The Q fever epidemic in The Netherlands: history, onset,
response and reflection
H. I. J. ROEST1*, J. J. H. C. TILBURG2, W. VAN DER HOEK3, P. VELLEMA4,
F. G. VAN ZIJDERVELD1, C. H. W. KLAASSEN2AND D. RAOULT5
1Department of Bacteriology and TSEs, Central Veterinary Institute of Wageningen UR, Lelystad,
2Department of Medical Microbiology and Infectious Diseases, Canisius Wilhelmina Hospital, Nijmegen,
3Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven,
4Department of Small Ruminant Health, Animal Health Service, Deventer, The Netherlands
5URM, Universite´ de la Mediterrane´e, CNRS-IRD UMR 6236, Faculte´ de Medecine, Marseille, France
(Accepted 1 September 2010; first published online 5 October 2010)
The 2007–2009 human Q fever epidemic in The Netherlands attracted attention due to its
magnitude and duration. The current epidemic and the historical background of Q fever in
The Netherlands are reviewed according to national and international publications.
Seroprevalence studies suggest that Q fever was endemic in The Netherlands several decades
before the disease was diagnosed in dairy goats and dairy sheep. This was in 2005 and the
increase in humans started in 2007. Q fever abortions were registered on 30 dairy goat and dairy
sheep farms between 2005 and 2009. A total of 3523 human cases were notified between 2007 and
2009. Proximity to aborting small ruminants and high numbers of susceptible humans are
probably the main causes of the human Q fever outbreak in The Netherlands. In general good
monitoring and surveillance systems are necessary to assess the real magnitude of Q fever.
Key words: Control, Coxiella, outbreaks, Q fever, zoonoses.
Q fever is a zoonosis caused by Coxiella burnetii, an
intracellular Gram-negative bacterium that is preva-
lent throughout the world . Domestic ruminants
are considered to be the main reservoir for Q fever in
humans , although other animal species, including
pet animals, birds and reptiles, may also be respon-
sible for human cases. Transmission to humans is
mainly accomplished through inhalation of contami-
nated aerosols. The main clinical symptom of Q fever
in goats and sheep is abortion and in cattle reduced
fertility. With abortion, 1000000000 C. burnetii/g
placenta can be excreted . Duration of shedding
of C. burnetii by infected livestock varies depending
on the excretion route and species. In milk, C. burnetii
can be excreted for 8 days in ewes and up to 13 months
in cattle. In faeces, C. burnetii can be excreted up to
8 days after lambing in ewes and up to 20 days in
goats . Goats may shed C. burnetii in two successive
kidding periods . Most animal species carrying
C. burnetii show no symptoms at all . In humans
infection with C. burnetii remains asymptomatic in
y60% of infected persons. In symptomatic patients,
acute Q fever usually presents as a flu-like, self-limiting
* Author for correspondence: Mr H. I. J. Roest, Department of
Bacteriology and TSEs, Central Veterinary Institute of Wageningen
UR, Edelhertweg 15, 8219 PH Lelystad, The Netherlands.
Epidemiol. Infect. (2011), 139, 1–12.
f Cambridge University Press 2010
disease, atypical pneumonia or hepatitis. Infection in
pregnancy may lead to adverse pregnancy outcomes,
such as spontaneous abortion or premature delivery.
About 1–5% of all Q fever cases may progress into
a chronic infection, often leading to life-threatening
endocarditis [4, 6–9].
Since 2007, a Q fever outbreak has been ongoing in
The Netherlands and this is referred to as the largest
outbreak of Q fever ever reported in the literature
. However, Q fever is not an entirely new disease in
The Netherlands. In this review we give an overview
of the history of Q fever in The Netherlands, both in
animals and in humans, the emergence of the disease
and the control measures that have recently been
taken. In conclusion, we put the outbreak in an inter-
Q fever becomes endemic, 1956–2005
Situation of Q fever in humans between 1956 and 2005
In the 1950s a comprehensive survey of the global
distribution of Q fever was commissioned by the
World Health Organization. In The Netherlands, be-
tween 1951 and 1954, almost 10000 human sera were
tested for Q fever with a complement-fixation test and
all were negative [11, 12]. In 1956, the first three
human cases were reported in The Netherlands .
Two patients might have been linked to imported
cattle or a visit abroad, while in the third patient there
was no obvious cause. In 1958 and 1967 two human
Q fever cases were described associated with the
handling of imported wool [14, 15].
The notification of infectious diseases started in
The Netherlands in 1865. The law changed several
times and the list of notifiable diseases became longer
with every change. Q fever was made notifiable in
1975, although it was a very rare disease at that time
. Between 1975 and 2006 the annual number of
cases increased from 0 to 32 per year (Fig. 1). Thirty-
three of the cases notified between 1979 and 1983 were
investigated more thoroughly. Twenty-two (67%)
of these patients were probably infected in The
Netherlands through contact with animals or animal
products . A survey in 1982/1983 among 432
persons, considered to be at high risk because of close
contact with animals and animal products, showed
high percentages (58% in taxidermists to 84% in
veterinarians) of seropositive responders with mainly
IgG antibodies against C. burnetii phase-II antigen,
indicating that Q fever had become endemic in
The Netherlands .
The increase in human cases between 1977 and
1983 (Fig. 1) was assessed by Richardus et al.  by
testing serum samples from persons, not considered to
be at high risk, taken in 1968, 1975, 1979, and 1983
with an indirect immunofluorescence test (IFT) for
specific IgG antibodies against C. burnetii phase-II
antigen. In adults an average seroprevalence of 46%
in 1968 and of 48% in 1983 was found. In children
seroprevalences varied from on average 54% in 1975
to 28% in 1979 and 1983. These results showed no
significant increase in the percentage of infected per-
sons over the years 1968–1983. The increased number
of notified cases since 1980 was explained by the
Q fever became notifiable for humans
in The Netherlands on 13 June 1975
Number of notified human cases of Q fever in The Netherlands
Fig. 1. Number of notified human cases in The Netherlands between 1975 and 2006.
2H. I. J. Roest and others
introduction of a sensitive indirect immunofluor-
escence test for IgM antibodies against C. burnetii. In
the same study  occupational groups with a high
risk of infection showed a significantly higher pro-
portion of seropositives compared to the low-risk con-
trol group, in 1983 84% of 221 veterinarians and 68%
of 94 residents of dairy farms were positive, whereas
in the control group on average 29% tested positive
for IgG antibodies against phase II of C. burnetii. The
age distribution suggested an early onset of infection
as antibody percentages over all age groups between
1 and 64 years were comparable . It remains un-
clear why seroprevalence in the non-high-risk groups,
varying between 30% and 50% in the 1980s, was high
while on average 23 clinical Q fever cases were de-
tected. Protective immunity from childhood  and
under-diagnosis  could have played a role, but the
serological test methods that were used in the 1980s
were developed in-house and are no longer available,
so the sensitivity and specificity of these tests can no
longer be verified.
Situation of Q fever in animals between 1956 and 2005
Surveys in the early 1950s indicated that the bovine
population was free of Q fever at that time [11, 12].
Between 1981 and 1987 the endemic state of Q fever in
farm animals was confirmed by seroprevalence studies
in cattle, sheep and goats [21, 22]. In 1981, 55% of
20 sampled cattle on one farm were tested positive.
In 1987, 10% of 1320 non-dairy cattle, 21% of 1160
dairy cattle and 3% of a total of 494 dairy heifers
were seropositive. At the herd level, about 36% were
found positive with an average of 35% seropositive
animals per herd. The occurrence of C. burnetii in
cattle herds seemed to be associated with abortions, as
77% of the herds with abortions had a mean sero-
prevalence for Q fever of 39%. For the 31% of the
herds without abortions, the mean seroprevalence was
only 17%. In sheep 3.5% (127/3603 sheep sera from
191 flocks) of the animals were found positive with
a herd prevalence of 27%. In goats 2/594 sera from
individual goats from 54 flocks were positive. In 1992
prevalence in 220 representative cat sera was 10% and
in 400 representative dog sera 13% (D. J. Houwers,
et al. unpublished data).
Transition period, 2005–2007
Changing situation of Q fever in animals since 2005
Clinical Q fever in animals was diagnosed in The
Netherlands for the first time in 2005 . In two
dairy goat herds with abortion problems C. burnetii
was detected by immunohistochemistry (IHC) on
placentas . From 2005 to 2007 Q fever abortions
were diagnosed on 15 dairy goat farms and one dairy
sheep farm (Table 1). Abortions, with herd rates up to
60%, were seen mainly in the final month of preg-
nancy without signs of general illness, although some
goats were temporarily a little sluggish with reduced
appetite. After abortion some goats showed symp-
toms of endometritis. Full-term kids were weak, with
low body weight and high mortality. In several ap-
parently healthy kids the rearing period was compli-
cated by respiratory and digestive tract disorders.
Treatment of pregnant goats with oxytetracyclines
did not reduce the abortion rate . Retrospectively,
C. burnetii could be detected by IHC in one preserved
dairy goat’s placenta from a farm with abortion
problems in 2001. In dairy cattle herds C. burnetii
antibodies were detected on 57% of 344 farms using
ELISA on bulk tank milk (BTM) samples during
2005–2006. It was calculated that on 35% of the
farms at least 30% of the cattle could be positive .
Changing situation in humans since 2007
In 2007, individual human Q fever cases were re-
ported, occurring after visits to dairy goat farms with
abortion problems [24, 26]. The first documented
outbreak of Q fever in The Netherlands was described
by Karagiannis et al.  and Van Steenbergen et al.
. A total of 168 human cases were notified in 2007
(Fig. 2). The epidemic became apparent by a number
of indicators: first, a medical microbiologist reported
two patients admitted to hospital with severe pneu-
monia, who did not respond to standard antibiotic
therapy. Four days later, a general practitioner in-
formed the Municipal Health Service (MHS) of an
unusual number of ten patients with atypical pneu-
monia in his practice. A similar report by another
general practitioner from the same area was received
2 weeks later. Finally, an increase in the number of
notifications for Q fever was noticed in the national
registration system of the National Institute for
Table 1. Number of dairy goat and dairy sheep farms
with confirmed Q fever abortions
2005 2006 2007 2008 2009 Total
Dairy sheep farms —
Dairy goat farms
* Including one farm with animals at two locations.
Review of the Dutch Q fever epidemic3
Public Health and the Environment (RIVM). No
specific source could be identified, but it was postu-
lated that the high number of abortions on the
surrounding dairy goat farms might be the source of
the human Q fever cases in the province of Noord-
Brabant. Airborne transmission of contaminated dust
particles could have been facilitated by the unusually
hot and dry weather in the spring of 2007.
In 2007, the outbreak was concentrated around a
single village and in this village a case-control study
was performed . Contact with manure, hay, and
straw proved to be a risk factor. Moreover, people
living in the eastern part of the village close to rumi-
nant farms, of which one dairy goat farm had a recent
history of abortion problems, were at higher risk than
people living in other parts of the village. Contact
with animals and consumption of raw milk products
were not significant risk factors in the multivariable
Notification criteria for a confirmed human Q fever
case were a clinical presentation with fever or pneu-
monia or hepatitis and confirmation of the diagnosis
in the laboratory by at least a fourfold rise in IgG
antibody titre against C. burnetii in paired sera or the
presence of IgM antibodies against phase II or anti-
bodies against C. burnetii phase I . A probable
case was defined as clinical signs with a single high
antibody titre .
Response phase, 2008–2010
Continuation of the human outbreak
In 2008, it soon became clear that the 2007 outbreak
was not an isolated incident. In May 2008 an out-
break of Q fever occurred in a psychiatric care
institution in Nijmegen, province of Gelderland,
y15 km from the 2007 outbreak area . At least 28
in-patients, employees, and visitors had laboratory-
confirmed Q fever illness and several patients of the
institution developed atypical pneumonia. A small
flock of sheep without clinical symptoms of Q fever
was present at the location. Patients had close contact
with lambs, including cuddling as part of the patients’
therapy sessions. Furthermore, on a dairy goat farm
close to the city of Nijmegen, a large number of goats
unexpectedly aborted their offspring. Q fever was
confirmed by PCR on vaginal swabs. The farmer
showed no clinical symptoms indicative for Q fever.
The farmer’s wife suffered from only moderate flu-like
symptoms, including fever and coughing, and for both
persons Q fever was confirmed by PCR on serum,
throat swabs, urine and faecal samples. To determine
the genetic relatedness between the human and animal
clinical samples from both locations multiple-locus
variable number tandem repeat analysis (MLVA) was
carried out. Clinical samples from other patients from
different locations in the same high-risk area were
Number of notifications
59 13 17 21 22 29 33 37 41 45 49 159 13 17 21 25 29 33 37 41 45 49 159 13 17 21 25 29 33 37 41 45 49 53 4 8 12 16
Year and week of onset of illness
Fig. 2. Number of notified human Q fever cases with a known first day of illness according to the week of onset of symptoms,
from 1 January 2007 to 11 May 2010. 2007 (n=168), 2008 (n=1000), 2009 (n=2355), 2010 (n=208). Total number of human
cases in 2007–2009 (n=3523) (compiled by F. Dijkstra).
4H. I. J. Roest and others
included in the study. All genotypes showed a high
degree of similarity with most genotypes differing
from each other by only a single marker, suggesting
a clonal origin (J. J. H. C. Tilburg & C. H. W.
Klaassen, unpublished observations) [33, 34].
Eventually, 1000 human Q fever cases were notified
in 2008 (Fig. 2). The centre of the outbreak and the
area with the most human cases were the same as in
2007, but there was a clear geographical spread to
adjacent areas (Fig. 3). The age distribution (range
7–87 years, average 51 years) was similar to 2007, but
the hospitalization rate decreased from 50% in 2007
to 21% in 2008 [10, 35]. The high hospitalization rate
of 50% in 2007 might be biased by active case-finding
The overall gender breakdown was the same in 2008
as in 2007: the female to male ratio was 1:1.7 .
In April 2009 a sharp increase in human cases was
observed again resulting in a total number of 2355
cases (Fig. 2). Again most of the human cases were
from the same area as in 2007 and 2008, with yet again
a wider geographical spread (Fig. 4). Pneumonia
is the predominant presentation of Q fever in The
Netherlands. For patients notified in 2008 for whom
clinical details were available, 545 were diagnosed
with pneumonia, 33 with hepatitis and 115 with other
febrile illness . The age median of 50 years in
2009 did not differ from that in 2008, neither did the
hospitalization rate of 20% nor the gender break
down of 1:1.7 female to male ratio .
The overall outbreak in humans consisted of at
least 10 separate clusters with multiple sources of ex-
posure. One cluster became apparent in 2008 with a
strong connection to one goat farm with abortion
problems. Patients were living downwind of the goat
farm. Living within 2 km of the goat farm was as-
sociated with a higher risk of Q fever infection com-
pared to living >5 km from the farm . In 2009,
no abortions were notified on this farm, nor in this
area, and veterinary measures such as the handling
of manure, hygiene measures and a visitors ban were
implemented (measures are clarified in the section
‘Response in the veterinary field’), but the number of
human cases still increased. To date, the source of this
Number of human Q fever cases
45 km zone
Fig. 3. Map of The Netherlands. Left: Number of human cases in 2007 and 2008. The red line shows the dairy goat and dairy
sheep voluntary vaccination area in 2008. Right: Dairy goat farms and dairy sheep farms with Q fever abortion history
between 2005 and 2008. [Compiled by National Institute for Public Health and the Environment (RIVM) and Animal Health
Review of the Dutch Q fever epidemic5
increase in 2009 remains unclear . In general, 59%
of the notified human cases in 2009 lived within a
5-km zone around a notified dairy goat or dairy sheep
farm, while 12% of the Dutch population live within
such zones .
In 2010 criteria for detection of C. burnetii in blood,
serum or a sample from the respiratory tract were
added to the notification criteria for human Q fever
cases. In addition, only acute cases with the day of
first illness within 90 days of notification are recorded
in the national infectious disease notification data-
During the period January to May 2010, 208
human cases were registered which indicates a de-
crease in the number of notified human cases com-
pared to 2009 (Fig. 2). Although weather conditions
may have been unfavourable for transmission, it is
hoped that the decrease in the number of human Q
fever cases was caused by reduced exposure due to
Dairy goat industry and prevalence of Q fever in
The dairy goat industry in The Netherlands is con-
centrated in the province of Noord-Brabant, with
farm sizes ranging from 300 to 7000 goats with an
average of at least 600 animals in 2007. Goat density
was 38.1 goats/km2. These farms often bordered
close to villages and cities. The total number of
registered small ruminant farms in The Netherlands
in 2008 was 52000. The number of professional dairy
goat farms with more than 200 adult goats was 350
and the professional dairy sheep industry consisted of
40 farms . Dairy goat farming in The Netherlands
started after the introduction of the European milk
quotation system for dairy cattle in 1984 and in-
creased after the outbreaks of classical swine fever in
1997 and foot-and-mouth disease in 2001. The total
number of goats increased from 7415 in 1983 to
178571 in 2000 and to 374184 in 2009. The total
number of dairy goats aged >1 year increased from
98077 in 2000 to 231090 in 2009 (Table 2) [40, 41].
In 2008, nationwide Q fever seroprevalence in all
small ruminants was low; only 7.8% of goats and
17.8% of goat farms were positive, and 2.4% of sheep
and 14.5% of sheep farms were positive. In 26% of
the BTM samples from 306 dairy goat and dairy sheep
farms C. burnetii DNA could be detected. Analysis
of the first 13 goat farms with abortions showed an
average number of goats per farm of 900 of which
Incidence per municipality
1 Jan. 2009 to 12 Aug. 2009 (10:00)
Number per 100000 inhabitants
Q fever infections per year
Number of goats per km2
Mandatory Q fever
Fig. 4. Map of The Netherlands. Left: Human Q fever incidence/100000 inhabitants per municipality in 2009. The blue line
shows the dairy goat and dairy sheep mandatory vaccination area in 2009. Right: Dairy goat farms with Q fever abortion
history between 2005 and 2009. Darker blue indicates more goats/km2. [Compiled by National Institute for Public Health and
the Environment (RIVM) and Animal Health Service (GD).]
6 H. I. J. Roest and others
20% aborted. The average number of sheep on the
two affected dairy sheep farms was 400 with an
abortion rate of 5% .
Response in the veterinary field
In June 2008, Q fever became notifiable for small
ruminants kept for milk production following the
advice of experts (Table 3). Additional measures were
taken to reduce the assumed risk associated with the
spread of manure and to restrict the number of
visitors to infected farms. In October 2008, voluntary
of Agriculture in the high-risk Q fever area in Noord-
Brabant with the so far unregistered phase-I Q fever
vaccine forruminants [Coxevac1,CevaSante ´ Animale,
France; Fig. 3 (red line), Table 3] . A total of
36000 goats were vaccinated in an area within a
radius of 45 km around the village of Uden. This was
the first time a Q fever vaccine had been used with the
ultimate goal of reducing the number of human Q
fever cases. In order to reduce the number of human
cases the exposure of humans to C. burnetii should be
reduced. To achieve this, excretion of C. burnetii from
the animal host should be minimized, particularly by
the prevention of abortion due to Q fever. Phase-I
Q fever vaccines, contrary to phase-II vaccines,
strongly reduce the number of abortions and excretion
of C. burnetii in challenged pregnant goats that were
initially Q fever-negative . In clinically Q fever-
infected goat herds vaccination with a phase-I vaccine
should reduce the excretion of C. burnetii, especially
in young animals vaccinated before the breeding
season . In general, vaccination with a phase-I
Q fever vaccine is expected to be effective in non-
infected goats. The effect of vaccination in Q fever-
infected goats is not clear and may imply a
continuation of the risk of shedding C. burnetii and
exposure to humans. According to the summary of
product characteristics (SPC), the phase-I Q fever
vaccine is not indicated for use in pregnant sheep.
Assessment of the efficacy of the phase-I vaccine in
pregnant cattle showed a similar probability of the
animals becoming shedders when vaccinated while
pregnant compared to non-vaccinated animals .
In February 2009, measures taken by the govern-
ment were tightened with a stringent hygiene protocol
made mandatory for all professional dairy goat and
dairy sheep farms in The Netherlands, independent of
their Q fever status. The hygiene protocol included
vermin control, measures for handling manure
(farmers were not allowed to remove manure from
their deep litter stables for at least 1 month after
the kidding season, were obligated to cover manure
during storage and transport, and had to underplough
manure immediately when spreading on farming land
or had to store it for at least 3 months), compulsory
rendering of aborted foetuses and placentas and im-
proved general farm hygiene (such as the prevention
of dust and aerosol formation, protective industrial
clothing, clean delivery equipment and the use of
sufficient high-quality bedding material). In addition,
farmers were advised to submit aborted foetuses for
pathological examination [39, 46]. Vaccination be-
came mandatory for all dairy goats and dairy sheep,
and the vaccination area was extended from the
45-km zone around Uden in 2008 (red line in Fig. 3)
to the whole province of Noord-Brabant and small
neighbouring areas in 2009 (indicated by the blue line
in Fig. 4).
In response to the increasing number of human
cases in 2009, additional measures were implemented
in October 2009: PCR positivity of BTM on dairy
goat and dairy sheep farms became a notification
criterion of Q fever in small ruminants in addition to
unexpectedly high abortion rates (>5%); a transport
ban of animals from Q fever-positive farms and a
visitors ban at Q fever-positive farms (Table 3).
Improved monitoring of farm infection status with
BTM monitoring was advised by experts. The back-
ground of this advice was that the abortion rate is
difficult to measure in a flock with over 600 animals,
and on infected farms C. burnetii can also be excreted
in large quantities during normal birth. In large in-
fected herds with many animals having normal deliv-
eries, the total amount of excreted bacteria can also
be very high with a subsequent risk for public health.
BTM monitoring could give insight to the number
of farms where C. burnetii is present. Initially, BTM
monitoring was take place every 2 months, but with
the increased awareness of the risk of Q fever and the
possible risk that Q fever-positive farms might pose
Table 2. Number of goats in The Netherlands [40, 41]
Total no. of
aged >1 year
n.r., No registration.
Review of the Dutch Q fever epidemic7
during kidding season, the frequency of monitoring
was increased to every 2 weeks. Due to BTM moni-
toring the number of Q fever-positive dairy goat and
dairy sheep farms had increased to 88 on 17 April
2010 (Fig. 5).
With changing public and political awareness of
Q fever, the Outbreak Management Team or expert
panels advised the Ministries of Health and Agri-
culture about additional risk reduction measures. At a
meeting in December 2009, experts stated that they
expected vaccination would not be sufficiently effec-
tive in reducing the excretion of C. burnetii in the 2010
kidding season, due to the fact that not all dairy goats
and dairy sheep had been vaccinated before the
2009 breeding season. A more considerable reduction
in the possible excretion of C. burnetii and thus,
environmental contamination, thereby attempting to
reduce human exposure and potential risk to public
health in 2010, might be achieved by preventing
pregnant Q fever-positive goats on Q fever-positive
farms from kidding. These animals were identified
as high-risk animals. Veterinary experts from the
national veterinary reference institute (the Central
Veterinary Institute of Wageningen UR), taking con-
sideration of the findings of Rousset et al. , be-
lieved it impossible to distinguish infected pregnant
animals from non-infected pregnant animals by lab-
oratory testing prior to the start of the kidding season.
This was the basis of the decision to cull all pregnant
animals on Q fever-positive farms. In addition,
breeding dairy goats and dairy sheep was prohibited
until at least June 2010. The culling started in late
Table 3. Overview of legislation concerning Q fever in small ruminants in The Netherlands 
implementation Document codeMeasure
12 June 2008 TRCJZ/2008/1622 Q fever notifiable in dairy goats and dairy sheep; notification when over 5%
abortions within 30 days at farms with more than 100 animals and when over
3% abortions within 30 days at farms with fewer than 100 animals (abortion
rates up to 5% are considered to be more or less normal)
Prohibited from removing manure from the stable for 90 days after notification
Visitors ban in place for 90 days after notification
Special dispensation for Coxevac (CEVA) Q fever vaccine to be used in
Voluntary vaccination in dairy sheep and dairy goats at farms with more than
50 sheep or goats, petting zoos and nursing farms in the restricted 45-km zone
Prohibited from farming more than 50 dairy goats and dairy sheep if certain
hygienic measures are not implemented, such as vermin control, manure
measures, rendering foetuses and placentas (see text)
Mandatory vaccination of dairy sheep and dairy goats on farms with more
than 50 animals, on care farms, petting zoos and zoos in the extended area
(Fig. 4) before 1 January 2010
Mandatory bulk tank milk monitoring for Q fever every 2 months
Prohibited from transporting dairy sheep and dairy goats from a positive farm.
Vaccinated animals may be transported to positive farms
Visitors ban in place at positive farms
Ban on increase of numbers of dairy goats and dairy sheep on a farm
Ban on reproduction of goats
Mandatory vaccination of dairy sheep and dairy goats, on care farms,
petting zoos, zoos, on farms open to the public, mobile sheep flocks, and in
natural reserves nationwide before 2011
Mandatory bulk tank milk monitoring for Q fever every 2 weeks
Prohibited from removing manure from the stable within 30 days after ending
of lambing season
If manure has to be removed from the stable, it should be stored on the farm
for 90 days
Culling of all pregnant goats and sheep on Q fever-positive dairy goat and
dairy sheep farms
Prohibited from adding sheep or goats to a farm
12 June 2008 TRCJZ/2008/1645
16 October 2008TRCJZ/2008/2817
2 February 2009TRCJZ/2009/244
20 April 2009 TRCJZ/2009/1142
1 October 2009Regulation 40823
9 December 2009Regulation 96744
1 January 2010Regulation 72246
14 December 2009
16 December 2009
16 December 2009Letter to Parliament;
Regulation 10178518 December 2009
8H. I. J. Roest and others
December 2009 and was completed in June 2010,
when a number of temporary animal measures im-
posed by the government ended and now require
The measures in the veterinary field were taken to
identify risk farms and to reduce the excretion of
C. burnetii from these farms. Although the effective-
ness of certain measures is still unclear and the lag
time of the measures and the contribution of en-
vironmental contamination with C. burnetii to the
exposure of humans is unknown, the decreasing
numbers of human cases in 2010 thus far might indi-
cate that the measures taken since 2008 have been
The Dutch Q fever epidemic in perspective
Q fever was present in The Netherlands long before it
became a problem in public health and animal hus-
bandry. In this period, Q fever appeared to be neither
Q fever-positive dairy goat
and dairy sheep farms
on bulk tank milk
5 km zone
02,55 10 15
Fig. 5. Map of The Netherlands with all 88 bulk tank milk-positive dairy goat and dairy sheep farms known on 17 April
2010. The red zone is the 5-km zone around a positive farm. [Compiled by Dutch Ministry of Agriculture, Nature and Food
Review of the Dutch Q fever epidemic9
a major health problem for humans, or for domestic
animals. This situation, with high seroprevalence in
animal populations but few human cases, exists in
most European countries . In the years 2005 and
2006, Q fever became a problem in the dairy goat and
dairy sheep industry. Abortion storms in small rumi-
nants were not confirmed prior to 2005, although
abortions with unknown aetiology are part of small
ruminant husbandry with abortion rates up to 5%.
It is not clear why Q fever became a major problem
in The Netherlands but not elsewhere. Several factors
could have facilitated a change in epidemiology in
goats: first, an increase in goat density in specific
areas of The Netherlands and second, extension of
the farms over the years. These two factors could
have affected in-herd and between-herd dynamics of
Q fever, resulting in outbreaks. Third, there could be
pathogen-related factors with circulation of a highly
virulent C. burnetii strain. In the years 2007 and 2008,
it became clear that Q fever also posed a problem to
public health. The connection between Q fever prob-
lems in the dairy goat and dairy sheep industry and in
the human population was made by several authors
based on epidemiological and C. burnetii typing-based
findings [28, 33, 35]. The increase in goat density
took place in the highly populated province of Noord-
Brabant (average population density in Noord-
Brabant is 497 inhabitants/km2, compared to an
average of 398 inhabitants/km2for The Netherlands).
This proximity to a source excreting high numbers
of C. burnetii during abortion, with transmission fa-
cilitated by dry weather and high numbers of suscep-
tible humans is probably the main cause of the human
Q fever outbreak in The Netherlands. The relation-
ship between the change in epidemiology of Q fever in
humans and changes in animal husbandry has been
shown earlier. After the collapse of the large state
farms in Bulgaria in the 1990s individual farmers
started to raise goats, which resulted in a more than
doubling of the number of goats to 1 million in 7 years
. This increase, together with a change to a more
extensive husbandry system, was believed responsible
for the increase of human cases. The increase in
human Q fever in Germany was also probably related
to socio-geographical factors associated with urbani-
zation of rural areas . Despite these examples no
general conclusions can be drawn, as C. burnetii is
endemic in domestic animals throughout Europe
and infection can be maintained in a wide range of
husbandry systems. Although risk factors, such as
an association between human infection and small
ruminants, the proximity of animals (especially dur-
ing parturition) and human populations, and specific
weather conditions are clear, there is still an incom-
plete understanding of transmission pathways with
regard to the maintenance of Q fever within the
animal reservoir and its transmission to humans .
In addition, to date there are no indications of Dutch
Q fever spreading to adjacent areas in Belgium and
The question can be raised if the Dutch outbreak is
indeed the largest of its kind. A posteriori, it would be
difficult to establish if the current epidemic in The
Netherlands, with 3523 human cases within three
consecutive years, represents a unique phenomenon.
In Paragyurische in Bulgaria, more than 2000 cases
that were probably due to Q fever were diagnosed in a
6-month episode in 1993. Although confirmation of
Q fever was hampered, these numbers of patients were
comparable to the 2355 in 2009 in The Netherlands.
The Q fever outbreak of the Balkans, named
‘Balkangrippe’, during the Second World War was at
least comparable in size. In 1941 over 1000 cases were
reported among German troops and during the years
1942–1945 comparable outbreaks were reported in
general terms . However, in these epidemics, no
systematic investigations were performed. The im-
portance of this in combination with the availability
of diagnostic tests was also shown in the epidemic in a
Swiss Alpine valley in 1983 . The hospitalization
of seven patients with atypical pneumonia was able to
be diagnosed as due to Q fever as a result of newly
available diagnostic tests. This detection was followed
by a very large retrospective study in which infection
was identified in nearly 15% of the inhabitants of the
valley, probably correlated with migration of sheep.
This showed that the proportion of patients present-
ing sufficiently severe symptoms to be hospitalized
accounted for only 2%, and that 56% were com-
pletely asymptomatic. This means that for each
patient being diagnosed, an additional 50 patients
probably remain undiagnosed. This is solely based on
systematic testing of the hospitalized patients with
fever. Under these conditions, it is very difficult to
evaluate the true incidence of Q fever, and it is highly
likely that some epidemics have gone completely un-
noticed. Thus, the reported incidence of Q fever de-
pends on three distinct elements. First, it depends on
the true incidence of the disease including existence of
epidemics. Second, the reported incidence depends on
sensitivity and specificity of the diagnostic tools used.
In the Dutch epidemic the use of serological tests,
10H. I. J. Roest and others
which are now commercially available and the use of
real-time PCR on various clinical specimens allowed a
better assessment of the incidence. Finally, the inter-
est of the clinicians and the awareness of the general
public incontestably reinforces the quality of detec-
tion and the percentage of detected patients. With
monitoring systems more cases might be detected, but
few data exist on large-scale monitoring of Q fever in
the human population. In France, preliminary data
showed a regular increase in the number of diagnosed
cases of acute Q fever which probably testifies to the
growing interest and the diagnostic capacities for this
disease. Retrospective research in The Netherlands
also shows that real-time syndrome surveillance might
have detected clusters of human Q fever cases up to
2 years earlier than 2007 .
The Q fever epidemic in humans in The Netherlands
arose from an endemic state and was preceded by
severe Q fever abortion problems in dairy goats and
dairy sheep. Dairy goats and dairy sheep are con-
sidered to be the main source of human outbreaks
and control measures were focused on these animal
species. Although it is too early to evaluate the mag-
nitude of the human Q fever epidemic in 2010, the
decrease in the number of human cases compared to
the previous year is promising. The proximity to small
ruminants excreting high numbers of C. burnetii
during abortion, with transmission facilitated by dry
weather and high numbers of susceptible humans
is probably the main cause of the human Q fever
outbreak in The Netherlands. Q fever outbreaks
can easily be missed in the human field as well in
the veterinary field. In general good monitoring and
surveillance systems are necessary to assess the real
magnitude of Q fever.
We thank R. A. Coutinho for critical reading of
the manuscript and suggestions for improvement,
F. Dijkstra for providing surveillance data, and
A. van der Spek for providing the map showing bulk
tank milk-positive farms.
DECLARATION OF INTEREST
1. Raoult D, Marrie TJ, Mege JL. Natural history and
pathophysiology of Q fever. Lancet Infectious Disease
2005; 5: 219–226.
2. Woldehiwet Z. Q fever (coxiellosis): epidemiology and
pathogenesis. Research in Veterinary Science 2004; 77:
3. Arricau Bouvery N, et al. Experimental Coxiella burnetii
infection in pregnant goats: excretion routes. Veterin-
ary Research 2003; 34: 423–433.
4. Arricau-Bouvery N, Rodolakis A. Is Q fever an emerging
or re-emerging zoonosis? Veterinary Research 2005; 36:
5. Berri M, et al. Goats may experience reproductive
failures and shed Coxiella burnetii at two successive
parturitions after a Q fever infection. Research in
Veterinary Science 2007; 83: 47–52.
6. Fenollar F, Fournier PE, Raoult D. Molecular detection
of Coxiella burnetii in the sera of patients with Q fever
endocarditis or vascular infection. Journal of Clinical
Microbiology 2004; 42: 4919–4924.
7. Klee SR, et al. Highly sensitive real-time PCR for
specific detection and quantification of Coxiella burne-
tii. BMC Microbiology 2006; 6: 2.
8. McQuiston JH, Childs JE, Thompson HA. Q fever.
Journal of the American Veterinary Medical Association
2002; 221: 796–799.
9. Musso D, Raoult D. Coxiella burnetii blood cultures
from acute and chronic Q-fever patients. Journal of
Clinical Microbiology 1995; 33: 3129–3132.
10. Schimmer B, et al. Large ongoing Q fever outbreak in
the south of The Netherlands, 2008. Eurosurveillance
2008; 13: 18939.
11. Kaplan MM, Bertagna P. The geographical distribution
of Q fever. Bulletin of the World Health Organization
1955; 13: 829–860.
12. Wolff JW, Kouwenaar W. Investigation on occurrence
of Q fever in Netherlands [in Dutch]. Nederlands
Tijdschrift voor Geneeskunde 1954; 98: 2726–2732.
13. Westra SA, Lopes Cardozo E, Ten Berg J. The first cases
of Q-fever in the Netherlands [in Dutch]. Nederlands
Tijdschrift voor Geneeskunde 1958; 102: 69–72.
14. Jordans GH. A case of Q fever [in Dutch]. Nederlands
Tijdschrift voor Geneeskunde 1958; 102: 1548–1549.
15. Terwindt VA, van Holten JW. Q fever [in Dutch].
Nederlands Tijdschrift voor Geneeskunde 1967; 111:
16. van Vliet JA. History of notification [in Dutch].
Tijdschrift voor Infectieziekten 2009; 2: 51–60.
17. Richardus JH, et al. Q fever in the Netherlands; a
description of 33 case reports observed between 1979
and 1983 [in Dutch]. Nederlands Tijdschrift voor
Geneeskunde 1984; 128: 2253–2258.
18. Richardus JH, et al. Q fever in the Netherlands: a sero-
epidemiological survey among human population
groups from 1968 to 1983. Epidemiology and Infection
1987; 98: 211–219.
19. Richardus JH. Q fever in the Netherlands – largely un-
known [in Dutch]. Infectieziekten Bulletin 1998; 9: 3–8.
Review of the Dutch Q fever epidemic 11
20. Gageldonk-Lafeber vAB, et al. Occurance of Q fever
in the Netherlands [in Dutch]. Infectieziekten Bulletin
2003; 14: 173–177.
21. Houwers DJ, Richardus JH. Infections with Coxiella
burnetii in man and animals in The Netherlands.
Zentralblatt fuer Bakteriologie, Mikrobiologie und
Hygiene, Series A 1987; 267: 30–36.
22. Anon. Is Q fever present in the Netherlands? [in Dutch].
Tijdschrift voor Diergeneeskunde 1981; 106: 41–42.
23. Vellema P. New diseases Q fever and pasteurellosis
appear [in Dutch]. Geitenhouderij 2006; July, pp. 14–15.
24. Wouda W, Dercksen DP. Abortion and stillbirth among
dairy goats as a consequence of Coxiella burnetii
[in Dutch]. Tijdschrift voor Diergeneeskunde 2007; 132:
25. Muskens J, Mars MH, Franken P. Q fever: an overview
[in Dutch]. Tijdschrift voor Diergeneeskunde 2007; 132:
26. Weevers A, et al. Pneumonia after visiting a goat
farm [in Dutch]. Nederlands Tijdschrift voor Medische
Microbiologie 2007; 15: 80–81.
27. KaragiannisI,et al.
Netherlands: a preliminary report. Eurosurveillance
2007; 12: 3247.
28. Van Steenbergen JE, et al. An outbreak of Q fever in
The Netherlands – possible link to goats [in Dutch].
Nederlands Tijdschrift voor Geneeskunde 2007; 151:
29. Karagiannis I, et al. Investigation of a Q fever outbreak
in a rural area of The Netherlands. Epidemiology and
Infection 2009; 137: 1283–1294.
30. Centre for Infectious Disease Control, National Institute
for Public Health and the Environment. (http://www.
index.jsp). Accessed 1 August 2009.
31. Schimmer B, et al. Sustained intensive transmission of
Q fever in the south of the Netherlands, 2009.
Eurosurveillance 2009; 14: 19210.
32. Koene RP, et al. A Q fever outbreak in a psychiatric
care institution in The Netherlands. Epidemiology
and Infection. Published online: 9 February 2010.
33. Klaassen CH, et al. Multigenotype Q fever outbreak,
the Netherlands [Letter]. Emerging Infectious Diseases
2009; 15: 613–614.
34. Tilburg JJHC, et al. Molecular typing of Coxiella
burnetii directly in various clinical samples shows a
possible clonal origin of the ongoing Q-fever outbreak
[Abstract]. Antonie van Leeuwenhoek International
Journal of General and Molecular Microbiology 2009;
35. van der Hoek W, et al. Q fever in the Netherlands: an
update on the epidemiology and control measures.
Eurosurveillance 2010; 15: 19520.
36. Schimmer B, et al. The use of a geographic information
system to identify a dairy goat farm as the most likely
source of an urban Q-fever outbreak. BMC Infectious
Diseases 2010; 10: 69.
37. Centre for Infectious Disease Control, National Institute
for Public Health and the Environment. (http://www.
Q fever outbreakin the
index.jsp). Accessed 2 April 2010.
38. Roest HJ, et al. Q fever in 2008 in the Netherlands and
the expectations of 2009 [in Dutch]. Tijdschrift voor
Diergeneeskunde 2009; 134: 300–303.
39. Van den Brom R, Vellema P. Q fever outbreaks in
small ruminants and people in the Netherlands. Small
Ruminant Research 2009; 86: 74–79.
40. Statline, database Statistics Netherlands (CBS). (http://
T& STB= G1,G2). Accessed 3 June 2010.
41. Statline, database Statistics Netherlands (CBS). (http://
G2&STB=T). Accessed 3 June 2010.
42. Dutch Ministry of Agriculture Nature and Food Quality
Accessed 28 March 2010.
43. Arricau-Bouvery N, et al. Effect of vaccination with
phase I and phase II Coxiella burnetii vaccines in preg-
nant goats. Vaccine 2005; 23: 4392–4402.
44. Rousset E, et al. Efficiency of a phase 1 vaccine for the
reduction of vaginal Coxiella burnetii shedding in a
clinically affected goat herd. Clinical Microbiology and
Infection 2009; 15: 188–189.
45. Guatteo R, et al. Assessing the within-herd prevalence
of Coxiella burnetii milk-shedder cows using a real-time
PCR applied to bulk tank milk. Zoonoses and Public
Health 2007; 54: 191–194.
46. Dutch Ministry of Agriculture Nature and Food Quality
(LNV). Hygiene plan for dairy goat and dairy
sheep farms [in Dutch] (http://www.minlnv.nl/portal/
7609889&p_mode=). Accessed 6 February 2009.
47. Rousset E, et al. Coxiella burnetii shedding routes and
antibody response after outbreaks of Q fever-induced
abortion in dairy goat herds. Applied Environmental
Microbiology 2009; 75: 428–433.
48. EFSA Panel on Animal Health and Welfare. Scientific
Opinion on Q fever. EFSA Journal 2010; 8: 1595.
49. Serbezov VS, et al. Q fever in Bulgaria and Slovakia.
Emerging Infectious Diseases 1999; 5: 388–394.
50. Hellenbrand W, et al. Changing epidemiology of Q fever
in Germany, 1947–1999. Emerging Infectious Diseases
2001; 7: 789–796.
51. Spicer AJ. Military significance of Q fever: a review.
52. Dupuis G, et al. An important outbreak of human Q
fever in a Swiss Alpine valley. International Journal of
Epidemiology 1987; 16: 282–287.
53. van den Wijngaard CC, et al. In search of hidden Q-fever
outbreaks: linking syndromic hospital clusters to in-
fected goat farms. Epidemiology and Infection. Published
online: 18 May 2010. doi:10.1017/S0950268810001032.
12H. I. J. Roest and others