Factors associated with microbiological quality of bovine colostrum in Colombian dairy herds

Journal Pre-proof Factors associated with microbiological quality of bovine colostrum in Colombian dairy herds Victor Guzmán, Julián Reyes-Vélez, Ibrahim Elsohaby, Martha Olivera-Angel PII:

S0958-6946(20)30040-6

DOI:

https://doi.org/10.1016/j.idairyj.2020.104670

Reference:

INDA 104670

To appear in:

International Dairy Journal

Received Date: 14 October 2019 Revised Date:

2 February 2020

Accepted Date: 4 February 2020

Please cite this article as: Guzmán, V., Reyes-Vélez, J., Elsohaby, I., Olivera-Angel, M., Factors associated with microbiological quality of bovine colostrum in Colombian dairy herds, International Dairy Journal, https://doi.org/10.1016/j.idairyj.2020.104670. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Ltd. All rights reserved.

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Factors associated with microbiological quality of bovine colostrum in Colombian dairy

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herds

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Victor Guzmán a, Julián Reyes-Vélez a,*, Ibrahim Elsohaby b,c, Martha Olivera-Angel a

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a

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Research Group. Calle 70 No. 52-21, Medellín, Colombia.

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b

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Medicine, Zagazig University, Zagazig City, Sharkia Province, Egypt

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c

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Island. Charlottetown, Canada.

Veterinary Medicine School, Faculty of Agrarian Sciences, University of Antioquia. Biogenesis

Department of Animal Medicine, Division of Infectious Diseases, Faculty of Veterinary

Department of Health Management. Atlantic Veterinary College, University of Prince Edward

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* Corresponding author. Tel.:

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E-mail address: [email protected] (J. Reyes-Vélez)

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_____________________________________________________________________________

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ABSTRACT

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The microbiological quality of colostrum and identify cow, calf and farm managemental factors

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associated with colostrum hygiene in Colombian dairy herds were determined. Colostrum

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samples (n = 255) from 44 herds were collected for bacteriological quality analysis. A survey

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about colostrum management was carried out for each birth event. Only 18% of the samples

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exceeded the threshold 100,000 cfu mL-1 for the total bacterial count (TBC), and more than

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54.5% of the herds have at least one colostrum sample above the TBC threshold. The total

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coliform count was higher than the threshold 10,000 cfu mL-1 in 24.3% of colostrum samples

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and 68.2% of herds. Associations between cow-calf factors and the colostrum hygiene were

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examined. The two-level logistic regression showed that the colostrum microbiological quality

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was influenced by suckling colostrum from mother, feeding colostrum with a bottle and when

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the colostrum came of large herds.

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______________________________________________________________________________

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1.

Introduction

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The microbiological quality of colostrum has been described as an essential factor for calf

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disease prevention. Bacterial contamination of colostrum leads to an increased risk of pathogen

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transfer and decreased absorption of immunoglobulin G (IgG) in the intestine (Lorenz, Mee,

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Earley, & More, 2011). The bacteria in colostrum bind to free immunoglobulins in the lumen of

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the intestine or directly can block the transport of the immunoglobulin molecules through the

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intestinal epithelial cells, interfering with the passive absorption of colostrum components and

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favoring failure of transfer of passive immunity (FTPI) (Godden, 2008). Microbial pathogen

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contamination of colostrum derived from the collection, milking techniques and storage can

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result in acute or chronic diseases (Fecteau, Baillargeon, Higgins, Paré, & Fortin, 2002; Godden

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et al., 2012).

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Bacterial contamination can be prevented through proper hygienic practices, such as

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udder and teat disinfection and the cleanliness of milking equipment, and other elements used to

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store and administer the colostrum (Fecteau et al., 2002). Moreover, heat treatment of colostrum

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at 60 °C for 30 min has been associated with reduced risk of calf illness and improved IgG

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concentrations (Godden et al., 2012). The total bacterial count (TBC) and total coliform count

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(TCC) in colostrum should be less than 100,000 and 10,000 total colony forming units per mL

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(cfu mL-1), respectively (McGuirk & Collins, 2004). However, the average of TBC and TCC in

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most of the herds often exceeds this threshold. One report showed that 82% of the samples

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analysed exceeded the upper limit of 100,000 cfu mL-1 (Godden, 2008). In another study, at least

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one type of pathogen microorganism was cultivated from 94.4% of the samples. A study carried

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out by Renaud et al. (2017), showed that the bacterial contamination of the utensils to supply

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colostrum, was frequent and that the visual assessment of these elements was a poor indicator of

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bacterial contamination. Literature about the bacteriological quality of bovine colostrum in Colombian dairy herds

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is limited. Therefore, the objectives of the present study were to determine the microbiological

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quality of colostrum consumed by calves in Colombian dairy herds from three regions of the

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country and to determine the effect of specific cow, calf and farm management factors on the

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hygienic quality of colostrum.

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2.

Materials and methods

2.1.

Herds and animals

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A total of 255 colostrum samples from 44 herds located at three different dairy producer

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regions (Antioquia, Boyacá and Cundinamarca) in Colombia were collected between October

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2017 and April 2018. Each herd was followed for six months to collect all the calving events.

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After each calving, the herds were followed for four weeks to collect individual calf information.

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All the herds enrolled were part of the Milk Quality Program (Biolactoseguridad), of Bayer

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Animal Health-Colombia. A general characterisation survey of the management factors of the

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newborn and colostrum was carried out in each herd. Additionally, individual information from

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each cow corresponding to the calf born was collected including breed, number of calving, dry

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period, and number of cows per herd. Also, individual information from calves such as calving

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ease, Cow-calf separation at birth, time staying with the cow, suckling from mother and feeding

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colostrum by bottle.

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2.2.

Samples and laboratory

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One colostrum sample per one calving event was collected, for an average of 5.8

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colostrum samples per herd, with a maximum of 22 and a minimum of one sample. A sample of

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30 mL of fresh colostrum consumed by each calf was collected by farm workers and preserved

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for analysis of bacterial contamination. The samples were frozen at the farm for 3 to 5 days until

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the project professionals transported it on a cooler box with ice bags to the University of

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Antioquia laboratory in Antioquia and LMV laboratory in Bogotá. All colostrum samples arrived

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frozen and were placed at –20 °C until testing. The TBC and TCC were determined by 3M

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aerobic colony count Petrifilm and 3M coliform count (CC) Petrifilm (3M, St. Paul, MN, USA),

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respectively. Three dilutions of 1:10 for petrifilm of mesophilic and 1:2 for petrifilm of coliforms

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and Escherichia coli were made with peptone water diluent 0.1%. It is recommended that

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colostrum contain <100,000 cfu mL-1 TBC and <10,000 cfu mL-1 TCC (McGuirk & Collins,

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2004).

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2.3.

Statistical analysis

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A descriptive analysis was performed for all the continuous and categorical predictors.

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Dichotomization of the TBC and TCC was performed based on the colostrum quality thresholds

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and used as outcomes in the bivariate analysis. A Chi-square and Fisher exact test were used to

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explore the associations between the colostrum quality outcomes and the categorical predictors at

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liberal P-value < 0.20. A two-level logistic model was used to explore any further association,

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adjusting by multiple variables. A backwards elimination process was used to elaborate the

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multivariate model at P-value <0.05. Marginal predictions were obtained for the log odds of the

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colostrum microbiological quality given the cow inventory and feeding from mother or bottle

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variables. Goodness of fit and the assumptions of the model were assessed accordingly. All the

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statistical analyses were carried out in STATA version 15.

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3.

Results

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The distributions of the colostrum microbiological results are presented in Table 1. Only

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18.1% of the colostrum samples and 54.5% of herds had TBC more than 100,000 cfu mL-1.

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However, TCC was more than 10,000 cfu mL-1 in 24.3% of the samples and 68.2% of the herds.

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There was a wide range of significant and non-significant associations between the TBC and

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TCC and each one of the calf, cow and herd level predictors (Table 2).

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The multivariate logistic regression showed three variables remaining in the final model,

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after the backwards elimination procedure (Table 3). The odds of bacterial contamination in

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colostrum feed to calves via suckling their mother was 15.82 higher than that feed by other

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methods. On the other hand, when the owner reported that the colostrum was bottle fed; the odd

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was 3.61 compared with other feeding practices. Although, the later variable was non-significant

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in the bivariate model, it forced into the final model due to the importance of this practice in the

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microbiological quality of colostrum. Regarding the cow inventory, the odds of bacterial

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contamination for larger herds (≥ 300 cows) was 4.61 times, when compared with smaller herds

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(< 100 cows). The marginal prediction of the log odds can be observed in Fig. 1. The herd

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variance was small (Estimate = 0.28, SE= 0.39); however, it was different from 0, showing a

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little clustering effect at the herd level.

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4.

Discussion

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The microbiological quality of colostrum was suboptimal in most of the samples

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analyzed and the microbiological contamination was a frequent finding, whereas 18.1% and

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24.3% of the colostrum samples had TBC and TCC greater than 100,000 cfu mL-1 and 10,000

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cfu mL-1, respectively. The presence of bacteria in the colostrum offered to the calves has been

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described as a disruptive factor of the systemic absorption of IgG molecules in the small

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intestine, and have a negative association with the IgG concentration (Godden, 2008; McGrath,

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Fox, McSweeney, & Kelly, 2016). These results were in agreement with another report from

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commercial dairy farms in Brazil, from which 24% of the colostrum samples were below the

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microbiological quality parameters and only 22.6% of colostrum samples met the recommended

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IgG concentration (Santos, Silva, Santos, & Bittar, 2017).

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Multiple risk factors have been reported to affect the bacterial contamination of

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colostrum (Fecteau et al., 2002) and different critical points during colostrum harvest have been

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described as well (Stewart et al., 2005). In the present study, two main feeding methods were

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observed amongst the herds naturally and artificially. Naturally fed colostrum was obtained

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directly from the mother and showed sub-optimal microbiological quality when compared with

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those fed with a bottle (which is artificially fed). This could be originated from non-adequate

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udder and teat hygiene. On the other hand, the lack of hygienic practices on the feeding utensils

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can also affect the TBC. In general, the colostrum harvest process has been reported as a critical

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control point for bacterial contamination (Stewart et al., 2005).

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The artificial rearing of calves requires from the farmer to provide to the calf with enough care and optimal management practices to ensure their health and welfare. The knowledge and

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experience of the personnel in the care of calves directly influences the results. It has been

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reported that the general attention of the hygiene provided by the calf feeding personnel may

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vary between the farms and can change over time (Fecteau et al., 2002). Larger herd size could

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have better practices; however, in our case, larger herd sizes were significantly associated with

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higher odds of having more bacterial load. In contrast, one study showed that herd size did not

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influence the bacteriological quality of colostrum (Houser, Donaldson, Kehoe, Heinrichs, &

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Jayarao, 2008). With the information collected, we did not find a plausible explanation for this

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condition, which invites us to propose new studies to deepen the differences in colostrum

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management that may be found at different herd sizes. This research is a contribution to the

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scarce literature about this subject in Colombian dairy herds, and for countries with similar dairy

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commercial systems in tropical areas. The inference of these results should be performed with

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caution, to similar dairy commercial systems in tropical high lands.

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5.

Conclusions

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In our work, we showed a great opportunity to improve the quality of the colostrum

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supplied to the calves, which should re-emerge in greater success in the passive transfer of

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immunoglobulins and increase the resilience to the disease. Implementing practices aimed at a

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hygienic harvest of colostrum either directly from the nipple or through bottles can positively

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impact the indicators. To achieve these objectives, it is mandatory to establish regular monitoring

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of hygienic and immunological quality of the colostrum to estimate the impact of these favorable

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practices.

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Acknowledgements

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The research work was endorsed by the Ethics Committee for Animal experimentation at

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the University of Antioquia Approval Number 120 of October 9, 2018. Thanks to the Veterinary

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medical staff of Bayer® Animal Health Colombia, the students of the University of La Salle in

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Bogotá and the students of the CES Medellín University, for their work and dedication and to the

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LMV laboratory and Doctor Víctor Cotrino for its availability and support. Special mention and

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acknowledgement to the SCCL company of Canada and the University of Prince Edward Island

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for its decisive support.

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References

194 195

Fecteau, G., Baillargeon, P., Higgins, R., Paré, J., & Fortin, M. (2002). Bacterial contamination

196

of colostrum fed to newborn calves in Québec dairy herds. Canadian Veterinary Journal,

197

43, 523–527.

198 199

Godden, S. (2008). Colostrum management for dairy calves. Veterinary Clinics of North America: Food Animal Practice, 24, 19–39.

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Godden, S. M., Smolenski, D. J., Donahue, M., Oakes, J. M., Bey, R., Wells, S., et al. (2012).

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Heat-treated colostrum and reduced morbidity in preweaned dairy calves: Results of a

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randomized trial and examination of mechanisms of effectiveness. Journal of Dairy

203

Science, 95, 4029–4040.

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Houser, B. A., Donaldson, S. C., Kehoe, S., Heinrichs, A. J., & Jayarao, B. M. (2008). A survey

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of bacteriological quality and the occurrence of Salmonella in raw bovine colostrum.

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Foodborne Pathogens and Disease, 5, 853–858.

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Lorenz, I., Mee, J. F., Earley, B., & More, S. J. (2011). Calf health from birth to weaning. I. General aspects of disease prevention. Irish Veterinary Journal, 64, Article 10. McGrath, B. A., Fox, P. F., McSweeney, P. L. H., & Kelly, A. L. (2016). Composition and properties of bovine colostrum: a review. Dairy Science & Technology, 96, 133–158. McGuirk, S. M., & Collins, M. (2004). Managing the production, storage, and delivery of colostrum. Veterinary Clinics of North America: Food Animal Practice, 20, 593–603. Renaud, D. L., Kelton, D. F., LeBlanc, S. J., Haley, D. B., Jalbert, A. B., & Duffield, T. F.

214

(2017). Validation of commercial luminometry swabs for total bacteria and coliform

215

counts in colostrum-feeding equipment. Journal of Dairy Science, 100, 9459–9465.

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Santos, G. dos, Silva, J. T. da, Santos, F. H. da R., & Bittar, C. M. M. (2017). Nutritional and

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microbiological quality of bovine colostrum samples in Brazil. Revista Brasileira de

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Zootecnia, 46, 72–79.

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Stewart, S., Godden, S., Bey, R., Rapnicki, P., Fetrow, J., Farnsworth, R., et al. (2005).

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Preventing bacterial contamination and proliferation during the harvest, storage, and

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feeding of fresh bovine colostrum. Journal of Dairy Science, 88, 2571–2578.

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Figure legend

Fig. 1. Marginal prediction of the log odds of the colostrum microbiological quality and herd management factors: bottle;

, no suckling from mother;

, fed from bottle.

, suckling from mother;

, not fed from

Table 1 Total number of colostrum samples tested and number of samples above threshold for total bacterial count (TBC) and total coliform count (TCC). a Herd

Samples tested

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38

1 2 1 22 3 3 8 6 14 10 1 6 3 10 8 5 1 4 6 3 3 4 3 4 20 4 8 5 1 4 7 2 3 8 4 16 9 3

Above threshold TBC TCC 0 0 0 0 1 1 4 9 2 2 0 3 2 1 2 0 0 1 0 2 1 0 1 1 1 0 0 1 3 1 1 0 0 0 1 1 1 1 1 0 0 0 1 0 0 1 3 3 0 2 0 2 0 2 0 2 0 0 1 1 1 2 1 0 0 2 5 4 0 1 0 4 1 1 2 1 1

39 40 41 42 43 44 Total a

5 15 1 3 3 3 255

0 8 1 0 1 0 46

1 6 1 2 0 0 62

Thresholds for TBC and TCC were >100,000 cfu mL-1 and TCC >10,000 cfu mL-1,

respectively; 255 colostrum samples were collected from 44 herds in Antioquia, Boyacá and Cundinamarca, Colombia.

2

Table 2 Bivariate analysis of management factors associated with microbiological quality of bovine colostrum in Colombian dairy herds. a Variables Number of calving <4 ≥4 Dry period (days) <50 ≥50 – <70 ≥70 Cow inventory <100 ≥100 – <200 ≥200 – <300 ≥300 Cow breed Pure breed Crossbreed Calving ease Normal Dystocia Colostrum IgG (g L-1) Low quality (<50 g L-1) High quality (≥50 g L-1) Cow-calf separation at birth Yes No Stays with the cow >1 day ≤1 day Suckling from mother No Yes Bottle feed practice No Yes

n

%

P-value TPC

TCC

165 90

65% 35%

0.794

0.118

11 160 84

4% 63% 33%

0.279

0.124

53 106 19 77

21% 42% 7% 30%

0.182

0.616

209 46

82% 18%

0.439

0.406

238 17

93% 7%

0.378

0.612

137 118

54% 46%

0.375

0.499

118 136

46% 54%

0.001

0.325

127 127

50% 50%

0.002

0.186

136 118

54% 46%

0.000

0.050

148 106

58% 42%

0.357

0.291

a

Abbreviations are: TBC, total bacterial count; TCC, total coliform count. Significance at P < 0.20. 3

Table 3 Two-level logistic regression model for management factors associated with the colostrum microbiological quality in 255 calves from 44 herds in Antioquia, Boyacá and Cundinamarca, Colombia.a Variable

a

OR

SE

P

95% CI LL UL

1.00 (ref) 15.82

10.21

0.00

4.46

56.07

Suckling from mother No Yes Bottle feed practice No Yes Cow inventory <100 ≥100 – <200 ≥200 – <300 ≥300

1.00 (ref) 3.61

2.13

0.03

1.13

11.50

1.00 (ref) 3.00 0.92 4.61

1.84 1.01 3.19

0.07 0.94 0.03

0.90 0.11 1.18

10.01 7.82 17.92

Intercept

0.01

0.01

0.00

0.00

0.04

Abbreviations are: OR, odds ratio; Se, standard error; P, P-value at significant level < 0.05;

CI, confidence interval; LL, lower limit; UL, upper limit.

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