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Rev. Inst. Med. trop. São Paulo

31 {2): 63-70, março-abril, 1989

NATURAL TRYPANOSOMA CRUZI INFECTION IN DOGS OF ENDEMIC AREAS OF THE

ARGENTINE REPUBLIC (1)

M a r t a A . L A U R I C E L L A (2), A n g e l J . S I N A G R A (2), I r e n e P A U L O N E (2), A d e l i n a R . R I A R T E (2) & E l s a L . S E G U R A (3)

S U M M A R Y

The population dynamics and the prevalence of chagasic infection of 352 dogs living in 108 rural houses infested by triatomines were studied. The region was divided into three sections according to increasing distances to an urban area. E a c h animal was identified by means of its particular characteristics and built, and its owners gave information about its habits. B y means of xenodiagnosis, serology and E C G studies, prevalences of infection, parasitological-serological correlation, percentage of altered electrocardiographic outlines and percentage of houses with parasitemic dogs, were determined.

T h e rural area showed a characteristic T . cruzi infection pattern and differences

in the canine population parameters with respect to the other areas were observed: a higher proportion of puppies than adult dogs, a more sedentary population, higher prevalences of infection, as measured by xenodiagnosis, in dogs, and the highest

proportion of bedroom insects infected with T . cruzi.

It is assumed that the sedentary characteristics of the human population in that rural area impinge in the blood offer to the triatomine population, and the rúgh percentage of parasitemic dogs of the area, contribute to the rise of "kissing

ougs" infected with T . cruzi found in bedrooms.

K E Y W O R D S : C h a g a s ' disease; Epidemiology; Dogs; Trypanosoma cruzi.

I N T R O D U C T I O N

The knowledge of t1

e dynamics of

transmis-sion of Trypanosoma cruzi in the domestic rural

environment is essential for the application of measures tending to diminish or abolish inciden ces of infection in humans and animals.

The elevated frequency of parasitemic dogs6

2 7

and the detection of high proportions of pro teins derived from canine blood in the contents

of T r i a t o m a infestans promesenteron2 6

, is evi-dence of the fundamental role the dog plays in the transmission of this flagellate.

I n 1916 Salvador M A Z Z A identified T . cruzi

in circulating blood of young dogs in the Pro-vince of J u j u y1 1

, and characterized the transpla-c e n t a l transmission in this host by following

infected females and their youngsters1 2.

(1) T h i s w o r k w a s s u p p o r t e d b y a g r a n t f r o m T D R W H O U N D P B a n k

(2) P r o f e s s i o n a l i n R e s e a r c h of t h e I n s t i t u t o N a c i o n a l d e D i a g n o s t i c o e I n v e s t i g a c i ó n d e l a E n f e r m e d a d d e C h a g a s ' D o c t o r M a r i o F a t a l a C h a b é n " ( I . N . D . I . E . C . H . )

(3) D i r e c t o r of I . N . D . I . E . C H .

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I n Brazil, the prevalence of infection as mea-sured by xenodiagnosis for naturally infected dogs, was of 1 8 . 3 %8

, and in Chile of 9 . 3 9 Í2 0

. I n endemic areas of our country, the prevalence of infection detected by serology, for dogs from ur

ban areas, was of 1 7 . 5 9r

5

. However, the highest

indices (64.291 and 6 5 . 2 9 r for xenodiagnosis and

serology respectively) corresponded to dogs Irom rural areas in the Province of Santiago del Este ro2 7.

T h e area chosen for this study covers a surfa

ce of 4 4 0 k m2 and it belongs to the R i o Hondo

County in the midwest of the Province of S a n -tiago del Estero. It's a valley one k m in width, crossed by the Dulce R i v e r and it is located bet ween 4 to 5 0 k m from the city of Termas de R i o Hondo. T h e zone shows the typical vegetation of the Fitogeographic Chaco Province forested with axebreakers (Aspidosperma spp and S c h i nopsis spp). Partial deforestation has generated a secondary formation of xerofilus shrubs (Aca cia spp and Larrea spp). T h i s area involves a

rural community of approximately 3 , 0 0 0 inhabi

tants, where the serological prevalence for C h a gas' Disease in children less than five years old is of 8 9 r1 6

. T h e province of Santiago del Estero

belongs to a vast central region of Argentina whe-re the absolute m a x i m u m temperatuwhe-res surpass 4 5 C and the relative annual humidity is less than

7 0 9 c ; this region is also coincident with the

isoli-ne of 7 5 % triatomiisoli-ne domicile infestation3.

As this rural community belongs to an area of high endemicity for C h a g a s ' Disease, an epide-miological surveillance project consisting in the use of appropriate tools and technology to dimi nish the vectorial transmission through sanitary agents b e l o n g i n g to the same c o m m u n i t y is

being implemented in this area1 6 1 1

. T h e objective of this work is to characterize the rural canine population and to obtain information on the

dy-namics of infection by T . cruzi. T h e realization

of these objectives will permit the planning of control strategies on the domestic reservoirs, contributing to abolish their parasite offer to the triatomine and, hence, to man.

M A T E R I A L S A N D M E T H O D S

A — Selection of the sample:

The study was performed with 3 5 2 dogs (D)

living in 1 0 8 houses. Only those not found during two consecutive visits to the house, and those presumably dangerous to the operators were ex eluded ( 1 2 / 3 5 2 ) .

T h e area (Fig. 1) was divided into three zones according to the distances to the city of Termas de R i o Hondo and to the structural characte ristics of the houses (huts: built with indigenous materials; brick: for which industrial technology was used; and m i x e d : a combination of both).

T h e rural zone (R) contained improved huts and huts in similar proportions and was the most distant to the city; the transitional (T) zone had the three types of houses in similar proportions and the periurban (Pe) zone had a majority of brick houses.

F i g . 1 — G e o g r a p h i c a l l o c a t i o n of t h e R i o H o n d o D e p a r t m e n t , S a n t i a g o d e l E s t e r o , A r g e n t i n a .

A sample of the canine population that be-longed to houses that had at least four triato-mines (kissing bugs) during the entomological survey performed in the zone the previous year, was selected. T h e search methodology used was that indicated by the Chagas National Service of one m a n hour of searching effort using

chemi-cal irritants1 5. Immediately after this survey the

area was sprayed with Deltamethrin and Benze-ne Hexachloride.

B — Characteristics of the population survey:

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Coding House number Dog number

Description Sex Age S i z e

Weight estimate

Questionnaire In t h i s a r e a , about o r i g i n , feeding habits are recorded.

Physical appearance

F i g . 2 — E p i d e m i o l o g i c a l s u r v e y m o d e l : i d e n t i f i c a t i o n c a r d , i d e n t i k i t a n d q u e s t i o n n a i r e .

C — Studies performed

House location Owner's f u l l name

Bui It Color Kind of h a i r P a r t i c u l a r signs

questions made to owners hunting, nocturnal, and and t r a n s i e n t migrations

On land — T o detect parasitemia,

xenodiag-nosis was done in 340 D using twenty T . infestans

according to the methodology described

pre-viously2

. E i g h t ml of non-heparinized braquioce-phalic-, yugular-, or saphena-vein blood were ex-tracted for the procurement of serum for anti T . cruzi specific antibodies on 331 A , and looking for parasites using the S T R O U T enrichment

me-thod2 4, on 42. With the purpose of detecting

chro-nic injuries, electrocardiographic records of 45% (85 E C G ) of the D older than two years of age, were obtained using a F u k u d a Century electro-cardiograph (SCC-1) with a paper velocity of 2.5 cm/sec without previous anesthesia of the ani-mals.

The houses included the home and the peri-domicile, the first constituted by the bedrooms, the gallery, and the yard or outside area next to the house, where the owners sleep in the sum-mer. T h e peridomicile was represented by the kitchen, the deposit and the animal pen. T h e number of "kissing b u g s " found in 102 houses, those found in their peridomicile, and those in the bedrooms with a previous application of pire-troid stimulants, was determined.

Evaluation of infection with T . cruzi was

per-formed on " k i s s i n g b u g s " found in bedrooms. T h e Average Triatomine Infestation (A.T.I.) was determined as the average of total " k i s s i n g b u g s " of the house; those corresponding to

bed-rooms (A.T.I.b) and peridomicile (A.T.I.p) were

also calculated.

In the laboratory — T h e blood obtained by conserving the sera in glycerin buffer (90% glyce-rin — 10% stabilized saline solution in equal amounts) was processed daily. T h e blood of three D chosen at random was observed daily

loo-king for the presence of T . cruzi. For the specific

antibody search in the serum of 326 D, the indirect immunofluorescence reaction was employed, using canine antigamma-globulin fluorescein tagged (Byosis S.A.). Titles accepted as positive were 16. Commercial indirect hemmagglutina-tion (Polychaco S.A.) was also used. Discordant samples were submitted to an E L I S A reaction using an antigen prepared from cultured epimas-tigotes2 5

.

A l l reactions were adapted to canine sera and their sensibility was evaluated using sera of 60 parasitemic D from the Moreno County

(Province of Santiago del Estero)9.

D — Statistical studies

S t a t i s t i c a l analysis of the data was done

using the x2 test for analysis of frequency2 3.

Signi-ficance was set at P = 95%

R E S U L T S

A — General characteristics of the canine popu-lation

The canine population density was of 3.4 D/ house and only two houses lodged more than six (11 and 13 D). T h e age distribution showed a 32% diminution of the D number of the 1-2 year interval with respect to D of the 0-1 year interval. Seventy five percent and 90% were be-tween 0-4 years old and 0-6 years old respectively. T h e number of males (72%) was significantly hi-gher than the number of females (28%). Seventy seven percent was over a year old and was classi fied according to activity, into guardians (68.8%), hunters (25.7%) and goat tenders locally called "goaters" (5.5%). See T a b l e 1.

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T A B L E 1

P e r c e n t a g e s a n d p r e v a l e n c e s of i n f e c t i o n ( P I ) b y s e r o l o g y of d o g s c l a s s i f i e d a c c o r d i n g to t h e i r r o l e a n d e n v i r o n m e n t ,

R o l e of d o g s i n t h e h o u s e g u a r d i a n s h u n t e r s g o a t e r s

PI ((; >

68.8 36.4

25.7 46.2

5.5 13.0

D o m i c i l e

E n v i r o n m e n t

S t o r a g e a r e a P e n

PI {<<)

89.4 59.7

8.4 36.4

2.2 33.3

lodged temporary workers, most of whom went to the sugar harvest in T u c u m a n where they stayed up to five months of the year; this way, 25% of the D abandoned the habitat transiently.

The D received unbalanced diets and the food was of low protein content.

Differences between the three zones were ob served: R showed two d i s t i n c t i v e c h a r a c t e ristics: a) the percentage of houses with tempo-rary workers was significantly lower (16%) than in T (28.2%) and in Pe (40.7%) P < 0.05; b) the decrease in the number of D of the interval of 1-2 years with respect to the 0-1 year interval was of 68.2%, much greater (P < 0.05) than the one registered in T (34.5%) and in Pe (12.5%). However, there were no differences between the parameters of T and Pe.

B — Characteristics of the infection by T . cruzi

The prevalence of parasitemic infection as seen by xenodiagnosis (Px), was of 19.4% with no differences between males (20.1% ) and fema-les (17.8%). Forty six percent of the houses had at least one D with positive xenodiagnosis and

in only one of 42 blood samples, T . cruzi was

detected by the S T R O U T method. T h i s sample belonged to a nine month old D that lived in the Pe area. T h e percentages of parasitemic dogs according to age intervals increased with each age group, and in those older than ten years old an i m p o r t a n t increment with respect to the younger ones was observed (Table 2).

Almost thirty four percent (33.8%) of the D

were reactive for specific anti T . cruzi antibodies

T A B L E 2

A g e s p e c i f i c p r e v a l e n c e s r a t e s of s e r o p o s i t i v i t y a n d T . c r u z i p a r a s i t e m i a i n d o g s .

D o g s e x a m i n e d b y a g e g r o u p s

A g e s 0-4 5 9 10-14 15 19 T o t a l

# d o g s e x a m i n e d 279 45 12 4 340

# d o g s x e n o p o s . 45 13 6 2 66

# d o g s s e r o p o s . 78 27 8 2 115

P X ('< V" 16.1 28.9 50.0 50.0 19.4

P i (' > )** 28.0 60.0 66.7 50.0 33.8

P x P i1* * 0.58 0.48 0.75 1.0 0.57

(;) P r e v a l e n c e r a t e s of i n f e c t i o n b y x e n o d i a g n o s i s

( # d o g s x e n o p o s . ) ( # d o g s e x a m i n e d )

(' '"') P r e v a l e n c e r a t e s of i n f e c t i o n b y s e r o l o g y ( # d o g s s e r o p o s . )

( # d o g s e x a m i n e d )

(***) P a r a s i t o l o g i c a l s e r o l o g i c a l c o r r e l a t i o n ( # d o g s x e n o p o s . )

( # d o g s s e r o p o s . )

and no differences were observed in the preva-lences of infection by serology (Pi) between ma-les (35.5%) and femama-les (32.2%). No differences

were seen in P i( P e l = 30.0%, P i( T ) = 33.0%, and

P il R ) = 40.2%. T h e P i for the different D

sub-groups classified according to their environment and activity in the house were determined. T h e P i of the hunters and guardians resulted signifi-cantly greater than those of the goaters (P < 0.05), and the P i of the dogs that slept in the houses was significantly greater than of those which slept in the peridomicile (P < 0.05) (Table 1).

The study of the dynamics of infection revea-led that 50% of the serologically reactive D con-tract infection before they reach five years of age. The parasitologic-serological correlation for all the D was of 57.7%, and of 70% for the first year of life, showing a similar tendency to that obser-ved for the age-specific parasite recovery.

F i v e electrocardiograms, either had eviden-ces of conduction disorders, incomplete blockade of the right branch, left anterior hemiblockade, or both. F o u r of the five animals were parasi-temic, all of them with positive serology.

The A . T . I , of 102 houses was of 43 + 42.9 "kissing b u g s " per house. Ninety nine percent of the houses had triatomines in bedrooms (A.T.

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"kis-sing b u g s " in the peridomicile ( A . T . I .p = 28 +

32.3). O n the other hand, out of 66% of the bed-room-insects examined, 30% of them were

infec-ted with T . cruzi (Table 3).

Area R showed distinctive characteristics with respect to infection patterns. Significant differences were observed (P < 0.05) in P x of area R (30.5%) with respect to that of T (17.1%) and of Pe (16.2%) for similar P i in all areas. Further-more, the difference in the percentage of insects

infected with T . cruzi found in the bedrooms of

the R area (39.7%) with respect to those of T (25.2%) and of Pe (27.8%), was significantly rent (P < 0.05) (See Table 3). There were no diffe-rences between the parameters of T and Pe.

D I S C U S S I O N

The subdivision of this area according to in-creasing distances to an urban conglomerate had the purpose to evaluate the influence of the

environment on T . cruzi transmission. A s is

fre-quent in rural areas, a transition of huts to brick houses as the distance to the city diminished, was observed. T a k i n g into a c c o u n t that the highest prevalences of seroreactivity are usually

seen in residents of non-plastered houses1 3

, it was not surprising to observe a characteristic epidemiological profile in this rural area. T h e parameters of the canine population and the

characteristics of infection by T . cruzi in the

rural area showed differences with those of the remaining areas. There was a greater proportion of cubs than adults, a more sedentary popula-tion, higher prevalences of infection as seen by xenodiagnosis in the dogs and the highest

pro-portion of T . cruzi-infected insects in the

bed-rooms. T h e high number of dogs less than one year compared to the rest, is an evidence of the difficulties that this population has to overcome

in the rural area, such as malnutrition, dehydra-tation, parasitism and its consequences, which impinge upon the health of the animals. How-ever, the possibility that in this area, infection

by T . cruzi could well be another cause of the

death of the puppies must be considered.

I n the rural area, significant increases in the number of houses with sedentary residents du-ring the whole year were detected, the migration to the sugar-cane harvest in T u c u m a n is an spo-radic fact, in contrast to what is observed in the periurban area where over 40% of its population has migratory habits. I n a house where tempo-rary migration of its human and animal inhabi-tants occurs, the triatomine population could be modified because of lack of ingesta; however, this hypothesis needs to be confirmed. T h e de-tection of chagasic infection observed in Chilean sedentary paleoindian tribes, which were for-merly nomads and had Bolivia as their

disper-sion center, would support this hypothesis2 1.

T h e highest prevalences of infection as mea-sured by xenodiagnosis in dogs, and the highest proportion of bedroom insects infected with T .

cruzi were observed in the rural area. T h e corre-lation between levels of triatomine infestation and parasitemia detected, agrees with that ob-served in dogs of other endemic areas of Argen-tina2 7- 2 8 and B r a z i l1 4.

It is not possible to infer from this work if

the infectivity by T . cruzi in domicile

triatomi-nes influences the prevalences of infection in dogs or vice versa. However, the influence of this reservoir in the domestic cycle is undeniable, evi-denced by the higher indices of seroreactivity in children who live in houses with infected ani-m a l s1 4

and the high frequency of domiciliary

tria-tomines which feed in dogs2 6 2 8

.

T A B L E 3

Detection of infection by T . cruzi in domiciliary triatomines found in bedrooms.

Area rural (R) transitional (T) periurban (Pe) T o t a l

# houses 22 48 32 102 % of infected bedroom

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I n this work the parasitological-serological correlation goes from 58% in young animals to 100% in senile dogs, as it was also observed in

other areas of Santiago del Estero6. T h i s is unlike

humans where this correlation descends from 100% in children less than four years old to 33%

in adults8, and is an indication of differences

be-tween the parasitological profiles of humans and dogs. Higher chances of reinfection in dogs, due

to their closer contact with the triatomines2 8

, and the peculiar characteristics of their immune system, could be the cause for these differences.

The numeric differences observed between males and females suggest an artificial selection made by their owners, frequent in rural areas. T h e similar prevalences of infection by xeno-diagnosis and serology in both sexes indicate a similar susceptibility to infection, as seen in humans, in contrast to that observed in experi-mental infections of mice with the B r a z i l strain of T . c r u z i1 8 or in certain strains of rats1 9.

The evidence that one out of two houses of the study area had at least one parasitemic dog, justifies the investigation of the infection mecha-nisms of this reservoir, evaluating the incidence

of perinatal1 2 and "contaminant" transmission4.

T h e high proportion of perinatally infected pup

pies studied by M A Z Z A1 2 and the contaminant

mechanisms of infection observed in animals4

bespeak for the evaluation of its influence spe-cially in desinsectized houses.

The unmistakable confirmation that this re-servoir contributes blood and flagellates to the triatomine population, supports the implemen-tation of measures tending to block its influence

by means of the development of v a c c i n e s2 2 or

the use of chemotherapy1 7.

R E S U M O

Infecção natural pelo T r y p a n o s o m a cruzi

em cáes de áreas endêmicas da República Ar-gentina.

Estudou-se a dinâmica populacional e a pre-valência de infecção chagásica de 352 cães viven-do em 108 moradias rurais infestadas por triato¬ míneos. A área foi dividida em três setores de acordo com suas crescentes distâncias em

rela-ção a u m povoado urbano. C a d a animal foi iden-tificado mediante suas características particu-lares, e seus donos deram informações a respeito de seus hábitos. A s prevalências de infecção fo-ram determinadas por sorologia, correlação pa¬ rasitológica-sorológica, percentual de traçados eletrocardiográficos alterados e o percentual de moradias com cães parasitados.

A área rural mostrou um padrão

caracterís-tico de infecção por T . cruzi e observaram-se

diferenças nos parâmetros de população canina em relação às restantes áreas: maior proporção de filhotes, maior população h u m a n a e canina sedentárias, maiores prevalências de infecção por xenodiagnóstico em cães e maior proporção

de barbeiros infectados com T . cruzi nos

cômo-dos da casa.

Supõe-se que as características sedentárias da população h u m a n a desta área rural é funda-mental para a oferta de sangue para as popula-ções triatomíneas, e a elevada porcentagem de cães parasitêmicos dessa área contribui para o

aumento de barbeiros infectados com T. cruzi

encontrados nos quartos de dormir.

A C K N O W L E D G M E N T S

We thank Dr. Roberto C h u i t for his profes-sional help in the area, and Mr. Domingo L u n a and Mr. Griseldo R o l d a n for technical collabo-ration. We also thank Dr. Mirta Carlomagno for editorial assistance. Our deepest thanks go to Dr. Carlos Del Prado for the photographs.

R E F E R E N C E S

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8. H O F F , R . ; M O T T , K . E . ; S I L V A , J . F . ; M E N E Z E S , V . ; H O F F , J . N . ; B A R R E T T , T . V . & S H E R L O C K , I. — P r e v a -l e n c e of p a r a s i t e m i a a n d s e r o r e a c t i v i t y to T . c r u z i i n a r u r a l p o p u l a t i o n of n o r t h e a s t B r a z i l . A m e r . J . t r o p . M e d .

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9. L A U R I C E L L A , M. A . ; W I S N I V E S K Y C O L L I , C ; R U I Z , A . M.; S O L A R Z , N . ; B U J A S , M. A . ; & S E G U R A , E . L . — E s t ú d i o s e r o l ó g i c o d e p o b l a c i o n e s . I n : C O N G R E S O A R G E N T I N O D E P R O T O Z O O L O G Í A y R E U N I Ó N SO¬ B R E E N F E R M E D A D D E C H A G A S , 1., H u e r t a G r a n d e , C ó r d o b a , 1984.

10. L A U R I C E L L A , M. A . ; R I A R T E , A . R . ; L A Z Z A R I , J . ; BA¬ R O U S S E , A . & S E G U R A , E . L . — E n f e r m e d a d d e C h a g a s e n p e r r o s e x p e r i m e n t a l m e n t e i n f e c t a d o s c o n T . c r u z i . M e -d i c i n a ( B . A i r e s ) , 46: 195 200, 1986.

11. M A Z Z A , S . — O b s e r v a c i ó n d e i n f e c c i ó n e s p o n t a n e a d e l p e r r o p o r el S c h i z o t r y p a n u m c r u z i . R e v . S o c . a r g e n t .

B i o l . , 2: 33-41, 1926.

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-N I Ó -N D E L A S O C I E D A D A R G E N T I N A D E P A T O L O G Í A

R E G I O N A L , 9., M e n d o z a . 1935. v . 1, p. 412-417.

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14. M O T T , K . E . ; M O T A , E . A . ; S H E R L O C K , I.; H O F F , R . ; M U N I Z , T . ; O L I V E I R A , T . & D R A P E R , C . C . — T . c r u z i i n f e c t i o n i n . d o g s a n d c a t s a n d h o u s e h o l d r e a c t i v i t y to T . c r u z i i n a r u r a l c o m m u n i t y i n t h e N o r t h e a s t B r a z i l . A m e r . J . t r o p . M e d . H y g . , 2 7 : 1123-1127, 1978.

15. N O R M A S T É C N I C A S Y D E P R O C E D I M I E N T O S P A R A L A L U C H A Q U Í M I C A C O N T R A E L V E C T O R D E L A E N -F E R M E D A D D E C H A G A S . B u e n o s A i r e s , P u b l i c a c i ó n d e l S e r v i c i o N a c i o n a l de C h a g a s d e l a R e p ú b l i c a A r g e n -t i n a , M i n i s -t é r i o d e S a l u d P u b l i c a y M e d i o A m b i e n -t e , 1 (1): 29-34, O c t . , 1983.

16. P A U L O N E , I . ; C H U I T , R . ; P E R E Z , A . ; W I S N I V E S K Y C O L L I , C . & S E G U R A , E . L . — F i e l d r e s e a r c h o n a n e p i d e -m i o l o g i c a l s u r v e i l l a n c e a l t e r n a t i v e of C h a g a s d i s e a s e t r a n s m i s s i o n : t h e P r i m a r y H e a l t h C a r e ( P H C ) s t r a t e g y i n r u r a l a r e a s . R e v . a r g e n t . M i c r o b i o l . , 20 ( s u p p l ) : 103-105,1988.

17. P E R E Z , A . ; L A N S E T T I , J . C ; D E R I S S I O , A . M.; P A U L O N E , I . ; C H U I T , R . & S E G U R A , E . L . — S e g u i m i e n t o l o n g i -t u d i n a l d e l a p o b l a c i ó n d e n i h o s d e 0-5 a ñ o s b a j o v i g i l a n c i a e p i d e m i o l ó g i c a p a r a l a E n f e r m e d a d d e C h a g a s e n T e r m a s de R i o H o n d o , S g o . d e l E s t e r o . I n : C O N G R E S O A R G E N -T I N O D E P R O -T O Z O O L O G Í A Y R E U N I O N S O B R E EN¬ F E R M E D A D D E C H A G A S , 2., L a F a l d a , C o r d o b a , 1987. p. 46.

18. P O S T A N , M.; M C D A N I E L , J . P . & D V O R A K , J . A . — S t u d i e s of T . c r u z i c l o n e s i n i n b r e d m i c e . I I C o u r s e of i n f e c t i o n of C 5 7 B L / 6 m i c e w i t h s i n g l e - c e l l - i s o l a t e d s t o c k s . A m e r . J . t r o p . M e d . H y g . , 33: 236-238, 1984.

19. R E V E L L I , S . S . ; A M E R I O , N . ; M O R E N O , H . S . ; V A L E N ¬ T I , J . L . ; B A L B A R R E Y , H . & M O R I N I , J . C . — E n f e r ¬ m e d a d d e C h a g a s c r ô n i c a e n l a r a t a . C a r a c t e r í s t i c a s s e r o ¬ l ó g i c a s , e l e c t r o c a r d i o g r á f i c a s e h i s t o p a t o l ó g i c a s . M e d i c i -n a ( B . A i r e s ) , 40 ( s u p p l . 1): 69-76, 1980.

20. R O J A S , A . ; S O T E L O , J . M.; V I L L A R R O E L , F . & C O N ¬ T R E R A S , C . M. — L a i m p o r t â n c i a d e l p e r r o y el g a t o e n l a e p i d e m i o l o g i a d e l a E n f e r m e d a d d e C h a g a s . B o l . c h i l . P a r a s i t . , 28: 42-43, 1973.

21. R O T H H A M M E R , F . — C h a g a s ' d i s e a s e i n C h i l e a n m u m ¬ m i e s . P a r a s i t . T o d a y , 1 (1): 3, 1985.

22. R U I Z , A . M.; E S T E V A , M.; R I A R T E , A . ; S U B I A S , E . & S E G U R A , E . L . — i m m u n o p r o t e c t i o n of m i c e a g a i n s t T . c r u z i w i t h a l y o p h i l i z e d f l a g e l l a r f r a c t i o n of t h e p a r a s i t e p l u s a d j u v a n t . I m m u n o l . L e t t . , 12: 1-4, 1986.

23. S O K A L , R . R . & R O H L F , F . J . — I n t r o d u c t i o n to b i o s t a ¬ t i s t i c s . S a n F r a n c i s c o , W . H . F r e e m a n & C o . , 1969.

24. S T R O U T , R . G . — A m e t h o d for c o n c e n t r a t i n g h e m o f l a g ¬ e l l a t e s . J . P a r a s i t . , 48: 100, 1962.

25. V O L L E R , A . ; D R A P E R , C . C ; B I D X E L L , D . E . & B A R ¬ T L E T T , A . — M i c r o p l a t e e n z y m e - l i n k e d i m m u n o s o r b e n t a s s a y for C h a g a s ' d i s e a s e . L a n c e t , 1: 426-428, 1975.

26. W I S N I V E S K Y C O L L I , C ; G U R T L E R , R . E . ; S O L A R Z , N . D . ; S A L O M O N , D . & R U I Z , A . M. — F e e d i n g p a t t e r n s of T . i n f e s t a n s ( H e m i p t e r a : R e d u v i i d a e ) i n r e l a t i o n to t r a n s m i s s i o n of A m e r i c a n T r y p a n o s o m i a s i s i n A r g e n t i n a .

J . m e d . E n t o m o l . , 19: 645-654, 1982.

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28. W I S N I V E S K Y - C O L L I , C ; R U I Z , A . M.; L E D E S M A , O . ; G U R T L E R , R . E . ; L A U R I C E L L A , M. A . ; S A L O M O N , D . O . ; S O L A R Z , N . & S E G U R A , E . L . — E c o l o g i a d o m é s t i c a de l a T r y p a n o s o m i a s i s a m e r i c a n a : p e r f i l a l i m e n t a r i o d e l T . i n f e s t a n s e n u n a r e a r u r a l d e l a p r o v i n c i a de S a n t i a g o

d e l E s t e r o . A r g e n t i n a . R e v . S o c . b r a s . M e d . t r o p . , 20: 31-39, 1987.

Referências

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