malaria and intestinal parasitosis among children presenting to the

1048 La Revue de Santé de la Méditerranée orientale, Vol. 9, No 5/6, 2003

Malaria and intestinal parasitosisamong children presenting to thePaediatric Centre in Sana’a, YemenA.A. Azazy1 and Y.A. Raja’a2

1Department of Parasitology; 2Department of Community Medicine, Faculty of Medicine and HealthSciences, Sana’a,Yemen.Received: 14/08/02; accepted: 16/03/03

ABSTRACT We studied the profile of malaria and intestinal parasitosis among children presenting to thePaediatric Health Centre in Sana’a from January 1998 to December 2000. In stool samples from 9014children, Ascaris lumbricoides, Entamoeba histolytica, Giardia lamblia and Trichuris trichiura were the mostcommon. Infection with parasites of direct life-cycle were similar in boys and girls. Schistosome infection wassignificantly higher in boys than girls, but girls were more infected with ascariasis. The only species of malariaparasite found in blood samples from 753 children with suspected malaria was Plasmodium falciparum, withthe highest rates in April–June. The majority of positive cases were Yemeni children, but 10.8% wereSudanese or Ethiopian.

Le paludisme et la parasitose intestinale chez les enfants consultant au centre pédiatrique deSanaa (République du Yémen)RESUME Nous avons étudié le profil du paludisme et de la parasitose intestinale chez des enfants amenésen consultation au centre pédiatrique de Sanaa de janvier 1998 à décembre 2000. Ascaris lumbricoides,Entamoeba histolytica, Giardia lamblia et Trichuris trichiura étaient les parasites les plus courants. L’infestationpar des parasites qui ont un cycle de vie direct était similaire chez les garçons et les filles. L’infestation pardes schistosomes était significativement plus élevée chez les garçons que chez les filles, tandis que les fillesétaient davantage touchées par l’ascaridiase. Plasmodium falciparum était la seule espèce de parasite dupaludisme trouvée dans les échantillons sanguins de 753 enfants suspects de paludisme, les taux les plusélevés entre avril et juin. La majorité des cas positifs étaient des enfants yéménites, mais 10,8 % étaient desSoudanais ou des Ethiopiens.

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Eastern Mediterranean Health Journal, Vol. 9, Nos 5/6, 2003 1049

IntroductionThe highest rates of protozoa and helminthinfections worldwide occur in the tropics.The distribution of these infections de-pends on conditions such as a suitable cli-mate and human activities such aspopulation movements and poor sanitation.

Malaria is the major public health prob-lem in Yemen [1], and has the typical afro-tropical pattern in which the predominantspecies is Plasmodium falciparum [2,3]. Aprevious study found that the incidence ofP. falciparum infection among Yemeni re-turnees in Al-Hodeidah governorate was13.9%, with some seasonal variations [3].

Transmission of ascariasis and trichuri-asis takes place throughout the year in re-gions with a temperate climate. Thesoil-transmitted parasites, mainly Ascarislumbricoides and Trichuris trichiura, areusually more prevalent where there isfavourable soil, warmth and moisture to-gether with poor sanitation. Studies in dif-ferent parts of Yemen have reportedprevalence rates of ascariasis ranging from16%–68% [4–6]. Meanwhile, trichuriasiswas reported, mostly from the same areas,in 1%–21% of the population [6,7].

Parasites with a direct life-cycle spreadmore easily among children and within thehousehold. Various studies in Yemen havebeen conducted on the different parasiteswith a direct life-cycle. For example, theprevalence of Entamoeba histolytica hasbeen reported to range from 1.7%–36%[4,7], while for Giardia lamblia it was9.0%–20.5% and for Hymenolepis nana2%–8.3% [6,8]. The lowest prevalencewas 0%-2% for Enterobius vermicularis[4,6].

The most prevalent water-borne para-site in Yemen is the schistosome. Schisto-somiasis is second to malaria in the list ofmajor public health problems in the country

[1] and intestinal schistosomiasis has beenreported in a number of different surveys[6–12]. Very low rates of infection havebeen reported for Fasciola hepatica, from0.5%–2.0% [4,7]. Low prevalence rates of0.1%–0.3% were reported for Taenia spp.[4,7].

With the exception of Farag’s study in1985 [4], all other published works fromYemen have focused on schoolchildren andchildren in the community. None of thestudies focused on children at the hospitallevel and none has investigated malariatransmission in Sana’a, the city capital ofthe country. The current study thereforeaimed to determine the profile of malariaand intestinal parasitic infections amongchildren attending the Paediatric HealthCentre in Sana’a.

MethodsThe Paediatric Health Centre in Sana’a pro-vides services to the community throughoutpatient clinics and admissions. The cen-tre receives patients from Sana’a city, sur-rounding areas and sometimes from othergovernorates, as well as referred casesfrom private clinics. Children with suspect-ed infections are referred to the laboratoryunit for investigation. In a record-based de-scriptive study, we reviewed the results of9014 stool samples from Yemeni childrenand 753 blood samples from Yemeni andother nationality children who had been re-ferred to the laboratory unit during the peri-od January 1998 to December 2000. Formalaria, additional questions about resi-dence, nationality and travel history toknown endemic areas were investigatedand recorded in the laboratory notes. Allstool and blood samples were examined inthe centre’s laboratory.



Children being investigated for intestinalprotozoa or helminth infections provided astool sample. A normal saline sedimentationtechnique was adopted for stool examina-tion. Formal ethyl acetate sedimentation ordirect smear methods were also used whennecessary. For children who complained ofpruritis ani or nocturnal enuresis, transpar-ent adhesive tape was used to take analswabs.

Children suffering febrile illnesses andsuspected of having malaria were asked togive a blood sample. Thick and a thin bloodfilms were prepared for each case. Thinfilms were fixed with absolute methanoland stained with 3% Giemsa diluted in pH7.2 buffered water for 30 minutes. Thickfilms were stained unfixed.

The data were analysed using Epi-Info,version 6.

ResultsThe age of the children ranged from 2months to 14 years.

MalariaOf 753 children examined for suspectedmalaria (484 boys and 269 girls), 130(17.3%) were positive for malaria. Theonly species of malaria parasite identifiedwas P. falciparum. The distribution of in-fection among the cases by age group, sexand nationality is shown in Table 1. Twiceas many boys (66.9%) as girls (33.1%)were infected. The highest rate of infectionwas in the age group 6–10 years. The ma-jority of children testing positive (89.2%)were Yemeni, but 8.5% were Sudanese and2.3% were Ethiopian. Most of the positivecases lived in Hezyaz, 25 km south ofSana’a, but some came from Arrowdhahon the opposite side of the city; some posi-tive cases had never been out of the Sana’aarea.

The highest seasonal rates of infectionwere recorded in the months June, Mayand April respectively (Figure 1).

Intestinal parasitesOf 9014 children examined, 2477 (27.5%)positive tests for intestinal parasites werefound. The intestinal parasites detectedamong infected children are shown in Table2. With the exception of Schistosoma man-soni and Taenia saginata, most of the in-testinal parasites were those with afeco–oral route of transmission. Four dif-ferent parasites, A. lumbricoides, E. his-tolytica, G. lamblia and T. trichiura, hadthe highest rates.

Overall, the infection rate was signifi-cantly higher among girls (1192, 31.5%)than boys (1285, 24.6%) (P < 0.001). Par-asites with a direct life-cycle showed asimilar sex distribution. However, the rateof A. lumbricoides infection among girlswas significantly higher than that amongboys. In contrast, the infection rate with E.histolytica was significantly higher amongboys than that among girls (P < 0.001).

Table1 Sex, age and nationality distributionof 130 children with a diagnosis ofPlasmodium falciparum infection

Variable Children infected (n = 130)No. %

SexMale 87 66.9Female 43 33.1

Age (years)0–5 15 11.56–10 89 68.511–14 26 20.0

NationalityYemeni 116 89.2Sudanese 11 8.5Ethiopian 3 2.3

n = total number of infected children.



Figure 1 Monthly distribution of cases among 130 children diagnosed with Plasmodiumfalciparum infection

DiscussionOur study revealed a parasite infection rateof 17.3% among children tested for malar-ia. The species of malaria found was exclu-sively P. falciparum. This is consistentwith the documented pattern of malaria inYemen, which is classified as afro-tropicalwith P. falciparum as the predominant spe-cies. Previous studies in Yemen have foundthat P. falciparum constitutes 90%–95% ofall diagnosed malaria cases [2,3]. The in-fection rates were highest in June, May andApril respectively. This finding indicatesthat malaria in Sana’a city may have itsown pattern of seasonality that is differentfrom Al-Hodiedah governorate.

The present study revealed that 10.8%of the malaria cases were children fromSudan and Ethiopia who may be either im-migrants or indiginous. Interestingly, somepositive cases in our study had never beenout of the Sana’a area, which is supposedto be a non-malarial area due to its high alti-tude (2400 m above sea level). Most of thepositive cases were children living in anarea called Hezyaz, about 25 km to the

south of Sana’a, which lies on the road thatconnects the capital with two endemic ar-eas, Taiz and Hodeidah cities. The main ac-tivity of the population in Hezyaz, besideagriculture, is serving food for travellers.Therefore, it can be hypothesized that in-fected mosquitoes hidden in vehicles areresponsible for transmission of the disease.Another possibility is that transmission ofmalaria is taking place in Sana’a city itself.This is backed up by the fact that somecases also came from another area on theopposite side of the city called Arrowdhah.

With the exception of S. mansoni andTaenia saginata, the intestinal parasites di-agnosed in the current study are those witha feco–oral route of transmission. It wasexpected that the infection rate with intesti-nal parasites would be similar among boysand girls. Surprisingly, however, the infec-tion rate among girls was greater than thatamong boys. Parasites with a direct life-cycle were found to have a similar sex dis-tribution. This was not the case with S.mansoni, where the rate among boys washigher than that among girls. This can be



Table 2 Pattern of intestinal parasites detected in 9014 tests for parasitic infections amongchildren

Parasite Positive testBoys (n = 1285) Girls (n = 1192) Total (n = 2477) χχχχχ 2 P-value

No. % No. % No. %

Ascaris lumbricoides 235 18.3 286 23.9 521 21.0 42.0 < 0.001

Entamoeba coli 258 20.0 248 20.8 506 20.4 0.83 0.36

Giardia lamblia 226 17.6 188 15.8 414 16.7 5.14 0.023

Trichuris trichiura 201 15.6 180 15.0 381 15.4 0.68 0.44

Entamoeba histolytica 160 12.5 129 10.8 289 11.7 6.15 0.013

Hymenolepis nana 149 11.6 123 10.3 272 11.0 3.84 0.05

Schistosoma mansoni 37 2.9 16 1.3 53 2.1 26.1 < 0.001

Enterobius vermicularis 13 1.2 20 1.7 33 1.3 3.78 0.052

Fasciola hepatica 4 0.3 2 0.2 6 0.2 1.95 0.16

Taenia saginata 2 0.2 0 0 2 0.1 NA NA

Total 1285 24.6 1192 31.5 2477 27.5 52.5 < 0.001

n = total number of tests.NA = not applicable.

attributed to boys having more activities in-volving contact with water than girlsthrough swimming and ablutions. As forascariasis, the rate of infection was higheramong girls than that among boys. Thiscan be explained by girls being involvedmore with food preparation than boys, ex-posing them to raw foods contaminatedwith larvated eggs.

ConclusionsHigh rates of infection with protozoa andhelminth parasites denote high levels of pol-

lution in the environment of the study area.More efforts are needed to improve envi-ronmental sanitation in Sana’a in order toreduce the rate of infection with intestinalparasites. To our knowledge, this is thefirst report that shows some evidence thatmalaria is being transmitted in Sana’a city.A special study to confirm or refute thesuggestion that the vector for malaria isbreeding in Sana’a is urgently needed.

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