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Journal of Infection and Public Health (2010) xxx, xxxxxx

REVIEW

Tuberculosis in Saudi Arabia: Can we change the way we deal with the disease?
Sahal Abdulaziz Al-Hajoj
Department of Comparative Medicine, King Faisal Specialist Hospital & Research Centre (MBC 03), PO Box 3354, Riyadh 11211, Saudi Arabia
Received 28 April 2009 ; received in revised form 28 September 2009; accepted 13 December 2009

KEYWORDS
Tuberculosis; Saudi Arabia; Control; Strategy

Summary Infection from Mycobacterium tuberculosis results in the death of three million people worldwide per annum of which an estimated one thousand are in Saudi Arabia. The WHO has set a target for successful treatment of 85% but Saudi Arabia is currently not meeting that target. We believe that the rst step in improving the control of tuberculosis in Saudi Arabia is to improve and unify the standards of diagnostic services and laboratories responsible for tuberculosis. This paper reviews the current status and suggests possible improvements. 2009 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.

Contents
Introduction.................................................................................................. Worldwide situation ..................................................................................... Epidemiology of TB in Saudi Arabia ...................................................................... Recent ndings .......................................................................................... Diagnosis and treatment of tuberculosis...................................................................... Microscopy and culture .................................................................................. National Tuberculosis program (NTP) and Directly Observed Therapy (DOTS)............................. Discrepancies in drug-resistance prole ................................................................. Moving forward .............................................................................................. Registry ................................................................................................. Social health workers involvement and screening ........................................................ Molecular techniques .................................................................................... 00 00 00 00 00 00 00 00 00 00 00 00

Tel.: +966 1 442 4992/464 7272x32971; fax: +966 1 442 7872. E-mail address: hajoj@kfshrc.edu.sa.

1876-0341/$ see front matter 2009 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.

doi:10.1016/j.jiph.2009.12.001

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S.A. Al-Hajoj
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Database ................................................................................................ Ongoing transmission .................................................................................... Screening program....................................................................................... Summary ................................................................................................ Conict of interest statement .............................................................................. References .................................................................................................

Introduction
Worldwide situation
The WHO estimated that worldwide there were an estimated 8.9 million new cases of TB in 2004, with 3.9 million new smear positive, with Africa (24%), South East Asia (35%) and the Western Pacic region (24%) together accounted for 83% of the global burden. Human immunodeciency virus (HIV) is a signicant contributor in some areas, notably sub-Saharan Africa and the United States where 31 and 26%, respectively, of new cases in adults were attributable to HIV and worldwide tuberculosis accounted for 11% of AIDS deaths worldwide [19,23]. This static global gure does not reect greater variations and dynamics within certain regions. The increases in sub-Saharan Africa and the former Soviet Union are the steepest. Industrialized countries have had steady or declining incidences, but increasing rates among foreign-born nationals or foreign citizen [21,31]. In London boroughs, TB notication rates have been shown to vary by a factor of 10 [21]. IS6110 typing was used to study strains of Mycobacterium tuberculosis collected in London between 1995 and 1997, and revealed that most tuberculosis in London is due to reactivation of previous infection or importation of infection by recent immigrants [20]. Better surveys are needed in high burden countries requiring high quality routine surveillance. Ultimately effective control of the disease requires an understanding of the dynamics of disease transmission, implementation of accurate and rapid diagnostics and typing methodologies, and efcacious treatment. The logistics of implementation of these among poor, migrating and rural people further the challenge [33].

Epidemiology of TB in Saudi Arabia

The WHO estimates of the disease burden in Saudi Arabia are found in Table 1. According to the WHO the incidence of TB all forms, smear positive TB and deaths from TB each rose by 6.2% between 1990 and 2004, but the prevalence declined. These gures

suggest that the notication rates of TB in Saudi Arabia increased during this period, as did the successful treatment rate, such that a decrease in the total number of cases was seen at the same time as the incidence and death rates increased [34,40]. Despite the noticeable improvements on notication and successful treatment rates yet Saudi Arabia has a moderate infection rate in comparison with the other countries-Table 2. Saudi Arabia has interesting and special population dynamics. There are up to six million expatriates mainly from endemic regions, in South and South East Asia and over two million pilgrims visiting the holy cities located in the western region of the Kingdom each year, with the majority of pilgrims coming from endemic areas. There are differences in the rate of TB infection in different regions of the country. For instance in Jeddah (Sea and Air ports for pilgrims arriving into Mecca) the infection rate can reach up to 64 cases per 100,000 compared with 32 per 100,000 in Riyadh (Central). The higher rate in Jeddah may have been caused by inux of pilgrims [1,9,10,25,32]. A study of 64 patients admitted to two hospitals with pneumonia during the 1994 Hajj pilgrimage cited M. tuberculosis as being the most common cause, infecting 20% of patients [17]. Nearly all of the patients were from developing countries and the authors suggested that older age, exhaustion, malnutrition and prior use of amoxicillin were contributing factors. A retrospective study of medical records of 157 patients with a nal diagnosis of tuberculosis was performed at the King Abdul Aziz Hospital, Jeddah, between July 1999 and July 2001. Fifty-seven patients (36%) were Saudis and 100 patients (64%) were nonSaudis with a mean age of 33 years (15.33). A prospective study of health care workers at the King Abdulaziz Hospital, Jeddah, found the rate of positive tuberculin skin testing was signicantly higher among non-nationals; 78.9% overall, 60.0% for Saudis compared with 81.8% for non-Saudis (p < 0.01) [30]. The mean response size for nonSaudis (13.9 +/7 mm) was signicantly larger than for Saudis (8.9 +/7 mm, p < 0.001). These data suggest that visitors and immigrants to Saudi Arabia are associated with a higher rate of tuberculosis dis-

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Tuberculosis in Saudi Arabia

Table 1 Figures from WHO report showing the estimation incidence, prevalence and mortality rate caused by tuberculosis in Saudi Arabia. 1990 Incidence, all forms HIV positive Incidence, smear positive HIV positive Incidence, smear positive Prevalence Mortality 8,919 (50/100,000) 4,013 (25/100,000) 2004 9,471 (40/100,000) 4 (<1/100,000) 4,262 (18/100,000) 1 (<1/100,000) Percent increase 6.2 6.2 References [19,35] [19,35] [19,35] [19,35]

14,069 (86/100,000) 1,035 (6/100,000)

13,267 (55/100,000) 1,099 (5/100,000)

5.7 6.2

[19,35] [19,35]

Table 2 Infection rate in Saudi Arabia compared with other countries. Country USA UK Saudi Arabia India Sub-Saharan Africa South Africa Infection rates 5.2 per 100,000 35 per 100,000 3264 per 100,000 180 per 100,000 290 per 100,000 509 per 100,000 Reference [22] [22] [33] [35] [23] [23]

ease, which is in agreement with data from Europe [37]. Recent report by Ministry of Health showed that TB infection rate has risen again. The report showed that the total cases of TB in the country have reached 3878 cases in 2007 with increment rate of 0.6 per 100 thousand compared to 2006 (3854 cases). Also the report showed that the percentages of Saudi among the total cases were 52.7 compared to 47.4 of non-Saudis http://www.moh.gov.sa/statistics/stats2007/Book %20Seha02.pdf.

lished phylogeographic clades; Central Asian-CAS 22.5%, ill-dened T clade 19.5%, East African Indian-EAI 13.5%, Haarlem 7.5%, Latin American Mediterranean-LAM 7.2%, Beijing 4.4%, Manu 2.7%, X 0.9%, and Bovis 0.9%. Two clonal complexes with unique spoligotyping signatures (octal codes 703777707770371, and 467777377413771) specic to Saudi Arabia were identied. These belonged to CAS and EAI clades, respectively, as conrmed upon secondary typing using mycobacterial interspersed repetitive units (MIRUs). The results obtained underline the predominance of historic clones of the principal genetic group 1 (PGG1), which are responsible for roughly 45% of all tuberculosis cases in Saudi Arabia. The high rate of clustering observed might be an indication of rapid ongoing transmission within certain communities and/or subpopulations in Saudi Arabia [8].

Diagnosis and treatment of tuberculosis

Microscopy and culture
In Saudi Arabia detection of M. tuberculosis is by Ziehl-Neelson staining, conrmation is by culture and isolation and speciation is by niacin and nitrate reactions. Drug susceptibility testing employs the Mycobacterial Growth Indicator Tube (MGIT) system (Becton Dickenson, Germany) in some laboratories, solid media (Lowenstein Jensen) in others, or is not performed at all. Recent visits to several laboratories in Saudi Arabia have shown a number of laboratories to require improvement in standards of equipment, training and record keeping [7] and personnel observation. Implementation of a quality assurance examination system, such as NEQUAS [20,22,36], and introduction of a central referral laboratory where speciation and drug susceptibility testing can be performed may help to level standards and comparability between diagnostic laboratories. Importantly, it would also provide

Recent ndings
A total of 1505 clinical isolates of M. tuberculosis, isolated between 2002 and 2005 from seven regions of Saudi Arabia were studied. The sample studied showed a male to female sex-ratio of 1.27 with half of the cases among foreign-born and 47% within the age-group of 2140 years, a total resistance rate of 19.7% and multiple drug resistance of 4.5%. Upon spoligotyping, a total of 387 individual patterns were obtained (clustering rate of 86.4%, 182 clusters containing between 2 and 130 isolates per cluster). A total of 94% of the strains matched to the spoligotype patterns in an international database SpolDB4 database (http://www.pasteurguadeloupe.fr:8081/SITVITDemo). Nearly 81% of the isolates in this study belonged to the estab-

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S.A. Al-Hajoj Empirical anti-tuberculosis therapy used in Saudi Arabia usually includes three to four rst line drugs including isoniazid, rifampicin, ethambutol, pyrazinamide and streptomycin. Despite the implementation of the NTP and DOTS, the number of patients effectively treated in Saudi Arabia has fallen below the WHO target of 85% with drug resistance, noncompliance and over the counter access to anti-tuberculosis treatment being contributing factors [5,15,37]. A retrospective study was conducted, which included 147 patients with culture proven diagnosis of tuberculosis seen at the King Khalid National Guard Hospital, Jeddah, between June 1993 and June 1999. One hundred and twenty-six patients completed treatment and, with patients lost to follow up considered as treatment failures, treatment success was 102/147 (69.4%) and failure 45/147 (30.6%). Noncompliance and drug resistance were cited as being signicantly associated with treatment failures [37].

4 access to testing for institutions that lack their own facilities and help to meet and raise standards set by the National Tuberculosis program (NTP).

National Tuberculosis program (NTP) and Directly Observed Therapy (DOTS)

In 1992, the Ministry of Health established a National Tuberculosis Control Committee to implement a control program throughout Saudi Arabia and in 1999 the committee decided to implement DOTS. The NTP in Saudi Arabia constitutes a manual, recording and reporting system, training, laboratory and X-ray services. Treatment services and drug and equipment supply is funded by the Ministry of Health. In Saudi Arabia there are several institutions providing healthcare for patients with tuberculosis; National Guard health affairs, Military Hospitals, Security forces Hospitals, university hospitals, private hospitals and Ministry of Health Hospitals. Patients attending private hospitals suspected of having TB are referred to government hospitals. There is no central system of record keeping, such that a patient currently receiving treatment at one institution may present to another with tuberculosis and be recorded as a new case [7]. All institutions should report to the Ministry of Health, the body responsible for collecting data on tuberculosis, but we believe that this is not being adhered to [7]. Saudi Arabias DOTS success rate is comparatively well below international gures (Table 3). As successful treatment is dependent on quality assured bacteriology, Saudi Arabia needs improvements to a number of laboratories across the country.

Discrepancies in drug-resistance prole

There are several studies that have shown different rates of tuberculosis drug resistance across the country over the last 20 years (Table 4). However, these studies should be treated with caution for the following reasons: for some studies the methodologies were not clearly described, some are now out of date, the studies were retrospective, none followed the WHO guidelines for drug-resistance surveys and some studies are contradictory [36,1114,16,18,26,27,29,38,39,41].

Table 3 Shows the success rates in treating drug resistant tuberculosis using directly observed therapy [D.O.T.S] in different countries. Once again the data showed that Saudi Arabia fall behind the set target 85% by WHO. Country Saudi Arabia China Europe Sub-Saharan Africa Thailand DOTS success rate drug susceptible TB % 65.0 85 83.0 81.0 85.0 DOTS success rate MDRTB % NA 57.0 57.0 72.7 57.0 Reference [19] [19] [22] [23] [19]

Table 4 City

Shows the mono and multi-drug resistance rates in different cities in Saudi Arabia. RIF 20.0 2.8 43.0 0.2 Percent of drug resistance INH PZA ETB 28.7 9.1 80.0 6.0 7.9 5.0 Se S 6.9 2.8 N/A S STR 22.8 1.6 53.0 0.7 % MDRTB 25.0 11.8 44.0 7.0 Reference [3,28] [3,13,16,18,30] [3,27] [3,11,14]

Jeddah/Taif (West) Riyadh (Central) Jazan (South) Dammam (East)

RIF = rifampicin, INH = isoniazid, PZA = pyrazinamide, ETB = ethambutol STR = streptomycin, S = sensitive, N/A = not available.

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5 ing the country may also help to reduce the number of infections brought into the country by immigration and visitors, as is done elsewhere, but the cost efcacy benet is not clear [24,31,35].

Tuberculosis in Saudi Arabia

Moving forward
Existing committees should update the NTP guidelines for Saudi Arabia in accordance with World Health Organization (WHO) established guidelines. The NTP guidelines should aim to address any lack of human resources and expertise. Lack of human resources development is an obstacle in Saudi Arabia and this lack of attention results in absence/deciency of training and continuing education [7]. Furthermore, diagnosis protocols should be updated in line with international standards and should be adopted unanimously across all institutions providing tuberculosis facilities, in order that standards can be unied and results compared. These should be implemented to improve the speed and accuracy of diagnosis. Communication between laboratories should be strengthened and ongoing education for laboratory and clinical staff may also be of value. The different frequencies of resistance across the country (Table 4) probably reect regional differences in both epidemiology and laboratory standards. Signicantly, there is no adopted standard methodology applied across the country [7]. We suggest that, at least as a short-term measure, laboratories with inadequate infrastructure or lack of trained personnel to perform the susceptibility testing should send their isolates to the nearest center, provisions and/or funding for which need to be provided by the Ministry of Health.

Molecular techniques
Molecular techniques for typing strains of M. tuberculosis are essential to identify cross contamination, outbreaks and transmission to be investigated [28]. In Saudi Arabia Restriction Fragment Length Polymorphisms (RFLPIS6110) and spoligotyping have already shown that internationally recognized multi-drug-resistant strains (Beijing) to be present [8]. In addition many imported families also were identied using, molecular tools. In another studies we identied cross contamination event and cross infection within a family. The wider implementation of molecular testing would enhance the understanding of the dynamics of M. tuberculosis and its dissemination within the country. Therefore, we propose that all isolates after initial diagnosis and identication should be transferred to a specialized center for genotyping and that genotypic results be linked with the patients le for follow up and future use.

Database Registry
To improve epidemiological surveys a central database in which all cases should be registered and updated at each consultation would enable clinicians to monitor patients that move from one region to another and allow continual access to treatment records. This would prevent patients registering as new patients at more than one center, without restricting their movement, and would facilitate DOTS programs across the country. Such a database would enable accurate determination of notication rates, treatment success and failures and drug resistance. We think it is the time to create a database in which we should have all the patients registered. The registry of the patients should be based on the national identication card and for the residents the Iqamma number should be used. Also the database should contain the pattern of susceptibility tests. Moreover we proposed that all isolates should be genotyped and all strains identication should be linked to the patient. This is extremely important so we can differentiate on the second episode either the patients came back with new infection, treatment failure, or with reactivation of an old infection. Also it is possible to know from genotype either the strain is virulent such as Beijing genotype or not. Genotyping also can recognize the outbreaks and the ongoing transmission. We at Tuberculosis Research Unit were able to create such database. What is missing in such database is the information from the rest of the country. Also we would like to see such database is accessible by all concerned chest physicians and infectious diseases and public health physicians running the National Tuberculosis program. The database should be updated on a continuous bases.

Social health workers involvement and screening

Social health workers may help to improve compliance by actively following patients to ensure that medications are taken according to the physicians prescription. This may compliment the DOTS program by actively seeking out patients who do not attend appointments. Screening of patients enter-

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S.A. Al-Hajoj ond visit and the test reading is not subjective like skin test. One of these two tests should be implemented to screen most vulnerable groups within the communities to detect latent TB or even catch those whom recently converted to sero-positive [2]. The advantages of these new tests in addition to what was mentioned that they, unlike skin test, do not cross react with other mycobacteria such environmental mycobacteria or do not react with BCG vaccine it self.

Ongoing transmission
Recent data showed that the country, despite the efforts by the health care takers, has ongoing transmission among citizens and residents equally. Also the data showed that the ongoing transmission is caused by both imported and endogenous strains (clades/families). These evidences raised the question about what can be done to break the cycle of transmission. It does not matter how much we treat and it does not matter which strategy we used, either Direct Observed Therapy, or any other strategy, we believe unless we break the cycle of ongoing transmission, TB infection will remain as ever uncontrollable disease. We believe there are reasons behind such active on going ongoing transmission including the fact that some patients (especially illegal residents) escape follow up after 23 weeks of starting the treatment from hospitals fearing the deportation after the completion of treatment. Unfortunately those individuals seek refuge within local nationals household or among farmers in large farms. They are involved in creation of drug-resistance strains as a result of their failure to complete the treatment and disease transmission. Other reasons including the lack of case nding strategies, many expatriates with TB hide a way after Hajj and Umra seasons. Strategies of case nding should be activated and large screening studies should take place across the country. For expatriates we believe the deportation policy should be reversed so no one feels the fear of the deportation and then they run a way from hospital after the slight improvement they noticed.

Summary
It is clear that tuberculosis in Saudi Arabia is in need for attention. This is supported by the increase in the infection rate 0.6% during 2007 compared to 2006 infection rate. This may be an indication of the improvements of the case detection but also could means that the rate is on increase. Several factors may inuence the rate of infection in Saudi Arabia. Theses factors include the huge number of expatriate worker force who are residents of this country. Also religious visitors whom target Mecca and Madina for Hajj and Umra. This is because both laborers and visitors mainly come form TB endemic countries. Recent data that showed that 2/3 of genotyped isolates are indeed imported strains [8]. The National TB program and status of laboratories are another two factors that play a major role in controlling the disease. A number of improvements to tuberculosis disease control and understanding of epidemiology have been outlined in this review. These include the standardization of practices and methodologies, implementation of a central reporting system and provision of access to specialized sensitivity testing and genotyping services available at a few centers. The cycle of active ongoing transmission should be stopped via active case nding and screening most vulnerable groups with most reliable tools. Diagnostic laboratory standards must be made uniform across the country [7]. Furthermore, publication of accurate and up-to-date data will increase knowledge and understanding of the current status. These require the inclusion and commitment of all those dedicated to the provision of healthcare services to patients with tuberculosis and adequate resource investment.

Screening program
Latent TB is the main source for active TB disease. According to the World Health Organization one third of the mankind is infected with latent TB. In Saudi Arabia the information about how much people are infected with latent TB is scarce. We do not know for instance what are the percentages of latent infection among Health care workers, prisoners, and contact groups. It is essential to screen at least those at high risk for latent TB using most reliable tools. Recently FDA approved two new interferon- gama release assays (IGRAs) which are are now available for the diagnosis of LTBI: the QuantiFERON-TB Gold (Cellestis, Victoria, Australia) and the T-SPOT.TB (Oxford Immunotec, Oxford, UK). Both tests are better than skin test in the specicity and sensitivity to diagnose latent TB. Also they have advantages over the skin test; including ease in performance, no need for sec-

Conict of interest statement

Funding: No funding sources. Competing interests: None declared. Ethical approval: Not required.

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