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Veterinary Parasitology
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a r t i c l e
i n f o
Keywords:
Disease burden, Parasitic zoonoses,
Economics, DALY, Emerging diseases
a b s t r a c t
Diseases resulting from zoonotic transmission of parasites are common. Humans become
infected through food, water, soil and close contact with animals. Most parasitic zoonoses
are neglected diseases despite causing a considerable global burden of ill health in humans
and having a substantial nancial burden on livestock industries. This review aims to bring
together the current data available on global burden estimates of parasitic zoonoses and
indicate any changes in the trends of these diseases. There is a clear need of such information as interventions to control zoonoses are often in their animal hosts. The costs of
such interventions together with animal health issues will drive the cost effectiveness of
intervention strategies. What is apparent is that collectively, parasitic zoonoses probably
have a similar human disease burden to any one of the big three human infectious diseases:
malaria, tuberculosis or HIV in addition to animal health burden. Although the global burden for most parasitic zoonoses is not yet known, the major contributors to the global
burden of parasitic zoonoses are toxoplasmosis, food borne trematode infections, cysticercosis, echinococcosis, leishmaniosis and zoonotic schistosomosis. In addition, diarrhoea
resulting from zoonotic protozoa may have a signicant impact.
2011 Elsevier B.V. All rights reserved.
1. Introduction
Of the nearly 1500 agents known to be infectious to
humans, 66 are protozoa and 287 are helminths infectious
agents, 66 are protozoa and 287 are helminths (Chomel,
2008; Taylor et al., 2001). The majority (60.3%) of emerging infectious diseases are zoonoses (Jones et al., 2008).
Zoonoses represent a large burden of disease and there
are changing patterns of disease burdens with disease
emergence. Human population growth and socioeconomic
changes result in the migration of populations into new
ecological regions and changes in animal husbandry practices which can impact on disease emergence and disease
burden (Macpherson, 2005). In addition improved diagnostics are demonstrating that many zoonoses have a higher
burden then previously recognised. Some new syndromes
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Table 1
Possible magnitude of the annual global burden of parasitic zoonoses with that of the global burden of malaria, tuberculosis and HIV for comparison.
Zoonosis
Important aetiologies
Possible Global
Burden (DALYs)*
Trends
Zoonotic
Schistosomosis
Echinococcosis
Schistosoma japonicum
? 106 107
Unknown
Echinococcus
granulosus
E. multilocularis
Taenia solium
T. saginata
2-5 10
US$2 10
2-5 106
Very low
Toxoplasma gondii
2-8 106
Unknown
Substantial animal
health costs
Possibly substantial
Cysticercosis
Toxoplasmosis
>0.5 106
Animal Fasciolosis is
very high
? 105 106
>1 10
? 106
39 106
71 106
36 106
CE emergent in NIS, AE
emergent in Europe
*
For most of these zoonoses, a global burden has yet to be published. The possible DALYs indicate a very crude estimate based on available data and serve
only to illustrate the likely magnitude of the disease burden.
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from the results of a systematic review on the association of epilepsy and neurocysticercosis (Ndimubanzi et al.,
2010). This study suggests that in low or middle income
endemic countries approximately 30% of epilepsy may be
attributable to neurocysticercosis. The global burden of
epilepsy estimated is to be 7.8 million DALYS. Of these,
6.5 million DALYs occur in Sub Saharan Africa, Latin America, South Asia and the Western Pacic (including China):
regions where T. solium is highly endemic. It is also interesting to note that the proportion of the total burden of
disease caused by epilepsy in the Middle East and North
Africa, middle income countries where pork consumption
is very low, is 0.378%: comparable to that of high income
countries (0.314%) where T. solium has largely been eliminated. In Latin America, middle income countries but with
high pork consumption, the proportion of the total disease
burden attributable to epilepsy is 0.707% (calculations from
data in (Lopez et al., 2006). Thus an estimate of over 2 million DALYs per annum (Table 1) would not be unreasonable,
although the actual global burden is still unknown.
The future trends on the burden of T. solium cysticercosis will depend on patterns of pork consumption, the
success of veterinary public health interventions and economic growth. Pork consumption is increasing in countries
such as China (Ortega et al., 2009), but rapid economic
development should also promote veterinary public health
programmes to control this parasite. Human cysticercosis,
dracunculiasis and lymphatic lariasis are the only human
parasitic diseases that have the potential to be eradicated
globally (Molyneux et al., 2004). Therefore with effective
investment in veterinary public health it may be possible
to eventually reduce the global burden of cysticercosis to
zero, although in some regions (such as sub-Saharan Africa)
cysticercosis will remain problematic for the foreseeable
future.
3.1.5. Other larval cestodoses
Human coenurosis caused by the larvae of Taenia multiceps, T. serialis or T. brauni are sporadically recorded in
the literature. CNS infection can be devastating and hence
result in a high disability weight. As reports of such infections are rare, the global burden of human coenurosis is
likely to be very low.
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There are more than 80 species of food-borne trematodes of which Fasciola spp., Clonorchis sinensis, Opisthorchis
spp., Fasciolopsis buski, Paragonimus spp., and to a lesser
extent Heterophyes spp. and Metagonimus spp. are of public
health importance. Of the estimated one billion people at
risk of infection (Keiser and Utzinger, 2005) up to nine million may suffer from symptomatic sequelae and between
10,000 to 11,000 people die each year (WHO, 1998b). Thus
an annual global burden of over 500,000 DALYs would
not be an unreasonable expectation (Table 1) although
more precise estimates are presently unavailable The foodborne trematode zoonoses are transmitted by ingestion
of metacercariae and are perpetuated through inadequate
sanitation, cultural and evolving food habits, growth of
aquaculture and by a wide range of domestic and wild
denitive hosts. The DALYs contributed by the food-borne
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signicantly to the economic burden and suffering of communities. It is known that S. bovis (a non zoonotic species)
can result in substantial economic losses in livestock (Hunt
McCauley et al., 1984) and hence, by analogy, direct production losses due to S. japonicum are likely.
Schistosomosis is strongly linked with poverty, and
despite recent improvements in the rural Chinese economy, which have resulted in a better standard of living,
the prevalence of S. japonicum and its associated morbidity have continued to rise in some localities. The downturn
in the global economy in 2007 resulted in the closure of
businesses in urban areas, employment opportunities contracted and millions of city residents returned to their
former rural villages: some of which were located in S.
japonicum endemic areas (McManus et al., 2010).
S. japonicum currently is an important zoonosis in ve
provinces in China where more than 50 million people
are at risk and approximately one million people and several hundred thousand livestock are infected (McManus
et al., 2010). S. japonicum also occurs in 28 provinces in the
Philippines and in discrete foci in the province of central
Sulawesi in Indonesia (King, 2009).
Water resource development, including irrigation and
the construction of dams for water conservation, hydroelectric power generation etc. in schistosomosis endemic
areas, such as the Gezira-Managil dam in Sudan, the Aswan
dam in Egypt, the Melkasadi dam in Ethiopia, the Kariba
dam in Zimbabwe and the Danling and Huangshi dams
in China have resulted in an increase in prevalence or
reemergence of the disease in those countries (Gryseels
et al., 2006; Steinmann et al., 2006). The recently completed
Three Gorges dam in China which has endemic S. japonicum foci above and below the dam is anticipated to have
an impact on the parasite increasing its current distribution
and intensity (McManus et al., 2010). As with other water
development projects it is anticipated that this will occur
through habitat alteration favoring increased snail breeding sites, increased grazing areas for important reservoir
hosts, occupational factors and an increase in the susceptible human population attracted to migrate to the endemic
areas from non-endemic regions of the country. Availability and use of latrines inuences the importance of humans
in contaminating the environment and their importance
vis a vis domestic and wild denitive hosts in maintaining
transmission.
S. japonicum was successfully eliminated from Japan
through snail control and socioeconomic changes. The
national schistosomosis control program in China is recognized as one of the most successful globally: the
cornerstone of the programme being mass chemotherapy.
Spatial epidemiological methods using geographical information systems (GIS), remote sensing (RS), incorporated
with advanced Bayesian based spatial statistics have been
important tools for identifying high-risk areas for S. japonicum transmission for Chinas control programme (Yang
et al., 2005). However, recent control successes appear
to be stalling. Together with the potential for its reemergence S. japonicum is regarded by the Chinese authorities
as being on par with HIV/AIDS, TB and hepatitis B as a
public health problem (Wang et al., 2008). A recent trial
carried out in two villages where in one all humans and
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demonstrated giving rise to a syndrome, known as disseminated strongyloidosis. Such infections are nearly always
fatal.
The degree to which zoonotic transmission occurs is
uncertain though primate and dog- parasite clades have
been described (Hasegawa et al., 2010). Further studies are
required to elucidate the importance of dogs and humans
in perpetuating transmission.
Strongyloidosis occurs all over the tropics and subtropics and in found in varying prevalences in both
developed and industrialized countries. Difculties in diagnosis and the variability of prevalence within a country
coupled to the parasites longevity in infected hosts has
resulted in estimates on the numbers infected globally from
as low as 3 million to over 100 million (Nolan et al., 2011).
S. stercoralis is recognised as a neglected disease of poverty
in the US where 68,000 to 110,000 individuals are infected
(Hotez, 2008).
The burden from this parasitic disease is uncertain
but may be considerable, particularly since impaired child
development will result in considerable numbers of YLDs
associated with infection. The proportion of this burden
that is from animal sources is likewise uncertain.
5.4. Angiostrongylosis
Angiostrongylus cantonensis is an emerging zoonosis
with the rst human cases being reported in 1945 and
thereafter cases were only sporadically reported essentially until the 1990s. In the last few decades human cases
have been reported from endemic areas including a number of Pacic island nations and Asia (Thailand, Taiwan,
China, Vietnam, Malaysia, Cambodia) to more recently
described foci in the US, Caribbean, Japan, Indonesia, New
Zealand and Australia. Worldwide more than 2800 cases of
human angiostrongylosis have been reported from over 30
countries (Wang and Lun, 2011).
Human infection results from eating infected raw or
undercooked land or aquatic snails (the primary intermediate host species), slugs or paratenic hosts such as prawns
and land crabs, predacious land planarians, freshwater
sh, frogs, toads or monitor lizards and in endemic areas
from unwashed contaminated vegetables. The geographical expansion of the parasites range has been facilitated
by the unintended introduction of infected denitive hosts
such as numerous species of rats. Establishment of the parasite has also been facilitated by the intended or accidental
introduction of snail intermediate host species.
Clinically humans present with a range of symptoms
from mild to eosinophilic meningitis and in extreme cases
such infections have been fatal. The average patient is ill for
two weeks but the condition can last for months. Although
the DALYs for this zoonosis is currently low it is increasing
as the parasite spreads geographically.
5.5. Dirolariosis
A number of species of Dirolaria (including D. immitis,
D. repens, D. roemeri, D. tenuis, D. ursi, D. striata, D. subdermata, D. magnilarvatum and D. corynodes) have been known
to infect humans who do not serve as denitive hosts. The
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small number of fatalities (Scallan et al., 2011), the disease generally has an acute non fatal outcome with few
long term sequaelae. In contrast there are reports from
lower income countries of signicant fatality rates in young
children and long term growth retardation (Chalmers and
Davies, 2010). These types of sequaelae will result in a considerable number of DALYs lost, but most of these DALYs
will be attributable to anthroponotic rather than zoonotic
transmission. In immunosupressed patients crytosporidiosis can be a major problem. In HIV patients infection can
be lifelong and result in premature mortality compared to
HIV patients without cryptosporidiosis. Thus it is possible
to attribute addition DALYs lost due to crytospridiosis in
HIV patients (Havelaar et al., 2000).
6.1.3. Blastocystosis
Blastocystis is now considered to be a zoonosis and it
is believed that animals such as pigs and chickens constitute large reservoirs for human infection via the faecal-oral
route (Tan, 2004). In addition high prevalence in domestic
dogs and cats suggest that these domestic animals could be
a source of human infection.
Blastocystis is reported to be one of the most common
protozoans found in faecal samples of both symptomatic
patients and asymptomatic individuals (Cirioni et al., 1999;
Taamasri et al., 2000; Windsor et al., 2002). Blastocystis
has a worldwide distribution and ndings of many surveys
reported it to be the most frequently isolated protozoan
parasite. Prevalence of Blastocystis infection is higher in low
income compared to high income countries with prevalences of up to 69% being reported from the former.
Despite the parasite being common and linked to
zoonotic transmission, the exact role of Blastocystis as a
cause of human disease is uncertain. A number of clinical and epidemiological studies implicate the parasite as a
potential pathogen whilst others exonerate it as an aetiology of intestinal disease. So whilst signicant progress
has been achieved on descriptions of the morphology and
genetic diversity of Blastocystis, most aspects of its life cycle,
molecular biology, and pathogenicity remain unresolved
(reviewed by Puthia and Tan, 2011; Stensvold et al., 2009)
Therefore until the clinical signicance of this parasite is
conrmed it is only possible to speculate on the likely
burden impact. Currently we have no indications that the
burden of blastocystosis is substantial
6.2. Microsporidiosis
Microsporidia were conrmed as a cause of encephalitis in 1959 (Matsubayashi et al., 1959). Subsequently
Microsporidia have been associated with intestinal disease
and other syndromes in HIV patients (Hennequin et al.,
1992). The number of articles describing human disease
has increased rapidly since 1990 and it is now known
that Microsporidia can infect virtually any organ system;
and patients with encephalitis, ocular infection, sinusitis,
myositis, and disseminated infection are well described in
the literature (Wieiss, 2011).
It now seems that Microsporidia are common enteric
pathogens causing self-limited infections in immune
competent hosts and have been reported globally. Serosur-
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