‚ese—r™h

ipidemiology of hum—n f—s™ioli—sisX — review

—nd proposed new ™l—ssifi™—tion

I P P

wF ƒF w—sEgom—D tFqF iste˜—nD 8 wFhF f—rgues

„he epidemiologi™—l pi™ture of hum—n f—s™ioli—sis h—s ™h—nged in re™ent ye—rsF „he num˜er of reports of hum—ns

p—s™iol— hep—ti™— h—s in™re—sed signifi™—ntly sin™e IWVH —nd sever—l geogr—phi™—l —re—s h—ve ˜een infe™ted with

des™ri˜ed —s endemi™ for the dise—se in hum—nsD with prev—len™e —nd intensity r—nging from low to very highF righ

prev—len™e of f—s™ioli—sis in hum—ns does not ne™ess—rily o™™ur in —re—s where f—s™ioli—sis is — m—jor veterin—ry pro˜lemF

rum—n f—s™ioli—sis ™—n no longer ˜e ™onsidered merely —s — se™ond—ry zoonoti™ dise—se ˜ut must ˜e ™onsidered to ˜e

—n import—nt hum—n p—r—siti™ dise—seF e™™ordinglyD we present in this —rti™le — proposed new ™l—ssifi™—tion for the

epidemiology of hum—n f—s™ioli—sisF „he following situ—tions —re distinguishedX imported ™—sesY —uto™hthonousD

isol—tedD non™onst—nt ™—sesY hypoED mesoED hyperED —nd holoendemi™sY epidemi™s in —re—s where f—s™ioli—sis is endemi™

in —nim—ls ˜ut not hum—nsY —nd epidemi™s in hum—n endemi™ —re—sF

†oir p—ge QRR le reÂsume en fr—n™Ë—isF in l— p— gin— QRR figur— un resumen en esp—nÄ olF

± sever—l —rti™les report th—t the in™iden™e is sntrodu™tion

signifi™—ntly —ggreg—ted within f—mily groups

p—s™ioli—sisD —n infe™tion ™—used ˜y the liver fluke ˜e™—use the individu—l mem˜ers h—ve sh—red the

s—me ™ont—min—ted foodY p—s™iol— hep—ti™—D h—s tr—dition—lly ˜een ™onsidered to

˜e —n import—nt veterin—ry dise—se ˜e™—use of the ± sever—l —rti™les h—ve reported out˜re—ks not

ne™ess—rily involving only f—mily mem˜ersY —nd su˜st—nti—l produ™tion —nd e™onomi™ losses it ™—uses

in livesto™kD p—rti™ul—rly sheep —nd ™—ttleF sn ™ontr—stD ± — few —rti™les h—ve reported epidemiologi™—l

surveys of — l—rge num˜er of infe™ted personsF hum—n f—s™ioli—sis h—s —lw—ys ˜een viewed —s —

se™ond—ry dise—se @ID PAF

„he pu˜li™ he—lth import—n™e of hum—n

‚e™ent developments

f—s™ioli—sis h—sD howeverD in™re—sed in re™ent ye—rsD

—s shown ˜y the high num˜er of hum—n ™—ses „he tr—dition—l epidemiologi™—l pi™ture of hum—n

f—s™ioli—sis h—s ™h—nged m—rkedly in re™ent ye—rsD —s re™orded over the period IWUH±WHX PSWR infe™ted

outlined ˜elowF persons in RP ™ountries lo™—ted on —ll ™ontinents @QAF

€reviouslyD ™—ses of hum—n f—s™ioli—sis h—d —lw—ys

qeogr—phi™—l distri˜ution ˜een linked to ™—ses —mong livesto™k in the —re—

™on™ernedF „he num˜ers of reported ™lini™—l ™—ses of hum—n

f—s™ioli—sis ™—used ˜y pF hep—ti™— —s well —s of infe™ted

persons identified during epidemiologi™—l surveys

h—ve in™re—sed signifi™—ntly sin™e IWVHF e re™ent „ypes of hum—n f—s™ioli—sis

review ˜y iste˜—n et —lF @RA ™ompiled — tot—l of UHUI

hum—n ™—ses reported from SI ™ountries over the l—st €u˜lished m—teri—l on hum—n f—s™ioli—sis f—lls into the

PS ye—rsD distri˜uted —s followsX efri™— @RVU ™—sesAD following ˜ro—d ™—tegories @QD RAX

emeri™— @QPTUAD esi— @QSRAD iurope @PWSIAD —nd

± the m—jority of —rti™les de—l only with individu—l

y™e—ni— @IPAF „he m—jor —sso™i—ted he—lth pro˜lems

™—se reportsY

—re found in ende—n ™ountries of ƒouth emeri™—D

northern efri™—D ssl—mi™ ‚epu˜li™ of sr—nD —nd

western iuropeF „he true num˜er of hum—n ™—ses

is undou˜tedly mu™h gre—ter th—n th—t reported @RAF

„he epidemiologi™—l —nd tr—nsmission ™h—r—™E

teristi™s of f—s™ioli—sis me—n th—t the dise—se h—s —

I

gh—irm—n —nd hire™torD hep—rtment of €—r—sitologyD p—™ulty of p—t™hy distri˜utionD with fo™i ˜eing rel—ted to the lo™—l

€h—rm—™yD niversity of †—len™i—D evF †i™ent endreÂs istelleÂs sGnD

distri˜ution of intermedi—te sn—il host popul—tions in

RTIHH furj—ssot±†—len™i—D ƒp—inF ‚equests for reprints should

freshw—ter ˜odies —s well —s to gener—l physiogr—phi™

˜e sent to €rofessor hr ƒF w—sEgom— —t this —ddressF

P —nd ™lim—ti™ ™onditionsF st is therefore not —ppropri—te

„itul—r €rofessorsD hep—rtment of €—r—sitologyD p—™ulty of €h—rm—™yD

to refer to the ™h—r—™teristi™s of f—s™ioli—sis —t the niversity of †—len™i—D evF †i™ent endreÂs istelleÂs sGnD RTIHH furj—ssot±

†—len™i—D ƒp—inF ™ountry levelD ˜ut r—ther to those in — given

‚eprint xoF SUVU physiogr—phi™—lly —nd ™lim—ti™—lly homogeneous —re—F

5 QRH ‡orld re—lth yrg—niz—tion IWWW fulletin of the ‡orld re—lth yrg—niz—tionD IWWWD UU @RA

ipidemiology of hum—n f—s™ioli—sis

highest levels thus f—r reported @PRD PSAF sn €ortoD rum—n endemi™ —re—s

€ortug—lD — prospe™tive study provided — geometri™ ƒurveys in sever—l regions indi™—te th—t there —re —re—s

me—n level in stools of PQQ epg @r—ngeD PS±PIHH epgAD with true endemi™ hum—n f—s™ioli—sisD r—nging from

—lthough most of the su˜je™ts shed IHI±QHH epg @IUAF low to very high prev—len™e —nd intensity @SAF ‚e™ent

elthough in gener—l the prev—len™e —nd estim—tes suggest th—t up to PFR million @TA or even up

intensity of egg outputs —re higher in ™hildren to IU million people @UA —re infe™ted with pF hep—ti™—

@US7D PR±RRRH epgA th—n —dults @RIFU7D IRR±VTR in the worldF ‡ry @VA h—s stressed the l—rge he—lth

epgAD in hyperendemi™ zones —dults either m—int—in pro˜lem ™—used ˜y f—s™ioli—sis in sever—l ™ountriesD

the p—r—sites they —™quired when young or ™—n ˜e —nd rillyer 8 ept @WA h—ve underlined the situ—tion in

newly infe™ted ˜e™—use they live in — zone of high the emeri™—sF „hese d—t— t—ke on gre—t import—n™e

infe™tion risk @PSAF ˜e™—use of the re™ognized pronoun™ed p—thogeni™ity

of f—s™ioli—sis in hum—ns @QD SD IHAF

qlo˜—l —n—lysis of the geogr—phi™—l distri˜ution „he p—r—site

of hum—n ™—ses shows th—t the expe™ted ™orrel—tion wost of the —re—s with — high endemi™ity of hum—n

˜etween —nim—l —nd hum—n f—s™ioli—sis o™™urs only —t f—s™ioli—sis involve pF hep—ti™—F roweverD in esi— the

— ˜—si™ levelF e high prev—len™e in hum—ns does not

distri˜ution of pF hep—ti™— —nd pF gig—nti™— overl—psD —nd

seem to ™orrel—te with —re—s where f—s™ioli—sis is —

this m—kes it diffi™ult to identify the p—rti™ul—r spe™ies

m—jor veterin—ry pro˜lem @RAF „husD ™l—ssifi™—tion of

involvedD whi™h is often referred to simply —s p—s™iol—

f—s™ioli—sis —s one of the prin™ip—l tropi™—l dise—ses

spF „his espe™i—lly o™™urs in ghin— @€rovin™e of

—ppe—rs w—rr—nted @IIAF

„—iw—nAD t—p—nD the ‚epu˜li™ of uore—D —nd the

€hilippines @QPAF

€rev—len™e of hum—n f—s™ioli—sis e simil—r pro˜lem o™™urs in igyptD where

‡here—s the prev—len™e of hum—n f—s™ioli—sis ™—n ˜e f—s™ioli—sis h—s —ppe—red —s —n emerging he—lth

negligi˜le in —re—s where the veterin—ry form of the pro˜lem @QQA with some rur—l —re—s ˜eing endemi™

dise—se o™™ursD the r—tes v—ry widely in —re—s where —nd h—ving prev—len™es in the r—nge U±IU7 @QRAF e

the dise—se in endemi™ to hum—nsF tot—l of PUFU million people —re —t riskD with the

ix—mples of very low prev—len™es —re HFQR±QFI num˜er infe™ted ˜eing —t le—st VQH HHH @VAF foth

™—ses per IHH HHH inh—˜it—nts in f—sseExorm—ndieD pF hep—ti™— —nd pF gig—nti™— —s well —s intermedi—te

pr—n™e @IPD IQAY HFVQ±IFIT ™—ses per IHH HHH forms h—ve ˜een foundD thus expl—ining why the fluke

inh—˜it—nts in gorsi™— @IRD ISAY —nd HFU7 prev—len™e spe™ies involved h—s not ˜een determined in most

@RI ™—ses per SVTI su˜je™ts studiedA in the †ss ‚egion inst—n™es @RAF

of ghile @ITAF sntermedi—te levels —re exemplified ˜y foth the —˜norm—l sperm—togeneti™ type

prev—len™es of QFP7 in the inner €orto regionD @eƒ„D in™luding diploidD triploidD —nd mixoploid

€ortug—l @IUAY UFQ7 in the xile delt—D igypt @IVAY ™hromosome types in whi™h no fertiliz—tion o™™ursA

VFU7 in g—j—m—r™—D €eru @IWAY —nd IHFW7 in goroz—lD —nd the norm—l sperm—togeneti™ type @xƒ„A of

€uerto ‚i™o @PHAF ix—mples of high prev—len™es —re p—s™iol— sppF h—ve ˜een found in sever—l esi—n

provided ˜y ISFTR7 in the €uno region @PIA —nd ™ountriesX ghin— @€rovin™e of „—iw—nAD sndi—D xep—lD

QRFP7 in the w—nt—ro v—lley @PPAD ˜oth in €eruF „he the €hilippinesD „h—il—ndD —nd †iet x—mF eƒ„ o™™urs

highest hum—n prev—len™es h—ve ˜een reported in the p—rti™ul—rly in t—p—n —nd the ‚epu˜li™ of uore—F

folivi—n eltipl—noX up to TTFU7 dete™ted using sn southEe—st esi—D eƒ„ flukes —re symp—tri™ with

™oprologi™—l te™hniques @PQ±PTA —nd up to SQ7 xƒ„ pF hep—ti™— —nd xƒ„ pF gig—nti™—F sn iuropeD

using immunologi™—l methods @PQD PU±PWAY higher ƒouth —nd xorth emeri™—D —nd y™e—ni—D where

r—tes of UP7 —nd IHH7D respe™tivelyD h—ve ˜een m—inly pF hep—ti™— o™™ursD —nd in efri™—D where

reported ˜y lo™—l folivi—n workers @QHAF pF gig—nti™— predomin—tesD only xƒ„ spe™imens h—ve

„he rel—tionship ˜etween the prev—len™e of ˜een found @QSAF

f—s™ioli—sis —nd —ge differs in hum—n endemi™ —nd t—p—nese flukes reprodu™e ˜y p—rthenogenesis

hum—n nonendemi™ —re—sF sn high prev—len™e —re—s ˜e™—use of their —˜norm—l g—metogenesisD reg—rdless

™hildren under IS ye—rs of —ge usu—lly present the of whether th—y —re diploidD triploidD or mixoploid

highest r—tes @ITD IVD IWD PID PRD PSAD in ™ontr—st to the @QTAF ƒtudies h—ve distinguished v—rious p—rthenogeE

™urrent situ—tion in hum—n nonendemi™ —re—sF neti™ lines th—t h—ve —risen independently of e—™h

otherD presum—˜ly through independent hy˜ridiz—E

tion ˜etween str—insF „he existen™e of su™h hy˜rids rum—n infe™tion intensities

would expl—in the ™ontinuing t—xonomi™ ™onfusion emong hum—n ™—ses low egg outputsD eFgF I±P eggs

reg—rding the t—xonomi™ st—tus of the t—p—nese liver per g of f—e™es @epgA @PHA —nd I±R epg @IWAD were until

flukes @QTAF inzym—ti™ studies h—ve ˜een un—˜le to re™ently the most ™ommonD with —n output of RRH

settle this issueD perh—ps ˜e™—use the worms epg @QIA ˜eing ™onsidered r—reF „hese egg outputs

reprodu™e p—rthenogeneti™—llyD with the popul—tions —reD howeverD very mu™h lower th—n those found in

ex—mined ™onsisting of des™end—nts of — single hum—n endemi™ —re—sF por ex—mpleD —mong folivi—n

individu—l @QUD QVAF ™hildrenD eggs in stools r—nged from PR to SHTR epgD

wole™ul—r te™hniques h—veD howeverD provided with —rithmeti™ —nd geometri™ me—n levels of

RUR±IHHI epg —nd PHI±QHW epgD respe™tivelyD the —n —nswer to this ™ontroversyF ‚i˜osom—l hxe

fulletin of the ‡orld re—lth yrg—niz—tionD IWWWD UU @RA QRI

‚ese—r™h

supr—spe™ifi™ lymn—eid phylogeny @RU±SHAF „he @rhxeA sequen™e studies h—ve shown th—t pF hep—ti™—

—nd pF gig—nti™— —re distin™tD with t—p—nese p—s™iol— spF import—n™e of these te™hniques is evident in view

h—ving —n rhxe sequen™e ™lose to th—t of pF gig—nti™— of the spe™ifi™ determin—tion pro˜lems in vymn—eiE

@QVD QWAF †ery re™entlyD r—shimoto et —lF @RHA h—ve d—e sn—ilsF woreoverD espe™i—lly the iIHEI helix of the

found th—t intermedi—te forms from t—p—n m—y ˜e †P v—ri—˜le region of the IVƒ ri˜osom—l ‚xe

—s™ri˜ed to pF gig—nti™—D ˜—sed on their mito™hondri—l @r‚xeA gene h—s proved useful in distinguishing

—nd nu™le—r hxe sequen™iesF por the time ˜eingD ˜etween lymn—eid spe™ies whi™h tr—nsmit —nd whi™h

howeverD the situ—tion is not ™le—r for other esi—n do not tr—nsmit f—s™iolid p—r—sitesD —s well —s in

™ountriesF distinguishing ˜etween those spe™ies th—t tr—nsmit

pF hep—ti™— —nd those th—t tr—nsmit pF gig—nti™— @RUD

RVD SIAF homesti™ —nim—l reservoir hosts

hxe sequen™e —nd isoenzyme studies showed sn the folivi—n eltipl—noD prev—len™e —nd intensity

not only th—t the iurope—n spe™ies vymn—e— trun™—tul— surveys show th—tD ˜esides sheep —nd ™—ttleD pigs —nd

donkeys —re effi™ient reservoirs of the p—r—siteX pigs o™™urs —lso in ƒouth emeri™— ˜ut th—t it is the only

@PUFI7 infe™tedD R±TS epg @me—nD PIFT epgAD sn—il spe™ies involved in tr—nsmission of f—s™ioli—sis in

estim—ted num˜er of eggs shed per host —nd per the folivi—n eltipl—no @RUD RVD SPAF

d—yD PHHH±IWS HHHAY donkeys @ISFR7 infe™tedD Q±IHI ƒever—l hxe pro˜es ™—p—˜le of dete™ting

epg @me—nD QVFV epgAD estim—ted num˜er of eggs shed pF hep—ti™— in lymn—eids h—ve ˜een developed @RUD

per host —nd per d—yD WHHH±VHV HHHA @RIAF RVD SQ±STAF yne su™h —ss—y dete™ts infe™ted sn—ils

‚e™ent studies h—veD moreoverD demonstr—ted immedi—tely —fter mir—™idi—l exposure —nd throughE

th—t eggs shed ˜y pigs —nd donkeys —re vi—˜leD iFeF —˜le out the p—r—site9s development period @SSAD ˜ut

to infe™t — lymn—eid sn—ilD —nd th—t the met—™er™—ri—e possi˜le ™rossEre—™tions with other digene—ns using

su˜sequently produ™ed —re infe™tive for —nother the s—me sn—il spe™ies h—ve not yet ˜een ev—lu—tedF

definitive host @f—rgues et —lFD unpu˜lished d—t—D u—pl—n et —lF reported the development of — highly

IWWWAF „his is the first o™™—sion th—t the need to t—ke sensitive —nd spe™ifi™ pro˜e for r—dioisotopi™ dete™E

pigs —nd donkeys into —™™ount in preventive —nd tion of pF hep—ti™—Einfe™ted sn—ilsD together with —n

™ontrol me—sures —g—inst hum—n f—s™ioli—sis h—s ˜een

effi™ient hxe extr—™tion proto™ol suit—˜le for l—rgeE

pointed out @RIAF

s™—le testing of fieldE™olle™ted sn—ils @STAF e modE

ifi™—tion th—t employs ™hemilumines™en™e —nd h—s —n

‡ild —nim—l reservoir hosts improved —ss—y effi™ien™y @sensitivityD IHH7Y spe™iE

sn gorsi™—D where the level of endemi™ity of hum—n fi™ityD bWW7A dete™ts infe™ted sn—ils immedi—tely

f—s™ioli—sis is lowD h—˜it—ts h—ve ˜een identified where following mir—™idi—l penetr—tion —nd does not ™rossE

lymn—eids —re infe™ted ˜ut whi™h h—ve no livesto™k hy˜ridize with hxe of other digene—n spe™ies th—t

presentF relminthologi™—l surveys showed th—t ˜l—™k sh—re the s—me sn—il hosts —nd overl—p their enzooti™

r—ts @‚—ttus r—ttusA were repe—tedly infe™ted ˜y liver r—nges with pF hep—ti™— @SUAF

flukes @RPD RQAF „he first ™—se of tr—nsmission of — p—s™iol—

edult st—ge morpho—n—tomi™—l @RRA —nd isoE spe™ies ˜y — sn—il not ˜elonging to the vymn—eid—e

enzyme studies @QUA h—ve reve—led no signifi™—nt f—mily @fiomph—l—ri— —lex—ndrin—D €l—nor˜id—eA w—s

differen™e ˜etween the flukes of rodents —nd ™—ttleF

re™ently reported in igypt @SVAF „he import—n™e of

p—s™ioli—sis in ‚F r—ttus w—s found in different en™l—ves

this dis™overy for the tr—nsmission of f—s™ioli—sis

throughout gorsi™—F e TEye—r study in — given

rem—insD howeverD to ˜e ev—lu—tedF

gorsi™—n endemiotope found — high me—n prev—len™e

@RSFIQ7A of pF hep—ti™— infe™tion in ‚F r—ttusD with —n

„r—nsmission

pF hep—ti™— —dult ˜urden per r—t of QFHR @r—ngeD I±IPAF

‚e™ent studies h—ve demonstr—ted th—t hum—ns pl—y —

woreoverD the p—thology indu™ed ˜y the flukesD

signifi™—nt role in the tr—nsmission of liver flukesD —t

lo™—ted in the m—in ˜ili—ry du™tD did not redu™e the r—t

le—st in hum—n hyperendemi™ zones su™h —s the

life sp—nD n—tur—lly infe™ted r—ts housed in the

folivi—n eltipl—noF ell the ne™ess—ry ™h—r—™teristi™s l—˜or—tory h—ving survived up to PP months @†—lero

™onverge @PRD PSD SWAX hum—n prev—len™es —re et —lFD unpu˜lished d—t—D IWWWAF

suffi™ient —nd m—int—ined over timeY egg outputs in ixperiment—l studies h—ve demonstr—ted the

hum—ns —re suffi™iently highY —nd p—r—site eggs shed vi—˜ility of pF hep—ti™— isol—tes from ˜l—™k r—tsD ˜oth for

with hum—n stools h—ve proved to ˜e vi—˜leF por the development of the intr—mollus™—n l—rv—l st—ge @w—sE

first timeD it h—s therefore ˜een shown th—t hum—ns gom— et —lFD unpu˜lished d—t—D IWWWA —nd su˜sequent

p—rti™ip—te in the tr—nsmission of the dise—se in those infe™tion of ˜l—™k r—ts with met—™er™—ri—e @RSAF st w—s

pl—™es where outdoor defe™—tion is pr—™tised @f—rE therefore ™on™luded th—t ‚F r—ttus ™—n pl—y —n

gues et —lFD unpu˜lished d—t—D IWWWAF import—nt role —s reservoir —nd p—rti™ip—te in the

geogr—phi™—l diffusion of the dise—se @RTAF

i™ology

pield —nd l—˜or—tory studies h—ve shown th—t sntermedi—te sn—il hosts

f—s™ioli—sis h—s — gre—t ™—p—™ity to spre—d th—t is xu™le—r —nd mito™hondri—l rhxe sequen™e —n—lysis

h—s proved useful for ˜oth spe™ifi™ determin—tion —nd rel—ted to the e™ologi™—l ni™heEwidening —˜ility of the

QRP fulletin of the ‡orld re—lth yrg—niz—tionD IWWWD UU @RA

ipidemiology of hum—n f—s™ioli—sis

no longer ˜e ™onsidered merely —s — se™ond—ry lymn—eid hosts —nd the ™onsider—˜le ™oloniz—tion —nd

zoonoti™ dise—se ˜ut must ˜e t—ken to ˜e —n —d—pt—tion ™—p—™ity of the p—r—siteF

import—nt hum—n p—r—siti™ dise—se @IIAF yn gorsi™—D numerous different types of

ell these d—t— indi™—te the need to review h—˜it—ts inh—˜ited ˜y the only tr—nsmitting sn—il

™urrent underst—nding on the epidemiology of spe™ies @THA m—y ˜e distinguished @TID TPAF ƒever—l

hum—n f—s™ioli—sis in —re—s where pF hep—ti™— is —typi™—l h—˜it—ts represent —n e™ologi™—l ni™he

presentF felow we present — proposed new epideE widening th—t is rel—ted to the extr—ordin—ry distri˜uE

miologi™—l ™l—ssifi™—tion for hum—n f—s™ioli—sisF tion of the dise—se on the isl—nd @TQD TRAF

F smported ™—sesX rum—n ™—ses di—gnosed in — zone „he presen™e of f—s™ioli—sis —t very high —ltitude

l—™king pF hep—ti™— @even —mong —nim—lsA ˜ut whi™h @QSHH±RPHH mA in different ende—n regions is —lso

were infe™ted in —n —re— where pF hep—ti™— worthy of mentionF „he highest prev—len™es —nd egg

tr—nsmission o™™urs @TVD TWAF outputs o™™ur in hum—ns pre™isely in these very high

F euto™hthonousD isol—tedD non™onst—nt ™—sesX rum—ns —ltitude zones of folivi— —nd €eru @PQ±PUD QHAF „his

who h—ve —™quired the infe™tion in the —re— where me—ns not only th—t sn—il —nd p—r—site were —˜le to

they live —nd where —nim—l f—s™ioli—sis is —lso ™olonize su™™essfully extreme ™onditions of very high

presentY these hum—n ™—ses —ppe—r spor—di™—llyD —ltitude ˜ut —lso th—t they h—ve ˜een —˜le to develop

without —ny ™onst—n™y @UHAF different —d—pt—tion str—tegies whi™h permit higher

F indemi™X „hree types of endemi™ situ—tions ™—n ˜e p—r—site tr—nsmission r—tes @TSAF

distinguished —™™ording to the prev—len™e in the

tot—l popul—tion o˜t—ined ˜y ™oprologi™—l di—gE

rum—n ™ont—min—tion

nosis @prev—len™e estim—ted from serologi™—l tests

‚e™ent studies h—ve shown th—t m—ny freshw—ter

m—y ˜e somewh—t higherAX

pl—nt spe™ies other th—n w—ter™ress m—y p—rti™ip—te in

± hypoendemi™X prev—len™e `I7Y —rithmeti™

hum—n infe™tionD depending on geogr—phi™—l zones

me—n intensity `SH epgY high epg levels only

—nd hum—n diet—ry h—˜its in the —re—s ™on™ernedX in

in spor—di™ ™—sesY hum—n p—rti™ip—tion in

pr—n™eD „—r—x—™um dens leonis @d—ndelion le—vesAD

tr—nsmission through egg shedding m—y ˜e

†—leri—nell— olitor— @l—m˜9s lettu™eAD —nd wenth— viridis

negle™tedY s—nit—tion ™h—r—™teristi™s usu—lly

@spe—rmintA @RAY in the ssl—mi™ ‚epu˜li™ of sr—nD other

in™lude l—trines —nd w—ste or sew—ge dispos—l

green le—fy x—sturtium sppF —nd wenth— sppF @VAY —nd in

f—™ilitiesY —nd outdoor defe™—tion is not

the folivi—n eltipl—noD tun™us —ndi™ol— @tun™—™e—eAD

™ommonly pr—™tised @IR±ITD UIAY

tun™us e˜r—™te—tus @tun™—™e—eAD wimulus gl—˜r—tus @ƒ™roE

± mesoendemi™XX prev—len™e I±IH7Y S±ISEye—rE

phul—ri—™e—eAD xosto™ spF @gi—nofit—sAD —mong others

olds m—y present higher prev—len™es @holoE

@PRD PUD QHAF

endemi™AY —rithmeti™ me—n intensity in hum—n

‡—ter h—s ˜een ™ited —s the sour™e of hum—n

™ommunities usu—lly SH±QHH epgY individu—l

infe™tionD whether dire™tly ˜y drinking or indire™tly

high epg levels m—y o™™urD —lthough intensities

˜y ™ont—min—ting veget—˜les or kit™hen utensils @QD SAF

bIHHH epg —re r—reY hum—n su˜je™ts m—y

snfe™tion ˜y ingestion of s—l—ds ™ont—min—ted with

p—rti™ip—te in tr—nsmission through egg shedE

met—™er™—ri—eE™—rrying w—ter used for irrig—tion h—s

dingY s—nit—tion ™h—r—™teristi™s m—y or m—y not

re™ently ˜een reported @IQAF sn folivi—D IQ7 of the in™lude l—trines —nd w—ste or sew—ge dispos—l

experiment—lly o˜t—ined met—™er™—ri—e —re —lw—ys f—™ilitiesY —nd outdoor defe™—tion m—y ˜e

flo—ting @TTAY this m—y ˜e rel—ted to m—ny of the pr—™tised @IUD IWAY

hum—n ™ont—min—tions in this zoneD where proper ± hyperendemi™X prev—len™e bIH7Y S±ISEye—rE

w—ste or sew—ge dispos—l f—™ilities —re l—™kingF „his is old ™hildren usu—lly present higher prev—len™es

™onsistent with underst—nding —˜out hum—n infe™E @holoendemi™AY —rithmeti™ me—n intensity in

tion in the emeri™—s in —re—s where people do not hum—n ™ommunities usu—lly bQHH epgY indiviE

h—ve — history of e—ting w—ter™ress @WAF du—l very high epg levels —re en™ounteredD with

‚e™ent experiment—l results suggest th—t huE intensities bIHHH epg ˜eing rel—tively frequentY

m—ns who ™onsume r—w dishes prep—red from fresh hum—n ™—ses ™ontri˜ute signifi™—ntly to tr—nsE

livers infe™ted with imm—ture flukes ™ould ˜e™ome mission through egg sheddingY s—nit—tion

infe™ted with f—s™ioli—sis @TUAF ™h—r—™teristi™s do not in™lude the use of

l—trinesY no proper w—ste or sew—ge dispos—l

f—™ilitiesY indis™rimin—te defe™—tion is ™omE

monly pr—™tised @PHD PP±PTAF €roposed new epidemiologi™—l

F ipidemi™X „here —re different types of out˜re—ks

™l—ssifi™—tion

—™™ording to the endemi™GnonEendemi™ situ—tion

st is evident th—t tod—y we h—ve — different of the zoneX

epidemiologi™—l ™on™eption of hum—n f—s™ioli—sisD ± epidemi™s in —re—s where f—s™ioli—sis is endemi™

with sever—l —re—s in the world ˜eing endemi™ for the in —nim—ls ˜ut not hum—nsX out˜re—ks —ppe—rE

dise—seD —nd th—t it h—s — ™onsider—˜le ™—p—™ity to ing in zones where previous hum—n reports

exp—nd geogr—phi™—lly due to the high —d—pt—˜ility of h—ve —lw—ys ˜een isol—ted —nd spor—di™Y su™h

the p—r—site —nd the su˜st—nti—l ™olonizing power of out˜re—ks usu—lly ™on™ern — very few indiviE

du—ls infe™ted from the s—me ™ont—min—tion the ve™tor lymn—eid spe™iesF rum—n f—s™ioli—sis ™—n

fulletin of the ‡orld re—lth yrg—niz—tionD IWWWD UU @RA QRQ

‚ese—r™h

sour™e @f—mily or sm—ll group reportsY ™onE e™knowledgements

t—min—ted wildD homeEgrownD or ™ommer™i—lly „his review is ˜—sed on the results of studies

grown w—ter™ress or other met—™er™—ri—eE ™ondu™ted m—inly in gorsi™— —nd folivi—F „he studies

™—rrying veget—˜lesA @ UP±URAY —nd in gorsi™— were supported ˜y ‡ry @€roje™t €h€

± epidemi™s in hum—n endemi™ —re—sX out˜re—ks xoF fPGIVIGIPSAD the ƒp—nish winistry of idu™—tion

in zones where the dise—se is endemi™ in

—nd ƒ™ien™e @€roje™t hqsg‰„ €fVUEHTPQAD pren™hE

hum—nsY — gre—ter num˜er of individu—ls m—y

ƒp—nish e™™iones sntegr—d—s TVGPRH @ere— RAD WIGVW

˜e involvedY usu—lly rel—ted to ™lim—ti™ ™ondiE

—nd rpEIPIGWHD —nd ˜y fin—n™i—l —id to the †—len™i—E

tions th—t h—ve f—voured ˜oth the p—r—site —nd

€—ris †s snterEuniversity egreementF „he studies in

the sn—ilsY —nd epidemi™s ™—n o™™ur in hypoE

folivi— were supported ˜y the ƒ„h €rogr—mme of the

endemi™ @US±UVAD mesoendemi™ @UWAD or hyE

gommission of the iurope—n gommunities @hq

perendemi™ @PUA —re—sF

ˆssX ƒ™ien™eD ‚ese—r™hD —nd hevelopment @gontr—™t

xoF „ƒQEg„WREHPWRAAD the €rogr—mme of ƒ™ientifi™

„his ™l—ssifi™—tion m—y ˜e — useful tool for

gooper—tion with v—tin emeri™— of the snstituto de glo˜—l —ssessment of the import—n™e of hum—n

gooper—™ioÂn s˜ero—meri™—n— of the egen™i— isp—E f—s™ioli—sisF ƒu™h — ™l—ssifi™—tion is —lso needed

nol— de gooper—™ioÂn sntern—™ion—l @sFgFsFEeFiFgFsFAD Ä ˜e™—useD with the re™ent registr—tion of tri™l—˜end—E

—nd ˜y the ƒp—nish winistry of idu™—tion —nd ƒ™ien™e zole for hum—n use —g—inst f—s™ioli—sis @VHAD new

@€roje™t hqsg‰„ xoF iWTEHHHIAF opportunities —re now —v—il—˜le for the ™ontrol of this

p—r—siteF n

‚e sumeÂ

ipide miologie de l— distom—tose he p—tique hum—ine X ˜il—n et projet de nouvelle

™l—ssifi™—tion

f—ut deÂsorm—is y voir une import—nte p—r—sitose ve t—˜le—u eÂpide miologique de l— distom—tose heÂp—tique

hum—ineF g9est pourquoi nous proposons d—ns notre hum—ine — ™h—nge ™es dernieÁ res —nne esF hepuis IWVHD

—rti™le une nouvelle ™l—ssifi™—tion e pideÂmiologique de on note une —ugment—tion sensi˜le des ™—s d9infest—tion

p—s™iol— hep—ti™— ™hez l9homme et plusieurs re gions ™ette m—l—dieF xous distinguons les situ—tions suiv—ntesX p—r

sont deÂsorm—is ™onsideÂre es ™omme de veÂrit—˜les zones ™—s importeÂsY ™—s —uto™htonesD isoleÂsD non ™onst—ntsY

d9endeÂmie hum—ineD —ve™ des nive—ux d9intensiteÂetde hypoED meÂsoED hyperE et holoendeÂmieY eÂpideÂmies

preÂv—len™e de l9infest—tion treÁs v—ri—˜lesF v— pre v—len™e surven—nt d—ns des zones ouÁ l— distom—tose est

de l— distom—tose hum—ine n9est p—s for™eÂment eÂleveÂel—Á endeÂmique ™hez l9—nim—l m—is non ™hez l9hommeY enfinD

ouÁ ™ette p—r—sitose pose un import—nt pro˜leÁme eÂpideÂmies surven—nt d—ns des zones d9endeÂmie

veÂteÂrin—ireF yn ne peut plus ™onsideÂrer l— distom—tose hum—ineF

heÂp—tique hum—ine ™omme une zoonose se™ond—ire X il

‚esumen

ipidemiologõ— de l— f—s™ioli—sis hum—n—X revisio n y propuest— de nuev— ™l—sifi™—™ioÂn

simplemente ™omo un— enfermed—d zoono ti™— se™unE v— situ—™io n epidemiolo gi™— de l— f—s™ioli—sis hum—n— h—

d—ri—D sino ™omo un— enfermed—d p—r—sit—ri— hum—n— ™—m˜i—do en los u ltimos —nÄ osF hesde IWVH el nu mero de

p—s™iol— import—nteF €or elloD en este —rtõ™ulo proponemos un— notifi™—™iones so˜re person—s infe™t—d—s por

h— —ument—do ™onsider—˜lementeD y en v—ri—s hep—ti™— nuev— ™l—sifi™—™io n epidemiolo gi™— de l— f—s™ioli—sis

zon—s geogr—Â fi™—s se h— senÄ —l—do l— existen™i— de hum—n—F ƒe distinguen l—s siguientes mod—lid—desX

verd—der—s endemi—s hum—n—sD ™on ™ifr—s de prev—len™i— ™—sos import—dosY ™—sos —uto ™tonosD —isl—dos y espoE

e intensid—d entre ˜—j—s y muy —lt—sF v—s zon—s de —lt— r—Â di™osY hipoendemi—sD mesoendemi—sD hiperendemi—s y

prev—len™i— de f—s™ioli—sis en el hom˜re no ™oin™iden holoendemi—sY epidemi—s en zon—s donde l— f—s™ioli—sis

ne™es—ri—mente ™on l—s zon—s donde l— enfermed—d es endeÂmi™— en los —nim—les pero no en los seres

™onstituye un pro˜lem— veterin—rio de primer— m—gnitudF hum—nosY y epidemi—s en zon—s donde es endeÂmi™— en

v— f—s™ioli—sis hum—n— y— no puede ™onsider—rse los seres hum—nosF

QRR fulletin of the ‡orld re—lth yrg—niz—tionD IWWWD UU @RA

ipidemiology of hum—n f—s™ioli—sis

‚eferen™es

IF w—lek ieF ƒn—ilEtr—nsmitted p—r—siti™ dise—ses †ols I —nd PF fo™— emeri™—n journ—l of hum—n f—s™ioli—sis in the folivi—n eltipl—noF

‚—tonD pvD g‚g €ressD IWVHX I±QQR —nd I±QPRF D IWWPD RTX THQ±THWF tropi™—l medi™ine —nd hygiene

PF for—y tgF p—s™ioli—sisF snX rillyer q†D ropl— giD edsF r—nd˜ook PRF iste˜—n tq et —lF €resen™e of very high prev—len™e —nd intensity

series in zoonoses D se™tion gF €—r—siti™ zoonosesD volF QF fo™— of infe™tion with p—s™iol— hep—ti™— —mong eym—r— ™hildren from

‚—tonD pvD g‚g €ressD IWVPX UI±VVF the xorthern folivi—n eltipl—noF e™t— tropi™—D IWWUD TTX I±IRF

QF ghen wqD wott uiF €rogress in —ssessment of mor˜idity due to PSF iste˜—n tq et —lF e popul—tionE˜—sed ™oprologi™—l study of

p—s™iol— hep—ti™— infe™tionX — review of re™ent liter—tureF „ropi™—l hum—n f—s™ioli—sis in — hyperendemi™ —re— of the folivi—n

D IWWHD VUX ‚I±‚QVF dise—ses ˜ulletin „ropi™—l medi™ine —nd intern—tion—l he—lthD IWWUD eltipl—noF

RF iste˜—n tqD f—rgues whD w—sEgom— ƒF qeogr—phi™—l PX TWS±TWWF

distri˜utionD di—gnosis —nd tre—tment of hum—n f—s™ioli—sisX — PTF engle s ‚ et —lF rum—n f—s™ioli—sis in folivi—X ™oprologi™—l surveys

reviewF ‚ese—r™h —nd reviews in p—r—sitologyD IWWVD SVX IQ±RVF in different provin™es of the hep—rtment of v— €—zF ‚ese—r™h —nd

SF w—sEgom— ƒD f—rgues whD iste˜—n tqF rum—n f—s™iolosisF D IWWUD SUX QQ±QUF reviews in p—r—sitology

snX h—lton t€D edF p—s™iolosisF ƒtF el˜—nsD rertsD ingl—ndD PUF fjorl—nd t et —lF en out˜re—k of —™ute f—s™ioli—sis —mong eym—r—

gommonwe—lth egri™ultur—l fure—ux @in pressAF indi—ns in the folivi—n eltipl—noF glini™—l infe™tious dise—sesD

TF ‚im rt et —lF poodE˜orne trem—todesX ignored or emergingc IWWSD PIX IPPV±IPQQF

€—r—sitology tod—yD IWWRD IHX PHU±PHWF PVF ƒtr—uss ‡ et —lF rum—n f—s™ioli—sis in folivi—X serologi™—l surveys

UF ropkins h‚F roming in on helminthsF emeri™—n journ—l of in vos endes provin™e of the hep—rtment of v— €—zF ‚ese—r™h —nd

tropi™—l medi™ine —nd hygiene D IWWPD RTX TPT±TQRF reviews in p—r—sitology D IWWUD SU@PAXIHW±IIQF

gontrol of food˜orne trem—tode infe™tionsF ‚eport of — ‡ry VF

PWF y9xeill ƒ et —lF smmunodi—gnosis of p—s™iol— hep—ti™— infe™tion

ixpert gommittee F qenev—D ‡orld re—lth yrg—niz—tionD IWWS

@f—s™iolosisA in — hum—n popul—tion in the folivi—n eltipl—no using

@‡ry „e™hni™—l ‚eport ƒeriesD xoF VRWAF

purified ™—thepsin v ™ysteine protein—seF emeri™—n journ—l of

WF rillyer q†D ept ‡F poodE˜orne trem—tode infe™tions in the

IWWVD SVX RIU±RPQF tropi™—l medi™ine —nd hygieneD

emeri™—sF €—r—sitology tod—yD IWWUD IQX VU±VVF

QHF w—sEgom— ƒ et —lF rum—n f—s™ioli—sis in folivi—X — gener—l

IHF w—sEgom— ƒ et —lF rep—ti™ trem—todi—sesF snX weyers ‡wD edF

—n—lysis —nd — ™riti™—l review of existing d—t—F ‚ese—r™h —nd

etl—s of infe™tious dise—sesF ‡—shingtonD hgD FƒF ermed por™es

D IWWSD SSX UQ±WQF reviews in p—r—sitology

snstitute of €—thology @in pressAF

QIF ek—h—ne r et —lF ‘hi—gnosis of f—s™ioli—sisF sF gomp—rison of the

IIF w—sEgom— ƒ et —lF ‘ p—s™ioli—sisD — new —ddition to the list of

effi™—™ies of v—rious ™on™entr—tion te™hni™s of ov— in stool“F

tropi™—l dise—ses “F €—per presented —tX s gongreso de l— ƒo™ied—d

t—p—nese journ—l of p—r—sitologyD IWUSD PRX SS±TH @in t—p—neseA

isp—nÄ ol— de wedi™in— „ropi™—l y ƒ—lud sntern—™ion—lD ghin™hoÂnD

QPF w—sEgom— ƒD f—rgues whF rum—n liver flukesX — reviewF

ƒp—inD PP±PR t—nu—ry IWWV @in ƒp—nishAF

‚ese—r™h —nd reviews in p—r—sitologyD IWWUD SUXIRR±PPSF

IPF foure e €D „hie˜—ult wF ‘p—s™ioli—sis ™—used ˜y p—s™iol—

QQF ilEuho˜y „F p—s™ioli—sisX —n emerging pro˜lem in igypt —nd the

hep—ti™— in vower xorm—ndy from IWVH to IWWH“F fulletin de l—

e˜str—™ts of the sntern—tion—l gonferen™e on snfe™tious regionF snX

D IWWQD IIX UW±VR @in pren™hAF ƒo™ieÂte pr—n™Ë—ise de €—r—sitologie

hise—ses —nd €u˜li™ re—lthD elex—ndri—D igyptD IU±PH y™to˜er

IQF g—del ƒ et —lF ‘iighteen ™—ses of hum—n f—s™ioli—sis in f—sseE

IWWU D ƒUQX RHF

xorm—ndieD IWWR±IWWS“F fulletin de l— ƒo™ieÂte pr—n™Ë—ise de

QRF p—r—g rF rum—n f—s™ioli—sisF „he igypti—n experien™eF snX

D IWWTD IRX QW±RQ @in pren™hAF €—r—sitologie

e˜str—™ts of the sntern—tion—l gonferen™e on snfe™tious hise—ses

IRF qilEfenito e et —lF ‘ƒtudy of distomi—sis ™—used ˜y p—s™iol—

ƒURX —nd €u˜li™ re—lthD elex—ndri—D igyptD IU±PH y™to˜er IWWUF

hep—ti™— in gorsi™—“F weÂditerr—neÂemeÂdi™—le @w—rseilleAD IWWID

RHF

RHQX PI±PS @in pren™hAF

QSF „er—s—ki uD ek—h—ne rD r—˜e ƒF „he geogr—phi™—l distri˜ution

ISF qilEfenito eF ‘ rum—n f—s™ioli—sis on the isl—nd of gorsi™—“F €hh

p—s™iol—A with norm—l —nd of ™ommon liver flukes @the genus

thesisD p—™ulty of wedi™ine —nd hentistryD niversity of †—len™i—D

t—p—nese journ—l of veterin—ry —˜norm—l sperm—togenesisF

†—len™i—D ƒp—inD IWWRX I±QPT @in ƒp—nishAF

s™ien™e D IWVPD RRX PPQ±PQIF

ITF ept ‡ et —lF ‘€rev—len™e of f—s™ioli—sis in hum—nsD horsesD pigs

QTF eg—tsum— „ et —lF qeneti™ v—ri—tion in the triploids of t—p—nese

—nd wild r—˜˜its in three provin™es of ghile“F foletõÂn de l— yfi™in—

p—s™iol— spe™iesD —nd rel—tionships with other spe™ies in the genusF

ƒ—nit—ri— €—n—meri™—n— D IWWQD IISX RHS±RIR @in ƒp—nishAF

tourn—l of helminthologyD IWWRD TVX IVI±IVTF

pF hep—ti™— infe™tion IUF ƒ—mp—io ƒilv— wvF ƒumm—ry of — report on

QUF €—s™u—l t et —lF ‘ile™trophoresis of n—tur—l popul—tions of

in northern €ortug—lF snX ghen wqD wott uiF €rogress in

p—s™iol— hep—ti™— p—r—sites of ‚—ttus r—ttus in gorsi™—“F †ie et

—ssessment of mor˜idity due to p—s™iol— hep—ti™— infe™tionX —

milieu D IWWHD RHX PTQ @in pren™hAF

review of re™ent liter—tureF „ropi™—l dise—ses ˜ulletinD IWWHD

€—r—gonimusF e™t— QVF fl—ir hF wole™ul—r v—ri—tion in f—s™iolids —nd

VUX ‚QVF

D IWWQD SQX PUU±PVWF tropi™—

IVF p—r—g rp et —lF e fo™us of hum—n f—s™ioli—sis in the xile helt—D

QWF edl—rd ‚h et —lF gomp—rison of the se™ond intern—l tr—ns™ri˜ed igyptF tourn—l of tropi™—l medi™ine —nd hygieneD IWUWD

sp—™er @ri˜osom—l hxeA from popul—tions —nd spe™ies of VPX IVV±IWHF

sntern—tion—l journ—l for p—r—sitologyD p—s™iolid—e @higene—AF IWF uno˜lo™h t et —lF rum—n f—s™ioli—sis in g—j—m—r™—G€eruF sF

IWWQD PQX RPQ±RPSF hi—gnosti™ methods —nd tre—tment with pr—ziqu—ntelF „ropi™—l

RHF r—shimoto u et —lF wito™hondri—l hxe —nd nu™le—r hxe medi™ine —nd p—r—sitology D IWVSD QTX VV±WHF

p—s™iol— spe™ies is pF gig—nti™—F indi™—te th—t the t—p—nese PHF fendezu €D pr—me eD rillyer q†F rum—n f—s™ioli—sis in goroz—lD

€—r—sitology rese—r™hD IWWUD VQX PPH±PPSF €uerto ‚i™oF tourn—l of p—r—sitologyD IWVPD TVX PWU±PWWF

RIF w—sEgom— ƒ et —lF ƒe™ond—ry reservoir role of domesti™ —nim—ls PIF ƒ—Â n™hez gD ep—ri™io ‡D rurt—do gF ‘histomi—sis of the liver in

other th—n sheep —nd ™—ttle in f—s™ioli—sis tr—nsmission in the the hum—n popul—tion of the esiloEez—ng—roE€uno river system“F

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