fr om 1 9 9 5 to 1 9 9 9
Estudo longitudinal clínico-sorológico da angiostrongilíase
abdominal em Guaporé, sul do Brasil, de 1 9 9 5 a 1 9 9 9
Carlos Graeff-Teixeira
1, Aline Hamilton Goulart
1, Charles de Ornellas Brum
1, Antonio Carlo Laitano
1,
Charlotte Sievers-Tostes
1, Graziela Maria Zanini
1, Patrícia Leão Bered
1, Alessandra Morassutti
1,
Stefan Geiger
3, Elizabeth Abrahms-Sandi
3, Fernanda Teixeira dos Santos Oliveira
1, Rafael Lucyk Maurer
1,
Luís Felipe Aguiar
1, Cinara Tentardini Garrido
1, Ana Cristina Aramburu da Silva
1,
Rubens Rodriguez
2, Hartwig Schulz-Key
3and Aventino Alfredo Agostini
2ABSTRACT
Ab do m in a l a n gio stro n gylia sis is a zo o n o tic in fe c tio n c a u se d b y Angiostrongylus c ostaric ensis, a n e m a to de with a n in tra -va sc u la r lo c a tio n in the m e se n te ry. Ou r o b je c tive wa s to a ddre ss se ve ra l a spe c ts o f the n a tu ra l histo ry o f this pa ra sito sis, i n a lo ngitudina l c linic a l a nd se ro e pide m io lo gic a l study. A to ta l o f 179 individua ls living in a rura l a re a with a c tive tra nsm issio n in so u the rn Bra zil we re fo llo we d fo r five ye a rs ( 1995- 1999) re su ltin g in ye a rly pre va le n c e o f 28.2 %, 4.2%, 10%, 20.2% a n d 2.8% a n d in c ide n c e s o f 0%, 5.9%, 8 % a n d 1.5%, re spe c tive ly. Bo th m e n a n d wo m a n we re a ffe c te d with highe r fre q u e n c ie s a t a ge 30- 49 ye a rs. In 32 in dividu a ls se ru m sa m ple s we re c o lle c te d a t a ll tim e po in ts a n d IgG a n tib o dy re a c tivity de te c te d b y ELISA wa s va ria b le a n d u su a lly pe rsistin g n o t lo n ge r tha n o n e ye a r. So m e in dividu a l a n tib o dy pa tte rn s we re su gge stive o f re - in fe c tio n . The re wa s n o a sso c ia tio n with o c c u rre n c e o f a b do m in a l pa in o r o f o the r e n te ro pa ra site s a n d the re wa s n o in dividu a l with a c o n firm e d ( histo pa tho lo gic ) dia gn o sis. Mo llu sk s we re fo u n d with in fe c tive third- sta ge la rva e in so m e ho u se s with a n o ve ra ll pre va le n c e o f 16% a n d a lo w pa ra sitic b u rde n . In c o n c lu sio n , a b do m in a l a n gio stro n gylia sis in so u the rn Bra zil m a y b e a fre q u e n t in fe c tio n with lo w m o rb idity a n d a gra du a lly de c re a sin g se ro lo gic a l re a c tivity.
Ke y-words:Ab d o m i n a l a n gi o stro n gyli a si s. Angio str o ngylus c o star ic e nsis. Ab d o m i n a l p a i n . Eo si n o p h i li c ga stro e n te ri ti s. Zo o n o si s.
RESUMO
An gi o stro n gi lí a se a b d o m i n a l é u m a zo o n o se c a u sa d a p e lo Angio str o ngylus c o star ic e nsis, n e m a tó d e o q u e se lo c a li za n o i n te ri o r d e va so s m e se n té ri c o s. No sso o b je ti vo f o i d e a b o rd a r vá ri o s a sp e c to s d a h i stó ri a n a tu ra l d a p a ra si to se , n u m e stu d o lo n gi tu d i n a l c lí n i c o - so ro ló gi c o . Um to ta l d e 1 7 9 i n d i ví d u o s re si d e n te s e m á re a ru ra l n o su l d o Bra si l, c o m tra n sm i ssã o a ti va , f o ra m se gu i d o s p o r c i n c o a n o s. Ne ste p e rí o d o f o ra m re gi stra d a s p re va lê n c i a s d e 2 8 ,2 %, 4 ,2 %, 1 0 %, 2 0 ,2 % e 2 ,8 % e i n c i d ê n c i a s d e 0 %, 5 ,9 %, 8 % e 1 ,5 %. Ta n to o se x o m a sc u li n o q u a n to o f e m i n i n o f o ra m a f e ta d o s c o m m a i o re s f re q u ê n c i a s n a f a i x a e tá ri a d o s 3 0 a o s 4 9 a n o s. Em 3 2 i n d i ví d u o s, a m o stra s d e so ro f o ra m c o le ta d a s e m to d a s a s e ta p a s e a re a ti vi d a d e d e IgG d e te c ta d a p o r ELISA f o i va ri á ve l e ge ra lm e n te n ã o p e rsi sti n d o m a i s d o q u e u m a n o . Algu n s p a d rõ e s i n d i vi d u a i s f o ra m su ge sti vo s d e re - i n f e c ç ã o . Nã o h o u ve a sso c i a ç ã o c o m a o c o rrê n c i a n e m d e d o r a b d o m i n a l n e m c o m o u tra s e n te ro p a ra si to se s e n ã o h o u ve n e n h u m c a so c o m d i a gn ó sti c o c o n f i rm a d o ( h i sto p a to ló gi c o ) d a i n f e c ç ã o . Mo lu sc o s f o ra m e n c o n tra d o s p o rta n d o la rva s i n f e c ta n te s d e te rc e i ro e sta d i o , e m a lgu m a s m o ra d i a s, c o m u m a p re va lê n c i a ge ra l d e 1 6 % e b a i x a s c a rga s p a ra si tá ri a s. Em c o n c lu sã o , a a n gi o stro n gi lí a se a b d o m i n a l n o su l d o Bra si l p o d e se r u m a i n f e c ç ã o f re q u e n te , p o ré m c o m b a i x a m o rb i d a d e e re a ti vi d a d e so ro ló gi c a d e gra d u a l d e c lí n i o .
Palavr as-chaves: An gi o stro n gi lí a se a b do m i n a l. Angio stro ngylus c o staric ensis. Do r a b do m i n a l. Ga stro e n te ri te e o si n o f í li c a . Zo o n o se .
1 . Lab o r ató r io de B io lo gia Par asitár ia da Fac uldade de B io c iê nc ias e Lab o r ató r io de Par asito lo gia Mo le c ular do Instituto de Pe sq uisas B io mé dic as da Po ntific ia Unive r sidade Cató lic a do Rio Gr ande do Sul, Po r to Ale gr e , RS. 2 .Instituto de Ciê nc ias B io ló gic as da Unive r sidade de Passo Fundo e Instituto de Pato lo gia de Passo Fundo , Passo Fundo , RS. 3 . Institut für Tr o pe nme dizin, Eb e r har d Kar ls Unive r sität, Tüb inge n – pr e se nt addr e ss: Institute fo r Co mpar ative Tr o pic al Me dic ine and Par asito lo gy, Ludwig- Maximilians- Unive r sität Münc he n, Munic h, Ge r many.
Wo r k suppo r te d b y: CAPES-DAAD-PROB RAL ( 0 5 5 /9 7 ) , Fo r tüne Pr o gr am ( Unive r sity o f Tüb inge n) , PUCRS, CNPq , FAPERGS.
Addr e ss to: Dr. Car lo s Gr ae ff- Te ixe ir a. Instituto de Pe sq uisas B io mé dic as/PUCRS. Av. Ipir anga 6 6 9 0 , HSL 2o
andar, sala 2 0 , 9 0 6 9 0 - 9 0 0 Po r to Ale gr e , RS. Te l: 5 5 5 1 3 3 2 0 - 3 0 0 0 e xt 2 1 7 0 , Fax: 5 5 5 1 3 3 2 0 3 3 1 2 ,
e mail: gr ae te ix@ puc r s. b r
An gi o s tr o n gylu s c o s ta r i c e n s i s i s a m e ta s tr o n gyl i d ne mato de , par asitic o f wild r o de nts. The wo r ms live inside the me se nte r ic ar te r ial syste m and te r r e str ial mo llusk s ar e
inte r me diate ho sts1 3. Human ac c ide ntal infe c tio n may r e sult
in ab do minal dise ase that has alr e ady b e e n r e po r te d fr o m
mo st c o untr ie s o f Ce ntr al and So uth Ame r ic a1 4. Diagno sis is o nly estab lished thr o ugh anato mic o patho lo gic al examinatio n
o f sur gic al o r b io psy spe c ime ns, sinc e the r e is no e vide nc e
o f lar val e liminatio n in the fe c e s, as se e n with e xpe r ime ntal
infe c tio n o f r o de nts6 1 3. Re sults fr o m c r o ss-se c tio nal studie s have b e e n pub lishe d5, inc luding an o utb r e ak in Guate mala9,
b e side s many c ase r e po r ts fr o m single o r small gr o ups o f
patie nts2 1 4 1 6. In 1 9 9 5 , a 4 1 -ye ar-o ld wo man was diagno se d
with ab do minal angio str o ngyliasis, living in a r ur al ar e a o f so uthe r n B r azil. That was the o ppo r tunity fo r atte mpting a
fir st de sc r iptio n o f the natur al histo r y o f this par asito sis, in a
po pulatio n-b ase d lo ngitudinal study.
MATERIAL AND METHODS
Co lo m b o - Usi n a is a r ur al c o mmunity in the munic ipality o f Guapo r é ( 5 2 ° 0 8 ’ W; 2 9 ° 0 2 ’S) in the so uthe r nmo st State o f Rio Gr ande do Sul, B r azil. This ar e a was se le c te d afte r the
histo patho lo gic al diagno sis o f ab do minal angio str o ngyliasis,
with de mo nstr atio n o f an intr a-ar te r ial ne mato de , in a lo c al
resident. Adult wo rms o f An gio stro n gylu s c o sta ric e n sis were also r e c o ve r e d fr o m mic e e xpe r ime ntally infe c te d with lar vae
fo und in slugs c o lle c te d in the imme diate sur r o undings o f
the ho use .
The ho use s in the c o mmunity ar e distr ib ute d wide ly apar t
alo ng a se c o ndar y r o ad le ading to the ne ighb o r ing to wn o f Anta Go r da. Lo c al r e side nts we r e r e giste r e d and the ho use s
we r e plo tte d o n a map, in June 1 9 9 5 . At this time , info r me d
c o nse nt to par tic ipate in the study was o b taine d fr o m e ac h
individual. The inve stigatio n pr o to c o l was appr o ve d b y the
e thic al c o mmitte e ( CEP-PUCRS, Pr o c e ss numb e r 0 1 /9 6 ) and pe r fo r me d ac c o r ding to B r azilian r e gulatio ns ( De c r e e
MS-CNS 1 9 6 /9 6 ) . Co lle c tio n o f se r a a nd fe c a l sa m ple s we r e
pe r fo r me d in July 1 9 9 6 , Mar c h 1 9 9 7 , Mar c h 1 9 9 8 , Oc to b e r 1 9 9 8 and Mar c h 1 9 9 9 .
Clinic al evaluation ( July 9 5 , Marc h 9 7 and Marc h 9 8 ) was
do ne b y a que stio nnair e fo c use d o n the ide ntific atio n and
desc ription of abdominal pain. A brief physic al examination was
undertaken looking for vital signs and abdominal examination
when abdominal pain was referred at that moment.
Se r um sample s we r e k e pt o n ic e until sto r age at -2 0 ° C in
the lab o r ato r y. ELISA-IgG ( 7 6 % se nsitivity; 9 1 % spe c ific ity)
was pe r fo r me d as de sc r ib e d e lse whe r e4. B r ie fly, the plate s
we r e se nsitize d with c r ude antige n o f fe m ale wo r m s at a
c o nc e ntr atio n o f 7
µ
g/ml and se r um sample s we r e dilute d 1 :5 0 0 in 0 .0 5 % Twe e n 2 0 , 5 % sk imme d milk PB S.For the detection of Stro ngylo ide s ste rco ra lis larvae in stools,
a modified Baermann method was used7. Approximately 5 g of
fresh fec al samples were plac ed on four layers of surgic al gauze
supported by a plastic mesh, partially immersed in tap water in
a plastic funnel and left overnight at room temperature. Larvae
found under the ste r e o mic r o sc o pe we r e ide ntifie d thr o ugh
e xaminatio n at a highe r magnific atio n unde r the mic r o sc o pe .
Fo r the de te c tio n o f he lminth e ggs and pr o to zo an c ysts, par t o f the fe c al sample s we r e mixe d with a 1 0 % fo r malin so lutio n
and pr o c e sse d in the lab o r ato r y b y Ritc hie me tho d1 7.
Fo r the de te c tio n o f En te ro b i u s ve rm i c u la ri s e ggs, the
me tho d o f Gr aham was pe r fo r me d. Afte r de taile d o r al and
wr itte n instr uc tio ns, the individuals c o lle c te d the sample s b y applic atio n o f a tr anspar e nt adhe sive tape in the pe r ine um
e ar ly in the mo r ning and plac e d the use d tape o ve r a glass
slide . Slide s we r e se ar c he d fo r e ggs unde r the mic r o sc o pe .
For the study on intermediate hosts in the area, houses were
randomly assigned as c ollec tion sites. Three c ollec tion sites were c hosen in the lower and another three in the upper sec tion of
the main road. Terrestrial mollusks were c ollec ted during the
same night by a sc reening of the surroundings of the houses by
two researc hers, beginning at 9 p.m. for 3 0 minutes. All mollusks found on the surfac e of the soil or vegetables were c ollec ted and
kept in a cotton bag with grass until examination in the laboratory.
The slugs we r e e visc e r ate d and the b o dy was minc e d and
inc ubated in a 3 0 % ( w/v) pepsin ( P-7 1 5 2 , Sigma) 0 .0 7 % ( v/v) hydroc hloric ac id solution, overnight at room temperature. The
pr e par atio ns we r e the n plac e d in a B ae r m ann funne l fo r
sedimentatio n and identific atio n o f metastro ngylid larvae. A
sample was inoc ulated pe r o s in albino mic e for the identific ation of adult worms inside the mesenteric arteries. The slugs were
ide ntifie d b y e xte r nal c har ac te r istic s and if ne c e ssar y b y
mic rosc opic examination of genitalia, with the expert supervision
of Dr. Georgina Mansur ( Malac ology Laboratory, PUCRS) .
RESULTS
At least one set of data was c ollec ted for 1 7 9 /1 9 8 individuals
living in the area. These presented the following demographic c harac teristic s: 8 3 males, 9 6 females, 3 3 ± 1 8 years-old and
age distribution shown in Figure 1 . Prevalenc e of antibodies
against A. c o sta ric e n sis antigen ranged from 2 .8 % to 2 8 % and inc idenc e from 0 % to 8 % , with the distr ib utio n sho wn in
Fi g u r e 1 - Ag e d i str i b u ti o n o f th e stu d y p o p u l a ti o n a t Li n h a Col om b o-Usi n a, Gu apor é , sou the r n Br azi l .
18 36
25 39
25
19
11
6
0 5 10 15 20 25 30 35 40 45
0 - 9 10 - 19 20 - 29 30 - 39 40 - 49 50 - 59 60 - 69 70 - 79
Age (years)
Absolute
individuals with positive serology, male and female individuals
were found to be equally affec ted: 1 :0 .9 5 and 0 .8 3 :1 in July 1 9 9 5
and Oc tober 1 9 9 8 , respec tively.
Tab l e 1 - Ab dom i n al an gi ostr on gyl i asi s i n Gu apor é , RS, Br azi l . Lon gitu din al serological stu dy, from Ju ly 1995 to March 1999.
Date Positive serology Total Examined Prevalence ( %) Incidence ( %) July 1 9 9 5 39 1 3 8 2 8 .2
-March 1 9 9 7 4 94 4 .2 0
March 1 9 9 8 9 90 1 0 .0 5 .9 October 1 9 9 8 22 1 0 9 2 0 .2 8 .0 March 1 9 9 9 2 69 2 .8 1 .5
0.0 5.0 10.0 15.0 20.0 25.0 30.0
July 1995 March 1997 March 1998 October 1998 March 1999 Prevalence (%) Incidence (%)
Figu re 2 - Pre vale n ce an d in cide n ce of abdom in al an giostron gyliasis as in dicate d by se ru m an tibodie s an ti-Angio str o ngylus co star icensis in IgG-ELISA in Lin ha Colom bo-Usin a, Gu aporé , sou the rn Brazil.
4 9
5
14 16
12
9 7
0 2 4 6 8 10 12 14 16 18
0 - 9 10 - 19 20 - 29 30 - 39 40 - 49 50 - 59 60 - 69 70 - 79
Age (years)
T
ot
al
sum
-Absolute
number
Figu re 3 - Age distribu tion of se rologically positive in dividu als am on g the popu lation stu die d from 1 9 9 5 to 1 9 9 9 , in Lin ha Colom bo-Usin a, Gu aporé , sou the rn Brazil.
Se r o lo gic a l fo llo w- up fo r 5 ye a r s wa s po ssib le in 3 2 individuals ( Table 2 ) : 1 9 /3 2 ( 4 0 .6 % ) had persistently negative
serology while only 1 /3 2 individuals had persistently positive
serology. This distribution is also seen within the group followed
for 4 years ( data not shown) . Individual serologic al reac tivity sho ws bo th var iability and diver sity o f patter ns ( Figur e 4 ) .
Presenc e of abdominal pain was reported by 3 8 , 2 3 and 1 4
individuals in January 1 9 9 6 , Marc h 1 9 9 7 and Marc h 1 9 9 8 ,
respec tively, without a strong assoc iation with the serologic al reac tivity seen in the ELISA ( Table 3 ) .
Asc a ris lum b ric o ide s and Gia rdia inte stina lis were the m o s t fr e q ue n tly fo un d e n te r o pa r a s ite s a n d s itua tio n s o f
c o -infe c tio n ar e sho wn in Tab le s 4 and 5 . Oc c ur r e nc e o f
enteroparasites and serologic al reac tivity to A. co sta rice nsis in
Neg Neg Neg Neg Neg 1 9
+ Neg Neg Neg Neg 4
+ Neg Neg + Neg 3
+ Neg + + Neg 2
+ + Neg + Neg 1
+ + + + Neg 1
+ + + + + 1
Neg Neg Neg Neg + 1
Total = 3 2
Table 3 - Lon gitu din al su rvey on abdomin al an giostron gyliasis in Lin ha Colom bo-Usin a, Gu aporé , RS, sou the rn Brazil, from 1 9 9 5 to 1 9 9 9 . Estimation of association ( Yu le’s coefficien t) between abdomin al pain ( Abd pain ) an d positive serology.
Dates and occurrence ELISA results
of abdominal pain Positive Negative Total Y ( Yule’s association coefficient) January 1 9 9 6
Abd pain + 9 29 38 Abd pain - 19 51 70 Total 28 80 1 0 8
- 0 .0 9 March 1 9 9 7
Abd pain + 1 22 23 Abd pain - 4 55 59
Total 5 77 82
- 0 .2 3 March 1 9 9 8
Abd pain + 3 11 14 Abd pain - 6 66 72
Total 9 77 86
+ 0 .5
Table 4 - Lon gitu din al su rvey on abdomin al an giostron gyliasis in Lin ha Colom bo-Usin a, Gu apor é , RS, sou the r n Br azil, fr om 1 9 9 5 to 1 9 9 9 . Coproparasitological su rvey ( Ritchie method) performed in 1995.
Diagnosis Isolated % Multiple % Total % infections infection
Gia rdia intestina lis 4 5 .0 1 1 .3 5 6 .3
Asca ris lum brico ides 1 1 .3 4 5 .0 5 6 .3
Io da m o eba sp 3 3 .8 0 0 .0 3 3 .8
Trichuris trichiura 0 0 .0 2 2 .5 2 2 .5
Enta m o eba co li 1 1 .3 1 1 .3 2 2 .5
Stro ngylo ides sterco ra lis 0 0 .0 1 1 .3 1 1 .3
Ta enia sp 0 0 .0 1 1 .3 1 1 .3
Entero bius verm icula ris 1 1 .3 0 0 .0 1 1 .3
Enta m o eba ha rtm a ni 1 1 .3 0 0 .0 1 1 .3 Negative 64 8 0 .0 0 0 .0 64 8 0 .0
Total 7 5 9 3 .8 1 0 1 2 .5 8 5 1 0 6 .3
Multiple infections
A. lum brico ides + T. trichiura 2
A. lum brico ides + S. stro ngylo ides 1
A. lum brico ides + Ta enia sp 1
G. intestina lis + E. co li 1
Total 5
0.00 1.00 2.00 3.00 4.00 5.00
jul-95 mar-97 mar-98 out-98 mar-99
E L ISA ra tio 077 019 cut-off 0.00 1.00 2.00 3.00 4.00 5.00 6.00 7.00
jul 95 mar 97 mar 98 oct 98
ELI S A ra ti o 020 900 cut-off 1 9 9 5 a nd 1 9 9 7 we r e no t signific a ntly a sso c ia te d ( Yule ’s
assoc iation c oeffic ient = -0 .1 1 and 0 .1 2 , respec tively for 1 9 9 5 and 1 9 9 7 data) . Prevalenc e of strongyloidiasis, as evaluated by the Baermann method, was 1 0 % and 4 % with an inc idenc e of
4 .2 % in Marc h 1 9 9 7 . In July 1 9 9 6 , a searc h for enterobiasis showed a prevalenc e of 4 .8 % ( 3 /6 3 ) .
The noc turnal searc h for terrestrial mollusks was suc c essful in 4 /6 sites ( Table 6 ) and metastrongylid larvae were found in 1 0 /6 0 mollusks, mainly slugs (Phyllo c a u lis va rie ga tu s) from the Veronic elid family. The spatial distribution of the c ollec ted
mollusks within eac h foc us is shown in Figure 5 . In house number 3 0 , where no slug was found in the noc turnal searc h, a dead slug was found by the peasant inside the well from where
water is pumped for human c onsumption.
Table 5 - Lon gitu din al su rvey on abdomin al an giostron gyliasis in Lin ha Colom bo-Usin a, Gu apor é , RS, sou the r n Br azil, fr om 1 9 9 5 to 1 9 9 9 . Coproparasitological su rvey performed ( Ritchie method) in 1997.
Diagnosis Isolated % Multiple % Total % infections infection
Asca ris lum brico ides 10 1 1 .7 8 9 .4 18 2 1 .7
Enta m o eba co li 6 7 .0 2 2 .3 8 9 .4
Trichuris trichiura 3 0 .0 6 7 .0 9 1 0 .5
Entero bius verm icula ris 2 2 .3 0 0 .0 2 2 .3
Ta enia sa gina ta 1 1 .1 0 0 .0 1 1 .1 Ancylostomatic larvae 0 0 .0 1 1 .1 1 1 .1
Gia rdia intestina lis 0 0 .0 1 1 .1 1 1 .1
Stro ngylo ides sterco ra lis 0 0 .0 1 1 .1 1 1 .1
Hym eno lepis na na 0 0 .0 1 1 .1 1 1 .1 Negative 63 7 4 .1 0 0 .0 63 7 4 .1
Total 8 5 1 0 0 .0 2 0 2 3 .5 1 0 5 1 2 3 .5
Multiple Infections
A. lum brico ides + T. trichiura 5 A. lum brico ides + H. na na 1
A. lumbricoides + ancylostomatic larvae 1
A. lum brico ides + S. sterco ra lis 1
G. intestina lis + E. co li 1
T. trichiura + E. co li 1
Total 1 0
Cor r ected Total 8 5 1 0 0 .0
0.00 1.00 2.00 3.00 4.00 5.00
jul-95 mar-97 mar-98 out-98 mar-99
E L ISA ra tio 042 039 cut-off 0.00 1.00 2.00 3.00 4.00 5.00 6.00 7.00
Jul 95 Mar 97 Mar 98 Oct 98 Mar 99
ELI S A ra ti o 001 005 cut-off
Figu re 4 - In dividu al serological reactivity ( IgG an ti-Angiostr ongylus costar icensis) alon g several tim e poin ts, from 1995 to 1999, in Lin ha Colombo-Usin a, Gu aporé, sou thern Brazil. The in dividu al 005 shows a strikin g in cre ase in hu m oral re activity, su gge stive of re -in fe ction . Individuals 001, 042, 039, 077 and 019 also presented a pattern suggestive of re-in fection with a variable bu t declin in g reactivity. Both 020 an d 900 show serocon version with persisten ce of reactivity u p to October 1998.
DISCUSSION
Longitudinal population-based studies are important for a
better evaluation of the epidemiology and natural history of infec tio n and disease. Mo st o f the kno wledge abo ut human
infe c tio n with An gi o stro n gylu s c o sta ri c e n si s c o me s fr o m
in dividua l o r s m a ll s e r ie s r e po r ts o f s ur gic a lly tr e a te d
individuals1 4. In southern B razil, surgic al intervention due to inte stinal pe r fo r atio n o r o b str uc tio n r e late d to ab do minal
angio stro ngyliasis is mo re frequent than o ther c o mplic ated
inflammato ry bo wel diseases, suc h as ulc erative c o litis and
tuberc ulosis1. But the more severe c linic al c ourses in infec tious diseases in general are usually only the tip o f the ice b e rg.
Olde r e ditio ns o f so m e te xtb o o k s3 pr e se nt ab do m inal
angiostrongyliasis as a pediatric problem, based on a report of a
c ase series from a pediatric hospital, that was published twic e updating a growing but c umulative number of c hildr e n1 1 1 2.
House 15 U Churc h Community center fence House 25 House 12 House 5 vg sw
Fi gu r e 5 - Sche m ati c dr awi n g of the su r r ou n di n gs of 4 ou t of the 6 h o u se s wh e r e a n o ctu r n a l se a r ch f o r te r r e str i a l m o l l u sk s wa s u n de r take n in Lin ha Colom bo-Usin a, Gu apor é . Mollu sks we r e fou n d i n shadowe d ar e as, i l l u str ati n g the f ocal di str i b u ti on of pote n ti al
A. co sta r ice nsis ve ctor s. Sm al l ci r cl e s i n shadowe d ar e as ( hou se s 1 2 an d 2 5 ) r e pr e se n t pi l e s of ston e s. At hou se 5 , the r e was a ston e wall ( sw) an d “vg” is the ve ge table garde n . At hou se 1 5 in the ce n te r of the shade d ar e a the r e i s a sm al l b u shy tr e e . Ar r ows poi n t Nor th.
Church
Table 6 - Presen ce of m etastron gylid larvae in terrestrial m ollu sks collected in immediate su rrou n din gs of 6 hou ses in Lin ha Colombo Usin a, Gu aporé, RS, Brazil, in March 1999.
Mollusk species Site no Infected Prevalence Parasitic
( %) burden
Phyllo ca ulis va riega tus
15 24 4 1 6 .7 3 , 2 , 1 , 2 25 12 2 1 6 .7 3 , 1 0 3
12 8 0 0 .0
5 10 3 3 0 .0 2 , 1 0 , 1 3
Bra dyba ena sim ila ris 5 5 1 2 0 .0 36
Lim a x fla vus 5 1 0 0 .0
se r o lo gy fo r ab do minal angio str o ngyliasis.
Variability in prevalenc e as seen in the present report may
be interpreted as resulting from foc ality and seasonality, two main
characteristics of zoonotic infections. A higher prevalence in 1 9 9 5 is c oinc ident with the oc c urrenc e of one c omplic ated c linic al
c ourse that was taken as the index c ase for the study. This fac t
may also result from a higher probability for severe c ases to
oc c ur among an inc reased number of infec ted people at the time.
Individual follow-up of antibody reac tivity as demonstrated by IgG-ELISA has shown indic ations for two main possibilities.
First, abdominal angiostrongyliasis appears not to be a persistent
infec tion. Most of the doc umented peaks in serologic al reac tivity
did not last more than a year and only a few individuals had per sistent po sitive ser o lo gy. These data fur ther suppo r t the
p r e s u m p ti o n th a t m a n i s n o t a we l l - a da p te d h o s t fo r A. co sta rice nsis, based on the pathologic al reports and on the failure to detec t L1 larvae in fec es. Sec ondly, most infec tions are asymptomatic . Not a single individual presented a very suggestive
c linic al pic ture of severe abdominal disease that would inc lude
at least an ac ute c ourse of abdominal pain and fever. Most
episodes of abdominal pain were transient or probably associated with viral or bac terial gastroenteritis.
Although not yet properly investigated, serologic al c
ross-reac tions with antigens from A. co sta rice nsis and other parasites
are known to oc c ur4. Other intestinal parasitoses were detec ted
in the population but no signific ant assoc iation with the anti-A. co sta rice nsis antibody reac tivity was detec ted. This is not against the idea that there are c ross-reac tive epitopes, sinc e intensity of
the nonspec ific response may be low depending on the c hronic ity
or parasitic burden of the heterologous infections1 0. Co-infections or multiple infec tions should be better investigated in order to
c larify all the missing bric ks in the knowledge of humoral c
ross-reac tivity among diverse c ombinatory situations.
The relatively low prevalenc e of other intestinal parasitosis
is not a surprise, sinc e loc al peasants, mostly desc endents of Italian immigrants, have good sanitary conditions and educational
level. The finding of a dead slug in the sourc e of water for human
c onsumption in one of the houses, adds support to the hypothesis
of water transmission of A. co sta rice nsis. This possible route for transmission was previously c ommented by Ubelaker et al1 8
reporting the emergence of third-stage larvae from experimentally
infec ted aquatic snails.
Several mollusk species are susceptible to A. co sta rice nsis
infection but only a few have a significant role as hosts, such as the
veronicelid slugs15. Infection was detected mainly in Phyllo ca ulis
va ri e ga tu s, the fir st inter mediate ho st desc r ib ed in B r azil8 with prevalence and parasitic burdens in the range as previously
reported15. Mollusks were usually found restricted to one area next
to the houses, where piles of stones, bricks or hay, and soil cracks
had provided shelter, as seen in Figure 5 . This focality in the
distribution of the intermediate host may be important to determine the absence of widespread infection in the human population.
health problem, infec tion may be regularly detec ted, with a
pr e do m in a n tly a s ym pto m a tic c o ur s e , us ua lly le a din g to
spontaneous remission.
ACKNOWLEDGEMENTS
We thank the staff o f lo c al Pub lic He alth Se r vic e s and Agric ultural Extension Program in Guaporé and the family of
MVB, the c ommunity and their several leaders at Linha
Colombo-Usina, for all kind of support provided during field work. To Eva
Medeiros Floriano and to the Transportation Sec tion, Prefeitura Universitária, PUCRS, for tec hnic al and logistic al help.
REFERENCES
1 . Ago stini AA, Ro dr igue z R, Mazzuc o R, B o r ge s J , Sto b b e J C, B e c k e r L, Gr ae ff- Te ixe ir a C. Angio str o ngilo se ab do minal – Pato lo gia c ir úr gic a de impo r tânc ia r e gio nal. J o r nal B r asile ir o de Me dic ina 8 0 : 4 0 - 4 2 , 2 0 0 1 . 2 . Ayala MAR. Angio str o ngilo ido se ab do minal no s e stado s do Par aná e Santa
Catar ina: apr e se ntaç ão de c inc o c aso s e r e visão da lite r atur a. Me mó r ias do Instituto Oswaldo Cr uz 8 2 : 2 9 - 3 6 , 1 9 8 7 .
3 . B lume nthal DS. Angio str o ngyliasis. In : Wyngaar de n J B , Smith LH ( e ds) Ce c il’s Te xtb o o k o f Me dic ine, Saunde r s, Philade lphia, p. 1 9 1 3 , 1 9 8 8 . 4 . Ge ige r SM, Laitano AC, Sie ve r s- To ste s C, Ago stini AA, Sc hulz- Ke y H, Gr ae
ff-Te ixe ir a C. De te c tio n o f the ac ute phase o f ab do minal angio str o ngyliasis with a par asite-spec ific IgG enzyme link ed immuno so r b ent assay. Memó r ias do Instituto Oswaldo Cr uz 9 6 : 5 1 5 - 5 1 8 , 2 0 0 1 .
5 . Gr a e ff- Te ixe ir a C, Ago stini AA, Ca m illo - Co ur a L, Fe r r e ir a - Da - Cr uz MF. Se r o e pide mio lo gy o f ab do minal angio str o ngylo sis: the standar dizatio n o f an immuno e nzymatic assay and pr e vale nc e o f antib o die s in two lo c alitie s in so uthe r n B r azil. Tr o pic al Me dic ine and Inte r natio nal He alth 2 : 2 5 4 -2 6 0 , 1 9 9 7 .
6 . Gr ae ff- Te ixe ir a C, Camillo - Co ur a L, Le nzi HL. Clinic al and e pide mio lo gic al aspe c ts o f ab do m inal angio str o ngyliasis in so uthe r n B r azil. Re vista do Instituto de Me dic ina Tr o pic al de São Paulo 3 3 : 3 7 3 - 3 7 8 , 1 9 9 1 . 7 . Graeff-Teixeira C, Medeiros E, Zanini GM, B rasil CAA, Cardozo B L, Dalpiaz
MG, B isol LW. Inexpensive alternative material for the isolation of larvae with the Baermann method. Memó rias do Instituto Oswaldo Cruz 9 2 :3 9 9 -4 0 0 , 1 9 9 7 . 8 . Gr a e ff- Te ix e ir a C, Th o m é J W, Pin to SCC, Ca m illo - Co ur a L, Le n zi HL.
Ph yllo c a u li s va r i e ga tu s - a n in te r m e dia te h o s t o f An gi o s tr o n gylu s c o s ta r i c e n s i s in s o uth B r a zil. Me m ó r ia s do I n s tituto Os wa ldo Cr uz 8 4 : 6 5 - 6 8 , 1 9 8 9 .
9 . Kr amme r MH, Gr e e r GJ , Quiño ne z J F, Padilla NR, He r nánde z B , Ar ana B A, Lo r e nzana R, Mo r e r a P, Highto we r AW, Eb e r har d ML, He r waldt B L. Fir st r e po r te d o utb r e ak o f ab do minal angio str o ngyliasis. Clinic al and Infe c tio us Dise ase s 2 6 : 3 6 5 -3 7 2 : 1 9 8 8 .
1 0 . Ke nne dy MW, To mlinso n LA, Fr ase r EM, Chr istie J F. The spe c ific ity o f the antib o dy r e spo nse to inte r nal antige ns o f Asc a ri s: he te r o ge ne ity in infe c te d humans, and MHC ( H- 2 ) c o ntr o l o f the r e pe r to ir e in mic e . Clinic al and Expe r ime ntal Immuno lo gy 8 0 : 2 1 9 - 2 2 4 , 1 9 9 0 .
1 1 . Lo b o -Sanahuj a F, Lo r ia-Co r té s R, Go nzále z G. Angio str o ngilo sis ab do minal. Aspe c to s c línic o s, tr atamie nto y r e visió n de la lite r atur a. B o le tim Me dic o de l Ho spital Infantil Me xic o 4 4 : 4 - 9 , 1 9 8 7 .
1 2 . Lo r ia- Co r té s R, Lo b o - Sanahuj a J F. Clinic al ab do minal angio str o ngyliasis. A study o f 1 1 6 c hildr e n with inte stinal e o sino philic gr anulo ma c ause d b y
1 3 . Mo r e r a P. Life histo r y and r e de sc r iptio n o f An gi o stro n gylu s c o sta ri c e n si s
Mo r e r a & Cé spe de s, 1 9 7 1 . Ame r ic an J o ur nal o f Tr o pic al Me dic ine and Hygie ne 2 2 : 6 1 3 -2 1 , 1 9 7 3
1 4 . Pe na G, Andr ade Filho J S, Assis SC. An gi o stro n gylu s c o sta ri c e n si s: Fir st r e c o r d o f its o c c ur r e nc e in the state o f Espir ito Santo , B r azil, and a r e vie w o f its ge o gr aphic distr ib utio n. Re vista do Instituto de Me dic ina Tr o pic al de São Paulo 3 7 : 3 6 9 -3 7 4 , 1 9 9 5 .
1 5 . Rambo PR, Agostini AA, Graeff-Teixeira C. Abdominal angiostrongyliasis in southern Brazil - prevalenc e and parasitic burden in mollusc intermediate hosts from 1 8 endemic foc i. Memó rias do Instituto Oswaldo Cruz 9 2 :9 -1 4 , 1 9 9 7 .
1 6 . Silve r a CT, Gh a li VS, R o ve n S, He im a n J , Ge lb A. An gio s tr o n gylia s is : a r a r e c a u s e o f ga s tr o i n te s ti n a l h e m o r r h a ge . Am e r i c a n J o u r n a l o f Gastr o e nte r o lo gy 8 4 : 3 2 9 -3 3 2 , 1 9 8 9 .
1 7 . Yo u n g KH, B u l l o c k S L, Me l vi n D M, S p r u i l l CL. E th yl a c e ta te a s a s u b s ti tu te fo r d i e th yl e th e r i n th e fo r m a l i n - e th e r s e d i m e n ta ti o n pr o c e dur e . J o ur nal o f Clinic al Mic r o b io lo gy 1 0 : 8 5 2 - 8 5 3 , 1 9 7 9 . 1 8 . Ub e l a k e r J E , B u l l i c k GR , Ca r u s o J . E m e r g e n c e o f t h i r d - s t a g e
