Bovine viral diarrhea virus (BVD virus or BVDV), a serious problem in cattle, has

now been proven to also cause illness, abortions, and most important of all, the

persistently infected (PI) state in alpacas. The virus’s ability to produce persistently

infected cria, the main way this disease would be spread, and its ability to cause

abortions are extremely important for the alpaca industry.

At this point, the vast majority of knowledge about BVDV and the disease that it

causes, bovine viral diarrhea (BVD), is about its effects in cattle, where it is considered

one of the most significant viral infections, causing major economic losses. The

information presented next is a brief synopsis of BVDV in cattle.

Despite the name, many animals with BVD do not have diarrhea. Other

manifestations of the virus include sub clinical infections, immunosupression, abortions,

congenital defects, persistent infection, and mucosal disease. The majority of cows

infected are either sub clinically ill (do not appear unwell) or only mildly unwell with low

fever and diarrhea. Because BVDV depresses the immune system, some animals will

become ill with other infections, usually pneumonia; others will have a classic case of

BVD with fever, discharge from the nose and eyes, erosions of the muzzle and in the

mouth, and severe diarrhea; others may have severe hemorrhagic (bloody) diarrhea and

die. Severity of illness is influenced by the age of the animal and its immunological and

physiological status, and the particular strain of the virus involved.

The most important aspect of BVDV is its effect on the developing fetus. BVDV

can cause abortions at any stage of gestation – from early embryo loss up to stillbirths at

term. Even a sub clinically infected cow can abort, and abortions may occur up to

several months after exposure to the virus. A unique feature is that if the cow is exposed

to the virus at a critical phase of her gestation (approximately 40 - 120 days) and does not

abort, she will produce a persistently infected (PI) calf. Because the developing fetus is

not immune competent at that stage of development it becomes immunotolerant to the

virus (does not recognize the virus as foreign); it is unable to make an immune response

to rid itself of the virus, and once born, is a permanent carrier and sheds huge

concentrations of the virus in every secretion – tears, nasal discharge, saliva, urine, and

feces. PI calves are the major source of the spread of BVD – they shed several billion

viral particles a day – about a thousand times more than what is shed by an acutely

infected non-PI animal. The only way to be PI is to be born PI. Some PI calves appear

completely normal, but most are poor-doers – poor weight gain, weak, and susceptible to

other diseases such as pneumonia; many PI calves die before they are a year old.

Infection of the pregnant cow with BVD later in pregnancy can result in calves that are not

PI but that have congenital defects such as cerebellar hyperplasia (underdevelopment of

the part of the brain that controls balance and co-ordination), cataracts, blindness,

hypotrichosis (sparse hair growth) or general growth retardation.

Acute infection with BVDV occurs through the nose or mouth by contact with

secretions from an infected animal (usually a PI animal) – saliva, nasal discharge, tears,

urine or feces – either directly from the infected animal itself or from items that have been

contaminated with those secretions, such as water troughs. BVDV is very infectious. An

acutely infected but non-PI animal sheds virus for a relatively short length of time (4 – 10

days, possibly up to 2 weeks) in comparison with a PI animal which sheds virus for its

entire life. Incubation period is 5 to 7 days. The virus cannot survive long in the

environment – a maximum of 2 weeks. Because it is a virus, antibiotics are of no use in

treating it.

There are hundreds of different strains of the virus, which can also be categorized

under type 1 (BVDV1) or type 2 (BVDV2) and by the terms cytopathic or non-cytopathic.

PI animals always have a non-cytopathic strain of BVDV. An entity called mucosal

disease occurs only in PI animals – they become superinfected with an antigenically

similar cytopathic strain of the virus (usually from a mutation in their own non-cytopathic

strain, or from a modified live vaccine); this leads to severe diarrhea and inevitably death.

Vaccines for cattle are available for BVD; however they do not confer 100% immunity.

There is not much published information concerning BVDV and camelids. Articles

published to date on BVDV and camelids have generally concluded that BVDV is not

much of a concern. In an article titled ‘A Medical Marvel’ in the winter 1999 edition of

Alpacas Magazine Randy Larson DVM stated what was likely the commonly held

viewpoint at that time: “BVD is an example of a significant disease of cattle that causes

undetectable problems in alpacas. BVD and other common cattle viruses just do not

469) makes mention of BVDV only as a cause of congenital defects and impaired

immunologic competence in calves and lambs.

In 1994, Mattson reported on a study of 270 llamas from 21 herds in Oregon; 4.4%

of them had antibodies to BVDV. Seven of the twelve llamas that had antibodies were

from one farm where cattle were in contact with the llamas.

In 2000, Belknap et al. from Colorado State University reported on three cases of

BVDV isolated from llamas (a stillborn fetus and two sudden deaths in adults that had

been losing condition) and concluded that BVDV should be considered as a cause of

of that statement (page 451) and also that it may be one of the causes of diarrhea in cria

(page 400).

In 2002, Goyal et al. in Minnesota reported on what appeared to be the first case of

BVDV isolated from a stillborn alpaca; there were no gross or histopathologic changes of

(appeared unwell) or from immunization. For example, most of us would have antibodies

to chickenpox from having that illness as children.) The alpacas that were unwell had

symptoms that ranged from having the appearance for a few days that their mouths were

uncomfortable eating their pelletized supplement, to being off feed and depressed, to one

death from hepatic lipidosis (that condition would have resulted from decreased feed

intake). None of them had diarrhea. Many of them, even those sub clinically infected,

showed stress breaks in their fleece.

The cria who was presumed in hindsight to be PI and the source of the infection

(he died without being tested) arrived at Farm A at the age of 3 months. He had been

born at full term on Farm B, also in Ontario, at a very low birth weight of 9 pounds. He

had done fairly well for the first 6 weeks of life and then developed repeated infections,

mostly pneumonia, had a frequent runny nose, and he had very poor weight gain. He

died at the age of 8 months after severe diarrhea. (This was his first episode of diarrhea

since having a bout with coccidia when he was much younger). Farm B, where he spent

the first three months of his life, had positive BVDV antibody levels in alpacas that had

been in contact with him. His mother had been on Farms C and D, in Alberta, in her early

pregnancy (when she would have contracted her sub clinical BVD infection resulting in

her producing this PI cria); Farm C had many abortions and Farm D had two stillbirths

and a cria that died at 36 hours of age in the same year that this female delivered her

presumed PI cria. Farms C and D have alpacas with positive BVDV antibody levels,

including the dams of the aborted fetuses, stillbirths and cria that died. Although it is

possible that the mother (who is not PI) became acutely infected at Farm D and

transmitted BVD to Farm C during the short time she would have been shedding virus, it

is more likely there were separate cases of PI animals on both those farms causing the

infections. None of the farms involved had any contact with cattle.

The proven PI cria, called Gabriel, born on Farm A (to a female who had been

infected by the above presumed PI cria) also had a very low birth weight of 12 pounds for

the farm he was born on. He had excellent weight gain to 33 pounds at the time of his

euthanization at a little over 6 weeks of age, after two sets of blood tests confirming he

was PI. (The fate of all proven PI animals is to be euthanized.) He had chronic diarrhea,

but was not unwell with it and was perky and active.

At this point it is unknown just how prevalent BVD is in alpacas. Alvarez et al.

reported in 2002 that 11.5% of alpacas in a rural community of Cusco in Peru had

antibodies to BVDV. The other reported case of BVDV in a stillborn alpaca fetus was in

Minnesota, and the llama cases were in Colorado, so this is not just a Canadian situation.

The practice of sending females with cria at side off to other farms for breeding is one of

the main ways BVD would spread – a PI cria may not show any signs of being unwell until

it is older and yet be infecting every animal it comes in contact with. Also, a pregnant

female going to a new owner may be carrying a PI fetus that, once born, will infect all the

alpacas at the new home. This case shows how BVDV traveled approximately 3500

kilometers (over 2000 miles) from Alberta to Ontario. Some PI cattle continue to appear

healthy; it is unknown how many PI alpacas may continue to appear normal. It is also

unknown what is the exact range of gestation in alpacas that infection of the dam will

result in the birth of a PI cria. Cattle have a 9 month gestation and it is in the period of

approximately 40 –120 days of gestation that there is the high risk of the fetus becoming

PI if the mother is infected with BVD.

Alpacas have a reputation for being easy aborters, and it is not unusual to hear of

poor doing cria – it is entirely possible that some of these cases may have been due to

BVDV. Unless the virus is specifically tested for there is no way of knowing that it is

present – in both the stillborn fetus from Minnesota and the aborted fetus from Ontario

there were no pathological changes to suggest BVD – it was only by testing for the

presence of the virus itself that it was found. In the euthanized PI cria there were no

pathological changes to suggest he was PI – but virus isolation from blood and most

tissues was positive. The adult alpaca that died after what must have been an acute BVD

infection had autopsy findings of hepatic lipidosis, but it would have been BVD that

caused her appetite to decline, resulting in the hepatic lipidosis. In her case, there would

not have been virus detected as it would be too long after the initial acute infection – she

would have to have had antibody testing. It is possible that some of the unexplained

cases of hepatic lipidosis in alpaca herds have been caused by BVD. Schwantje and

Stephen’s paper on ‘Communicable Disease Risks to Wildlife from Camelids in British

Columbia’ reported a positive BVDV antibody rate of 6% in a sample of 175 llamas from

twelve farms, with the rate per farm varying from 0% for many farms to a high of 22% on

one farm. This paper also reported on a survey of 90 llama and alpaca farms asking

about illness and death in the preceding year; the primary cause of death (26% of cases)

was neonatal failure to thrive or stillbirths. The report also reviewed the diagnoses of

llama and alpaca submissions to the B.C. Animal Health Centre between 1993 and 2000:

9% of the diagnoses were idiopathic (meaning no cause found) abortion. It is quite

possible there is a connection between BVDV and some of those cases of neonatal

failure to thrive, stillbirths and abortions. Until aborted and stillborn fetuses and autopsied

animals are tested specifically for the presence of BVD virus or antibodies, depending on

the clinical situation, we will not know how prevalent this is. Only a completely closed

herd (no animals coming into the herd) with good biosecurity measures (all visitors with

footwear not contaminated by manure; no fence line contact with other livestock) can be

sure to be safe from BVDV.

Testing for BVDV is complicated, with different tests being used in different

situations. Having antibodies (blood test) to BVDV shows that the animal was exposed

to the virus (from a clinical or sub clinical infection, or from immunization), but it is

unknown how long antibodies are detectable for after exposure. PI animals would not

have antibodies (unless they were tested as newborns soon after ingesting their mother’s

antibody-containing colostrum). To detect the PI state the animal has to be tested for the

virus itself, and there must be two positive tests three weeks apart to prove the PI state, in

case the first positive test was an acute infection and not from being PI. Virus isolation is

the ‘gold standard’ test for detecting BVDV – it can be done on blood (live animal) or

tissue (dead animal). The ELISA blood test for the virus is used to detect PI animals over

the age of 3 months (the maternal antibodies from colostrum interfere with the test before

that age, and also sometimes interfere with virus isolation.) The ELISA test on skin

biopsies or ear notches can be used to detect PI calves under the age of three months.

The PCR test (blood) is not affected by maternal antibody and is also used to detect PI

animals under the age of three months. Immunohistochemistry is used on formalin fixed

tissue from autopsies; however as noted above this test was negative in the stillborn fetus

in Minnesota despite BVDV being detected by PCR and virus isolation;

immunohistochemistry was positive in the aborted fetus in Ontario. Your veterinarian

should consult with a veterinarian virologist or with the lab that he/she uses for BVDV

diagnosis in cattle. Most labs doing BVDV testing are affiliated with universities, or are

state or provincially funded; not many private labs offer BVDV testing.

For the veterinarians reading this article: the aborted alpaca fetus from Farm A was

positive for BVDV type 1 on virus isolation from skin and positive for BVDV in multiple

tissues using immunohistochemistry on formalin-fixed tissue. Gabriel, the PI cria, was

found to be positive for BVDV type 1 at birth (using virus isolation on placenta), at 3 days

of age (using virus isolation from buffy coat cells and PCR on both EDTA blood and

plasma), at 25 days of age (using virus isolation on both EDTA blood, plasma and PCR

on both EDTA blood, plasma) and at 6 weeks of age (using virus isolation on buffy coat

cells, plasma, serum and multiple tissues, including skin and brain, PCR on both plasma

and serum). At 6 weeks of age Gabriel was also IDEXX BVDV ELISA positive using fresh

ear notch and positive for BVDV in immunohistochemistry tests using multiple tissues,

including skin and brain. He continued to be antibody negative for both BVDV type 1 and

type 2 until euthanasia.

At this time, a reasonable recommendation is that all aborted or stillborn fetuses,

all unusually low birth weight and ‘poor doing’ cria and all unexplained deaths be tested

for BVD virus and/or antibodies, depending on the case. If BVDV is found then further

testing should be done to determine how the virus entered the herd - specifically is there

still a PI animal present, or has it gone back to another farm. Any cria subsequently born

to females who were pregnant when BVD was active in the herd should be tested to see if

they are PI. It is important that you bring this information to the attention of your

veterinarian as it will be at least a year before it is published in a veterinary journal. It

would also be very helpful if you or your vet notified the lab in your area where aborted

fetuses or autopsies are sent for testing about this, so that testing specifically for BVDV

will become routine in abortions, stillbirths, and unexplained deaths in alpacas.

The complete story of how this discovery was made has been written up and called

www.silvercloudalpacas.com

Addendum: Just before going to press, we have received a report from an alpaca

breeder who recently had three abortions and one cria death. After being made aware of

the findings in this article, he had blood tests done for BVDV antibodies. All the eighteen

alpacas over the age of one year on his farm have tested positive for BVDV antibodies.

His alpacas have not had contact with any alpacas from any of the farms mentioned in

this article.

Further Addendum: After this article was submitted for publication we have

received further reports of BVD virus being isolated from dead alpacas and aborted

fetuses – these were from owners or vets who had been made aware of the findings in

this article and from labs that had been notified to start testing for the virus.

Alvarez S., Rivera G.H., Pezo D., Garcia W. (2002). “Deteccion de anticuerpos contra

pestivirus en rumiantes de una comunidad campesina de la provincia de Canchis,

Belknap E.B., Collins J.K., Larsen R.S., Conrad K.P. (2000). “Bovine viral diarrhea virus

State University Press.

Goyal S.M., Bouljihad M., Haugerud S., Ridpath J.F. (2002). “Isolation of bovine viral

Press.

Schwantje H., Stephen C. (2003) “Communicable Disease Risks to Wildlife From

Camelids in British Columbia.” [on-line]. Available:

http://wlapwww.gov.bc.ca/wld/documents/wldhealth/camelid_risk03.pdf

Wentz P.A., Belknap E.B., Brock K.V., Collins J.K., Pugh D.G. (2003). “Evaluation of

Nancy Carr MD has alpaca farm A, Silver Cloud Alpacas, near Elginburg in eastern

Ontario, Canada. She would like to assure readers that her herd is now completely

healthy and not contagious, and in fact is one of the very few herds in North America

where all the cria have been tested to make sure they are not PI. She can be reached at

www.silvercloudalpacas.com

Susy Carman DVM PhD is in Diagnostic Virology, Animal Health Laboratory, Laboratory

Services Division, University of Guelph, Box 3612, Guelph, Ontario, Canada N1H 6R8.

NEED TO KNOW

abortions, and, most important of all, the persistently infected state in alpacas.

persistently infected (PI) cria who sheds huge amounts of virus its whole life and is

the major source of the spread of BVD.

the potential for BVD to spread between herds is significant because of the

practice of females with cria at side going to other farms for breeding.

profound impact on the alpaca industry.

should be tested specifically for BVDV, as there are usually no pathological

changes to suggest BVDV. Your veterinarian should consult with a veterinarian

virologist or lab that does BVDV testing about the appropriate tests to be ordered.