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Tuberculosis in Saudi Arabia: can we change the

way we deal with the disease?
ARTICLE JANUARY 2010
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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 ....................................................................................

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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
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

00
00
00
00
00
00

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-

Please cite this article in press as: Al-Hajoj SA. Tuberculosis in Saudi Arabia: Can we change the way we deal with
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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.

Incidence, all forms

HIV positive
Incidence, smear
positive
HIV positive
Incidence, smear
positive
Prevalence
Mortality

1990

2004

Percent increase

References

8,919 (50/100,000)

4,013 (25/100,000)

9,471 (40/100,000)
4 (<1/100,000)
4,262 (18/100,000)

6.2

6.2

[19,35]
[19,35]
[19,35]

1 (<1/100,000)

[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

Infection rates

Reference

USA
UK
Saudi Arabia
India
Sub-Saharan Africa
South Africa

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

[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.

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-

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

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S.A. Al-Hajoj

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.

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].

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

DOTS success rate drug susceptible TB %

DOTS success rate MDRTB %

Reference

Saudi Arabia
China
Europe
Sub-Saharan Africa
Thailand

65.0
85
83.0
81.0
85.0

NA
57.0
57.0
72.7
57.0

[19]
[19]
[22]
[23]
[19]

Table 4

Shows the mono and multi-drug resistance rates in different cities in Saudi Arabia.

City

RIF

Percent of drug resistance

INH PZA ETB

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

20.0
2.8
43.0
0.2

28.7
9.1
80.0
6.0

7.9
5.0
Se
S

6.9
2.8
N/A
S

STR

% MDRTB

Reference

22.8
1.6
53.0
0.7

25.0
11.8
44.0
7.0

[3,28]
[3,13,16,18,30]
[3,27]
[3,11,14]

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

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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.

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].

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.

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-

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.

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S.A. Al-Hajoj

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.

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-

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.

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.

Conict of interest statement

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

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Tuberculosis in Saudi Arabia

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