a survey of virus infections of the respiratory tract of

J. Hyg., Camb. (1980), 85, 257 2 5 7

Printed in Oreat Britain

A survey of virus infections of the respiratory tract ofcattle and their association with disease

BY E. J. STOTT, L. H. THOMAS, A. P. COLLINS, S. CROUCH,J. JEBBETT, G. S. SMITH, P. D. LUTHER AND R. CASWELL*

Agricultural Research Council, Institute for Research on AnimalDiseases, Compton, Newbury, Berkshire, RGIG ONN, and

*Milk Marketing Board, Warren Farm, Lambourn, Berkshire

{Received 1 February 1980)

SUMMARY

A total of 1590 calves wore investigated between May 1972 and December 1975.Twenty-two per cent were treated for respiratory disease and 2*5 % died of pneu-monia. Almost 80 % of the respiratory illness occurred in six sharp outbreaks.Samples for virology were collected routinely from 127 healthy calves and from354 calves treated for respiratory signs and comprised 1143 nasopharyngeal swabsand 1009 sera. Virus infections were detected on 540 occasions including 135 byparainfluenzavirus typo 3 (Pi-3), 78 by respiratory synoytial virus (RSV), 103 byrhinovirus, 49 by bovine virus diarrhoea virus (BVDV), 29 by adenoviruscs, 53 byreoviruses and 88 by enteroviruses. The seasonal and ago distribution of infectionsdiffered between viruses. Only infections by RSV, Pi-3 and BVDV were signifi-cantly associated with disease.

INTRODUCTION

Acute respiratory disease is thought to bo a major cause of economic loss in thebeef industry. Howover, its precise incidence, its exact cost and its causes allremain uncertain.

Two approaches have been used extensively in attempts to show that virusescause respiratory disease in calves: first, animals were investigated during out-breaks of illness for evidence of virus infection and, secondly, viruses isolated fromthe bovine respiratory tract were inoculated experimentally into susceptibleanimals (see reviews by Darbyshire & Roberts, 19G8; Phillip & Darbyshire, 1971;Mohanty, 1978). Much valuable information was obtained about the range ofdifferent viruses which infect the bovine respiratory tract and about their patho-genic potential. Howover, although investigations of cattle with respiratory diseaserevealed widespread infection by parainfluenza virus, typo 3 (Pi-3), rhinoviruses(RV), bovine virus diarrhoea virus (BVDV), adenoviruscs (AD), rcoviruses (REO),enteroviruses (ENT) and, more recently, respiratory syncytial virus (RSV), fewworkers studied the same animals when healthy. Without a clear understanding ofthe ecology of these viruses and their distribution in normal, healthy cattle, it wasdifficult to assess their aetiological significance when found in animals with disease.

0022-1724/80/0017-1980 $01.00 © 1080 Cambridge University Press

https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0022172400063294Downloaded from https://www.cambridge.org/core. IP address: 65.21.228.167, on 21 Apr 2022 at 00:18:16, subject to the Cambridge Core terms of use, available at

https://www.cambridge.org/core/terms

https://doi.org/10.1017/S0022172400063294

https://www.cambridge.org/core

258 E. J. STOTT AND OTHERS

Interpretation was further confounded by the finding that several different virusesoften circulated simultaneously during an outbreak of disease (Rosenquist el al.1970; Rosenquist & Dobson, 1974). Furthermore although large amounts of virusinoculated intratracheally induced pneumonia in some experimental animals, inmany others there was little or no disease and the pathogenicity of such virusesdisseminated under natural conditions remained uncertain. Thus, the naturalhistory of these viruses is poorly understood.

This paper, which expands and intensifies our earlier work (Thomas & Collins,1974), describes an epidemiological investigation over three years in which virusinfections were followed in groups of animals during periods of health and disease.

MATERIALS AND METHODS

Population studied

The survey took place on a largo beef-rearing farm in the South of England.Calves were collected together within the first 10 days of life from farms within aradius of 200 miles in both England and Wales and reared in groups of approxi-mately 100 animals until slaughter about 18 months later. Records of treatmentwere kept for each animal and post-mortem examinations were carried out on allanimals that died. Seventeen groups born between May 1972 and Juno 1975 wereinvestigated.

Virological samples

The virological survey covered the period October 1972 to September 1975.Seven or eight animals for routino virological study wore selected at random fromeach group. Nasopharyngeal swabs (NS) collected as described by Thomas & Stott(1975) and blood were taken from these calves every 3 or 4 weeks. Where possible,calves were sampled from arrival at the farm until they were 9 months old. Whenpossible NS and paired serum samples were also collected from animals whichwere treated for respiratory disease.

Virus isolation

Two tubes of secondary calf kidney (CK) cells and two tubes of primary orsecondary calf testis (CTe) cells were each inoculated with 0*2 ml of NS extract.The CK cells were maintained in Eagles' basal medium (Flow Laboratories)containing 2% heat-inactivated fetal calf serum, 5% tryptoso phosphate broth,0*1% sodium bicarbonate, 100/jg/ml ampicillin, 100//g/ml kanamycin and 50units/ml fungizone; the pH was adjusted to 7*2 with 25 mmol HEPES buffer andthe tubes were rolled at 33°C. Medium for CTo cells (Caul, Jacobs & Clarke, 1974)was adjusted to pH 7*8 with 25 mmol HEPES buffer. The tubes were held station-ery at 37 °C. The medium of all cultures was changed 24 h after inoculation and theywere then examined microscopically three times each week for evidence of cyto-pathic effects (CPE). Fluid from cultures showing CPE or non-specific degenerationwas passed to fresh cultures. Specimens which did not cause CPE after 21 days inCK cultures, or 42 days in CTe cells were considered negative; those whichproduced transmissible CPE were stored for identification.



https://doi.org/10.1017/S0022172400063294


Viruses in the respiratory tract of cattle 259

Identification of viruses

Preliminary identification of viruses was based on the appearance of CPE andthe type of cultures in which it occurred. Parainfluenza virus type 3 was identifiedby an haemagglutination-inhibition (HI) test with specific antiserum, enteroviruses,adonoviruses and respiratory syncytial virus were identified by neutralizationtests with specific antisera. Rhinoviruses were shown to bo stable to chloroform,not inhibited by 20 /*g/ml of bromodeoxyuridine, inactivated at pH 3 and to passthrough a 50 nm Milliporo filter.

Virus antibody titration

Sera were inactivated at 50°C for 30 min before use and absorbed overnightwith 10% human group ' O ' erythrocytes if used in HI tests. Antibodies againstPi-3 and reovirus typo 1 (REO) were measured by HI in microtitro plates. Rhino-virus typo 1, bovino virus diarrhoea virus and RSV antibodies were titrated inmicroneutralization tests. Antibodies against infectious bovino rhinotracheitisvirus (IBR) were measured by passive haomagglutination (Shimizu et al. 1972;Kirby, Martin & Ostler, 1974). A fourfold or greater rise in antibody titro betweensuccessivo sorum samples titrated in tho same test was taken as evidence ofinfection.

RESULTS

Prevalence of respiratory disease

A total of 1590 calves in 17 groups were involved in tho survey (Table 1).Between May 1972 and December 1975, 41 animals (2*0%) died from pneumoniaand 29 from other causes; 354 (22*3 %) required treatment for respiratory disease.Tho incidence of respiratory disease varied between groups, from only 3 % ingroup 11 to 42% in group 12. Only 23 (7*5%) of 300 calves born in January orFebruary required treatment, whereas 05 (32-5%) of 200 born in March and 107(31*7%) of 527 born between July and September were treated.

Tho ago at which respiratory disease and death occurred is shown in Table 2.Of 354 cases of respiratory disease 97*5 % were animals less than 9 months oldand 07*2 % were under 5 months old. Only two animals older than 9 months diedfrom pneumonia.

The seasonal distribution of respiratory disease (Fig. 1, top profile) indicatedthat two outbreaks of illness occurred in each of tho three winters. Almost 80 %of the 354 cases of respiratory illness detected during the survey occurred duringtho six outbreaks which occurred in November 1972, April and October 1973,February and December 1974 and March 1975.

Prevalence of virus infections

Tho routine virological survey was based on 127 animals (Table 1) from whichNS and sera were collected at regular intervals. Nasal swabs collected from 185of tho 354 calves treated for respiratory signs were also examined virologically.Viruses were isolated from 194 of tho 958 NS collected routinely from animals intho survey and also from 49 of 185 swabs taken from calves undergoing treatment



https://doi.org/10.1017/S0022172400063294



Table 1. Population studied and respiratory disease recorded between May 1972and December 1975

Group

123456789

1011121314151017

Breed*

HxFAxFAxFAxFHxFHxFHxFP BHxFHxFHxFMBMBMBMBMBMB

"Dni ft ofbirth

May 1972Aug. 1972Sept. 1972Nov. 1972Mar. 1973May 1973July 1973Sop. 1973Nov. 1973Jan. 1974Fob. 1974July 1974Sop. 1974Nov. 1974Jan. 1975Mar. 1975Juno 1975

No ofanimals

10673836894

10495

101104100100799695

10610680

T)nnfhaJ-'t'Cil/JiO

A1

Pnoumonia

1400200140022

10582

Other

12013204220012252

Respiratoryilmnaalllli

No.

2417202528

7283320

93

3327151137

8

0/

/o2323353730

729331993

422816103510

Routine virology

No.

78888888088888888

X

T)iiT*A.f i n n

(months)

6-112-91-90-60-90-90-90-7—

0-90-90-90-70-50-40-00-3

Totals 1590 41(2-6%) 29 354 22-3 127

H x F = Horoford crossed Friesian. A x F = Abordoon Angus crossed Friosian. PB = Purobreeds: 50 calves wore Canadian Holstoin, 61 woro British Friosian. MB ssMixed broods,consisting of Hereford, S. Devon, Charolais and Simontal.

Table 2. Respiratory disease according to age

AT A n t l i r%f

lifo

123450780

> 9

'otal

"Pn f\\ i in nn i n.X. llUUlltUliiC*

deaths278

11132322

41

Troatmonts

No.

360727

108102433

238

9

354

0/

/o10-218-97-0

30-52-86-89-30-0

10-72-6

100

for respiratory illness (Table 3). Most commonly isolated viruses were Pi-3 andENT. All of the 24 RV isolated were neutralized by antiserum to bovine rhinovirustype 1. One of the 29 AD was typo 2 and the remainder type 3. Seventy of the 88ENT were neutralized by antisera to the LCR4 and M03 strains and thereforebelong to bovine enterovirus type 1 (Western Hemisphere Committee, 1975); theother 18 were not neutralized by antisera to strains F220A, M80, M153, T10 orT11F (Huck & Cartwright, 1964).



https://doi.org/10.1017/S0022172400063294



20

10

60

40

20

B 40o

1 2 0uu

CU

40

20

20

Fig. 1. Monthly incidonco of treatments for respiratory disoaso and virus infections.

Table 3. Viruses isolated from nasopharyngeal swabs, Warren Farm, October 1972 toSeptember 1975

No. of indicated virusoa isolated*

"AA1

Treated |

A_ JPi-3

, 1 1RS 1

U 1 Liii..L RV

H119721

LMi1973

-L—

• fc- IDVD

1 •L •1974

JL1975

Typo ofanimal

Normal survoyTreatedTotal

N/Soxamincd

058185

1143

Pi-3

012788

RS

540

RV

180

24

AD

227

29

Ent

835

88

Untypod

505

Total

10440

243

* Pi-3 =* Parainflucnzavirua typo 3. RS = Respiratory Syncytial Virus. RV = Rhino virustypo 1. AD = Adonovirus: 1 strain from a normal animal was typo 2, tho romaindor woro typo3. Ent =3 Entorovirusoa.

Virus infections were also diagnosed on 327 occasions from 1009 sera collectedfrom animals in the routine survey (Table 4). Infection by IBR virus was notdetected.

Tho combination of virus isolation and serology detected a total of 540 separateinfections by at least seven different virus groups during the investigation: 491 intho routine survey of healthy calves and 49 in animals with acute respiratorydisease (Table 5).

Tho method of diagnosis varied considerably for tho different virus groups when14 HYG 85



https://doi.org/10.1017/S0022172400063294



Table 4. Virus infections diagnosed serologically, Warren Farm, October 1972 toSeptember 1975

No. infections with indicated virus*

Serooxaminod Pi-3 RS RV BVD REO Total

lOGOf 72 00 84 40 53 327

* BVD = bovino virus diarrhoea virus.t The 1000 sera woro collected serially ovory 3 or 4 weeks from 127 calves in tho routino

survoy. Henco they wero equivalent to 042 (1000-127) paired sora.

Table 5. Method of diagnosis of virus infections, Warren Farm, October 1972 toSeptember 1975

No. of infections with indicated virusTypo ofAnimal

Routino normalsurvoy

Treated

Method ofdiagnosis

Isolation onlyBoth isolation

and sorologySorology only

Total

Isolation only

Pi-3

3025

47108

27

RS

50

GO74

4

RV

135

7007

G

BVD

00

4040

0

AD

22ND

ND22

7

REOENT

00

5353

0

83ND

ND

83

5

UT

5ND

ND

50

Total

1G430

207

401

40

Total 135 78 103 40 20 53 88 5 540

both NS and sera were tested. Although 50% of Pi-3 infections and 19% of RVinfections wero diagnosed by virus isolation, less than 7 % of RSV and no BVDVor REO infections were detected in this way (Table 5).

Tho monthly distribution of the four virus infections shown in Fig. 1 indicatedthat most infections by Pi-3, RSV and to a lesser degree RV, occurred in sharpoutbreaks once or twice per year. Outbreaks involving two or three viruses oftenoccurred in tho same month, for example in October 1972, February 1974 andFebruary 1975. Seventy-eight per cent Pi-3, 75% RV, 74% REO and 73% RSVinfections were detected during the winter months, October to March. Infectionsby BVDV and ENT showed no marked seasonal distribution, 55 % being detectedin the winter months. Most AD infections (77%) were found in the summermonths.

The age of calves when infections were diagnosed varied for individual viruses(Fig. 2). There were two peaks of incidence of Pi-3 infections: over 17% weroinfected in the third month of life and 43 % in tho seventh month. The incidenceof RSV infections remained low until 5-0 months after birth, when 21 % of calveswere infected; this figure fell only slightly in the succeeding 3 months. Rhinovirusinfections were found in 20 % of calves in tho second month, thereafter thoincidence declined to 0% in tho fourth month before rising again to 18% in thoseventh month. Tho pattern of ENT infections was quite distinct and showed asingle sharp peak of 34 % in tho fifth month of life. Infections with BVDV, AD andREO did not show any marked trends which could be related to ago.



https://doi.org/10.1017/S0022172400063294



s

ifec

ted

AgeNo.

50

40

30

20

10

1 1

1 1

1 1

llll 1I1I I0 1 2 3 4 5 6 7 8 9

112 112 120 120 112 110 85 70 30

Fig. 2. Proportion of animals infected by Pi-3 (•) , RS virus (•), RV (£3) andENT (g3) according to ago.

Table 0. Reinfection or persistence of viruses

VirusosTypo ofdiagnosis

FirstSecond*

Total

Pi-3

8010

108

RS

041074

RV

811007

BVD

472

40

AD

202

22

REO

485

53

ENT

502483

Toti

40878

480

• Second diagnosis was mado when infection with a particular vims was found in twosoparato investigations of tho samo animal.

Of the 480 virus infections diagnosed 78 were found in animals that had previousovidenco of infection with tho samo agent (Table 6), suggesting either reinfectionor persistence of tho virus. Second diagnoses of Pi-3, RSV, RV and ENT infectionswore most common.

Omitting these second infections, tho percentage of animals in each ago groupwith ovidenco of first infection was calculated. Tho cumulative percentage for eachvirus at each month of ago is shown in Fig. 3. Tho number of infections with Pi-3and RV increased most rapidly in tho first 3 months of life, so that at 3i monthsalmost 40 % of calves had experienced their first infection with these two virusesand by 9 months 85 % and 75 % respectively had been infected. In contrast, only10 %, 18 % and 9 % respectively had evidence of infection by RSV, REO or ENTat 3J months. Infections by RSV and ENT were found more frequently after 4months of age, so that by 9 months RSV had been diagnosed in 70 % and ENT in50 % of calves.

14-2



https://doi.org/10.1017/S0022172400063294



75

50

25

• Pi-3

DVD

«——f—«r

0 1 2 3 4 5 6 7 8Age (months)

Fig. 3. Cumulativo porcontago of animals which havo oxporionccd thoir first infoctionaccording to ago.

Association between respiratory disease and virus infection

There were 0 months during tho survey when moro than 5 % of the total animalsin the farm under 9 months old were treated for respiratory disease (Fig. 1 andTable 7). Out of a total of 942 virological investigations in tho whole survoy, 204(21*7%) were undertaken during tho 0 months in which there wore outbreaks ofdisease (Table 7). If virus infections occurred at random and wore unrolated torespiratory disease it would bo expected that about 20 % of those diagnosed wouldbe detected during tho six outbreaks. Tho percentages for infections by RV(29-9 %), BVDV (18-4 %), AD (22-7 %), REO (28-3 %) and ENT (10-9 %) wore notsignificantly different from tho expected 21*7% (P>0*05). However, 38% ofPi-3 infections and 58-1 % of RSV infections were diagnosed during outbreaks ofdisease. These values were significantly different (P< 0*001) from tho expected21*7%, and indicated a significant association between infections with these twoviruses and outbreaks of respiratory disease.

Tho five groups of calves with a low incidence of respiratory disease (10% orless) were compared (Table 8) with tho six groups with a high incidence (30 % ormoro). Of tho animals investigated virologically tho proportion infected by Pi-3,RV, AD, REO and ENT were similar for both high and low disease groups.However, significantly more RSV and BVDV infections (P<0-01) were detectedin calves from tho groups in which 30 % or more were treated for respiratory disease.

DISCUSSIONTho prevalence of respiratory disease in beef calves in tho United Kingdom is

not precisely known. In tho current survoy, 22*2% of calves were treated for



https://doi.org/10.1017/S0022172400063294


Tab

le 7

. V

irus

inf

ecti

ons

and

outb

reak

s* o

f di

seas

e, W

arre

n F

arm

, O

ctob

er 1

972

to S

epte

mbe

r 19

75

Out

brea

k

Yea

r M

onth

1972

N

ov.

1973

A

pr.

Oct

.19

74

Feb

.D

ec.

1975

M

ar.

Tot

al d

urin

g ou

tbre

aks

Tot

al t

hrou

ghou

t su

rvey

% d

urin

g ou

tbre

aks

Xs

Pro

babi

lity}

Ani

mal

str

eate

d(%

)

17-7 5-5

7-9

9-1

13-4

11-7

No.

vir

olog

ical

inve

stig

atio

ns!

47 24 31 54 24 24 204

942 21-7

Pi-

3

15 2 20 4 0 0 41 108

38

018

-06

<0-0

01

No.

infe

ctio

ns w

ith

indi

cate

d vi

rus

RS 1 3 4 13 4 18 43 74 58

160

-58

< 0-

001

RV 4 1 6 15 1 2 29 97 29-9 3-80

>0-

05

A BV

D 4 1 0 4 0 0 9 49 18-4 0-56

>0-

3

AD 0 1 3 0 1 0 5 22 22-7 0-02

>0-

8

RE

O 7 1 6 0 1 0 15 53 28-3 1-24

>0-

2

EN

T 0 2 5 3 3 1 14 83 16-9 1-56

>0-

2

* O

utbr

eak

= an

y m

onth

in w

liich

mor

e th

an 5

% o

f an

imal

s un

der

9 m

ontl

is r

equi

red

trea

tmen

t fo

r re

spir

ator

y di

seas

e,f

Inve

stig

atio

n =

occa

sion

on

whi

ch "

both

pai

red

sera

and

NS

wer

e co

llect

ed f

rom

an

anim

al.

% C

alcu

late

d us

ing

Yat

e's

mod

ifica

tion

for

smal

l num

bers

.

C3

Crc



https://doi.org/10.1017/S0022172400063294



Table 8. Infections in groups with high or low incidence of respiratory disease

No. calves . . .No. troatod . . .No. invosti gated %No. infected

Pi-3RSRVBVDADREOENT

Low diseasegroups*

40038 (7-8%)40

28 (70%)9 (23%)

24 (00%)0 (23%)7 (18%)

14 (35%)10 (48%)

High diseasogroupsf

531185 (34-8%)48

32 (07%)20 (54%)28 (58%)22 (40%)11 (23%)17 (35%)24 (50%)

• Group 0, 10, 11, 15 and 17 (Tablo 1) in which ^ 1 0 % of calvos roquirod troatmont forrespiratory diseaso.

t Group 3, 4, 5, 8, 12 and 10 (Tablo 1) in which >30% of calves roquirod troatmont forrospiratory disoaso.

% No. of calves in virological survoy.

respiratory diseaso and 2*5% died from pneumonia. Similar figures have beenobtained from other surveys (Thomas, 1978). The low incidence of diseaso (7*5%)in calves born in January and February and the high incidence (32 %) in calvesborn in March, July and September is striking. If this observation is confirmed inlarger surveys, it would indicate that the current practice of early autumn calvingincreases the likelihood of respiratory diseaso. Our observations that 07*2% ofdiseaso occurred in animals under 5 months old and that 80 % of cases were foundduring sharply defined outbreaks in the winter months confirm established beliefs.

Relatively few attempts have been made to survoy virus infections in normalcattle; Dawson el al. (1900) sampled 20 calves regularly for 18 weeks. No viruseswere isolated but six calves had serological evidence of Pi-3 infection when signs ofrespiratory diseaso were observed. In Australia 20 calves were continuouslystudied for 0 months (St George, Hass & Horsfall, 1972). Pi-3 was isolated from 21nasal swabs from four calves and ENT from 41 faecal swabs of 10 calves. Serolo-gical evidence of BVD and Pi-3 infection was also found. A sorological survey of 47calves during 0 months (Thomas & Collins, 1974) revealed frequent infection byPi-3, BVDV and REO viruses. A smaller survoy of 0 calves over 14 months inNew Zealand also detected Pi-3 and ENT (Burgess, 1977). Because of the smallnumbers of animals involved (less than 50), no conclusions were made aboutseasonal or ago distribution of viruses, nor was a statistically significant associationbetween virus infection and respiratory diseaso established in these surveys.However, an investigation of over 200 calves in Holland revealed a strikingcorrelation between RSV infection and bronchopneumonia of yearling cattle(Holzhauer & van Nieuwstadt, 1970; Holzhauer, 1978).

In our own survey tho optimum method of diagnosis was not the samo for allviruses. Although virus isolation and serology were almost equally effective indiagnosing Pi-3 infection, for most other agents virus isolation was relatively



https://doi.org/10.1017/S0022172400063294



inefficient. Other workers have experienced difficulty in isolating RSV and RVfrom cattle (Wellemans & Leunen, 1975; Mohanty, Lillie & Ingling, 1976;Lehmkuhl & Gough, 1977; Mohanty & Lillie, 1968). Only cytopathic strains ofBVDV would have been isolated in this survey and probably most BVDV infectionsare by non-cytopathic strains (Kodama et al. 1974) and therefore would only havebeen diagnosed sorologically. Furthermore, many BVDV and REO infections mayhave been primarily enteric rather than respiratory and virus isolation from NSwould bo inefficient in such cases. The method of diagnosis is important in inter-preting the results since, for example, sorological diagnosis may bo difficult in ayoung calf with large amounts of maternal antibody.

During the routine survey, 491 virus infections were detected in 942 investiga-tions of 127 apparently healthy calves, indicating that virus infection is not onlycommon but frequently symptomless. This rate of virus infection (52 %) is muchhigher than the 5-21% found in similar surveys of children (Bell et al. 1961;Chanock & Parrott, 1965; Holzel et al. 1965; Coonoy, Hall & Fox, 1972). Between13% and 18% of Pi-3, RSV or RV infections were not primary infections andindicate, either virus persistence or failure of a primary infection to give adequateprotection against reinfection. Similar repeated infection of children by Pi-3 andRSV is well documented (Chanock, Boll & Parrott, 1961; Beem, 1967; Hendersonetal.ldiO).

Calves were born at intervals of approximately 2 months throughout the survoy;there wore no late spring or early autumn calving peaks as frequently occur oncommercial beef farms. The effect of season and ago on the incidenco of virusinfection can therefore bo assessed independently. The marked increase, in thewinter months, of infections by Pi-3 and RSV, and their tendency to occur insharp outbreaks aro also similar to findings in children (Chanock ct al. 1961;Chanock & Parrott, 1965; Kim et al. 1973). Howovcr, the lack of marked seasonaldistribution of ENT infections and the increase in AD infections in the summercontrast with findings in man (Spigland et al. 1966; Monto & Cavallaro, 1971).

Primary infections with Pi-3 and RV seemed to occur earlier than with RSV,REO or ENT. This may bo because maternal antibody reduced the efficiency ofserological diagnosis of RSV and REO or protected calves more efficiently againsttheso viruses than Pi-3 and RV. A third explanation may bo a real difference in agosuscoptibility, although the latter two hypotheses aro not supported by data fromchildren (Cooney, Fox & Hall, 1975).

A statistically significant association between virus infections and disease wasdetected, first, by comparing the incidenco of infections during outbreaks ofdisease with the incidenco at other times and, secondly, by comparing the fre-quency of virus infections in groups with a high incidenco of disease with thosewith a low incidence. In the first comparison, only RSV and Pi-3 were significantlyassociated with disease. Furthermore, with the exception of RSV, most virusinfections (62% for Pi-3 to 83% for ENT) were detected when there was nosignificant disease on the farm. In the second comparison only RSV and BVDVwere associated with high incidenco of disease. If BVDV has an aetiological role inrespiratory disease, it may bo through its ability to persist in cells of the reticulo-



https://doi.org/10.1017/S0022172400063294


268 E. J . STOTT A"ND OTHERS

endothelial system and thereby suppress immune responses over long periods. If so,its association with disease might not be demonstrated by the first comparisonwhich is a temporal one between acute infections and disease.

It must be stressed that this survey, showing significant association betweencertain viruses and respiratory disease, does not, and is not intended to prove anaetiological role for such viruses. Proof requires reproduction of disease by thevirus or, at least, its prevention by a vaccine against the agent. Nevertheless, oursurvey considerably strengthens the case for RSV being important in the aetiologyof calf respiratory disease and, equally relevant, argues against the overall impor-tance of RV, AD, REO and ENT. These conclusions are again remarkably similarto those derived from studies of lower respiratory disease in young children(Tyeryar, Richardson & Belsho, 1978) and are consistent with a growing numberof recent studies in calves highlighting the importance of RSV (Wellomans &Leunen, 1075; Holzhauer & van Nieuwstadt, 1970; Lehmkuhl & Gough, 1977;Bryson etal. 1978).

It is not known how far these results derived from one farm apply nationally.However, the calves were derived from many, widely scattered farms all overEngland and Wales and must represent the national beef herd, at least virologically.Ultimately, this question can only bo resolved by similar surveys in other centreson many different farms.

Wo thank Dr P. Lamont and the Central Veterinary Laboratory, Weybridgo,for antisera to adenoviruscs and enteroviruses. Wo are grateful to Dr A. J. Starkfor statistical advice and analyses.

REFERENCESBEEM, M. (1007). Ropoatcd infoctions with respiratory syncytial virus. Journal of Immunology

98, 1115-22.BELL, J. A., HEUDNER, R. J., ROSEN, L., ROWE, W. P., COLE, R. M., MASTROTA, F. M.,

FLOYD, T. M., CIIANOCK, R. M. & SIIVEDOFF, R. A. (1001). Illness and microbial oxporioncosof nursery children at Junior village American Journal of Hygiene 74, 207-02.

BRYSON, D. G., MCFERRAN, J. B., BALL, H. J. & NEILL, S. D. (1078). Observations onoutbreaks of respiratory discaso in housed calves. 1. Epidomiological, clinical and micro*biological findings. Veterinary Record 103,485-0.

BURGESS, G. W. (1077). A study of ondomic viruses in a group of calvos. New ZealandVeterinary Journal 25,178-0.

CAUL, E. 0., JACOBS, J. W. & CLARKE, S. K. R. (1074). Bovino tostis colls for routino isolationof rospiratory syncytial virus from infants. Journal of Medical Microbiology 7, 301-4.

CIIANOCK, R. M., BELL, J. A. & PARROTT, R. H. (1001). Natural history of parainfluonzainfection. Perspectives in Virology 11,120-38.

CIIANOCK, R. M. & PARROTT, R. H. (1005). Acuto respiratory disease in infancy and child-hood; present understanding and prospects for prevention. Pediatrics 36, 21-30.

COONEY, M. K., Fox, J. P. & HALL, C. E. (1075). Tho Seattlo Virus Watch. VI. Observationsof infections with an illness duo to parainflucnza, mumps and respiratory syncytial virusesand Mycoplasma pnoumonia. American Journal of Epidemiology 101, 532-51.

COONEY, M. K., HALL, C. E. & Fox, J. P. (1072). Soattlo virus Watch. III . Evaluation ofisolation methods and summary of infections detected, by virus isolations. American Journalof Epidemiology 96, 280-305.

DARDYSHIRE, J. H. & RODERTS, D. H. (1008). Somo respiratory virus and mycoplasmainfections of animals. Journal of Clinical Pathology, supplement no. 2, pp. 01-87.



https://doi.org/10.1017/S0022172400063294


Viruses in the respiratory tract of cattle 269DAWSON, P. S., STUART, P., DARBYSHIRE, J. H., PARKER, W. H. & MCCREA, C. T. (I960).

Respiratory disease in a group of intensively reared calves. Veterinary Record 78, 543-6.HENDERSON, F. W., COLLIER, A. M., CLYDE, W. A. & DENNY, F. W. (1970). Respiratory

syncytial virus infections, reinfections and immunity. New England Journal of Medicine300, 530-34.

HOLZEL, A., PARKER, L., PATTERSON, W. H., CARTMEL, D., WHITE, L. L. R., PURDY, R.,THOMSON, K. H. & Tonm, J. O'H. (1905). Virus isolations from throats of children admittedto hospital with respiratory and other diseases, Manchester 1902-64. British MedicalJournal i, 014-9.

HOLZHAUER, C. (1978). Bronchopnoumonia of yearling cattle. Doctoral Thesis, University ofUtrecht.

HOLZHAUER, C. & VAN NIEUWSTADT, A. P. K.M.I . (1976). Do otiologischo rol van hotBovino Respiratory syncytial virus bij pinkengriep. Tijdschrift voor Dicrgcneeskunde 101,1023-31.

HUCK, R. A. & CARTWRIGHT, S. F. (1904). Isolation and classification of viruses from cattloduring outbreaks of mucosal or respiratory diseaso and from herds with reproductivedisordors. Journal of Comparative Pallwlogy 74,346-05.

KIM, H. W., ARROBIO, J. O., BRANDT, C. D., JEFFRIES, B. C, PYLES, O., REID, J. L., CHANOCK,R. M. & PARROTT, R. H. (1973). Epidomiology of respiratory syncytial virus infection inWashington D.C. 1. Importanco of tho virus in different respiratory disease syndromes andtomporal distribution of infection. American Journal of Epidemiology 98, 210-25.

KIRBY, F. D., MARTIN, H. T. & OSTLER, D. C. (1074). An indirect hoomagglutination tost fortho detection and assay of antibody to infectious bovino rhinotrachoitis virus. VeterinaryRecord 94,301-2.

KODAMA, K., SASAKAI, N., FUKUYAMA, D., IZUMIDA, A. & ISHII, F. (1974). Studies on cyto-pathogonic bovino viral diarrhoea virus. Rccovory, identification and properties of thoisolated vims. Bulletin of the Nippon Veterinary and Zootcchnical College 23, 51-9.

LEIIMKUHL, H. D. & Gouair, P. M. (1977). Investigations of causativo agonts of bovinorespiratory tract discaso in a boof cow-calf herd with an early weaning program. AmericanJournal of Veterinary Research 38,1717-20.

MOHANTY, S. B. (1978). Bovino Respiratory viruses. Advances in Veterinary Science andComparative Medicine 22, 83-109.

MOHANTY, S. B. & LILLIK, M. G. (1908). Isolation of a bovino rhinovirus. Proceedings of theSociety for Experimental Biology and Mcdicino 128,850-52.

MOHANTY, S. B., LILLIK, M. Q. & INGLING, A. L. (1970). Eflbct of serum and nasal neutralizingantibodies on bovino rospiratory syncytial virus infection in calves. Journal of InfectiousDiseases 134,409-13.

MONTO, A. S. & CAVALLARO, J. J. (1071). Tho Tccumsoh study of rospiratory illness. II .Pattorn8 of occurronco of infection witli respiratory pathogons, 1905-1909. AmericanJournal of Epidemiology 94,280-89.

PHILLIP, J. I. H. & DARUYSHIRK, J. H. (1971). Respiratory viruses of cattlo. Advances inVeterinary Science ami Comparative Medicine 15,159-99.

ROSENQUI8T, B. D. & DOUSON, A. W. (1074). Multiplo viral infection in calves with acutobovino respiratory tract discaso. American Journal of Veterinary Research 35, 303-5.

ROSENQUI8T, B. D., ENGLISH, J. E., JOHNSON, D. W. & LOAN, R. W. (1970). Mixed viralaetiology of a shipping fovcr epizootic in cattlo. American Journal of Veterinary Research31, 089-94.

ST GEORGE, T. D., IIASS, C. R. & HORSFALL, N. (1972). Infections with viruses and bacteria inintensivoly roared calves in Northern Queensland. Australian Veterinary Journal 48, 7-11.

SinMizu, Y., I8AYAMA, Y., KAWAKAMI, Y., MURASE, N. & KAWANO, T. (1972). Micro indirecthaomagglutination tost for detecting antibody against infectious bovino rhinotrachitisvirus. National Institute of Animal Health Quarterly 12,1-7.

SPIGLAND, I., Fox, J. P., ELVEBACK, L. R., WASSERMAN, F. E., KETLER, A., BRANDT, C. D. &KOGON, A. (1900). Tho Vims Watch program. A continuing survcillanco of viral infectionsin metropolitan Now York families. II . Laboratory mothods and preliminary report oninfections rovcalcd by virus isolation. American Journal of Epidemiology 83, 413-35.

THOMAS, L. H. (1978). Discaso incidenco and epidemiology - tho situation in tho U.K.Current Topics in Veterinary Medicine 3, 57-05.



https://doi.org/10.1017/S0022172400063294



THOMAS, L. H. & COLLINS, A. P. (1974). Virus infection and incidence of respiratory disoaso:a serological study of four micro-organisms at a largo beef-rearing farm. Veterinary Record94, 606-9.

THOMAS, L. H. & STOTT, E. J. (1975). Comparison of threo methods for sampling tho bovinoupper respiratory tract for viruses. Research in Veterinary Science 18, 227-9.

TYERYAR, F. J., RICHARDSON, L. S. & BELSHE, R. B. (1978). Report of a Workshop on respi-ratory syncytial virus and parainfluenza viruses. Journal of Infectious Diseases 137, 835-40.

WELLEMANS, G. & LEUNEN, J. (1976). Lo vims rdspiratoiro syncytial ot les troubles rdspira-toires des bovins. Annalcs de Mtd&cin Vcterinaire 119, 359-09.

WESTERN HEMISPHERE COMMITTEE ON ANIMAL VIRUS CLASSIFICATION (1975). An updatedlisting of animal rofcronco virus recommendations. American Journal oj Veterinary Research36, 801-72.



https://doi.org/10.1017/S0022172400063294


a survey of virus infections of the respiratory tract of

Documents