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Rathkjen and Dall Acta Vet Scand (2017) 59:4
DOI 10.1186/s13028-016-0270-z
RESEARCH
Control anderadication ofporcine
reproductive andrespiratory syndrome virus
type 2 using a modied-live type 2 vaccine
incombination witha load, close, homogenise
model: an area elimination study
Poul H. Rathkjen1* and Johannes Dall2
Abstract
Background: Porcine reproductive and respiratory syndrome virus (PRRSV) causes significant animal and economic
losses worldwide. The infection is difficult to control and PRRSV elimination at local level requires coordinated inter-
vention among multiple farms. This case study describes a successful elimination of PRRSV from all 12 herds on the
Horne Peninsula, Denmark, using a combination of load, close, homogenise (LCH) using PRRSV type 2 modified-live
vaccine, optimised pig flow, and’10 Golden Rules’ (10GR) for biosecurity management. To the authors’ knowledge, this
is the first successful European PRRSV area elimination project documented in detail. The PRRSV type 2 modified-live
vaccine was used as part of the LCH method in breeding herds. Complete or partial depopulation was performed in
some infected herds. A simplified biosecurity protocol (10GR) based on the McREBEL™ system of pig flow manage-
ment, was employed in all herds and at all times throughout the study.
Results: At study commencement, all herds were infected with PRRSV, and most were actively shedding virus. In
just over 18 months, all 12 herds on the Horne Peninsula were confirmed to be PRRSV negative by polymerase chain
reaction testing and negative for antibodies against PRRSV by enzyme–linked immunosorbent assay testing. All herds
were subsequently obtained ‘Specific Pathogen Free’ status for PRRSV.
Conclusions: This study provides compelling evidence suggesting that an area elimination plan combining LCH with
PRRSV type 2 vaccination, optimised pig flow, and 10GR for biosecurity management can effectively eliminate PRRSV
from a geographic area. Additionally this study confirms the value of a previously unpublished, simplified alternative
to the McREBEL system for controlling PRRSV.
Keywords: Area regional control, Elimination, Modified-live vaccine, Load close homogenise, PRRS
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Background
Porcine reproductive and respiratory syndrome (PRRS)
is one of the most prevalent viral swine diseases in the
world, responsible for substantial economic losses world-
wide [1]. In the US, PRRS is estimated to cause annual
losses of around $664 million [2]. A 2012 economic anal-
ysis in nine Dutch sow herds found that the mean eco-
nomic loss per sow per 18-week outbreak of PRRSV was
€126 [3].
Porcine reproductive and respiratory syndrome is
caused by the PRRS virus (PRRSV) and was first reported
in the late 1980s [4]. Two PRRSV genotypes have been
described: type 1 and type 2, isolated in Europe and
North America, respectively. Sequence comparison has
Open Access
Acta Veterinaria Scandinavica
*Correspondence: poul.rathkjen@boehringer-ingelheim.com
1 Boehringer Ingelheim Vetmedica GmbH, Binger Straße 173,
55216 Ingelheim, Germany
Full list of author information is available at the end of the article
Page 2 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
highlighted significant genetic differences between them
[5].
Porcine reproductive and respiratory syndrome causes
high morbidity and mortality, poor reproductive per-
formance and slow piglet growth rates [1]. e extent
of reproductive symptoms varies depending on age,
pregnancy status and stage of gestation [6, 7]. In non-
pregnant sows, PRRS can develop without symptoms,
or cause appetite loss or fever [6]. In pregnant sows, the
virus may cross the placenta during late gestation, infect
developing foetuses and increase the risk of abortion,
early farrowing and foetal death [8, 9]. Neonatal and
nursery pigs may experience respiratory distress, listless-
ness, pneumonia, high fever, anorexia, conjunctivitis and
growth retardation [6, 10–12]. In growing and finishing
pigs, the severity of PRRS varies from no detectable signs
to fatal pneumonia, depending on the viral strain and the
presence of opportunistic bacterial or viral coinfections
[13].
At both herd and individual level, PRRSV infection is
difficult to control for several reasons. PRRSV infection
can be completely cleared by the porcine immune sys-
tem, but considerable gaps remain in our understanding
of the immunological response to PRRSV [14]. In the
field, the diversity of PRRSV is increasing [15]. Levels of
genetic similarity between vaccine and field challenge
have often been used as a predictor of vaccine efficacy,
but the ability of a vaccine to protect against a certain
field virus is not linked to the level of sequence homology
it shares with the challenging strain: the degree of genetic
similarity does not predict the cross-protective ability of
the vaccine [14]. Despite these challenges, vaccination
is a popular method of controlling PRRS and reducing
losses caused by it. Multiple vaccines are commercially
available [11].
Accepted PRRSV control and elimination models for
multiple herds include herd closure with either total herd
replacement or with normal herd replacement rates, and
depopulation/repopulation of infected herds [16, 17].
Herd closure involves preventing entry of new animals,
while depopulation/repopulation involves complete
removal of PRRSV-positive animals from a herd, clean-
ing and decontaminating the site, then replacing with
PRRSV–negative animals bred elsewhere [17]. Depopu-
lation/repopulation is effective, but expensive because of
requirements for large external breeding projects [17] and
loss of productivity after depopulation [2]. Alternatively,
the load, close, homogenise (LCH) (also known as load,
close, expose) model allows the PRRSV status to stabilise
in a breeding herd before introduction of new PRRSV-
negative animals [18, 19]. Using this model, PRRSV can
be completely eliminated from large breeding (sow) herds
[14] without incurring substantial losses of productive
time (i.e. time without weaned pigs) for the breeding herd.
LCH is accomplished by loading herds with gilts before
closing the herds to new animals for minimum of 200days
[14]. Uniform PRRS status must then be achieved either
by simultaneous vaccination or by inoculation with serum
containing resident virus [19]. e LCH model is inex-
pensive compared with depopulation/repopulation of a
breeding stock [20], and broadly recognised as effective at
stabilising PRRSV-positive breeding herds [21, 22], but it
requires stringent biosecurity measures to prevent virus
transmission within the herd.
e Management Changes to Reduce Exposure to
Bacteria to Eliminate Losses™ (McREBEL) system was
developed in 1994 to reduce the spread of PRRSV and
secondary bacterial infections among farrowing house
pigs, and to nursery pigs [22–24]. e McREBEL system
helps stabilise PRRSV infection within the breeding herd
and reduce mortality among infected nursery pigs [24].
e McREBEL system has several advantages, but the sys-
tem can be difficult to implement for many reasons. For
example, farm staff can be unwilling to abandon cross-
fostering and perform piglet euthanasia, and staff incen-
tive plans need to be reviewed to ensure its success [24].
e Horne Peninsula is a region in the southern Danish
island of Funen, approximately 50 kilometres southwest
of Odense. e peninsula is a naturally limited geograph-
ical area; it is surrounded with water on three sides, and
spans approximately 6 kilometres North to South, and
10 kilometres East to West. It is an area with intensive
pig farming: 12 herds are situated on the peninsula, and
include breeding, wean-to-finish and finishing produc-
tion, but no other herds are situated within 4km.
Until the current elimination plan started, all farms on
the Horne Peninsula repeatedly experienced PRRS out-
breaks despite multiple attempts to control the virus.
Common problems were periodic outbreaks of abortion,
many stillborn piglets, poorly-lactating sows, poorly–
performing piglets at weaning, and high mortality in one
particular finisher herd. Different attempts to control the
PRRSV in the area had already been tried, but with low
success. Prior control attempts included depopulation,
vaccinating incoming gilts with PRRS modified-live vac-
cine (MLV) in quarantine and systematically implement-
ing some McREBEL rules to varying degrees. Overall, a
systematic approach to control or eliminate PRRSV from
the whole area was needed.
e objective of this area elimination case study was to
eliminate PRRSV infection as defined by absence of pigs
with PRRSV and corresponding antibodies from all herds
on the Horne Peninsula, Denmark, using a combination
of LCH using PRRS modified-live type 2 vaccine, opti-
mised pig flow, and implementation of’10Golden Rules’
(10GR) for biosecurity management.
Page 3 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
Methods
Herds
e study area included all 12 herds on the Horne Pen-
insula: five finisher herds, four breeding herds, two
wean-to-finish herds, and one gilt quarantine (Table1).
Breeding herds contained sows, gilts ready for breed-
ing, and weaned piglets. Wean-to-finish herds received
weaned piglets from breeding herds and raised them
until slaughter. Finisher herds received piglets at around
11weeks of age, and raised them until slaughter.
In total, the herds on the peninsula contained approxi-
mately 15,000 animals. Movement of animals between
the 12 herds was coordinated in two separate pig flows:
Flow 1 and Flow 2. All animals in Flow 1 originated from
F1B1 and F1B2, and all animals in Flow 2 originated from
F2B1 and F2B2. eherds in each flow were controlled
by four separate owners who worked closely with each
other. PRRSV-negative gilts were imported into F2B1
only after completing 12weeks in all in, all out (AIAO)
quarantine: no other herds received animals from outside
of the Horne Peninsula. Animals were exported out of
the Horne Peninsula from the nursery of F1B2 only. All
other animal movements were within the herds on the
peninsula.
Layout offarm buildings
Breeding herds contained separate areas: farrowing
rooms and nursery rooms. F1WF1 had four nursery
rooms and six finisher rooms: all were separate, but all
pigs entered through one nursery room and passed
through others whilst in transit. Similarly, pigs moving
from nursery to finisher rooms passed through several
rooms containing piglets of other ages. At study com-
mencement, F1WF1 operated as continuous flow. F1WF2
comprised two barns: a nursery and a finishing barn,
both of which had multiple rooms. AIAO production was
observed in all rooms in both the nursery and finishing
barns. Finishing herds contained pigs separated into dif-
ferent rooms by age group, and AIAO production was
observed. F1Q consisted of two adjacent buildings, con-
nected by corridors. One building housed pregnant sows
and finishers that arrived from F1B2, and the other build-
ing housed gilts in acclimatisation and quarantine. Sepa-
rate rooms were entered from the corridor, and rooms
did not share airspace and were not connected under the
floor slats. Strict AIAO production was observed.
Study timeframe
e study began in the first week of July, 2013.
Week 0
Load close homogenise was commenced at Week 0 in
F1B1 and F1B2. At Week 0, F1Q was loaded with gilts
10–32weeks of age, and sites with sows and gilts were
closed for the next 29weeks. All sows, gilts (existing and
newly-introduced), boars and piglets (older than 1week)
Table 1 Overview ofherds included inthe study
F1B1 Flow 1 Breeding Herd 1, F1B2 Flow 1 Breeding Herd 2, F1F1 Flow 1 Finisher Herd 1, F1F2 Flow 1 Finisher Herd 2, F1Q Flow 1 Quarantine, F1WF1 Flow 1 Wean-
Finish 1, F1WF2 Flow 1 Wean-Finish 2, F2B1 Flow 2 Breeding Herd 1, F2B2 Flow 2 Breeding Herd 2, F2F1 Flow 2 Finisher Herd 1, F2F2 Flow 2 Finisher Herd 2, F2F3 Flow 2
Finisher Herd 3
Herd name Owner Type of
production Number andtype
ofanimals Age ranges, weeks Approximate
weight ranges, kg
Flow 1
F1B1 Owner 1 Breeding 500 sows Piglets: 0–4 Piglets: 1–7
F1B2 Owner 1 Breeding 300 sows Piglets: 0–4
Weaned piglets: 4–12 1–7, 5–30
F1Q Owner 1 Gilt quarantine 200 pregnant sows
550 gilts
1000 finishers
10–32
12–18 30–120
30–110
F1WF1 Owner 2 Wean-to-finish 1220 finishers 4–18 7–110
F1WF2 Owner 3 Wean-to-finish 2000 finishers 4–18 7–110
F1F1 Owner 2 Finishing 1000 finishers 11–18 30–110
F1F2 Owner 4 Finishing 800 finishers 11–18 30–110
Flow 2
F2B1 Owner 5 Breeding 400 sows
2000 growers Piglets: 1–4
Weaned piglets: 4–12 1–7
5–30
F2B2 Owner 5 Breeding 320 sows
1300 growers Piglets 1–4
Weaned piglets: 4–12 1–7
5–30
F2F1 Owner 6 Finishing 1600 finishers 11–18 30–110
F2F2 Owner 7 Finishing 900 finishers 11–18 30–110
F2F3 Owner 5 Finishing 1000 finishers 11–18 30–110
Page 4 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
on all sites except F2B1 and F2B2 were homogenised by
vaccination with 2 ml PRRSV type 2 MLV (Ingelvac®
Boehringer Ingelheim Vetmedica Inc., St. Joseph, MO,
USA). F2B1 and F2B2 were already PRRSV positive-
stable at study commencement, so homogenisation was
deemed unnecessary. From Weeks 0–10, Finisher pigs
in F2F1, F2F3 and F2F3 were vaccinated with 2ml PRRS
type 2 MLV upon arrival from F2B1 and F2B2, to avoid
introducing naïve pigs. Vaccinations were performed
according to the manufacturer’s guidelines on dose and
administration (Boehringer Ingelheim Vetmedica GmbH,
Germany).
Depopulation commenced in F2B1 and F2B2. e
nursery rooms containing the two oldest age groups (pig-
lets older than 8weeks) were depopulated.
Weeks 2–4
All piglets in F1B1 and F1B2 were vaccinated with 2ml
PRRSV type 2 MLV when they reached 7 days of age.
Vaccination of sows, boars and gilts was repeated at
Week 4. All animals in F2F1, F2F2 and F2F3 that had not
been vaccinated previously were also vaccinated at Week
4.
Weeks 6–16
On a rolling basis from Week 6 to 16, all weaned piglets
(3 weeks of age) that had not already been vaccinated
when entering breeding herd nurseries or wean-to-finish
nurseries, were vaccinated with 2ml PRRSV type 2 MLV
upon arrival.
At Week 16, depopulation of nursery rooms in F1B2,
and partial depopulation of nursery rooms in F1WF1
commenced.
All timesthroughout the study
Sampling and diagnostic testing to determine PRRSV
shedding and exposure status continued every 5 weeks
from study commencement, until all herds were con-
firmed PRRSV and antibody negative by polymerase
chain reaction (PCR) and enzyme-linked immunosorb-
ent assay (ELISA), respectively.
e 10GR for biosecurity and pig flow management
were employed in all herds and at all times throughout
the study (Table2). ese rules were devised in 2005 by
Boehringer Ingelheim, and are based on the principles of
the McREBEL system for disease management [23].
10 Golden Rules forbiosecurity management
Staff members received training in the 10GR from
the responsible veterinarian on each farm. Training
emphasised the importance of open and frequent com-
munication among staff members. To ensure optimal
compliance with the 10GR, farms were audited by the
farm veterinarian at 5-week intervals throughout the
study. If the audit found that the 10GR were not being fol-
lowed, this was communicated to the staff, and corrected.
Sampling anddiagnostic testing ofPRRSV status
Piglets were randomly selected from among all parity
sows. To determine PRRSV status among weaning-age
piglets 8weeks before study commencement, blood sam-
ples were taken from 3-week old (pre-wean) piglets, and
piglets 2, 3, 4, 6, 7 and 8weeks after weaning in breeding
herd nurseries. Samples were then taken at 5-week inter-
vals throughout the study. Serum was harvested from the
blood samples by routine methods.
In breeding and WF herds, blood samples were taken
from at least 30 animals at each time point, and com-
prised samples from a minimum of 5 animals per age
group (each week of age). ese sample sizes were ade-
quate to detect at least one positive sample with 95% con-
fidence if the prevalence of PRRSV positive pigs was 10%
or higher [25], and to meet the sample size requirements
needed for declaring of PRRSV free Specific Pathogen
Free (SPF) status [26].
In finisher herds, blood samples were taken from at
least 20 animals. is sample size was adequate to detect
at least one positive sample with 95% confidence if the
prevalence of PRRSV positive pigs was 15% or higher.
Fewer samples were taken from finisher herds than from
breeding and WF herds because it was assumed that if
pigs were infected with PRRSV during the early finishing
period, the prevalence of infected pigs would be higher.
is sample size also met the sample size requirements
needed for declaration of PRRS free SPF status in routine
monitoring of negative herds.
Individual serum samples were used to evaluate PRRSV
exposure status (indicated by the presence of PRRSV
antibodies in serum). An ELISA method (IDEXX Herd-
Check PRRS X3 ELISA, IDEXX Laboratories Inc., West-
brook, ME, USA) was used to detect PRRSV antibodies.
Serum samples from each age group were pooled, and
used to determine PRRSV shedding status (indicated
by the presence of viral DNA in serum). Reverse tran-
scriptase PCR (rtPCR) was used to detect PRRSV RNA.
Combining PCR and ELISA increased the confidence
that detection would occur if pigs were exposed to
PRRSV.
A herd was declared to have a positive exposure
status (ELISA positive; presence of anti-PRRSV anti-
bodies) if one or more individual serum samples was
positive (Sample: Positive ratio cut off >0.4). A herd
was declared to have a positive shedding status (PCR
positive; presence of PRRSV RNA) if one or more
pooled serum samples was PCR positive for PRRSV
RNA. PRRSV was considered eliminated from a herd
Page 5 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
after PRRSV RNA or antibodies were not detected after
testing at four consecutive time points (taken at 5week
intervals).
PRRS status ofherds, andocial declaration ofPRRSV
Specic Pathogen Free status
roughout the study, overall PRRS status of herds
throughout the study was classified according to the
American Association of Swine Veterinarians (AASV)
terminology, taking into account both PRRSV shed-
ding and exposure status [27]. Herds were classified as
either: negative (ELISA negative and PCR negative),
positive-stable (ELISA positive but PCR negative); or
positive-unstable (ELISA positive and PCR positive).
In addition, declaration of PRRSV free SPF status was
sought, according to the regulations from SPF–SUS,
Denmark [26]. PRRSV SPF status can be granted only
when PRRSV has been eliminated (proven PCR and
ELISA negative) from a herd. To meet the requirements
for PRRSV free SPF declaration, 30 PRRSV-negative sen-
tinel gilts were placed into each herd after samples from
herds tested both PCR and ELISA negative. PRRSV free
SPF status was confirmed if the sentinels remained PCR
and ELISA negative after 6months.
Table 2 The 10 Golden Rules
AIAO all in all out, MLV modied-live vaccine, PRRSV porcine reproductive and respiratory syndrome virus
Rule Rationale
1 Minimise cross-fostering and movement of piglets: cross-foster only
surplus piglets The immune system is immature in newborn piglets; immunity depends
on passive immunisation transmitted via colostrum [37]. Piglets
receive optimal protection from their own mothers so should only be
moved if a sow cannot support her whole litter. Furthermore, moving
piglets to other sows causes weight loss in both moved piglets and
their new litter mates [38]
2 Avoid cross-fostering after 48 h Maternal immune protection starts to decrease when piglets reach
3 days of age [37]. Cross-fostering before maternal protection
decreases is strongly recommended
3 Avoid spreading disease when handling piglets by keeping piglets in
pens Urine, blood, faeces and semen are vehicles for PRRSV transmission;
special attention should be paid to the use of equipment (e.g. needles
and castration equipment)
4 Change needles between litters PRRSV is easily transmitted among pigs by needles, so regular replace-
ment of needles (at least between litters) is recommended. Diseased
piglets should be treated after healthy piglets
5 Do not move diseased piglets Diseased piglets often have compromised immunity and comorbidities
that increase the likelihood that they are also carrying PRRSV. Their
viral load is also likely to be higher, increasing the risk of spreading
infection. Therefore diseased piglets should remain with the same
sow to limit viral spread: if a piglet is too weak for this, it should be
euthanised
6 Wean all piglets from each batch simultaneously, and ban weaned
piglets from the farrowing rooms Holding smaller piglets back in the farrowing rooms for quality before
they are weaned can jeopardise PRRS control programmes [39]. Such
piglets are more likely to be diseased, and to spread PRRSV to others
7 Maintain strict AIAO batch production at all times from weaning to
finishing After piglets are weaned, batch production should continue, and should
be either by site, barn or room. If a batch is not completely removed
before placement of new pigs, infection pressure rapidly increases. Do
not share needles, equipment, personnel and protective equipment
between batches (unless cleaned and disinfected)
8 Avoid contact between age groups Risk of infection is increased 13-fold if contact is permitted between
growing pigs of different ages during restocking of rooms [40]. Mixing
PRRSV-positive pigs in one age group with PRRSV-negative, non-
vaccinated pigs in other age groups greatly increases PRRSV shedding
[41, 42]
9 Avoid contact between sows and piglets (<6 months of age) Breeding herds and grower/finisher pigs should never be in contact (i.e.
when moving pigs and sows around the farm) because cross-contam-
ination between groups can occur
10 Introduce incoming and home-produced gilts via quarantine. Admin-
ister PRRSV MLV upon entry to quarantine areas Natural immunisation of gilts should be avoided because it cannot be
monitored or controlled. If natural immunisation occurred just before
entering a breeding site, there would be a high risk of introducing
wild-type PRRSV to the breeding herd. While in quarantine, gilts
should be immunised twice with PRRS MLV (vaccinations should be
administered 4 weeks apart)
Page 6 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
Results
Time taken toeliminate PRRSV fromall farms onthe Horne
Peninsula
e study extended from July 2013 to July 2015. All herds
on the Horne Peninsula were initially PRRSV positive-
unstable except F2B1 and F2B2, which were positive-
stable (Fig.1; Additional file1). All herds had confirmed
PRRSV free SPF status by April 2015; less than 2years
after study commencement (Table3).
Elimination inbreeding herds
F1B1 and F1B2 were initially weaning PCR and ELISA
positive piglets. By September 2013, both were weaning
PCR negative, but ELISA positive piglets. ree-week old
piglets remained ELISA positive on all sampling points
until July 2014 (51weeks after LCH was implemented).
ese antibodies were presumed to be maternal because
no samples were PCR positive at the same time points.
Virus was detected in 5-week old and 7-week old pig-
lets in the F1B2 nursery in November 2013. e virus
was isolated from the ELISA and PCR positive piglets in
F1B2, and the virus gene open reading frame 5 (ORF-5)
was sequenced (Bioscreen GmBH, Hannover, Germany),
and shown to have 99.17% sequence homology to the
PRRSV type 2 MLV strain. e nursery was depopulated
to prevent the virus spreading to the sows. e oldest
pigs (26–32kg) were exported out of the peninsula, but
the youngest pigs (14–26kg; too small to be sold) were
moved to isolation rooms in F1Q, where they were vac-
cinated and slaughtered at a later time point. Remaining
piglets that were considered to be negative were moved
to F1WF2. e empty nursery was cleaned and disin-
fected before repopulation, and no virus was subse-
quently detected on the site.
In November 2014, two samples (both from F1B2)
tested close to the ELISA assay cut-off, and in March
2015, another sample (from F1B2) tested ELISA positive.
None of these samples were simultaneously PCR posi-
tive so all were assumed to be false-positives (Additional
file2).
PCR testing of samples from 10 week old piglets in
F1B1 and F1B2 nurseries revealed that PRRSV remained
present until Week 23 (Fig.2). No virus was detected in
any 10-week old piglets from Week 28 onwards.
At study commencement, F2B1 and F2B2 were PRRSV
positive-stable, and weaning PRRSV PCR negative pig-
lets. Piglets became PCR positive in the later nursery
rooms, so the two rooms containing the oldest age groups
were depopulated. F2B1 and F2B2 received PRRSV free
SPF status in July 2014.
Elimination inwean‑to‑nish andnisher herds
F1WF1 was partially depopulated in October 2013,
after piglet vaccination (at weaning) stopped, and then
all piglets tested PCR negative until February 2014. Up
to 20% of piglets continued to test ELISA positive until
age 6–7weeks, probably due to the presence of maternal
antibodies (Additional file3).
F1WF2 received a batch of presumed PCR negative
piglets from F1B2 in November 2013, but PCR positive
Fig. 1 Locations of herds on the Horne Peninsula, and PRRSV status at study commencement. F1B1 Flow 1 Breeding Herd 1, F1B2 Flow 1 Breeding
Herd 2, F1F1 Flow 1 Finisher Herd 1, F1F2 Flow 1 Finisher Herd 2, F1Q Flow 1 Quarantine, F1WF1 Flow 1 Wean-Finish 1, F1WF2 Flow 1 Wean-Finish
2, F2B1 Flow 2 Breeding Herd 1, F2B2 Flow 2 Breeding Herd 2, F2F1 Flow 2 Finisher Herd 1, F2F2 Flow 2 Finisher Herd 2, F2F3 Flow 2 Finisher Herd 3,
PRRS porcine reproductive and respiratory syndrome
Page 7 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
Table 3 Time forherds toobtain ocial PRRS free SPF status
Herd PRRS free SPF status
achieved Notes
F1B1 January 2015 July 2013: weaned ELISA and PCR positive piglets at study commencement
September 2013: weaned PCR negative but ELISA positive piglets
July 2014: three-week old piglets remained ELISA positive until July 2014
F1B2 January 2015 July 2013: weaned ELISA and PCR positive piglets at study commencement
September 2013: weaned PCR negative but ELISA positive piglets
November 2013: sentinels were about to be introduced, but two age groups tested PCR positive
(5-week old and 7-week old piglets in nursery rooms). Sequencing revealed 99.17% homology to
PRRS type 2 MLV
The nursery was depopulated to prevent PRRS spreading to the sows:
Oldest pigs (26–32 kg) were exported out of the area
Younger pigs (14–26 kg) were moved to isolation rooms in F1Q, vaccinated, then eventually
slaughtered
Piglets considered to be PCR negative were moved to F1WF2. (these were the only extra facilities
available)
The nursery was cleaned and disinfected before repopulation
November 2014: two samples were close to the ELISA assay cut-off (SP > 0.4)
March 2015: one sample was ELISA positive, but simultaneously PCR negative. This was assumed to
be false positive
F1WF1 Finishers depopulated in
February 2015 October 2013: partially depopulated
October 2013–February 2014: ≤20% of samples tested from piglets were ELISA positive until age
6–7 weeks. All samples were PCR negative 100% of pigs older than 7 weeks were ELISA and PCR
negative
February 2014: samples from 17-week old piglets were ELISA positive, but PCR negative
March 2014: 16- and 18-week pigs were found to be PCR and ELISA positive
April 2014: finisher rooms partially depopulated again. The site then remained PCR and ELISA nega-
tive until October 2014
October 2014: samples from 17- to 18-week old piglets were ELISA and PCR positive (possibly from
F1WF2)
December 2014: samples from 11-week old piglets were ELISA negative, PCR positive. Samples from
13- to 15-week old piglets were both ELISA and PCR positive
January 2015: Total depopulation
F1WF2 January 2015 November 2013: received a batch of PCR positive pigs from F1B2 (although these were considered
PRRS negative when moved). Lack of compliance with Golden Rule 8 meant the finisher rooms
were continuously PCR positive until October 2014
October 2014: finisher barn depopulated, but infection probably spread to nearby F1WF1. Gradual
repopulation from nursery. Herd then remained PCR and ELISA negative for the remainder of the
study
F1F1 April 2015 October 2013: received depopulated (30 kg) pigs from F1WF1. Samples tested ELISA and PCR posi-
tive until March 2015, until the whole herd was depopulated
March 2015: repopulated
F1F2 January 2014 November 2013: received PRRS type 2 MLV vaccinated pigs from F1WF1 until October 2013. Partial
depopulation. Received pigs from F1WF1 since November 2013 on an AIAO basis.
F1Q January 2015 July 2013. Mass vaccination of all gilts and sows (two times, 4 weeks apart, according to same
schedule as in F1B1 and F1B2). Gilts remained in quarantine for 12 weeks. These gilts had been
transferred to breeding herds by December 2013
November 2013: received pigs 14–26 kg from F1B2. These pigs were placed in an isolated room,
vaccinated with PRRS type 2 MLV, then later slaughtered to prevent PRRSV from spreading to the
rest of the site
January 2014: PRRS negative gilts bred elsewhere were introduced to gilt quarantine
April 2014: acclimatised (external) gilts were moved to breeding herds
F2B1 July 2014 July 2013: weaned PCR negative piglets at study commencement
F2B2 July 2014 July 2013: weaned PCR negative piglets at study commencement. Nursery rooms containing oldest
two age groups were depopulated
F2F1 August 2015 (but no PRRS
positive pigs since Octo-
ber 2013)
July 2013: received PCR positive piglets from F2B2 at study commencement. From Weeks 0–10, all
finisher pigs were vaccinated after introduction. Partially depopulated, and then only received
PRRS negative animals
October 2013: samples tested PCR negative, and remained negative for the remainder of the study
F2F2 November 2013 July 2013: received PCR positive piglets from F2B2 at study commencement From Weeks 0–10, all
finisher pigs were vaccinated after introduction. Partially depopulated, then received only PRRS
negative animals
November 2013: samples tested PCR negative, and remained negative for the remainder of the
study
Page 8 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
piglets were detected shortly afterwards. Despite regu-
lar auditing of procedures by the veterinarian, staff were
not able to comply with Golden Rule 8 (avoid contact
between age groups; Table2). is resulted in finisher
rooms remaining continuously PCR positive until they
were depopulated in October 2014.
F1F2 remained PCR positive until November 2013;
5 months after study commencement, and received
PRRSV free SPF status in April 2014. F2F1 tested PCR
negative in October 2013, and F2F2 and F2F3 tested PCR
negative one month later, and remained both PCR and
ELISA negative for the remainder of the study. PRRSV
free SPF status was declared in October 2013 for F2F1,
and in November 2013 for F2F2 and F2F3.
Re‑infection inF1WF1 andF1F1
In October 2014, just before PRRSV free SPF status was
to be declared for F1WF1, and at the same time that the
finisher rooms of F1WF2 were depopulated due to rein-
fection, 20 and 100% of samples from 17- to 18-week
old piglets, respectively, tested positive by ELISA, and
pooled samples from both age groups were PCR positive
(Additional file3). ree months later, PRRSV had spread
to nearby F1F1, which had also been close to PRRSV
elimination. e re-infection prompted full depopula-
tion of both sites, and no new pigs were introduced until
March 2015. No further samples tested either ELISA or
PCR positive after repopulation. F1F1 was the last on
the peninsula to achieve PRRSV free SPF status, in April
2015.
Discussion
e objective of the area elimination case study reported
here was to eliminate PRRSV from all herds on the Horne
Peninsula, Denmark, using a combination of LCH using
PRRSV type 2 MLV, optimised pig flow, and implementa-
tion of the 10GR for biosecurity management. is study
shows that these techniques, in combination, successfully
eliminated PRRSV from all herds on the Horne Penin-
sula, Denmark, according to Danish SPF-SUS regulations
[26]. Eighteen months later (November 2016), all herds
still retain PRRSV free SPF status. To the authors’ knowl-
edge, this is the first successful European PRRSV area
elimination project documented in detail.
roughout the study, overall PRRS status of herds was
classified according to the AASV terminology, and then
PRRS was deemed eliminated from a herd when PRRS
free SPF status was declared, according to the regula-
tions from SPF–SUS, Denmark [26]. e use of AASV
terminology throughout the study enabled herd status
to be monitored month by month, thus allowing rapid
response to re-infection. PRRS free SPF status was sought
to fetch the maximum price when the pigs were sold.
At study commencement, all herds in both flows tested
PCR positive for PRRSV infection according to AASV
terminology [27], and all except F2B1 and F2B2 were pos-
itive-unstable. F2B1 and F2B2 were positive-stable. ese
initial observations indicated that infection control and pig
flow management techniques were sub-optimal, permit-
ting PRRSV transmission among herds and age groups.
Study commenced in July 2013. Positive-unstable dened as ELISA positive for PRRS antibody, and PCR positive for PRRSV RNA (actively shedding); positive -stable
dened as ELISA positive for PRRS antibody in serum but PCR negative (not shedding)
F1B1 Flow 1 Breeding Herd 1, F1B2 Flow 1 Breeding Herd 2, F1F1 Flow 1 Finisher Herd 1, F1F2 Flow 1 Finisher Herd 2, F1Q Flow 1 Quarantine, F1WF1 Flow 1 Wean-
Finish 1, F1WF2 Flow 1 Wean-Finish 2, F2B1 Flow 2 Breeding Herd 1, F2B2 Flow 2 Breeding Herd 2, F2F1 Flow 2 Finisher Herd 1, F2F2 Flow 2 Finisher Herd 2, F2F3 Flow 2
Finisher Herd 3, PRRS porcine reproductive and respiratory syndrome
Table 3 continued
Herd PRRS free SPF status
achieved Notes
F2F3 November 2013 July 2013: received PCR positive piglets from F2B2 at study commencement. From Weeks 0–10, all
finisher pigs were vaccinated after introduction. Partially depopulated, then received only PRRS
negative animals
November 2013: samples tested PCR negative, and remained negative for the remainder of the
study
Fig. 2 PRRSV ELISA and PCR monitoring of 10-week old piglets
in F1B1 and F1B2. A minimum of 5 samples were taken at each
sampling point. ELISA was performed on individual samples; PCR was
performed on a pooled sample at each time point. ELISA enzyme-
linked immunosorbent assay, PCR polymerase chain reaction
Page 9 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
To begin eliminating PRRSV, LCH was initiated in
F1B1 and F1B2. Herd closure avoided introducing
PRRSV from external sites, and decreased the number of
susceptible animals in the herds: both limiting viral trans-
mission [17]. Simultaneous vaccination of all animals at
both Week 0 and Week 4 increased herd immunity and
may have promoted viral elimination by reducing the
number of naïve animals. e vaccine used in this study
is derived from a type 2 (North American) PRRSV strain,
and its efficacy has been clearly demonstrated against
both homologous and heterologous strains [28, 29].
e LCH model is a useful tool for PRRSV area elimi-
nation programs, and has repeatedly allowed control in
individual farms [17, 22]. One of the limitations of LCH
is the need for stringent biosecurity measures to pre-
vent virus transmission. In this study, staff reviewed
internal and external biosecurity procedures and imple-
mented the 10GR, devised in 2005 by Boehringer Ingel-
heim, based on 10years of field experience in controlling
PRRSV spread. e 10GR are based on the principles of
the McREBEL system for disease management [23], and
were developed to simplify the McREBEL procedures
and increase the likelihood of implementation. e 10GR
are reported here for the first time.
e 10GR involved restricting the movement of pigs to
prevent PRRSV transmission between age groups, and
quarantining gilts before introducing them to breeding
herds to avoid infecting them with PRRSV. F1WF1 was
considered the most difficult farm from which to elimi-
nate PRRSV because of its complex pig flow, which made
implementing the 10GR difficult. Despite this difficulty,
the 10GR were stringently followed in all herds, in both
flows, at all times (except in F1WF2, which was unable to
comply with rule 8), and this was ensured through regu-
lar auditing of all farms. is foundation of good man-
agement practice contributed to the success of PRRSV
MLV vaccination and the LCH control model in eliminat-
ing PRRSV from the study area.
A study on transmission of PRRSV between herds in
Ontario concluded that sharing herd ownership and
transportation were among the most important factors
for the spread of PRRSV between herds [30]. Indeed,
sharing of personnel and transportation between F1B1,
F1B2 and F1Q (under the same ownership) may have
contributed to the endemicity of PRRSV in the Horne
Peninsula before this study began. Although shared own-
ership may cause problems, it can also facilitate com-
munication between producers, which is critical to the
success of regional PRRSV control and elimination pro-
jects [31]. e naturally limited geographical area, the
close relationship between the herd owners, and supervi-
sion of all herds by the same veterinarian probably con-
tributed to the successful outcome of this study.
Using a combination of LCH, use of PRRSV type 2
MLV and the 10GR, PRRSV was successfully eliminated
from F1B1 and F1B2 by January 2015. PCR positive pigs
were detected in the nursery of F1B2 in November 2013,
and most animals were exported away from the Horne
Peninsula, or to quarantine in F1Q, but some presumed
PRRSV negative pigs were moved to F1WF2. Unfortu-
nately, these animals re-introduced PRRSV into F1WF2,
and so having an emergency plan to remove infected pigs
from the elimination area as soon as they are detected
is a key learning from this study. We also suggest that
extending the vaccination period of piglets at weaning
to span a whole sow cycle (20weeks) may have avoided
the emergence of PRRSV positive pigs in F1B2. Genetic
sequencing revealed that the virus strain had over 99%
ORF-5 sequence homology to the PRRSV type 2MLV
strain. Although re-infection was disappointing, we were
encouraged that field virus was not detected.
F1WF1 tested PRRSV ELISA and PCR negative in four
sampling points over 6months, but became re–infected
in October 2014, at the same time that F1WF2 finisher
rooms were depopulated following reinfection. F1WF1
and F1WF2 did not share personnel, transportation or
equipment, so the infection in in F1WF1 may have been
due to airborne transmission of PRRSV from F1WF2, less
than 500m away. Airborne transmission was previously
shown under Danish field conditions [32], but no further
investigations to confirm this were undertaken in the
current study.
Depopulation of the oldest pigs in the nurseries of F2B1
and F2B2 helped to immediately disrupt transmission of
PRRSV from nursery to finisher areas, as has been pre-
viously shown [33]. Despite depopulation, nurseries in
breeding herds remained ELISA positive until September
2013, because piglets born to infected sows had maternal
antibodies in serum. is was also the case in nurseries in
F1B1 and F1B2, which also remained ELISA positive for
several months after becoming PCR negative. A combi-
nation of depopulation and strict application of the 10GR
led to the rapid elimination of PRRSV (ELISA and PCR
negative) in F2B1 and F2B2 in just 2months after study
commencement, and declaration of PRRSV free SPF sta-
tus 6 months later. Depopulation of the oldest pigs in
nursery rooms of breeding herds enabled rapid PRRSV
elimination from finisher herds too, by ensuring that no
PRRSV positive piglets were introduced to finisher herds.
e authors note some limitations to the current study.
To show that PRRSV area elimination is possible using
the methods described, the Horne Peninsula was delib-
erately chosen as a limited geographical area, with few
herd owners and simple transportation routes between
herds. e breeding herds in this study were compara-
ble in size and production to the Danish average in 2015
Page 10 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
(742 sows and 22,077 piglets), while the finisher sites pro-
duced about half as many pigs as the Danish average for
finisher sites (8008 pigs slaughtered in 2015) [34]. How-
ever, the authors acknowledge that elimination would be
far more complex in less well defined areas. e current
project was driven by a small number of stakeholders
who dedicated time to planning and sampling. Extend-
ing this project to larger regions with more owners and
increased animal transport would require substantially
more planning. For example, empty barns would have to
be identified so that PRRSV positive pigs could be moved
from sites close to achieving PRRSV elimination, to pre-
vent setbacks.
Furthermore, larger projects with more owners may
encounter problems with commitment and communi-
cation. In this project, six veterinarians were involved
with overseeing the study, and ensuring implementa-
tion of the 10GR. All but one of these veterinarians were
from the same practice (Porcus Pig Practice), making the
sharing of information and decisions simple. In larger
projects, more stakeholders from different practices
(and perhaps with competing interests) may make com-
munication more difficult. Employment of a full-time
project coordinator would be recommended, as would
involvement of pig producers and representatives from
SEGES Danish Pig Research Centre, slaughterhouses
and SPF-Denmark.
PRRS is one of the most economically devastating
swine diseases, causing substantial animal losses and
medication expenses [35, 36]. In Denmark, the costs of
PRRS are estimated to be between €4 and €139 per sow,
per year [20]. e LCH method is an effective PRRSV
elimination strategy when combined with stringent bios-
ecurity measures: this was further confirmed in the pre-
sent study. A detailed cost-benefit analysis is needed to
understand the return on investment for this area PRRSV
elimination method.
Conclusions
PRRSV was eliminated from all herds on the Horne Pen-
insula, Denmark, in just over 18 months, after employ-
ing a combination of LCH, vaccination using PRRSV
type 2 MLV and the 10GR for biosecurity management.
Eighteen months later (November 2016), all herds still
have PRRSV free SPF status. Elimination may have been
achieved more quickly if the PRRSV positive pigs that
were depopulated from F1B2 had been moved out of
the area: this would have reduced the risk of area spread.
Finally, the 10GR helped improve biosecurity manage-
ment in all farms on the peninsula, and may offer a sim-
plified alternative to the McREBEL system for controlling
PRRSV.
Abbreviations
10GR: 10 Golden Rules; AIAO: all in, all out; ELISA: enzyme-linked immunosorb-
ent assay; LCH: load, close, homogenise; McREBEL: Management Changes to
Reduce Exposure to Bacteria to Eliminate Losses; MLV: modified–live vaccine;
ORF: open reading frame; PCR: polymerase chain reaction; PRRS: porcine
reproductive and respiratory syndrome; PRRSV: porcine reproductive and
respiratory syndrome virus; SPF: specific pathogen free.
Authors’ contributions
JD was the driver and initiator of this area elimination project. He brought
pig producers in the area together and facilitated the decision-making pro-
cess. He was the daily contact, undertook practical training of staff, and per-
formed diagnostic sampling together with his colleagues from Porcus Pig
Practice. JD was directly responsible for the breeding herds in Flow 1. PHR
designed the elimination programme outline, the 10GR, and the diagnostic
programme. He collected, processed and presented diagnostic information
and drafted the manuscript. Both authors have read and approved the final
manuscript.
Authors’ information
JD is a veterinarian: a specialist in pig health and production, and co-owner of
Porcus Pig Practice. PHR is a Veterinarian, Global Technical Manager, PRRS at
Boehringer Ingelheim Vetmedica GmbH.
Author details
1 Boehringer Ingelheim Vetmedica GmbH, Binger Straße 173, 55216 Ingel-
heim, Germany. 2 PORCUS svinefagdyrlaeger og agronomer, Oerbaekvej 276,
5220 Odense, Denmark.
Acknowledgements
The authors would like to thank the veterinarians in Porcus Pig Practice for
providing assistance with diagnostic sampling, and Lars Rasmussen and Jes-
per Bisgaard Sanden; responsible for WF herds and Flow 2 herds, respectively.
Editorial assistance with this manuscript was provided by InterComm
International, Cambridge, UK and this service was funded by Boehringer
Ingelheim Vetmedica GmbH.
Competing interests
PHR is currently an employee of Boehringer Ingelheim Vetmedica GmbH (Vet-
erinarian, Global Technical Manager PRRS). In connection with presentations
following this study at two meetings for veterinarians and farmers in Denmark,
and for symposia in Romania and the UK, JD received fees for consultancy,
travel and accommodation from Boehringer Ingelheim Vetmedica Denmark.
Consent for publication
Consent for informing public about the results and procedures employed in
this Horne Land PRRS Eradication program has been given by the owners of
the farms that participated.
Additional les
Additional le1. PCR and ELISA results from breeding herds 8 weeks
before study commencement. Additional data showing individual PCR
and ELISA results from piglets of different age groups in the breeding
herds, 8 weeks before study commencement.
Additional le2. Individual value plot of PRRS ELISA status of pre-wean
piglets (3 weeks of age) in LCH breeding herds. Additional data showing
ELISA S:P values on all sampling points for up to 90 weeks after implemen-
tation of LCH, measured in 3-week old piglets.
Additional le3. PCR and ELISA results from F1WF1 (receiving piglets
from LCH breeding herds) until 60 weeks after LCH commencement. Addi-
tional data showing individual PCR and ELISA results from piglets of differ-
ent age groups on the WF1 site, throughout the entire study duration.
Page 11 of 12
Rathkjen and Dall Acta Vet Scand (2017) 59:4
Funding
All diagnostic testing of samples from the study farms was funded by
Boehringer Ingelheim Denmark. Diagnostic samples were collected by
veterinarians from Porcus Pig Practice under normal commercial conditions.
Boehringer Ingelheim Animal Health GmbH funded the publication fee for
this manuscript.
Received: 4 August 2016 Accepted: 20 December 2016
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