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Paediatrica Indonesiana

VOLUME 54

January ‡_____

NUMBER 1

Original
Article

Soil-transmitted helminth infection and skin
prick test reactivity in children
Schenny Regina Lubis, Lily Irsa, Rita Evalina, Supriatmo, M. Sjabaroeddin

Abstract

Background Allergic diseases cause an increasingly

M

ore than two billion people
worldwide
are
chronically
infected with soil-transmitted
helminths
(STHs)
including
Ascaris lumbricoides, Trichuris
trichiura and
hookworms Ancylostoma duodenale and
Necator americanus.1 The International
Study of Asthma and Allergy in Childhood
(ISAAC) reported large diferences in the
prevalence of self-reported symptoms of
allergic disease. For asthma symptoms, the
highest prevalences were from centers in the
United Kingdom, Australia, New Zealand, and
Ireland, while the lowest prevalences were
from centers in China, Indonesia, India, and
Ethiopia. ___ In addition, a Makassar,
,QGRQHVLD_VWXG\_LQ______UHSRUWHG_D_____SUHYDOH
QFH_LQ_ moderate-severe allergic rhinitis.5
Soil-transmitted
helminth
infections may induce strong allergic
responses in humans. There are close
similarities in allergic inflammation
caused by host immune responses to
environmental allergens and to parasite
antigens. _ Nonetheless,

large
burden in developed countries and in urban areas of
middle-income countries. Parasitic infections may
induce
allergic
responses in
humans,
particularly soil-transmitted helminth (STH) infections
that are prevalent in childhood in developing
countries.
Although
soil-transmitted
helminth
infections have been
associated
with
lower
prevalence of allergen skin test reactivity, study
outcomes remain inconclusive.
Objective To analyze for an association between STH
infections and skin prick test reactivity in children.
Methods :
H_FRQGXFWHG_D_FURVV_VHFWLRQDO_VWXG\_LQ_$XJXVW______
DPRQJ_SULPDU\_VFKRRO_VWXGHQWV_DJHG______\HDUV__DW_6HFD
QJJDQJ_ Subdistrict, Langkat District, North Sumatera
Province. Sixty
HLJKW_FKLOGUHQ_ZHUH_UHFUXLWHG_LQ_WKLV_VWXG\_FRQVLVWHG_RI____
FKLOGUHQ_
ZLWK_67+_LQIHFWLRQV_DQG_WKH_RWKHU____FKLOGUHQ_ZLWKRXW_D
Q\_67+_ infection. Soil-transmitted helminth
infections were determined by Kato-Katz stool
examinations. All subjects underwent skin prick tests
for seven allergens. Results were considered to be
SRVLWLYH_LI_ZKHDO_GLDPHWHUV_ •___PP_ DQG_QHJDWLYH_ZKHQ_
ZKHDO_
GLDPHWHUV_____PP__'DWD_ZDV_DQDO\VHG_E\_&KL_VTXDUH_WHV
W_ Results Stool examinations revealed that the most
common infection was T.
trichiura_ ______ VXEMHFWV___ IROORZHG_ E\_ PL[HG_
infections (T. trichiura and A.
lumbricoides________VXEMHFWV___DQG_ A.
lumbricoides______VXEMHFWV___7KHUH_ZDV_D_VLJQLILFDQW_DVVRF
LDWLRQ_
EHWZHHQ_67+_LQIHFWLRQV_DQG_QHJDWLYH_VNLQ_SULFN_WHVW_3 ________
In addition, there were significant associations with
negative VNLQ_SULFN_WHVWV_3 _______
negative skin prick tests for each helminth type: A.
Conclusion Children with STH infections tend to have
lumbricoides_ 3 ________ T. trichiura 3
negative skin prick test results. [Paediatr Indones.
______ DQG_ PL[HG_ LQIHFWLRQ_ 3 ________ 6HYHUH_
2014;54:52-6.].
infection intensity was also significantly associated with

No. Jl. Adam Malik Hospital. University of North Sumatera Medical School.Keywords: soil-transmitted helminth. 1. H.$__. Vol. University of North Sumatera Medical School. January 2014 . Department of Child Health. Adam Malik Hospital. Indonesia. Medan. Reprint requests to: Schenny Regina Lubis. 54. skin prick test This study was presented at the Child Health National Congress . H.21.. %XQJD_/DX_1R______0HGDQ_________7HO_________________²___ ______ ________)D[_________________(_PDLO__VFKHQQ\UHJLQD#\DKRR_F RP_ 52_‡_Paediatr Indones.9__0DQDGR__-XO\___²_________ From the Department of Child Health.

Langkat District. a country with a low prevalence of DVFDULDVLV_HVWLPDWHG_WR_EH____LQ_DGXOWV_DQG_FKLOG UHQ___ EXW_ KLJK_ SUHYDOHQFH_ RI_ DVWKPD_ ______ DPR QJ_ adolescents).9 Our study was designed to investigate the relationship between STH infections and skin prick test results in children.trichiura may protect against the development of allergen skin test reactivity in later childhood. quick._ Even today skin testing remains the main test for confirming an allergic response. currently using corticosteroids at the time of enrollment. it is easy. New primary care guidelines for the management of asthma.8 With the right technique and interpretation. Brazil study found that early infection of T. or with a history of dermatographism were excluded. In addition. this test has higher sensitivity and specificity. We calculated the PLQLPXP_ UHTXLUHG_ QXPEHU_ RI_ VXEMHFWV_ WR_ EH_ ___ I RU_ . with and without STH infection. DUDQJ_*DGLQJ_DQG_6'1________5LQWLV__LQ_6HF DQJJDQJ_ Subdistrict. less expensive.Schenny Regina Lubis et al: Soil-transmitted helminth infection and skin prick test several epidemiological studies suggested an inverse relationship between STH infections and allergies. :H_LQFOXGHG_FKLOGUHQ_DJHG___WR____\HDUV_ZKRVH _SDUHQWV_ were willing to fill out questionnaires. a Salvador. Subjects were consisted of two groups. and painless. Methods This cross-sectional study was conducted in August _____LQ_FKLOGUHQ_IURP___SULPDU\_VFKRROV__6'1 ________ . lumbricoides and asthma severity among children with asthma in Costa Rica._ Furthermore. A cross-sectional study pointed out the possible inverse association between sensitization to A. as well as good allergen quality. rhinitis and eczema now recommend allergy testing as part of an atopic child workup. Children using PHGLFDWLRQV_VXFK_DV_DQWLKLVWDPLQHV_ZLWKLQ___GD\V _SULRU_ WR_HQUROOPHQW__DQWLKHOPLQWLFV_ZLWKLQ___PRQWKV_S ULRU_WR_ enrollment. North Sumatra Province.

cat dander. Results Allergens were produced by the Department of Pharmacy. feathers. Surabaya. A. cotton. or severe. 94 children Hospital. January 2014_‡_53 . Dr. house dust.lumbricoides__PLOG_________(3*___PRGHUDW The data collected was processed. STH infection group (Table 2). moderate. :RUOG_+HDOWK_2UJDQL]DWLRQ_([SHUW_&RPPLWW This study was approved by the Ethics HH______ criteria were used to sub-classify Committee of the University of North the STH groups: A Sumatra Medical School. . RQ________VXEMHFWV_LQ_67+_LQIHFWLRQ_JURXS_DQ Stool specimens were analyzed by G_______ subjects in non STH infection Kato-Katz method for the presence and group. Severity of infection was classified as Negative skin prick test was significantly mild. _______(3*___RU_VHYHUH_LQIHFWLRQ_•_______( DQG_SUHVHQWHG_XVLQJ_6366_YHUVLRQ_______7R_DV 3*___DQG_ T. H_______ analyzed.(EPG) on stool microscopic _2YHUDOO_ SPT results were considered to be examinations. Vol. cockroach. Positive skin severity of infection. to be positive in the Comparing the two groups. Informed consent was provided by subjects’ SULFN_ WHVW_ 3 ________ 6NLQ_ SULFN_ WHVW_ ZDV_ QHJDWLYH_ parents or guardians. and fungi. 1. based on the asso-ciated with all three infection types. No. Soetomo During the study period. VHVV_WKH_ association between STH infections trichiura_PLOG_______(3*___PRGHUDWH______ and skin prick test results in children. The SPTs were ZHUH_ performed on the volar forearm area with a FRQVHFXWLYHO\_ VHOHFWHG__ FRQVLVWHG_ RI_ ___ FKLOGU HQ_ blood lancet at a 45_ angle to ZLWK_67+_LQIHFWLRQV_DQG____FKLOGUHQ_ZLWKRXW_ WKH_IRUHDUP__6HQVLWL]DWLRQ_ZDV_DVVHVVHG_______ 67+_ infection. Subjects’ characteristics PLQXWHV_ after skin puncture and considered are shown in Table 1. The positive if at least one allergen was positive. Appropriate SULFN_WHVW_UHVXOWV_ZHUH_REVHUYHG_LQ___VXEMHFWV_LQ_ treatment was given to all children with 67+_ infection group and 14 subjects in non STH infections after stool analysis. we _______ (3*___RU_VHYHUH_•_______(3*____ used Chi-square test with Subjects underwent skin prick tests D_VLJQLILFDQFH_OHYHO_RI_3_______ (SPT) of seven allergens including house dust mites. number of eggs per gram lumbricoides Paediatr Indones. Positive underwent DQG_QHJDWLYH_FRQWUROV_ZHUH____KLVWDPLQH_DQG VWRRO_ H[DPLQDWLRQ_ VFUHHQLQJ__ ___ RXW_ RI_ WKHP_ ______ NaCl. there was a FDVH_RI_D_UHG_ZKHDO_•__PP_LQ_GLDPHWHU__RU_ sig-nificant relationship between STH QHJDWLYH_LQ_ infection and skin WKH_FDVH_RI_D_UHG_ZKHDO____PP_LQ_GLDPHWHU_ each group. respectively. 54.

1 We found that -sity was significantly associated with negative SPT 3 ________ EXW_ PLOG_ DQG_ PRGHUDWH_ LQIHFWLRQV_ ZHUH_ the prevalences of A.lumbricoides + T.trichiura 526_RQUKVKX 526_PGICVKX G P__ G P___ __ __ ___ _____ _ ____ 0 ___ _____ A.trichiura +PVGPUKV[_QH_KPHGEVK QP _____/KNF _____/QFGTCVG _____5GXGTG _ 526__UMKP_RTKEM_VGUV 2_XCNWG __ __ 0 0 ____ ___ ___ ___ _____ _____ . trichiura. and not (Table 3).Schenny Regina Lubis et al: Soil-transmitted helminth infection and skin prick test 3 ________T. T._#UUQEKCVKQP_DGVYGGP_56*_KPHGEVKQP_CPF_UMKP_RTKEM_VGUV_TGUWNV 8CTKCDNGU 56*_KPHGEVKQP_ITQ 0QP_56*_KPHGEVKQP_ITQ WR WR_ 526_RQUKVKXG__ P___ P_ 526_PGICVKXG_ ____ P___ ___ 2_XCNWG _____ ___ ___ _P_ 526__UMKP_RTKEM_V GUV_ Table 3.lumbricoid es T._4GNCVKQPUJKR_QH_526_VQ_V[RG_CPF_UGXGTKV[_QH_KPHGEVKQP 8CTKCDNGU 6[RG_QH_KPHGEVKQ P A. trichiura_3 ______DQG_PL[HG_LQIHFWLRQ_ be approximately 1.__ A Nottingham 3 _____VWXG\_UHSRUWHG_WKDW_PRUH_WKDQ___ELOOLRQ_S ________ )XUWKHUPRUH__ VHYHUH_ LQIHFWLRQ_ LQWHQ HRSOH_ are chronically infected with STH. PL[HG_ LQIHFWLRQV_ ZHUH_ _______ _______ DQG_ _______ Table 1.5 billion people. lumbricoides._%JCTCEVGTKUVKEU_QH_UWDLGEVU %JCTCEVGTKUVKEU 56*_KPHGEVKQP_ITQ 0QP_56*_KPHGEVKQP_ITQ WR P___ WR P___ ) GPFGT__ P_ / ____ CNGU (GOCNG ____ _ _ ____ ____ U _ _ /GCP_CIG_ _______ _______ 5&__[GCTU / ____ _______ ____ _______ GCP_YGKIJV_ ____ 5&__MI /GCP_JGKIJV_ ____ ______ ____ ______ ____ _____ _____ _____ _____ 5&__EO *KUVQT[_QH_CVQR[__P 2QUKVKXG 0GICVKXG Table 2.

54. January 2014 UHVSHFWLYHO\__7KH_DYHUDJH_DJH_RI_RXU_VXEMHFWV_ZDV _______ \ HDUV__$______.Discussion Soil-transmitted helminth is a common afliction in the tropics causing serious public health problems in developing countries.14 while in Ecuador the peak prevalence and intensity of infection was 5 to 15 years of age. lumbricoides. the ascariasis global infection burden was estimated to 54_‡_Paediatr Indones. 1.HQ\DQ__VWXG\_DOVR_IRXQG_WKH_P HDQ_DJH_ of infected children to be about 11 years. 11 _ 7KH_ _____ GDWD_ IURP_ North Sumatera reported the percentages for A. trichiura and mixed infections to be ____________DQG________UHVSHFWLYHO\____In China.15 Epidemiological studies in London reported that children with allergies and severe worm infection at an early age have significantly reduced skin prick test reactivity. . No. T. Vol._ Furthermore. active worm infection.

ascariasis. T./____ DQG_ WUDQVIRUPLQJ_ JU RZWK_ factor-B (TGF-B).________ We also found a significant relationship between the helminth type and skin prick test results. The principal mechanism appears to be the increased production of anti-inflammatory F\WRNLQHV__ VXFK_ DV_ . exposure to the nematodes A. we found a significant relationship between STH infection and negative skin SULFN_WHVW_UHVXOWV_3 ________ Two mechanisms modulate allergic inflammatory reactions. lumbricoides. such as mebendazole DQG_ SUD]LTXDQWHO_ HYHU\_ __ PRQWKV_ IRU_ ___ PR QWKV__ in chronically infected children had been found to increase atopic reactivity./_____. lumbricoides was protective against allergy inflammation. there is a significant relationship between STH infections and negative skin prick test results in primary school children./____. lumbricoides and T. acute infection with invasive parasitic worm larvae occurs in the lungs. helminth parasites may suppress parasite-specific and aeroallergenspecific immune responses. In early infection._______ Secondly. during chronic infection.__ We found a significant relationship between severe infection and negative skin prick test .___ Similarly. Hyperendemic avoid afecting the the skin prick test results. A London study stated that a large immune response to A. provided protection against the effects of allergen skin prick test reactivity. trichiura induces the secretion of antiinflammatory cytokines which suppress allergies. A. and mixed worm infections appeared to suppress immune system regulation./_____OH DGLQJ_WR_ mucus production and smooth muscle cell contraction which promote airway allergies. These larvae antigens induce helper 7___7K___FHOOV_DQG_WKH_UHOHDVH_RI_PHGLDWRUV__V XFK_DV_ LQWHUOHXNLQ_.___ In conclusion. trichiura and mixed infections were associated with decreased incidence of allergies.Schenny Regina Lubis et al: Soil-transmitted helminth infection and skin prick test the most common chronic infection.19 The intensity of helminth infection also afects the immune response. Severe trichiuris. Firstly. The production of large amounts of anti-inflammatory cytokines may suppress immune responses to environmental allergens and directly downregulate allergic responses to inhibit the activation of allergies. the primary target of a parasite-specific immune response. Positive skin prick test results in children with STH infections are lower than in uninfected children. Epidemiological studies in the United States reported that the intensity of severe and multiple infections promotes stronger influence on immune system regulation. as diagnosed by the skin prick test. The administration of antihelmintics. larvae secrete large amounts of allergenic substances that are likely to be the primary stimulus for immunoglobulin-E (IgE) production in infected individuals.__ Another study found that R[DQWHO_S\UDQWHO_WKHUDS\_IRU____PRQWKV_RQ_D_U HJXODU_ basis increased total serum IgE levels significantly./____DQG_.

allergic J Rahmawati. Am J Resp Crit Costa between rhinitis severity.QGRQHVLD_____________ ___ prevalence of symptoms of asthma. Flohr C.Ascaris lumbricoides and severity of childhood References 1. et al. ___ 5RGULJXHV_/&__1HZFRPEH_3__&XQKD_66__$OFDQWDUD_1HYHV_ NM. Soto-Quiros ME. Morris A. anamnesis and allergy testing. Vol. Atopy. Do helminth parasites protect against atopy and allergic asthma 5. 54. Punagi AQ. and atopic eczema: ISAAC. Cruz rhinoconjunctivitis. Hunninghake GM. We excluded children who had used anthelPLQWLFV_ZLWKLQ_WKH___PRQWKV_SULRU_WR_HQUROOPH QW_WR_ ______________ 9. 0HG_- &RRSHU_ 3-__ %DUUHWR_ 0/__ 5RGULJXHV_ /&__ Human allergy and geohelminth infections: a review of the literature and proposed conceptual model to guide the 7KH_ . InnovAiT. Sylvia JS. _________________ allergen skin test reactivity in later childhood. Britton J. Worldwide variation in Rica. Clin in Makassar. and mite-specific immunoglobulin E in allergic ___ &RRSHU_-3__&KLFR_ 0(__ in a rural area of Ecuador. Savitri E. Sensitization to UHVXOWV_LQ_FKLOGUHQ_3 _______ patients ___ Care Med. Munasir Z.QWHUQDWLRQDO_ 6WXG\_ RI_ $VWKPD_ DQG_ $OO investigation HUJLHV_ LQ_ Childhood (ISAAC) Steering of SRVVLEOH_FDXVDO_DVVRFLDWLRQV__ %U_0HG_%XOO_________________ 8. Pemeriksaan penunjang klinis: uji kulit terhadap Paediatr Indones. Relationship rhinitis %ODQG_ 0__*ULIILQ_ *(__1XWPDQ_ 7%__ Allergic Committee.PPXQRO__________________ 8. _______________ symptoms. atopy. _______________ 4. 1. No. skin prick test reactivity disease? Clin Exp Allergy. et al. Early infection with Trichuris trichura and Lancet. January 2014_‡_55 . Genser B. Ly &OLQ_([S_$OOHUJ\__________________ NP. Quinnell RJ. AA. Allergy _. Liang C. Avila L. and geohelminth infections in .

et al.UXL]H_<&__6RXYHULMQ_-+__et al.__3HUH]_0__'L_3ULVFR_0&__/RSH ]_5__$OYDUH]_ N. Buku DMDU_DOHUJL_LPXQRORJL_DQDN___QG_HG__- rural area of WKH_WURSLFV__- DNDUWD__. Ruiz ____ 0RQWUHVRU_$__&URPSWRQ_':7__+DOO_$__ %XQG\_'$3__6DYLROL_ L. et al. ____ Pasaribu S. Am J Resp LPPXQH_K\SRUHVSRQVLYHQHVV__ _. et al. Atopy.PPXQRO___________________ ____ &RRSHU_3__&KLFR_0(__5RGULJXHV_/&__2UGRQH]_0__6WUDFKDQ_ D. children infected with geohelminth parasites in a editors. Firmansyah I. Ginting SA. Munasir Z. Pediatr . _________________ ____ /\ QFK_15__+DJHO_. Intensity of ____ 3DOPHU_/-__&HOHGRQ_-&__:HLVV_67__:DQJ_ %__)DQJ_=__. et al.QIHFW_ 'LV________________ ___ &ULW_&DUH_0HG___________________ 15. Ng’ang’a LW. evaluation of soil-transmitted helminthiasis and asthma. Prado RC. In: Akib AAP.QGRQHVLD________S________ ____ :RUGHPDQQ_ 0__ 'LD]_ 5__ +HUHGLD_ /0__ &ROODGR_ 0DGXUJD_ AM. %LJJHODDU_ $__ 5RGULJXHV_ /&__ YDQ_ 5HH_ 5__ YDQ_ GHU_ asthma.-__ Kamngo J. Kurniati N.__ Ascaris lumbricoides infection intestinal infection with multiple worm species is is associated with increased risk of childhood related to regulatory cytokine output and asthma and atopy in rural China. Reduced risk of atopy among school-age increases mite skin-test reactivity in Gabonese schoolchildren. Factors associated with the Perzanowski MS. Lubis CP. Carter MC. ____ 7XUQHU_ -'__ -DFNVRQ_ -$__ )DXONQHU_ +__ _______________ %HKQNH_ -__ (OVH_ . urban children in Kenya. J Infect Dis. ____ 14. J Pediatr. DQG_WKH_K\JLHQH_K\SRWKHVLV__6FLHQFH_________________ 19.QGRQHV_________________ Atopic phenotype is an important determinant of 'DOLPXQWKH_ :__ 6LUHJDU_ &__ /XELV_ 0__ 3DVDULEX_ 6_ immunoglobulin E-mediated inflammation and _ /XELV_ &3__ Treatment of intestinal expression of T helper cell helminthiasis: mebendazole only or mebendazole- W\SH___F\WRNLQHV_WR_DVFDULV_DQWLJHQV_LQ_FKLOGUHQ_H[SRV HG_WR_ DVFDULDVLV__-_. Vaughan JW. Grifin GE.X_ . Association of atopy.Schenny Regina Lubis et al: Soil-transmitted helminth infection and skin prick test alergen.PPXQRO____________________ $QDN_. Cooper PJ. Ngari P. Trop Med _ . _______________ Long-term treatment of intestinal helminths Cooper PJ.UHPVQHU_3*__YDQ_5HH_5__$OOHU transmission J\__SDUDVLWHV_ of among soil-transmitted helminthiasis schoolchildren. J Allergy Clin Immunol.QW_+HDOWK________________ 11. and antibodies to Ascaris among rural and =HH_-6__+RHNVPD_. Lubis M. ____ 9DQ_ GHQ_ Odhiambo J. dermatitis and intestinal helminth infections in *HQHYD__:RUOG_+HDOWK_2UJDQL]DWLRQ________S______ Cuban children. atopic schistosomiasis of community level. In: Guidelines for the Espinosa A.QIHFW_'LV___________________ pyrantel pamoate? Paediatr Indones. _______________ . Lubis IZ. allergic rhinoconjunctivitis. <D]GDQEDNKVK_0__.NDWDQ_'RNWHU_ _$OOHUJ\_&OLQ_. Chico ME. Sandoval C. Nutman TB. Can intestinal helminth infections (geohelminths) expression affect of the asthma development and and allergic GLVHDVH"_&OLQ_([S_. Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum.

1. No. January 2014 . 54.56_‡_Paediatr Indones. Vol.