Studies on Calf Diarrhoea in Mozambique: Prevalence of Bacterial Pathogens
© The Author(s) 2002
Received: 14 May 2003
Accepted: 19 October 2003
Published: 31 March 2004
The prevalence of diarrhoea in calves was investigated in 8 dairy farms in Mozambique at 4 occasions during 2 consecutive years. A total of 1241 calves up to 6 months of age were reared in the farms, and 63 (5%) of them had signs of diarrhoea. Two farms had an overall higher prevalence (13% and 21%) of diarrhoea. Faecal samples were collected from all diarrhoeal calves (n = 63) and from 330 healthy calves and analysed for Salmonella species, Campylobacter jejuni and enterotoxigenic Escherichia coli (ETEC). Salmonella spp. was isolated in only 2% of all calves. Campylobacter was isolated in 11% of all calves, irrespective of health condition, and was more frequent (25%) in one of the 2 diarrhoeal farms (p = 0.001). 80% of the isolates were identified as C. jejuni. No ETEC strains were detected among the 55 tested strains from diarrhoeal calves, but 22/55 (40%) strains from diarrhoeal calves and 14/88 (16%) strains from healthy calves carried the K99 adhesin (p = 0.001). 6,757 E. coli isolates were typed with a biochemical fingerprinting method (the PhenePlate™) giving the same E. coli diversity in healthy and diarrhoeal calves. Thus it was concluded: i) the overall prevalence of diarrhoea was low, but 2 farms had a higher prevalence that could be due to an outbreak situation, ii) Salmonella did not seem to be associated with diarrhoea, iii) Campylobacter jejuni was common at one of the 2 diarrhoeal farms and iv) ETEC strains were not found, but K99 antigen was more prevalent in E. coli strains from diarrhoeal calves than from healthy, as well as more prevalent in one diarrhoeal farm.
Keywordsbacteria calf diarrhoea E. coli Campylobacter Salmonella, prevalence dairy ETEC K99.
Studier av kalve med diarré i Mozambique: Prevalens av bakterie patogener.
Prevalensen av diarré hos kalvar undersöktes på åtta mjölkproducerande gårdar i Mozambique vid fyra tillfällen under 2 konsekutiva år. Totalt uppföddes 1 241 kalvar upp till 6 månaders ålder på gårdarna och 63 (5%) av dessa hade tecken på diarré. Två gårdar uppvisade en hög prevalens (13% och 21% ) av diarré. Fekala prover insamlades från alla kalvar med diarré (n = 63) och från 330 friska kalvar. Proverna analyserades med avseende på förekomst av Salmonella spp., Campylobacter jejuni och enterotoxinbildande E. coli (ETEC). Salmonella spp. isolerades hos bara 2% av alla kalvar. Campylobacter isolerades i 11% av alla kalvar, oberoende av hälsotillstånd och påvisades oftare (25%) i en av de två gårdarna med ökad diarréförekomst (p=0.001). 80% av isolaten identifierades som C. jejuni. Inga ETEC stammar påvisades bland de 55 testade E. coli stammarna från kalvar med diarré, men 22/55 (40%) stammar från kalvar med diarré och 14/88 (16%) stammar från friska kalvar uppvisade K99 adhesin (p=0.001). Vidare typades 6 757 isolat av E. coli med hjälp av en biokemisk fingerprinting metod (PhenePlateTM). Samma diversitet erhölls bland kalvar med och utan diarré.
Det konkluderas att i) den totala frekvensen av diarré var låg men 2 gårdar uppvisade högre frekvenser, vilket kunde tyda på lokala utbrott; ii) Salmonella tycktes inte vara associerad med diarré; iii) Campylobacter var vanlig på en av de 2 gårdarna med diarréproblem; och iv) ETEC påvisades ej men K99 antigen påvisades oftare hos E. coli stammar isolerade från kalvar med diarré än från friska kalvar, liksom oftare.
Keywordsbacteria calf diarrhoea E. coli Campylobacter Salmonella, prevalence dairy ETEC K99.
Cattle rearing is a tradition in Mozambique. It plays an important role to the country's economy and social welfare. Because of the presence of Tse-Tse fly in the central and northern parts of the country the cattle population is mainly concentrated to southern provinces. Among the factors, which have been hindering cattle production in Mozambique, mortality of calves is one that causes major concern. Presence of infectious agents, poor management and poor nutrition are some of the factors which can be pointed out as causes of calf disease and mortality. However, there is a lack of data on the role of infectious disease in calf morbidity and mortality in Mozambique. The common conditions affecting calves are merely described as diarrhoea and/or pneumonia without identification of their aetiology. The number of cases of diarrhoea is normally higher during the rainy seasons, from October/November to March than during the dry seasons, from March to October.
Diarrhoea in calves can be caused by a variety of pathogens including bacteria, viruses, protozoa and intestinal parasites. Among bacteria, enterotoxigenic Escherichia coli (ETEC) and Salmonella are known to be the most common and economically important agents , but other bacteria, e.g. Campylobacter spp. have also been identified as cause of enteric disease and diarrhoea in calves [12, 34, 28]. The 2 latter groups also contain important human pathogens that may cause outbreaks of food-borne diseases  and thus are of high public health importance. In acute neonatal diarrhoea, an important disease of calves, 4 micro-organisms in particular, are of widespread occurrence and proven enteropathogenicity: rotavirus, coronavirus, cryptosporidia and enterotoxigenic E. coli (ETEC) [2, 27, 25].
Two of the more prominent virulence factors identified for ETEC strains are (i) expression of fimbrial (pili) antigens that enables the bacteria to adhere to and to colonise the luminal surface of the small bowel and (ii) elaboration of one or more enterotoxins that influence intestinal secretion of fluids . The most common observed fimbriae on ETEC from calves with diarrhoea are F5, also named K99 and F41, but strains with F165 fimbriae have also been isolated . K99 antigen is a fimbrial adhesin distinct from the capsular polysaccharide K antigens . Two biological classes of enterotoxins are produced by ETEC: heat labile (LT) and heat stable (STa and STb) [13, 14, 17, 38]. Most bovine ETEC produce STa enterotoxin and K99 fimbriae [26, 19].
The aim of this study was to investigate the prevalence of diarrhoea in dairy farms in Mozambique and the prevalence of Salmonella, Campylobacter jejuni and ETEC in diarrhoeic and healthy calves. We were also interested to investigate the prevalence of fimbrial antigen K99 among the E. coli isolates.
Materials and methods
Herds studied and sampling protocol
Eight dairy farms (F1 to F8) were chosen for this study, 5 of them located in 2 southern provinces: Maputo (F1 to F3) and Gaza (F4 and F5); 2 in central provinces: Sofala (F6) and Manica (F7) and one (F8) in the northern province of Nampula. The selected farms have a level of organisation which allow gathering of data and collecting samples of reasonable quality for research purposes and they are at easy reach to the laboratory. For some of the farms we also had data produced from a previous survey on bovine virus diarrhoea virus (BVDV), rotavirus and coronavirus in calf diarrhoea [5, 6].
The sampling was carried out on 4 occasions: during rainy and dry seasons in 1994 (S1 and S2) and during rainy and dry seasons in 1995 (S3 and S4). Management of the calves in the farms with variations depending on the conditions of the farm was in general as follows: calves were left to suckle their dams up to 3 days after birth. They were then housed in individual boxes and fed with milk and wheat barn. Hay and water were offered ad libitum after removal from the dam. At one month of age they were moved to a common pen where they were kept up to the age of 4 to 6 months, and milk was gradually replaced by forage and mixtures of cereal by-products. The age of the calves on sampling occasion varied from 1 week to 6 months, and their breed was a mixture of Holstein Friesian and local "Landim" breed. Diarrhoea was considered if faeces were semi-liquid to liquid, with or without other abnormal characteristics such as presence of blood or mucous.
Any calf with faeces whithout these characteristics was considered non-diarrhoeic or healthy. All samples were collected by the same veterinarian who also decided whether the calf was diarrhoeic or healthy upon stool examination. On each sampling occasion, all diarrhoeic calves and about 30% of the healthy calves were sampled from each farm. Faecal samples were collected directly from the rectum of the calf with a plastic glove. The samples were cultured on the same day or stored at 4°C and cultured within 3 days.
Cultures and bacterial isolation
For isolation of Salmonella strains, a small portion of the faecal samples was inoculated into Selenite-F and Tetrationate broths and streaked out on MacConkey and brilliant green agar after overnight incubation at 37°C. Suspected colonies were subjected to biochemical testing according to . Slide agglutination test was used for identification of serovars according to the Kauffmann-White Schema .
For isolation of Campylobacter, a small portion of faecal samples was suspended in 0.85% saline, filtered through 0.45 mm Milipore filter papers. Filters were then cultured in Preston broth (Oxoid) and incubated overnight at 37°C. Cultures were then inoculated onto Preston agar plates and incubated for 48 h in an atmosphere of 5% oxygen, 10% CO2 and 85% nitrogen. Suspected colonies were identified based on their motility, hydrolysis of sodium hippurate and sensitivity to cefalotin and nalidixic acid.
For isolation of E. coli strains, faecal samples were inoculated onto MacConkey agar plates which were incubated at 37°C for 18–24 h. Lactose positive colonies were confirmed as E. coli using the standard biochemical tests recommended by . Each faecal sample was also cultured on 5% sheep blood agar, incubated at 37°C for 24 h and inspected for the presence of other bacterial pathogens, e.g. Bacillus spp., Corynebacterium spp., Pseudomonas aeruginosa.
Analysis of E. coli
Typing of E. coli isolates. Twenty-four E. coli like colonies from each faecal sample were phenotyped with the PhenePlate™ rapid screening system . Each Phene Plate (the PhP-RE plates, PhPlate AB, Sweden, http://www.phplate.se) contains 8 rows of 12 dehydrated reagents, selected to yield a high discrimination within E. coli. In the first column of wells, 300 μl of growth media containing 1% (w/v) proteose peptone and 0.11% (w/v) bromothymol blue were inoculated. In the remaining wells 150 μl of the medium were inoculated. Bacterial isolates were inoculated into the first well of each row, mixed and 25 μl of bacterial suspension were inoculated into the remaining wells of the same row. Plates were incubated at 37°C and the absorbance at 620 nm was measured after 16, 40, and 64 h. The results were automatically read by a microplate reader. Storing of data, calculations of diversity and cluster analysis were performed by the PhenePlate™ software (PhPlate AB). According to data from biochemical fingerprinting, the isolates could be subdivided into different phenotypes. PhP-types with more than one isolate were called common (C) and those with only one isolate were called single (S) PhP-types.
Testing of ETEC. Isolates representing common PhP types present in the diarrhoeal and healthy calves were selected and tested for K99 antigen. E. coli isolates were streaked on minimal glucose agar for expression of K99 antigen. Plates were then incubated at 37°C for 24 h, and a single isolated colony was used for slide agglutination using K99 antiserum, and agglutination was observed under light microscope. Detection of STa and LT on the common PhP types from diarrhoeal calves was performed by PCR . Positive and negative controls were included in both tests which were performed at the National Veterinary Institute (SVA), Uppsala, Sweden.
The Chi-square test was used with Yate's correction when applicable. Calculations were perfomed with Statgraphics, version 2.6, Statistical Graphics Corporation, STSC, USA.
Prevalence of calves with diarrhoea and no. of samples from each farm.
Total no. of calves in the herd
No. of calves with diarrhoea (%)
Number of samples
A total of 393 faecal samples were collected from healthy (n = 330) and diarrhoeal (n = 63) calves. Salmonella (n = 8) was found in 3 farms in both healthy (n = 5) and diarrhoeal (n = 3) calves. According to serotyping they belonged to 5 different serovars: S. Ohio, S. Newport and S. Uganda in diarrhoeal calves and S. Arhus, S. Newport, S. Typhimurium and S. Uganda in healthy calves.
Prevalence of Salmonella spp. and Campylobacter spp. in calves.
No. of calves with diarrhoea (%)
No. of samples
No. of samples with Salmonella (%)
No. of samples with Campylobacter (%)
E. coli was found in 76% of the calves, and no significant difference between prevalence in healthy and diarrhoeal calves was observed. A total number of 6,757 isolates from 252 healthy (5,670 isolates) and from 47 diarrhoeal calves (1,087 isolates) were subject to typing with the PhenePlate™ system. Most faecal samples showed the presence of one dominating PhP-type and a few single types. The diversity among E. coli isolates in diarrhoeal calves was similar to that of healthy calves (0.949 and 0.958 respectively).
Escherichia coli strains tested for K99 antigen.
No. of strains tested
No. of K99 positive strains (%)
The presence of genes for enterotoxins STa and LT was investigated by PCR on the same selected 55 strains from diarrhoeal calves and, since all the results were negative, the isolates from healthy calves were not further assayed for STa and LT genes.
The prevalence of diarrhoea among all calves in this study was 5% (Table 1). Similar prevalences have been found by  and  in Swedish herds. Results from studies in other countries show higher prevalences of diarrhoea [32, 37, 24]. In Mozambique,  reported an overall prevalence of diarrhoeic calves as high as 36% but this percentage includes values of prevalences of diarrhoea from other farms not included in the present study. In our study, diarrhoea in calves was observed in 6 of the 8 farms studied. Farms F3 and F6 were the farms with the highest mean prevalences (Table 1), and almost 90% of the cases occurring in seasons S1 and S2 of the study (Fig. 1). This might indicate an outbreak situation during that period. Possibly the relatively big size of these 2 farms, reared in an intensive system with unhygienic calving accommodation, makes them more prone to outbreaks of infectious diseases. The lower incidence of diarrhoea in these farms during 1995 could thus reflect a more "normal" situation with no outbreaks of infection. Also, diarrhoeal outbreaks in calves seem to be more common in the rainy season, and the rainfall in 1994 was more intense than in 1995. Farms F7 and F8 were the farms with no diarrhoea which may have been due to the semi-intensive rearing system in those farms (animals are left grazing at daytime and kept in a kraal at night).
The diarrhoeal syndrome has a complex etiopathogenesis, because various infectious agents, either alone or in combination, may be associated with field outbreaks. In addition, environmental, management, and nutritional factors influence the severity and outcome of the disease. Rotavirus, coronavirus, enterotoxigenic E. coli and Crytosporidium parvum are the 4 major pathogens associated with neonatal calf diarrhoea worldwide. These organisms are responsible for the vast majority (75%–95%) of enteric infections in neonatal calves worldwide . Moreover, Salmonella spp. may be particularly important in dairy calves [7, 35, 46]. The ETEC strains are often associated with diarrhoea in 2 to 3-day-old calves .
None of the diarrhoeal pathogens investigated here could be clearly associated with diarrhoea in the calves. The involvement of infectious agents other than those investigated is also possible.  reported the presence of serum antibodies to Bovine virus diarrhoea virus (BVDV) in dairy and beef calves in Mozambique. The higher prevalences in their study, 92%, 87% and 86%, were found in farms F1, F2 and F3 of our study. In another study by  in the same farms, a significant statistical association of diarrhoea and the presence of group A rotavirus antigen in faecal samples from calves was shown and bovine coronavirus infections were found to be common.  found bovine enteric coronavirus as the major infectious cause of neonatal calf diarrhoea in some Ethiopian dairy herds. In a survey on faecal samples from 218 diarrhoeic dairy calves by Cryptosporidium and Rotavirus were the most commonly detected agents. Since our study was aimed at investigating bacterial pathogens, these kinds of infectious agents were not searched for. Most of the samples (87%) without Enterobacteria and Campylobacter came from farms F3 and F6, the 2 farms with high prevalences of diarrhoea. This strengthens our previous suggestion that other pathogens than the ones studied here had caused the diarrhoea. However, the fact that the bacterial pathogens investigated were not found in those samples may also have been due to other factors, e.g. shedding of the agent did not coincide with the sampling occasion, failure to detect the causative agent, some cases of diarrhoea might not be associated with infectious agents but, instead, due to management or to nutritional factors.
Salmonella was only isolated from 2% of the 393 animals studied, and it was not possible to associate the finding with the occurrence of diarrhoea. In some European countries Salmonella has been identified as a widespread diarrhoeal agent in dairy calves [35, 4] and the importance for human health of animal reservoirs of Salmonella species has long been recognised . In Africa,  could not detect Salmonella excretion on any of 108 diarrhoeic dairy calves in Ethiopia, although earlier studies in Addis Abeba had reported S. Dublin and S. Typhimurium as causes of disease in calves . C. jejuni was isolated in 11% of both diarrhoeic and healthy calves. An equal occurrence of Campylobacter spp. in diarrhoeic and normal calves has also been observed in England and Scotland [40, 41], which supports suggestions that the association of Campylobacter with enteritis in cattle remains circumstantial as they are common in both healthy and diarrhoeic calves [3, 33]. In our investigation, however, we found a high percentage (25%) of Campylobacter in one of the 2 considered as high prevalence farms (Table 2, farm F3), all of which but one were identified as C. jejuni. This might indicate an association of C. jejuni with an earlier outbreak of calf diarrhoea in this particular farm. Our study thus indicates that the bovine reservoirs may be a potential source of C. jejuni food borne disease in humans. Outbreaks of C. jejuni enteritis in persons have been associated with bovine faecal contamination of unpasteurized milk .
E. coli was excreted by more than half of the diarrhoeic calves, but since this organism is regarded as a normal member of the intestinal flora of warm blooded animals, the finding of E. coli as such was regarded as indicative of a normal flora. Enterotoxin producing E. coli is a common cause of diarrhoea in animals as well as in humans [42, 45, 23, 16]. The diversities of E. coli isolated in healthy and diarrhoeal calves were roughly the same. This fact speaks against that diarrhoea in several calves was caused by single pathogenic strains of E. coli, like ETEC, since this should have resulted in lowered diversities in these calves. A close correlation between enterotoxigenicity and the presence of the K99 antigen has been confirmed by some authors [22, 39], but  have reported non-enterotoxigenic E. coli possessing the K99 antigen. In the present study, enterotoxins STa and LT were not detected in any E. coli isolates from the diarrhoeal calves, however, 40% of these isolates were K99 positive. Although we did find a higher prevalence of K99 positive in isolates from diarrhoeal calves, it is difficult to draw conclusions as to an etiological role of K99 from these findings. Furthermore,  found that LT- ST- K99+ strains may exist in healthy calves.
In conclusion: the overall prevalence of diarrhoea was low (5.1%) but 2 farms had high prevalence (13% and 21%); Salmonella was rare and did not seem to be associated with diarrhoea; C. jejuni was more common, and had a high prevalence at one diarrhoeal farm; and STa and LT producing E. coli (ETEC) were not found but K99 antigen was more prevalent in E. coli strains from diarrhoeal than from healthy calves and was furthermore associated with one diarrhoeal farm.
We express our gratitude to: Professor Olof Holmberg for his excellent contribution on the first proposal of this study; Associate professor Anders Franklin and Verena Rehbinder at the National Veterinary Institute (SVA), Uppsala, Sweden, for the detection of STa and LT enterotoxins; Dr Eva Berndston at Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden, for helping on the identification of Campylobacter isolates and Sigbrit Mattsson at SVA, for the detection of the adhesin factor K99 and the identification of the Salmonella serovars. We also thank Boel Brändström for her prompt and kind technical assistance whenever it was needed at SVA. The assistance from staff at the Bacteriology sector at the National Veterinary Research Institute (INIVE), Maputo, from staff at the Provincial Veterinary Laboratories, from workers in the farms and from the Field Veterinary Officers in Mozambique is highly appreciated. This study was supported by the Swedish Agency for Research Cooperation with Developing countries (SIDA/SAREC) within the project MOZ-BIL 20.
- Abraham G, Roeder PL, Zewdu R: Agents associated with neonatal diarrhea in Ethiopian dairy calves. Trop Anim Hlth Prod. 1992, 24: 74-80. 10.1007/BF02356948.View ArticleGoogle Scholar
- Acres SD, Laing CJ, Saunders JR, Radostitis OM: Acute undifferentiated neonatal diarrhea in beef calves I. Occurrence and distribution of infectious agents. Canad J Comp Med. 1975, 39: 116-132.Google Scholar
- Allsup TN, Hunter D: The isolation of vibrio from diseased and healthy calves. Laboratory Vet Rec. 1973, 93: 389-392.View ArticlePubMedGoogle Scholar
- Anonymous: Trends and sources of zoonotic agents in animals, feedstuffs, food and man in the European Union. Community Reference Laboratory for the Epidemiology of Zoonoses B, Berlin, Germany. 1997, 163-164.Google Scholar
- Baule C, Banze J: Bovine virus diarrhoea virus infections in calves from selected farms in Mozambique. Bull Anim Hlth Prod Afr. 1994, 42: 279-286.Google Scholar
- Baule C, Svenson L, Sigstam G, Alenius S: Rotavirus and Coronavirus infections in calves in Mozambique. Bull Anim Hlth Prod Afr. 1995, 43: 1-9.Google Scholar
- Bulgin MS, Anderson BC, Ward ACS, Evermann JF: Infectious agents associated with neonatal calf disease in southwestern Idaho and Oregon. J Am Vet Med Assoc. 1982, 180: 1222-1226.PubMedGoogle Scholar
- Contrepois M, Fairbrother JM, Kaura YK, Girardeau JP: Prevalence of CS31A and F165 surface antigens in Escherichia coli isolates from animals in France, Canada and India. FEMS Microbiol Lett. 1989, 59: 319-323. 10.1111/j.1574-6968.1989.tb03132.x.View ArticleGoogle Scholar
- Cowan ST, Steel KJ: Manual for identification of medical bacteria. 1965, Cambridge University. Press, LondonGoogle Scholar
- De la Fuente R, Garcia A, Ruiz-Santa-Quiteria JA, Luzón M, Garcia SS, Orden S, Gomes-Bautista MM: Proportional morbidity rates of enteropathogens among diarrheic dairy calves in central Spain. Prev Vet Med. 1998, 34: 145-152. 10.1016/S0167-5877(98)00077-4.View ArticleGoogle Scholar
- De Rycke J, Bernard S, Laporte J, Naciri M, Popoff MR, Rodolakis MR: Prevalence of various enteropathogens in the feces of diarrheic and healthy calves. Ann Rech Vét. 1986, 17: 159-168.PubMedGoogle Scholar
- Firehammer BD, Myers LL: Campylobacter fetus subsp. jejuni: its possible significance in enteric disease of calves and lambs. Am J Vet Res. 1981, 42: 918-922.PubMedGoogle Scholar
- Gaastra W, de Graaf FK: Host- specific fimbrial adhesins of noninvasive enterotoxigenic Escherichia coli strains. Microbiol Rev. 1982, 46: 129-161.PubMed CentralPubMedGoogle Scholar
- Gross RJ, Rowe B: Escherichia coli diarrhea. J Hyg. 1985, 95: 531-550.PubMed CentralView ArticlePubMedGoogle Scholar
- Gyles CL: Escherichia coli. Pathogenesis of Bacterial Infections in Animals. Edited by: Gyles CL, Thoen CO. 1986, Iowa State University Press Ames, Iowa, 114-131. 1,Google Scholar
- Holland RE: Some infectious causes of diarrhea in young farm animals. Microbiol Rev. 1990, 3: 345-375.Google Scholar
- Holmgren J: Toxins affecting intestinal transport processes. The virulence of Escherichia coli: reviews and methods. Edited by: Sussman M. 1985, Academic Press, Inc., New York, 177-191.Google Scholar
- House JA: Economic impact of Rotavirus and other neonatal agents of animals. J Am Vet Med Assoc. 1978, 173: 573-576.PubMedGoogle Scholar
- Kaeckenbeeck A: Toxines des Escherichia coli des diarrhées du veau. Resistence and pathogenic plasmids. Edited by: Pohl P, Leunen J. 1981, CEC Seminar, NIVR, Brussels, 275-Google Scholar
- Kauffmann F: Serological Diagnosis of Salmonella-Species. Kauffmann-White-Schema. 1972, 1Google Scholar
- Kühn I, Möllby R: The PhP RS system – A simple microplate method for studying coliform bacterial populations. J Microbiol Meth. 1993, 17: 255-259. 10.1016/0167-7012(93)90054-L.View ArticleGoogle Scholar
- Larivière S, Lallier R, Morin M: Evaluation of Various Methods for Detection of Enteropathogenic Escherichia coli in Diarrheic Calves. Am J Vet Res. 1979, 40: 130-134.PubMedGoogle Scholar
- Levin MM: Escherichia coli that cause diarrhea: Enterotoxigenic, Enteropathogenic, Enteroinvasive, Enterohemorrhagic, and Enteroadherent. J Infect Dis. 1987, 155: 377-389.View ArticleGoogle Scholar
- McDonough SP, Stull CL, Osburn BI: Enteric pathogens in intensively reared veal calves. Am J Vet Res. 1994, 55: 1516-1520.PubMedGoogle Scholar
- Moon HW, McClurkin AW, Isaacson RE, Pohlenz J, Skartvedt SM, Gillette KG, Baetz AL: Pathogenic relationships of Rotavirus, Escherichia coli, and other agents in mixed infections in calves. J Am Vet Med Assoc. 1978, 173: 577-583.PubMedGoogle Scholar
- Moon HW, Whipp SC, Skartvedt SM: Etiologic diagnosis of diarrheal diseases of calves: frequency and methods for detecting enterotoxin and K99 production by Escherichia coli. Am J Vet Res. 1976, 37: 1025-1029.PubMedGoogle Scholar
- Morin M, Lariviere S, Lallier R: Pathological and microbiological observations made on spontaneous cases of acute neonatal calf diarrhea. Can J Comp Med. 1976, 40: 228-240.PubMed CentralPubMedGoogle Scholar
- Myers LL, Firehammer BD, Border MM, Shop DS: Prevalence of enteric pathogens in the feces of healthy beef calves. Am J Vet Res. 1984, 45: 1544-1548.PubMedGoogle Scholar
- Olsson SO, Viring S, Emanuelsson U, Jacobsson SO: Calf diseases and mortality in Swedish dairy herds. Acta Vet Scand. 1993, 34: 263-269.PubMedGoogle Scholar
- Orskov I, Orskov F, Smith HW, Sojka WJ: The establishment of K99, a thermolabile, transmissible Escherichia coli K antigen, previously called "Kco", possessed by calf and lamb enteropathogenic strains. Acta Path Microbiol Scand sect B. 1975, 83: 31-36.Google Scholar
- Pegram RG, Roeder PL, Hall MLM, Rowe B: Trop Animal Hlth Prod. 1981, 13: 203-207. 10.1007/BF02237926.View ArticleGoogle Scholar
- Pohjola S, Oksanen H, Neuvonen E, Veijalainen P, Henriksson K: Certain enteropathogens in calves of Finnish dairy herds with recurrent outbreaks of diarrhea. Prev Vet Med. 1986, 3: 547-558. 10.1016/0167-5877(86)90033-4.View ArticleGoogle Scholar
- Prescott JF, Bruin-Mosch CW: Carriage of Campylobacter jejuni in healthy diarrheic animals. Am J Vet Res. 1981, 42: 164-165.PubMedGoogle Scholar
- Prescott JF, Munroe DL: Campylobacter jejuni enteritis in man and domestic animals. J Am Vet Med Assoc. 1982, 160: 511-518.Google Scholar
- Reynolds DJ, Morgan JH, Chanter N, Jones PW, Bridger JC, Debney TG, Bunch KJ: Microbiology of calf diarrhea in southern Britain. Vet Rec. 1986, 119: 34-39.View ArticlePubMedGoogle Scholar
- Robinson DA, WJ E, GL G, Matchett AA, Robertson L: Campylobacter enteritis associated with consumption of unpasteurised milk. Br Med J. 1979, 1: 1171-1173.PubMed CentralView ArticlePubMedGoogle Scholar
- Roy JHB: The calf. 1990, Butterworths, London, 53-117. 5Google Scholar
- Scotland SM, Gross RJ, Rowe B: Laboratory tests for enterotoxin production, enteroinvasive and adhesion in diarrhoegenic Escherichia coli. The virulence of Escherichia coli: reviews and methods. Edited by: Sussman M. 1985, Academic Press, Inc., New York, 395-405.Google Scholar
- Sherwood D, Snodgrass DR, Lawson GHK: Prevalence of enterotoxigenic Escherichia coli in calves in Scotland and northen England. Vet Rec. 1983, 113: 208-212.View ArticlePubMedGoogle Scholar
- Snodgrass DR, Sherwood D, Terzolo HG, Synge BA: A field survey of the aetiology of neonatal calf diarrhea. Proc XIIth World Congr on Diseases of Cattle. Utrecht Netherlands. 1982, 1: 380-384.Google Scholar
- Snodgrass DR, Terzolo HR, Sherwood D, Campbell I, Menzies JD, Synge BA: Aetiology of diarrhea in young calves. Vet Rec. 1986, 119: 31-34.View ArticlePubMedGoogle Scholar
- Tzipori S: The aetiology and diagnosis of calf diarrhoea. Vet Rec. 1981, 108: 510-514.View ArticlePubMedGoogle Scholar
- Tzipori S: The relative importance of enteric pathogens affecting neonates of domestic animals. Adv vet Sci Comp Med. 1985, 29: 103-206.PubMedGoogle Scholar
- Viring S, Olsson SO, Alenius S, Emanuelsson U, Jacobsson SO, Larson B, Linde N, Uggla A: Studies of Enteric Pathogens and Gamma-Globulin levels of Neonatal Calves in Sweden. Acta Vet Scand. 1993, 34: 271-279.PubMedGoogle Scholar
- Wadström T, Baloda SB: Molecular aspects on small bowel colonization by enterotoxigenic Escherichia coli. Microecol Ther. 1986, 16: 243-255.Google Scholar
- Waltner-Toews D, Martin SW, Meek AH: An epidemiological study of selected calf pathogens on Holstein dairy farms in southwestern Ontario. Can J Vet Res. 1986, 50: 307-313.PubMed CentralPubMedGoogle Scholar
- WHO BW: Enteric infections due to Campylobacter, Yersinia, Salmonella and Shigella. 1980, 58: 519-537.Google Scholar
- Woodward MJ, Carroll PJ, Wray C: Detection of entero- and vercyto-toxin genes in Escherichia coli from diarrhoeal disease in animals using the polymerase chain reaction. Vet Microbiol. 1992, 31: 251-261. 10.1016/0378-1135(92)90083-6.View ArticlePubMedGoogle Scholar