Prevalence of Parasitic Infections Among Thai Patientsat the King Chulalongkorn Memorial Hospital, Bangkok,Thailand

SURANG NUCHPRA YOON, M.D., M.P.H., Ph.D. *, ***,P ADET SIRIY ASA TIEN, B.Sc., M.D., DTM & H, Ph.D. *,KANYARAT KRAIVICHIAN, B.Sc., M.D., DTM & H, M.Sc.*,CHANTIMA PORKSAKORN, B.Sc.*, ***,ISSARANG NUCHPRA YOON, M.D., Ph.D. **, ***

AbstractParasitic diseases are still considered to be a major public health problem. Most patients

with parasitic infections are asymptomatic and therefore remain undetected. Asymptomatic parasiticinfections are usually discovered by routine parasite examination. To determine the result of parasiteexamination at the Parasitology Unit, Out Patient Department, King Chulalongkorn Memorial Hos-pital, Bangkok, Thailand, the authors collected the data of individuals examined for parasite infec-tions from June to December 1997. A total of 6,231 Thais provided the data for analysis. Evidenceof parasitic infections was found in 557 (8.94%) cases. The disease was most prevalent in males(57.3%), and in the age group >15-30 years old (11.13%). The population from the Northeast ofThailand was found to harbor parasites with the highest prevalence rate (17.03%), while it was 11.90per cent in the northern group. The parasitic prevalence rates in the West, East, South and Centralregions were 10.60 per cent, 8.90 per cent, 7.74 per cent, and 4.92 per cent, respectively. The para-site most commonly identified was Strongyloides stercoralis (33.39%), while giardiasis was the mostcommon protozoan infection (14.36%). The highest infection rates of S. stercoralis, hookworms,Opisthorchis viverrini, and Gnathostoma spinigerum were found in northeasterners. People from theNorth of Thailand were infected mostly with G. lamblia. People of working-age from northeasternas well as northern regions harbored pathogenic parasites with high prevalence rates. To preventparasitic infections, health education for these high risk groups should be provided.

Key word: Parasitic Infections, A University Hospital Study, Thailand

NUCHPRA YOON S~ SIRIY ASATIEN P,KRAIVICHIAN K, PORKSAKORN C, NUCHPRA YOON IJ Med Assoc Thai 2002; 85 (Suppll): S415-423

* Department of Parasitology,** Department of Pediatrics,

*** Chulalongkorn Medical Research Center, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand.

8416 S. NUCHPRAYOON et al.

Parasitic infections affect people in mostdeveloping countries worldwide. Intestinal parasiticinfections are the most common parasitic infec-tions, with high prevalence rates in many regions ofthe world(l). Malabsorption, diarrhoea, blood loss,impaired work capacity, and retarded growth dueto intestinal parasitic infections constitute importanthealth and social problems(2). The public health sig-nificance of foodborne trematode infections is also

recognized in terms of morbidity, loss of producti-vity and absenteeism, health care costs, and agricul-turallosses(3). These trematode infections are almost

exclusively found in people living in Southeast Asiaand Western Pacific Regions(3).

In Thailand, parasitic diseases have beenconsidereda major public health problemfor decades.A national epidemiological survey in 1996 showedthat infections caused by parasitic helminths affectedmore than 35 per cent of the Thai population(4).Generally, morbidity from parasitic infections is mildbut chronic. The significant impact of parasitic infec-tions on public health has mostly been ignoredby the Ministry of Public Health. The problem maybe worsen with the fact that many cases of intestinalparasitic infections are asymptomatic and thereforeremain undetected. The authors report the result ofparasite examination correlated with the regionsfrom which the patients came, at the ParasitologyUnit, Out Patient Department, King ChulalongkornMemorial Hospital, Bangkok, Thailand.

MATERIAL AND METHOD

Study populationData of stool examination from all partici-

pants were obtained from the Parasitology Unit, OutPatient Department, King Chulalongkorn MemorialHospital, Bangkok, Thailand from June to December1997. The total number of subjects was 6,231. Thedetails of sex, age, residence, and kinds of helminthsor protozoa recovered were recorded and confirmedby two individuals. The provinces of all the sub-jects who participated in this study were grouped byregions. The prevalence rates of parasitic infectionsin the subjects from the northern, central, north-eastern, western, eastern, and southern regions areindicated in the map of Thailand (Fig. 1).

Diagnosis of parasitic infectionsTo determine intestinal parasitic infections,

stool specimens were examined by the direct smear

J Med Assoc Thai. June 2002

method and formalin-ether concentration techniquefor the presence of helminth eggs or larvae and pro-tozoa as previously described(5-8). About ten grainsof each stool specimen was examined microscopi-cally by using the direct smear technique. The rest ofthe specimen was processed by the formalin-etherconcentration technique. To avoid contamination,specific precautions were explained to all individualson how to handle the stool specimens before send-ing them to the laboratory.

Special techniques recommended by theParasitology Unit of King Chulalongkorn MemorialHospital were also used for diagnosis of particularparasites. Gnathostomiasis was determined by a skintest using soluble antigen extract from the third-stage larvae of Gnathostoma spinigerum. A sero-logic test (Indirect hemagglutination (IRA) test,Cellognost@Amoebiasis) was used as an additionaltest for Entamoeba histolytica. ELISAs for Toxo-plasma gondii IgM and IgG antibodies were per-formed for diagnosis of toxoplasmosis. Detectionof Cryptosporidium spp. and Cyclospora spp. wasdone by using modified cold Kinyoun acid-faststain. Microsporidium spp. was recovered by usingTrichrome stain. Pneumocystis carinii, Plasmodiumspp., and filarial parasites were examined by Giemsastain as previously described(9,10).

Data analysisThe data were recorded and analyzed by

using Excel 6.0 software program. Differences inprevalence rates were compared by the Chi squaretest. Statistic analysis was performed with the levelof significance at p-values <0.05.

RESULTSOf the 6,231 individuals registered for the

parasite examination, 2,935 (47.10%) were male and3,296 (52.90%) were female (Table 1). The ages ofall participants ranged from 18 days to 104 yearswith the mean:tSD of 40.15:t18.9 years. Most studyindividuals were in the age group >15-30 years(33.61%). The lowest number was found in childrenless than 15 years (4.24%). The age group >30-45,>45-60, and >60 years comprised 1,682 (26.99%),1,098 (17.62%), and 1,093 (17.54%) individuals,respectively. The majority of study individuals werefrom the central region of Thailand (3,574 indivi-duals; 57.36%) (Table 2). There were 1,662(26.67%)individuals from the northeastern region. The num-

Vol.85 Suppl 1 PARASITIC INFECTIONS: THAILAND S417

Fig. 1. Prevalence of parasitic infections classified by regions.

Table 1. Prevalence of parasitic infections classified by age and sex.

Age group Number examined Number infected

(years) Total Male Female Total Male Female% % % % % %

15 264 4.24 141 53.41 123 46.59 18 6.82 10 7.09 8 6.50>15-30 2,094 33.61 974 46.51 1,120 53.49 233 11.13 137 14.07 96 8.57>30-45 1.682 26.99 823 48.93 859 51.07 165 9.81 96 11.66 69 8.03>45-60 1.098 17.62 487 44.35 611 55.65 70 6.38 35 7.19 35 5.73>60 1,093 17.54 510 46.66 583 53.34 71 6.50 41 8.04 30 5.15

Total 6,231 100 2,935 47.10 3,296 52.90 557 8.94 319 10.87 238 7.22

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ber of individuals from the East, North, South, andWest of Thailand were 382 (6.13%), 294 (4.72%),168 (2.70%), and 151 (2.42%), respectively.

Parasitic infections classified by age and sexAmong the 6,231 individuals examined,

557 (8.94%) cases were infected with at least oneparasite (Table 1). The highest prevalence rate ofparasitic infections was found in the age group> 15-30 years (11.13%), The parasitic infection rates were9.81 per cent, 6.82 per cent, 6.50 per cent, and 6.38per cent among individuals in the age group >30-45, ::;15,>60, and >45-60 years, respectively. Males(10.87%) were infected with parasites more thanfemales (7.22%) in all age groups. There was asignificant difference in the infection rates of malesand females in the age group >15-30 (p<O,OOI)and>30-45 (p<0.05) years.

Highest prevalence of parasitic infections foundin the northeastern population

Parasitic infections were most common in

the northeastern group (17.03%) (Fig. 1, Table 2).The prevalence rate of parasitic infections of 11.90per cent was found in subjects from the north region.Those from the West, East, and South of Thailandwere found to harbor parasites with the prevalencerates of 10.60 per cent, 8.90 per cent, and 7.74 percent, respectively. The lowest prevalence rate ofparasitic infections of 4.92 per cent was found inthe central group.

Strongyloid stercoralis identified most commonlyThe highest proportion of parasites identi-

fied among infected cases was S. stercoralis(33.39%)(Fig. 2). The second most common parasite iden-tified in the infected cases was hookworms, as wellas liver fluke (Opisthorchis viverrini) (24.06%).4.67per cent of the subjects were infected with Gnatho-stoma spinigerum. Other helminths found less fre-quently were Trichuris trichiura (1.80%), Echino-stoma spp. (1.26%), Taenia spp. (1.08%), Ascarislumbricoides (0.36%), and Hymenolepis diminuta(0.18%). Among protozoan infections, giardiasiscaused by Giardia lamblia was most commonlyfound (14.36%), The proportions of Entamoeba his-tolytica, Cryptosporidium spp" Toxoplasma gondii,Sarcocystis spp" Plasmodium spp" and Isosporabellifound among infected cases were 1.26 per cent, 1.08per cent, 0.90 per cent, 0.90 per cent, 0.36 per cent,and 0,36 per cent, respectively.

Isospora belli

Plasnwdium spp.

Sarcocystis spp.

Toxoplasma gondii

Cryptosporidium spp.

Entamoeba histolyticaGiardia lamblia

Hymenolepis diminuta

Ascaris lumbricoides

Taenia spp.

Echinostoma spp.

Trichuris trichiura

Gnathostoma spinigerum

Opisthorchis viverrini

Hookworms

Strongyloid stercoralis

Fig. 2.

(%)

0 5 10 15 20 3525 30 40

ID

Helminthic infections

Protozoan infections

Proportion of parasites identified in infected patients, except Toxoplasma gondii diagnosed by ELISA, Entamoeba histolytica by IHA and Gnatho-stoma spinigerum by skin test.

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8420 S. NUCHPRAYOON et al.

Mixed infection by soil-transmitted helminthsOf the 6,231 individuals, 52 (0.83%) har-

bored more than one parasite (Fig. 3). The majorityof mixed infections among infected cases were thecombination of S. stercoralis and hookworm infec-tions (15 cases; 0.24%). Interestingly, co-infectionof S. stercoralis and O. viverrini (10 cases; 0.16%)was the second most common.

Prevalence of parasites commonly identified ineach region

The percentages of infections caused bythe helminths commonly identified, S. stercoralis(6.08%), hookworm (4.45%), O. viverrini (5.17%),and G. spinigerum (0.72%), were highest in thenortheastern population (Table 2). S. stercoralis, O.viverrini, and G. spinigerum were the second most

One protozoa identified:E. histolytica = 7 casesCryptosporidium spp. = 6 casesT. gondii = 5 casesPlasmodium spp. =2 casL belli = 2 cases

One helminth indentitied:

Taenia spp. = 6 casesH. diminuta = 1 casesA. lumhricoides = 2 cases

G. spinigerum = 26 cases

J Med Assoc Thai June 2002

common in subjects from the North with the pre-valence rates of 5.44 per cent, 3.40 per cent, and0.68 per cent, respectively. Hookworm infectionswere the second most common in the western popu-lation (3.31%). The protozoan infection commonlyidentified, giardiasis, was found most common inthe northerners (2.04%), and secondary most com-mon in the northeasterners (1.62%).

DISCUSSION

The prevalence of parasitic infections in apopulation who visited the Parasitology Unit, OutPatient Department, King Chulalongkorn MemorialHospital, Bangkok, Thailand were reported routinelyand requested parasite examination. Based on theparasitic prevalence of the national survey in 1996(35%), the present data showed lower percentages

104

Uninfected = 5,674 cases

Fig. 3. A Venn Diagram showing pattern of mixed parasitic infections.

Vo!.85 Suppl 1 PARASITIC INFECTIONS: THAILAND S421

of infected cases (8.94%). This may be due to thefact that most people infected with parasites areasymptomatic, therefore, they usually do not comefor parasite examination. The high prevalence ratesof parasitic infections were found in the workingage groups, and especially in males (Table 1). Thepresent study also showed that individuals from theNortheast of Thailand harbored parasites with thehighest prevalence rate (Fig. 1, Table 2). It is pos-sible that this high risk group had high risk beha-vior for parasitic infections. Parasitic infections werefound to be lowest in those from the Central region.The results suggested that the majority had betterpersonal and community hygiene, and sanitationcompared to the other regions.

Soil-transmitted helminths, the main causeof intestinalparasitic infections, affect people world-wide including Thailand. From the national survey,hookworms are the most common parasites (22%)found in Thailand, followed by O. viverrini (12%)(4). Hookworm infections are a major health pro-blem in the southern region of Thailand while opis-thorchis is more prevalent in the northern and north-eastern regions(4). The authors showed that amonginfected cases, the most common parasitic infectionswere due to soil-transmitted helminths (Fig. 2).Moreover, the majority of mixed parasitic infectionswere also caused by soil-transmitted helminths (Fig.3). An interesting finding was that the prevalenceof strongyloidiasisin infected cases was higher thanthe prevalence of hookworm infection and opisthor-chiasis (Fig. 2). Agriculture is the main occupationfor Thai people, and as in other tropical countries,they work in fields routinely without wearing appro-priate shoes, and the lack of sanitary latrines, seemto be the major causes of soil-transmitted parasiticinfections(7). Several other factors may contributeto the high prevalence of soil-transmitted helminthinfections, including type of soil, amount of rainfall,temperature and humidity(ll). The majority of thestudy population were from areas in which the eco-system of wet and dry lands markedly affected thepopulation density of S. stercoralis larvae. Furtherstudy may help to answer this question.

The authors found that the highest infectionrates of S. stercoralis, hookworms, and O. viverriniwere found in the northeasterners (Table 2). Farmersor plantation workers are most likely to contributeto the patterns of high soil-transmitted helminthinfections(2), while eating habits are a major causefor opisthorchiasis(3). It could be that the majority

of the participantswere farmers or plantationworkers,and rarely use sandals when working on their farmswhere larvae of soil-transmitted helminths are moreprevalent. Opisthorchiasis was also more prevalentin northerners. Furthermore, infection caused by G.spinigerum was found to be prevalent in the north-eastern and northern groups. Since both O. viverriniand G. spinigerum are carried by fish, the behaviorof eating uncooked or insufficiently cooked aquaticfood, especially fresh-water fish, is responsible forthe increase in opisthorchiasis(3) as well as gnatho-stomiasis.

Internal autoinfection may cause fatal dis-seminated strongyloidiasis in an immunocompro-mised host(12). The present data emphasize thatpatients who have to receive immunosuppressivetherapy should be investigated for strongyloidiasis.Hookworm infections cause anemia and influencebehavior and learning as well as problem-solvingcapacities(13-15).The effect of hookworm infectionson anemia in adults could be significant, particularlyfor females of reproductive age(16). While anemiais commonly found in Thailand(6,8), investigationfor hookworm infections in suspected cases shouldnot be avoided. Thailand is recognized as being themost highly endemic country for opisthorchiasis dueto O. viverrini. It is a serious public health problemby virtue of its association with cholangiocarcinoma(17-21). Therefore, health education to reduce thehigh risk behavior of consumption of uncooked orpartially cooked fresh-water fish is necessary.

Giardiasis was the most common protozoaninfection highly prevalent in the people from thenorthern region (Table 2). Giardia is a commonmajor cause of outbreaks of waterborne infection(22). Inadequate quality water supply and foodcontaminated by fecal materials are responsible forgiardiasis(2). Therefore, strategies to control thedisease are to improve personal hygiene and waterquality as well as to provide health education.

For control of parasitic diseases, surveil-lance and mass treatment therapy should be conti-nuously implementedto minimize host reservoirs andprevent infections(23). Health education to sustainpositive health behavior has to be continued. Empha-sis has to be given to using sanitary latrines and thesustainable habit of wearing shoes for interruptionof soil-transmitted helminth infections, as well asavoiding consumption of uncooked or partiallycooked fresh-water fish for interruption of opisthor-chiasis and gnathostomiasis.

8422 S. NUCHPRA YOON et al.

ACKNOWLEDGEMENTSThe authors would to thank all the staffs of

the Department of Parasitology, Faculty of Medi-cine, Chulalongkom University, Bangkok, Thailand

J Med AssocThai June 2002

for their technical support. SN and CP are supportedby the Thailand Research Fund (grant RGJ/PHD/00179/2541).

(Received for publication on March 1.. 2002)

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