Articolul 6 PDF
Articolul 6 PDF
Articolul 6 PDF
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0893-8512/08/$08.00⫹0 doi:10.1128/CMR.00050-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.
INTRODUCTION .......................................................................................................................................................380
Taxonomy of Echinococcus spp...........................................................................................................................................381
Neotropical Species of Echinococcus in the Final Host .....................................................................................381
Characteristics of the Strobilar Stages of E. vogeli and E. oligarthrus............................................................382
The Metacestode of E. vogeli in the Natural Intermediate Host and in Humans .........................................382
Histogenesis and Pathogenesis of the Metacestode of E. vogeli in Polycystic Echinococcosis.....................384
The Metacestode of E. oligarthrus in the Natural Intermediate Host .............................................................384
Histogenesis and Pathogenesis of the Metacestode of E. oligarthrus in Unicystic Echinococcosis .............385
MEDICAL ASPECTS OF NEOTROPICAL ECHINOCOCCOSES ....................................................................385
Clinical Characteristics of Polycystic and Unicystic Echinococcoses..............................................................386
Clinical Characteristics of Polycystic Echinococcosis (E. vogeli) (Types I to V) ...........................................386
Type I....................................................................................................................................................................386
Type II ..................................................................................................................................................................388
Type III.................................................................................................................................................................389
Type IV .................................................................................................................................................................390
Type V...................................................................................................................................................................390
Clinical Characteristics of Unicystic Echinococcosis (E. oligarthrus) (Types VI and VII)...........................391
Type VI .................................................................................................................................................................391
Type VII................................................................................................................................................................391
Consequences of Medical Treatment ...................................................................................................................391
DIAGNOSIS OF POLYCYSTIC ECHINOCOCCOSIS (E. VOGELI).................................................................392
Patients’ Histories...................................................................................................................................................393
Sex and Age Distribution.......................................................................................................................................393
Laboratory Findings ...............................................................................................................................................393
Physical Examination of the Abdomen ................................................................................................................393
Radiological Imaging..............................................................................................................................................393
Serological Tests .....................................................................................................................................................394
Parasitological Diagnosis.......................................................................................................................................395
EPIDEMIOLOGY .......................................................................................................................................................395
Geographical Distribution of Neotropical Echinococcoses ...............................................................................395
Natural Hosts of E. vogeli and E. oligarthrus ......................................................................................................396
CONCLUSIONS .........................................................................................................................................................399
ACKNOWLEDGMENTS ...........................................................................................................................................400
REFERENCES ............................................................................................................................................................400
380
VOL. 21, 2008 NEW ASPECTS OF NEOTROPICAL ECHINOCOCCOSIS 381
FIG. 1. Life cycle of Echinococcus vogeli in neotropical forests and the course of domiciliary transmission to humans.
echinococcosis; E. multilocularis Leuckart 1863, which causes mals of at least eight families (56). A major obstacle to a better
alveolar echinococcosis; and E. vogeli Rausch et Bernstein understanding of the taxonomic status of genotypes of cestodes
1972, which causes polycystic echinococcosis. in the genus Echinococcus has been the lack of investigations
involving experimental infections of ungulates and rodents that
Taxonomy of Echinococcus spp. serve as intermediate hosts. Thus far, no genotype has been
shown to be reproductively isolated, and the status of the
Two species, E. granulosus and E. multilocularis, occur in various nominal taxa therefore remains uncertain.
natural hosts in the northern hemisphere. The former now has
a cosmopolitan distribution in livestock-raising countries, hav-
Neotropical Species of Echinococcus in the Final Host
ing been introduced with animals from Europe beginning in
the early 16th century (55). The taxonomy of cestodes of the The two neotropical species and their respective hosts ap-
genus Echinococcus has been complicated by typological de- pear also to represent assemblages of ancient origin, as indi-
scriptions (1) of numerous taxa, the majority now recognized cated by the typical occurrence of their metacestodes in hys-
as E. granulosus. tricognath rodents. Those rodents were the dominant small
Several genotypes, ostensibly having metacestodes adapted terrestrial herbivores in South America by the Miocene epoch,
to the various species of domestic ungulates, have been distin- from ca. 22 million to 5 million years BP (25). The family
guished by molecular-genetic methods (84), but otherwise they Taeniidae is represented in South America by a few species of
are morphologically and biologically like E. granulosus. Such the genus Taenia, in addition to the indigenous E. vogeli and E.
genotypes appear to have arisen after the domestication of oligarthrus. During the Pliocene epoch, formation of the Pan-
ungulates, beginning about 8,000 years before the present (BP) amanian isthmus enabled numerous faunal exchanges between
(35). Echinococcus granulosus and its natural hosts (wolf [Canis North America and South America; various species of Taenia,
lupus L.] and deer [family Cervidae]) appear to represent an but none of Echinococcus, dispersed into South America with
ancient assemblage in the holarctic zones of tundra and taiga. their hosts by way of the isthmus of Panama. The cougar, Puma
By contrast, E. multilocularis shows little genetic variation (68), concolor (L.), for example, of North American origin and now
but it also, like E. granulosus, exhibits morphological variation having an extensive geographic range in South America (90),
in the strobila, and host-induced variation in the metacestode harbors at least one nearctic species of Taenia and has become
occurs (62). The recently described E. shiquicus Xiao et al. a common final host of the neotropical E. oligarthrus. It is
2005 resembles E. multilocularis morphologically; the metaces- evident that E. oligarthrus is capable of development in any
tode was found in pikas (family Ochotonidae) and differs mor- species of felid in the neotropical region and probably in the
phologically from that developing in the typical intermediate Nearctic as well.
hosts of E. multilocularis, rodents of the family Arvicolidae. Of the four species of Echinococcus considered in this re-
Such rodents are sympatric with pikas, from which the meta- view, only E. oligarthrus has wild cats (Felidae) as a final host
cestode of E. shiquicus was studied. Of the four species of (60). The strobilar stages of the three others occur in carni-
Echinococcus recognized here, the metacestode of E. mul- vores of the family Canidae, each in a characteristic species of
tilocularis exhibits the least degree of host specificity, having final host under natural conditions, but the domestic dog, Ca-
been recorded in natural infections in small, herbivorous mam- nis lupus forma familiaris, can readily replace their natural final
382 D’ALESSANDRO AND RAUSCH CLIN. MICROBIOL. REV.
FIG. 3. The paca, intermediate host of Echinococcus vogeli. (Cour- FIG. 5. Strobilar stage of Echinococcus vogeli (length, 12 mm) from
tesy of Ignacio Borero, University del Valle, Cali, Colombia.) an experimentally infected domestic dog.
VOL. 21, 2008 NEW ASPECTS OF NEOTROPICAL ECHINOCOCCOSIS 383
vesicles, isolated or frequently contiguous. In two animals, FIG. 8. Vesicles of Echinococcus vogeli in the mesentery near the
metacestodes occurred additionally in the hepatic ligament caecum in a naturally infected paca, Carimagua, Colombia.
and in the mesentery near the cecum. The greatest numbers
were in the left and median lobes, the largest of the four lobes
making up the liver of the paca. They were situated at all levels Brood capsules each contained 10 to 480 (average, 81) proto-
within the hepatic parenchyma but mostly were near the sur- scoleces (64). When fully developed, protoscoleces were 158 to
face, partially covered by Glisson’s capsule (64), there protrud- 203 m in length by 108 to 145 m in diameter (average, 175
ing slightly above the hepatic surface (Fig. 6). The metaces- by 133 m).
todes were white and somewhat translucent, contrasting As seen in thick sections of liver, transected metacestodes of
markedly with the dark color of the liver. Within the paren- E. vogeli, when occurring singly, showed no indication of ex-
chyma, they were surrounded by connective tissue 70 to 250 ogenous proliferation. When two or more were contiguous,
m in thickness, the outer surface of which formed a boundary their separate boundaries usually could be discerned, and each
distinct from the unaffected hepatic tissue. When partially ex- appeared to have arisen from a single egg. The findings indi-
posed under Glisson’s capsule, the covering layer over the cated that proliferation in the liver does not occur in the
metacestode was only 20 to 30 m in thickness. natural intermediate host. However, in one paca, vesicles in-
When transected in situ, the metacestodes were seen to be volving mesentery and cecum formed a mass that could have
enclosed within a laminated membrane variable in thickness arisen by means of proliferation (Fig. 8).
and often exhibiting folding. Intrusions of laminated mem- A difference in the developmental process and its conse-
brane usually produce a few trabeculae, forming chambers quences between the natural intermediate hosts and humans is
lined by germinal tissue from which the brood capsules arose not unique to E. vogeli, but that relationship is like that per-
(Fig. 7). Brood capsules were large and relatively few, more or taining to the metacestode of E. multilocularis. When voles
less spherical to pyriform, with the smaller end of each at- ingest a few eggs of E. multilocularis, development of the meta-
tached to the germinal tissue. They range from 424 m to l.56 cestode takes place only in the liver and infective protoscoleces
mm in length by 389 m to 1.45 mm in maximal diameter. are produced within 2 to 3 months; when infections are severe,
more hepatic lobes are affected, and exogenous proliferation
of germinal tissue may result in formation of masses of meta-
cestode in the peritoneal cavity but other organs usually are
not invaded.
The pattern of development of E. multilocularis is also dif-
ferent in the human host. Therein, development takes place in
the liver, where the membranes of the metacestode continue to
proliferate for the life of the host but protoscoleces are rarely
produced. Also in the human host, the membranes of the
metacestode proliferate only around the periphery of the le-
sion; the internal bulk of the lesion is replaced by connective
tissue in which areas of necrosis usually develop. Marked hep-
atomegaly is characteristic, and diffuse calcification is typical in
cases with advanced disease. The metacestode of E. multilocu-
laris may extend into contiguous organs (e.g., kidney); metas-
FIG. 7. Transected metacestode of Echinococcus vogeli, showing
tasis to distant sites (e.g., lung or brain) sometimes may occur.
brood capsules and other tissues, in the liver of a naturally infected The metacestodes of E. granulosus and, evidently, of E. oli-
paca, El Porvenir, Colombia. garthrus are alike in that their developments in the natural
384 D’ALESSANDRO AND RAUSCH CLIN. MICROBIOL. REV.
observed, proliferation did not occur. In contrast to that of E. hemisphere, and it is widely present in Eurasia and in north-
vogeli, in which brood capsules are few and scattered (Fig. 7), ern North America. An atypical form of the metacestode of
the germinal tissue in the metacestode of E. oligarthrus usually E. granulosus in the liver of ungulates, characterized by
is covered by brood capsules that, according to our observa- small vesicles without protoscoleces in a dense matrix of
tions of sections, often form contiguous layers that may fill connective tissue, often has been confused with the meta-
most of the lumen. The protoscoleces are somewhat larger cestode of E. multilocularis, but its identity has been clearly
than those of E. vogeli, having a diameter of 218 to 230 m in established (47, 89, 93). Vogel proposed that the atypical
spiny rats (78). The rostellar hooks of the unicystic metaces- forms of E. granulosus in the liver of ungulates be designated
tode are consistently shorter than those of E. vogeli, and in that “multicystic” (89).
stage, the two species are distinguished as well by strongly Similar multicystic metacestodes have rarely been reported
defined differences in the shape of the hooks (65). Rodriguez in humans but have been the basis of considerable confusion in
et al. (70) have given a detailed description of the metacestode South America, where their occurrence has been taken to lend
of E. oligarthrus from the spiny rat Proechimys guairae. support to the “unicist” concept that one species of Echino-
coccus (E. granulosus) causes both of the aforementioned
forms of echinococcosis, compared with the “dualist” view
Histogenesis and Pathogenesis of the Metacestode of
(now recognized as valid) that two species of Echinococcus are
E. oligarthrus in Unicystic Echinococcosis
involved (33, 88, 94). In addition to the possible occurrence of
Like those of E. granulosus, the oncospheres of E. oligarthrus the multicystic form of E. granulosus in humans in South
may pass through the liver and be transported by the systemic America, such cases, considered in retrospect, might have been
circulation to various loci in natural, as well as atypical, inter- caused by E. vogeli or, less likely, by E. oligarthrus. Some alve-
mediate hosts. At the present, in humans, only three cases of olar lesions have been described in Argentina and reported to
unicystic echinococcosis have been recognized; thus, the po- have occurred in humans in Chile and Uruguay. Because the
tential range of loci in the human body is not known. In anomalous multicystic metacestode of E. granulosus does not
humans, the metacestode of E. oligarthrus has been described produce protoscoleces, rostellar hooks necessary for identifi-
as a more or less spherical structure that enlarges concentri- cation have not been available. As a consequence, we do not
cally, and pathogenesis appears to result from pressure effects know if the neotropical species of Echinococcus occur in those
caused by its expansion. Two of the three known cases involved countries (19, 22, 85, 86, 87, 88).
retro-ocular location of single vesicles, with production of sig- In Costa Rica, a human case of echinococcosis in the liver
nificant exophthalmos (4, 39). In the third case, the autopsy of was studied and tentatively diagnosed as being due to E. oli-
a patient who died of tetanus at 70 years of age revealed two garthrus, probably because that species had been found in a
metacestodes, each about 1.5 cm in diameter, in the left wall of Costa Rican cougar (6). The patient was an immigrant who had
the ventricle (16). In those patients, development of the meta- spent 27 of his 53 years in Spain. Later on, the study of the
cestode was evidently normal, and the rostellar hooks of pro- hooks demonstrated that he was infected by E. granulosus, but
toscoleces provided the means of identification of the organism the metacestode morphologically somewhat resembled a mul-
as E. oligarthrus. ticystic echinococcus. One of us (A.D.) studied the hooks of
the protoscoleces and was in agreement with R. Arroyo and R.
Brenes, who kindly sent samples of the specimens and had
MEDICAL ASPECTS OF NEOTROPICAL
recognized that the infection was due to E. granulosus (R.
ECHINOCOCCOSES
Arroyo, personal communication [7 April 1993]).
Polycystic and unicystic echinococcoses are helminthic in- D’Alessandro et al. (17) reported cases of polycystic echi-
fections that occur exclusively in rural areas of the Neotro- nococcosis in persons from four countries (Colombia, Ecua-
pics (60). As indicated earlier in this article, E. granulosus, dor, Panama, and Venezuela), and these cases involved tumor-
the cause of cystic echinococcosis, occurs widely in the like masses in the liver. The patients had resections or biopsies
southern cone of South America, particularly in sheep and of the lesions. The presurgical diagnoses were cancer of the
other ungulates in areas in which livestock is raised in Uru- gall bladder with metastases, tumor, abscess or hepatic cirrho-
guay, Argentina, Chile, the Andean regions of Peru and sis, gastric tumor, and chondrosarcoma of a rib. The clinical
Bolivia, and the state of Rio Grande do Sul in Brazil. On the and surgical diagnoses were found by pathologists to be erro-
other hand, autochthonous human cases of cystic echino- neous. Those and later reports on other autochthonous cases
coccosis are rare in other South American countries, al- described alveolar, multicystic, or multilocular echinococcosis,
though dogs and domestic ungulates may sometimes be in- due to E. granulosus or E. multilocularis and, only more re-
fected. The reason for this situation is not clear, but perhaps cently, due to E. oligarthrus. However, experimental infection
epidemiological conditions do not favor the infection in of cats and dogs, the only way to obtain the cestodes at the
humans, or less likely, the genotype of the cestode in those strobilar stage at the time, was not attempted. D’Alessandro et
regions does not readily infect humans. In those areas, al. (14, 17, 18) and Rausch et al. (65) were able to establish the
metacestodes of E. granulosus usually are found to occur in infections in such mammals, using metacestodes from humans
immigrants from other countries, especially from Europe. and other animals from Colombia. Findings from experimental
Human cases of infection by the two neotropical species of animals established that the metacestodes developing in hu-
Echinococcus are seen mostly where E. granulosus is not mans were polycystic and were that of E. vogeli and thus rep-
endemic. E. multilocularis, the etiologic agent of alveolar resented a new parasitic infection for humans. In addition, they
echinococcosis, is limited in occurrence to the northern established the criteria for not only the differential diagnosis of
386 D’ALESSANDRO AND RAUSCH CLIN. MICROBIOL. REV.
TABLE 1. Frequency of clinical characteristics of polycystic and unicystic neotropical echinococcoses according to species
Polycystic
I Cysts in the liver and abdominal cavity 19 11 0 1 30 (37)
II Cysts in the liver and abdominal cavity plus hepatic insufficiency 9 12 0 0 21 (26)
III Cysts in the liver and lung/chest 4 7 0 0 11 (14)
IV Cysts only in the mesentery of the intestine or of the stomach 9 4 0 0 13 (16)
V Calcified cysts in the liver and lungb 1 2 0 0 3 (4)
Unicystic
VI Cysts only in the orbit 0 0 2 0 2 (2)
VII Cysts only in the heart 0 0 1 0 1 (1)
Total 42 36 3 1 81 (100)
a
E. cf. vogeli causes infections with polycystic lesions but with no hooks found.
b
The total number of these patients with liver cysts was 66/81 (81%), and the number with lung cysts was 11/81 (14%).
c
Excludes the E. granulosus case.
infection with the two neotropical species, E. vogeli and E. to consider that some of those persons from areas in which the
oligarthrus, but also criteria separating the causative agents infection is endemic may have had asymptomatic infections by
from the other two recognized species, E. granulosus and E. E. vogeli. Therefore, the number of infected persons in the
multilocularis. neotropical countries may be 232 and, in Brazil alone, 160 (52;
Fortunately, in recent years, investigators have become in- U. Meneghelli, personal communication [2006]). Forty Brazil-
creasingly aware of and interested in the two zoonoses caused ian cases of polycystic echinococcosis occurring in the states of
by the neotropical cestodes and have improved their capabil- Para and Amapa, in the western Amazonian region, were sum-
ities for recognition and diagnosis of such infections. Due to its marized by Soares et al. (76). Included in that group were 14
frequency, polycystic echinococcosis is no longer a medical cases reported by Orlando Fonseca and Aurelio Costa in 1995
curiosity, and it should be considered in the differential diag- (12).
nosis of polycystic masses in humans. On the other hand, As of March 2007, the clinical information from 81 patients
human infections with the unicystic metacestode of E. oliga- is available among the 172 known cases (Table 1). By far, the
rthrus have been rarely diagnosed. liver was the organ most frequently affected. Indeed, in 81% of
the cases, metacestodes were found in the liver alone or with
vesicles situated in the abdomen, in the liver and the lungs/
Clinical Characteristics of Polycystic and
pleural cavities, or only as calcified vesicles in the liver. Organs
Unicystic Echinococcoses
involved in the abdomen included the diaphragm, spleen, pan-
The clinical characteristics of polycystic echinococcosis in creas, omentum, mesenteries, rectal-vesical sac, ovaries,
patients depend on the location of the metacestode as well as uterus, abdominal wall, psoas muscle, and vertebra. In the
the extent of invasion of tissues, particularly the liver (Table 1). chest, the lungs were infiltrated in 11 (14%) cases; also in-
D’Alessandro et al. (17) published observations on all re- volved were ribs, intercostals and subscapular muscle, pleura,
ported or known cases of polycystic echinococcosis. In addi- pericardium, auricle, vena cava, and other large mediastinal
tion, D’Alessandro invited senior parasitologists of Central vessels. The remaining 13 polycystic lesions were located only
American and South American countries to report, during in the mesentery. Of unicystic lesions, due to metacestodes of
various meetings of the Federación Latinoamericana de Para- E. oligarthrus, one was located in the heart and two were in the
sitologos, the status of echinococcosis in their countries, in orbit. Those single-site infections were reported as being not
particular concerning polycystic echinococcosis in humans and concomitant or secondary to any other lesions located else-
other animals. Their contributions have been reported (12). where in the body.
The present report includes all data, published and unpub-
lished, obtained from reliable sources since that time. Clinical Characteristics of Polycystic Echinococcosis
The total number of known cases of neotropical echinococ- (E. vogeli) (Types I to V)
cosis, as of March 2007, is 172. Included in that number are 18
new cases observed by Ulysses Meneghelli (personal commu- Examination of the patients’ case histories offered the op-
nication [October 2006]). In addition, two serological surveys portunity to group them in types so that frequency of clinical
in Brazil demonstrated that 41 of 1,064 and 19 of 40 persons features, severity of the illness, complications, types of treat-
(total, 60 of 1,104 [5%]) showed antibodies for Echinococcus in ments used, and mortality could be better assessed.
the counterelectrophoresis test. Whether all those 60 persons Type I. The most common type of presentation, type I,
had asymptomatic echinococcosis is not known, because one included lesions in the liver (Fig. 11) and in the abdomen, seen
single test may overlook or involve a cross-reaction with other in 30 of 81 (37%) cases (Table 1). The patients presented with
conditions or parasitic infections. Nonetheless, it seems logical palpable, hard, and rounded masses, painful or not painful,
VOL. 21, 2008 NEW ASPECTS OF NEOTROPICAL ECHINOCOCCOSIS 387
TABLE 2. Management and treatment of 78 cases of polycystic echinococcosis and 3 cases of unicystic echinococcosis with sufficient information
No. of patients with indicated treatment or outcome No. of patients
Clinical disease who died after
Surgery
typea Lapa/biopsyb
Albendazole Died of Autopsy Calcified Total (% of all study
Survived Died alone PEc finding cysts patients) completion
I 7 17 0 5 1 30 (37) 1
II 0 8 4 4 4 1 21 (26) 5
III 0 3 1 3 3 1 11 (14) 3
IV 3 7 0 1 1 1 13 (16)
V 3 3 (4)
VI 2 (2)
VII 1 (1)
circulation compatible with portal hypertension; she died at tomy, after which albendazole was administered for a period of
home in 1999. Serological tests (enzyme-linked immunosor- 6 months. At 11 months following surgery, examination by
bent assay [ELISA] and immunoblot [IB]) were always positive means of CT revealed no evidence of recurrence. Cures were
for echinococcosis. also reported by Chigot et al. (10), who followed a similar
Ghiotti Siqueira et al. (29) evidently cured a patient from course of treatment, including CT scanning, and the patient
whom all metacestodes in the liver, omentum, and peritoneum remained well for at least 3 years. In another series, 1 patient
were removed by means of partial hepatectomy and omentec- died, but 16 improved after surgery (76).
Chemotherapy sometimes has been used in the treatment of
polycystic echinococcosis. In one series of patients, five were
treated with albendazole alone, with apparently favorable re-
sults (76). The courses of treatment were reportedly for dif-
ferent lengths of time and with different degrees of success. It
was not known if the patients followed the regimen of treat-
ment, and usually they did not continue to take the drug or
only attended a clinic and returned home. In most cases it was
not possible to determine the ultimate fate of those individuals.
Type II. The second type of clinical presentation, type II, is
similar to type I but includes signs that the vesicles are located
close to and compressing the portal blood supply and/or the
biliary system of the liver. That compression evoked jaundice,
only after he became icteric or had some other disorder. He series (49), had three small cysts in the intestinal mesenteries
was killed in a street accident. The autopsy was conducted by that were removed surgically at the Disconessen Hospital in
a medical examiner. It was not possible to obtain information Paramaribo in 1985. The diagnosis was echinococcosis. She
about the lesions caused by E. vogeli. voluntarily attended the clinic, had been well after surgery, and
A relevant case history of one patient who died in a surgical had taken mebendazole (3 g/day) for three months. At the time
accident also is presented here. This is a remarkable case of her attendance at the clinic she was well, her serology (by
history of a patient whose disease presentation was classified as ELISA and IB) was negative, and an ultrasonic examination
type III; one of us (A.D.) had the opportunity to meet this also was negative. She had been well for 14 years, and it was
patient. At the end of 1983, while in Bogota, A.D. was invited concluded that she had been cured (48, 49). This case also was
to discuss with a group of colleagues the case of a Colombian exceptional because she could be located and traced. The fates
woman of about 35 years of age with polycystic echinococcosis. of many of the humans suffering from polycystic echinococco-
The diagnosis had been made by means of a liver biopsy and a sis considered in this review are unknown, because many re-
detailed study of thoracic images, in particular of the large
turned to their homes from the modern hospitals where they
vessels and the heart. The discussion was to determine whether
had undergone treatment.
surgery might be indicated or beneficial to the patient. A.D.’s
Another case history of a type IV patient is given here (12).
opinion was that surgery would be too risky, particularly to a
A 78-year-old man evaluated in Colombia complained of a
patient who at the time was asymptomatic. After the meeting,
painful mass in the left hemiabdomen. He was diagnosed as
A.D. was able to talk with the patient, who flatly refused to
undergo surgery, because she had been well since the hepatic possibly having an echinococcal cyst of the spleen (based on a
biopsy and was asymptomatic. Twelve years later, in 1996, it calcification observed in the roentgenogram) or a leiomyoma
was learned that she was working at a local hospital and was of the small intestine. At surgery, the mass was found to be
still asymptomatic. The case was presented again at a medical attached to the posterior wall of the abdomen, surrounded by
meeting, and a new set of thoracic images revealed ever-en- a loop of the small intestine. The mass, along with 90 cm of the
larging lesions in the heart and in the large vessels in the intestine, was resected, but portions of cysts remained attached
mediastinum. It was strongly recommended that the patient to the base of the mesenteries; also, fluid from the mass was
should have surgery and that a description of the unique case spilled into the abdominal cavity. The etiologic agent was iden-
should be published. A year later, it was learned that the tified as E. vogeli. The patient was well for seven months and
patient had developed congestive heart failure and had gone to then died of a myocardial infarction.
a different hospital, where an auricular resection had been Type V. Calcified cysts of the liver and mesentery are cate-
successfully performed. The operation was well tolerated and gorized as type V. Three cases of dead and calcified cysts, two
the patient had become asymptomatic. She was convinced, resembling infections by E. vogeli and the third caused by E.
however, that a complete cure would depend on the excision of vogeli, have been reported. Meneghelli et al. (45) reported two
the hepatic lesion. In 1998, during surgery to remove the he- Brazilian cases of hepatic calcification that resembled lesions
patic lesion, the patient died of a surgical accident. A complete in other patients having polycystic echinococcosis. R. L.
report of the case would no doubt be informative. Rausch thought that the clinical, epidemiological, and radio-
Type IV. In the type IV patients, lesions were limited to the logical data provided were compatible with the suggested di-
mesentery of the small or large intestine (and in one case, in agnosis. One of the two patients had presented with abdominal
that of the stomach) of 13 (16%) of the 78 patients. The liver distention that had been attributed to calculus cholecystitis,
and other organs were reported to be free of metacestodes. but at surgery, the gall bladder was normal. The thoracic X
The lesions and pain were centrally located in the abdomen, ray revealed small, calcified nodules in the lungs and a large
and at surgery, the vesicles in the mesenteries could be excised, conglomeration of cysts particularly at the margin of the
sometimes along with portions of the intestine surrounding the liver. The second patient was asymptomatic but had similar
cystic mass. Surgery was well tolerated by seven patients, but
hepatic calcifications. He had lived in rural areas, was fa-
for three, only a biopsy specimen could be obtained because
miliar with pacas, and always had kept dogs. His case was
the metacestode involved large vessels, making surgery too risky.
considered to be similar to that of the first type V patient
In some of the cases involving operations, portions of the poly-
described.
cystic mass remained attached to the posterior wall of the abdo-
The third case was reported by Moraes et al. (46). A calcified
men, too close to vessels to attempt removal. All were treated
with albendazole. One was considered cured after surgery and a mass situated in the mesentery was discovered by X ray of the
second after two years of albendazole treatment alone (44). lumbar region for evaluation of possible prolapse of an inter-
Nine cases of polycystic echinococcosis recently were re- vertebral disk. The cystic structure was calcified, but some
ported in Suriname. In four of the nine patients, the metaces- rostellar hooks were found in the mass after its surgical re-
todes involved the intestinal mesentery (4, 48, 49). In 1999, the moval, permitting identification of E. vogeli.
late Beltus Oostburg (University of Suriname in Paramaribo) Those three cases, involving dead metacestodes of E. vogeli,
organized a field trip to visit each of the areas of residence of illustrate that some patients, when infected, exhibit an unusual
the patients mentioned above to determine the outcome of tissue response. Total calcification of the metacestodes and their
their illness. Fortunately, one of the patients had attended the presence only in the mesenteries, may be indicative of a defensive
clinic organized for the purpose. Her case history is presented host response to infection by E. vogeli. Such a relationship be-
here. tween the cestode and the host has been explored already in
A 25-year-old Amerindian woman, case 2 of the Suriname human infections caused by E. multilocularis (30, 32).
VOL. 21, 2008 NEW ASPECTS OF NEOTROPICAL ECHINOCOCCOSIS 391
TABLE 3. Outcome of 78 human cases of polycystic echinococcosis tion in the number and size of cysts may be evident. Abdominal
No. (%) pain or respiratory signs may disappear in days or weeks. The
Outcome or parameter
of cases use of mebendazole has been limited, because it is less soluble
Uncomplicated surgery ...................................................................................35 (45) (26, 54, 66).
Death due to surgical accident ...................................................................... 5 (6) To summarize Table 2 and Table 3, 23 (29%) of 78 patients
Death due to polycystic echinococcosis during the
study and after the study ended ............................................................18 (23) died. Mortality by type of polycystic echinococcosis was as
Total mortality .................................................................................................23 (29) follows: one patient, four patients, three patients, and one
Treatment with albendazole alone................................................................13 (16)
Success (Meneghelli et al., 1992 关44兴) ...................................................... 6a patient had types I, II, III, and IV, respectively. Nine patients
No action on cysts (Almeida et al., 1997 关2兴).......................................... 1/1 died after the study was completed; five of them were had type
Improved symptoms (Pastora et al., 2003 关52兴) ...................................... 2/2
Improvement/US negative at 1 yr (Pieres et al. 关53兴) ............................ 1/1 II, the category with highest mortality, probably due to hepatic
Improvement (Soares et al., 2004 关76兴).................................................... 5/5b failure and its complications. The only patients most probably
cured were treated surgically in combination with chemother-
Total cured ....................................................................................................... 5 (6)
Total nondead cases........................................................................................59 (76) apy (albendazole). Apparently, however, albendazole alone
a
was parasitostatic against the metacestode of E. vogeli. As a
Two cases achieved partial success (one later died, one was albendazole
resistant), and four achieved full success (patients did not complete follow-up). consequence of past experience, we learned that patients are
b
Patients did not complete follow-up. best handled by surgical intervention followed by a few weeks
of therapy with albendazole. When the invasion by the meta-
cestode involves essential organs or especially vulnerable parts
cosis, those who had died from E. vogeli infections; the confu- of organs, the judgment of the surgeon must determine
sion has been recognized and corrected. whether to leave portions of the metacestode and continue
Of the 13 patients treated only with albendazole, results for therapy with albendazole or, in the future, perhaps to admin-
the first six were reported as partially or wholly successful. ister other drugs that reduce the invasiveness or are para-
Meneghelli et al. (44) had followed them for 10 to 30 months, sitocidal for the metacestode. Liver transplant has also been
the elapsed time now being about 15 years. To obtain addi- considered as a possibility (44).
tional information, we contacted Ulysses Meneghelli (personal We consider that the metacestode of E. oligarthrus is uni-
correspondence [27 October 2006]). Unfortunately, he had lost cystic, single or multiple (when multiple, each cyst is separate
contact with all but two patients. One had died of hemorrhage and independent), and that it does not proliferate in the hu-
due to the rupture of esophageal varices, and the second had man host but that its structure in humans is evidently identical
active polycystic echinococcosis that did not respond to che- with that in the natural intermediate host (see above). Micro-
motherapy with albendazole. scopic and macroscopic findings from the three known cases of
The observations from the other investigations listed in Ta- unicystic echinococcosis were unlike those from cases of infec-
ble 3 indicated results of albendazole treatment similar to tion by E. vogeli. Anatomically, the unicystic metacestode ex-
those of Meneghelli et al.: diminished size of the metacestodes hibits a quite different arrangement of brood capsules, and of
and clinical improvement in the patient. It seems therefore course, the size and form of rostellar hooks of protoscoleces
that the drug is not parasitocidal but rather parasitostatic. are diagnostic. Only a few metacestodes of E. oligarthrus, from
Nonetheless, it may be used to ameliorate the overall condition a cardiac infection in one individual, have been studied. One
of patients, both pre- and postsurgery. The experience gained cannot certainly predict that lesions of long standing may not
during the last 10 years indicates that surgery is a very impor- exhibit some greater degree of invasiveness, or other E. vogeli-
tant part of treatment for patients who can tolerate the pro- like characteristics in the human host, but interspecific simi-
cedure (depending on age, general health, and willingness to larities of such magnitude would not be expected to occur
undergo the operation, etc.). In the group of patients evaluated among species of Echinococcus.
in this review, surgery was carried out in almost half of the 78 E. vogeli (and evidently E. oligarthrus) is less organ-specific
cases surveyed; only five patients died of surgical accident (as than is the metacestode of E. multilocularis, which usually
mentioned above). The only five patients that seem to have remains localized in the liver. E. multilocularis undergoes in-
been cured were treated surgically with the additional chemo- trahepatic proliferation, typically not producing protoscoleces
therapy with albendazole. CT scan and US, performed after in the human host; extension into the peritoneal cavity does
treatment was terminated, were negative (10, 29, 42, 44, not occur, but contiguous organs (kidney) may be invaded, and
49, 53). occasionally metastasis to lung or brain may occur. E. vogeli
Albendazole has been administered at a dosage of 10 mg/kg appears to be the most pathogenic of the four species of the
of body weight/day, divided into two or three doses daily. The genus Echinococcus.
usual schedule has been three months of treatment with a
2-week interval between months, but higher dosages have been DIAGNOSIS OF POLYCYSTIC ECHINOCOCCOSIS
used, as well as longer treatment with no interruptions. Side (E. VOGELI)
effects discerned have included increased aminotransferase,
leucopenia, proteinuria, alopecia, gastrointestinal symptoms, Before this illness was recognized as being due to a parasitic
and allergic reactions. Such side effects were transitory and infection, the intra-abdominal masses were erroneously con-
disappeared if the drug was discontinued and treatment could sidered to represent a variety of disorders, including hepatic
then be restarted with no ill effects. Early during treatment, tumor, abscess, cirrhosis or cholecystitis, gall bladder cancer,
appetite improved, temperature was reduced, and general mesenteric tumor, and costal chondrosarcoma (17). With mod-
well-being improved. After three weeks of treatment, reduc- ern diagnostic methods, the recognition of polycystic echino-
VOL. 21, 2008 NEW ASPECTS OF NEOTROPICAL ECHINOCOCCOSIS 393
coccosis has been greatly facilitated. Moreover, with an in- reported in about 21% of cases, ranging from 9 to 28%, but it
creasing number of published reports concerning this disease, is not considered to have specific diagnostic value.
medical personnel in tropical areas, as in Colombia and more
recently in Brazil, have been keenly interested in undertaking Physical Examination of the Abdomen
epidemiological surveys (51, 69).
In most instances, the patients affected with polycystic echi-
nococcosis consult for abdominal pain and have recognized the
Patients’ Histories presence of a mass in the abdomen close to the liver. Hepa-
Geographical origin of the patients is very important. They tomegaly was usually present because that organ was certainly
typically are born, or have lived for prolonged periods, in rural involved in 80% of cases of polycystic echinococcosis. When
tropical areas of continental South America, particularly in the metacestode is located in the mesentery, it usually can be
regions with past or present abundance of wildlife. Familiarity palpated as a mass separate from the liver.
with pacas, hunting pacas, knowledge of possible presence of
“water vesicles” in their livers, and whether domestic dogs Radiological Imaging
were fed viscera of pacas are demographic data that are very
useful to the clinician in reaching a correct diagnosis. Pro- With the help of the newer radiological techniques, US and
longed contact with domestic dogs is equally important. (It was CT, the tridimensional form of the metacestode becomes vis-
mentioned earlier that neotropical echinococcosis occurs out- ible, making possible the detection of its polycystic character,
side the geographical area of transmission of E. granulosus to which was not demonstrable by palpation and simple X ray
humans.) only. As a consequence, the differential diagnoses became less
complicated and diagnosis required consideration of fewer ill-
nesses. (Definitive diagnosis, however, is accomplished by
Sex and Age Distribution study of the metacestode itself, obtained by means of biopsy,
surgery, or autopsy.) A simple X ray may show the parasitic
The number of cases that has been published and those mass and any calcifications in the parasite suggestive of echi-
findings from reliable sources make a total of 172. Those for nococcosis. Calcifications are annular, 2 to 3 cm in diameter,
which information is sufficient number 81. Of those cases, 45% with a radiodense halo and a clear center. They are located
were males and 55% were females. The median age was 43 within the polycystic lesions in the liver or elsewhere in the
years. That figure is the same as that obtained in our previous abdomen if there are extensions into other organs (Fig. 14 and
review of cases 10 years ago. Ages of patients ranged from 6 to 18). Initially, we used simple tomography that could show the
77 years. The youngest age group, 6 to 22 years, made up 16% lobulated character of lesions.
of the total. The youngest patient from whom data were re- US of the polycystic lesions shows multiple rounded, uniloc-
corded was 6 years old; a 12-year-old child died of portal ular, anechoid formations with regular walls. That picture by
hypertension 1.7 years after the onset of symptoms (26). Of the itself does not provide the diagnosis of echinococcosis but is
81 patients for whom adequate information is available, 6, 12, useful in assessing serological findings. For those reasons, US
16, 19, 17, 4, and 5 patients were in the first, second, third, has become important in field studies of human populations at
fourth, fifth, sixth, and seventh decades of life, respectively. the time of confirming serological tests. In surveys of popula-
Most of the patients infected with E. vogeli were born and tions, US is considered to be more accurate than serology (27,
had lived all their lives in rural tropical areas of Central Amer- 75). Portable equipment is available at affordable prices, and
ica and South America where wildlife was abundant, and it was therefore, US is also being used in developing countries in-
impossible to determine the duration of their infection. If the stead of the much more expensive apparatus for CT.
infected individual had moved permanently to a city dwelling, CT scans show multiple, hypodense, cystic structure, round
it was possible to determine the approximate age of the Echi- or ovoid, of various sizes, often coalescent in liver, spleen,
nococcus infection, which, for three of our patients, were 12, pancreas, omentum, pelvis, and lung, etc. Calcifications of vari-
25, or 60 years. Symptoms had appeared at 2, 10, and 36 years able appearance, usually solid and small but at times large and
of age, respectively, after the patients left the rural area. The bizarre, can be detected and help to make an accurate diag-
median age at diagnosis of alveolar echinococcosis (E. nosis. Meneghelli et al. (44, 45) published excellent US and CT
multilocularis) was 53 years (91). photos of Brazilian patients with polycystic echinococcosis.
Also included in their publications are images showing changes
Laboratory Findings in size and number of cysts following albendazole treatment
(Fig. 22). CT scanning is expensive but is the best procedure, so
General observations, including our own, indicate that lab- far, for differential diagnosis of polycystic lesions (cystic echi-
oratory findings, outside of the obvious significance of mor- nococcosis, polycystic liver and kidney disease, primary or met-
phological features of the cestodes, are not useful in the diag- astatic malignancies, and hepatic amebic abscess [15], pancre-
nosis of neotropical echinococcoses. However, it is important atic epithelioma, ovarian cyst and, in the lungs, dermatoid cysts
to assess possible injury to the liver when infiltration of the with inclusions, neurinoma, aortic aneurism, primary bronchial
biliary system may be diagnosed. Increases of alkaline phos- carcinoma, metastatic sarcoma, seminoma, and lesions in ovary
phatase, bilirubin, liver transaminases, and gamma globulin and uterus, etc.) and for assessment of albendazole treatment.
and diminished albumen and hemoglobin are common findings We are not aware of reports on the use of magnetic resonance
in cases of polycystic echinococcosis (45). Eosinophilia was imaging in diagnosing polycystic echinococcosis.
394 D’ALESSANDRO AND RAUSCH CLIN. MICROBIOL. REV.
FIG. 23. Large rostellar hooks from protoscoleces of Echinococcus vogeli, E. oligarthrus, and E. granulosus (left to right, all at the same
magnification).
positive in 4 of 5 (the case with a negative result was also We have listed in Table 4 a total of 172 cases in 12 Central
negative by IB test), and 18 of the 19 patients with positive American and South American countries, from Nicaragua and
results described above also had positive IB tests. A single Costa Rica in the north to Argentina in the south (86, 87, 88),
serological test for the diagnosis of echinococcosis, either pos- as well as Uruguay (19, 22) and Chile (85). Fifty-four cases
itive or negative, may be misleading: a negative test should not were due to E. vogeli, 114 cases were due to Echinococcus cf.
be taken to exclude infection, and the opposite may be true. vogeli, and 3 cases were due to E. oligarthrus. E. vogeli and E.
oligarthrus occur only in the Neotropics, with the exception of
Parasitological Diagnosis one recorded instance of E. oligarthrus in Mexico. Two human
cases of submaxillary echinococcosis in India were erroneously
Metacestodes of the three species of Echinococcus occurring reported to have been caused by E. oligarthrus but instead were
in Central America and South America are distinguishable on caused by E. granulosus (13, 37, 71). The number of reported
the basis of form and size of rostellar hooks from protoscoleces cases of E. vogeli infection has increased within the last 10
(Fig. 23). If rostellar hooks are not observed, definitive iden- years, going from 72 persons in 11 countries to 172 in 12
tification usually is not possible. countries. Peru is the newest country of record. The country
with most cases was formerly Colombia but now is Brazil, with
EPIDEMIOLOGY 58% of all reported cases. Polycystic echinococcosis has re-
ceived much attention and emphasis from the medical profes-
Geographical Distribution of Neotropical Echinococcoses sion in Brazil, which accounts for the relatively large number of
The number and distribution of cases of polycystic and uni- reported cases in that country. We consider that the total
cystic echinococcosis are presented in Tables 1 and 4. Table 1
indicates that of the 81 patients we evaluated, three were
determined to be infected by E. oligarthrus and 42 were in- TABLE 4. Number of cases of echinococcosis in the Neotropics by
fected by E. vogeli, and for 36 patients, rostellar hooks were not country and species of Echinococcusa
found and identification of the cestode could not be made. In No. of cases with indicated infection
those 36, the diagnosis was stated to be polycystic echinococ- Country
E. vogeli E. cf. vogeli E. oligarthrus E. granulosus Total
cosis. Our judgment now, after more than 20 years of evalua-
tions of lesions produced in polycystic echinococcosis, is that Nicaragua 1 1
the etiological agent was E. vogeli. The structures of the meta- Costa Rica 1 1 2
Panama 2 2
cestodes, the pathogenic processes, and the epidemiological Colombia 15 14 29
information provided by the patients (metacestodes with and Ecuador 6 5 11
without hooks, the patients’ knowledge of pacas and their Venezuela 2 1 1 4
infections, the awareness of feeding liver of pacas, with any Peru 1 1
Brazil 21 77 1 99
cysts present, to domestic dogs, and the presence of domestic Suriname 7 1 1 9
dogs around previous or current dwellings of patients) were Uruguay 2 2
similar whether or not the species of cestode could be identi- Argentinab 11 11
fied. In addition, the lesions observed in the patients with E. Chile 1 1
vogeli infections in which rostellar hooks were present were
Total 54 114 3 1 172
similar to those in which hooks could not be found. In our
a
judgment, when rostellar hooks are not found in polycystic As of March 2007. (Adapted and updated from reference 12 with permission
from Elsevier.) E. cf. vogeli, E. vogeli causing infections with polycystic lesions but
lesions, it is diagnostically acceptable to designate the etiologic with no hooks found.
agent Echinococcus cf. vogeli. b
Synanthropic infections by E. granulosus not included.
396 D’ALESSANDRO AND RAUSCH CLIN. MICROBIOL. REV.
FIG. 25. Map of Central America and South America, indicating the geographic range of the bush dog, as compiled from various sources.
be acquired by the ingestion of eggs of that cestode expelled pacas could not be determined. The paca (Fig. 3) is a large
with the feces of a bush dog. The accidental microepidemic in (weighing up to 13.5 kg) hystricognath rodent of nocturnal
numerous primates in a zoo, described above, is a tragic ex- habits. When alarmed, it takes readily to water, near which it
ample. In another example of accidental transmission, nutrias is usually found. It is hunted (not trapped) for food by local
became infected by E. vogeli in a second American zoo where people, who appreciate its meat. Pacas are herbivorous, and
South American carnivores were housed. Infections might also their diet consists mainly of fruits of arborescent plants, with
occur in humans in close contact with wild canids or felids kept some herbaceous vegetation seasonally (25). In the state of
as pets in people’s dwellings (11, 65, 81). Chiapas, in southern Mexico, Gallina (28) determined that
Among the 2,809 rodents surveyed in Colombia, metaces- pacas consumed the fruits of trees of 18 species, representing
todes of Echinococcus were found in only the pacas and the 18 families. Periods of fruit production by trees of the various
spiny rats (Proechimys spp.; 6 of 1,168) (18), but agoutis, species overlap, making such food resources generally avail-
Dasyprocta spp., are known to be a prominent host of the able. Because bush dogs hunt in packs on land (and in water if
metacestode of E. oligarthrus. The distribution of pacas and pacas enter watercourses to escape them), it is considered that
agoutis extends from southern Mexico to Ecuador and, east of their fecal deposits are extensively dispersed in habitat where
the Andes, south to Bolivia, Paraguay, northeastern Argentina, the rodents forage. Under such conditions, incidental ingestion
and Santa Catalina, Brazil. They also occur in the Lesser An- of eggs must account for the comparatively high prevalence of
tilles (Fig. 26). the metacestodes of E. vogeli in the intermediate host.
Of 325 pacas, 96 (29.5%) were infected. In 61, the species Age classes of pacas were estimated: adults were animals of
was E. vogeli; in 12, the species was Echinococcus cf. vogeli; and more than 7.5 kg, subadults were animals between 5.5 kg and
in 3 (0.9%), the species was E. oligarthrus. The identity of 7.5 kg, and juveniles were animals of less than 5.5 kg. The
metacestodes, all without rostellar hooks, in the remaining 20 frequency of infection in the adult class (28/95; 29.5%) was
398 D’ALESSANDRO AND RAUSCH CLIN. MICROBIOL. REV.
FIG. 26. Map of Central America and South America, showing the geographic ranges of the paca and agoutis. (Reprinted from reference 12
with permission from Elsevier.)
found to be significantly greater than that of infection in the ing domestic swine; T. hydatigena possibly occurs in wild pigs
subadult class (8/50; 16%), and the subadult infection fre- (indigenous species) in South America.
quency was significantly greater than the juvenile class infec- In mammals of the four species from which metacestodes of
tion frequency (0/26). Echinococcus have been recorded in Argentina and Chile, only in
In a field study in Brazil, Pastore et al. (51) asked the local the case of the European hare was it well established that the
people if they had seen cysts in animals other than pacas. A cestode was E. granulosus (73). The taxonomic statuses of meta-
large proportion of them indicated that domestic pigs fre- cestodes recorded from rodents of the genera Microcavia, Oct-
quently showed large cysts in the abdomen. Those authors odon, and Myocastor are undetermined because at the time of
stated that there were no data indicating that pigs participate earlier publications, neotropical species of Echinococcus were not
in the cycle of E. vogeli. We had the opportunity to study one well distinguished (3, 20) and E. vogeli had not yet been described.
such cyst, and Gustavo Morales, who reviewed the histopathol- We know that the nutria (Myocastor sp.) is susceptible to exper-
ogy, reported that possibly it was a peritoneal reaction to a imental infection with E. vogeli (Fig. 27) (59).
foreign body. The wall was fibrous and had a pseudoepithelium The strobilar stage of E. oligarthrus has been reported from
with no parasitic elements. However, another cestode, Taenia 6 of the 10 species of felids occurring in South America and
hydatigena, occurs in dogs, and its metacestode may be found Central America. It was first collected from a cougar examined
in the abdomen of pigs and other ungulates in which the by J. Natterer in Brazil during the 1830s but incorrectly iden-
cysticercus is attached to, or in, abdominal organs. The identity tified as Taenia crassicollis Rudolphi 1810 (⫽ Taenia taeniae-
of that cestode can be determined from the rostellar hooks of formis Batsch 1786, a common cestode in the house cat) by
the cysticercus. Pigs also are susceptible to infection by E. Diesing (23). Lühe (40) restudied Diesing’s cestodes from fe-
granulosus, but the tropical forest is not an environment favor- lids and correctly recognized that morphologically, they corre-
VOL. 21, 2008 NEW ASPECTS OF NEOTROPICAL ECHINOCOCCOSIS 399
beneficial, but means of establishing such programs seem gen- 21. Deutsch, L. A. 1983. An encounter between bush dog (Speothos venaticus)
and paca (Agouti paca). J. Mammal. 64:532–533.
erally to be unavailable. The risk of acquiring echinococcosis 22. Dévé, F., R. Piaggio-Blanco, and F. Garcia-Capurro. 1936. Échinococcose
(sensu lato) is seen to be greatly diminished if dogs are not hépatique maligne micropolykystique infiltrate. Forme intermédiara entre
kept (57), but the ancient association between people and their l’échinococcose hydatic et l’échinococcose alveolaire. Arch. Urug. Med. Cir.
Est. 8:3–28.
dogs is disrupted only under exceptional demands for changes 23. Diesing, C. M. 1850. Systema helminthum. Historiae naturalis classica, vol.
in lifestyle. XI. [Reprint, H. R. Engelmann (J. Cramer), Weinheim, Germany, 1960.]
Vindobonae, Braumüller, Germany.
24. Drüwa, P. 1982. Perro de grulleiro, der Südamerikanische Waldhund—ein
ACKNOWLEDGMENTS Rätsel für die Hundeforschung. Zeitsch. Kölner Zoo. 25:71–81.
25. Eisenberg, J. F. 1989. Mammals of the Neotropics. The Northern Neotro-
We express our thanks to Ulysses Meneghelli, who kindly provided pics, vol. 1. University of Chicago Press, Chicago, IL.
information on the outcome of patients he had treated earlier with 26. Ferreira, M. S., S. A. Nishioka, A. Rocha, and A. D’Alessandro. 1995. Echi-
albendazole from unpublished results of a human serological survey nococcus vogeli polycystic hydatid disease: report of two Brazilian casesout-
for echinococcosis in Brazil as well as permission to use some of the side the Amazon region. Trans. Roy. Soc. Trop. Med. Hyg. 89:286–287.
imaging from his patients. We also thank Mark Wiser, Maria Frontini, 27. Frider, B., J. Moguilensky, J. C. Salvitti, M. Odriozol, and E. Larrieu. 1999.
and Kris Swalm, Tulane University, School of Public Health and Trop- Epidemiological surveillance of human hydatidosis by means of ultrasonog-
raphy: Its contribution to the evaluation of control programs. Acta Trop.
ical Medicine, Department of Tropical Medicine, Epidemiology and 79:219–223.
Computing Services, respectively, for their help with the preparation of 28. Gallina, S. 1981. Contribución al conocimiento de los hábitos alimenticios
the manuscript due to their expertise with the computer. Special del tapezcuintle (Aguti paca Lin.) en Lancajá-Chansayab, Chiapas, p. 58–67.
thanks to Virginia Rausch, Burke Museum of Natural History, Uni- In P. R. Castillo (ed.), Estudios ecológicos en el trópico Mexicano, publica-
versity of Washington, for her interest and help in this work and for tion 6. Instituto de Ecologı́a A. C., Mexico, D.F., Mexico
preparing the drawing of the life cycle. We are grateful as well to Mark 29. Ghiotti Siqueira, N., F. Barbosa de Almeida, S. R. Silva Chalub, J. R.
Derby and David Wolbrecht, University of Washington, who kindly Machadao-Silva, and R. Rodrigues-Silva. 2007. Successful outcome of he-
provided technical assistance. patic polycystic echinococcosis managed with surgery and chemotherapy.
Trans. R. Soc. Trop. Med. Hyg. 101:624–626.
30. Gottstein, B. 1992. Molecular and immunological diagnosis of echinococco-
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