Pet roundworms and hookworms: A continuing need for global worming

Abstract

Ascarids and ancylostomatids are the most important parasites affecting dogs and cats worldwide, in terms of diffusion and risk for animal and human health. Different misconceptions have led the general public and pet owners to minimize the importance of these intestinal worms. A low grade of interest is also registered among veterinary professions, although there is a significant merit in keeping our guard up against these parasites. This article reviews current knowledge of ascarids and ancylostomatids, with a special focus on pathogenicity, epidemiology and control methods in veterinary and human medicine.

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R E V I E W Open Access
Pet roundworms and hookworms: A continuing
need for global worming
Donato Traversa
Abstract
Ascarids and ancylostomatids are the most important parasites affecting dogs and cats worldwide, in terms of
diffusion and risk for animal and human health. Different misconceptions have led the general public and pet
owners to minimize the importance of these intestinal worms. A low grade of interest is also registered among
veterinary professions, although there is a significant merit in keeping our guard up against these parasites. This
article reviews current knowledge of ascarids and ancylostomatids, with a special focus on pathogenicity,
epidemiology and control methods in veterinary and human medicine.
Review
Background
The relationship between human beings and domesticated
small animals began about 15.000 years ago [1]. Such
association has led to the dispersion of pets all over the
World, along with the spread of their pathogens. Some of
them are common and zoonotic: as a consequence, there
is a continuing interest on their sanitary impact, and on
prevention and control methods. In the past few years the
attention of the Scientific Community has been attracted
by feline and canine extra-intestinal parasitic nematodes,
which are emerging in several countries and spreading
into regions previously free from these parasites. Indeed,
global climate change is influencing the ecology of
helminths with multiple hosts and different transmission
routes. As key examples, this is the case of the insect-
borne filariae and eyeworm [2-4] and of the snail-borne
lungworms Aelurostrongylus abstrusus and Angiostrongy-
lus vasorum [3,5]. This new concern has caused the
misconception that intestinal worms of cats and dogs do
not deserve a high-standard level of attention anymore,
especially because the routine use of certain anthelmintics
is believed to have reduced their diffusion and impact on
animal health and welfare [6]. Indeed, the use of broad
spectrum drugs, which are sold (often over-the-counter)
in a plethora of formulations, carries the risk that leads
the general public to minimize the importance of the
“common intestinal worms”and to erode the importance
of the veterinarian in controlling parasites of veterinary
and human impact. This low-grade of interest and atten-
tion is crucial if one considers that several pet intestinal
nematodes are zoonotic and endemic globally, and the
spread of these parasites may be favoured by current
climate changes. In fact, these parasites have periods of
development and survival in the environment, which are
often at the basis of transmission routes in important
sapro-zoonoses.
Different species of ascarids (commonly known as
“roundworms”) and ancylostomatids (commonly known
as “hookworms”) may affect the small intestine of dogs
and cats [7]. Actually, they remain the most important
parasites affecting companion animals worldwide and
maintain the primacy in terms of dispersion and risk
for animal and human health. This is of particular
importance also because some driving forces are now-
adays favouring their spread, e.g. the increase of wild
fox populations in sub-urban and urban areas. For
example, wild foxes may act as reservoirs and amplifiers
of canine ascarids, thus they re-enforce environmental
contamination and risk of infection [8].
There is, in turn, a significant merit in keeping our guard
up against these nematodes even when other parasites are
attracting attention and interest. Therefore, the aim of this
article is to review the most important features of
roundworms and hookworms affecting companion animals,
along with critical and focused appraisals on the import-
ance of their pathogenicity, epidemiology and control
methods in veterinary and human medicine.
Correspondence: dtraversa@unite.it
Department of Comparative Biomedical Sciences, University of Teramo,
Teramo, Italy
© 2012 Traversa; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
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Intestinal nematodes are complex and interesting
Pets can be parasitized by different nematodes, intestinal
roundworms, hookworms and whipworms being the
most common. Main aspects of trichuroid whipworms
(i.e. Trichuris vulpis) affecting the large bowel of dogs
have been recently described elsewhere [9], thus this
species will be excluded from this article.
Toxocara canis and Toxocara cati are the two major
ascarids globally infecting dogs and cats, respectively.
Both species have a complex and fascinating biological
cycle, which relies on different pathways of larval
migrations and transmission, depending upon mainly
the source of infection and animal age.
Bitches are a major source of infection for their off-
spring because, after an infection occurs in their life,
they harbour somatic larvae. These resting larvae will
mobilize during pregnancies and infect subsequent
litters even when re-infections do not occur. Pups
become infected in utero by the second month of
gestation, which result in egg shedding after a minimum
period of about two weeks after birth [10,11]. When
mobilized larvae are transmitted via the lactogenic route
litters can also be infected by colostrum and milk for at
least 38 days after delivery [12,13]. These vertical infec-
tions occur regardless of the presence of the intestinal
parasitosis in the bitch but, in general, a proportion of
mobilized larvae may reach the intestine of the dam,
then mature and cause a patent infection with high egg
shedding lasting weeks after whelping. Bitches can be re-
infected also by ingesting immature ascarids defecated
by their suckling offspring. Therefore, lactation may either
cause or reinforce a patent infection in bitches, which pro-
vides another source of environmental contamination and
infection for puppies [13].
While T. cati is not transplacentally transmitted, lacto-
genic infection may occur in kittens during the first days of
nursing [14,15]. It has been recently shown that the acute
infection of the queen during a late phase of pregnancy
causes the milk-borne infection in the offspring [15].
Dogs and cats of all ages can also acquire the infection
by ingesting Toxocara embryonated eggs from the envir-
onment and eating paratenic hosts (e.g. invertebrates,
ruminants, rodents, birds) harboring tissutal larvae
[13,16-18].
The prepatent period for toxocarosis by T. canis is at
minimum 4–5 weeks after ingestion of embryonated eggs
or resting larvae, and 2–3 weeks for prenatal infections,
while kittens start to shed T. cati eggs after about 7–8 weeks
post infection [13,19,20].
A third roundworm, Toxascaris leonina, affects both
dogs and cats. This species is, in general, less diffuse
than Toxocara spp., especially because transmissions via
the placenta and mammary glands do not occur.
Animals become infected only by ingesting larvated eggs
from the environment or tissutal larvae in paratenic
hosts, e.g. rodents [13].
Pathogenesis and symptoms due to adult stages are
similar to Toxocara spp. (see below) but the infection
does not occur in animals aged less than about 2 months.
Prepatency period is about 10–11 weeks [20,21].
Among the most common hookworms, Ancylostoma
caninum and Ancylostoma tubaeforme are species-specific
for dogs and cats respectively, while Ancylostoma bra-
ziliense,Ancylostoma ceylanicum and Uncinaria stenoce-
phala affect both species [7,17,22]. In general A. caninum,
A. tubaeforme and U. stenocephala are spread especially in
warm countries (Ancylostoma spp.) and in colder areas of
temperateandsubarcticregions(
U. stenocephala)inboth
hemispheres; the remaining hookworms are most often
present in sub-tropical and tropical countries [20,23-26]. As
for roundworms, hookworms have a complex biological
cycle, in which different sources and ways of infec-
tion are possible. The most important infectious stage is
represented by filariform larvae present in the soil, which
infect a suitable host by actively penetrating the skin
(especially for Ancylostoma spp.) and/or via the oral route
(i.e. Ancylostoma spp., Uncinaria spp.) [7,13,22,27].
Nursing is a relevant source of infectious larvae of A.
caninum for puppies. In fact, it is well established that,
when infection occurs in adult dogs, a proportion of
larvae invade different body regions. These resting stages
survive for years and are, in turn, reactivated during
oestrus and in the last 2–3 weeks of pregnancy, when
they are passed via the milk to the litter for at least
3 weeks after delivery [26,28-30]. A bitch harbouring
somatic larvae is infectious for three consecutive litters,
although the larval output is reduced in each lactation
[30-34]. Conversely, there is a scattered and conflicting
body of bibliographic information on the transplacentary
transmission [13,20,26,35,36]. Indeed, if in utero infec-
tion occurs at all, it is obfuscated by the lactogenic route
and, in any case, prenatal transmission by A. caninum
does not occur in all puppies from a litter [7,27,37-39].
It has also been reported that larvae of A. caninum dor-
mant in musculature may be re-activated following fac-
tors driving stress, e.g. severe illness or corticosteroid
therapies, which then reach the intestine causing patent
infections in the adult dog [27]. In utero and lactogenic
infections do not occur for A. tubaeforme, even though
literature is scarce and the extent of milk transmission is
stated to be not well known [7,17,27]. For the other
canine and feline hookworms vertical infections do not
appear to occur at all [7,17,39,40].
Paratenic hosts are also important in transmitting
ancylostomosis in dogs and cats which prey on ani-
mals (e.g. rodents). Prepatent period for A. caninum,
A. tubaeforme and U. stenocephala is about 2–3 weeks
[7,17,20].
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In summary, there are major factors making round-
worms and hookworms the most common endoparasites
in pets all over the World. First of all, the possibility of
puppies and kittens being infected by their dam by
transmammary and/or transplacental route/s is a power-
ful host-finding strategy. Also, pups have daily thousands
epg counts for T. canis and animals often shed millions
of hookworm eggs for weeks, thus causing a high envir-
onmental contamination. Ascarid eggs can survive for
years in extreme environmental conditions, thus are
available for ingestion at any time. Infected paratenic
hosts are ubiquitous, being a constant source of infec-
tion especially for cats, given their hunting instinct.
Is age a decisive circumstance for host-finding strategies
of intestinal nematodes?
There is a long-standing misconception on the age cat-
egories of dogs and cats, which can be infected. In fact,
it is often thought that “intestinal worms”are only a
health problem of puppies and kittens and that adult
animals are, instead, resistant.
The real truth is that pets are exposed to roundworm
and hookworm infections throughout the year and for
all their life. Specifically, parasitic burdens, egg output
and infection rates are higher in puppies and kittens but
it is nowadays established that patent intestinal infec-
tions occur in dogs and cats of all ages [41-50].
Adult dogs can be re-infected by T. canis even when
under regular control programs [46,51]. Also, they have
the same susceptibility for patent infections as naïve
patients when later re-exposed and even when repeat-
edly exposed to the parasite and having circulating anti-
bodies vs ascarid surface antigens [52,53]. Patent ascaridosis
may be detected in animals older than 3 years or more, and
may also establish when infection occurs with a few
larvated ova [11,46,54-56]. Also, nursing bitches may
present heavy patent infections by about 4 weeks after de-
livery [27].
Analogously, the chance that a cat develops a patent
intestinal infection by T. cati remains high throughout its
life. For instance, one of the major causes of infection for
adult cats is the ingestion of larvated eggs acquired from
the environment by their perpetual self-grooming [27].
For its biological cycle, the infection by T. leonina is
much more common in adult animals than in young
subjects [27].
Some studies have unwaveringly indicated a signifi-
cantly higher prevalence of canine hookworms in young
dogs [41,44,47,57]. Nonetheless, there is evidence that
prevalence of A. caninum in dogs <11 months of age
can be significantly lower than infection rates in dogs
aged 1–6 and >6 years [58] and that there is no relation-
ship between host age and prevalence of Ancylostoma
spp. [59]. Analogously, prevalence of U. stenocephala
can be higher in dogs of more than 3 years of age than
in puppies of less than 4 months [60]. Surveys performed
in the USA have underscored high infection rates in
young puppies and only slight age-related decrease of
prevalence after 1–2 [47] or 7 years of age [54]. It is worth
mentioning that, after resting larvae of A. caninum are re-
activated in pregnancy, they can cause auto-infection of
the dam, thus reinforcing opportunities for adult dogs to
show patent ancylostomosis [13]. In general, old dogs
infected by A. caninum usually display a prolonged prepa-
tency and a reduced period of egg shedding, likely
due to partial immunity or age resistance [13]. Given
that A. tubaeforme is not transmitted in utero or via the
milk, the infection can be present in cats of all ages and not
only in kittens. There are studies that have shown an in-
creasing trend of infection rate in 1–5 year old cats rather
than in younger animals [42,53].
An investigation carried out in the USA on the most
common canine and feline endoparasites in thousands
of pets has shown that, after animals under 6 months of
age (as expected), the most parasitized category of
animals are patients more than 10 years old [53]. The
possible explanation of such a high degree of parasitism
in old animals may reside in a loss of immune response
against previously experienced parasites [61,62]. Another
possible reason may be a loss of compliance of pet
owners, who, perhaps, become less willing to engage in
chemopreventative measures in old pets [53]. Such
changing approach of pet owners should be discouraged
by veterinarians not only for the pathogenicity of
intestinal worms, but also because there is no practical
reason to consider an old animal a less effective source
of infection for other pets and human beings in
comparison to puppies and kittens.
Biology and pathogenicity of intestinal nematodes:
Threats for pets and humans
Virtually 100% of dogs and cats, from the cosseted and
beloved pet to the stray animal, have been in contact
with ascarids and ancylostomatids or, at least, are at risk
of disease.
Ascarids live free in the lumen of the small intestine feed-
ing on its content. Mild infections are usually not accom-
panied by clinical signs either in larval migration or in
patent infections. When the number of canine roundworms
is moderate-high, larval migrations can cause cough, frothy
nasal discharge, pneumonia and edema of the lungs. Death
mostly occurs in this larval phase and especially within a
few days after birth in puppies borne after a severe
transplacental infection [13]. Adult roundworms in pups
cause by the second-third week of age a mucoid enteritis
characterized by vomiting, diarrhoea, ascites, anorexia,
anaemia, unthriftiness, emaciation, poor coat, nasal dis-
charge, and pot belly (Figure 1) due to heavy worm burden,
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dysbacteriosis and gas formation. In severe circumstances
animals may suffer from thickened intestine, partial or total
obstruction or occlusion, duodenum dilatation, peritonitis,
bile and pancreatic ducts blockage, rupture of the intestine
and worms at different stages expelled with the vomitus or
the faeces (Figure 2); indeed, pups and kittens with heavy
infections may expel a large mass of worms in vomitus
[13,16,20,27], thus causing distress for the owner as the
worms are large and usually alive. Nursling puppies suffer
severe discomfort, whimper and shriek and, when walking
or standing, present a straddle-legged posture of the hind
limbs [27]. Penetration of the peritoneal cavity after gut wall
perforation, with subsequent peritonitis and massive blood
loss, have also been reported [63,64].
Infected kittens may show a catarrhal enteritis with vari-
able appetite, vomiting after feeding, diarrhoea alternated
with constipation, developmental disturbances, anaemia
and anorexia, especially after severe infections [65,66]. In
adult cats T. cati may cause vomiting, enlargement of the
abdomen, anorexia and even gastric perforation with
presence of adult parasites in the abdominal cavity [67,68].
A case of a feline infection by T. canis characterized
by an eosinophilic granulomatous dissemination of larvae
has been reported in a pyrexic cat [69].
Toxascaris leonina has a less dramatic pathogenicity,
but in dogs it may cause pica, digestive disturbances and
reduced growth, while in cats the infection can be seen
as an enteritis with vomiting and diarrhoea, even bloody
[17,70,71].
Hookworms have been regarded as the most faithful
intestinal parasites of dogs and cats [36]. Indeed, they
are responsible for developmental impairment, severe
clinical signs and high death rate, especially in young
subjects. These worms live anchored to the gut mucosa
by their oral capsule and have a relevant blood-sucking
activity. Indeed, while A. braziliense may present a mild
pathogenic impact, the other hookworms are intensive
hematophagous and cause important exsanguination. In
general, ancylostomosis in pets induces a mild enteritis
to a fatal hemorrhagic diarrhoea with anemia, depending
upon different drivers, e.g. age of the animal, parasitic
burden and species involved [16,17,20,27,29].
Juveniles of A. caninum burrow deeply and massively into
the mucosa, thus symptoms can be severe and life-
threatening especially for puppies, in which even fatal
diseases may occur in pre-patency. After a milk-borne
infection, pups, which have low iron reserves, are healthy in
the first week of age, and then show profound blood loss
and deteriorate rapidly within the second-third week
after birth. Age is a crucial factor in the outcome of
canine ancylostomosis, because as the animal grows,
resistance increases, regardless of whether the animal
has experienced one or more infections. However,
further infections may be inhibited by a pre-existent
hookworm populations (i.e. premunition) and, in general,
symptoms in adult dogs are dependent upon state of
nutrition, hematopoietic capacity, presence of stressful
conditions. In general, adults with a mild parasitic burden
with A. caninum suffer with a moderate anaemia for the
capacity to which their bone marrow has to compensate,
but these animals may develop a more intense microcytic
hypochromic anaemia in any case. Heavy infections always
Figure 1 Pot belly in a roundworm-infected puppy.
Figure 2 Adults of Toxocara canis spontaneously expelled with
the faeces by a puppy.
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present with chronic iron deficiency anaemia, poor coat,
loss of weight, bloody and mucous faeces, reduced growth,
circulatory collapse, lack of stamina and poor general
physical condition [13,20,27,36].
Cats affected by A. tubaeforme suffer with enteritis, blood
loss, diarrhoeic faeces, reduced weight, regenerative anemia,
cachexia and even death [13,65,72].
Uncinaria stenocephala has a less intense haematopha-
gous activity compared to Ancylostoma spp. and removes
small amounts of blood; heavy infections in young animals
may be characterized by mild anaemia, hypoalbuminemia,
anorexia, diarrhoea and lethargy [20,27].
The majority of canine and feline roundworms and
hookworms are potentially zoonotic.
Human beings can be hosts of ascarids when they inad-
vertently ingest embryonated eggs from the soil (i.e. sapro-
zoonosis) or tissutal larvae. For instance, this happens by
putting unwashed fingers into the mouth, or eating raw
contaminated vegetables or meat of paratenic hosts [73].
As an example, a relatively common source of human
infection is food, represented by vegetables harvested from
farms using animal dung as fertilizer [18,73,74] or by raw
or undercooked liver or meat from ruminants, pigs,
chickens [18,75,76]. A relatively unexploited source of
infection for humans is represented by embryonated ascarid
eggs present on dogs’fur [56,77]. The real proportion of
petswhosefuristrulycontaminatedbyinfectiouseggsand
whether they are a real threat for humans still remains to
be elucidated. However, direct contact with an animal
infected by roundworms should not be considered
hazardous for the following reasons: Toxocara eggs need
about 2–6 weeks before infectivity is reached, they are
strongly adhesive on animal’s coats and difficult to ingest,
most of them are not viable, and, finally, several fur grams
need to be swallowed to cause infection [78-84]. Moreover,
thepresenceofnon-canidparasiticovaonfurofdogs
indicates that animals become contaminated in the
environment, possibly through scent-rolling, rather than
from their own defecations [56].
Once infective elements are ingested, larvae penetrate
the gut wall and reach the bloodstream wandering
throughout the body, i.e. eyes, heart, muscles, brain,
lungs, liver. Thereby, larvae do not molt nor reach the
adulthood but, however, induce severe local reactions
and damage, which may lead to different syndromes (see
next section).
With regard to hookworms, pets and humans suffer from
a skin condition when free-living infective larvae species
present in the soil, enter into the skin to reach the intestine
via the bloodstream. In pets the cutaneous damage leads to
different degrees of itching, erythema, vesicular or papular
lesions, acanthosis, hyperkeratinization, cellular infiltrates
and perivascular cuffing, especially at the interdigital skin
[22,26,36]. However, infectious larvae of animal hookworms
may penetrate human skin, causing local lesions, intestinal
distress and even ocular/neurological signs; however, the
aetiological role of each animal hookworm in causing dis-
ease in humans remains to be elucidated (see next section).
Pet roundworms and hookworms are zoonotic
Soil-transmitted helminthoses affects more than 2 billion
people worldwide [85]. The zoonotic ability of Toxocara
spp. has been established since the 1950’s [86,87] and
presently it is well known that pet ascarids cause human
infections globally, as demonstrated by several surveys
carried out in all corners of the World [18,88].
Indeed, T. canis is largely acknowledged as a major
culprit of human syndromes by animal ascarids, but it is
likely that some human infections are caused by T. cati
as well [88,89].
Some infections are asymptomatic [90,91] and the
degree of damage and elicited signs depend upon the
tissue/s invaded, number of migrating larvae, host age and
immune response. When symptoms are present, two
major syndromes may occur, i.e. the so-called “visceral
larva migrans”(VLM), encompassing important organs
(mainly liver, lungs, brain) and “ocular larva migrans”
(OLM), due to damage to eye and optic nerve; other
minor syndromes, e.g. covert, neural, and atopyc
toxocarosis, are also reported [88,90,91].
Children, in particular toddlers, are the most frequent
subjects suffering from VLM, often with severe clinical
symptoms. The high occurrence in children is due to
frequent exposure to areas (e.g. sandpits, sandboxes,
gardens, playgrounds) potentially contaminated by Toxo-
cara eggs and to low hygiene standards [79]. Also, geo-
phagic pica (e.g. due to iron or zinc deficiency or to
behavior disorders), which may affect up to 10% of
children, is another relevant risk factor [79,92].
VLM in 1–5 year old children is characterized by fever,
leucocytosis, eosinophilia, hypergammaglobulinaemia,
general malaise, abdominal distress and pain; when
larvae infect the liver, patients can suffer from hepato-
megaly, granulomatous hepatitis or even necrosis [79,93-
95]. There are cases of bronchiolitis/pneumonitis with
wheezing, cough and asthma-like bronchospasm, and of
myocarditis, nephritis, and involvement of the central
nervous system with meningoencephalitis, seizures, and
neuropsychiatric signs [79,88,94,96-98].
OLM usually occurs without signs of VLM in children
aged 5–10 years and in adults as well [92,99], and is
characterized by impaired vision to total loss of sight, due
to endophthalmitis, retinal granulomas and detach-
ment of the macula [88,100]. Other signs are complaints of
“seeing lights”, squint and glaucoma; more importantly,
OLM may mimic a retinoblastoma, thus erroneously indu-
cing enucleatio bulbi [99,101,102]. Hundreds of cases of
unilateral blindness and of more or less severe eye damage
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have been calculated to occur yearly in US childhood due
to OLM and dozens of unnecessary eye enucleations due to
misdiagnosis with retinoblastoma are described [6,27,74].
A third condition, called “covert toxocarosis”, might
be caused to long-term exposure to migrating larvae in
specific target organs. In children older than toddlers,
this form presents vaguely with behavioral changes,
seizures and sleep alterations, cough, asthma, abdominal
discomfort, headache, while in adults it may present
with weakness, rash and itching, abdominal pain and
breathing distress [103-108].
Finally, skin conditions, like pruritus, urticaria and dif-
ferent eczematous lesions, have been found in association
with toxocarosis in both childhood and adults [88,109].
There are reports of juveniles of feline roundworms
identified in the liver and the brain of two children from
the USA and Israel [110,111]. Interestingly, there are
published cases of adult T. cati passed from the anus or
the mouth of children, but it is very likely that these
cases originated by an altered behavior, i.e. taking worms
from vomitus or faeces from an infected animal
[112,113]. It seems that T. leonina does not display
zoonotic potential. However, there are a couple of
published reports of possible human infections by this
species: a case of osteomyositis with cutaneous abscesses
containing worms identified as T. leonina has been
described in the 1960’s in the former USSR [114], while
a case of ocular infection by a suspected Toxascaris spp.
larva has been described from Africa [115].
Humans may be infected by free-living hookworm larvae
when walking barefoot, when in close contact with poten-
tial contaminated soil (e.g. gardeners), or when sunbathing
on beaches in risky areas. Larvae of A. braziliense cause the
so-called “cutaneous larva migrans”(CLM), a dermatitis
with long serpiginous and persistent tracks underneath the
human skin. The role of other hookworms in causing CLM
needs to be clarified. The US CDC states “CLM”to be
known also as “creeping eruption”,being“a zoonotic infec-
tion with hookworm species that do not use humans as a
definitive host, the most common being A. braziliense and
A. caninum”[116]. Also, the CDC states that “Alarger
group of hookworms infecting animals can invade and
parasitize humans (A. ceylanicum) or can penetrate the
human skin (causing cutaneous larva migrans), but do not
develop any further (A.braziliense,A. caninum,Uncinaria
stenocephala)”[116].
Indeed, the geographic distribution of CLM overlaps
that of A. braziliense [25,117] and interestingly, it does not
occur where this species is absent, e.g. in Mexico, West
US coasts and Australia [24,26]. These epidemiological
features have led us to consider A. braziliense as the only
species causing human CLM, although CLM-like cases
have been reported from India, a country where A. brazi-
liense is not present [26].
Indeed, A. tubaeforme does not penetrate human skin
or has a little skin penetration and, although A. caninum
and U. stenocephala are indicated as cause of CLM, their
role as agents of skin lesions in humans is still unclear
[26,36,116,118,119]. There is an old report of a self-
infection by larvae of U. stenocephala, which showed
that they can penetrate human skin [120]. Skin penetra-
tion by larvae of A. caninum has been associated with
follicolitis, ephemeral and papular/pustolar eruptions
[121-123] and to the penetration of muscle fibers and
lung infiltrates [124]. However, this latter identification
was grasped on epidemiological and biological bases and
not on a specific identification of the parasite [124]. In-
deed, myositis occurred in human volunteers after skin
infection by larvae of this canine hookworm [125], thus
corroborating the hypothesis that larval A. caninum may
indeed cause muscular damage. These larvae have also
been associated with a sort of human OLM, a unilateral
sub-acute neuroretinitis with loss of vision [126] and, as
those of A. ceylanicum, can reach adulthood in the
human gut. In particular, a relatively newly discovered
human disease caused by A. caninum is an eosinophilic
enteritis regarded as an emergent disease in some areas,
e.g. Australia and USA. This syndrome, not known
before the 1990’s [126-128], poses important diagnostic
challenges. It can be even caused by a single hookworm
in the intestinal lumen and is characterized by
abdominal pain, discomfort and distension, weight loss,
diarrhoea and rectal bleeding [22,128-130]. Occasionally
also A. ceylanicum can develop to adult stages in human
bowel, causing intestinal distress [22,131].
Treatment and control methods: Need for compromises?
Different parasiticide classes are available for treatment
and control of intestinal nematodes, being (pro-) benzimi-
dazoles (e.g. febantel, fenbendazole), tetrahydropirimidines
(e.g. pyrantel), cyclooctadepsipeptides (i.e. emodepside)
and macrocyclic lactones (e.g. ivermectin, selamectin,
moxidectin, milbemycin oxime) the most used.
Provided below are some key examples of major mole-
cules available for treatment and control of ascarids and
ancylostomatids.
Acomparativestudyevaluated the efficacy of three for-
mulations containing mebendazole or fenbendazole alone,
or febantel in association with pyrantel and with the
cestocide praziquantel [132]. All formulations proved to be
effective against infections by ascarids and ancylostomatids
in dogs, with different therapeutic efficacies, up to 100%
[132]. A multi-centric investigation indicated that the
combination of febantel, pyrantel and praziquantel has an
efficacy of ~99.9% against canine T. canis and hookworms
[133]. Another recent study has demonstrated the efficacy
and safety of tablets containing pyrantel, oxantel, and
praziquantel against natural and/or experimental infections
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by T. canis,A. caninum and other canine endoparasites
[134]. In cats an association containing pyrantel and
praziquantel has high efficacy against ascarids and ancylos-
tomatids [133,135].
Recent experimental and field studies have evaluated
the cyclooctadepsipeptid emodepside. Emodepside is
available in a spot on formulation for cats (containing also
praziquantel), which has efficacy up to 100% in treating
infection by T. cati or T. leonina at different stages
[136,137]. This formulation also has 100% efficacy against
mature A. tubaeforme and efficacy of >95% and >97%
against L4 and immature adults, respectively [138]. Tablets
marketed for dogs containing emodepside (and prazi-
quantel) have been shown to be safe and efficacious
>92-99% against natural or experimental infections
caused by L3s and/or L4, immature and mature adults of
canine T. canis and T. leonina [139]. Four different labora-
tory investigations have demonstrated that this association
has >95% and >98% efficacy against larval and adult
U. stenocephala and A. caninum, respectively [140]. A mul-
ticentre study evaluating the same anthelmintic association
showed high efficacy in reducing egg counts (i.e. geometric
mean egg counts reduced by 99.9-100%) in dogs infected
by T. canis,T. leonina,U. stenocephala,A. caninum,under
field conditions [141]. Emodepside is also present in a
newly marketed oral suspension for dogs, also containing
the triazinetrione derivative toltrazuril for the simultaneous
treatment of coccidiosis. This formulation has shown effi-
cacy of ≥94.7-99.3% and 100% against immature and adult
stages of T. canis respectively, and of ≥99.5-100% against
adults of A. caninum and U. stenocephala, respectively, ori-
ginated from natural and experimental infections [142]. A
multicentre investigation carried out across Europe has also
indicated efficacy of 100% and 99.9% against T. canis and
Ancylostomatidae based on faecal egg count reduction
[143]. This oral suspension for dogs has been also proved
to be effective in experimental feline infections by T. cati
and A. tubaeforme [144].
With regard to macrolactones, the efficacy of a chew-
able formulation containing ivermectin (and pyrantel)
against natural or induced roundworms and hookworms
in dogs has been documented to range from 90.1% to
99.6% [145,146]. This association is effective also in the
treatment of dogs experimentally infected with A. brazi-
liense [147]. In cats with mixed infections, an ivermectin-
based chewable formulation showed 92.8% and 90.7% effi-
cacy, respectively, against adult stages of A. braziliense
and A. tubaeforme, while the number of eggs per gram of
feces decreased 98.1% by 7 days after administration
[148].
By 2000’s the endectocide selamectin has demon-
strated efficacy and safety against these parasites [149].
For instance, studies in experimental and natural infec-
tions have demonstrated the efficacy of topical selamectin
against adult T. canis and T. leonina and in reducing
the fecal excretion of T. canis eggs in dogs as well
[150]. A series of field investigations carried out in
the USA and Europe demonstrated the safety and ef-
ficacy of the monthly topical administration of the
same ML in the treatment of experimentally and
naturally acquired ascaridosis and ancylostomosis in
cats [151,152].
A spot-on formulation containing the endectocide
moxidectin together with the ectoparasiticide imidaclo-
prid has high efficacy against canine intestinal nema-
todes in mono-specific and mixed infections [153,154].
For example, in the aforementioned multi-centric study
[133] this spot on formulation showed 98.8% efficacy
against T. canis and 99.9% against Ancylostomatidae.
The same spot on formulation has 100% efficacy against
adult stages of T. cati, up to 98.3% efficacy against im-
mature adults and fourth-stage larvae of the same as-
carid, and up to 100% efficacy against adult stages of
Ancylostoma and immature adults and third-stage larvae
of A. tubaeforme [133,155].
The ML milbemycin oxime also has high efficacy in
removal of roundworms and hookworms from naturally
infected dogs and cats with patent infections [156,157].
For instance, adults of A. caninum and T. canis in natur-
ally infected dogs are killed by milbemycin oxime
[158,159]. The molecule has been shown to be effective
also in experimental ascaridosis of pups [160] and to
have a certain degree of activity against canine ancylos-
tomosis [161,162]. In other trials the molecule has been
proven to be active against T. cati [163] and fourth-stage
larvae and adults of A. tubaeforme in cats [164]. Milbe-
mycin oxime is available in associations either with lufe-
nuron or praziquantel. In dogs, the oral associations of
milbemycin oxime with lufenuron has shown 91.5% effi-
cacy against naturally ascaridosis [165]. In the multicentre
field study mentioned earlier the association containing
milbemycin oxime and praziquantel has achieved geomet-
ric mean egg counts reduced by 99.4%-99.8% in dogs
infected by roundworms and A. caninum [141]. In
cats, this association has efficacy up to 96.5-100%
against fourth-stage larvae and adult stages of T. cati
and of 93.5% against hookworms [135,166].
Furthermore, milbemycin oxime has been recently
marketed in a monthly, chewable, tablet for dogs, also
containing the insecticide spinosad. This formulation
has a 99.3-100% efficacy in treating and controlling in-
testinal nematodes in naturally and experimentally
infected dogs [167,168].
What emerges is that veterinarians have a broad
spectrum of parasiticidal formulations that can be
selected according to each individual possible scenario
and owner and animal compliances. For instance, good
compliance (i.e. 87.5%) of the owned pets treated with
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oral tablets containing pyrantel/oxantel/praziquantel has
been documented [134] and, analogously, practices across
Europe have reported a high acceptance by dogs trea-
ted with the oral tablets containing emodepside [141].
The oral suspension containing emodepside and tol-
trazuril has an acceptance rated as good and medium
in 90% and 9% respectively, in dogs treated in the multi-
center study mentioned above [143] and high palatability
when administered in cats [144]. Flavoured chewable
tablets containing milbemycin oxime presented also high
acceptance by treated animals, going from 64% to 94.8%
directly from the owners’hand [141,169]. Hence, sev-
eral oral formulations, due to their tasty flavor, allow
a treatment with minimal distress to the animal and
the owner.
It is worth noting that the formulation containing moxi-
dectin and imidacloprid has the advantage of the easy-to-
apply dermal spot-on administration in parasitized dogs
[170]. This is important also in feline clinical practice, given
that indocile or feral cats refusing oral formulations can be
easily treated with the spot-on containing moxidectin or
emodepside [171,172].
The use of antiparasitic molecules should be pro-
grammed also according to other factors, related to the
nematode biology and their epidemiological features in
different regions. Geographical spread of these parasites,
their clinical importance, and especially the high resistance
of infectious stages in the environment regardless season or
climate (e.g. ascarid ova resist to harsh chemicals, broad
temperature ranges and several degrees of moisture),
suggest careful attention to prevention approaches [13,88].
Puppies have been considered in the past as the main focus
for antiparasitic treatments to control ascarids. However,
the demonstrations that intestinal nematodes may indeed
infect adult pets and that animals which have been
vertically infected by T. canis are more susceptible to re-
infections if compared to naïve dogs [13,18,46] change our
perspective in focused control programs. Also, adult cats
maybeoftenre-infectedbyT. leonina, especially if they go
outside for hunting [17]. These cats are also more suscep-
tible to infection by A. tubaeforme, because they can eat
contaminated grass or larvae while grooming, or because
larvae can penetrate their skin when they are out-
doors. Obviously, the same risk to of being infected
by A. caninum is run by adult dogs when living or
walking in contaminated areas.
Regular “de-worming”or “worming”, an imprecise term
but common in daily language today [13], is the basis for
an effective chemoprophylaxis irrespective the age of the
pet.
Taking control of ascarids as the key example, the
major sources of infection and contamination are pup-
pies from 3 weeks and 6 months of age and nursing
bitches.
Puppies should wormed with safe formulations able to
kill the parasites and to reduce egg shedding in the
environment. As an example, a recent study has shown
the efficacy of two associations, i.e. milbemycin oxime-
based (99.9%) and febantel/pyrantel -based (98.5%), in
reducing shedding of Toxocara eggs [173]. Given that
the lactogenic transmission lasts at least 5 weeks post
partum, treating puppies at two, four, six and eight
weeks of age, and then monthly until 6 months of age
may suppress shedding of T. canis eggs in the whole
period of puppy-hood. The need for a frequent parasiti-
cide administration in pups is due to the continued
exposition to re-infections, via the milk and the environ-
ment, and to the fact that they may already harbor
migrating larvae after birth. If a parasiticide is not admi-
nistered within the 4
th
week of age, female ascarids may
reach the adulthood and become gravid, thus eggs are
shed by the pup when it is as young as about 21 days.
No transplacental transmission occurs in cats, thus
kittens can be subjected to fortnightly treatments by the
3
rd
week of age. Given that re-infections may occur
throughout the suckling period, dams should be treated
with their offspring for the first 2–3 months to avoid
patent infections in nursing animals [13,16,17,27].
Treatment of pregnant and/or lactating animals is
facilitated by the availability on the market of molecules
which can be administered safely in different time peri-
ods or for the whole pregnancy and/or lactation, for
instance pyrantel or milbemycin oxime, or other broad
spectrum drugs. On the other hand, treating pregnant
dams is questioned, although sometimes advised in some
worm control programs [13,174,175]. Prolonged daily
administration of fenbendazole can reduce prenatal
infection but such regimen is expensive and can suffer
from lack of compliance by the owner [13,176]. Less-
frequent administration of ML, can be effective in inter-
rupting vertical transmission with different schemes of
treatment [13]. Despite the absence of label claims, such
an approach could lead to increased compliance of the
owners [13].
Owners and veterinarians should always thoroughly
follow manufacturer’s indications for each of the selected
parasiticides administered to bitches, queens, puppies
and kittens.
Other than these general scientific concepts, indications
from the US Companion Animal Parasite Council (CAPC)
and the European Scientific Counsel Companion Animal
Parasites (ESCCAP) should be taken into account. These
two organisations have published guidelines for treatment
and control of major parasites affecting companion
animals [68,177].
Treatment of puppies and kittens at two, four, six and
eight weeks of age is suggested by CAPC. Thereafter,
animals should be put on monthly preventives as soon
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as label recommendations allow. Indeed, kittens do not
need to be treated for ascarids until 6 weeks of age but,
given the risk for hookworm infection, it is suggested
they are treated at 2 weeks of age and then placed on
the monthly scheme using molecules effective in pre-
venting heartworm infections and having efficacy against
roundworms as well. If puppies and kittens are not trea-
ted until 6 to 8 weeks of age or later, they should be put
on a monthly preventive according to label recommen-
dations, dewormed again in 2 weeks, and then maintained
on monthly preventives thereafter [68]. In other words, a
lifelong preventative program, using a “monthly-interval”
(i.e. parasiticide administration at 4-week intervals, in ac-
cordance with the pharmacokinetics of the molecule used)
is supported to exclude any risk of infection for the own-
ers [13]. The veterinarian should monitor and evaluate the
efficacy of i) initial treatments, ii) monthly control
product, and iii) client compliance by 2–4 fecal examina-
tions in the first year and 1–2 examinations per year
thereafter [68].
The ESCCAP recently advised that pups should re-
ceive a parasiticide at 2 weeks of age, then at fortnightly
intervals until two weeks after weaning. Thereafter, pup-
pies should undergo monthly treatments until six
months old. Fortnightly treatment of kittens can start at
3 weeks of age and should be repeated fortnightly until
two weeks after weaning, then monthly for six months.
With regard to adult dogs and cats, annual or twice
yearly treatments for Toxocara spp. does not reduce the
risk of patent infections and, also, worming four times a
year does not necessarily eliminate patent infections;
conversely, the ESCCAP states that monthly worm treat-
ment can largely prevent patent infections [177]. In
other words, a treatment frequency of at least 4 times
per year, or at intervals not exceeding 3 months, or even
a monthly treatment, are general recommendations,
according to different scenarios, e.g. real zoonotic risks,
presence of children in the pet owners family, pregnancy
of bitch or queen, housing conditions [13,177]. When a
year-round-control is not performed (e.g. because an
owner disagrees with a frequent anthelmintic adminis-
tration, or local legislation requires diagnosis or risk as-
sessment prior to treat an animal), regular faecal
examinations (e.g. every 1–3 months) of susceptible ani-
mals is considered a feasible way of evaluating the re-
occurrence of intestinal nematodes [177].
A compromise between these two views from North
America and Europe seems to be a good choice [13], if
particular situations do not apply. A minimum number
of 4 administrations per year or treatments at intervals
of 4–6 weeks can be effective in preventing most patent
infections, while a worming frequency of less than 3–4
times per year does not influence parasite prevalence
[13,178]. Nonetheless, no impact on patent parasitic
infections in pet populations has been found after an-
nual or bi-annual anthelmintic treatments [51]. In this
latter study more than a half of a Swiss canine popula-
tion has been found to shed helminth eggs at least once
in 1 year despite quarterly deworming. More specifically,
a yearly incidence of 32% of T. canis infection has been
found in dogs that received four anthelmintic treatments
per year [51].
As mentioned earlier, in US settings the routine
monthly parasiticide administration is sometimes per-
formed along with annual or semi-annual fecal examina-
tions [47,68].
In any case, the monthly treatment approach appears
to have several benefits, especially when performed with
a macrolactone, which can accomplish the suppression
of most important parasitic nematodes affecting pets
[179].
On the other hand, the possibility of using a year
round treatment is particularly important in those
regions where there is a systematic necessity to perform
the annual chemoprophylaxis for other major parasites.
A year-round control program with molecules which
can be monthly administered for the prevention of
cardio-pulmonary nematodes, i.e. Dirofilaria immitis
(e.g. ivermectin, moxidectin, milbemycin oxime) and
Angiostrongylus vasorum (i.e. moxidectin), is powerful
also to achieve a decrease in prevalence of intestinal
nematodes [49,180].
A year round program would be powerful also in feline
patients, given that the level of nematode transmission is
higher in free-roaming cats than in cats which receive
adequate sanitary care [181]. However, recent studies
have proved high prevalence rates, at least for T. cati,
also in pet household cats [182-184].
The other side of the coin says that frequent use of
anthelmintics in companion animals could have
detrimental effects. In the past decades the abuse of
parasiticides has led to the emergence of livestock and
horse parasites resistant to one or more anthelmintic
classes. As a general approach, the administration of a
broad-spectrum parasiticide without a copromicroscopic
examination should be discouraged considering that the
unnecessary use of anthelmintics has major influence in
promoting drug resistance. Hence, a concern related to
frequent anthelmintic treatments could be an increase of
drug resistant populations of pet nematodes, especially
for long-term indiscriminate use of parasiticides, which
have been on the market (often over-the-counter) over a
long time. Indeed, at the moment there is only evidence
of resistance to pyrantel in A. caninum [185]. Although
pyrantel is not used for monthly prevention of cardio-
pulmonary parasites and no data have emerged for
roundworms, a high level of attention should always be
maintained to detect any hint of drug resistance in pet
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nematodes. This is even more relevant considering that
there is the first laboratory evidence that D. immitis can
develop a degree, although yet to be established, of sur-
vival to certain parasiticides [186].
The present very limited evidence of drug resistance in
small animal parasites is likely due to the fact that pets
are most often kept individually or in small numbers,
thus dynamics of parasitic populations and influence on
refugia is very different from what happens in livestock.
Pets are usually treated individually, thus most round-
worms and hookworms in a given area escape from the
treatment and remain in the refugium [13]. Nonetheless,
the indiscriminate use of anthelmintics in concentrated
groups of small animals (e.g. kennels, colonies, shelters,
breeding facilities) might nurture the development of re-
sistant nematodes [187].
The importance of copromicroscopic examinations
The misconceptions that only young animals should be
dewormed and a single treatment clears a “generally”
parasitized animal, induce negligence in performing
diagnostic copromicroscopy in veterinary practices.
Conversely, systematic copromicroscopic examinations
should be regularly instituted for companion animals,
which, in turn, are virtually subjected for all their life-
span to continuous re-infection by roundworms and
hookworms, even when they have a lifestyle far from
that of stray animals or of animals kept in shelter or
refuges [47,188-190].
Copromicroscopic techniques, e.g. floatation methods
or commercial kits, are easy to perform in clinical
practices. Nonetheless, diagnostic challenges may arise
for both ascaridosis and ancylostomosis. Pre-patency
period greatly affects diagnosis and effective control pro-
grams: parasitic ova can be detected at faecal examin-
ation only after nematode development, mating and
patency, i.e. in some cases even a few weeks post infec-
tion and appearance of clinical signs. As a key example,
it has been shown that the vast majority of dogs aged
less that 6 weeks are infected by intestinal roundworms,
although they may score negative at the copromicro-
scopic examination [6,191]. The same challenge may
occur in puppies infected by hookworm larvae origi-
nated from their dam, in that these nematodes shed eggs
by the tenth day of infection, thus after the symptoms
appear. Diagnosis in these pups may be achieved only on
clinical signs like, for instance, pale mucosae and soft to
liquid dark faeces. Also, symptoms caused by acute
ancylostomosis due to sudden exposure to infective lar-
vae in whelps and adults may appear about four days
before egg shedding, thus making diagnosis very prob-
lematic [16,27].
Faecal examinations should not be related to patient’s
health and must be performed regardless of the presence
of gastrointestinal symptoms (e.g. diarrhoea, vomiting,
etc.). This is of importance given that, for instance, no
significant differences in nematode infection in symp-
tomatic dogs, compared with animals without clinical
signs has been found [49,53,192]. However, asymptom-
atic animals are usually considered parasite-free, thus
their owners may be not interested in routine examin-
ation for parasites with subsequent treatment if neces-
sary [59]. Such an approach should be discouraged,
given that asymptomatic dogs are as likely to be infected
as animals with clinical evidence. Therefore, these
categories present the same level of zoonotic risk, which
may not be fully appreciated by pet owners [59,193-195].
There are, however, situations where awareness of pet
owners on zoonotic diseases is very high and they accept
to have their pets undertaken on regular control plans
[47,196]. Furthermore, repeated faecal examinations
throughout the lifespan of a pet are of paramount
importance even in well- cared for dogs and cats, given
that recurrence of parasites is possible, regardless of
whether they undergo a control anthelmintic program
or not [51,53].
From a practical standpoint, the pneumonic phase of
larval migrations can only be suspected for the
simultaneous appearance of respiratory symptoms in all
puppies of a litter within two weeks after birth. Specific
diagnosis of patent toxocarosis is achieved through stand-
ard copromicroscopic floatation because eggs of T. canis,
T. cati and T. leonina (Figure 3) are usually present in
high number and easy to identify. However, in certain
areas of the World (e.g. North America) the raccoon
roundworm Baylisascaris procyonis can pose diagnostic
challenges. This ascarid causes patent infections also in
dogs [197,198], and its eggs greatly resemble those of
T. canis, thus representing a diagnostic problem and an
important danger for human health. In fact, the vast
majority of humans who ingest infective eggs of B. procyo-
nis suffer from severe permanent neurological damage or
even die [199]. Hence, at least where this parasite is
endemic, veterinary personnel must be skillful and trained
in recognizing eggs of B. procyonis for preservation of the
public health of people eventually exposed to faeces elimi-
nated by dogs infected by B. procyonis.Eventhoughthisis
true for North America, this parasite has been introduced
also in Europe and Asia with its natural wild host [200].
Hence, what the future will hold on this life-threatening
zoonosis in other continents is currently unknown.
Diagnosis of ancylostomosis in dogs and cats cannot
be achieved at the species level for the overlapping
morphological and morphometric features of Ancylostoma
spp. eggs (Figure 3). Coprocultures can be performed for a
specific diagnosis but, from a practical standpoint, the
presence of hookworm eggs in pets’faeces would require
a parasiticide treatment regardless of the species affecting
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the animal. Eggs of U. stenocephala (Figure 3) can be
identified by their larger size [36].
Veterinarians should convince pet owners of the import-
ance of periodic faecal examinations. In the first year of life
any pet should undergo at least 2–4 copromicroscopic
examinations and then, when adult, it should be examined
more than once per year according to health status, lifestyle
and frequency of treatments. Specifically, free ranging
animals and those living indoors but allowed to go
outside should always be subjected to regular examination
of the faeces. Particular attention should be given to
copromicroscopic analyses carried out in the worm con-
trol programs. When a monthly-based treatment program
is not performed, faecal examinations every 1–3months
of susceptible pets is an efficacious way of evaluating
the re-occurrence of intestinal parasitoses in previously
treated animals. Indeed, post-treatment faecal examina-
tions are important to evaluate success of drug admin-
istration and, in a future perspective, to detect any
indication of drug resistance in ancylostomatids and
ascarids. On the other hand, coprophagy is relatively
commonindogs,thusthepresenceofeggsinstool
samples after treatment could often be due not to
failure of treatments but rather to ingestion of their
own defecation or other animals’faeces [84].
Awareness of the general public and pet owners: A need
to enhance risk perception without causing alarm
Controlling ascaridosis and ancylostomosis in pets is
crucial to reduce infection risk for other companion
animals and to minimize public health hazards. All
categories involved in pet medicine should take care of
animal health and public behavior, given that human
syndromes caused by pet nematodes may lead to
permanent damage [18,88].
Awareness of pet owners and the general public and
continuous education of veterinarians are at the basis of
effective prevention. Dissemination of understanding
and knowledge of transmission routes, at-risk categories
and areas, and control methods are pivotal to minimize
possibilities of human and animal infections. Although
virtually all of the majority of roundworms and hook-
worms affecting dogs and cats may cause human
diseases, the public risk perception in general is poor. As
a key example, despite the infection by Toxocara spp. is
the most prevalent human helminthosis in some indus-
trialized countries, public awareness of this syndrome is
scant [201]. A survey carried out in the UK has shown
than less than the half of the people interviewed, includ-
ing pet-owners and non-pet-owners, perceived the risk
of transmission of nematodes from pets to humans.
Interestingly, no differences in hazard awareness was
found between people who owned a pet and people who
did not [202]. Another study performed in a developed
area of Brazil has demonstrated that the majority of dog
owners did not know about intestinal parasites, sources
of infections, possible risk factors for zoonoses and fo-
cused prophylactic measures. Therefore, the high pres-
ence of zoonotic species in owned dogs of the
studied region, along with the lack of information
Figure 3 Floatation with zinc sulphate: eggs of Toxocara canis (A), Toxocara cati (B), Toxascaris leonina (C), Uncinaria stenocephala (D1)
and Ancylostoma caninum (D2).
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known by owners, endorse that the risk of zoonotic
infection by canine intestinal nematodes may be in-
deed high [59].
Veterinarians, who are the most appropriate and ques-
tioned source of information on zoonoses, should always
provide pet owners with accurate worming schedules
and their efficacy, and appropriate all-day-life measures.
This is of particular importance if one considers that
veterinarians are a more congruous source of knowledge
on zoonoses than physicians [203]. Nonetheless, lack of
education has been well documented also in veterinary
professions [203-205]. In Canada less than the half of
practitioners working in small animal practices declared
that they talked with pet-owners about the zoonotic risk
of pet endoparasites, while the remaining did so only
under particular circumstances or did not at all [206]. In
the USA it has been recently suggested that a national
surveillance program should be established in order to
better understand specific aetiology of human larva
migrans syndromes and their actual incidence, in order
to aim for focused intervention programs [18]. More
interview- based studies are warranted in other countries
to implement our understanding of how the risk percep-
tion is diffused in the population and, more importantly,
to implement awareness of the general public and of pet
owners.
No practical methods exist to eliminate infective
elements of intestinal nematodes of pets (especially for
ascarids) present on the ground, thus prevention of
initial contamination of the environments is the key
goal. Veterinarians should inform all owners about ways
of transmission for their pet and for themselves, and
about clinical evidence for diseases and methods of
prevention. On the other hand, any pet owner should
clearly acquire relevant information and have appropri-
ate behavior. In fact, an important cause of the heavy
outdoor presence of infectious parasitic elements is lack
of education (and of awareness on the actual zoonotic
risk) by pet owners. Sites shared by children and animals
like backyards, sandpits, parks, playgrounds, beaches,
often represent a risk for the heavy contamination by
pet faeces. Public parks may be highly contaminated by
eggs of T. canis, while sand-boxes and sand-pits by those
of T. cati [18,88,90,207,208]. Hence, common prevention
practices, which should be known by any pet owner are
covering sandboxes, avoiding animal defecation in public
areas or at least always clean animal faeces from the
ground. In fact, educating owners on regular removal
and disposal of faeces and to empty cat litter trays is of
paramount importance to minimize environmental con-
tamination and risk of transmission to both animals and
humans [6,79]. When walking their pets in public areas,
all owners should respect local indications (Figure 4)
and keep their animals in reserved areas, if present.
With regard to hookworms, sites favoring survival and
development of free-living larvae are shaded, warm,
humid and well-drained soils. Furthermore, unpaved
runs are highly favorable for hookworm larvae because
of mixing of faeces and soils. Prevention of animal and
human ancylostomosis relies on adequate hygiene
measures (e.g. hand and feet washing), removal of pet
faeces and, importantly, wearing shoes and avoiding
lying on risky areas or, in any case, where there is the
likelihood that animals usually defecate.
Hookworms and travelling
Tourists travelling in at risk zones for CLM should be
careful in walking barefoot on beaches and in lying
down on the sand, especially because A. braziliense is
endemic in popular tourist areas. These human categor-
ies are susceptible to infection at their vacation destin-
ation and then may return home infected at the end of
the holiday, often providing a challenging dilemma to
their physician.
Nonetheless, autochthonous reports of CLM have been
reported from countries where the tropical A. braziliense
is absent, thus these cases are considered “unexpected”
[26]. Unfortunately no identification to species of larvae
found at biopsies has been performed, thus only hypoth-
eses are available on the identity of hookworm involved.
As key examples, CLM cases possibly by U. stenocephala
and/or A. caninum have been recorded in the UK and
New Zealand. Several other local cases of CLM by
unidentified hookworms have been described in Italy,
Serbia, Germany, France and UK as well [26]. Although
few in number, these cases in areas where A. caninum,
A. tubaeforme and U. stenocephala are present, show a
possible risk for human infections, characterized by
skin conditions, which, possibly, could also involve
other conditions (e.g. pneumonitis). Also, it cannot be
ruled out that these few cases published could be the
tip of the iceberg and that others are not diagnosed or
not even referred to physicians. The number of CLM in
“unexpected”countries could be much higher than
thought, thus not only travelers and tourists spending
holidays in tropical zones considered “risky”can be
faced with these infections but all humans exposed to
soil contaminated by larval hookworms.
Conclusion
Given the clinical importance of intestinal nematodes
affecting pets, their ubiquitous presence and the
zoonotic impact some of them have, public education is
crucial for reducing risk exposure in both humans and
companion animals. At the same time pet owners and,
in general, the public opinion should maintain a self-
confidence that keeping a pet is safe and a positive ex-
perience. This is also true when close-contact occurs
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between the pet and the owner, even when some behav-
iour can be questionable (Figure 5). Actually, it is estab-
lished that direct contact with infected pets presents no
relevant risk in the transmission of intestinal nematodes
and there is no association between pet ownership and
infection occurrence [78,79]. Owners should have confi-
dence that ownership of any companion animal is bene-
ficial and safe as long as their pets are healthy [18]. Pet
owners enjoy a plethora of advantages by living with
dogs and/or cats. For instance, children, the elderly and
disabled persons particularly benefit from their contact
with a beloved pet. Companion animals represent a way
of life for a lot of the people and this relationship
provides socialization, mental health, and physical well-
being: those who own a pet have been shown to display
reduction in blood pressure and cholesterol levels,
require less medical care, and it has also been reported
that there is an improvement of life quality and quick
recovery after heartbreaking events [209-213]. Therefore,
owning companion animals is vital for the majority of
families, especially when children and the elderly are
present [212,214]. However, the potential risks of pet-
originating zoonoses should always be kept in mind.
This has become even more so in recent years, when
several sociological changes have influenced the relation-
ships between physicians and veterinarians. In fact, the
major goal of the re-discovered “One Health Program”
(i.e. “the collaborative work of multiple disciplines to help
attain optimal health of people, animals, and our
environment”) highlights the crucial role of a tight tie
between the human health operators, vet practitioners,
and the general public [213].
For instance advances in chemotherapy for AIDS and
new possibilities of organ transplants, and the
prolonged life expectancy, have increased the number
of immunocompromised patients in human communi-
ties. These subjects need to be aware of possible
zoonotic parasites and of all measures to prevent
infections for their pets and for themselves. It is worth
highlighting that immunocompromised individuals
should not give up their animal, as it has been demon-
strated that pet ownership minimizes depression and
Figure 4 Dog-reserved areas and indications for pet owners in public areas in Valencia, Spain (A), Praha, Czech Republic (B) and
Melbourne, Australia (C).
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that standard hygiene measures reduce at minimum the
risk of acquiring zoonotic infections in this particular
category [215,216].
A desirable goal for effective control programs would
also be to understand which are changes and trends in
terms of prevalence of infection by ascarids and hook-
worms in canine and feline populations, with the simul-
taneous aim to track incidence of human cases caused
by each of the single aetiological agents. This would be a
basic step to cope with current weaknesses in prevention
approaches and to establish where to intervene with fo-
cused plans. In fact, updated information on prevalence
of parasites of dogs and cats and the risk factors asso-
ciated with infection, as well as reinforcing veterinary
and public health concerns, is of crucial relevance
because common awareness is non-existent or often
based on outdated information.
The cornerstone to control intestinal parasitoses of
pets is a combination of strategic worming methods
(especially puppies, kittens and dams), wearing footwear
when needed, supervising playing children and their
interactions with pets, breaking faecal-oral routes by
washing hands and removal and disposal of faeces from
public and private grounds and litter trays, alimentary
habits [216-218].
Ten years ago it was perceived that veterinary parasit-
ology was becoming irrelevant in routine clinical practice
[219]. Regrettably, after more than ten years this perception
is practically a reality in several settings. The involvement
of practitioners in a worming control program is no more
than the administration of one of the several broad-
spectrum parasiticides available on the market, even in the
absence of evident parasitosis or without a copromicro-
scopic examination. Such a fallacy comes from the miscon-
ceptions that a deep knowledge of epidemiology and
biology of certain parasites is superfluous and that control
of major helminths can be achieved just with a periodic
medication. Nonetheless, roundworms and hookworms re-
main today the most diffused nematodes affecting pets
around the world and they still cause zoonotic infections in
humans.Thereis,therefore,theevidence,thatscientists,
pet owners and veterinarians should re-consider their ap-
proach on parasitology and foster their interest not only in
emergent parasites like cardio-pulmonary nematodes or
water-borne protozoa, but also in “old-fashioned”intestinal
worms.
Figure 5 Close contact between privately owned pets and their owners. Although this behavior can be questionable, it cannot be
considered at risk of infection with zoonotic nematodes for the owners.
Traversa Parasites & Vectors 2012, 5:91 Page 14 of 19
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Given that parasitic zoonoses are too often neglected
or underappreciated, and may be mismanaged or
underdiagnosed by both veterinarians and physicians
[213], a strong education outreach by veterinary and
medical practitioners should be accomplished [214,220].
Veterinarians must keep their guard up against zoonotic
parasitoses of pets and constantly provide advice and
improve knowledge of their clients, with a special focus
on those human categories, who are at higher risk of in-
fection, in order to allow pets to remain integral mem-
bers of household and families. Furthermore, owners
should become aware of “invisible”beneficial effects of a
lifespan control program based on routine faecal exami-
nations and frequent worming.
New concepts for accurate preventative plans have
been generated based on several individual and
epidemiological circumstances. The role of the veteri-
narians and constant compliance of the owners are
crucial for the success of worm control programs in
pets. Additionally, the present climate changes and
global warming supports the need for a continuous
global worming, given that faster egg embryonation
and increased over-wintering of infectious elements in
the environment will likely increase the spread of
helminths affecting companion animals and humans in
several areas of the World, as recently hypothesized
for sub-Arctic and Arctic regions [221].
Competing interests
Scientific aspects of the article have not been influenced by any third party.
Acknowledgements
The author thanks Angela Di Cesare for the elaboration of bibliographic data,
Riccardo Lia for Figures 1 and 3D, Asaf Kohane for Figure 2 and Antonio
Frangipane di Regalbono for Figure 3C.
The author expresses his gratitude and devotion to his loves in Figure 5:
Alessandra, Maria, Pata, Inca, Ruffi and Trizma.
Author contribution
DT conceived the intellectual content of the article and wrote the text.
Received: 16 February 2012 Accepted: 22 April 2012
Published: 10 May 2012
References
1. Morey DF: The early evolution of the domestic dog. Sci Am 1994, 82:336–347.
2. Otranto D, Traversa D: Thelazia eyeworm: an original endo- and ecto-
parasitic nematode. Trends Parasitol 2005, 21:1–4.
3. Traversa D, Di Cesare A, Conboy G: Canine and feline cardiopulmonary
parasitic nematodes in Europe: emerging and underestimated. Parasit
Vectors 2010, 3:62.
4. Otranto D, Eberhard ML: Zoonotic helminths affecting the human eye.
Parasit Vectors 2011, 4:41.
5. Jefferies R, Shaw SE, Willesen J, Viney ME, Morgan ER: Elucidating the
spread of the emerging canid nematode Angiostrongylus vasorum
between Palaearctic and Nearctic ecozones. Infect Genet Evol 2010,
10:561–568.
6. Robertson ID, Thompson RC: Enteric parasitic zoonoses of domesticated
dogs and cats. Microbes Infect 2002, 4:867–873.
7. Anderson RC: Nematode Parasites of Vertebrates.InTheir development and
transmission. 2nd edition. Guilford: CABI; 2000.
8. Antolová D, Reiterová K, Miterpáková M, Stanko M, Dubinský P: Circulation
of Toxocara spp. in suburban and rural ecosystems in the Slovak
Republic. Vet Parasitol 2004, 126:317–324.
9. Traversa D: Are we paying too much attention to cardio-pulmonary
nematodes and neglecting old-fashioned worms like Trichuris vulpis?
Parasit Vectors 2011, 4:32.
10. Lloyd S, Amersinghe PH, Soulsby EJL: Periparturient immunosuppression
in the bitch and its influence on infection with Toxocara canis.J Small
Anim Pract 1983, 24:237–247.
11. Lloyd S: Toxocara canis:thedog.InIn Toxocara and Toxocariasis
Clinical, Epidemiological and Molecular Perspectives. Edited by Lewis JW,
Maizels RM. London: British Society for Parasitology. Institute of Biology;
1993:11–24.
12. Zimmermann U, Löwenstein MD, Stoye M: Migration and distribution of
Toxocara canis Werner 1782 (Anisakidae) larvae in the definitive host
(beagle) following primary infection and reinfection. Zentralbl
Veterinarmed B 1985, 32:1–28. (in German).
13. Epe C: Intestinal nematodes: biology and control. Vet Clin North Am Small
Anim Pract 2009, 39:1091–1107. vi-vii.
14. Swerczek TW, Nielsen SW, Helmboldt CF: Transmammary passage of
Toxocara cati in the cat. Am J Vet Res 1971, 32:89–92.
15. Coati N, Schnieder T, Epe C: Vertical transmission of Toxocara cati Schrank
1788 (Anisakidae) in the cat. Parasitol Res 2004, 92:142–146.
16. Bowman DD: Georgi's Parasitology for Veterinarians. 9th edition.: Saunders
Company; 2009.
17. Bowman DD, Hendrix CM, Lindsay DS, Barr SC: Feline Clinical Parasitology.
Iowa State University: Blackwell Science Company; 2002.
18. Lee CY, Schantz PM, Kazacos KR, Montgomery SP, Bowman DD:
Epidemiologic and zoonotic aspects of ascarid infections in dogs and
cats. Trends Parasitol 2010, 26:155–161.
19. Parsons JC: Ascarid infections of cats and dogs. Vet Clin North Am Small
Anim Pract 1987, 17:1307–1339.
20. Taylor MA, Coop RL, Wall RL: Veterinary Parasitology. 3rth edition.: Blackwell
Publishing; 2007.
21. Sprent JF: Observations on the development of Toxocara canis (Werner,
1782) in the dog. Parasitology 1958, 48:184–209.
22. Prociv P: Zoonotic hookworm infections (Ancylostomosis).InIn Zoonoses.
1st edition. Edited by Palmer SR, Soulsby EJL, Simpson DIH.: Oxford Medical
Publications; 1998.
23. Manning L, Chambers S, Paltridge G, Maurice P: Cutaneous larva migrans
(hookworm) acquired in Christchurch. New Zealand. N Z Med J 2006,
119:1910–1913.
24. Palmer CS, Traub RJ, Robertson ID, Hobbs RP, Elliot A, While L, Rees R,
Thompson RC: The veterinary and public health significance of
hookworm in dogs and cats in Australia and the status of A. ceylanicum.
Vet Parasitol 2007, 145:304–313.
25. Traub RJ, Hobbs RP, Adams PJ, Behnke JM, Harris PD, Thompson RC: A case
of mistaken identity reappraisal of the species of canid and felid
hookworms (Ancylostoma) present in Australia and India. Parasitology
2007, 134:113–119.
26. Bowman DD, Montgomery SP, Zajac AM, Eberhard ML, Kazacos KR:
Hookworms of dogs and cats as agents of cutaneous larva migrans.
Trends Parasitol 2010, 26:162–167.
27. Bowman DD: Georgi's Parasitology for Veterinarians. 7th edition.: Saunders
Company; 2002.
28. Stoye M: Galactogenic and prenatal Toxocara canis infections in dogs
(Beagle). Dtsch Tierarztl Woch 1976, 83:107–108. in German.
29. Stoye M: Biology, pathogenicity, diagnosis and control of Ancylostoma
caninum.Dtsch Tierarztl Woch 1992, 99:315–321. in German.
30. BosseM,ManhardtJ,StoyeM:Epidemiology and Control of neonatal
Helminth Infections of the dog. Fortschr Vet Med 1980, 30:247–256. in German.
31. Stoye M: Ascarid and Ancylostomatid infections of the dog. Tieraerztl Prax
1983, 11:229–243. in German.
32. Stoye M: Ascarid and hookworm infections in the dog biology, epizootology
and control. Berl Muench Tieraerzt Wschr 1979, 92:464–472. in German.
33. Clapham PA: Canine hookworm disease. J Small Anim Pract 1962, 3:133–136.
34. Stoye M: Studies on the possibility of prenatal and galactogenic
infections with Ancylostoma caninum Ercolani 1859 (Ancylostomidae) in
the dog. Zbl Vet Med B 1973, 20:1–39. in German.
35. Stone WM, Peckham JC: Infectivity of Ancylostoma caninum larvae
from canine milk. Am J Vet Res 1970, 31:1693–1694.
Traversa Parasites & Vectors 2012, 5:91 Page 15 of 19
http://www.parasitesandvectors.com/content/5/1/91

36. Kalkofen UP: Hookworms of dogs and cats. Vet Clin North Am Small Anim
Pract 1987, 17:1341–1354.
37. Enigk K, Stoye M: Studies of the pathway of infection of Ancylostoma
caninum.Med Klin 1968, 63:1012–1017. in German.
38. Soulsby EJL: Helminths, Arthropods and Protozoa of Domesticated Animals.
7th edition.: Bailliere Tindall; 1982.
39. Miller TA: Vaccination against the canine hookworm diseases. Adv
Parasitol 1971, 9:153–183.
40. Walker MJ, Jacobs DE: Pathophysiology of Uncinaria stenocephala
infections of dogs. Vet Annual 1985, 25:263–271.
41. Visco RJ, Corwin RM, Selby LA: Effect of age and sex on the prevalence
ofintestinal parasitism in dogs. J Am Vet Med Assoc 1977, 170:835–837.
42. Visco RJ, Corwin RM, Selby LA: Effect of age and sex on the prevalence of
intestinal parasitism in cats. J Am Vet Med Assoc 1978, 1978(172):797–800.
43. Lloyd S: Toxocarosis.InIn: Zoonoses. Biology, Clinical Practice and Public
Health Control. Edited by Palmer SR, Soulsby EJL, Simpson DIH. Oxford:
Oxford University Press; 1998:841–854.
44. Malloy WF, Embil JA: Prevalence of Toxocara spp. and other parasites in
dogs and cats in Halifax, Nova Scotia. Can J Comp Med 1978, 42:29–31.
45. Martínez-Barbabosa I, Vázquez Tsuji O, Cabello RR, Cárdenas EM, Chasin OA:
The prevalence of Toxocara cati in domestic cats in Mexico City. Vet
Parasitol 2003, 114:43–49.
46. Fahrion AS, Staebler S, Deplazes P: Patent Toxocara canis infections in
previously exposed and in helminth-free dogs after infection with low
numbers of embryonated eggs. Vet Parasitol 2008, 152:108–115.
47. Little SE, Johnson EM, Lewis D, Jaklitsch RP, Payton ME, Blagburn BL,
Bowman DD, Moroff S, Tams T, Rich L, Aucoin D: Prevalence of intestinal
parasites in pet dogs in the United States. Vet Parasitol 2009, 166:144–152.
48. Scorza AV, Duncan C, Miles L, Lappin MR: Prevalence of selected zoonotic
and vector-borne agents in dogs and cats in Costa Rica. Vet Parasito
2011, 183:178–183.
49. Savilla TM, Joy JE, May JD, Somerville CC: Prevalence of dog intestinal
nematode parasites in south central West Virginia, USA. Vet Parasitol
2011, 178:115–120.
50. Barutzki D, Schaper R: Results of parasitological examinations of faecal
samples from cats and dogs in Germany between 2003 and 2010.
Parasitol Res 2011, 109(Suppl 1):S45–60.
51. Sager H, Moret ChS, Grimm F, Deplazes P, Doherr MG, Gottstein B:
Coprological study on intestinal helminths in Swiss dogs: temporal
aspects of anthelminthic treatment. Parasitol Res 2006, 98:333–338.
52. Maizels RM, Meghji M: Repeated patent infection of adult dogs with
Toxocara canis.J Helminthol 1984, 58:327–333.
53. Gates MC, Nolan TJ: Endoparasite prevalence and recurrence across
different age groups of dogs and cats. Vet Parasitol 2009, 166:153–158.
54. Blagburn BL, Lindsay DS, Vaughan JL, Rippey NS, Wright JC, Lynn RC, Kelch
WJ, Ritchie GC, Hepler DI: Prevalence of canine parasites based on fecal
flotation. Comp Cont Ed 1996, 18:483–509.
55. Barutzki D, Schaper R: Endoparasites in dogs and cats in Germany
1999–2002. Parasitol Res 2003, 90(Suppl 3):S148–150.
56. Roddie G, Stafford P, Holland C, Wolfe A: Contamination of dog hair with
eggs of Toxocara canis.Vet Parasitol 2008, 152:85–93.
57. Sowemimo OA: The prevalence and intensity of gastrointestinal parasites
of dogs in Ile-Ife, Nigeria. J Helminthol 2009, 83:27–31.
58. Fontanarrosa MF, Vezzani D, Basabe J, Eiras DF: An epidemiological
study of gastrointestinal parasites of dogs from Southern Greater
Buenos Aires (Argentina): age, gender, breed, mixed infections, and
seasonal and spatial patterns. Vet Parasitol 2006, 136:283–295.
59. Katagiri S, Oliveira-Sequeira TC: Prevalence of dog intestinal parasites and
risk perception of zoonotic infection by dog owners in Sao Paulo State,
Brazil. Zoonoses Public Health 2008, 55:406–413.
60. Martinez-Moreno FJ, Hernandez S, Lopez-Cobos E, Becerra C, Acosta I,
Martinez-Moreno A: Estimation of canine intestinal parasites in
Cordoba (Spain) and their risk to public health. Vet Parasitol 2007,
143:7–13.
61. Day MJ: Immune system development in the dog and cat. J Comp Pathol
2007, 137(Suppl 1):S10–15.
62. Muirhead TL, McClure JT, Wichtel JJ, Stryhn H, Frederick Markham RJ,
McFarlane D, Lunn DP: The effect of age on serum antibody titers
after rabies and influenza vaccination in healthy horses. J Vet Intern
Med 2008, 22(3):654–661.
63. Vossmann T, Stoye M: Clinical, hematologic and serologic findings in puppies
after prenatal infection with Toxocara canis Werner 1782 (Anisakidae). Journal
of Veterinary Medicine Series B 1986, 33:574–585. in German.
64. Dade JW, Williams JF: Hepatic and peritoneal invasions by adult ascarids
(Toxocara canis) in dog. Vet Med Small Anim Clin 1975, 70:947–949.
65. Hendrix CM: Helminth infections of the feline small and large intestine:
diagnosis and treatment. Vet Med 1995, 90:456–476.
66. Eckert J: Helminthosen von Hund und Katze.InIn Veterinarmedizinische
Parasitologie. 5th edition. Edited by Rommel M, Eckert J, Kutzer E, Körting W,
Schneider T. Berlin: Verlag Paul Parey; 2000:545–604.
67. Aoki S, Yamagami T, Saeki H, Washizu M: Perforated gastric ulcer caused
by Toxocara cati in a cat. J Jao Vet Med Assoc 1990, 43:207–210.
68. Companion Animal Parasite Council. [www.capcvet.org].
69. Parsons JC, Bowman DD, Gillette DM, Grieve RB: Disseminated
granulomatous disease in a cat caused by larvae of Toxocara canis.
J Comp Pathol 1988, 99:343–346.
70. Okoshi S, Usui M: Experimental studies on Toxascaris leonina. II. Diagnosis
and treatment of toxascariasis in dogs and cats. Nihon Juigaku Zasshi
1967, 29:245–250. in Japanese.
71. Fei ACY, Jeng CR, Lay RY: Toxascaris leonina infection in a kitten. J Chinese
Soc Vet Sci 1986, 12:61–63.
72. Onwuliri CO, Nwosu AB, Anya AO: Experimental Ancylostoma tubaeforme
infection of cats: changes in blood values and worm burden in relation
to single infections of varying size. Z Parasitenkd M 1981, 64:149–155.
73. Glickman LT, Shofer FS: Zoonotic visceral and ocular larva migrans. Vet
Clin North Am Small Anim Pract 1987, 17:39–53.
74. Glickman LT, Schantz PM: Epidemiology and pathogenesis of zoonotic
toxocariasis. Epidemiol Rev 1981, 3:230–250.
75. Stürchler D, Weiss N, Gassner M: Transmission of toxocariasis. J Infect Dis
1990, 162(2):571.
76. Salem G, Schantz P: Toxocaral visceral larva migrans after ingestion of
raw lamb liver. Clin Infect Dis 1992, 15:743–744.
77. Wolfe A, Wright IP: Human toxocariasis and direct contact with dogs. Vet
Rec 2003, 152:419–422.
78. Overgaauw PAM: Aspects of Toxocara epidemiology: toxocarosis in dogs
and cats. Crit Rev Microbiol 1997, 23:233–251.
79. Overgaauw PAM: Aspects of Toxocara epidemiology: human toxocarosis.
Crit Rev Microbiol 1997, 23:215–231.
80. Overgaauw PAM, Van Knapen F: Negligible risk of visceral or ocular larva
migrans from petting a dog. Ned Tijdschr Geneeskd 2004, 148:1600–1603.
81. Overgaauw PA, van Zutphen L, Hoek D, Yaya FO, Roelfsema J, Pinelli E, van
Knapen F, Kortbeek LM: Zoonotic parasites in fecal samples and fur from
dogs and cats in The Netherlands. Vet Parasitol 2009, 163:115–122.
82. Puccini V: Soulsby EJL: Guida alle Malattie Parassitarie. Bologna, Italy:
Edagricole; 1992.
83. Keegan JD, Holland CV: Contamination of the hair of owned dogs with
the eggs of Toxocara spp. Vet Parasitol 2010, 173:161–164.
84. Nagy A, Ziadinov I, Schweiger A, Schnyder M, Deplazes P: Hair coat
contamination with zoonotic helminth eggs of farm and pet dogs and
foxes. Berl Munch Tierarztl Wochenschr 2011, 124:503–511. in German.
85. World Health Organization and partners unveil new coordinated approach to
treat millions suffering from neglected tropical disease. [http://whqlibdoc.who.
int/press_release/2006/PR].
86. Wilder HC: Nematode endophthalmitis. Trans Am Acad Ophthalmol
Otolaryngol 1950, 55:99–109.
87. Beaver PC, Snyder CH, Carrera GM, Dent JH, Lafferty JW: Chronic
eosinophilia due to visceral larva migrans; report of three cases.
Pediatrics 1952, 9:7–19.
88. Despommier D: Toxocariasis: clinical aspects, epidemiology, medical
ecology, and molecular aspects. Clin Microbiol Rev 2003, 16:265–272.
89. Dubinsky P, Havasiova-Reiterova K, Petko B, Hovorka I, Tomasovicova O:
Role of small mammals in the epidemiology of toxocariasis. Parasitology
1995, 110:187–193.
90. Holland CV, Smith HV: Toxocara: The Enigmatic Parasite.: CABI Publishing; 2006.
91. Dogan N, Dinleyici EC, Bor O, Toz SO, Ozbel Y: Seroepidemiological survey
for Toxocara canis infection in the northwestern part of Turkey. Turkiye
Parazitol Derg 2007, 31:288–291.
92. Schantz PM: Toxocara larva migrans now. AmJTrop Med Hyg 1989, 41:21–34.
93. Worley G, Green JA, Frothingham TE, Sturner RA, Walls KW, Pakalnis VA, Ellis GS Jr:
Toxocara canis infection: clinical and epidemiological associations with
seropositivity in kindergarten children. JInfectDis1984, 149:591–597.
Traversa Parasites & Vectors 2012, 5:91 Page 16 of 19
http://www.parasitesandvectors.com/content/5/1/91

94. Magnaval JF, Michault A, Calon N, Charlet JP: Epidemiology of human
toxocariasis in La Reunion. Trans R Soc Trop Med Hyg 1994, 88:531–533.
95. Rayes AA, Teixeira D, Serufo JC, Nobre V, Antunes CM, Lambertucci JR:
Human toxocariasis and pyogenic liver abscess: a possible association.
Am J Gastroenterol 2001, 96:563–566.
96. Mimoso MG, Pereira MC, Estevao MH, Barroso AA, Mota HC: Eosinophilic
meningoencephalitis due to Toxocara canis. Eur J Pediatr 1993, 152:783–784.
97. Shetty AK, Aviles DH: Nephrotic syndrome associated with Toxocara canis
infection. Ann Trop Paediatr 1999, 19:297–300.
98. Prunier F, Delepine S, Victor J, de Gentile L, Moreau C, Laporte J, Dupuis JM,
Geslin P: Loffler's fibroblastic endocarditis. A report of a case complicating
toxocarosis. Arch Mal Coeur Vaiss 2001, 94:226–230. in French.
99. Dinning WJ, Gillespie SH, Cooling RJ, Maizels RM: Toxocariasis: a practical
approach to management of ocular disease. Eye (Lond) 1988, 2(Pt 5):580–582.
100. Small KW, McCuen BW 2nd, de Juan E Jr, Machemer R: Am J Ophthalmol
1989, 108:10–14.
101. Lopez-Velez R, Suarez de Figueroa M, Gimeno L, Garcia-Camacho A, Fenoy S,
Guillen JL, Castellote L: Ocular toxocariasis or retinoblastoma? Enferm Infecc
Microbiol Clin 1995, 13:242–245. in Spanish.
102. Wolach B, Sinnreich Z, Uziel Y, Gotesman G, Pomerantz A: Toxocariasis: a
diagnostic dilemma. Isr J Med Sci 1995, 31:689–692.
103. Critchley EM, Vakil SD, Hutchinson DN, Taylor P: Toxoplasma,Toxocara, and
epilepsy. Epilepsia 1982, 23:315–321.
104. Taylor MR, Keane CT, O'Connor P, Girdwood RW, Smith H: Clinical features
of covert toxocariasis. Scand J Infect Dis 1987, 19:693–696.
105. Glickman LT, Magnaval JF, Domanski LM, Shofer FS, Lauria SS, Gottstein B,
Brochier B: Visceral larva migrans in French adults: a new disease
syndrome? Am J Epidemiol 1987, 125:1019–1034.
106. Nathwani D, Laing RB, Currie PF: Covert toxocariasis–a cause of recurrent
abdominal pain in childhood. Br J Clin Pract 1992, 46:271.
107. Konate A, Duhamel O, Basset D, Ayral J, Poirette A, Granier P, Ramdani M,
Gislon J: Toxocariasis and functional intestinal disorders. Presentation of
4 cases. Gastroenterol Clin Biol 1996, 20:909–911. in French.
108. Sharghi N, Schantz PM, Caramico L, Ballas K, Teague BA, Hotez PJ:
Environmental exposure to Toxocara as a possible risk factor for asthma:
a clinic-based case–control study. Clin Infect Dis 2001, 32:E111–116.
109. Gavignet B, Piarroux R, Aubin F, Millon L, Humbert P: Cutaneous manifestations
of human toxocariasis. JAmAcadDermatol2008, 59:1031–1042.
110. Karpinski FE Jr, Everts-Suarez EA, Sawitz WG: Larval granulomatosis (visceral
larva migrans). AMA J Dis Child 1956, 92:34–40.
111. Schoenfeld AE, Ghitnic E, Rosen N: Granulomatous encephalitis due to
Toxocara larvae (Visceral Larva Migrans). Harefuah 1964, 66:337–340.
112. von Reyn CF, Roberts TM, Owen R, Beaver PC: Infection of an infant with
an adult Toxocara cati (Nematoda). J Pediatr 1978, 93:247–249.
113. Beaver PC, Jung RC, Cupp EW: Clinical parasitology. 9th edition. Philadelphia,
PA: Lea and Febiger; 1984.
114. Grinberg AI: Rare cases of Toxascaris leonina and Toxocara mystax in
man. Med Parasitol 1961, 30:626.
115. Beaver PC, Bowman DD: Ascaridoid larva (Nematoda) from the eye of a
child in Uganda. AmJTrop Med Hyg 1984, 33:1272–1274.
116. Centers for Disease Control & Prevention. [http://www.dpd.cdc.gov/dpdx/
html/hookworm.htm].
117. Hochedez P, Caumes E: Hookworm-related cutaneous larva migrans. J
Travel Med 2007, 14:326–333.
118. Euzeby J: Les Maladies Vermineuses des Animaux Domestiques et leurs
Incidences sur la Pathologie Humaine. Maladies dues aux Nemathelminthes.
Vigot Frères, Paris, France : 1961.
119. De Carneri I, Castellino S: Incapacità delle larve di Ancylostoma
tubaeforme di provocare dermatiti nell’uomo. Rev Parasitol 1961, 25:31–24.
120. Fulleborn F: Durch hakenwurmlarven des hundes (Uncinaria
stenocephala) beim meschen erzeugte “creeping eruption”.Abh Gebiet
Auslandskunde 1927, 26:121–133.
121. Caumes E, Ly F, Bricaire F: Cutaneous larva migrans with folliculitis: report of
seven cases and review of the literature. Br J Dermatol 2002, 146:314–316.
122. Malvy D, Ezzedine K, Pistone T, Receveur MC, Longy-Boursier M: Extensive
cutaneous larva migrans with folliculitis mimicking multimetameric
herpes zoster presentation in an adult traveler returning from Thailand.
J Travel Med 2006, 13:244–247.
123. Rivera-Roig V, Sanchez JL, Hillyer GV: Hookworm folliculitis. Int J Dermatol
2008, 47:246–248.
124. Little MD, Halsey NA, Cline BL, Katz SP: Ancylostoma larva in a muscle fiber
of man following cutaneous larva migrans. AmJTrop Med Hyg 1983,
32:1285–1288.
125. Hunter GW 3rd, Worth CB: Variations in response to filariform larvae of
Ancylostoma caninum in the skin of man. J Parasitol 1945, 31:366–372.
126. Garcia CA, Sabrosa NA, Gomes AB: Segundo Pde S, Garcia Filho CA,
Sabrosa AS: Diffuse unilateral subacute neuroretinitis-DUSN. Int
Ophthalmol Clin 2008, 48:119–129.
127. Prociv P, Croese J: Human eosinophilic enteritis caused by dog
hookworm Ancylostoma caninum.Lancet 1990, 335:1299–1302.
128. Prociv P, Croese J: Human enteric infection with Ancylostoma caninum:
hookworms reappraised in the light of a "new" zoonosis. Acta Trop 1996,
62:23–44.
129. McCarthy J, Moore TA: Emerging helminth zoonoses. Int J Parasitol 2000,
30:1351–1360.
130. Walker NI, Croese J, Clouston AD, Parry M, Loukas A, Prociv P: Eosinophilic
enteritis in northeastern Australia. Pathology, association with Ancylostoma
caninum, and implications. Am J Surg Pathol 1995, 19:328–337.
131. Tu CH, Liao WC, Chiang TH, Wang HP: Pet parasites infesting the human
colon. Gastrointest Endosc 2008, 67:159–160.
132. Miro G, Mateo M, Montoya A, Vela E, Calonge R: Survey of intestinal
parasites in stray dogs in the Madrid area and comparison of the
efficacy of three anthelmintics in naturally infected dogs. Parasitol Res
2007, 100:317–320.
133. Hellmann K, Knoppe T, Radeloff I, Heine J: The anthelmintic efficacy
and the safety of a combination of imidacloprid and moxidectin
spot-on in cats and dogs under field conditions in Europe. Parasitol
Res 2003, 90(Suppl 3):S142–143.
134. Schmid K, Rohdich N, Zschiesche E, Kok DJ, Allan MJ: Efficacy, safety and
palatability of a new broad-spectrum anthelmintic formulation in dogs.
Vet Rec 2010, 167:647–651.
135. Catton DG, Van Schalkwyk PC: The effica cy of two anthelmintics
against ascarids and hookworms in nat urally infected cats. Parasitol
Res 2003, 90(Suppl 3):S144–145.
136. Altreuther G, Buch J, Charles SD, Davis WL, Krieger KJ, Radeloff I: Field
evaluation of the efficacy and safety of emodepside/praziquantel spot-
on solution against naturally acquired nematode and cestode infections
in domestic cats. Parasitol Res 2005, 97(Suppl 1):S58–64.
137. Reinemeyer CR, Charles SD, Buch J, Settje T, Altreuther G, Cruthers L, McCall JW,
Young DR, Epe C: Evaluation of the efficacy of emodepside plus praziquantel
topical solution against ascarid infections (Toxocara cati or Toxascaris
leonina) in cats. Parasitol Res 2005, 97(Suppl 1):S41–50.
138. Altreuther G, Borgsteede FH, Buch J, Charles SD, Cruthers L, Epe C, Young DR,
Krieger KJ: Efficacy of a topically administered combination of emodepside
and praziquantel against mature and immature Ancylostoma tubaeforme in
domestic cats. Parasito l Res 2005, 97(Suppl 1):S51–57.
139. Altreuther G, Schimmel A, Schroeder I, Bach T, Charles S, Kok DJ, Kraemer F,
Wolken S, Young D, Krieger KJ: Efficacy of emodepside plus praziquantel
tablets (Profender tablets for dogs) against mature and immature
infections with Toxocara canis and Toxascaris leonina in dogs. Parasitol
Res 2009, 105(Suppl 1):S1–8.
140. Schimmel A, Altreuther G, Schroeder I, Charles S, Cruthers L, Ketzis J, Kok DJ,
Kraemer F, McCall JW, Krieger KJ: Efficacy of emodepside plus
praziquantel tablets (Profender tablets for dogs) against mature and
immature adult Ancylostoma caninum and Uncinaria stenocephala
infections in dogs. Parasitol Res 2009, 105(Suppl 1):S9–16.
141. Altreuther G, Radeloff I, LeSueur C, Schimmel A, Krieger KJ: Field evaluation
of the efficacy and safety of emodepside plus praziquantel tablets
(Profender tablets for dogs) against naturally acquired nematode and
cestode infections in dogs. Parasitol Res 2009, 105(Suppl 1):S23–29.
142. Schimmel A, Schroeder I, Altreuther G, Settje T, Charles S, Wolken S, Kok DJ,
Ketzis J, Young D, Hutchens D, Krieger KJ: Efficacy of emodepside plus
toltrazuril (Procox
W
oral suspension for dogs) against Toxocara canis,
Uncinaria stenocephala and Ancylostoma caninum in dogs. Parasitol Res
2011, 109(Suppl 1):S1–8.
143. Altreuther G, Gasda N, Adler K, Hellmann K, Thurieau H, Schimmel A,
Hutchens D, Krieger KJ: Field evaluations of the efficacy and safety of
Emodepside plus toltrazuril (Procox
W
oral suspension for dogs) against
naturally acquired nematode and Isospora spp. infections in dogs.
Parasitol Res 2011, 109:S21–28. Suppl 1.
Traversa Parasites & Vectors 2012, 5:91 Page 17 of 19
http://www.parasitesandvectors.com/content/5/1/91

144. Petry G, Kruedewagen E, Bach T, Gasda N, Krieger KJ: Efficacy of Procox
W
oral suspension for dogs (0.1% emodepside and 2% toltrazuril) against
experimental nematode (Toxocara cati and Ancylostoma tubaeforme)
infections in cats. Parasitol Res 2011, 109(Suppl 1):S37–43.
145. Clark JN, Daurio CP, Plue RE, Wallace DH, Longhofer SL: Efficacy of
ivermectin and pyrantel pamoate combined in a chewable formulation
against heartworm, hookworm, and ascarid infections in dogs. Am J Vet
Res 1992, 53:517–520.
146. Nolan TJ, Hawdon JM, Longhofer SL, Daurio CP, Schad GA: Efficacy of an
ivermectin/pyrantel pamoate chewable formulation against the canine
hookworms, Uncinaria stenocephala and Ancylostoma caninum.Vet
Parasitol 1992, 41:121–125.
147. Shoop WL, Michael BF, Soll MD, Clark JN: Efficacy of an ivermectin and
pyrantel pamoate combination against adult hookworm, Ancylostoma
braziliense, in dogs. Aust Vet J 1996, 73:84–85.
148. Nolan TJ, Niamatali S, Bhopale V, Longhofer SL, Schad GA: Efficacy of a chewable
formulation of ivermectin against a mixed infection of Ancylostoma braziliense
and Ancylostoma tubaeforme in cats. Am J Vet Res 1992, 53:1411–1413.
149. Bishop BF, Bruce CI, Evans NA, Goudie AC, Gration KA, Gibson SP, Pacey MS,
Perry DA, Walshe ND, Witty MJ: Selamectin: a novel broad-spectrum
endectocide for dogs and cats. Vet Parasitol 2000, 91:163–176.
150. McTier TL, Siedek EM, Clemence RG, Wren JA, Bowman DD, Hellmann K,
Holbert MS, Murphy MG, Young DR, Cruthers LR, Smith DG, Shanks DJ,
Rowan TG, Jernigan AD: Efficacy of selamectin against experimentally
induced and naturally acquired ascarid (Toxocara canis and Toxascaris
leonina) infections in dogs. Vet Parasitol 2000, 91:333–345.
151. Six RH, Sture GH, Thomas CA, Clemence RG, Benchaoui HA, Boy MG,
Watson P, Smith DG, Jernigan AD, Rowan TG: Efficacy and safety of
selamectin against gastrointestinal nematodes in cats presented as
veterinary patients. Vet Parasitol 2000, 91:321–331.
152. McTier TL, Shanks DJ, Wren JA, Six RH, Bowman DD, McCall JW, Pengo G,
Genchi C, Smothers CD, Rowan TG, Jernigan AD: Efficacy of selamectin
against experimentally induced and naturally acquired infections of
Toxocara cati and Ancylostoma tubaeforme in cats. Vet Parasitol 2000,
91:311–319.
153. Anonymous: Evaluation of the Effectiveness of a Combination of
Imidacloprid and Moxidectin against Natural Infections with Trichuris
vulpis in Dogs.InFreedom of information summary, Advantage Multi for
dogs, NADA 141–251, Federal Drug Administration. 2006:25–27.
154. EMEA: Advocate Public Assessment report 2009WC500060915. 2009:44–45.
155. Arther RG, Charles S, Ciszewski DK, Davis WL, Settje TS: Imidacloprid/
moxidectin topical solution for the prevention of heartworm disease
and the treatment and control of flea and intestinal nematodes of
cats. Vet Parasitol 2005, 133:219–225.
156. Blagburn BL, Hendrix CM, Lindsay DS, Vaughan JL, Hepler DI, Wright JC:
Efficacy of milbemycin oxime against naturally acquired or
experimentally induced Ancylostoma spp and Trichuris vulpis infections
in dogs. Am J Vet Res 1992, 53:513–516.
157. Sakamoto T, Seki I, Kikuchi K, Nakahara H, Ogasawara H, Hattori M, Hakura R:
Anthelmintic effect of milbemycin D on parasites in dogs. Journal of the
Faculty of Agriculture Iwate University 1984, 17:69–81.
158. Bowman DD, Johnson RC, Hepler DI: Effects of milbemycin oxime on
adult hookworms in dogs with naturally acquired infections. Am J Vet
Res 1990, 51:487–490.
159. Wade CG, Mercer SH, Hepler DI, Craig TM: Effect of milbemycin oxime
against Ancylostoma caninum in dogs with naturally acquired infection.
Am J Vet Res 1991, 52:951–953.
160. Bowman DD, Parsons JC, Grieve RB, Hepler DI: Effects of milbemycin on
adult Toxocara canis in dogs with experimentally induced infection. Am J
Vet Res 1988, 49:1986–1989.
161. Niamatali S, Bhopale V, Schad GA: Efficacy of milbemycin oxime against
experimentally induced Ancylostoma caninum and Uncinaria
stenocephala infections in dogs. J Am Vet Med Assoc 1992, 201:1385–1387.
162. Shoop WL, Egerton JR, Seward RL, Eary CH, Haines HW, Michael BF:
Anthelmintic activity of milbemycin oxime against adult and immature
Uncinaria stenocephala in dogs. Aust Vet J 1993, 70:187–188.
163. Fukase T, In T, Chinone S, Akihama S, Itagaki H: Anthelmintic efficacy of
milbemycin D against Toxocara cati and Ancylostoma tubaeforme in
domestic cats. J Vet Med Sci 1991, 53(5):817–821.
164. Humbert-Droz E, Buscher G, Cavalleri D, Junquera P: Efficacy of milbemycin
oxime against fourth-stage larvae and adults of Ancylostoma tubaeforme
in experimentally infected cats. Vet Rec 2004, 154:140–143.
165. Bowman DD, Legg W, Stansfield DG: Efficacy of moxidectin 6-month
injectable and milbemycin oxime/lufenuron tablets against naturally
acquired trichuris vulpis infections in dogs. Vet Ther 2002, 3:286–289.
166. Schenker R, Bowman D, Epe C, Cody R, Seewald W, Strehlau G, Junquera P:
Efficacy of a milbemycin oxime-praziquantel combination product
against adult and immature stages of Toxocara cati in cats and kittens
after induced infection. Vet Parasitol 2007, 145:90–93.
167. Snyder DE, Wiseman S: Dose confirmation and non-interference
evaluations of the oral efficacy of a combination of milbemycin oxime
and spinosad against the dose limiting parasites, adult cat flea
(Ctenocephalides felis) and hookworm (Ancylostoma caninum), in dogs.
Vet Parasitol 2012, 184:284–290.
168. Schnitzler B, Hayes B, Wiseman S, Snyder DE: Confirmation of the efficacy
of a combination tablet of spinosad and milbemycin oxime against
naturally acquired infections of canine intestinal nematode parasites. Vet
Parasitol 2012, 184:279–283.
169. Palatability/Acceptability Trial of 3 Way and 2 Way Chewable
Formulations in Dogs.InStudy NAH-02-0054.: ; Final Report 0/24/04.
170. Bianciardi P, Otranto D: Treatment of dog thelaziosis caused by Thelazia
callipaeda (Spirurida, Thelaziidae) using a topical formulation of
imidacloprid 10% and moxidectin 2.5%. Vet Parasitol 2005, 129:89–93.
171. Traversa D, Di Cesare A, Milillo P, Lohr B, Iorio R, Pampurini F, Schaper R,
Paoletti B, Heine J: Efficacy and safety of imidacloprid 10 %/moxidectin
1 % spot-on formulation in the treatment of feline aelurostrongylosis.
Parasitol Res 2009, 105(Suppl 1):S55–62.
172. Traversa D, Milillo P, Di Cesare A, Lohr B, Iorio R, Pampurini F, Schaper R,
Bartolini R, Heine J: Efficacy and safety of emodepside 2.1%/praziquantel
8.6% spot-on formulation in the treatment of feline aelurostrongylosis.
Parasitol Res 2009, 105(Suppl 1):S83–89.
173. Schenker R, Cody R, Strehlau G, Alexander D, Junquera P: Comparative
effects of milbemycin oxime-based and febantel-pyrantel embonate-
based anthelmintic tablets on Toxocara canis egg shedding in naturally
infected pups. Vet Parasitol 2006, 137:369–373.
174. Fisher MA, Jacobs DE, Hutchinson MJ, Dick IG: Studies on the control of
Toxocara canis in breeding kennels. Vet Parasitol 1994, 55:87–92.
175. Epe C, Schnieder T, Stoye M: Opportunities and Limitations of
chemotherapeutic control of vertical infections of Toxocara canis and
Ancylostoma caninum in the dog. Der Praktische Tierarzt 1996, 6:483–490. in
German.
176. Barriga OO: A critical look at the importance, prevalence and control of
toxocariasis and the possibilities of immunological control. Vet Parasitol
1988, 29:195–234.
177. European Scientific Counsel Companion Animal Parasites. [www.esccap.org].
178. Coati N, Hellmann K, Mencke N, Epe C: Recent investigation on the
prevalence of gastrointestinal nematodes in cats from France and
Germany. Parasitol Res 2003, 90:146–147.
179. Deplazes P: Helminthosen von Hund und Katze.InIn Veterinarmedizinische
Parasitologie. Edited by Schnyder T. Stuttgart: Parey; 2006:444–518.
180. Asano K, Suzuki K, Matsumoto T, Sakai T, Asano R: Prevalence of dogs with
intestinal parasites in Tochigi, Japan in 1979, 1991 and 2002. Vet Parasitol
2004, 120:243–248.
181. Beelitz P, Göbel E, Gothe R: Fauna and incidence of endoparasites in
kittens and their mothers from different husbandry situations in south
Germany. Tierarztl Prax 1992, 20:297–300.
182. López J, Abarca K, Paredes P, Inzunza E: Intestinal parasites in dogs and
cats with gastrointestinal symptoms in Santiago, Chile. Rev Med Chil 2006,
134:193–200.
183. Miró G, Montoya A, Jiménez S, Frisuelos C, Mateo M, Fuentes I: Prevalence
of antibodies to Toxoplasma gondii and intestinal parasites in stray,
farm and household cats in Spain. Vet Parasitol 2004, 126:249–255.
184. Nutter FB, Dubey JP, Levine JF, Breitschwerdt EB, Ford RB, Stoskopf MK:
Seroprevalences of antibodies against Bartonella henselae and
Toxoplasma gondii and fecal shedding of Cryptosporidium spp, Giardia
spp, and Toxocara cati in feral and pet domestic cats. J Am Vet Med Assoc
2004, 225:1394–1398.
185. Kopp SR, Kotze AC, McCarthy JS, Coleman GT: High-level pyrantel resistance in
the hookworm Ancylostoma caninum.Vet Parasitol 2007, 143:299–304.
Traversa Parasites & Vectors 2012, 5:91 Page 18 of 19
http://www.parasitesandvectors.com/content/5/1/91

186. Blagburn BL: Heartworms and resistance: Truth or fiction? [http://www.
bayeranimalhealthsymposium.com/blagburn_heartworm.shtml].
187. Irwin PJ: Companion animal parasitology: a clinical perspective. Int J
Parasitol 2002, 32:581–593.
188. Jordan HE, Mullins ST, Stebbins ME: Endoparasitism in dogs: 21,583 cases
(1981–1990). J Am Vet Med Assoc 1993, 203:547–549.
189. Nolan TJ, Smith G: Time series analysis of the prevalence of endoparasitic
infections in cats and dogs presented to a veterinary teaching hospital.
Vet Parasitol 1995, 59:87–96.
190. Hackett T, Lappin MR: Prevalence of enteric pathogens in dogs of
north-central Colorado. J Am Anim Hosp Assoc 2003, 39:52–56.
191. Holland CV, O'Lorcain P, Taylor MR, Kelly A: Sero-epidemiology of
toxocariasis in school children. Parasitology 1995, 110(5):535–545.
192. Gates MC, Nolan TJ: Risk factors for endoparasitism in dogs: retrospective
case–control study of 6578 veterinary teaching hospital cases. J Small
Anim Pract 2009, 50:636–640.
193. Stehr-Green JK, Schantz PM: The impact of zoonotic diseases transmitted
by pets on human health and the economy. Vet Clin North Am Small
Anim Pract 1987, 17:1–15.
194. McCarthy J, Moore TA: Emerging helminth zoonoses. Int J Parasitol 2000,
30:1351–1360.
195. Traub RJ, Monis PT, Robertson ID: Molecular epidemiology: a
multidisciplinary approach to understanding parasitic zoonoses. Int J
Parasitol 2005, 35:1295–1307.
196. Bugg RJ, Robertson ID, Elliot AD, Thompson RCA: Gastrointestinal parasites
of urban dogs in Perth, Western Australia. Vet J 1999, 157:295–301.
197. Kazacos KR: Baylisascaris procyonis and related species.InIn Parasitic
Diseases of Wild Mammals. 2nd edition. Edited by Samuel WM, Pybus MJ,
Kocan AA. Ames IA: Iowa State University Press; 2001:301–341.
198. Kazacos KR: Unusual fecal parasite in a dog. NAVC Clinician’sBrief2006, 4:37–39.
199. Pai PJ, Blackburn BG, Kazacos KR, Warrier RP, Bégué RE: Full recovery from
Baylisascaris procyonis eosinophilic meningitis. Emerg Infect Dis 2007,
13:928–930.
200. Popiołek M, Szczęsna-Staśkiewicz J, Bartoszewicz M, Okarma H, Smalec B,
Zalewski A: Helminth parasites of an introduced invasive carnivore
species, the raccoon (Procyon lotor L.), from the Warta Mouth National
Park (Poland). J Parasitol 2011, 97:357–360.
201. Rubinstensky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU: Human
toxocariasis: diagnosis, worldwide seroprevalences and clinical
expression of the systemic and ocular forms. Ann Trop Med Parasitol 2010,
104:3–23.
202. Wells DL: Public understanding of toxocariasis. Public Health 2007,
121:187–188.
203. Harvey JB, Roberts JM, Schantz PM: Survey of veterinarians’
recommendations for treatment and control of intestinal parasites in
dogs: public health implications. J Am Vet Med Assoc 1991, 199:702–707.
204. Kornblatt AN, Schantz PM: Veterinary and public health considerations in
canine roundworm control: a survey of practicing veterinarians. J Am Vet
Med Assoc 1980, 177:1212–1215.
205. Overgaauw PAM: Effect of a government educational campaign in the
Netherlands on awareness of Toxocara and toxocarosis. Prev Vet Med
1996, 28:165–174.
206. Stull JW, Carr AP, Chomel BB, Berghaus RD, Hird DW: Small animal
deworming protocols, client education, and veterinarian perception of
zoonotic parasites in western Canada. Can Vet J 2007, 48:269–276.
207. Tharaldsen J: Parasitic organisms from dogs and cats in sandpits from
nursery schools in Oslo. Norsk Veterinaertidsskrift 1982, 94:251–254.
208. Jansen J, Van Knapen F: Toxocara eggs in public parks and sandboxes in
Utrecht. Tijdschr Diergeneeskd 1993, 118:611–614.
209. Headey B, Krause P: Health benefits and potential budgets savings due to
pets, Australian and German results. A Aust Social Mon 1999, 2:4–6.
210. Wilson CC: The pet as an anxiolytic intervention. J Nerv Ment Dis 1991,
179:482–489.
211. Friedmann E, Thomas SA: Pet ownership, social support, and one-year
survival after acute myocardial infarction in the Cardiac Arrhythmia
Suppression Trial (CAST). Am J Cardiol 1995, 76:1213–1217.
212. Beck AM, Meyers NM: Health enhancement and companion animal
ownership. Annu Rev Public Health 1996, 17:247–257.
213. Paul M, King L, Carlin EP: Zoonoses of people and their pets: a US
perspective on significant pet-associated parasitic diseases. Trends
Parasitol 2010, 26:153–154.
214. Robertson ID, Irwin PJ, Lymbery AJ, Thompson RCA: The role of companion
animals in the emergence of parasitic zoonoses. Int J Parasitol 2000,
30:1369–1377.
215. Angulo FJ, Glaser CA, Juranek DD, Lappin MR, Regnery RL: Caring for pets of
immunocompromised persons. J Am Vet Med Assoc 1994, 205:1711–1718.
216. Wong SK, Feinstein LH, Heidmann P: Healthy pets, healthy people. JAm
Vet Med Assoc 1999, 215:335–338.
217. Schantz PM: Of worms, dogs and human hosts: continuing challenges for
veterinarians in prevention of human disease. J Am Vet Med Assoc 1994,
204:1023–1028.
218. Thompson RCA: The future impact of societal and cultural factors on
parasitic disease –some emerging issues. Int J Parasitol 2001, 31:949–959.
219. Zajac AM, Sangster NC, Geary TG: Why veterinarians should care more
about parasitology. Parasitol Today 2000, 16:504–506.
220. Robinson RA, Pugh RN: Dogs, zoonoses and immunosuppression. J R Soc
Promot Health 2002, 122:95–98.
221. Jenkins EJ, Schurer JM, Gesy KM: Old problems on a new playing field:
Helminth zoonoses transmitted among dogs, wildlife, and people in a
changing northern climate. Vet Parasitol 2011, 182:54–69.
doi:10.1186/1756-3305-5-91
Cite this article as: Traversa: Pet roundworms and hookworms: A
continuing need for global worming. Parasites & Vectors 2012 5:91.
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