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Contents lists available at ScienceDirect

Veterinary Microbiology
journal homepage: www.elsevier.com/locate/vetmic

Zoonotic risks from small ruminants

M. Ganter
Clinic for Swine and Small Ruminants, University of Veterinary Medicine, Hannover, Germany

A R T I C L E I N F O A B S T R A C T

Zoonoses are infections that spread naturally between species (sometimes by a vector) from animals to
Keywords: other animal species or to humans or from humans to animals. Most of the zoonoses diagnosed in sheep
BSE
and goats are transmitted by close contact of man with these animals and are, more often, occupational
Brucellosis
Chlamydophila
diseases that principally affect breeders, veterinarians and/or slaughterhouse workers. Some other
Coxiella diseases have an airborne transmission and affect the population in the vicinity of sheep/goat farms. Due
Goat to the fact that small ruminants are almost the only remaining animals which are migrating in
Orf industrialised countries, there is a severe risk for transmitting the diseases. Some other zoonotic diseases
Q fever are foodborne diseases, which are mainly transmitted from animals to humans and to other animal
Sheep species by contaminated food and water. Within the last decade central Europe was threatened by some
Transmissible Encephalopathy new infections, e.g., bluetongue disease and schmallenberg disease, which although not of zoonotic
Zoonoses
interest, are caused by pathogens transmitted by vectors. Causal agents of both diseases have found
highly effective indigenous vectors. In the future, climate change may possibly modify conditions for the
vectors and influence their distribution and competence. By this, other vector-borne zoonotic infections
may propagate into former disease free countries. Changes in human behaviour in consummation and
processing of food, in animal housing and management may also influence future risks for zoonosis.
Monitoring, prevention and control measures are proposed to limit further epidemics and to enable the
containment of outbreaks. Measures depend mainly on the damage evoked or anticipated by the disease,
the local situation, and the epidemiology of the zoonoses, the presence of the infective agent in wild and
other animals, as well as the resistance of the causal microorganisms in the environment and the
possibility to breed sheep and goats which are resistant to specific infections. In this review, the clinical
signs in animals and humans of the main sheep and goat zoonoses, as well as the transmission route and
the control measures are reported. Brucellosis, chlamydophilosis, Q fever, Orf, Rift valley fever and Bovine
Spongiform Encephalopathy are described in greater detail, in order to determine factors that contribute
to the choice of the control strategies.
ã 2015 Elsevier B.V. All rights reserved.

1. Introduction large dairy goat farms. However, it has been known for a long time
that small ruminants can be of importance in transmission of
Zoonoses are infectious diseases, which are transmitted from various other pathogens to humans, e.g., the agents of brucellosis,
animals to humans (zooanthroponoses) and from humans to Orf, Rift valley fever. In this review, the clinical signs of the main
animals (anthropozoonoses). At least 71% of all human pathogens sheep and goat zoonoses, as well as the transmission mode and the
are zoonotic and about 75% of all emerging human pathogens over control measures are reported. Brucellosis, chlamydophilosis, Q
the past 10 years have been caused by pathogens originating from fever, Orf, Rift Valley fever and Bovine Spongiform Encephalopathy,
an animal or from products of animal origin (Wolfe et al., 2007; are described in greater detail, in order to determine factors that
Rodolakis, 2014). Table 1 describes most microbial zoonotic contribute to the choice of the control strategies.
diseases.
Small ruminants are important as source of infections for 2. Bacterial diseases
humans, a fact that has come under concern since the Q fever
epidemic in the Netherlands from 2007 to 2010. The outbreak in 2.1. Brucellosis
humans occurred subsequently to the occurrence of Q fever in
Brucellosis is still an important zoonosis in the para-Mediter-
ranean countries. It is also endemic in the Middle East, Western
E-mail address: martin.ganter@tiho-hannover.de (M. Ganter). Asia, Africa and South America (Pappas et al., 2006). Northern and

http://dx.doi.org/10.1016/j.vetmic.2015.07.015
0378-1135/ ã 2015 Elsevier B.V. All rights reserved.

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Table 1
Zoonotic diseases of small ruminants.

Disease Agent Small ruminants Humans Other Control

animal measures
species that
can be
infected
Clinical signs Mode of Clinical signs Mode of
transmission transmission
Bacterial diseases
Anthrax Bacillus anthracis Fever, lack of Consumption Cutaneous form Direct contact Numerous Vaccination of
rumination, or breathing of (skin sore, with infected animal ruminants,
excitement or bacterial spores developing into animals or species restriction of
depression, ulcer with black contaminated animal
pulmonary and center), gastro- animal products movements,
pharyngeal oedema, intestinal form (e.g., handling hygiene
uncoordinated (fever, nausea, infected animal measures,
movement, hae- haemorrhagic carcasses or collection of
morrhagic discharge, diarrhea, loss of products, dead animals
swellings, sudden appetite, breathing and sufficient
death stomach pain), bacterial spores, heating in
respiratory form eating rendering
(throat ache, undercooked plants, training
coughing, tired- contaminated of exposed
ness, difficult meat) people,
breathing antibiotic
treatment

Brucellosis Brucella melitensis, B. Late term abortion, Ingestion of Undulant fever, Consumption of Cattle, Vaccination, test
abortus stillbirth, orchitis, contaminated arthritis, liver contaminated horses, and slaughter,
epididymitis, material (e.g., damage and dairy products, mules, training of
arthritis, fever, feed, water, miscarriages breathing of donkeys, people involved
depression, weight aborted contaminated pigs
loss, diarrhoea material) dust, direct
contact of open
wounds with
contaminated
tissues, fluids, or
surfaces

Campylobacter infections Campylobacter fetus subsp. Sheep: abortion, Oral infection Intestinal Oral infection Pigs, poultry Training of
intestinalis,C. jejuni stillbirth, birth of through inflammation through exposed people,
weak lambs, contaminated (diarrhoea, consumption of hygiene
increased neonatal forages or abdominal pain, contaminated measures,
mortality; goats: water fever, nausea, food or water, antibiotic
asymptomatic vomiting), handling of treatment
infections in adults, arthritis, infected females
diarrhoea, fever, convulsions and during
arthritis in kids meningitis, parturition
abortion,
endocarditis

Caseous lymphadenitis Corynebacterium Abscesses in lymph Contact with Painful skin Direct skin Horses, pigs, Vaccination, test
pseudotuberculosis nodes, progressive contaminated wounds with contact with Camels. and slaughter,
weight loss material, purulent contaminated training of
consumption of material and material exposed people
contaminated necrosis,
forages, at abscessation of
sucking (lambs/ lymph nodes
kids)

Chlamydophila infection Chlamydophila abortus Late term abortion, Contact with Flu-like signs Consumption of Cattle Vaccination of
retained foetal infected with headache, contaminated ewes and does,
membranes, pregnant ewes/ chills, fever, joint food or water, training of
stillbirths, does at pain, light inhalation of exposed people
epididymitis, lambing/ sensitivity, contaminated
pneumonia, aborting vomiting, sore dust, contact
conjunctivitis process/post- throat, with
partum, pneumonitis; contaminated
through abortion animal material
contaminated
bedding/waste,
inhalation of
contaminated
dust

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Table 1 (Continued)
Disease Agent Small ruminants Humans Other Control
animal measures
species that
can be
infected
Clinical signs Mode of Clinical signs Mode of
transmission transmission
Erysipelothrix infection Erysipelothrix Polyarthritis, Cutaneus, oral Erythema, cutaneus Pigs, poultry, Vaccination,
rhusiopathiae abortion arthritis, fish hygiene
endocarditis, measures, dry
sepsis bedding

Leptospirosis Various Leptospira species Abortion, stillbirth, Contact with High fever, Contact with Rodents Rodent control,
and serotypes birth of weak urine or other severe contaminated (Norway hygiene
newborns, material from headache, chills, material, water rats, striped measures,
haemoglobinuria, infected muscular ache, or soil, field mice, vaccination,
haemolytic anaemia, animals, water, abdominal pain, consumption of hamsters), antibiotic
jaundice soil, forages vomiting, contaminated cattle, pigs, treatment
jaundice, food or water dogs
diarrhoea, rash,
meningitis, liver
failure

Listeriosis Listeria monocytogenes Meningoencephalitis Oral intake of Diarrhoea, Consumption of cattle Training of
signs, facial paralysis, contaminated premature contaminated exposed people,
abortion, septicaemia feed childbirth, food (e.g., hygiene
in lambs and kids, (especially, miscarriage/ unpaste- measures,
iridocyclitis, mastitis silage) or water, stillbirth, health reurised dairy or antibiotic
inhalation of problems in meat products), treatment
contaminated newborns, fever, contact with
dust myalgia, material from
headache, infected ewes/
abdominal does
cramping,
nausea,
vomiting

Paratuberculosis Mycobacterium avium After long Infection of Diarrhoea, Consumption of Cattle, wild Vaccination,
(possible involvement subsp. paratuberculosis asymptomatic period young lambs/ weight loss contaminated ruminants, hygiene
of causal agent in consequently to kids in early food (e.g., hares, measures
Crohn's disease) neonatal infection, life, during unpaste- rabbits
weight loss, transient sucking or by reurised dairy
diarrhoea, emaciation ingestion of products)
contaminated
material

Q fever Coxiella burnetii Abortion, stillbirth, Consumption High fever, flu- Handling of Cattle, cats, Vaccination of
birth of weak lambs/ of like symptoms, contaminated most ruminants,
kids, contaminated pneumonitis, material from mammalian manure
haemoglobinuria, forages, tick sweats, non infected species, management,
haemolytic anaemia, bites, direct productive animals, reptiles, restriction of
jaundice contact with cough, nausea, inhalation of birds, animal
contaminated vomiting, contaminated insects, e.g. movement,
material from diarrhea, dust, ticks. hygiene
infected abdominal pain, consumption of measures,
animals chest pain, contaminated training of
hepatitis, food (e.g., exposed people,
abortion, unpaste- vaccination of
endocarditis, reurised dairy people at risk
chronic fatique products)
syndrome

Salmonellosis Various Salmonella Abortion, in lambs/ Oral intake of Severe vomiting, Oral intake of Poultry, all Training of
species and serotypes kids: diarrhoea, fever, bacteria abdominal pain, bacteria through mammals, exposed people,
arthritis through fever, headache contaminated reptiles, hygiene
contaminated food or water, wild or measures,
feed or water direct contact domestic antibiotic
with infected birds treatment
animals

Staphylococcal infections Staphylococcus aureus Mastitis, skin lesions Direct contact Toxicosis by Consumption of All animals Hygiene
with infected staphylococcal contaminated measures
animals, enterotoxin: food (e.g.,
transmission severe vomiting, unpaste-
through hands abdominal pain, reurised dairy

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Table 1 (Continued)
Disease Agent Small ruminants Humans Other Control
animal measures
species that
can be
infected
Clinical signs Mode of Clinical signs Mode of
transmission transmission
of milkers or at diarrhoea, products), direct
suckling headache; contact with
bacterial infected animals
infection: skin or
cutaneous
lesions

Tuberculosis Mycobacterium bovis, M. Lymphadenitis, lower Ingestion or Cough, Ingestion or Other Test and
caprae respiratory tract inhalation of unexplained inhalation of ruminants, slaughter
disease, mastitis causal agent in weight loss, causal agent in wild infected
close contact fatigue, night close contact mammals animals, training
with infected sweets, chills, with infected (badgers) of exposed
animals loss of appetite, animals people, hygiene
lymphadenitis measures,
antibiotic
treatment

Mycotic diseases
Ringworm Microsporum spp., Ring-shaped, crusty Direct contact Red scaly Direct contact Cattle, cats, Vaccination
Trichophyton spp. patches on skin, with with infected patches on skin, with infected dogs against
wool or hair loss animals that itch and animals or with Trichophyton
may form contaminated verrucosum,
blisters with fomites antifungal
secretion, round treatment
bald patches on
scalp or beard,
thickened,
discoloured nails

Viral diseases
Orf (contagious ecthyma) Parapoxvirus Skin lesions on lips, Direct contact Skin lesions on Direct contact Chamois, Vaccination of
nostrils, gingiva, with infected fingers. with infected reindeer, sheep and goats,
tongue, teats, vulva, animals or animals or with aurochs training of
prepuce and coronary infective tissue contaminated exposed people
band; elevation of surfaces (e.g.,
skin that progress to clothing,
blisters that encrust brushes, clippers

Rabies Lyssavirus Change in behaviour, Bite by infected Fever, fatigue, Bite by infected Main hosts Control of rabies
apprehension, animal headache, vomit, animal of the virus: in dogs and wild
aggresiveness, hyper- appetite dogs, other carnivores,
excitability, decrease, carnivores, disinfection,
irritability, hyper- sleepiness, bats care in contact
salivation, nervous- partial paralysis, with potentially
ness, solitude, hyper-salivation, infected animals
anorexia, change in agitation,
voice, paralysis, death disorientation

Rift valley fever Bunyavirus Abortions, Mosquitoes, Asymptomatic, Mosquitoes, Other Vaccination of
malformed coughing, self-limiting airborne ruminants, ruminants,
newborns, fever, sneezing infection; less camelids, vector control,
anorexia, conjun- often: fever, monkeys training of
ctivitis, nasal dis- headache, exposed people
charge, death (in muscular pain,
lambs/kids) nausea,
meningitis, reti-
nitis,
haemorrhagic
fever, jaundice,
death

Vesicular stomatitis Vesiculovirus Self-limiting Insect vectors Flu-like signs, Contact with Cattle, Hygiene
infection: blisters on headaches, infected animals horses, pigs measures,
tongue, gingiva, teats, fever, muscle temporary
coronary band; aches isolation of
cachexia, lethargy, infected
pyrexia animals, limiting
exposure to
insect vectors

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Table 1 (Continued)
Disease Agent Small ruminants Humans Other Control
animal measures
species that
can be
infected
Clinical signs Mode of Clinical signs Mode of
transmission transmission
Diseases caused by unconventional agents

Bovine spongiforme Bovine spongiforme Unusual social Consumption New variant of Consumption of Cattle, cats, Active
encephalopathy and encephalopathy prion behaviour, extreme of Creutzfeldt food from minks, monitoring of
other zoonotic protein nervous reactions to contaminated Jakob disease infected wapitis and fallen stock,
transmissible stimuli, changes in meal (progressive ruminants other monitoring at
spongiform fleece colour, nervousness, Cervidae, slaughter,
encephalopathies progressive ataxia, myoclonias, nyalas and condemnation
pruritus, inability to ataxia, amnesia, great kudus of specific risk
feed, progressive hallucinations, material,
degenerating loss of vigilance, breeding for
condition dementia, resistance
acinetic
mutismus)

Central Europe, Canada, the United States, Israel, South-East Asia, between various geographic areas, even within the same country.
Australia and New Zealand are considered to be free from the In developed countries, in which infection is present, reported
disease. In several industrialised countries, animal brucellosis is morbidity rate is generally less than 1 case per 100,000 inhabitants.
under control, but there are sporadic cases of human brucellosis In contrast, in other areas, e.g., some Arab countries, reports reach
acquired outside those countries. In endemic areas, human up to 200 cases per 100,000 inhabitants (Blasco and Molina-Flores,
brucellosis is mainly caused by consumption of dairy products 2011). Altogether, a figure of 500,000 new cases per year is usually
from sheep and goats. Therefore, fight against brucellosis is still an accepted as a global estimate (Pappas et al., 2006).
important issue, either by vaccination or by test and slaughter, Contact with animals and occupational exposure, as well as
based on the Rose-Bengal-Test (Rodolakis, 2014). In sheep or goats, food habits and lack of hygienic measures, represent the main risk
burcellosis is mainly the result of infection by Brucella melitensis, of factors for B. melitensis infection in humans. Because human-to-
which three biovars have been identified. This organism is the human transmission is rare, small ruminants are the main
main aetiological agent of the disease in humans, also termed reservoir for transmission to humans. Humans can be infected
‘Malta fever’. by contact with infected animals by means of the conjunctival or
oronasal mucosae, especially around the time of the animals'
2.1.1. Brucella melitensis disease in sheep and goats
parturition. They may also become infected by ingestion of
Infections with B. melitensis induce abortion and infertility in
contaminated animal products, mainly of dairy products, e.g.,
small ruminants. The incidence is very high in southern and
homemade cheese from raw milk. Meat products are less
eastern parts of the European Union and in many low-income
frequently associated with contamination, because they are
countries. These, in total, include over 70% of the susceptible world
usually cooked before consumption. People in professions or jobs
livestock (FAO, 2009).
with direct contact to livestock (e.g., farmers, butchers, abattoir
Infection with B. melitensis in small ruminants can cause a
workers, veterinarians, laboratory personnel) are at higher risk to
generalised infection, which may persist for years. In pregnant
acquire the disease. Skin, wool, manure and maintenance of farm
ewes and does, the bacteria multiply in the uterus and mammary
premises are also source of infection (Blasco and Molina-Flores,
glands. Abortions occur in the second half of pregnancy. Moreover,
2011; Rodolakis, 2014).
premature births, birth of weak lambs/kids, retention of foetal
The disease can be insidious and may be present in many
membranes and decreased milk production are other frequent
atypical forms. Most common signs of human brucellosis include
signs. Affected foetuses do not show any specific macroscopic
undulant fever, fatigue, headaches, sweats, arthralgia, chills,
lesions. The mammary glands are often infected, with shedding of
malaise, weight loss and myalgia. Spontaneous abortions, mainly
B. melitensis in milk frequent and continuing for several months.
in the first or second trimester of pregnancy, can be seen in women.
Animal to animal transmission usually takes place at the time of
Inadequate treatment is responsible for severe and debilitating
parturition or abortion, as the result of the large number of bacteria
long-standing disease, with severe complications as endocarditis
discharged with the placenta and the uterine fluids. Vaginal
or neurobrucellosis, but the overall case fatality rate is less than 1%
shedding may continue for several weeks after that. Animals are
(Blasco and Molina-Flores, 2011; Godfroid et al., 2011; Rodolakis,
mainly infected by ingestion or inhalation of the causative agent.
2014).
Entry through the skin is also possible after local abrasions.
Chronically infected flocks/herds show cyclic outbreaks of 2.1.3. Prevention and control
abortion, interrupted by short or long ‘silent’ periods. After According to the International Animal Health Code of the World
abortion, a normal parturition may follow in the next lambing/ Organisation for Animal Health, a country is considered to be
kidding, although bacteria shedding can occur again at that time. In officially free from brucellosis if the following conditions prevail
rams and bucks, B. melitensis infection results in orchitis and/or concurrently.
epididymitis (Rodolakis, 2014).
 99.8% of farms in the country to qualify as officially free from
2.1.2. Brucellosis in humans brucellosis.
The global incidence of human brucellosis is not well known,  No case of brucellosis in sheep or goat farms to be reported for at
because of the low reporting figures. Great variations exist least five years.

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 No sheep or goats to be vaccinated against the disease for at least 2.2.1. Clinical signs of chlamydophilosis in small ruminants
three years. The proportion of sublinically and enzootically infected sheep/
goat farms is high. Investigations in northern Germany in 2004–
B. melitensis infections have been traditionally neglected, 05 have revealed infection in 55% of all sheep farms. The highest
because small ruminant production represents generally a low- incidence was evident in migrating flocks, with a mean intra flock
income activity practiced by landless farmers from marginal rural prevalence of 34% (Ganter et al., 2005). In the majority of cases,
areas in the developing world. Due to these marginal and usually abortion occurs in late pregnancy with no previous, specific clinical
nomadic farming systems, the control and eradication of signs, although occasionally vaginal bleeding can be observed a
brucellosis is extremely difficult (Blasco and Molina-Flores, few days before abortion (Rodolakis et al., 1984). Mating of females
2011). Many countries are suffering a re-emergence of the disease that had aborted can lead to infection of the male animals (
in sheep/goats and, also, in humans. Rodolakis and Souriau, 1986), which can potentially lead to
As there is no safe and effective vaccine available for humans, epididymitis.
prevention of human brucellosis is based on control of the disease Possibly, dynamics of infection and risk of abortion depend on
in the animals and on education of people directly involved in the management and timing of mating and lambing. In closed flocks,
animal and food industries. Strategies to reduce prevalence of B. with seasonal lambing, some abortion cases can usually occur in a
melitensis infection may be applied, depending on the level of few older ewes/does four to two weeks before start of the lambing
infection, the animal management system, as well as the financial, season. Younger females are often mated later in the breeding
technical and personnel resources available. In regions with season, hence abortion cases in those animals would occur later in
endemic brucellosis, vaccination with B. melitensis Rev 1 vaccine the lambing season.
is used most widely. Vaccination is efficient for prevention of
clinical brucellosis in sheep and goats and should be considered as 2.2.2. Clinical signs of human chlamydophilosis
the main tool for control of the disease, particularly in nomadic and Zoonotic infections with C. abortus are rarely reported or
extensive transhumaning flocks/herds. In many low-income remain undiagnosed, as the organism induces asymptomatic
countries, a whole flock/herd vaccination of all susceptible sheep infection or mild flu-like illness in humans (Cross et al., 1991),
and goats is the only reasonable strategy to control brucellosis, headache, conjunctivitis (Tontis and Zwahlen, 1991), urogenital
independent of the prevalence of infection (Blasco and Molina- disorders (Stepanek et al., 1983) or, in rare cases, pneumonia
Flores, 2011; Lacasta et al., 2015). (Rodolakis, 2014).
For eradication of brucellosis, measures additional to vaccina- Transmission of C. abortus from small ruminants to humans
tion are also required. Eradication could be achieved based on occurs through inhalation of infectious dust and aerosols during or
combination of vaccination of young replacements (3–4 months after abortion or normal parturition. In pregnant women, infection
old, both males and females) in combination with test and with C. abortus may cause fever, nausea, vomiting and severe
slaughter of adult animals found to be seropositive. The basic headache, frequently associated with abdominal pain, followed by
principle is to avoid introduction of infected animals into healthy abortion and severe complications: septicaemic shock, acute renal
flocks. This could be achieved by an effective control of all animal failure, disseminated intravascular coagulation, pulmonary oede-
movement, which is the most problematic issue. The final ma and respiratory dyspnoea (Pospiscill et al., 2002; Walder et al.,
eradication step is to stop Rev 1 vaccination and apply an exclusive 2005). If the affected women are treated appropriately with
test and slaughter program (Blasco and Molina-Flores, 2011). antibiotics, recovery can be complete and uneventful, although
death of one patient has been described (Beer et al., 1982;
Rodolakis, 2014).
2.2. Chlamydophila infection

2.2.3. Prevention and control

Chlamydophilosis is a significant cause of abortion in small
There is no vaccine available for human chlamydophilosis.
ruminants in countries, where the brucellosis has been controlled
Therefore, prevention depends on its control in animals and
and the second most important cause after brucellosis in most
training of farmers and the exposed population in general.
other regions, except for New Zealand. The economic losses from
Veterinarians and farmers may prevent Chlamydophila abortions
Chlamydophila-associated abortion are severe. In previously
by hygiene measures, treatment and immunisation of animals
uninfected farms, 30% to >60% of pregnant ewes or does may
(Rodolakis, 2014). However, nowhere in the world is enforced an
abort, but such cases are rare. After introduction into a naïve flock/
active control program of the disease, which remains an increased
herd, increased abortion rates are mostly observed during the
risk for people, especially in flocks with enzootic chlamydophilosis.
second year of introduction and are followed by a subsequent or
Prevention of the disease in small ruminants is based on hygiene
even a third year of increased abortion rates, after which the
and biosecurity measures, strategic administration of antibiotics
disease takes on a cyclic nature: abortion affects less than 10% of
and vaccination of susceptible animals by attenuated or inactivated
pregnant females for several years until all primiparous sheep and
vaccines (Rodolakis et al., 1998; Innes and Wheelhouse, 2010;
goats have aborted (Rodolakis, 2014). Under enzootic situations, in
Menzies, 2012; Rodolakis, 2014; Lacasta et al., 2015; Rodolakis and
large farms, abortion rate in animals pregnant for the first time is
Laroucau, 2015)
significantly higher than in older sheep/goats, which rarely
exceeds 4%. Prevention and control of chlamydophilosis programs
2.3. Q fever
focus on reduction of economic losses due to abortion in small
ruminants, as Chlamydophila abortus is considered to be of danger
Q fever is caused by Coxiella burnetii, which is a Gram-negative,
for people associated with small ruminants (e.g., farmers,
obligate intracellular bacterium, very small and immotile. The
veterinarians) rather than for the general population. The
term ‘Q fever’ was first used in the 1930’s by Derrick to describe a
organism also presents a significant hazard for pregnant women
feverish illness in slaughterhouse employees in Brisbane, Queens-
in close contact with infected sheep or goats (Johnson et al., 1985;
land, Australia (Derrick, 1937). With material collected from these
Berthier et al., 1991; Pospiscill et al., 2002; Villemonteix et al. 1990;
people, Burnet and Freeman (1937) succeeded to infect and induce
Walder et al., 2005; Rodolakis, 2014).
fever in guinea pigs, mice and monkeys and could even isolate the
agent. Independently from the Australian team, Davis and Cox

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isolated the bacteria from ticks in the USA (Davis and Cox, 1938). In anorexia and coughing. In some cases, enteritis can be present.
order to honour both scientists and their teams, the new agent was Some patients show a severe atypical pneumonia with dry
named C. burnetii (Maurin and Raoult, 1999). Due to its coughing and severe headache. These patients often have to be
intracellular growth, Coxiella had been considered as a ‘Rickett- hospitalised and treated intensively. More rare cases show
sia-like’ organism. Recent studies using 16S rRNA gene sequencing hepatitis, myocarditis, peri- or endocarditis and neurological
and genome analysis indicated that it was a g-proteobacterium manifestations, e.g., disorientation, meningitis, meningoencepha-
(order Legionellales), hence it is no longer classified in the litis (Babudieri, 1959; Maurin and Raoult, 1999, 2002; Kofteridis
a-proteobacterial Rickettsia group (Stein et al., 1993; Seshadri et al., 2004; Woldehiwet, 2004; Raoult et al., 2005; Eibach et al.,
et al., 2003). Coxiellaceae is now a family in the order Legionellales, 2012; Bothe et al., 2013). Children show, in general, milder
with only one species, C. burnetii. symptoms than adults (Maltezou and Raoult, 2002).
There is a wide range of animal species, which can be infected In 1–2% of infected individuals, chronic infections can develop,
by C. burnetii, including mammals, birds, reptiles, arthopodes and often associated with endocarditis. Immunocompromising con-
humans. Due to their small infective dose, C. burnetii is a major ditions and underlying heart disease or vascular disease are the
zoonotic pathogen, especially for individuals in contact with most important risk factors to consider in potential cases of long-
livestock. Thus, farms with infected sheep/goat act as a special risk standing Q fever (Brouqui et al., 1993). Infections in pregnant
for humans (Serbezow et al., 1999; Maurin and Raoult, 1999; women carry a risk for abortion and stillbirth, also associated with
Woldehiwet, 2004; Arricau-Bouvery and Rodolakis, 2005; Porten increased risk for subsequent long-standing infection (Maurin and
et al., 2006; Roest et al., 2011; Runge et al., 2012; Eibach et al., 2012; Raoult, 1999, 2002; Woldehiwet, 2004). During the outbreak of the
Bothe et al., 2013) disease in the Netherlands, very few patients developed chronic Q
fever, although a much larger group suffered from persistent
2.3.1. Clinical signs of Q fever in small ruminants fatigue and other long-term effects of the infection. Unlike chronic
In general, subclinical disease or peristent infections with C. Q fever, persistent fatigue is not a life-threatening condition, but it
burnetii are prevailing in sheep or goats. Large disease outbreaks can be debilitating and have serious adverse effects in a person’s
are characterised by abortion, stillbirth or delivery of weak lambs, quality of life (Morroy et al., 2011).
as well as placentitis or post-partum metritis, when naïve animals In general, criteria for confirmation of cases of Q fever are (i) a
are infected during pregnancy (Marrie, 1990; Runge and Ganter, clinical presentation with fever, and pneumonia or hepatitis, and
2008; Roest et al., 2011; Runge et al., 2012; Georgiev et al., 2013; (ii) confirmation of the diagnosis in the laboratory by at least a
Lang, 2015). Abortion rates up to 60%, mainly in the final month of four-fold increase of IgG titre against C. burnetii in paired blood
pregnancy, were seen during the outbreak of the disease in goats in serum samples or the presence of IgM antibodies against phase II
The Netherlands last decade, with no signs of general illness. After or antibodies against C. burnetii phase I (Wagner-Wiening et al.,
abortion, some goats showed signs of endometritis. Full-term kids 2006; Roest et al., 2011). Q fever can also be confirmed by PCR on
were weak, with low body weight and high mortality. In several blood serum, throat swabs, laryngeal lavage, urine or faecal
apparently healthy kids, respiratory or digestive tract disorders samples (Eibach et al., 2012; Roest et al., 2013).
were seen. Treatment of pregnant goats with oxytetracyclines did
not reduce abortion incidence (Roest et al., 2011). 2.3.3. Lessons learned from the Q fever outbreaks in The Netherlands
There is increased shedding of C. burnetii, especially in the peri- and Germany
parturient period, through the birth products. Prolonged faecal The world’s ever worst outbreak of Q fever in humans has been
shedding, as well as excretion in milk and urine over weeks are recorded in the Netherlands, in 2007–2009. The outbreak was
important for perpetuating and maintaining the infection within preceded by a very high incidence of abortions in dairy goat herds
animal populations (Berri et al., 2007; Rodolakis et al., 2007; de during 2005–2009. A total of 3523 human cases were diagnosed
Cremoux et al., 2012b; Sting et al., 2013). As there is no active between 2007 and 2009. Proximity to aborting small ruminants
surveillance in small ruminants, aetiological investigations are and increased numbers of susceptible humans were probably the
often performed in cases of severe peri-parturient losses or after main causes of the outbreak (Roest et al., 2011). In the Netherlands,
occurrence of human disease. before that outbreak, 10–20 cases in humans had been diagnosed
annually. In 2005, the first abortions due to Q fever occurred in a
2.3.2. Clinical signs of human Q fever dairy goat farm. In 2006, abortion storms in dairy goat farms
The main sources of human infections are inhalation of increased alarmingly, with up to 60% incidence of abortion in some
infective dust/aerosols, especially from ruminants, and direct herds. This was followed by increasing numbers of cases of the
contact to infected animals. About half of infected humans show an disease in humans, with 168 cases in 2007, 100 cases in 2008 and
asymptomatic seroconversion. After an incubation period of two to 2355 diagnoses in 2009. Epidemiological investigations revealed
three (occasionally up to five) weeks, depending on the infective dairy goat farms in the south west of the Netherlands as the source
dose, in most acute cases the patients show flu-like signs with of human infections. During the winter 2009–10, strict biosecurity
fever up to 40  C, shivering, headache, fatigue, muscular pain, measures were imposed in dairy goat farms, after which incidence

Table 2
Factors that may affect epidemiology of Q fever.

Factor Sheep Goats in large units

Parturition Seasonality of breeding period Breeding synchronisation and
artificial insemination
Housing Pasture, migration, transhumance Indoor living
Faeces Dry Dry
Contact with humans Regular Less frequent
Most susceptible humans Naïve individuals Personnel with long-standing,
close contact
Distribution of Coxiella burnetii within farms Quick and continuous Very quick
Rearing of future replacement animals With their dams Often, motherless rearing

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of human cases decreased sharply in 2010 (Roest et al., 2011;  Information of all involved persons.
Hogerwerf et al., 2011).  Maintenance of simple biosecurity measures, including wearing
The Dutch goat population increased quickly and a more protective equipment by personnel (including FFP-3 breathing
industrial production had been established, with an average herd masks), disinfection of all utilities (including samples) before
size of approx. 900 dairy goats, maintained indoors throughout the taking out of the farm and safe disposal of all consumables and
year and with several herds within a relatively small area. equipment.
Management of herds included, in many cases, oestrus synchroni-  Indoor maintenance of all animals, implementation of measures
sation of some hundred does followed by artificial insemination to keep animals other than sheep/goats out of the farm, rodent
and lambing within some days, conditions supporting increased control.
risk of transmission of C. burnetii by fomites. Large numbers of the  Shearing of animals in the farm and storage or safe disposal of
organism could be transported during kidding into the surround- the wool.
ing environment, by ventilation and/or manure transportation,  Vaccination of all animals in the affected farm to achieve
especially in conditions of dry weather. These could affect reduction of bacterial shedding.
increased numbers of susceptible humans (Berri et al., 2003;  Administration of tetracycline to animals at two-to three-week
Tissot-Dupont et al., 2004). intervals, from 95th day of pregnancy onwards, to reduce
In Germany, the majority of human Q fever infections are abortion incidence risk due to other agents, e.g. Chlamydophila
associated with sheep and rarely with goats, even though Q fever abortus.
occurs rarely in sheep or goats (Anon, 2009c; Georgiev et al., 2013).  Handling of manure: storage under silage film for nine months,
In one case, the source for many human infections was one ewe which is safer, as use of burned lime, which is bactericidal for C.
with healthy twin lambs exhibited in a market, which shed large burnetii, but has a risk for setting fire.
numbers of the organism (Porten et al., 2006). The close  Restrictions in human movements.
association between infections in small ruminants and human  Cooperation and commitment for implementation of measures
outbreaks is not allied to reduced incidence of C. burnetii in sheep/ between farmers, veterinarians, personnel in the public health
goats, in comparison to the incidence in cattle (Sting et al., 2002). departments and laboratory staff.
Epidemiological studies have indicated that infection of humans by  Tracing on and tracing back.
bacterial strains from small ruminants (Tilburg et al., 2012;
Frangoulidis et al., 2013). Besides differences in virulence factors
and species adapted strain differences (Frangoulidis et al., 2014), 3. Viral diseases
there are other factors (e.g., housing, contact of animals with
humans, management of manure, management of mating, 3.1. Orf virus infections
parturition) that affect epidemiology of C. burnetii, as detailed in
Table 2 (Berri et al., 2003; Tissot-Dupont et al.2004; Gilstorf et al., Orf virus is an epitheliotropic DNA parapoxvirus with a
2008; Porten et al., 2006). worldwide distribution. In humans, Orf virus infection occurs
In southern Germany, where human Q fever outbreaks are mainly in relatively well-defined ‘at risk’ populations, which
relatively frequent, transhumance and outdoor lambing over the include veterinary surgeons, shepherds and abattoir workers, in
whole year is common in sheep. Q fever infected sheep flocks can whom it is an occupational hazard (Nettleton et al., 1996).
spread the organism over large distances and for a long period of Household meat processing or unsupervised animal slaughter is
time, so that the endemic infection of sheep leads to frequent, also considered a risk for the disease in humans. In Germany,
small-scale outbreaks in the human population of that densely Muslims buy mostly lambs, which can be infected by Orf virus,
populated area. In northern Germany, seasonal lambing is placing people at risk to develop the disease (Nougairede et al.,
common, so that lambing is mainly indoors during February to 2013). In case of overt clinical signs the risk for the spread of the
March. Therefore, likelihood of transmission of the organism from virus to man is low (Yirrell et al., 1994). Transmissions of Orf virus to
a positive but housed flock is smaller than in the southern parts of humans are probably much more frequent than anticipated from
the country. Despite this, various epidemiological studies have lambs with mild lesions, as often people allow (infected) lambs to
shown a baseline seroprevalence in sheep of 2–3%, although in suckle at their fingers, so that lesions are induced on the finger and
high risk areas, that may increase to 30%. (Ganter et al., 2005; the virus is easily transmitted, especially when there are already
Janowetz et al., 2009; Hilbert et al., 2012). some small wounds on it. Especially during the parturition season,
It is unclear under which conditions the low baseline infection it becomes more and more fashionable to send whole groups of
rate in sheep/goat farms turns to an outbreak, which is not always children from kindergardens to sheep/goat farms to present
indicated by an increased abortion rate. Number of bacteria shed farming, but ignoring the risk for potential transmission of Orf Virus
by clinically healthy ewes/goats during and after parturition can be (and other zoonotic agents) to children and adults.
high enough to infect numerous persons, due to the fact that
infective dose of C. burnetii in humans is estimated to be only one 3.1.1. Clinical signs of orf in small ruminants
(1) organism (Jones et al., 2006). Under the seasonal reproductive A detailed report regarding orf in small ruminants is presented
pattern in sheep, these outbreaks can be self-limiting and the in another paper of this special issue (Spyrou and Valiakos, 2015).
number of animals from which the organism can be recovered, In general, clinical signs of orf consist mainly of skin lesions
decreases. localised primarily in the lips and the nostrils of lambs, as well as in
the vulva and the teats of adult female animals and the prepuce of
adult male animals. Nevertheless, rarely, systemic signs may also
2.3.4. Prevention and control
develop (Reid and Rodger, 2007).
Vaccination of small ruminants with C. burnetii (Arricau-
Bouvery et al., 2005; Hogerwerf et al., 2011; de Cremoux et al.,
3.1.2. Clinical signs of orf in humans
2012a; Eibach et al., 2013). In previous studies, we have concluded
Human orf lesions generally appear on fingers, hands or forearms,
on the following measures that should be implemented in cases of
after a three- to seven-day incubation period. A typical lesion slowly
acute Q fever outbreaks in flocks with the risk of transmission of
progresses from a small, erythematous macule or papule to a large
the organism to humans (Eibach et al., 2012, 2013).
nodule with a red centre, white halo and peripheral erythema. The

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nodule weeps, ulcerates and crusts over. Papillomas might develop symptoms, characterised by fever, headache, muscular pain,
before the lesion regresses. Most infections are self-limited, nausea and photophobia. Recovery occurs within four to seven
resolving in four to eight weeks without leaving a scar. Potential days. Some patients develop haemorrhagic fever with jaundice,
complications include erythema multiforme, deforming scars, and with a case fatality rate of 0.5–2.0%. Neurologic disorders or
secondary bacterial infections; severe disease has occurred in blindness are rare complications after the febrile period (Pepin
immunocompromised hosts. Treatment consists of basic wound et al., 2010; Rodolakis, 2014).
care, but case reports suggest that topical imiquimod might facilitate
healing. In humans, protective immunity to orf is incomplete; 3.2.3. Prevention and control
persons can be infected multiple times. Rift valley fever is transmitted to humans by mosquito bites or
by handling infected animals or placentas, blood, meat and body
3.1.3. Prevention and control fluids from such animals. Drinking raw milk of infected ruminants
Persons who handle animals with orf should wear non- can also transmit the virus (Rodolakis, 2014).
permeable gloves, avoid exposure of open wounds and meticu- Sterilisation of male mosquitos by radiation and use of
lously wash skin wounds with soap and water after handling larvicides at mosquito breeding sites can help to control vector
animals. In addition, slaughterhouses should verify that all animals populations, if these breeding sites are clearly identified and are
to be sold or butchered are in good health; animals with orf lesions not too extended. However, measures to control the vectors are
should be disposed off in a safe manner. Physicians, including poorly efficient and are only palliative in the face of viral
dermatologists, should be informed of the potential for Orf virus epidemics. Animal movement restrictions or banning has low
infection; suspected infections should be confirmed by microbiol- effect on the course of an outbreak within infected areas, but it can
ogy laboratories (Nougairede et al., 2013). Most physicians have reduce expansion of the virus from infected to uninfected areas. In
not encountered patients with orf and might mistake orf lesions for countries free from the disease, livestock and meat should only be
life-threatening conditions, e.g. cutaneous anthrax or neoplasias. imported from countries with official disease-free status. Within
Rapid diagnosis is critical for preventing unwarranted psychologi- different parts of Africa, sentinel farm monitoring has been used to
cal stress, unnecessary surgeries, and inappropriate antibiotic use monitor the circulation of the virus in susceptible animal
(Bogoch et al., 2012). Non-permeable gloves should be used during populations.
direct contact with lesions in humans, despite that human-to- However, only vaccination of susceptible animals provides
human transmission has not been reported. effective control of the disease (Rodolakis, 2014). Modified
attenuated or inactivated vaccines have been developed for
3.2. Rift valley fever veterinary use. The attenuated vaccine based on the Smithburn
strain provides a long term protection, but has a severe residual
Rift valley fever is caused by a mosquito-borne virus that affects virulence, which induces abortions and foetal malformations if
ruminant species in Africa, especially after rain fall, when administered in pregnant animals. This limits its use to areas
increased numbers of mosquitos induce increased circulation of threatened by an imminent outbreak (Pepin et al., 2010; Rodolakis,
the virus. The virus circulates between ruminants; sheep and goats 2014). The inactivated vaccine does not have these adverse
are particularly susceptible and fatality in newborn animals is reactions, but requires a second booster injection to provide full
increased. Humans can become infected with the virus following protection and, thus, it is only recommended for pregnant small
contact with infected animals or animal products, although less ruminants in countries free from the disease. Whatever vaccine is
likely as a result of a mosquito bite. Rift valley fever in humans is used, vaccination must be performed before the onset of the
generally mild or inapparent, but occasionally severe and outbreak, as there is a high risk to transmit the virus from an
potentially fatal complications of the disease can occur (Swanepoel asymptomatic viraemic animal through use of multi-dose contain-
and Coetzer, 2004; Chevalier et al., 2010; Fischer et al., 2013). ers and re-use of needles and syringes during mass animal
Beside the losses, major economic disturbances is induced by trade vaccination campaigns (Davies and Martin, 2003; Rodolakis, 2014).
restrictions, as, even after the outbreaks, livestock trades may be Routine vaccination of livestock in Africa has been prohibitively
restricted for several years (Rodolakis, 2014). expensive, leading to endemicity of the disease in most African
The virus can be transmitted by several mosquito species and countries, so public health messages addressed to residents and
can spread out of Africa, so it can be a worldwide threat for human visitors to endemic areas regarding modes of disease transmission
and animal health. Spreads to the Arabian Peninsula in 2000 and necessary precaution are paramount for prevention of and
(Balkhy and Memish, 2003) and to Madagascar and the Comoros in controlling outbreaks (Balkhy and Memish, 2003). Appropriate
2007–08 (Sissoko et al., 2009) show the possibility for spreading. protective clothing, e.g., shirts with long sleeves and trousers, use
This has renewed the interest into the virus and into the of insecticide-impregnated mosquito bed nets, personal insect
development of preventive measures to contain future outbreaks repellent and avoidance of sleeping outdoors and of outdoor
(Rodolakis, 2014). activities at peak mosquito biting times are simple, yet important
protective measures. In the epizootic regions, meat and milk
3.2.1. Clinical signs of Rift valley fever in small ruminants should be thoroughly cooked before eating (Rodolakis, 2014).
In endemic areas, the disease is asymptomatic. Susceptible
sheep and goats may show fever with no other clinical signs or 4. Diseases induced by unconventional agents
with conjunctivitis, nasal discharge, weakness and decrease in
milk yield. In adults, case fatality may reach up to 30%. Infections 4.1. Bovine spongiform encephalopathy and other zoonotic
during pregnancy induce an increased rate of abortions or foetal transmissible spongiform encephalopathies
malformation, mainly the arthrogyposis-hydranencephaly syn-
drome, whilst newborns usually die due to acute hepatitis Bovine spongiform encephalopathy was first recognised in
(Rodolakis, 2014). 1986. The commonly accepted cause of the transmissible spongi-
form encephalopathies is a transmissible agent called prion (PrP),
3.2.2. Clinical signs of Rift valley fever in humans which is an abnormal form of a protein (Prusiner, 1982).
In general, Rift valley fever in humans is asymptomatic. Histologically, these diseases are characterised by spongiform
Alternatively, they may develop a self-limiting fever with flu-like degeneration of the central nervous system. Although the main

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pathological changes during the course of the disease occur in the Bovine spongiform encephalopathy can also be transmitted to
brain, the infectious agent accumulates early in the lymphoid sheep by inoculation with affected bovine brain homogenate.
tissue (Glatzel et al., 2000). Bovine spongiform encephalopathy has Clinical signs vary in the different sheep breeds used by different
never been confirmed to be naturally occurring in sheep. However, researchers. In a study performed in NPU Cheviots sheep, after a
there remains a possibility that sheep or goats might have been long incubation period, these were affected by a relatively acute
infected with the bovine spongiform encephalopathy agent in the illness of short duration: less than one week and sometimes even
past and that a low amount of the infectious agent might have only one day (Foster et al., 2001a,b). In this case, the main sign was
persisted through horizontal transmission. This is because of the ataxia with little pruritus. In another study, carried out in French
following reasons. indigenous sheep, there was intense pruritus leading to loss of
fleece and ataxia with degenerating condition until death after a
 Especially in the United Kingdom, sheep flocks and goat herds clinical course of around three months (Baron et al., 2000).
were exposed in the past to contaminated feedstuffs, similar to
those that gave rise to the spongiform encephalopathy epidemic 4.1.2. Clinical signs of new variant of Creutzfeldt–Jakob disease (vCJD)
in cattle, albeit at a much smaller level (Schreuder and in humans
Sommerville, 2003). Since the end of 1995, sporadic cases of Creutzfeldt–Jakob
 Sheep can be infected experimentally with the bovine spongi- disease were diagnosed in the United Kingdom and in France in
form encephalopathy agent, by means of the oral route (Foster teenagers. Before 1995, Creutzfeldt–Jakob disease had been
et al., 2001a,b; Bellwothy et al., 2008). diagnosed in young patients only in four cases, with only a single
 Bovine spongiform encephalopathy has been diagnosed in a goat case in the United Kingdom. All new cases showed a histopatho-
in France (Eloit et al., 2005); it was considered as a probable logical pattern typical for Kuru disease, which occurred in only 5%
diagnosis in a goat in the United Kingdom, in which original of all sporadic Creutzfeldt–Jakob disease cases. On the other hand,
diagnosis was classical scrapie, and could not be excluded as a all cases of variant Creutzfeldt–Jakob disease showed a unique
diagnosis in another goat in the United Kingdom. histopathological pattern that had not been demonstrated in any
 Bovine spongiform encephalopathy has been transmitted case before. Therefore, these patterns fitted into a new variant of
between sheep in an experimental setting (Bellworthy et al., the disease. Due to the chronological sequence, variant
2008). Creutzfeldt–Jakob disease appeared plausible to be a consequence
 The clinical signs of bovine spongiform encephalopathy in sheep of oral bovine spongiform encephalopathy infection in humans.
/ goats resemble those of classical scrapie, so the disease could Age at the onset of the disease is between 16 and 48 years. At the
have remained undetected until post-mortem tests to distin- beginning, behavioural changes and compromises, like anxious-
guish the two diseases became available and their use made ness, depression, apathy and sleep disturbances occur. Other early
mandatory in the European Union in 2005 (Anon, 2009a). signs of this variant of the disease are ataxia and sensibility
disorders, especially painful persistent paraesthesias. Later on,
At present, sheep/goats are known to be susceptible to classical progressive dementia and myoclonias are seen. The patients die
scrapie, atypical scrapie and to bovine spongiform encephalopathy. after 7.5–22.5 months (Will et al., 1996; Bruce et al., 1997; Schicker,
Of these diseases, only bovine spongiform encephalopathy is 1998).
actually known to be zoonotic (Anon, 2007).
4.1.3. Prevention and control of bovine spongiform encephalopathy
4.1.1. Clinical signs of bovine spongiform encephalopathy and classical There are appreciable differences in the genetic susceptibility of
scrapie in sheep and goats sheep to transmissible spongiform encepalopathies. There are forms
Clinical signs of natural scrapie in sheep can last from two of the sheep prion protein gene that confer a high resistance (the ARR
weeks to six months and often begins with unusual social homozygote genotype) or semi-resistance (ARR heterozygote
behaviour and extreme nervous reactions to stimuli, e.g., human genotypes) to bovine spongiform encephalopathy (Baylis, 2002)
contact. The general condition of the affected animal deteriorates, and classical scrapie. Genetic resistance provides the opportunity for
sometimes accompanied by a change in the fleece colour, Ataxia is public health protection strategies that allow only animals of the
common and pruritus can result from the animal scratching an resistant genotype or semi-resistant genotypes to be brought into
apparently intense itch against fence posts or by biting the affected the food chain. The genetic susceptibility of goats to transmissible
area (Parry, 1984), e.g., around the base of the tail; occasionally, the spongiform encephalopathies is not sufficiently well understood to
whole of the side of the body can be denuded of wool. In the final provide a basis for similar strategies for goats (Anon, 2009b).
stages of the disease, although the appetite may appear normal, For early detection of bovine spongiform encephalopathy in
the animals lose the ability to feed themselves and the condition sheep or goats, an active and passive surveillance program has
degenerates. Ewes in the clinical phase of the disease can lamb been established in the European Union, based on slaughter checks
clinically healthy lambs and rams remain fertile and active even and investigations in fallen stock. In order to minimise risk of
when affected by ataxic signs (Giadinis et al., 2013). natural transmission of the bovine spongiform encephalopathy
After experimental infection with different scrapie agent strains agent to sheep, selection of sheep for scrapie resistance is
and by various routes, including intracerebral, subcutaneous, oral mandatory for breeders in the European Union. In cases of bovine
and intravenous, it has been found that the clinical signs depend on spongiform encephalopathy in a sheep/goat farm, the whole
the strain of the causal agent and the genetic of the prion protein population of the farm will have to be destroyed. In cases of
(PrP)-gene of sheep. Clinical signs described were, in some trials, of classical scrapie, measures depend on genetic susceptibility of
short duration, usually only two to three weeks and the animals in the farm, whether all animals or only the genetically
predominant sign was lack of co-ordination of gait, sometimes susceptible animals are culled and destroyed. In atypical scrapie, in
recumbency, but with little accompanying pruritus (Foster et al., most cases, only the affected animals are culled.
1996). Other experimental sources of infection could induce For how long these measures will remain in implementation in
clinical signs of longer duration. Outcome of experimental the European Union remains unclear. The Food Standard Agency
infections on incubation period, brain pathology and biochemistry has a proposed decision to stop bovine spongiform encephalopa-
depends on the scrapie agent strain used for infection and the PrP- thy testing of healthy cattle slaughtered for human consumption
gene status of the infected sheep. (Gleadle, 2012). Due to the low numbers of detected bovine

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spongiform encephalopathy cases in small ruminants, it is a losses. If the goal is the elimination of the agent, more support from
question of time when control measures will also be relaxed for the community or the government is necessary. That time was the
small ruminants. first attempt to control a zoonotic disease by implementing a
mandatory program for breeding for resistance against a disease.
5. Concluding remarks There might be some other diseases, which could possibly be
candidates for breeding for resistance.
As it is well shown by the situation of brucellosis, eradication of Bovine spongiform encephalopathy and the consequences of
a disease is long, difficult and too expensive in some countries. In the crisis should also induce a reflection about risks, risk
most cases, prevention of zoonoses will be based on vaccination of assessment and awareness of risks in science, in media and in
animals and training of the exposed population. Development of the population. All together, the number of BSE cases found in
inexpensive, safe and effective vaccines, allowing discrimination of small ruminants can be counted on the fingers of one hand.
infected from vaccinated animals (DIVA) is essential, as is Whether other transmissible encephalopathies can be transmitted
development of cheap, rapid and accurate diagnostic tools. Indeed, from small ruminants to humans is still under investigation, but
as outbreaks of zoonoses in animals precede human cases, has an extremely small probability. But all together, risk for
establishment of an active animal surveillance system to detect humans to acquire a transmissible encephalopathies from small
new cases is essential in providing early warning for veterinary and ruminants is extremely small and we must re-evaluate all the
human public health authorities. The Q fever outbreak in The measures implemented following the bovine spongiform enceph-
Netherlands illustrated that; in spite of the number of slaughtered alopathy crisis, not only the monitoring, but also the condemnation
goats, the government was blamed for the delay to implement the and burning of ‘specific risk material’. In comparison to the risk to
monitoring of bulk tank milk and for having taken more account of acquire the disease from small ruminants, the risk for humans to
the interests of the farmers than of public health (Bults et al., 2012), acquire other diseases from small ruminants, e.g., Q fever,
because the farmers were compensated, but the patients with chlamydophilosis or brucellosis, is much more significant and
chronic Q fever were not, while some of them had lost their work. tangible. Acceptance of respective vaccination programs in
The risk for humans to acquire a zoonotic disease from small humans, e.g., against Q fever, is extremely small in European
ruminants is relative high compared to other farm animal species. countries. Therefore, it may be time to implement active
There are also situations in which this risk can be further increased. monitoring programs and control measures in small ruminants,
During lambing, the risk to transmit C. burnetii or C. abortus is to reduce the risk for human infections. With the sensitive modern
increased and the organisms can be transmitted by aerosols. diagnostic methods, it can be comparatively easy and inexpensive
Especially pregnant women should avoid small ruminant farms to establish a control program. Animals in flocks infected by C.
during the parturition period. The second important risk factor is burnetii or C. abortus can be vaccinated before pregnancy or treated
the consumption of raw milk or raw/undercooked meat, as B. in late pregnancy and further control measures, like lambing
melitensis is thus transmitted. Direct contact is necessary to acquire indoors and increased biosecurity, can be established until
infections with Orf virus or other bacteria, e.g., Corynebacterium lambing. This is only possible if owners of animals with a zoonotic
pseudotuberculosis. disease are not stigmatised and if the costs for the monitoring and
The risk for humans to become infected by zoonotic agents from the control measures are covered by the community and not only
small ruminants is very variable and depends on the agent as well by the farmer.
as human behaviour. Changes in animals housing and manage-
ment of animals in combination with reduction of human exposure Conflict of interest
to zoonotic agents increase risk of outbreaks, as seen in the Q fever
outbreak in the Netherlands (Roest et al., 2011). Changes in human The author has no conflict of interest.
habits, e.g., in food purchases or in meal preparation, can increase
risk to acquire zoonotic infections (Nougairede et al., 2013). References
Training of exposed people is an important measure to reduce
the risk. This education begins with the farmer introducing and Anon, 2007. Opinion of the scientific panel on biological hazards (BIOHAZ) on
certain aspects related to the risk of transmissible spongiform
reflecting biosecurity measures in the farm. Whether or not encephalopathies (TSEs) in ovine and caprine animals. EFSA J. 44, 1–10.
treatment or prophylactic measures against a zoonotic agent is .Anon, 2009. High Level UK. contingency plan for the emergence of naturally
established, depends most on the financial losses, e.g., due to an occurring BSE (or other zoonotic TSEs) in sheep or Goats, http://archive.defra.
gov.uk/foodfarm/farmanimal/diseases/atoz/bse/science-research/documents/
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