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Revista Colombiana de Ciencias Pecuarias

Print version ISSN 0120-0690

Rev Colom Cienc Pecua vol.30 no.1 Medellín Jan./Mar. 2017

http://dx.doi.org/10.17533/udea.rccp.v30n1a06 

Original Article

Factors associated with Mycobacterium avium subsp. paratuberculosis in dairy cows from Northern Antioquia, Colombia1

Factores asociados con el estatus serológico de Mycobacterium avium subsp. paratuberculosis en vacas lecheras del norte de Antioquia, Colombia

Fatores associados ao estado sorológico de Mycobacterium avium subsp. paratuberculosis em soro de gado leiteira no norte de Antioquia, Colombia

Jorge A Fernández Silva1  *  , Nicolás F Ramírez Vásquez2  , Nathalia M Correa Valencia2 

1Epidemiología y Medicina Preventiva para la Salud Animal y Humana (EMPreSAH), Escuela de Medicina Veterinaria, Facultad de Ciencias Agrarias, Universidad de Antioquia UdeA, Calle 70 No. 52-21, Medellín, Colombia.

2Epidemiología y Salud Pública Veterinaria, Centauro Research Group, Escuela de Medicina Veterinaria, Facultad de Ciencias Agrarias, Universidad de Antioquia UdeA, Calle 70 No. 52-21, Medellín, Colombia.

Summary

Background:

Johne´s disease (JD) is a severe enteritis that affects ruminants and has been diagnosed in cattle and sheep in Colombia. However, epidemiological information on the disease in this country is scarce.

Objective:

to identify factors associated with the JD serum enzyme-linked immunosorbent assay (ELISA) status of dairy cows.

Methods:

a cross-sectional study was carried out in 307 asymptomatic adult Holstein dairy cows from 14 herds in nine districts of Belmira and San Pedro de los Milagros municipalities during November, 2007. From 19 to 25 cows, ≥ 2 years of age were randomly selected and blood sampled from every herd. A commercial ELISA kit was used to analyze sera. Information regarding cow related factors (age, farm-born, parity, and daily milk yield) and herd management practices (i.e. herd size, herd average milk production, current presence of symptomatic animals, cattle purchase, own animals grazing in foreign pastures, feeding of calves before weaning, manure spread on pastures, and sighting of birds in feed storing areas) was collected using questionnaires. Descriptive statistics were computed for all variables and a multivariable logistic regression model was constructed (p<0.05).

Results:

ten percent (31/307; 95% CI: 7.0-14.0%) of the animals were positive by ELISA. In 70% (10/14) of the herds, ELISA detected at least one positive animal. Cow and herd factors “parity” and “feeding of calves before weaning” showed weak and strong associations with ELISA positive results, respectively. The odds ratio (OR) for JD seropositivity increased 20% (OR = 1.20; 95% CI: 0.98-1.47; p = 0.067) in cows with > 1 parity. The OR was 0.74 times lower (OR = 0.26; 95% CI: 0.096-0.70; p<0.01) in herds feeding calves with pooled colostrum from several cows, compared to herds feeding calves with colostrum from their own dams.

Conclusion:

JD seroprevalence was 10 and 70% at animal and herd-level, respectively. Cow and herd factors “parity” and “feeding of calves before weaning” showed weak and strong association with positive results, respectively.

Key words: cattle; epidemiology; paratuberculosis; serology

Resumen

Antecedentes:

la enfermedad de Johne (EJ) es una enteritis severa que afecta rumiantes, y ha sido diagnosticada en bovinos y ovejas en Colombia. Sin embargo, la información epidemiológica de la enfermedad en el país es escaza.

Objetivo:

identificar los factores asociados con el estatus serológico de la EJ mediante ensayo de inmunoabsorción ligado a enzimas (ELISA) en vacas lecheras.

Métodos:

se realizó un estudio transversal en 307 vacas lecheras adultas asintomáticas de 14 hatos en 9 veredas en los municipios de Belmira y San Pedro de los Milagros, en noviembre de 2007. De cada hato se seleccionaron aleatoriamente 19-25 vacas, mayores de 2 años de edad y se tomaron muestras de sangre. Se utilizó un kit comercial de ELISA para analizar el suero. Se recolectó información mediante cuestionarios sobre características individuales de las vacas y prácticas de manejo de los hatos. Se realizó un estudio estadístico descriptivo para todas las variables de interés y se construyó un modelo de regresión logística multivariada, considerando un nivel de significancia de p<0,05.

Resultados:

el 10% de los animales fue positivo a ELISA (31/307; 95% CI: 7,0-14%). En el 70% (10/14) de los hatos al menos un animal fue detectado como positivo por ELISA. Los factores a nivel individual y a nivel hato “número de partos” y “tipo de alimentación de terneras antes del destete” mostraron una asociación débil y fuerte con los resultados positivos de ELISA, respectivamente. El odds ratio (OR) para la seropositividad a EJ aumentó en un 20% (OR = 1,20; 95% CI: 0,98-1,47; p = 0,067) en vacas con más de un parto, mientras que fue 0,74 veces menor (OR = 0,26; 95% CI: 0,096-0,70; p<0,01) en hatos que alimentan sus terneras con mezcla de calostro proveniente de varias vacas, en comparación con aquellos hatos que solo utilizan el calostro de la propia madre.

Conclusión:

la seroprevalencia de EJ fue del 10 y del 70% a nivel individual y a nivel hato, respectivamente. Los factores a nivel individual y a nivel hato “número de partos” y “tipo de alimentación de terneras antes del destete” mostraron una asociación débil y fuerte con los resultados positivos de ELISA, respectivamente.

Palabras-clave: epidemiología; ganado; paratuberculosis; serología

Resumo

Antecedentes:

a doença de Johne (DJ) é uma enterite grave que afeta o ruminantes, e tem sido diagnosticada em bovinos e ovinos na Colômbia. No entanto, a informação epidemiológica da doença no país é escassa.

Objetivo:

identificar os fatores associados ao estado sorológico de DJ em vacas leiteiras por ensaio imunossorvente ligado a enzima (ELISA).

Métodos:

estudo transversal foi realizado em 307 vacas leiteiras adultos assintomáticos em 9 de 14 aldeias nos municípios de Belmira y San Pedro de los Milagros, em novembro de 2007. Em cada rebanho foram selecionados aleatoriamente 19-25 vacas com mais de 2 anos de idade e amostras de sangue foram tomadas. Um kit de ELISA comercial é utilizado para testar soros. As informações foram coletadas por meio de questionários sobre as características individuais de animais e práticas de gestão do rebanho. A análise estatística descritiva foi realizada para todas as variáveis de interesse e modelo de regressão logística multivariada foi construído, considerando um nível de significância de p<0,05.

Resultados:

dez por cento dos animais foram positivos no ELISA (31/307; 95% CI: 7,0-14%). No 70% (10/14) os rebanhos pelo menos, um animal foi detectado como positivo por ELISA. Os fatores a nível individual como a nível do rebanho "paridade" e "tipo de alimentação bezerros antes do desmame" mostraram uma associação fraca e forte com os resultados positivos de ELISA, respectivamente. O odds ratio (OR) para DJ soropositividade aumentou em um 20% (OR = 1,20; 95% CI: 0,98-1,47; p = 0,067) em vacas com mais de um nascimento, enquanto era 0,74 vezes menor (OR = 0,26; 95% CI: 0,096-0,70; p<0,01) em rebanhos que alimentam seus filhotes com a mistura de colostro de várias vacas, em comparação com apenas dados de uso que o colostro da mãe.

Conclusão:

DJ soroprevalência foi de 10 e 70% a nível individual como a nível do rebanho, respectivamente. Os fatores a nível individual e do rebanho "paridade" e "tipo de alimentação bezerros antes do desmame" mostrou fraca associação e forte com os resultados positivos de ELISA, respectivamente.

Palavras-Chave: epidemiologia; gado; paratuberculosis; sorologia

Introduction

Johne´s disease (JD) or paratuberculosis is a severe enteritis that affects cattle and other domestic and wild ruminants (Harris and Barletta, 2001). The causal agent of JD is Mycobacterium avium subspecies paratuberculosis (MAP), a Gram-positive, facultative, mycobactin-dependant, slow growing, and acid-fast bacillus (Chiodini et al., 1984; Sweeney, 1996). MAP has also been associated with the human inflammatory bowel disease known as Crohn’s disease (Chacon et al., 2004; Atreya et al., 2014; Sechi and Dow, 2015).

Johne´s disease causes substantial economic losses to the cattle industry due to increased premature culling, replacement costs, decreased milk yield, reduced feed conversion efficiency, fertility problems, reduced slaughter values, and increased susceptibility to other diseases or conditions (Johnson et al., 2001; Kudahl et al., 2004; Weber, 2006; Beaudeau et al., 2007; Gonda et al., 2007; Nielsen and Toft, 2009; Richardson and More, 2009; McAloon et al., 2016). It is known that this disease has a global distribution (Barkema et al., 2010; Manning and Collins, 2010).

Prevention and control of JD demands knowledge on the disease presence, frequency, and distribution as well as those factors influencing its entrance and perpetuation in herds. Herd management practices can increase or decrease the probability of MAP entering or circulating in a dairy cattle population. These practices vary, not only between countries or agro ecological zones, but also between regions and herds, thus requiring to determine specific factors associated with JD status of animals or herds in each region.

Previous studies have identified a number of cow and herd management factors that can influence MAP status. Most of these studies have been conducted using the herd as the unit of analysis, and have used serological results to establish the MAP diagnosis of animals, as well as the subsequent identification of risk factors (Collins et al., 1994; Goodger et al., 1996; Johnson-Ifearulundu and Kaneene, 1999; Jakobsen et al., 2000; Hacker et al., 2004; Dieguez et al., 2008; Nielsen et al, 2008; Tiwari et al., 2009; Sorge et al., 2012; Pieper et al., 2015; Vilar et al., 2015). However, other diagnostic methods, such as PCR (Ansari-Lari et al., 2009), fecal culture (Obasanjo et al., 1997), and mixed methods (Kobayashi et al., 2007) have been used to establish JD prevalence and risk factors.

A previous study reported MAP seroprevalence of 3.6% (14/696) and 2% (1/28) at the herd and animal-level, respectively. In addition, days in milk between 100-200 days (OR = 4.42) and >200 days (OR = 3.45), and the daily milk yield between 20-40 L/cow (OR = 2.53) and >40 L/cow (OR = 20.38) were identified as risk factors for MAP seropositivity (Correa-Valencia et al., 2016).

The objective of this study was to identify cow and herd management factors associated with the serological individual status to MAP (based on ELISA -enzyme-linked immunosorbent assay- results) in 307 asymptomatic lactating Holstein cows from 14 herds in San Pedro de los Milagros, Antioquia (Colombia).

Materials and methods

Ethical considerations

The study was conducted following the Statute of Good Scientific Practices of the Justus-Liebig-University Giessen (Statute of Justus Liebig University Giessen for Ensuring Good Academic Practice, 29th May 2002).

Herds and animals

In November 2007, 14 herds located in nine districts of two municipalities (Belmira and San Pedro de los Milagros) in the Northern dairy region of Antioquia province, Colombia, were sampled for detecting anti-MAP antibodies. Blood samples were collected from 307 asymptomatic Holstein cows over two years of age. One of the herds presented sporadic clinical cases compatible with JD, which was confirmed by PCR and histopathology (Zapata et al., 2010; Ramírez et al., 2011). The animals tested in every herd were randomly selected (Table 1).

Table 1 Results of Mycobacterium avium subsp. paratuberculosis ELISA of dairy cows in 14 dairy herds located in 9 district of two municipalities in Northern Antioquia, Colombia. 

a Herd with history of JD (Zapata et al., 2010). b Corresponds to a representative sample of animals ≥ 2 years of age

Enzyme-linked immunosorbent assay (ELISA)

The indirect unabsorbed ELISA, based on the detection of MAP−lipoarabinomannan (LAM, Svanovir Para−TB Ab ELISA Kit®, Svanova Biotech AB, Uppsala, Sweden) was used to detect anti-MAP antibodies. Percent positivity (PP) by ELISA considered the optical density values (OD) obtained at 450 nm, using the following formula:

PP = mean OD value (sample or negative control) / mean OD value (positive control) x 100.

An ELISA-positive case was defined as an animal with a PP ≥ 53 and a negative case as an animal with a PP ≤ 31. Eight out of 307 (2%) doubtful results (PP >31 - < 53) were considered negative. Regarding the factors associated with MAP status, a positive or negative ELISA result was considered the outcome or dependent variable.

Factors associated with MAP serologic status

Information regarding cow and herd management practices was collected to determine factors that could be associated with the cow serological status. Cow factors and herd management practices have been associated with JD status in previous studies using the same diagnostic test (ELISA). Two questionnaires were administered to herd managers and/or owners during sample collection. The first questionnaire asked for information regarding cow factors such as identification (number and name), age, farm-born, parity, and daily milk yield. The second questionnaire asked for information regarding herd management practices related to maintenance or transmission of MAP within and between herds. Questions related to herd management practices were distributed into four groups; Group 1: general information of the herd (farm size, access to veterinary services, daily milk production, and cattle population); Group 2: information regarding presence of the disease in the herd (current presentation of symptomatic animals, and cases of Johne’s disease observed during the last two years); Group 3: management factors affecting MAP transmission between herds (cattle purchase, own animals grazing on foreign pastures, foreign animals grazing on own pastures); and Group 4: factors regarding housing and hygiene (existence of a calving area, type of calf housing before weaning, feeding of calves before weaning, spreading of manure on pastures, and bird sighting in feed storing areas, Table 2).

Table 2 Cow and herd predictors associated with Mycobacterium avium subsp. paratuberculosis ELISA status in 307 dairy cows of Northern Antioquia, Colombia 

Case definition

The case definition for a MAP-infected animal was a cow with an ELISA seropositive result (PP ≥ 53).

Statistical analysis

The data collected during the study (Table 2) was saved in Excel (Microsoft Corp., Redmond, WA, USA) and then exported to Stata 12.0 (StataCorp, 2011, Texas, USA) for statistical analysis. The data was examined for biologically implausible entries. Erroneous data were removed or corrected. Descriptive statistics were computed for all variables (Table 3 and 4). An initial exploratory analysis of the data was conducted using Chi−square and Fisher’s exact tests. Results of the initial exploratory analysis revealed that “parity”, “herd population (heads)”, “own animals grazing in foreign pastures”, “feeding of calves before weaning”, and “spread on pastures” were significantly associated with cow serological status (data not shown). Subsequently, Pearson and Spearman correlation analysis was executed for continuous and categorical variables, respectively. An unconditional mixed−effects logistic regression analysis, grouped by herd to account for clustering, was performed. The criteria of Hosmer-Lemeshow (p<0.25) was used to retain variables for the multivariable model. A multivariable mixed−effects logistic regression model, grouped by herd, was performed using a significance level of p<0.05. The results from the final model are presented as odds ratios (OR) with 95% confidence intervals (CIs). The response variable was the serum status ELISA for MAP (positive or negative). The cluster effect was random and all risk factors (parity, own animals grazing in foreign pastures, feeding of calves before weaning, spreading of manure on pastures, birds sighting in feed storing areas) were fixed effects. The logistic model took the general form: (Y) ~ binary outcome (probability π), Logit (π) = ß0 intercept + ß1 Parityij + ß2 average daily milk production of the herd (lt) + ß3 herd population (heads) + ß4 own animals grazing in foreign pasturesj + ß5 feeding of calves before weaningj + ß6 spreading of manure on pasturesj + ß7 birds sighting in feed storing areas + eij Where Yij= outcome variable at i-th cow and the jth farm π = fitted probability of the outcome, ß1 to ß5 = coefficients associated with each covariate, eij = random residual effect.

Results

ELISA

Ten percent (10.1%, 31/307; 95% CI: 6.7-13.5%), and 89.9% (276/307; 95% CI: 86.5-93.3%) of the samples produced positive and negative results by ELISA, respectively. In 70% (10/14) of the herds, ELISA detected at least one seropositive animal (Table 1).

Factors associated with MAP serologic status

Analysis of correlation revealed collinearity (>0.80) between the variable “age” (years) and “parity” according to previous concepts (Dohoo et al., 2010); therefore, the former was excluded from the analysis. The results of the univariable analysis revealed that the factors “parity”, “herd daily average milk production (liters)”, “whole cattle population”, “own animals grazing in foreign pastures”, “feeding of calves before weaning”, “manure spread on pastures”, and “birds sighted in feedstuff store” were significantly associated with cow serological status (p<0.25; Table 4). These variables were selected for the multivariable analysis. In the final logistic regression model, the factors identified were as follows: “parity” (OR = 1.20), and “feeding of calves before weaning” (OR = 0.26; Table 5).

Table 3 Descriptive summary of quantitative variables in dairy cows of the Northern dairy region of Antioquia, Colombia, according to Mycobacterium avium subsp. paratuberculosis ELISA results. 

aVariable excluded from the unconditional analysis due to collinearity (>0.80).

Table 4 Unconditional analysis of factors associated with the Mycobacterium avium subsp. paratuberculosis ELISA status in 307 dairy cows of Northern Antioquia, Colombia. 

aVariables used for the multivariable analysis (p<0.25).

Table 5 Factors associated to Mycobacterium avium subsp. paratuberculosis ELISA status (multivariable logistic regression). 

Wald chi2 = 9.76; p = 0.0076

Discussion

The proportion of ELISA positive results obtained from animals (10.1%) and herds (70%) is consistent with the apparent prevalence of JD in other Latin-American countries, using both unabsorbed and absorbed ELISAs (Fernandez-Silva et al., 2014).

The factors “feeding of calves before weaning” and “parity” were significantly associated with the ELISA status of the cow in the initial exploratory analysis, in both the bivariable and multivariable analysis. Mycobacterium avium subspecies paratuberculosis (MAP) has been isolated from colostrum of subclinically infected cows (Streeter et al., 1995; Pithua et al., 2011; Stabel et al., 2014; Laurin et al., 2015; Jenvey et al., 2016). Additionally, the practice of feeding calves with colostrum collected from known MAP infected cows (Dieguez et al., 2008), as well as the practice of feeding calves pooled colostrum from multiple cows (Nielsen et al., 2008) have been identified as risk factors for MAP in dairy herds. Therefore, our results indicating a protective factor (OR = 0.26) disagree with this previous evidence and should be interpreted carefully. It is also possible that MAP contaminated teats can increase the likelihood of infection via suckling directly from an infected dam, compared to feeding from a colostrum mix of MAP free cows (Pithua et al., 2011). In our study, information regarding the method of colostrum feeding was not collected; therefore, this hypothesis cannot be confirmed. “Parity” was associated with JD serological status in previous studies, in which high parity (≥ 5) was associated with the probability of a positive ELISA result (Jakobsen et al., 2000). Additionally, the probability of a positive ELISA result was two to three times lower for first parity cows relative to cows in other parities (Nielsen et al., 2002).

Factors “born in a foreign herd” (Wells and Wagner, 2000; Tiwari et al., 2009; Sorge et al., 2012), “comingle with foreign cattle” (Fredriksen et al., 2004) and “manure spread on pastures” (Obasanjo et al., 1997), have previously been associated with JD status of herds. However, the present study found no significant associations in the multivariable analysis in relation to the herd ELISA status. This could be explained by the fact that our study was smaller concerning sample size in terms of number of herds. With our small sample size and our cow-based analysis, it is possible that significant associations, although present, could not be detected. In order to achieve a higher power, bigger sample sizes should be used. Unfortunately, a bigger sample size was not affordable at the time of the present exploratory study.

In Colombian dairy production systems, the purchase and exchange of animals between herds is relatively common. Animals regularly purchased for replacement or for fattening, are kept in the herd of origin until weaning and then transported to their final destination. This practice increases the risk of JD transmission to free herds due to introduction of young, subclinically infected, animals (Manning and Collins, 2010). Similar to what was found in the present study, spreading manure on pastures has been reported as a factor associated with the MAP culture results in the univariate, but not in the multiple logistic regression analysis in a previous study in the United States (Obasanjo et al., 1997). In Colombia, it is common practice to spread slurry (cattle feces alone or in combination with pig feces) as manure for pasture. This type of mix has already been identified as a potential source of MAP for cattle, considering its survival capacity for long periods (up to 252 days at 5 °C) in cattle, pig, and cattle-pig slurry (Jorgensen et al., 1977). MAP can withstand simulated composting, manure packing and liquid storage of manure from dairy farms (Grewal et al., 2006).

The low number of cattle and herds sampled is the main weakness of this study, but it can significantly contribute to the knowledge of JD in the country. Another disadvantage is the use of ELISA results as the outcome or dependent variable. ELISA is a very useful and economic tool to determine JD infection status of animals but it has low sensitivity to detect antibodies in asymptomatic adult cattle (Nielsen and Toft, 2011). However, ELISA has been widely used for prevalence and risk factor determinations, it is inexpensive, easy to perform, and results can be compared with previous national and international studies.

Conclusion

“Parity” was a risk factor for MAP status while feeding of calves before weaning” appeared to be protective for the serological status to MAP in the herds tested. Additional studies are necessary to increase epidemiological knowledge of JD in Colombia.

Acknowledgments

Thanks to ALECOL academic cooperation agreement (German Academic Exchange Service−DAAD, Universidad de Antioquia and Colciencias-Ministerio de Educación Nacional), Departamento de Formación Académica de Haciendas de la Facultad de Ciencias Agrarias UdeA, Michale Bülte, Amir Abdulmawjood, Ömer Akineden, Estrategia de sostenibilidad CODI 2013-2014 UdeA, and Michael Palacio, Ferney Agudelo, and Julian Reyes for logistic support at the UdeA, Colombia.

Conflicts of interest

The authors declare they have no conflicts of interest with regard to the work presented in this report

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1To cite this article: Fernàndez JA, Ramìrez NF, Correa NM. Factors associated with Mycobacterium avium subsp. paratuberculosis in dairy cows from Northern Antioquia, Colombia. Rev Colomb Cienc Pecu 2017; 30:48-59

Received: December 16, 2015; Accepted: May 20, 2016

*Corresponding author: Jorge Arturo Fernández Silva. Escuela de Medicina Veterinaria, Facultad de Ciencias Agrarias, Universidad de Antioquia UdeA, Calle 70 No. 52-21, Medellín, Colombia. E-mail: jorge.fernandez@udea.edu.co

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