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Salmonella Infections in Asir Region, Southern
Saudi Arabia: Expatriate Implications
Gaafar M. Malik, MRCP; Abdul Hameed A. Al-Wabel, MPH, MD; Mohamed M. El Bagir Khalafalla Ahmed,
FRCP; Naser E. Bilal, MD; Ashock Shenoy, MD; Mohamed Abdalla, MD; Tag Elsir Mekki, MBBS
From the Department of Medicine (Drs. Malik, Al-Wabel, Ahmed, Abdalla, Mekki), and Department of Microbiology (Drs. Shenoy and Bilal), College of
Medicine, Asir Central Hospital, Abha.
Address reprint requests and correspondence to Dr. Malik: Assistant Professor of Medicine, King Saud University - Abha Branch, P.O. Box 641, Abha,
Saudi Arabia.
Accepted for publication 20 September 1992.
One hundred forty-two cases of salmonella infection seen in Asir region, Southern Saudi Arabia, during the period
of 1989-1991 inclusive, were analyzed. Ninety-four cases were found to have enteric fever and 48 cases were found
to have Salmonella enteritidis gastroenteritis. Enteric fever is more common in non-Saudis (64%) than in the
indigenous Saudi population (34%). Salmonella enteritidis gastroenteritis is more common among the Saudi
population (75%) than non-Saudis (25%). The clinical presentation of both types of salmonella infection is outlined.
Enteric fever is more common among expatriates who recently came from India (40.5%), Egypt (10.6%), Pakistan
(6.4%), and Syria (4.3%). Salmonella typhi resistant to tetracycline, ampicillin, and chloramphenicol are more
common among Indian patients (75% of resistant cases) and Syrian patients (12.5-28% of resistant cases).
Resistance to cotrimoxazole is commonly encountered in Indians (50% of resistant cases) and Egyptians (33.3%).
Salmonella enteritidis resistant to tetracycline, ampicillin, and chloramphenicol is more common among Saudis
(66.7% of resistant cases) and Filipinos (16.7-33.3% of resistant cases). Recommendations regarding screening of
expatriates for enteric fever and proper drug therapy of possible resistant cases are outlined. Ann Saudi Med
1993;13(3):242-245.
GM Malik, AHA Al-Wabel, MMEBK Ahmed, NE Bilal, A Shenoy, M Abdalla, TE Mekki, Salmonella Infections in
Asir Region, Southern Saudi Arabia: Expatriate Implications. 1993; 13(3): 242-245
Salmonella infections are still a major health problem in many developing countries [1]. The clinical spectrum
of salmonella infection varies greatly with different geographical regions. These differences were related to
environmental and nutritional factors [2] as well as differences in the virulence of the organisms [3]. The Kingdom
of Saudi Arabia is served by a large number of expatriates from different countries in which salmonella infection is
endemic. In our clinical practice, we have observed that enteric fever is not so common among the indigenous Saudi
population, while cases are frequently seen among foreigners who have traveled recently to their countries where
typhoid is endemic. Reviewing the literature, no published reports about salmonella infection in the southern part of
Saudi Arabia could be found. This study was undertaken to assess the magnitude of the problem in the Asir region
and the influence of the large number of expatriates on the disease pattern.
Material and Methods
The case records of 142 patients diagnosed as having salmonella infection in both Asir Central Hospital and
Lassan Fever Hospital in Abha over the period of 1989-1991 inclusive were reviewed. Asir Central Hospital is the
main referral hospital of Asir region while Lassan Hospital is the referral hospital for fevers and infectious diseases.
The cases diagnosed by a positive blood, stool, urine, or bone marrow culture were selected for analysis. Typhoid
and paratyphoid fevers which were suspected on clinical grounds with negative culture were included only if there
was evidence of a rising Widal agglutination titer for the O antigen on two or more occasions, a week or more apart.
Results
One hundred forty-two patients were identified to have salmonella infection. Ninety-four cases had enteric fever
and 48 had Salmonella enteritidis gastroenteritis. The average age of the patients was 21.9 years (range of two
months to 60 years). Fifty percent of the cases of Salmonella enteritidis gastroenteritis were found among children
below the age of 14 years. Eighty-six were males (60.6%) and 56 were females (39.4%). This male predominance
might be a reflection of the fact that the majority of cases of enteric fever were foreign male laborers as shown in
Table 1.
Table 1 shows the distribution of the cases according to nationalities. Enteric fever is found to be more common
Salmonella Infections in Asir Region, Southern Saudi Arabia: Expatriate Implications
Annals of Saudi Medicine, Vol 13 No. 3; 1993
in foreigners (66%) than in the indigenous Saudi population (34%). Salmonella enteritidis gastroenteritis is more
common among Saudis (75%) than among foreigners (25%). All the expatriates who presented with enteric fever
gave a history of travel to their home country during the eight weeks prior to the illness. Among foreigners, enteric
fever is more common in Indians (40.5%), Egyptians (10.6%), Pakistanis (6.4%) and Syrians (4.3%). Foreigners
who commonly presented with Salmonella enteritidis gastroenteritis were Filipinos (12.4%).
Table 2 summarizes the clinical features of both enteric fever and Salmonella enteritidis. The most common
presenting symptoms of enteric fever were fever (100%), headache (55.3%), vomiting (42.5%), abdominal pain
(40.5%), and diarrhea (34%). Rare symptoms include constipation (4.3%), dry cough (4.3%), and arthralgia (2.1%).
The most common physical signs of enteric fever were a temperature above 37.5°C (74.5%), anemia (23.4%),
hepatomegaly (21.3%), splenomegaly (19.1%), and abdominal tenderness in 12.8%. Rare signs include
lymphadenopathy (6.4%), lung crepitations (4.3%), and skin rash (2.1%). The most common symptoms of
Salmonella enteritidis infections are diarrhea (91.7%), abdominal pain (87.5%), fever (79.2%), and vomiting in
62.5%. Headache is a rare symptom (4.2%). The most common findings in Salmonella enteritidis infection are
abdominal tenderness (79.2%) and a temperature above 37.5°C (37.5%). All cases of Salmonella enteritidis were
isolated from the stool except four cases: two from discharging bone sinuses in a sicklemic and a patient with an
infected compound fracture; the other two from infected skin lesions in a sicklemic and a patient with splenectomy.
Table 3 shows the pattern of antibiotic resistance of salmonella isolates in relation to different nationalities.
Resistant salmonella typhi or paratyphi to tetracycline, ampicillin and chloramphenicol is more common in isolates
from Indian patients (75% of resistance isolated to each antibiotic). Isolates from Syrian patients show resistance to
ampicillin (18.8%) and chloramphenicol (25%). Resistance to cotrimoxazole is also more common among Indians
(50%) and Egyptians (33.3%). Regarding Salmonella enteritidis isolates, resistance to tetracycline, ampicillin, and
chloramphenicol is more common in isolates from Saudi patients. Resistant isolates (66.7%) to each antibiotic were
found in Saudi patients. Isolates from Filipino patients also showed resistance to tetracycline (16.65%), ampicillin
(33.3%), and chloramphenicol (33.3%).
Table 1. Distribution of 142 cases of Salmonella typhi, Salmonella paratyphians and Salmonella enteritidis in the Asir
region, according to nationality.
Nationality
Salmonella typhi
& paratyphi
Salmonella
enteritidis
Total
No.
(%)
No.
(%)
No
(%)
Saudi
32
(34)
36
(75)
68
(47.9)
Indian
38
(40.5)
-
-
38
(26.8)
Egyptian
10
(10.6)
-
-
10
( 7.1)
Pakistani
6
( 6.4)
2
( 4.2)
8
( 5.6)
Filipino
-
-
6
( 12.4)
6
( 4.2)
Syrian
4
( 4.3)
-
4
( 2.8)
Sudanese
2
( 2.1)
2
( 4.2)
4
( 2.8)
Sri Lankan
-
-
2
( 4.2)
2
( 1.4)
Palestinian
2
( 2.1)
-
-
2
( 1.4)
Total
94
(100)
48
(100)
142
(100)
Salmonella Infections in Asir Region, Southern Saudi Arabia: Expatriate Implications
Annals of Saudi Medicine, Vol 13 No. 3; 1993
Table 2. Symptoms and signs of 142 patients diagnosed as having enteric fever or Salmonella enteritidis gastroenteritis in
the Asir region.
Salmonella typhi &
paratyphi
Salmonella
enteritidis
No.
(%)
No.
(%)
Symptoms
Fever
94
(100)
38
(79.2)
Headache
52
(55.3)
2
( 4.2)
Vomiting
40
(42.5)
30
(62.5)
Abdominal pain
& distention
38
(40.4)
42
(87.5)
Diarrhea
32
(34.0)
44
(91.7)
Constipation
4
( 4.3)
-
-
Dry cough
4
( 4.3)
-
-
Arthralgia
2
( 2.1)
-
-
Signs
Temp. > 37.5°C
70
(74.5)
18
(37.5)
Anemia
(pale conjunctivae)
22
(23.4)
-
-
Hepatomegaly
20
(21.3)
-
-
Splenomegaly
18
(19.1)
-
-
Abdominal tenderness
12
(12.8)
38
(79.2)
Cervical lymph-
adenopathy
6
( 6.4)
-
-
Lung crepitations
4
( 4.3)
-
-
Skin rash
2
( 2.1)
-
-
Discharging bone sinus
-
-
2
( 4.2)
Skin infection
-
-
2
( 4.2)
Table 3. Pattern of antibiotic resistance to Salmonella infection according to nationality in the Asir region.
Antibiotics
Salmonella typhi or paratyphi
Salmonella enteritidis
Resistance
(%)
Nationality
No.
(%)
Resistance
(%)
Nationality
No.
(%)
Tetracycline
16/40
(40)
Indian
=
12
(75)
12/44
(24.3)
Saudi
=
8
(66.7)
Sudanese
=
2
(12.5)
Sudanese
=
2
(16.65)
Syrian
=
2
(12.5)
Filipino
=
2
(16.65)
Ampicillin
16/52
(38.8)
Indian
=
12
(75)
6/44
(13.6)
Saudi
=
4
(66.7)
Syrian
=
3
(18.8)
Filipino
=
2
(33.3)
Saudi
=
1
(16.2)
Co-trimoxazole
6/16
(37.5)
Indian
=
3
(50)
-
-
-
-
Egyptian
=
2
(33.3)
Saudi
=
1
(16.7)
Chloramphenicol
16/50
(32)
Indian
=
12
(75)
6/36
(16.7)
Saudi
=
4
(66.7)
Syrian
=
4
(25)
Filipino
=
2
(33.3)
Carbenicillin
2/8
(25)
Sudanese
=
2
-
-
-
-
-
Nalidixic acid
2/2
(100)
Sudanese
=
2
-
-
-
-
-
Cefoxitin
0/40
(0)
-
2/26
(7.7)
Filipino
=
2
Salmonella Infections in Asir Region, Southern Saudi Arabia: Expatriate Implications
Annals of Saudi Medicine, Vol 13 No. 3; 1993
Discussion
The results of this retrospective study confirmed our observation that enteric fever is more common among
foreigners than in the indigenous Saudi population.
All the non-Saudis gave a history of recent travel to their respective countries, which implies that they had
probably contracted the infection from their home countries. Similar observations have been reported from other
Gulf countries, particularly Kuwait, which is also served by a large number of foreign laborers [4,5]. Salmonella
enteritidis gastroenteritis is found to be more common among Saudis than non-Saudis, in agreement with reports
from the Riyadh area [6], Eastern Province [7], and Western Province [8] of Saudi Arabia.
Regarding the clinical findings of enteric fever, results are similar to those reported from other countries like
India [9], Kuwait [5], and Canada [10]. The disease is generally mild with no serious complications or fatalities seen
in this series. This is similar to what has been found in studies from Singapore [11]. The clinical features of
Salmonella enteritidis gastroenteritis in the Asir region are similar to those reported from other parts of the Kingdom
[6,7]. Salmonella typhi and paratyphi isolates which are resistant to ampicillin, chloramphenicol, tetracycline, and
cotrimoxazole are common in patients coming from the Indian subcontinent. Similar reports of resistant Salmonella
to the standard chemotherapy are now accumulating from Southeast Asia and other parts of the world [4,12-14].
Isolates from Syrian patients have exhibited some resistance to tetracycline, ampicillin, and chloramphenicol, while
isolates from Egyptians have shown resistance to cotrimoxazole.
Practicing physicians in Saudi Arabia should be alerted to the possibility of encountering organisms resistant to
the standard enteric fever chemotherapy in patients coming from these countries. Since there is a large number of
laborers moving between these countries and the Kingdom, there is a chance of importing the resistant enteric fever
organism to the Kingdom. Public health measures should be enforced to ensure the proper evaluation of laborers
before employment by using stool cultures and agglutination tests for salmonella, especially for food handlers.
Alternative antibiotics should be used in cases of enteric fever coming from Southeast Asia in which resistance is
suspected. Reports have shown that the third generation cephalosporins, aminoglycosides, and quinolones are a
better alternative [4,15-17]. Salmonella enteritidis organism, which is more common among the Saudi population,
exhibited some resistance to tetracycline, ampicillin, and chloramphenicol. This observation has also been reported
in the Jeddah region [8]. Other antibiotics should be used if antibiotic treatment is required for severe cases.
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