection, both in developing and industrialized countries. [34],[35] In Saudi Arabia, HIV prevalence is 0-0.1% [9],[10],[11],[12] Testing for HIV infection was carried out only on a fraction of our cases. Therefore, we did not have enough data for analysis of the association between HIV infection and EPTB. We believe that as recommended by CDC it is important to screen the HIV/AIDS patients for TB despite the low incidence of HIV/AIDS in KSA. [36] Further studies are required to study the association between TB and HIV/AIDS.

In conclusion, results of our study suggest that younger age and female gender may be independent risk factors for EPTB, relative to PTB in Saudi Arabia. Further studies in other high burden countries are needed. Based on our results TB control programs might target young and female populations for early diagnosis of EPTB.

 
   References Top

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Correspondence Address:
Fawzia Al-Otaibi
Microbiology Unit, Department of Pathology / Micropathology (32), College of Medicine and king Saud University, King Khalid University Hospital, PO Box 2925, Riyadh-114 61
Saudi Arabia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.64327

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Archives of Industrial Hygiene and Toxicology. 2010; 61(3)
[Pubmed] | [DOI]
22 A case report of occupational middle ear tuberculosis in a nurse
Lalić, H., Kukuljan, M., Pavičić, M.
Arhiv za Higijenu Rada i Toksikologiju. 2010; 61(3): 333-337
[Pubmed]



 

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