A STUDY OF MATERNAL DIETARY INTAKE DURING PREGNANCY IN RIYADH, SAUDI ARABIA Khalid S. Almurshed, PhD,* Ibrahim A. Bani, MD, PhD,* Mohammed A. Al-Kanhal, PhD,* Mohammed A. Al-Amri, MSc† *Department of Community Health Sciences, College of Applied Medical Sciences, King Saud University & †Prince Salman Hospital, Riyadh, Saudi Arabia ______________________________________________________________________________ هدف الدراسة : أجريت هذه الدراسة لتقييم النظام الغذائي للنساء الحوامل و علاقته بالمواليد. طريقة الدراسة: شملت العينة 114 امرأة حامل في الأسابيع العشرين الأخيرة من فترة الحمل. جمعت عينة النساء الحوامل من عيادة الحوامل في مستشفى الأمير سلمان في مدينة الرياض بالمملكة العربية السعودية وذلك باستخدام الاختيار العشوائي لأفراد العينة. تمت المقابلة الشخصية لكل امرأة لمدة ساعة عبأ خلالها الاستبيان و أخذت قياسات أبعاد الجسم بالإضافة إلى أخذ عينة وريدية من الدم وقد شمل الاستبيان الحالة الاجتماعية, استذكار الغذاء المستهلك خلال الساعات الأربع والعشرين السابقة للمقابلة, تكرار استهلاك بعض الأغذية, بالإضافة إلى العادات الغذائية لكل امرأة. نتائج الدراسة: بلغ متوسط المستهلك من العناصر الغذائية الموصى بها للنساء الحوامل (RDA) المعدلات التالية: 51.8%, 93.9%, 82.5% و 98.2% لكل من الطاقة الغذائية, فيتامين ب1 (B1), الكالسيوم والحديد, على التوالي. كما أن ما نسبته 13.2% من النساء قد أحسسن بنوع من الوحم. وجد أن ما نسبته 2.8% و 4.4% من أفراد العينة كان لديهن نقص في التغذية, وذلك عند استخدام الطول و محيط وسط الذراع كمؤشرين لذلك, على التوالي. الاستنتاج: للتقليل من المخاطر التي قد تتعرض لها النساء الحوامل ومواليدهن, لابد من الإرشادات الغذائية التي تسهل عليهن اختيار الأغذية عالية القيمة الغذائية. الكلمات المرجعية: نظام غذائي   الحوامل    السعودية ________________________________________________________________________ Objective: This study was carried outto evaluate the dietary nutrient intake of pregnant women. The relationship between dietary intake and pregnancy outcome was also studied.  Method: A total of 114 pregnant women were studied, using systematic random sampling. Results: The percentages of the mean nutrient intake below the recommended dietary allowances (RDA) for pregnant women were as the follows: 51.8%, 93.9%, 82.5% and 98.2% for energy, vitamin B1, calcium and iron, respectively. Moreover, 13.2% of the women experienced some form of pica. Using height and mid-arm circumferences, about 2.8% and 4.4% were seen to be undernourished respectively. Conclusion: Saudi pregnant women need guidance in selecting nutrient dense foods to reduce maternal and outcome health hazards. Key Words:  Dietary intake, Pregnant women, Saudi Arabia. _____________________________________________________________________________________
INTRODUCTION Throughout the world, pregnancy and lactation are considered vulnerable periods for both the mother and the child. The role of maternal health and nutrition has been emphasized by the recognition of the problem of low birth weight which affects some 20 million newborns annually, mainly in developing countries. This is essentially an end result of interference with fetal growth following inadequate nutrition and infections in pregnant women in these countries.1       Malnutrition in pregnancy not only has an ill effect on the newborn, but also impairs the mother’s owns health. When the pregnant woman's diet does not supply the required nutrients for her needs and for those of the fetus, the fetal requirements are met
_____________________________________________________________________________________ Correspondence to: Dr. Ibrahim Bani, Department of Family & Community Medicine, Faculty of Medicine, Jazan University, P.O. Box 114, Jazan, Saudi Arabia   E-mail:
by withdrawing these from the tissues of the pregnant mother. This tissue depletion weakens the mother and increases the probability of serious complications and the chances of delivering an infant with low birth weight (LBW) who is unlikely to feed adequately early in life.2 This is why some researchers suggest that improving food intake during pregnancy might reduce LBW.3       The economic development of the Kingdom of Saudi Arabia has been globally recognized. However, this rapid development and urbanization, coupled with the changing patterns of lifestyle and food habits, has precipitated the various health-related problems besides the nutritional problems already in existence before the nineteen seventies. The dietary habits of the Saudi people have been influenced by an influx of foreign workers, availability of wide range of imported goods, and a rise in purchasing power.4 The prevalent traditional eating habits coupled with the novel western lifestyle is leading towards the rising incidence of obesity.5       Rapid economic development and modernization have stimulated some interest in the dietary patterns of vulnerable groups. Data on the dietary patterns of 1200 pregnant Saudi women were collected using structured food frequency recall questionnaires.6 It showed that the average daily intake of pregnant Saudi mothers was far from satisfactory in three food groups (milk and its products, meat and vegetables). However, the consumption of cereals and fruits was adequate. Recently, the National Survey of pregnant and lactating women revealed that dietary practices of 50 to 70% of the respondents had not changed. However, 22.9% of lactating women and 13.6% of the pregnant ones had increased their consumption of dates.7 This could be due to their traditional beliefs about dates which are widely consumed local produce.       In a study of food habits of Saudi women during pregnancy, the percentage of women with dietary cravings, pica, and aversions were 38, 8.8 and 66.4 respectively.8 Identification of nutritional shortfalls that affected a substantial proportion of pregnant women may be useful in developing recommendations for nutrition education. We evaluated the nutritional status of a sample of pregnant women who came to the antenatal clinic at Prince Salman General Hospital in Riyadh, Saudi Arabia. METHODS A total of 114 pregnant Saudi women were selected by systematic random sampling from the antenatal clinic at Prince Salman Hospital in Riyadh, Saudi Arabia. All the women were in the last 20 weeks (second half) of gestation. They were healthy and had no chronic diseases. Based on records provided by the antenatal clinic, approximately 220 potentially eligible women were seen. The dietitian recruited 116 of these women (41.9%). The exclusion criteria included refusal, missing three appointments or delivery in another hospital (i.e. moved from the area). Although, the recruitment rates were somewhat low, the demographics of the study population were not more statistically significant than that of the total antenatal clinic population, which suggested that the cohort was generally representative.       Nutritional status was assessed in a personal interview. The interviews were conducted by a trained dietitian.  Weight was measured to the nearest 0.2 Kg using Continental Scale Corporation Bridge View, Illinois, USA. The weight was taken without shoes and with as few clothes as possible. Height was measured in centimeters using a rod attached to the weighing scale.       Mid-upper arm circumference was measured to the nearest 0.1 cm using a flexible non-stretch tape. The women stood erect and sideway to the measurer. The point at the midpoint of upper left arm i.e. midway between acromion process and tip of the olecranon was located. The tape was wrapped gently, but firmly around the arm at midpoint and the measurement taken.       The triceps skinfold thickness was measured at the midpoint of the upper arm using Harpenden caliper. At the midpoint of the upper arm, the skinfold was pulled and the caliper was applied. Two measurements were taken. A third measurement was taken and the mean of the closest pair was recorded if there was a big difference between the first two.       Pregnancy outcome date, birth weight, length and head circumference were obtained during physical examination of the newborn infant by the midwife within 24 hours of delivery. Infants who were less than 2500 grams at birth were considered as infants with low birth weight.       In addition, a questionnaire covering the 24-hour diet recall was used and analyzed using Food Composition for Middle East to calculate nutrient intake.9 The food frequency consumption and dietary habits including cravings and aversion were recorded.  Also at the time of the interview, a small venous sample was obtained. Coulter Counter (Coulter T540) machine was used for hematological analysis. Pregnancy outcome data including infant’s birth weight, recumbent height, and head circumference were obtained within the first 24 hours after delivery by trained medical staff at Prince Salaman Hospital.       Statistical analyses including Student T-test, Pearson’s Correlation Chi-square, and Fisher’s exact test were calculated as appropriate. RESULTS The mean age of the women was 28+6.54 years with a range of 17-42 years. 11.4 percent of them were less than 20 years. The majority of the women (74.6%) got married below the age of 20 years. The mean age at marriage was 18+3.39. Fifty-six percent of the women and 32.5 percent of their husbands had a low level of education (illiterate, read and write). The majority of women (89.5%) were housewives and 10.5% of them had jobs outside the home.       The daily intake of different nutrients for pregnant women as well as their comparisons with the recommended dietary allowance (RDAs) /National Research Council (NRC) USA are shown in Table 1. More than 80% of pregnant Saudi women exceeded the RDAs in their intakes of protein (80.7%) and retinol (81.6%). Intakes of vitamin B1 (93.9%), calcium (82.5%), iron (98.2%) and energy (51.8%) were shown to be below the RDAs. Table 1: Nutrient intake of pregnant women

Nutrient Mean+SD RD (%)
Protein (gm) 77.0+22.1 60 (128.0)
Fat (gm) 38.5+16.0 47 (82.0)
Carbohydrate (gm) 28.7+79.5 31.8 (90.0)
Energy (kcal) 1793.0+480.0 2504 (70.0)
Fiber (gm) 13.4+6.1 22.0 (61.0)
Calcium (mg) 802.1+349.6 1295 (62.0)
Phosphorous (mg) 1174.5+438.4 1298 (90.0)
Iron (mg) 11.5+5.0 30 (38.4)
Retinol (ug) 1445.4+671.6 1300 (111.0)
Vitamin B1 (mg) 0.7+0.5 1.6 (45.0)
Vitamin B2 (mg) 1.6+0.6 1.8 (86.1)
Vitamin C (mg) 91.3+66.2 70 (130.0)
      Figure 1 shows the distribution of the women's intake according to the number of different choices in the diet from six food groups in a 24-hour period. Forty-five point six percent of the women had two servings of milk or milk products, and only 1.8% had four servings to meet the recommended dietary allowances for milk and milk products. Thirty percent of the women had four servings of the meat group (lamb, beef, poultry and fish) meeting the recommended dietary allowances for animal protein, 23.7% had five or more servings and the rest (45.6%) had less than the recommended dietary allowances. The average daily intake in the present study is far from satisfactory in respect of milk, meat, and cereals. The present study revealed that women with specific cravings, pica and aversions were 28.1%, 13.2% and 47.4%, respectively.          Figure 1: Food intake of pregnant women represented by food exchanges       The mean weight, height and mid-arm circumferences+SD were 70+13.6 kg, 154.9+6.0 cm and 25.3+5.2 cm, respectively. Using the following criteria: height <140 cm and mid-arm circumference <23 cm as cut-off points, two point six percent of the women were at risk for malnutrition using the height criterion and 4.4% at risk using the mid-arm circumference criterion. Maternal anthropometric measurements were not significantly correlated with the pregnancy outcomes (birth weight and infant length) as shown in Table 2.       Using hemoglobin level, prevalence of anemia in the present study was 19%. However, 31%, 42% and 85% were below the cut-off levels10 for haematocrit, mean corpuscular volume and serum iron, respectively. DISCUSSION Women’s nutritional status is closely tied to their reproductive capacity. Nutritional status influences age at menarche, fetal wastage, birth weight, women’s ability to go through pregnancy, and nursing without compromising their own nutritional well-being and health status.11       The relationship between early marriage and pregnancy outcome was examined. In the present
Table 2: Correlation – Maternal anthropometrics and pregnancy outcomes*
Maternal Anthropometrics R (value)
Mean+SD Birth weight Length
Weight (kg) 70.4+13.6 0.1768 0.105 0.1327 0.177
Height (cm) 154.9+6.0 -0.0628 0.329 0.0836 0.280
Mid arm circumference (cm) 30.2+5.2 0.1505 0.143 0.1099 0.221
Triceps skinfold thickness (mm) 25.3+9.5 0.0924 0.257 0.0262 0.427
Body mass index 29.6+5.48 0.1944 0.084 0.940 0.256

study, women younger than 20 years of age represented 11.4% of participating mothers. They were at risk of having malnutrition and other health problems. Teenage girls in the East Mediterranean Region are markedly underweight with little adipose tissue and depleted muscle mass.12  Furthermore, it was reported that this phenomena of high prevalence of adolescence pregnancy had resulted in increased  risk of spontaneous abortion, a combination of fetal death and infant mortality, premature deliveries, low birth-weight, and fetal mal-presentation in Saudi Arabia.13,14 Not-withstanding tradition, teenage pregnancy should be discouraged.       In the present study, the diets of the pregnant mothers' were below the RDA for Vitamin B1 (93.9%), calcium (82.5%), iron (98.2%) and energy (51.8%). This profile revealed that the average nutrient intake was deficient in some of the important nutrients. Pregnant Saudi women in a comparable  study5 had diets deficient in energy, vitamin B1, calcium, and iron. The low energy intake of pregnant women is a common problem in other parts of the world.15 In the present study, the mean intake of protein exceeded the RDA in 80.7% of mothers. Although the protein intake of the majority of mothers was sufficient, the calories were low. Therefore, the protein had to be used as a source of calories resulting in a diet inadequate of proteins.       In a recent study16 in the United States, it was reported that pregnant women enrolled in the Special Supplemental Program for Women, Infants, and Children (WIC) consumed only 85% of the RDA for energy. The most notable nutrient shortfall was iron; 90% of the women reported consuming less than 2/3 of the RDA.       In the present study, food consumption pattern was investigated by assessing the frequencies of food intake per day according to basic food groups, milk and milk products, meat group, fruits and vegetables, bread and cereals and fat and oil groups. The results revealed that the women needed to improve their intake of milk, meat and the cereal group.       Diet during pregnancy is frequently considered a composite of local beliefs, traditions and practices relating reproduction. The present study revealed that the percentage of pregnant women with specific cravings for certain foods, pica and aversions was 28.1, 13.2 and 47.4, respectively. Differences in food cravings and aversions were possibly in response to beliefs about what should be consumed.17 In the present study, women craved mainly meat (25.9%). In the Sudan, 93% of pregnant women had various cravings.18 Twenty percent of Sudanese women believed that if not fulfilled, food cravings in pregnancy had a direct lasting effect on the child. A recent study showed that among 321 pregnant Saudi women, the percentage of cravings, pica and aversions were 38, 8.8 and 66.4 respectively.8       In the present study, the proportion of underweight women ranged from 2.6 to 4.4% using height and arm circumference indicators, respectively. Four different kinds of information may be related to height.19 Firstly, height may predict overall maternity body stores. Secondly, being short has been related to difficulties in labor and obstetric mortality. Thirdly, height may reflect socioeconomic status. Fourthly, maternal height is a phenotype expression of the genetic component. Specific maternal height cut-off points for a country or region need to be established for predicting risk of low birth infants. The assessment of nutritional status was complicated by the lack of pregnancy weight in the present study. Therefore, arm circumference was used as an indicator for nutritional status.       The results of this study showed no significant relationship between dietary intake and pregnancy outcomes, which is in agreement with observations made by many authors.20,21 Scholl et al (1991) suggested that there might be a direct relationship between maternal intake and birth-weight when maternal stores are low or depleted under conditions of frank poverty or famine.       Our findings about maternal anthropometric measurements were not significantly correlated with pregnancy outcomes. We found that 19% of the mothers were anemic. Iron deficiency anemia is believed to be a common health problem in the Arabian Gulf.22 Factors responsible for anemia in Saudi Arabia have not been investigated. It is possible that iron deficiency anemia is related to eating habits. In a recent report of the National Nutrition Survey, it was revealed that mothers increased their consumption of tea and coffee during pregnancy.7 This could affect their iron.       It is concluded from the findings of this study that pregnant women need to increase their intake of foods rich in iron, calcium, vitamin B1 and energy. The results suggest that pregnant women need guidance in selecting nutrient dense foods.  Moreover, the results of this study emphasize the importance of nutritional profile of pregnant women, so that proper nutrition counseling and education could be given. ACKNOWLEDGMENT The authors wish to thank the administration and staff of Prince Salman Hospital in facilitating this work. We also thank Mr. Khan Moshraf Hussain for his computer technical assistance.       REFERENCES 1.     Metcoff J. Maternal nutrition and fetal outcome. Am J Clin Nutr 1981;34:708-21. 2.     Simpouolos AP. Selected vitamins, minerals and functional consequences of maternal malnutrition. World Rev Nutr Diet 1991; 61 suppl: S87-121. 3.     Ramakrishnan U. Nutrition and low birth weight: from research to practice. Am J Clin Nutr 2004; 79(1):17-21. 4.     Gibbon A. Cultural and cross cultural influence on the dietary habits in Saudi Arabia. In Moyal AF, ed. Diet and Lifestyle, New Technology. Proceeding of 10th International Congress of Dietetics. John Libbey, 1988; 39-143. 5.     Al-Shoshan AA. The affluent diet and its consequences: Saudi Arabia - A case in point. World Rev Nutr Diet 1992; 9:113-65. 6.        Al-Shoshan AA, Kanawatti AA, Ali AE. Maternal nutrition and pregnancy outcome of Saudi mothers in Riyadh, Technical Report. Riyadh: Nutrition Department, Ministry of Health, 1992; 21-7. 7.        King Abdul Aziz City for Science and Technology (KACST). Evaluation of the nutritional status of the people of Saudi Arabia, Final Report. Riyadh: King Abdul Aziz City for Science and Technology, 1997; 138-39. 8.     Al-Kanhal MA, Bani IA. Food habits during pregnancy among Saudi women.  International J Vit Nutr Res 1994; 65:206-10. 9.     Pellet PL and Shadavevian S. Food composition table for use in the Middle East, 1970  2nd edition. American University of Beirute. 10.   World Health Organization. Nutritional anemias: A report of WHO experts. WHO Technical Series. No. 503.9. 1972, Geneva: WHO. 11.   Brems S, Berg A. Eating down during pregnancy, nutrition, obstetrics and cultural considerations in the Third World, Technical Report. 1988 Washington D.C.: Population and Human Resources Department, The World Bank. 12.   World Health Organization. Maternal and infant mortality in Eastern Mediterranean Region (Office RMRO), Technical Publications Series. 1988 Alexandria, Egypt: Regional Office for Eastern Mediterranean. 13.   Shawky S, Milaat W. Early teenage marriage and subsequent pregnancy outcome. Eastern Mediterrean Health Journal 2000;6(1):46-54. 14.   Krueger WW. Size at birth in Najran Saudi Arabia. Annals of Saudi Medicine    1988; 8(2):113-116. 15.   Arija V, Cuco G, Vila J, Iranzo R, Fernandez-Ballart J. Food consumption, dietary habits and nutritional status of the population of Reus: follow-up from preconception throughout pregnancy and after birth. Med Clin 2004; 123(1):5-11. 16.   Swensen AR, Harnack L J, Ross J A. Nutritional assessment of pregnant  women enrolled in the Special Supplementation Program for Women, Infants and Children (WIC). J Am Diet Assoc 2001; 101:903-5. 17.   Snow LF, Johnson SM. Folklore, food and female reproductive cycle. E Coll Food Nutr 1978; 7:41-9. 18.   Osman AK. Dietary practices and aversions during pregnancy and lactation among Sudanese women. J Trop Paed 1985; 35:185-90. 19.   Martorell R. Maternal height as an indicator of risk. In: Krasovec K, Anderson MA, eds. Maternal nutrition and pregnancy outcome. 1991 Pan American Health organization. 20.   Susser M. Maternal weight gain, infant birthweight, and diet, Causal sequences. Am J Clin Nutr 1991; 53:1384-96. 21.   Scholl TO, Hediger ML, Khoo C, Heals MF, Rawon NL.  Maternal weight or  gain; diet and infant birthweight: Correlations during adolescent pregnancy. J Clin Epidem 1991; 44:423-8. 22.   Musaiger AO. The state of food and nutrition in the Arabian Gulf countries. World Rev Nutr Diet 1987; 54:105-73.



AN OUTBREAK OF FOODBORNE DIARRHEAL ILLNESS AMONG SOLDIERS IN MINA DURING HAJJ: THE ROLE OF CONSUMER FOOD HANDLING BEHAVIORS Abdulla S. Al-Joudi, MD, MSc (Epidemiology) Department of Family and Community Medicine, College of Medicine, King Faisal University, Dammam, Saudi Arabia _____________________________________________________________________________ هدف الدراسة: معرفة مصدر فاشية تسمم غذائي حدثت في معسكر في منى خلال موسم الحج إلى مكة بالمملكة العربية السعودية وقياس انتشارها واقتراح طرق الوقاية من أمثالها في المستقبل. طريقة الدراسة : دراسة أترابية استرجاعية لمعرفة أنواع الطعام والظروف المسئولة عن حدوث فاشية التسمم . نتائج الدراسة: من خمسين جندي سعودي  16 (39%) أصيب بالنزلة المعوية التي ظهرت على شكل اسهال (100%) ومغص معوي (87.5%) بلغ متوسط مدة الحضانة للميكروب  12.63±4.8528  ساعة. ويدل منحنى الوباء على أن الفاشية حدثت من مصدر مشترك. كانت وجبة الغداء الوجبة الوحيدة التي لها ارتباط بالمرض يعتد به إحصائيا. وكان الرز الطعام الوحيد الذي له ارتباط بالمرض يعتد به إحصائيا. الخلاصة: تناول الأرز الملوث كان هو السبب في حصول هذه الفاشية. العامل. والعوامل المؤدية إلى الفاشية تشمل سلوكيات المستهلكين غير الصحيحة في التعامل مع الطعام بتركه في درجة حرارة مناسبة لتكاثر الميكروب وعدم تسخينه بشكل كافي عند استهلاكه مجددا. الكلمات المرجعية: فاشية التسمم الغذائي، المملكة العربية السعودية،  الحج، سلوكيات المستهلك. ________________________________________________________________________ Objective: An investigation of the outbreak was initiated as a result of the number of cases of gastroenteritis reporting to a general hospital in Mina during the pilgrimage to Makkah (HAJJ).  This study was conducted to identify the source of the outbreak, assess its extent, and make recommendations to prevent similar outbreaks in the future. Methodology: A case was defined as any individual who developed diarrhea with or without abdominal pain after eating at the camp in Mina on 3rd January 2006. A retrospective cohort study was conducted to identify food items and circumstances responsible for this outbreak. Laboratory tests included stool cultures of all diarrhea patients, and rectal swabs from all food handlers were cultured for enteric pathogens. Results:A total of 50 Saudi Male Soldiers were interviewed. Out of these, 16 (39%) had developed gastroenteritis, most commonly manifested by diarrhea (100%), and abdominal colic (87.5%). The mean incubation period was 12.6 ± 4.9 hours and the epidemic curve suggested a common point source outbreak. Out of three served meals, lunch was found to have a statistically significant association with illness (p=0.0230).  Out of five food items served, rice was the only food item found to have a statistically significant association with illness (p=0.0230). No food remnants were found for sampling. All results of stool cultures of all diarrhea patients, and rectal swabs from all food handlers were inconclusive. Conclusions: This outbreak was most likely caused by eating contaminated rice served at lunch on 3rd January. The most likely organisms were Bacillus cereus, and/or Clostridium perfringens. Consuming food that was kept at an unsafe temperature wihout being reheated was the most probable important factor leading to this outbreak. Key Words:Foodborne Outbreak, Saudi Arabia, Hajj, Consumer behaviors. ________________________________________________________________________________ Correspondence to: Dr. Abdullah S. Al-Joudi, P.O. Box 31987, Al-Khobar, Saudi Arabia E-mail:

INTRODUCTION Foodborne disease outbreaks (FBDO) are recognized by the illness of individuals usually within a short but variable period of time after a common meal.1 A national policy for reporting, notifying, and recording incidents of bacterial food poisoning in Saudi Arabia was established in 1984.2,3 Since then, food poisoning outbreaks exhibiting seasonal and regional variations have been reported from different regions of the Kingdom.2,4,5 Food poisoning outbreaks associated with mass catering are not rare, and have been reported even from developed countries.6         A high number of outbreaks is reported in the Hajj period (the pilgrimage to Makkah) in Saudi Arabia. The number of food poisoning incidents in the Hajj season for the last 12 years ranges from 44 to 132.7 These incidents are the result of too many factors. The influx of people from all over the world with different cultures, beliefs, and behavior, present the problem of food handling, especially when food hygiene standards are compromised and some people are not accustomed to foodborne pathogens.8, 9       Food handlers are known to play an important role in food safety and in the transmission of foodborne infections since they are likely to introduce pathogens into foods during production, processing and distribution.10 In fact, asympto-matic food handlers have been incriminated in many food poisoning outbreaks.10-12 Background On 4th January 2006, a number of soldiers with gastroenteritis symptoms, including diarrhea, and abdominal cramp, presented to Emergency Department of a General Hospital in Mina after consuming a meal provided at their camp on 3rd January 2006. The hospital reported the incident to Makkah Directorate of Health Affairs which in turn reported it to the Hajj Preventive Medicine Committee. On 5th January the author was requested to investigate this outbreak. Objectives This study was conducted to identify the source of the outbreak of gastroenteritis, to assess its extent, and to make recommendations for the prevention of similar outbreaks. METHODOLOGY Study area and population Mina is a holy place where pilgrims settle for a few days to perform their rituals. All the cases came from one tent occupied by 50 soldiers located in a government camp in Mina. The camp was served by a catering company that prepared and distributed three meals daily (breakfast, lunch, and dinner). Source of information In order to make a preliminary assessment of the situation, to develop the case definition and generate a hypothesis, and design the questionnaire, the investigator met the doctors, nurses, and health inspectors who dealt with the situation. The Emergency Department records were reviewed, and a preliminary list of the names of patient’s was obtained. Case definition For the purpose of this investigation, a case of food poisoning was defined as “any individual who developed diarrhea with or without abdominal pain, and vomiting after eating at the specified tent in the specified camp in Mina on 3rd January 2005.” Study design Since the outbreak occurred very rapidly, in a small well-defined population, it was decided that a retrospective cohort study13 to identify food items and other factors responsible for the outbreak be conducted. Data collection The soldiers were personally interviewed, using a structured questionnaire that enquired about demographic data, symptoms of gastroenteritis, date and time of meal, date and time of onset of symptoms, food items eaten, and history of hospitalization and any recent history of diarrheal illness. An open-ended interview was conducted with the food handlers from the catering company. Information on the list of food items prepared, ingredients, preparation techniques, method of preservation of each food item and the job description of each food handler were obtained. The food-handlers were then examined for their level of personal hygiene, external injuries, presence of skin infections, and validity of health certificate. The municipal team visited and inspected the food preparation site for general sanitation.  Laboratory tests included stool cultures of all diarrhea patients, and rectal swabs from all food handlers. All specimens were cultured for enteric pathogens at the Makkah Public Health Laboratory. Statistical analysis Epi-Info program for windows, (version 3.2.2), was used for data entry, tabulation and analysis. Tables were constructed to compare the attack rates (AR) of gastroenteritis for persons exposed and unexposed to each food item, followed by a calculation of relative risks (RR) as a measure of association. Statistical significance of an association was taken as <0.05 and 95% confidence intervals (95% CI) were estimated. RESULTS All soldiers, all of whom were Saudis, from the suspected tent participated in the study. Their ages ranged from 21 to 48 years with a mean age of 33.9 ± 7.4 years. All participants shared the same suspected meals.       Sixteen (39%) out of the 50 participants met the case definition. Apart from diarrhea (100%), other common symptoms included abdominal colic (87.5%), nausea (25%), headache (18.8%), and vomiting (6.3%).

Time of Exposure
9      12     15      18      21    24       3      6       9       12      15     18     21     24     3       6       9   12    Jan 3rd                                                      Jan 4th                                              Jan 5th Time of Onset (Hours/Date)
      Out of 16 patients, 10 (62.5%) sought medical care, but none of them required hospitalization. All patients recovered with no complications or death. The mean incubation period was 12.6 ± 4.9 hours (median = 12.3 hours, range = 3 to 22.5 hours). The epidemic curve suggested a common point source outbreak (Figure 1).       Table 1 shows that out of the three meals served on 3rd January 2005, lunch was the only meal that had a statistically significant positive association with the illness (RR= infinity, X 2 = 5.16, p = 0.023).  All those who developed symptoms had eaten lunch. None of the soldiers who had skipped lunch that day reported any symptoms.       Table 2 shows that out of the five food items served at lunch, rice was the only food item that had a statistically significant positive association with the illness (RR= infinity, X 2 =5.16, p=0.023).        Based on the interview with the cases, lunch was served at 12 o’clock. A few minutes after that, soldiers were asked to carry out an urgent assignment. The assignment was terminated about an hour late. The food left in the tent without any air conditioning for a period ranging from 1 to 4 hours, with a mean of 2.8 ± 1.8 hours, was consumed without being reheated.       According to the Municipal health inspectors report, the food preparation hall, the floor and tables were clean. No food remnants were available for sampling at the time of inspection. The interview with the restaurant staff revealed that they were well-trained and had valid health certificates. The preparation of the meal in question and food items was proper. The rice and meat were cooked separately but served in the same dish. The laboratory results of stool samples of patients and food handlers were inconclusive.
Figure 1: Epidemic curve of gastroenteritis cases in the Mina camp in Makkah, Hajj season 3rd January 2006 (N=16) Table 1: Attack rates and relative risk for meals served in the Mina camp in Makkah on 3rd January 2005 (N=50)
Food items Ate Did not eat X2 RR 95% CI p-value
Ill/total AR (%) Ill/total AR (%)
Breakfast 7/23 30.4 9/27 33.3 0.95 0.91 0.40-2.07 0.8266
Lunch 16/41 39.0 0/9 0 5.16 Infinity - 0.0230
Dinner 3/11 27.3 13/39 33.3 0.14 0.82 0.28-2.37 0.7035
Table 2: Attack rates and relative risk for food items served in lunch in Mina camp in Makkah on 3rd January 2005 (N=50)
Food items Ate Did not eat X2 RR 95% CI p-value
Ill (total) AR (%) Ill (total) AR (%)
Rice 16/41 39 0/9 0 5.16 Infinity - 0.0230
Meat 15/40 37.5 1/10 10 2.78 3.75 0.56-25.12 0.0954
Dessert 6/12 50 10/38 26.3 2.35 1.90 0.87-4.13 0.1252
Beans 5/11 45.5 11/39 28.2 1.17 1.61 0.71-3.65 0.2787
Jew's mallow 3/7 42.9 13/43 30.2 0.44 1.42 0.54-3.73 0.5066

DISCUSSION Although the food samples were not analyzed and the laboratory results were inconclusive, clinical and epidemiological evidence suggests that Bacillus cereus, and/or Clostridium perfringens1,14 were the most likely causative organisms. The mean incubation period and clinical picture that indicated the absence of fever and predominance of diarrhea, and the presence of abdominal colic were compatible with the clinical presentation of Bacillus cereus, and/or Clostridium perfringens. The variation in the incubation periods could be explained by the variation in doses of inoculation, the susceptibility of the individual or quality of information.       The most likely food item that acted as a vehicle for the transmission in this outbreak was rice served at lunch on 3rd January. A statistically significant association was found between eating lunch and illness and between eating rice and illness. Rice was probably contaminated when it was kept at ambient temperature for a prolonged period of time permitting the multiplication of the causative organism. Rice is more associated with Bacillus cereus, while meat is more associated with Clostridium perfringens.1,14 However, it was not possible to discriminate between rice and meat, as the vehicle of transmission in this scenario since they were mostly eaten together. The lack of a statistically significant association between meat and illness does not rule out the possibility of cross contamination of meat with rice because they were served together on the same dish, though cooked separately.       Hillers et al reviewed the consumer food handling behaviors associated with the prevention of 13 foodborne illnesses. They found that behavior related to keeping foods at safe temperatures is of primary importance in preventing illness caused by Bacillus cereus and Clostridium perfringens and of secondary importance in preventing illness caused by Staphylococcus aureus. 15 In this incident, patients, who were all male, reported that they had consumed the food that was kept at an unsafe temperature without being reheated. This behavior according to a recently published Meta-analysis was found to be a major risk factor for developing a foodborne diarrheal illness among males.16        The lack of food samples, inconclusiveness of laboratory results, and the possibility of recall bias are among the limitations of this study. CONCLUSION It can be concluded that contaminated rice eaten on 3rd January was the vehicle for this foodborne outbreak and the most likely organisms were Bacillus cereus, and Clostridium perfringens. Consuming food that was kept at an unsafe temperature without being reheated was the most important factor that probably led to this outbreak. RECOMMENDATION An improvement in consumer food-handling behavior through effective health education programs is likely to reduce the risk and incidence of foodborne disease17. To prevent future outbreaks, a number of steps were suggested. Food must be kept at temperature above 60°C if it is to be served within a few hours. Those requiring refrigeration should be stored at temperatures no higher than 7°C to avoid the multiplication of pathogens.18,19  Proper training of food handlers for this can prevent foodborne disease transmission.19,20 Hajj related health education and training programs that emphasize the importance of proper food handling practices, personal hygiene, and food sanitation need to be conducted. Strict hygienic conditions during food preparation for large numbers of people, proper food delivery, and hygienic handling as well as temperature control during serving are strongly recommended. ACKNOWLEDGMENT The author is grateful to Dr Yagob Al-Mazrou, Assistant Deputy Minister for Preventive Medicine and President of Hajj Preventive Medicine Program for reviewing this work. Many thanks go to Dr Adel Turkstani, the Head of Epidemiology Surveillance Unit of Hajj Preventive Medicine Program and his field team for their cooperation in data collection. REFERENCES: 1.        Heymann DL. editor. Control of communicable diseases Manual. 18th ed. Washington DC: American Public Health Association, 2004: 211-6, 469-73. 2.        Jaralla JS, Khoja TA, Izmiry MA. Reports of bacterial food poisoning in Riyadh Region of Saudi Arabia: a one-year retrospective study. Saudi Med J 1993;14:46-9. 3.        Kurdi TS. Guidelines for Gastroenteritis Management. Riyadh: Ministry of Health, 1995: 1-14. 4.        Malik GM, AlWabel AA, Ahmed MB. Salmonella infection in Asir Region, Southern Saudi Arabia: Expatriate implications. Ann Saudi Med 1993;13(3):242-5. 5.        Al-Awaidy ST, Fontaine RE. An outbreak of salmonellosis among Filipinos in a private camp, Saudi Arabia. Eastern Medit Health J 1996;2(1):107-14. 6.        Gaulin C, Viger YB, Fillion L. An outbreak of Bacillus cereus implicating a part-time banquet caterer. Can J Public Health.  2002;93(5):353-5 7.        Al-Mazrou YY. Food poisoning in Saudi Arabia: Potential for prevention. Saudi Med J 2004;25(1):11-14 8.        World Health Organization. Emerging foodborne diseases, fact sheet 124. Revised January 2002. Available from URL: (accessed 2006 October 2). 9.        Green AD, Roberts KI. Recent trends in infectious diseases for travelers. Occup Med (Lond) 2002;50:560-5 10.     Angelillo IF, Viggiani NM, Rizzo L, Bianco A. Food handlers and foodborne diseases: knowledge, attitude, and reported behavior in Italy. J of Food Prot 2000;63(3):381-5. 11.     Maguire H, Pharoah P, Walsh B, et al. Hospital outbreak of Salmonella virchow possibly associated with food handler. J Hosp Infect 2000;44(4):261-6. 12.     Faustini A, Sangalli M, Fantasia M, et al. An outbreak of Salmonella Hadar associated with food consumption at a building site canteen. Eur J Epidemiol 1998; 14 (1): 99-106. 13.     Dicker R. editor. Investigating an Outbreak. In: Principles of Epidemiology: An Introduction to Applied Epidemiology and Biostatistics. 2nd ed. Atlanta Georgia: Centers for Disease Control and Prevention, 1998: 375. 14.     Black RE. Diarrheal Diseases. In: Nelson KE, editor. Infectious Disease Epidemiology. 1st ed. Maryland: Aspen Publication, 2001: 504-6. 15.     Hillers VN, Medeiros L, Kendall P, Chen G, DiMascola S. Consumer food-handling behaviors associated with prevention of  13 foodborne illness. J Food Prot. 2003;66(10): 1893-9. 16.      Patil SR, Cates S, Morales R Consumer food safety knowledge, practices, and demographic differences: findings from a meta-analysis. J Food Prot. 2005;68(9):1884-94. 17.     Redmond EC, Griffith CJ. Consumer food handling in the home: a review of food safety studies. J Food Prot. 2003;66(1):130-61 18.     Slutsker L, Villarino ME, Jarvis WR, Goulding J. Food Disease Prevention in Health Care Facilities. In: Bennet JV, Brashman PS, editors. Hospital infection. 4th ed. Baltimore: Williams and Wilkins Publishers, 1998: 333-43. 19.     Trickett J. Food Hygiene for Food Handlers. 2nd ed. Hampshire: International Thomson business Press, 1996:33-5. 20.     Anglim AM, Far BM. Nosocomial gastrointestinal tract infection. In: Mayhall CG, editor. Hospital Epidemiology and infection control. 2nd ed. Baltimore: William and Wilkins, 2000; 196-225.



CARE-SEEKING BEHAVIOR FOR FEVER IN CHILDREN UNDER FIVE YEARS IN AN URBAN AREA IN EASTERN SUDAN Muntasir T. Salah, MD,* Ishag Adam, MD,†Elfatih M. Malik, MD‡ *Faculty of Medicine, Ribat University, †Faculty of Medicine, University of Khartoum and The Academy of Medical Sciences and Technology, ‡National Malaria Control Programme, Federal Ministry of Health, Sudan _________________________________________________________________________________________________________ مقدمة : التشخيص المبكر والعلاج الناجع يعتبران مكونان أساسيان لمكافحة الملاريا. إن تقدير الأمهات لسبب الحمى، فترة المرض، إتاحة الخدمات الطبية وتكلفتها المتوقعة، استخدام الأدوية التقليدية وتقدير المريض لمستوي الحمى تعتبر من المحددات المهمة للعلاج الفعال للحمى عند الأطفال. طريقة الدراسة: هذه الدراسة المقطعية تمت بمدينة كسلا بشرق السودان بغرض التعرف على سلوك الأمهات المرتبط بالحمى عند الأطفال أقل من 5 سنوات. جمعت البيانات بواسطة استبيان معد سلفاً وحللت باستخدام برنامج SPSS نتائج الدراسة: تم معاينة (350) من ربات المنازل. أغلب المشاركات (85.7%) نلن علي الأقل تعليماً أساسياً و244 (69.7%) منهن ليس لديهن عمل خارج المنزل. سبعة وثلاثون ومئتان (67.7%) من الأمهات لديهن معرفة معقولة عن الملاريا والتي تعتبر عند 143 (40.9%) منهن فقط سبباً للحمى عندما تكون منخفضة ولكن هذا العدد ً يتضاعف تقريباً عندما تكون الحمى عالية. .ينسحب هذا الأمر أيضاً على طلب الاستشارة من المصادر المتاحة وكذلك استخدام أدوية الملاريا، حيث وجد  أن الحمى العالية تدفع 319 (91.1%) من الأمهات لطلب الاستشارة من العاملين الصحيين و281 (80.3%) لتناول أدوية الملاريا خلاف الكلوركين. الخلاصة: مستوي الحمى ( منخفضة / عالية ) يتحكم في تحديد سبب الحمى، اختيار مصدر الاستشارة واستخدام أدوية الملاريا. جهود  التوعية الصحية يجب أن تركز على أهمية طلب الاستشارة مبكراً، الالتزام بالعلاج الموصى به والتعرف والتعامل مع علامات الخطورة قبل الوصول للوحدة الصحية. الكلمات المرجعية : الملاريا ، الحمى ، السلوك المرتبط بطلب العلاج ، السودان _________________________________________________________________________________________________ Background: Early diagnosis and prompt treatment are the basic elements of malaria control. The mother's perceptions about the cause of the fever, duration of sickness, accessibility and the anticipated cost of treatment, frequent use of traditional medicine, and judgement of the severity of the fever are the most important determinants for effective treatment of fever in children. Subjects and Methods: This cross-sectional study was conducted in Kassala city, in Eastern Sudan to investigate the caregivers' care-seeking behaviour related to fever among children < 5 years. Data was collected by trained social workers using a  structured questionnaire and was analysed by means of SPSS. Results: Three-hundred fifty housewives were interviewed. The majority (85.7%) had had at least basic education and 244 (69.7%) were full-time  housewives. A total of 237 (67.7%) mothers were found to have adequate knowledge about malaria. Malaria was perceived by  only 143 (40.9%) of the respondents as a cause of low grade fever and this percentage was almost doubled in the case of high fever. There were similar findings with respect to the selection of treatment sources and the use of antimalarial drugs. High fever urged 319 (91.1%) to seek advice from health workers and 281 (80.3%) to take drugs other than chloroquine. Conclusion: The intensity of fever (low/ high) governed the respondent's perceived causes of fever, decision about available treatment options and the type of antimalarial drugs they used. Health education programmes should focus on the importance of seeking early advice, compliance with prescribed treatment and awareness and handling of danger signs before presenting at health facility. Key Words: Malaria, Fever, Treatment-seeking behaviour, Sudan. _____________________________________________________________________________________ Correspondence to: Dr. Elfatih M. Malik, National Malaria Control Programme, Federal Ministry of Health, P.O. Box 1204, Khartoum, Sudan E-mail:
INTRODUCTION Health-seeking behaviour refers to the sequence of actions that patients and/or their parents take to solve their problem. The sequence of events begins with the identification of symptoms and then the formulation of a treatment strategy by the head of the household in consultation with other adult family members.1 Health seeking behaviour is not just a one off isolated event. It is an integral part of a person’s, a family’s or a community’s identity, which had evolved from social, personal, cultural and experiential factors.2 A variety of factors have been identified as the leading causes of poor utilization of primary health care services. These include poor socio-economic status, lack of accessibility, cultural beliefs and perceptions, low literacy level of the mothers and large family size.3       Malaria remains a major global problem, taking an enormous toll on the health and economy especially of poor communities. About 60% of malaria cases, more than 80% of malaria deaths and about 18% of deaths in children under 5 years of age occur in Sub-Saharan Africa.4 In Sudan, malaria accounts for 20-40% of all outpatient visits, 30-50% of hospital admission and 15-20% of registered deaths.5       Early diagnosis and prompt treatment are the basic elements of malaria control. They shorten the duration of the disease and prevent the development of complications and a great majority of deaths.6  The mother's knowledge and perceptions about the cause of fever, duration of sickness, accessibility and the anticipated cost of treatment, frequent use of traditional medicine, and the perceived intensity and severity of sickness were the main factors that determined early and effective treatment of children under 5 years.7-10 For instance, in Kenya the above- mentioned determinants made people go through different treatments: self-treatment, public health facilities, private, consultation of herbalists and not doing anything.9 In the Philippines, six treatment categories were identified: self-treatment with western medicine, self-treatment with traditional medicine, presentation at a consultation clinic of traditional healers, coping with the illness without treatment, the use of other methods such as sponging and not doing anything.11 Experience also showed that the majority of mothers managed their child's disease at home and used both traditional and modern treatment,12 after which they took the child to the health facility.13       The present study was conducted in Eastern Sudan to investigate the caregivers' knowledge and perceived causes of fever. Also the study aimed to explore caregivers' classification of fever in under 5-year-old children, and describe the sources and types of treatment offered to the children with fever. The results would assist in the reorientation of the ongoing health education programme to improve health-seeking behaviour and practices at home. SUBJECTS AND METHODS From January to March 2004, a community-based cross-sectional survey was conducted in Kassala city, Eastern Sudan. Every 8-12 years the area experiences a devastating flood. The last one (August 2002) led to the destruction of 70% of the houses. The area is characterized by variable malaria transmission in two seasons: post-flood in September-October and during the relatively cold period in January-February.14       After taking their consent, the housewives with children under the age of five years were interviewed. The sample size was calculated using the known formula (n=(p*q*Z2)/d2) where (n) is the sample size, (p) is the sample proportion, (q) is equal to (1-p), (Z) is the appropriate cut-off point on the standard normal distribution at 95% confidence and (d) is the degree of precision. Assuming that 70% of the housewives would respond to fever in different ways (p), if (Z) is set as (1.96) at 95% and if the degree of accuracy is taken as 5% (0.05), a total of at least 323 housewives would be needed. The investigators, however, decided to call on 400 households to compensate for refusals, and homes that had no children under five. Using the probability proportion to size, the required sample was obtained from the city's 4 major blocks.  Within each block, subjects were obtained by a systematic random allocation.       Data was collected by 4 trained social workers using a structured questionnaire. The questionnaire covered the socio-demographic profile, knowledge about malaria symptoms, the causes of fever from a caregiver's point of view and the treatment options in the case of "mild" and "severe" fever. "Mild/ severe" fever were common terms used by the natives to describe the fever. Knowledge about the symptoms of malaria was considered adequate if the respondent mentioned fever, inadequate if she mentioned other suggestive symptoms but not fever, and considered as lacking knowledge if she mentioned symptoms that bore no relation to malaria.       Data was analysed using SPSS for windows version 10.0. Tables were generated to describe the frequency, percentage and the percentage of differences in relation to the intensity of fever. Cross-tabulation was carried out to test association between caregivers, knowledge about fever and the education level, and occupation separately. Also the association between the level of education and selecting from the available treatment options was tested. Chi-square test was computed and the association was considered as significant at a p-value equal to or less than (0.05). RESULTS Three hundred and fifty housewives were interviewed with a compliance rate of 87.5%. Their educational level varied from none (14.3%) to that of a university graduate (16%) but the majority had basic education (69.7%). The majority of the respondents were housewives (69.7%) and about one quarter were employed.       A total of 237 (67.7%) mothers were found to have adequate knowledge about malaria and the rest either had inadequate knowledge (28.3%) or lacked the knowledge (4.0%) (Table 1). There was no significant difference between the level of knowledge and level of education (P0.5) but mothers who were full-time housewives had better knowledge than those who were employed (P=0.00) - data not shown. Table 1: Education level, occupation and knowledge about malaria (n=350)

Variables Frequency (%)
Educational level:
No education 50 (14.3)
Basic 244 (69.7)
University 56 (16)
Housewives 244 (69.7)
Employee 88 (25.1)
Others 18 (5.2)
Level of knowledge:
Adequate 237 (67.7)
Partial 113 (32.3)
      The caregiver's perceived causes of fever varied according to the intensity of the fever (Table 2). Malaria, was perceived as a cause by only 143 (40.9%) if the fever was mild and by 275 (78.6%) respondents if it was severe. This variation was also observed with the reported practices (Table 3) and preferred anti-malarial drugs for treatment (Table 4). Respondents who had any level of education preferred to consult health workers rather than consult other sources (p=0.00) - data not shown. Table 2: Caregivers' perceived cause of low and high fever
Perceived causes Intensity of fever % of difference
Low (%) High (%)
Malaria 143 (40.9) 275 (78.6) (+) 37.7
Respiratory dis. 131 (37.4) 39 (11.1) (-) 26.3
Teething 11 (3.1) 4 (1.1) (-) 2.0
Mixed 44 (12.6) 22 (6.3) (-) 6.3
Others 21 (6.0) 10 (2.9) (-) 3.1
Total 350 350 -
Table 3: Selection from available treatment options (ATP) in relation to intensity of fever
ATP Intensity of fever % of difference
Low (%) High (%)
Consult health personnel 141 (40.4) 319 (91.1) (+) 50.7
Self investigation for malaria 53 (15.1) 12 (3.4) (-) 11.7
Self-treatment with drugs 82 (23.4) 10 (2.9) (-) 20.5
Traditional herbs or medicine 46 (13.1) 6 (1.7) (-) 11.4
Mixture of two or more 28 (8.0) 3 (0.9) (-) 7.1
Total 350 (100) 350 (100)
Table 4: Preferred anti-malaria drugs for treatment of fever
Drugs preferred Intensity of fever % of difference
Low (%) High (%)
Chloroquine 232 (66.3) 69 (19.7) (-) 46.6
Sulfadoxine/ pyrimethamine 29 (8.3) 164 (46.9) (+) 38.6
Quinine 10 (2.9) 91 (26.0) (+) 23.1
Mixed 21 (6.0) 14 (4.0)   (-) 2.0
Others 58 (16.6) 12 (3.4)   (-) 13.2
Total 350 (100) 350 (100) -
DISCUSSION Malaria was the commonest febrile illness in the study area. This may explain the high level of knowledge reflected by this study as 60% of the respondents had adequate knowledge, while the rest had partial knowledge about the symptoms of malaria. This is in accord with other observations where recognition and classification of clinical features by the caregiver was the key to intervention.10  In contrast to the findings of other investigations,15 the level of education of the caregivers had no significant relation with positive malaria- related knowledge. This may be explained by the fact that malaria is a known problem in the area. What is unique in this study is that being full-time housewives, was found to have a significant relation.       The local understanding of febrile illness and associated treatment was complex.16 Caregivers in the area classified fever according to its intensity (mild/severe). It seemed that the perceived causes, treatment practices and anti-malarial drugs preferred depended largely on that.  In this study, malaria was considered a cause, treatment was sought from health personnel, and more potent, drugs such as quinine were used when the fever was classified as severe. Only 40.9% considered malaria the cause of mild fever while the majority of respondents (78.6%) shifted to malaria when the fever was severe. While 232 (66.3%) respondents would give chloroquine for mild fever, only 69 (19.7%) would not give chloroquine for severe fever even if they perceived malaria as a cause.       Treatment practices varied according to the evaluation of the symptoms and perceived treatment effects.16 The initial reaction of most caretakers, was to do something immediately after realizing that the child was sick, irrespective of the illness.16 In our study, this depended on the perceived intensity of fever. Only 141 (40.4%) of caregivers were likely to consult health personnel as their first option for mild fever. This is similar to what has been reported by other investigators.15,17 If the episode evolved into a more serious condition, the need for treatment services changed,9,18 as was found in our situation where 319 (91.1%) reported consulting the health personnel for severe fever. In Kenya, it was reported that patients were more likely to start with self-treatment at home and wait for some time to observe the progress of the illness.9 Self-treatment with drugs reported in this study was less than 25%. That was similar to what was reported in other urban areas of Sudan.19         In conclusion, housewives with children under 5 years had adequate knowledge about malaria. Their decision about selecting from available treatment options as a response to fever depended largely on the intensity of fever as did their choice of antimalarial drugs.   This was likely to lead to a delay in the treatment of malaria and unfortunate consequences. Health education programmes should be directed at emphasizing the importance of seeking early treatment, taking drugs as prescribed and promptly, and raising mothers' awareness of the danger signs. ACKNOWLEDGEMENT The authors would like to thank the respondents and the data collectors for their contribution to this study. REFERENCES 1.        Shaheen R, Rahman MS. Sociology of Health Care Decision: Exploration at a Public Hospital Dispensing Traditional Medicine in Bangladesh. World Health and population 2001; 4 (available at: productid=17593&cat=389&page=1  2.        MacKian S. A review of health seeking behaviour: problems and prospects. HSD/WP/05/03. available at www.hsd.lshtm. seeking_behaviour.pdf. 3.        Shaikh BT, Hatcher J. Health seeking behaviour and health service utilization in Pakistan: challenging the policy makers. J Public Health 2005; 27:49-54. 4.        WHO/UNICEF. World Malaria Report 2005.  www.rbm.who. int/wmr2005. 5.        Malik EM, Khalafalla OM. Malaria in Sudan: past, present and the future. Gazera J of Health Sciences 2004; 1 (supp): 47-53. 6.        WHO. Roll Back Malaria Strategic Framework for Scaling up Effective Malaria Case Management. partnership/wg/wg_management/docs/framework.pdf March 2004. 7.        Muller O, Traore C, Becher H, Kouyate B. Malaria morbidity, treatment-seeking behaviour, and mortality in a cohort of young children in rural Burkina Faso. Trop Med Int Health 2003;8:290-296. 8.        Comoro C, Nsimba SED, Warsame M, Tomson G. Local understanding, perception and reported practices of mothers/guardians ad health workers on childhood malaria in Tanzania district-implications for malaria control. Acta Tropica 2003;87:305-13. 9.        Nyamongo IK. Health care switching behaviour of malaria patients in a Kenyan rural community. Soc Sci Med 2002;54:377-86. 10.      Hill Z, Kendali C, Arthur P, Kirkwood B, Adjei E. Recognizing childhood illnesses and their traditional explanations: exploring options for care-seeking interventions in the context of the IMCI strategy in rural Ghana. Trop Med Int Health 2003;8:668-76. 11.      Espino F, Manderson L. Treatment seeking for malaria in Morong, Bataan, the Philippines. Soc Sci Med 2000;50:1309-16. 12.      Thera MA, D'Alessandro U, Thiero M, Ouedraogo A, Packou J, Souleymane OA, et al. Child malaria treatment practices among mothers in the districts of Yanfolila, Sikasso region, Mali. Trop Med Int Health 2000;5:876-81. 13.      Tarimo DS, Lwihula GK, Minjas JN, Bygbjerg IC. Mother's perceptions and knowledge on childhood malaria in the holoendemic Kibaha district, Tanzania: implications for malaria control and the IMCI strategy. Trop Med Int Health 2000; 5:179-84. 14.      Al Gadal AA. Malaria in the Sudan. In Proceedings of the conference on malaria in Africa, ed. Buck AA, PP. 1986; 156-159. Washington DC: American Institute of Biological Sciences. 15.      Njama D, Dorsey G, Guwatudde D, Kigonya K, Greenhouse B, Musisi S, et al. Urban malaria: primary caregivers, knowledge, attitudes, practices and predictors of malaria incidence in a cohort of Ugandian children. Trop Med Int Health 2000; 8:685-92. 16.      Nsungwa-Sabiiti J, Kallander K, Nsabagasani X, Namusisi K, Pariyo G, Johansson A, Tomson G, Peterson S. Local fever illness classifications: implications for home management of malaria strategies. Trop Med Int Health 2004;9:1191-9. 17.      Nuwaha F. people's perception of malaria in mbarara, Uganda. Trop Med Int Health 2002; 7:462-70. 18.      Konradsen F, Amerasinghe PH, Perera D, Van der Hoek W, Amerasinghe FP. A village treatment center for malaria: community response in Sri Lanka. Soc Sci Med Mar 2000; 50(6):879-89. 19.      Abdel-Hameed AA. Malaria case management at the community level in Gezera, Sudan. Afr J Med Sci 2001;30 (Suppl):43-6.


Erectile Dysfunction Among Diabetic Patients

ERECTILE DYSFUNCTION AMONG DIABETIC PATIENTS IN SAUDI ARABIA: A HOSPITAL-BASED PRIMARY CARE STUDY Yousef A. Al-Turki, DPHC, ABFM Department of Family and Community Medicine, College of Medicine, King Saud University, Riyadh, Saudi Arabia ______________________________________________________________________ هدف الدراسة: تهدف الدراسة إلى تقدير حجم مشكلة الضعف الجنسي لدى مرضى السكري الرجال المراجعين للعيادة الأولية في مستشفى الملك خالد الجامعي في مدينة الرياض بالمملكة العربية السعودية. طريقة الدراسة: شملت الدراسة 186 مريضا للسكري ممن راجعوا عيادة الرعاية الصحية الأولية خلال الفترة من 13 نوفمبر 2005 إلى 13 يونيو 2006. تم مقابلة المرضى خلال الاستشارة الطبية لعيادة استشاري في طب الأسرة ومناقشة مدى معاناة المريض من الضعف الجنسي، مع تحديد درجة الضعف الجنسي إن وجد: طبيعي، ضعف جزئي، ضعف كلي. نتائج الدراسة: بينت الدراسة التي أجريت على 186 من مرضى السكري أن 11,2% من المرضى يعانون من ضعف كامل وشديد في الانتصاب للعضو الذكري، بينما بينت الدراسة أن 64% من مرضى السكري في العينة يعانون من ضعف جزئي في الانتصاب أثناء المعاشرة الزوجية. الخلاصة والتوصيات: أهمية مناقشة مرضى السكري عن جانب الضعف الجنسي في المعاشرة الزوجية مع توخي الخصوصية والسرية أثناء الاستشارة الطبية، حيث أن البعض من المرضى قد يتردد في الإفصاح عن معاناته، مع أهمية إرشادهم إلى الطريقة الصحيحة للعلاج تحت إشراف طبي. الكلمات المرجعية : الضعف الجنسي، السكري، الرعاية الأولية. _____________________________________________________________________________ Objectives: The aim of the present study was to estimate the prevalence of erectile dysfunction  in men with diabetes mellitus attending a primary care clinic in King Khalid University Hospital, Riyadh, Saudi Arabia. Methods: A cross sectional study was carried out on men with diabetes mellitus followed in a primary care clinic of King Khalid University Hospital in Riyadh, Saudi Arabia, from 13 November 2005 to 13 June 2006. A total of 186 diabetic patients were interviewed. Data collection forms were completed by a member of the medical staff, a family medicine consultant, during the consultation of diabetic patients in the primary care clinic. Erectile dysfunction was categorized as absent erectile dysfunction (normal function), partial erectile dysfunction, and complete erectile dysfunction. The data was analyzed using the Statistical Package of Social Science (SPSS) version 11.5. A p-value of less than 0.05 was considered statistically significant. Results: A total of 186 men with diabetes mellitus were interviewed during the study period. The majority of diabetic patients (95%) had type 2 diabetes. Most of the patients (68.8%) were on oral hypoglycemic agents, 24.7% on insulin injection, and 6.5% on diet only. The present study showed that 11.2% of the diabetic patients were suffering from complete and severe erectile dysfunction, while 64% of the patients complained of partial erectile dysfunction which was affecting their marital relationship. The cardiovascular risk factors in the 186 diabetic patients were hypertension 34.9%, smoking 13.4%, obesity 40%, and dyslipidemia 16.6%. Conclusions: Complete (severe) and partial erectile dysfunction was quite common among adult diabetic patients in a hospital-based primary care setting in Saudi Arabia. It is important for primary care physicians to diagnose erectile dysfunction in diabetic patients, and to counsel them early, as most patients are hesitant to discuss their concern during a consultation. Further studies are recommended to evaluate the effect of other risk factors on erectile dysfunction in diabetic patients. Key Words: Erectile dysfunction, diabetes, primary care. _____________________________________________________________________________________ Correspondence to: Dr. Yousef A. Al-Turki, Assistant Professor and Consultant Family Medicine, King Khalid University Hospital, College of Medicine, King Saud University, P.O. Box 28054, Riyadh 11437, Saudi Arabia     E-mail:
INTRODUCTION Awareness of Erectile Dysfunction (ED) as a significantly common complication of diabetes has increased in recent years, mainly because of increasing knowledge of male sexual function and the rapidly expanding treatments for impotence. Studies of ED suggest that its prevalence in men with diabetes ranges from 35-75% and 26% in general population. The onset of ED also occurs 10-15 years earlier in men with diabetes than it does in those without diabetes.1  Erectile dysfunction  in men is multifactorial in origin: age, smoking, diabetes, heart disease, depression, and hypertension being the major factors.2 Diabetes is associated with accelerated large vessel atherosclerosis, microvascular arterial disease, autonomic neuropathy, dyslipidemia, concomitant hypertension, and prominent endothelial dysfunction. All of these conditions contribute to ED.3 The association between diabetes mellitus (DM) and ED is well established.4 Erectile Dysfunction is an important cause of decreased quality of life in men with diabetes. Impotence can cause great domestic disharmony and may be the basis of many seemingly inexplicable psychological and physical symptoms.5       Erectile dysfunction affects about 100 million men worldwide, particularly in men with diabetes. Its incidence increases with advancing age.2,3 Although around 10% of men aged 40-70 years have complete ED, only a few seek medical help.6       With recent advances in treatment and the growing body of epidemiological research on the cause of the problem, treatment and prevention of ED are possible.7       In Saudi Arabia, a multicenter cross-sectional study of patients with ED attending selected andrology and urology clinics in Jeddah revealed that 30% of the patients had diabetes.8 In Jordan, one study at the National Center for Diabetes in Amman showed that the prevalence of ED among diabetic patients was high at 62%, increasing with age and poor glycemic control.9       The aim of the present study was to estimate the extent of the problem of ED among men with DM attending a primary care clinic in King Khalid University Hospital, Riyadh, Saudi Arabia. METHOD A cross sectional study was carried out on men with DM attending a primary care clinic of King Khalid University Hospital in Riyadh, Saudi Arabia, from 13 November 2005 to 13 June 2006. A total of 186 diabetic patients were interviewed and data collection forms were completed by one family medicine consultant during the consultation of diabetic patients in the primary care clinic. Erectile dysfunction was categorized as absent ED (normal function), partial ED, and complete ED. The collected data was checked and entered into a personal computer. This was analyzed using the Statistical Package of Social Science (SPSS) version 11.5. To construct frequency distribution and cross-tabulation for variables. A p. value of less than 0.05 was considered statistically significant. RESULTS A total of 186 men with DM were interviewed during the study period. A majority of diabetic patients (95%) were type 2 diabetes.  Their age groups were as follows: 41.9% were between 40 and 60 years, 50% were 60 years and above, 7.5% between 20 and 40 years, and 0.5% between 12 and 20 years. A majority of patients (95.7%)  were married. Most (68.8%) were on oral hypoglycemic agents, 24.7% on insulin injections, and 6.5% on diet only. The duration of diabetes was as follows: 25.8% 15 years or more, 16.7%.             Table 1: Erectile dysfunction in diabetic patients (N=186)

Erectile dysfunction No. (%)
Absent (normal sexual function)   42 (22.6)
Partial erectile dysfunction 119 (64.0)
Complete erectile dysfunction   21 (11.2)
Unknown  4 (2.2)
Total 186 (100)
Table 2: Glycemic control in diabetic patients (N=186)
Glycemic control No. (%)
< 7 51 (27.4)
7 – <9 55 (29.6)
9 - <11 32 (17.2)
11 and above 5 (2.7)
Not done 43 (23.1)
Fasting blood sugar (mmol/L):
<6 39 (21.0)
6 - <8 67 (36.0)
8 - <10 36 (19.3)
10 and above 34 (18.3)
Not done      10 (5.4)
2 hours post prandial (mmol/L):
<8 34 (18.3)
8 - <11 31 (16.7)
11-<15 56 (30.1)
15 and above 48 (25.8)
Not done      17 (9.1)
Total 186 (100)
Table 3: Cardiovascular risk factors in diabetic patients (N=186)
Cardiovascular risk factors No. (%)
Smokers   25 (13.4)
Hypertensive   65 (34.9)
Total cholesterol (<5.2) 143 (76.9)
Total cholesterol (5.2-6.2)   22 (11.8)
Total cholesterol (6.2)   9 (4.8)
Not done 12 (6.5)
Obesity (Body Mass Index):
BMI <25 29 (15.6)
BMI 25 - <30 80 (43.0)
BMI 30 - <35 47 (25.2)
BMI 35 - <40 20 (10.8)
BMI 40 7 (3.8)
Not done 3 (1.6)
24-hour urine collection for total proteinuria:
Abnormal 78 (42.0)
Normal 41 (22.0)
Not done 67 (36.0)
Total 186 (100)
between 10 and 15 years, 24.2% between 5 and 10 years, 32.3% between one and 5 years, and 1.1% were less than one year.       The present study showed that 11.2% of the diabetic patients had complete and severe ED, while 64% of the patients complained of partial ED which had affected their marital relationship. The cardiovascular risk factors among 186 diabetic patients were as follows: 34.9% had hypertension, 13.4% smoked, 40% were obese, and 16.6% had dyslipidemia.       Table 1 shows ED in 186 men with DM followed in a primary care clinic at King Khalid University Hospital. Table 2 shows glycemic controls among diabetic patients. Table 3      shows cardiovascular risk factors: smoking, hypertension, dyslipedimia, and obesity among diabetic patients in the present study.              The study showed that 42% of the diabetic patients had abnormal total proteinuria. Table 4 shows the possible relational effect of other risk factors on ED in 186 diabetic patients followed in the primary care clinic at King Khalid University Hospital, Riyadh, Saudi Arabia. DISCUSSION Erectile dysfunction can be defined as the persistent inability to achieve or maintain a penile erection sufficient for satisfactory sexual performance. The most important means of diagnosing ED is to obtain a complete medical and sexual history. It is also important to
Table 4: Cross tabulation for the effect of some related risk factors on erectile dysfunction in diabetic patients (N=186)
Risk Factors Complete ED No. (%) Partial ED No. (%) Normal SF No. (%) Total No. Chi-square  p-value
Age: 0.000
<20 0 0 1 1
20-<40 0 3 (21.4) 11 (78.6) 14
40-<60 4 (5.2) 58 (75.3) 15 (19.5) 77
60 17 (18.9) 58 (64.4) 15 (16.7) 90
Duration of DM (years): 0.105
< 1 0 2 0 2
1- <5 5 (8.5) 37 (62.7) 17 (28.8) 59
5- <10 2 (4.5) 28 (63.6) 14 (31.8) 44
10- <15 4 (12.9) 21 (67.7) 6 (19.4) 31
15 10 (21.7) 31 (67.4) 5 (10.9) 46
Glycemic control (HBA1C): 0.660
<7 4 (8.2) 33 (67.3) 12 (24.5)
7 -<9 5 (9.3) 41 (75.9) 8 (14.8)
9- <11 4 (12.9) 18 (58.1) 9 (29.0)
11 0 4 (80.0) 1 (20.0)
Smoking: 0.246
Smoker 2 (8.0) 14 (56.0) 9 (36.0)
Body mass index (BMI): 0.031
< 25 3 (10.7) 17 (60.7) 8 (28.6) 28
25- <30 7 (9.0) 53 (67.9) 18 (23.1) 78
30- <35 4 (8.5) 35 (74.5) 8 (17.0) 47
35- <40 6 (30.0) 6 (30.0) 8 (40.0) 20
40 1 (14.3) 6 (85.7) 0 7
Hypertension: 0.077
Hypertensive 11 (17.5) 42 (66.7) 10 (15.9) 63
ED=Erectile dysfunction, SF=Sexual function, DM=Diabetes mellitus
distinguish this condition from other sexual dysfunctions such as premature ejaculation and loss of libido.10       Erectile dysfunction is under-recognized, not often discussed and is a commonly untreated complication of diabetes. However, it is also one of most treatable diabetic complications.1 It is a disorder that affects both the patient and his wife. The present study showed that 11.2% of the diabetic patients suffered from complete and severe ED, while 64% complained of partial ED which was affecting their marital relationship.       In the past, patients have underreported this problem because of embarrassment and the belief that not much could be done to alleviate it. The availability and marketing of new therapies for erectile dysfunction have greatly increased public awareness of the problem.11 It is estimated that 35-75% of men with diabetes have ED, and compared to age-matched control subjects, men with diabetes develop ED 5-10 years earlier.3       In American men, the incidence of ED increases markedly with age. Between the ages of 40 and 70 years, the probability of complete ED triples from 5.1% to 15%.11 In a cross-sectional survey of 541 men with diabetes at a community-based clinic, in the Massachusetts Aging Male Survey, the prevalence of ED increased progressively with age. The prevalence was 6% in the age group 20-40 years and 52% in the age group 55-59 years. Beyond the age of 60 year, 55-95% of men with diabetes were affected by ED, compared to 50% in an unselected population in the Massachusetts Aging Male Survey.3  A study undertaken in Jordan,  of 988 married diabetic men at the National Center For Diabetes, Endocrinology and Genetics between January and August 2004 showed the overall prevalence of ED as 62%. The prevalence and severity of ED in that study increased with age, and 7% were already on treatment.9       In Saudi Arabia, a multicenter cross-sectional study of 388 patients who attended 6 andrology and urology clinics within a period of 3 months were subjected to a modified structural interview questionnaire to collect demographic data and risk factors for ED. This revealed that 30% of them were diabetic, 15% hypertensive, and 56% were smokers.8 In the present study, the cardiovascular risk factors among 186 diabetic patients were hypertension 34.9%, smoking 13.4%, obesity 40%, and dyslipidemia 16.6%.  Strict glycemic control in diabetes is now strongly emphasized as a result of the large body of evidence indicating that strict diabetic control can delay and reduce the adverse effects of diabetes on multiple systems.12-15 The present study showed that 27.4% of the diabetic patients had HBA1C less than 7, while 49.5% of patients had HBA1C ≥ 7, and HBA1C were not done for 23.1% of the study sample.       Erectile dysfunction in men with diabetes is correlated with HBA1C, so the lower the HBA1C concentration, the better the mean erectile function score.3,12       The management of diabetes has always been an important part of the work of the general practitioner. For many diabetics, their general practitioner is their only source of health care and is the 'gateway' to other services. Improved knowledge of doctors of the functional and social aspects of diabetes mellitus would, therefore, improve the quality of care for patients.5,16 Education, support, and reassurance may be enough to restore sexual function in some patients. In other patients, however, different ED therapies should be tried.17-24 Involvement of the wife, even indirectly (bearing in mind the cultural values and belief), in the therapeutic decision is likely to increase the morale, help the patients to accept and cope with their condition.25       In conclusion, ED was quite common among adult diabetic patients in a hospital-based primary care setting. It is important for primary care physicians to diagnose the condition in diabetic patients, and counsel them early, as most patients are hesitant to discuss their concerns during the consultation. Further studies are recommended to evaluate the effect of other risk factors on ED among diabetic patients, and to investigate whether ED is due to psychogenic or organic complication of diabetes mellitus itself. REFERENCES 1.        Chu N, Edelman S. Diabetes and erectile dysfunction. Clinical Diabetes 2001;19:45-7. 2.        Thompson I, Tangen C, Goodman P, Probstfield J, Moinpour C, Coltman C. Erectile dysfunction and subsequent cardiovascular disease. JAMA 2005;294(23):2996-3002. 3.        Thethi T, Adjaye A, Fonseca V. Erectile dysfunction. Clinical Diabetes 2005;23:105-13. 4.        Lipshultz L, Kim E. Treatment of erectile dysfunction in men with diabetes. JAMA 1999;281(5):465-6. 5.        Abolfotouh M. Effect of diabetes mellitus on quality of life: A review. Annals of Saudi Medicine 1999;19(6):518-24. 6.        Wagner G, Tejada I. Update on male erectile dysfunction. BMJ 1998;316:678-82. 7.        Bacon C, Mittleman M, Kawachi I, Giovannucci E, Glasser D, Rimm E. Sexual function in men older than 50 years of age: results from the health professionals' follow-up study. Annals of Internal Medicine 2003;139(3):161-8. 8.        Al Helali N, Abolfotouh M, Ghanem H. Pattern of erectile dysfunction in Jeddah city. Saudi Med J 2001;22(1):34-8. 9.        Khatib F, Jarrah N, Shegem N, Bateiha A, Abu-Ali R, Ajlouni K. Sexual dysfunction among Jordanian men with diabetes. Saudi Med J 2006;27(3):351-6. 10.     Fazio L, Brock G. Erectile Dysfunction: management update.CMAJ 2004;170(9):1429-37. 11.     Viera A, Clenney T, Shenenberger D, Green G. Newer pharmacological alternative for erectile dysfunction. American Family Physician 1999;60(4):1159-68. 12.     Miller K. Does Glycemic Control correlate with erectile dysfunction. American Family Physician 2000;62(5):1141-2. 13.     Ahmed A. History of Diabetes Mellitus. Saudi Med J 2002;23(4):373-8. 14.     Cefalu W, Weir G. New technologies in Diabetes Care. Modern Medicine 2006;23:55-62. 15.     Alzaid A, Sobki S. The diagnosis of Diabetes Mellitus. A contest between 3 points. Saudi Med J 2001;22(10):839-42. 16.     Schmittdiel J, Shortell S, Rundall T, Bodenheimer T, Selby J. Effect of primary health care orientation on chronic care management. Annals of Family Medicine 2006;4:117-23. 17.     Coughlin L. The American Urological Association Updates Guidelines on management of erectile dysfunction. American Family Physician 2006;73(2):340-2. 18.     Lexchin J. Lifestyle's drugs: issues for debate. CMAJ 2001;164(10):1449-51. 19.     Kaye J, Jick H. Incidence of erectile dysfunction and characteristics of patients before and after the introduction of sildenafil in the United Kingdom: cross sectional study with comparison patients. BMJ 2003;326:424-5. 20.     Michelakis E, Tymchak W, Archer S. Sildenafil: from the bench to the bedside. CMAJ 2000;163(9):1171-5. 21.     Soliman H, Milad M, Ayyat F, zein T, Hussein S. Penile implants in the treatment of organic Impotence. Saudi Med J 2001;22(1):30-3. 22.     Al Maleky A. The penile support: A new method for the treatment of Impotence (Erectile dysfunction). Saudi Med J 2003;24(2):231-3. 23.     Freemantle N. Valuing the effects of sildenafil in Erectile Dysfunction. BMJ 2000;320:1156-7. 24.     Akbar D, Al Ghamdi A. Is hypertension well controlled in hypertensive Diabetics. Saudi Med J 2003;24(4):356-60. 25.     Kattan S. The Acceptance and satisfaction of Saudi males to vasoactive autoinjection intracavernous therapy, external negative pressure device and penile prosthesis in the treatment of Erectile Dysfunction. Annals of Saudi Medicine2002;22(3-4):149-52.



PREVALENCE OF ANTIBODIES TO HUMAN PARVOVIRUS B19 IN SAUDI WOMEN OF CHILDBEARING AGE IN MAKKAH Hani O. Ghazi, PhD Department of Microbiology, Faculty of Medical Sciences, Umm Al-Qura University, Makkah, Saudi Arabia ______________________________________________________________________ هدف الدراسة : أجريت هذه الدراسة لتحديد نسبة انتشار الأجسام المناعية بنوعيها (ج) و (م) والمضادة لفيروس البارفو B19 لدى الأمهات السعوديات بمدينة مكة المكرمة. طريقة الدراسة : تم جمع 1200 عينة من الأمهات أثناء الزيارة الجنينية الأولى وذلك لتقدير الأجسام المناعية المضادة لفيروس البارفو B19 بنوعيها (ج) و (م) (IgG and IgM) وذلك باستخدام المقايسة النوعية الماصة والرابطة للإنزيم (ELISA) . نتائج الدراسة : من خلال عينة الدراسة (1200) وجد أن 560 (46.6%) يوجد لديهم أجسام مضادة لفيروس البارفو B19 من النوع (ج) ، بينما 27 (2.25%) يوجد لديهم أجسام مضادة لفيروس البارفو B19 من النوع (م) . الاستنتاج : نستنتج من هذه الدراسة أن نسبة التعرض لفيروس البارفو B19 لدى الأمهات السعوديات في مدينة مكة المكرمة تمثل (46.6%) أما نسبة إصابة الأمهات بفيروس البارفو B19 فتمثل (2.25%) ، وهذه النسب في الواقع تقع ضمن النسب العالمية عند مقارنتها بالدراسات السابقة التي أجريت في الدول الأخرى . الكلمات المرجعية : مكة المكرمة ، المملكة العربية السعودية ، النساء الحوامل ، فيروس البارفو B19 ، تقنية المقايسة المناعية الماصة والرابطة للإنزيم (ELISA) . ______________________________________________________________________________ Objectives: To determine the seroprevalence rate of immunoglobulin G (IgG) and immunoglobulin M (IgM) to parvovirus B19 in pregnant Saudi women in Makkah.  Subjects and Methods: Using enzyme-linked immunosorbent assay (ELISA), a total of 1200 serum samples were tested for antibodies to parvovirus B19 known to cause a variety of clinical syndromes in women and newborn infants.  Results: Parvovirus B19 IgG antibodies detected in 46.6% and IgM antibodies were found in 2.25% of different age groups. Conclusion: The previous exposure to parvovirus B19 was determined, and 560 (46.6%) of 1200 pregnant Saudi women tested at their first antenatal visit were seropositive for specific IgG. The rate of maternal infection in susceptible pregnancies was 2.25%. These results were in accordance with previous studies performed in other countries. Key Words : Makkah, Saudi Arabia, pregnant women, parvovirus B19, ELISA. _____________________________________________________________________________________
INTRODUCTION Parvovirus B19 is a single-stranded DNA-virus that was serendipitously discovered in the mid-1970s by Yvonne  Crossart, a medical virologist, screening blood donors for hepatitis1. During electrophoresis, an abnormal band was noted in sample number 19, panel B. Therefore, the virus was named "B19", and subsequently identified as a parvovirus. Parvovirus B19 infection, an acute self-limiting disease also known as the fifth disease or erythema infection, commonly occurs in children of primary school age. The typical rash ('slapped cheek' appearance) is immune mediated, since it coincides with the appearance of IgM and IgG specific antibodies.1       The virus binds to its cellular receptor, the P-antigen, and has a tropism for immature erythrocytes in the bone marrow or fetal liver.2 Infection leads to an inhibition of erythropoeisis, resulting in anemia. Other tissues, such as the myocardium and endothelial cells, can also be affected.3 Clinical signs are usually fever and rash, arthralgia or such signs as febrile illness with malaise. The infection can also be
_____________________________________________________________________________________ Correspondence to: Dr. Hani O. Ghazi, Associate Professor of Virology, Faculty of Medical Sciences, P.O. Box 7091, Makkah, Saudi Arabia                E-mail:
asymptomatic. In pregnant women, the virus is known to be associated with fetal anemia, fetal hydrops, spontaneous abortion and intrauterine fetal death (IUFD).4,5 Several cases of IUFD caused by a combination of infection in the second or third trimester and hydrops are reported.6-9 Parvovirus B19 has also been demonstrated to be a significant cause of mid- trimester abortions.10       However, most infections with parvovirus B19 remains asymptomatic, and therefore, the majority of exposed persons have no recollection of previous symptoms.11 "The specific immunoglobin M (IgM) antibody detection has been the core diagnostic test for acute parvovirus B19 infection,  while the appearance of immunoglobulin G (IgG) antibodies is indicative of previous exposure to the virus.12 The prevalence of seropositivity to parvovirus B19 infection in pregnant women, in Saudi Arabia, has not been previously described. The aim, therefore, of this study was to determine the seroprevalence of parvovirus B19 in the obstetric population in Makkah, Saudi Arabia, and to compare the results to those of other countries. SUBJECTS AND METHODS A total of 1200 randomly selected pregnant Saudi women in their first trimester attending the Maternity and Children's Hospital, Al-Noor Specialist Hospital, Hera General Hospital and King Abdul-Aziz General Hospital in Makkah city, for antenatal care were included in the study.       The study was carried out from November 2005 to October 2006. The age range of the patients was 16-45 years, with a mean age of 27 years. 10ml samples of blood were collected from each of the patients after informed consent. Serum was separated, aliquoted into two eppendorf tubes and stored at -20 ºC until testing. Human serum IgG and IgM antibodies to parvovirus B19 were detected by enzyme-linked immunosorbent assay (ELISA) (EIA gen parvovirus B19 IgG kit, EIA gin parvovirus B19 IgM kit- Adaltis, Italia). Ethical Consideration An informed consent was obtained from each individual before inclusion in the study. Every subject had been informed about the procedure before the blood sample was collected, making absolutely certain that she understood the procedure to be carried out. These subjects were also made aware that they could refuse to participate in the study without prejudice. RESULTS Of the 1200 women who were tested for the presence of specific IgG antibodies 560 women (46.6%) tested positive for parvovirus B19 antibodies in the first trimester of pregnancy, implying immunity for parvovirus (Table 1). Twenty-seven (2.25%) women tested positive for IgM parvovirus B19 antibodies in the first trimester of pregnancy. The seroprevalence of IgG and IgM for parvovirus B19 specific IgG and IgM antibodies among different age groups increased with age: the lowest prevalence respectively (33.6%) (0.81%) was detected in women between 16-20 years of age reaching (53.9%) in those above the age of 36 for IgG antibodies and (3.92%) for IgM in  women above the age of 40 (Table 2). Table 1: IgG and IgM seropositivity for parvovirus B19 in Saudi pregnant women in Makkah

No. of antenatal sera tested No. of positive IgG (%) No. of positive IgM (%)
1200 560 (46.6) 27 (2.25)
Table 2: Parvovirus B19 IgG and IgM among different age groups of Saudi pregnant women in Makkah
Age groups No. of positive IgG/No. tested (%) No. of positive IgM/No. tested (%)
16-20   41/122 (33.6) 1/122 (0.8)
21-25 122/281 (43.4) 5/281 (1.8)
26-30 183/381 (48.0) 7/381 (1.8)
31-35 110/213 (51.6) 7/213 (3.3)
35-40   82/152 (53.9) 5/152 (3.3)
41-45   22/51 (43.1)         2/51 (3.9)
DISCUSSION Infection with parvovirus is common worldwide. The yearly peak incidence of infection occurs in the spring and epidemics occur every 4 years.13 The prevalence of IgG antibodies directed against B19 in the population ranges from 2 to 15% in children 1-5 years old, 15-60% in children 6-19 years old, 30-60% in adults and more than 85% in the geriatric population.14 About 35-45% of women of childbearing age do not possess protective IgG antibodies against B19.15 The incidence of acute B19 infection in pregnancy is approximately 1-2% in endemic periods, but in epidemic periods the infection rate may rise to 10%.16-18       The prevalence of parvovirus B19 infection in pregnant women, in Saudi Arabia and other countries in the Arabian Gulf (except Kuwait) has not been described previously. In Kuwait, England, USA, Spain and Japan, the prevalence was found to be 53.3, 53, 49.7, 35 and 33% respectively.19-23 In our study, seropositivity was found in 46.6%, which is similar to other studies. This is lower than the 81% reported in one area of Sweden between 1990-1991.24       The overall seroprevalence for IgG and IgM of parvovirus B19 in pregnant Saudi women in Makkah city was 46.6 and 2.25% respectively (Table 1). Seroprevalence of IgG antibodies to B19 is known to be age dependent.19 Similarly, our study showed an effect of age, in both IgG parvovirus B19 seroprevalence and the incidence of seropositive IgM (Table 2) . The incidence of acute infection in our obstetric population was 2.25%, which is comparable to previous reports.19-22       Parvovirus B19 infection is difficult to prevent since the infection is frequently asymptomatic and exposure is common during epidemics. Preventing the infection in pregnancy would be one possible application of the present candidate vaccine.25 Recently, Ballou et al (2003) described a recombinant parvovirus B19 vaccine composed of VP1 and VP2 capsid protein, which proved to be immunogenic and safe to use in human volunteers.26 Vaccination of non-immune pregnant women could be a highly effective method of preventing fetal infection with B19. However, the cost-effectiveness of this strategy in the general population is uncertain. This study may also suggest that there is a need to launch an awareness program for pregnant women. Additional studies of this nature should be encouraged to improve the knowledge of the Saudi population about the risks of exposure of pregnant women to parvovirus B19.       ACKNOWLEDGMENT This research was supported by a grant from Umm Al-Qura University, Makkah, Saudi Arabia. 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