INFECCIOSAS Prevalencia Agentes Patogenos Diarreas Neonatales

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TheVeterinary Record, September 20, 2008

MATERIALS AND METHODS

Farms, animals and collection of samplesA list of 420 rural veterinary practices in Switzerland wasestablished, and from this list 70 practices located withina radius of approximately 80 km from the Clinic forRuminants of the University of Berne were selected ran-domly. Veterinarians were asked by mail to participate in thestudy. The sample size for herds with diarrhoeic calves wascalculated for an estimated prevalence ofC parvum of 50 percent among calves with diarrhoea, allowing for clusteringwithin herds, a standard error less than 5 per cent, and anintraclass coefficient rho of 03 (Bennett and others 1991); a

sample size of 210 diarrhoeic calves in 70 herds was derived.The participating veterinarians were asked to consider thefollowing inclusion criteria: dairy farms with more than 15milking cows, and samples to be collected from three calvesaged one to 21 days with acute diarrhoea of less than 48 hoursduration from each farm. The samples had to be collectedbetween October 1, 2005 and April 30, 2006. Calves that hadbeen treated with either antibiotics or halofuginone, or thatsuffered from other diseases such as pneumonia, omphalitisor polyarthritis, and calves from suckler herds were excludedfrom the study. A herd was classified as positive for one of thefour pathogens if at least two calves excreted the pathogen.

Samples of faeces and serum were collected by the veteri-narians from calves fulfilling the inclusion criteria before theywere treated, and sent to the Clinic for Ruminants withina day. The name of each calfs owner, and its identificationnumber, age, breed, sex and clinical condition were recordedon a standardised form. The clinical data included the calf sbody temperature, heart rate, respiratory rate, general condi-tion, appetite, suckling reflex, degree of dehydration, and theconsistency of its faeces.

Laboratory analysesThe faecal samples were analysed for the presence ofC par-vum, rotavirus, BCV and E coli K99 by standard diagnosticmethods. Oocysts of C parvum were detected by a modi-fied Ziehl-Neelsen staining method (Kaufmann 1996). Thesamples were tested for rotavirus by antigen-capture ELISA(Pathfinder Rotavirus EIA; Bio-Rad Laboratories) accordingto the manufacturers instructions. The excretion ofBCV wasdiagnosed by a non-commercial biphasic antigen-captureELISA assay in 96-well microELISA plates (Immulon M 129A; Dynatech). For the diagnosis ofE coli K99, each samplewas cultured on minimal casein agar (MINCA agar medium;

DIARRHOEA is one of the most serious diseases of neonatalcalves. It causes major economic losses due to mortality, poorgrowth and the costs of treatment. It is a complex, multifacto-rial disease that is affected by the intrinsic characteristics of thecalf, its nutritional and immunological status, the managementof the herd, the environment, and various infectious agents(Bendali and others 1999a, Scott and others 2004). Calves areat the greatest risk of developing diarrhoea in the first monthof life and the incidence of diarrhoea decreases with age (Frankand Kaneene 1993, Bendali and others 1999b).

The four major enteropathogens associated with neonatalcalf diarrhoea worldwide are Cryptosporidium parvum, rotavi-rus, bovine coronavirus (BCV) and enterotoxigenic Escherichiacoli (E coliK99) (Garcia and others 2000). Salmonella spe-cies can also cause diarrhoea and septicaemia, particularlywhen calves are brought together from different farms andraised intensively on milk replacer diets (Naylor 2002). Otheragents, such as Campylobacter jejuni and Campylobacter spu-torum biovar faecalis, Clostridium species, parvovirus, calici-virus, bredavirus and torovirus are also pathogenic in calves,but their importance in the field is uncertain (Mansfeld andothers 2007). There has recently been interest in Clostridiumdifficile (Songer 2004, Arroyo and others 2005, Songer andAnderson 2006, Hammitt and others 2008) as a potentialcause of enteritis in calves, but further studies are needed toevaluate its role.

The prevalence of the different aetiological agents varieswith the calf s age, and multiple infections are common. Theclinical signs induced by the different microorganisms aresimilar, and an aetiological diagnosis can only be reached inthe laboratory. The identification of the infectious agent(s)involved is important for planning preventive measures andcontrolling the disease. However, after an agent has beenidentified, it is difficult to determine whether it is responsi-ble for the diarrhoea in the individual or in the herd, becausemost of the agents are also found in healthy calves (Saif andSmith 1985, Janke 1989, Fagan and others 1995).

The main aim of the present study was to determine theprevalence ofC parvum, rotavirus, BCV and E coliK99 in dairycalves aged one to 21 days suffering from acute diarrhoea indairy herds in western Switzerland at the individual and atthe herd level. The belief that C parvum is the most commonorganism identified in cases of neonatal diarrhoea in the regionwas examined. In addition, the results of standardised labora-tory methods were compared with the results obtained withrapid tests, and the immunological status (the level of serumimmunoglobulins) of the diarrhoeic calves was investigated.

Veterinary Record(2008)163, 362-366

F. Lanz Uhde,DrMedVet,T. Kaufmann,DrMedVet,M. Meylan,DrMedVet,FVH, PhD, DrHabil,Clinic for Ruminants,H. Sager,DrMedVet, FVH,PhD,Institute of Veterinary

Parasitology,S. Albini,DrMedVet, FVH,Institute of VeterinaryBacteriology,R. Zanoni,DrMedVet,DrHabil,Institute of VeterinaryVirology,Vetsuisse Faculty,University of Berne,Bremgartenstrasse 109a,3012 Berne, SwitzerlandE. Schelling,DrMedVet,PhD,Swiss Tropical Institute,Basel, Switzerland

Correspondence toDr Meylan

Prevalence of four enteropathogens in thefaeces of young diarrhoeic dairy calves in

SwitzerlandF. Lanz Uhde, T. Kaufmann, H. Sager, S. Albini, R. Zanoni, E. Schelling,

M. Meylan

The prevalences ofCryptosporidium parvum, rotavirus, bovine coronavirus (BCV), and enterotoxigenicEscherichia coli(E coliK99) were determined in diarrhoeic dairy calves aged one to 21 days on 71 dairyfarms in western Switzerland during the winter of 2005 to 2006. Faecal samples from 147 untreated calvessuffering from acute diarrhoea were analysed by standardised diagnostic methods, and the immunoglobulinstatus of each calf was evaluated. The prevalences ofC parvum, rotavirus, BCVand E coliK99 were 550 percent, 587 per cent, 78 per cent and 55 per cent, respectively. The proportions of herds positive for therespective pathogens among the herds with diarrhoeic calves were 417 per cent, 521 per cent, 21 per centand 21 per cent. The immunoglobulin concentration in the serum of 905 per cent of the diarrhoeic calves

was below 8 g/l.

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ence of the four pathogens, either individually or in combina-tion, was evaluated with a logistic regression model. Similarly,the immunoglobulin levels were evaluated for their associa-tion with the occurrence of the four pathogens. Possible asso-ciations between the immunoglobulin levels and the age ofthe calves (in days), and between the immunoglobulin levels

and the clinical scores were investigated by a linear regres-sion model.To compare the results of the rapid tests with the results

of the standard diagnostic methods, the test results wererecorded as either positive or negative for each pathogen.The sensitivity and specificity of the rapid tests were com-pared with those of the standard diagnostic tests (Thrusfield2005). The data were analysed by using Intercooled STATA 8.2(StataCorp).

RESULTS

Samples of faeces and serum from 174 diarrhoeic calves in79 dairy herds were submitted by 32 veterinary practitioners

between October 2005 and April 2006; 147 of the calves from71 herds fulfilled the inclusion criteria and only these sampleswere used for further analyses. The targeted sample size ofthree calves from each herd was not achieved; samples fromfour calves were available from two herds, from three calvesfrom 24 herds, from two calves from 22 herds, and only onesample was sent from the remaining 23 herds.

The mean age of the calves was 83 days (95 per cent con-fidence interval [CI] 77 to 89, range one to 20 days). Thedistribution of the breeds was as follows: 327 per cent redHolstein, 231 per cent fleckvieh (red Holstein x simmental),156 per cent Holstein Friesian, 41 per cent brown Swiss and245 per cent mixed breeds. There were 483 per cent malesand 517 per cent females. Nearly all the calves (925 per cent)showed few or no clinical signs of deterioration in condition,

and the other 75 per cent showed moderate to severe signsof lethargy and weakness. The suckling reflex was present in905 per cent of the calves (Table 1).

Enteric pathogens were found in 912 per cent of the faecalsamples. The calculated individual prevalences were 55 percent for C parvum, 587 per cent for rotavirus, 78 per centfor BCV and 55 per cent for E coliK99 (Table 2). There wereno significant associations between the pathogens diagnosedand clinical scores of the calves.

Infections with only one pathogen were found in 586per cent of the samples. The most frequent combination wasrotavirus and C parvum (19 per cent). The proportions ofsingle and combined infections are given in Table 3.

The herd prevalences were 417 per cent for C parvum,521 per cent for rotavirus, 21 per cent for BCV and 21 percent for E coliK99. When the herd prevalences were calcu-lated on the basis of the results from only the first two calvessampled in each herd they were slightly lower for rotavirusand C parvum than when they were calculated on the basis ofall results from herds from which at least two samples wereavailable without consideration of the number of samples(two or three) per herd (Table 4).

The analyses of the faecal samples with the four immuno-chromatographic rapid tests were positive for C parvum in449 per cent and for rotavirus in 469 per cent of the sam-ples. None of the samples were positive for BCV and only onesample was positive for E coli K99. The sensitivity and specifi-city of the rapid tests were therefore calculated only for theFASTest CRYPTO Strip (sensitivity 835 per cent, specificity 100per cent) and the FASTest ROTA Strip (sensitivity 841 per cent,specificity 100 per cent).

The serum immunoglobulin concentration of 905 percent of the calves was less than 8 g/l (Fig 1). There were nosignificant associations between the serum immunoglobulin

Axcell) mixed with PolyViteX (PVX-M; BioMrieux) andincubated aerobically at 37C for 24 hours. Colonies of Ecoli were then identified phenotypically. The presence of F5(K99) was examined by slide agglutination with monovalentF5 (K99)-rabbit-antiserum (Statens Serum Institute).

In parallel, all the faecal samples were analysed by fourrapid tests: FASTest CRYPTO Strip, FASTest ROTA Strip, FASTestBCV Strip and FASTestE coliK99 Strip (MegaCor Diagnostics).They were based on immunochromatographic techniques

and used as described by the manufacturer. The results werecompared with those obtained by the established laboratorymethods. The serum immunoglobulin levels were deter-mined with the Paragon Serum Protein Electrophoresis Kit(Beckman Coulter) according to the manufacturers instruc-tions.

Statistical analysesFor the individual calves with diarrhoea, logistic regressionmodels with random effect on the herd level (xtlogit pro-cedure) were used to calculate estimates of the prevalenceof each of the four enteropathogens and for the 12 possiblecombinations. Clustering within herds (random effect inthe model) was taken into consideration because the calveswithin the same herd would be less independent than calvesfrom different herds (Bendali and others 1999b). At the herdlevel, the proportions of positive herds among the herdswith diarrhoeic calves (herd prevalence) was calculated onthe basis of the classification of herds as positive for a givenpathogen when at least two calves excreted it; all other herdswhere at least two samples were available were considerednegative for this infectious agent. Herds from which only onesample had been submitted were not included in the calcula-tion of herd prevalences. In addition, the herd prevalenceswere calculated by using only the results from the first twocalves examined in each herd, according to the same clas-sification criteria.

A clinical score for the calves was generated on the basis ofthe clinical data to test for possible associations between theclinical signs and infection with specific pathogens (Naciriand others 1999). The sum of the scores for the followingfive variables were used: general condition, appetite, suck-ling reflex, degree of dehydration and consistency of faeces(Table 1). The association of the clinical scores with the pres-

TABLE 1: Percentages of the 147 diarrhoeic calves showingdifferent clinical signs and the scores assigned to calculate anoverall clinical score

Clinical observation Scoring Percentage

General conditionNormal 0 388Slightly affected 1 537Moderately affected 2 41Severely affected 4 34

AppetiteGood 0 490Reduced 2 435Anorectic 4 75

Suckling reflexGood 0 566Moderate 2 340Absent 4 95

Degree of dehydrationNot dehydrated 0 531Slightly dehydrated 1 374Moderately dehydrated 2 81Severely dehydrated 4 14

Consistency of faecesMushy 0 422Watery 4 578


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become diarrhoeic shortly after being sampled; the methodof selecting healthy controls in herds with diarrhoea maytherefore lead to bias (Busato and others 1998, Luginbhland others 2005). Finally, it is often not possible to samplenon-diarrhoeic calves on farms with a high morbidity. Forthese reasons a healthy control group within the herds understudy was not included.

Herds with three samples available were more likely tohave two calves positive for one of the pathogens, and theherd prevalences were accordingly slightly higher in thisanalysis than when only the first two calves sampled wereused in the analysis, a method that gives a more conservativeestimate of the prevalences of the pathogens. The distribu-

tion and the relative prevalences of the different pathogenswere the same in both analyses. The decision to restrict herdpositivity to the herds in which pathogens had been foundin at least two calves was made because the four pathogenshave been reported to be excreted by healthy animals in acontaminated environment (Scott and other 2004). However,finding the same pathogen in two calves with acute diarrhoeasuggests that it is likely to be implicated in the pathogenesisof the disease in the herd.

Infection with more than one pathogen was observed inmore than 40 per cent of the calves. In agreement with previ-ous surveys worldwide, the most common mixed infectionwas rotavirus and C parvum (Snodgrass and others 1986, dela Fuente and others 1999, Garcia and others 2000, Joachimand others 2003, Hfle 2005).

There is good evidence that rotavirus is a primary pathogencausing acute diarrhoea in neonatal calves (Torres-Medinaand others 1985, Reynolds and others 1986, Snodgrass andothers 1986, Busato and others 1998, Garcia and others 2000),and that it can be detected more frequently in the faeces ofdiarrhoeic than of non-diarrhoeic calves (De Rycke and oth-ers 1986, Snodgrass and others 1986, Busato and others 1998,Haschek and others 2006). In this study rotavirus was theinfectious agent excreted most commonly by the calves withdiarrhoea, not only alone but also in mixed infections withother pathogens, indicating that rotavirus has a predomi-nant role in the pathogenesis of neonatal calf diarrhoea inSwitzerland.

C parvum was first reported in association with calf diar-rhoea by Panciera and others (1971). It also has the poten-tial to cause disease in immunocompromised human beings(Fayer and others 2000). Today, it is found worldwide with aprevalence in young calves of between 14 per cent and over80 per cent, depending on the age, health and housing of the

levels and the clinical scores or age of the calves or the patho-gens diagnosed.

DISCUSSION

Diarrhoea in neonatal calves is one of the major problems

in Swiss dairy herds (Sommer 1994, Strk and others 1997),but there have been few studies of the pathogens causing theproblem (Luginbhl and Pfister 1996, Strk and others 1997,Luginbhl and others 2005). There is little information avail-able for dairy calves owing to the small numbers of animalsstudied and the lack of detailed information on individualanimals, but there have been larger scale investigations ofsuckler cow operations (Busato and others 1997a, b, 1998,Steiner and others 1997, Lentze and others 1999). The aimof this study was therefore to determine the prevalence ofC parvum, rotavirus, BCV and E coliK99 in one to 21-day-old calves with acute diarrhoea in 71 dairy herds in westernSwitzerland with neonatal calf diarrhoea as a herd problem.The immunoglobulin levels in the serum of the calves withdiarrhoea were also evaluated because a failure of passive

transfer is a well-known risk factor for neonatal disease incalves (Barrington and others 2002).

The incidence of diarrhoea in calves is highest during thewinter months and the greatest risk for a calf occurs dur-ing its first month of life (Frank and Kaneene 1993, Bendaliand others 1999a, Gutzwiller 2002, Scott and others 2004,Mansfeld and others 2007). For these reasons, samples werecollected between October and April and only calves lessthan three weeks of age were included. The best diagnosticresults are obtained early in the course of the disease (Scottand others 2004, Mansfeld and others 2007) and previoustreatment with antimicrobials or halofuginone can lead tofalse-negative test results. The calves that had suffered fromdiarrhoea for more than 48 hours when examined by theveterinarian or had already been treated by the owner weretherefore excluded from the study. After a pathogen had beendiagnosed, the farmers wanted to take preventive measures(particularly treatment with halofuginone in the case ofcryptosporidiosis) as soon as possible, and no further sam-pling was therefore possible from untreated calves after theinitial diagnosis.

When they were examined, the majority of the calveswere in good general condition and systemic signs of diseasewere mostly mild. This was probably due to the fact that onlycalves that had had acute diarrhoea for less than 48 hourswere sampled.

As a result, no association was found between the patho-gens detected and the clinical scores of the calves. The calveswere sampled only once, and single sampling may give false-negative results because rotavirus, BCV and cryptosporidiaare excreted in a cyclical pattern. Furthermore, intermittentshedding of pathogens has been reported in both healthy anddiseased animals (Trotz-Williams and others 2005, Singh andothers 2006), and it is known that healthy control animals can

TABLE 2: Percentages of the 147 calves with diarrhoea thatwere positive for Cryptosporidium parvum, rotavirus, bovinecoronavirus (BCV), and Escherichia coliK99 by standardlaboratory methods and their mean (95 per cent confidenceinterval [CI]) calculated prevalences

Infectious agent Percentage positive

Calculated prevalence

(%) (95 per centCI)

C parvum 537 550 (405-688)Rotavirus 558 587 (429-728)BCV 88 78 (27-209)E coliK99 95 55 (17-167)

TABLE 3: Percentages of the 147 calves with diarrhoea thatwere positive for Cryptosporidium parvum, rotavirus, bovinecoronavirus (BCV), Escherichia coliK99 or combinations of theseagents

Infectious agent Positive (%)

C parvum 286Rotavirus 272BCV 14E coliK99 14C parvum, rotavirus 190C parvum, BCV 27C parvum, E coliK99 0Rotavirus, BCV 07Rotavirus, E coliK99 54BCV, E coliK99 14C parvum, rotavirus, BCV 20C parvum, rotavirus, E coliK99 07C parvum, BCV, E coliK99 0Rotavirus, BCV, E coliK99 0C parvum, rotavirus, BCV,E coliK99 07No pathogen 88


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not for diarrhoea. However, Par and others (1993) suggestedthat high immunoglobulin levels decrease the duration ofepisodes of diarrhoea. The results of this study show thatover 90 per cent of the calves with diarrhoea had less than8 g/l of immunoglobulins in their serum (a level which is

generally considered to be too low to provide adequate pas-sive immunity), and that more than 50 per cent of them hadless than 4 g/l. More than 10 g/l is considered to be necessaryto provide ideal passive immunity (Besser and others 1991).These results indicate that it is important to ensure that neo-natal dairy calves in Switzerland receive adequate quantitiesof colostrum.

The results suggest that the rapid commercial tests forfield use are satisfactory for the detection of C parvum androtavirus in faecal samples. There were too few cases ofBCVand E coliK99 for the results of the other two tests to be inter-preted. The use of rapid tests solely for the two most prevalentpathogens cannot be recommended, because it is importantto investigate all the possible causes in herds with neonatalcalf diarrhoea; tests not only for rotavirus and C parvum but

also for BCV and E coli should be included in investigationsof diarrhoea in young calves.

The results of this study show that rotavirus and C parvumare both widely prevalent in Swiss dairy herds in neonatalcalves with diarrhoea. It is important to identify the infec-tious agents involved so that a suitable approach to the con-trol of the disease can be taken, and appropriate advice oncolostrum feeding, calf nutrition, hygiene and therapeuticregimens can be given (Scott and others 2004). The low lev-els of serum immunoglobulins in most of the calves indicatethat they had received insufficient colostrum.

ACKNOWLEDGEMENTS

The authors thank the veterinary practitioners for their helpwith sample collection and the technical staff for the labora-tory work. The rapid tests used in this study were in partprovided by Veterinaria.

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BENNETT, S., WOODS, T., LIYANAGE, W. M. & SMITH, D. L. (1991) A

animals (Garber and others 1994, Lentze and others 1999,Naciri and others 1999, De la Fuente and others 1999, Garciaand others 2000, Lefay and others 2000, Joachim and others2003, Trotz-Williams and others 2005, Haschek and others2006, Singh and others 2006). A strong and highly signifi-cant association between infection with C parvum and theoccurrence of diarrhoea has been observed in studies byNaciri and others (1999), Joachim and others (2003), Trotz-Williams and others (2005), Singh and others (2006) and

Haschek and others (2006). Calves shedding oocysts have athree times higher risk of being diarrhoeic than uninfectedcalves. A highly significant association between the numbersof oocysts being shed and the presence of diarrhoea has alsobeen suggested (Trotz-Williams and others 2005). The preva-lence ofC parvum in calves up to four weeks of age has prob-ably been underestimated. Not all laboratories have includedthis parasite in their routine test panel and some researchershave considered cryptosporidiosis to be of minor impor-tance. Although cryptosporidia are now acknowledged asprimary pathogens, not all veterinarians seem to be aware oftheir importance (Joachim and others 2003). In the presentstudy, 286 per cent of the diarrhoeic calves were shedding theorganism alone, but it was not the most prevalent infectiousagent associated with diarrhoea in the calves because rota-

virus was detected more frequently. However, the estimatesof prevalence had broadly overlapping confidence intervals,indicating that rotavirus and C parvum were of similar sig-nificance.

The relatively low prevalence of BCV agrees with theresults of other studies in Switzerland (Busato and others1998, Luginbhl and others 2005), and similar observationshave been made in Sweden (Bjrkman and others 2003).No classical cases of neonatal diarrhoea caused byE coliK99were observed in either of these studies. In contrast, BCVappeared to be of major importance in Austria (Haschekand others 2006). The results of this study do not support animportant role for BCV in causing diarrhoea in these calves.However, BCV is known to infect calves up to three monthsof age (Scott and others 2004), whereas the mean age ofthe calves was only about eight days. It is possible that BCVwould have been more prevalent in older calves. The resultsof the study should only be extrapolated to older calves withcaution.

The relationship between the serum immunoglobulinconcentration of neonatal calves and their risk of developingdiarrhoea is controversial. Some authors have observed a clearcorrelation between diarrhoea and low levels of serum immu-noglobulin (Barrington and others 2002, Lipp 2005), whereasothers have observed no correlation (Donovan and others1998, Gutzwiller 2002). The results of a survey by Gutzwiller(2002) indicated that high blood levels of maternal antibod-ies were of minor importance for the protection of calvesagainst diarrhoea caused by viruses and cryptosporidia; itwas hypothesised that immunoglobulins have to be presentin the gut rather than in the blood in order to protect calvesfrom viral enteritis. Donovan and others (1998) found thatlow serum immunoglobulin levels in newborn calves were asignificant risk factor for septicaemia and pneumonia, but

TABLE 4: Mean (95 per cent confidence interval [CI]) herd prevalences of the four infectiousagents calculated for 48 herds from which at least two samples were available

Herd prevalence (%) calculated on the basis of results fromInfectious agents Two or three calves in each herd First two calves only in each herd

Cryptosporidium parvum 417 (272-561) 354 (214-495)

Rotavirus 521 (374-667) 375 (233-517)Bovine coronavirus 21 (0-63) 0Escherichia coliK99 21 (0-63) 21 (0-63)

Calveswithdiarrhoea(%)

50

40

30

20

10

00-2 >2-4 >4-6 >6-8 >8-10 >10

Immunoglobulin concentration (g/l)

FIG 1: Percentages of the 147 calves with diarrhoea that haddifferent ranges of immunoglobulin concentration in theirserum


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INFECCIOSAS Prevalencia Agentes Patogenos Diarreas Neonatales