Economic Impacts of Salmonella Dublin in Dairy Farms: Panel Evidence From Denmark

IF 4 3区 经济学 Q1 AGRICULTURAL ECONOMICS & POLICY
Dagim Belay, Jakob Vesterlund Olsen
{"title":"Economic Impacts of Salmonella Dublin in Dairy Farms: Panel Evidence From Denmark","authors":"Dagim Belay,&nbsp;Jakob Vesterlund Olsen","doi":"10.1111/agec.70016","DOIUrl":null,"url":null,"abstract":"<p>Zoonotic1 livestock diseases, such as Salmonella Dublin (SDB), have become a major public health concern in recent decades due to their potential to affect animal protein production, trade, human health, livelihoods, and food security (Hennessy and Marsh <span>2021</span>). The increased globalization, expansion of human populations, intensification of animal production systems, and changes in land use and climate increase the risk of zoonotic diseases spreading as epidemics and pandemics (Leal et al. <span>2022</span>). This calls for the need for effective surveillance and monitoring systems to mitigate their impact as highlighted during the COVID-19 pandemic. SDB, a strain commonly found in cattle, is one of the most important zoonotic diseases, with rising incidence and widespread antibiotic resistance, which makes it difficult to treat and deadly, killing up to 12% of human infections (Helms et al. <span>2003</span>; Harvey et al. <span>2017</span>; Srednik et al. <span>2021</span>; Velasquez-Munoz et al. <span>2024</span>; do Amarante et al. <span>2025</span>). It can remain latent in herds for extended periods in healthy-appearing animals, spreading through infected animal trade, animal contact, or manure, which complicates control and eradication efforts (Nielsen et al. <span>2004</span>; Velasquez-Munoz et al. <span>2024</span>). Despite the high prevalence of SDB in cattle (e.g., 60% in Great Britain (APHA <span>2022</span>) and 18% in the US (Frye <span>2021</span>)), its role as the main source of human Dublin infections (Helms et al. <span>2003</span>; Harvey et al. <span>2017</span>, Velasquez-Munoz et al. <span>2024</span>) and its capacity to cause severe illness and death in cattle, particularly in calves (Peters <span>1985</span>; Holschbach and Peek <span>2018</span>; SEGES <span>2022</span>), regulatory bodies worldwide have yet to implement adequate measures to control or eradicate SDB in cattle farming.</p><p>The absence of effective monitoring systems and the growing issue of multidrug antibiotic resistance in SDB infections present significant challenges for controlling the disease (Harvey et al. <span>2017</span>). These factors, coupled with the lack of comprehensive farm-level economic estimates, undermine efforts to convince policymakers and farmers to implement stronger regulations and interventions. For instance, while society may aim to reduce human Dublin infections originating from cattle, as seen with initiatives like Denmark's SDB eradication plan in 2008, empirical evidence does not indicate significant farmer participation in SDB reduction efforts, contrary to predictions based solely on cow-level milk yield outcomes (Nielsen et al. <span>2012a, 2012b</span>; Nielsen et al. <span>2013</span>), which often fail to account for the complexities of farm management and production behavior (Seegers et al. <span>2003</span>). Understanding the economic impacts of SDB at the farm level is crucial for identifying farmers' incentives to engage in eradication efforts and for designing effective regulatory policies aimed at mitigating SDB in cattle farming (Velasquez-Munoz et al. <span>2024</span>). This paper aims to provide the first comprehensive empirical estimates of the economic burden of SDB infections on dairy farms, leveraging a unique panel dataset of SDB antibody test results from all dairy farms in Denmark.</p><p>Two strands of literature are relevant for the present study. First, unlike much of the existing literature that primarily focuses on the public health costs of salmonellosis, our study contributes to the agricultural economics literature by specifically investigating the economic impact on farm operations, which has received relatively little attention. Other studies have largely focused on the effects of surveillance schemes not estimating the economic burden and did not focus on SDB specifically (e.g., Ollinger and Bovay <span>2018, 2020</span>; Ollinger and Houser <span>2020</span>). Moreover, existing studies on animal farming have been limited by small sample sizes, lack of data on farmers' production and managerial behavior, failure to examine standard measures of economic performance, and reliance on cost-benefit analysis, computer-based simulation models, and optimization methods (Bergevoet et al. <span>2009</span>; Nielsen et al. <span>2012a</span>; Nielsen et al. <span>2013</span>; Ågren et al. <span>2015</span>; Rasmussen et al. <span>2024</span>). The study aims to address these limitations by using unique long farm-level panel data covering all Danish dairy herds that contain detailed information on production and economic statistics and registered SDB antibodies in tank milk (Optical Density Counts [ODC]) to approximate SDB infections in dairy cows (Cummings et al. <span>2018</span>). SDB transmits through feces and the infection with SDB bacteria can cause Salmonellosis with clinical signs of the disease or the cow can be infected without being clinically ill (Nielsen et al. <span>2004</span>; Holschbach and Peek <span>2018</span>). If a cow has been infected by the bacteria, it develops antibodies detectable in milk samples when the concentration is high enough. The duration from the first infection until a high ODC can be found in the tank milk samples depends on the epidemiological development in the herd (Nielsen et al. <span>2004</span>). The eradication of the bacteria depends on biosecurity measures preventing newborn calves and heifers from being infected (Nielsen et al. <span>2012b</span>).</p><p>Specifically, the paper's key contributions are: (i) it utilizes a unique panel dataset of tests for SDB antibodies for the entire population of Danish dairy farms; (ii) it employs rigorous high-dimensional fixed effects regression models, including farm, quarter, and farm by year fixed effects for quarterly analysis, and farm and year fixed effects for annual analysis, that help address all time-invariant and most time-varying unobservable confounding variables, along with other relevant covariates that account for observable confounders; (iii) it analyzes milk yield at the farm/herd level over a long period; (iv) it takes into account farmers' management and production behavior; (v) in addition to milk yield, the most common outcome in previous studies (e.g., Nielsen et al. <span>2012a</span>); it examines additional range of outcomes, including calf mortality and production costs; (vi) it utilizes more recent data from 2011 to 2021, enabling the analysis of changes in adaptation to and costs of SDB infections since earlier studies; and (vii) in contrast to previous studies, we also conduct a simulation study to estimate the sectoral economic burden of SDB using the lower and upper bounds of the econometric estimates, thereby providing a confidence interval for the reliability of our burden estimation. These factors make the results directly relevant to policy decisions (Seegers et al. <span>2003</span>).</p><p>Second, this study enhances the existing literature on the economic impacts of livestock diseases by incorporating asymptomatic chronic infections into the estimation of disease economic burdens, an area that has been relatively underexplored. Previous research has predominantly concentrated on one-time disease outbreaks (Caskie et al. <span>1999</span>; Bennett <span>2003</span>; Pendell et al. <span>2007</span>; Park et al. <span>2008</span>; Saghaian et al. <span>2008</span>; Ihle et al. <span>2012</span>; Knight-Jones &amp;Rushton <span>2013</span>; Cairns et al. <span>2017</span>) and has primarily examined epizootic2 and enzootic3 diseases within the beef (Pendell et al. <span>2007</span>; Park et al. <span>2008</span>; Ihle et al. <span>2012</span>; Knight-Jones and Rushton <span>2013</span>; Cairns et al. <span>2017</span>) and poultry sectors (Saghaian et al. <span>2008</span>; Antunes et al. <span>2016</span>). These studies have primarily analyzed data on symptomatic individuals or herds, where the visible impacts of disease on health and production are more easily measurable. In contrast, this study emphasizes the significant yet often-overlooked effects of asymptomatic life-long infections on production behavior and decision-making in the dairy sector by utilizing data on both symptomatic and asymptomatic infections (Harvey et al. <span>2017</span>; Cummings et al. <span>2018</span>). This dimension is particularly important for SDB due to its One Health implications, as its high prevalence in cattle and antibiotic resistance pose a public health threat, potentially leading to outbreaks and pandemics (Harvey et al. <span>2017</span>; Velasquez-Munoz et al. <span>2024</span>).</p><p>Incorporating asymptomatic infections into our data improves our understanding of the economic burden of zoonotic diseases. First, despite lacking visible symptoms, asymptomatic carriers can act as reservoirs for pathogens, facilitating disease spread and potential outbreaks (Nielsen et al. <span>2004</span>; Harvey et al. <span>2017</span>; Cummings et al. <span>2018</span>). Second, these infections can significantly affect management practices and economic outcomes; farmers unaware of them may neglect crucial biosecurity measures, leading to unexpected productivity losses, increased veterinary costs, and potentially significant human health impact (Helms et al. <span>2003</span>; Harvey et al. <span>2017</span>). We argue that recognizing the prevalence of asymptomatic cases and their potential economic impacts could shift farmers’ perceptions of overall herd health, leading to more effective management strategies and ultimately reducing the economic risks associated with zoonotic diseases. This study specifically examines the impact of SDB infections on farmers' production behavior in the dairy sector, utilizing a unique panel dataset that includes test results for SDB antibodies—including asymptomatic infections—and production statistics from all dairy farms in Denmark.</p><p>The remainder of the paper is organized as follows: Section 2 describes the data; Section 3 outlines the empirical strategy; Section 4 presents the main results, including robustness tests; Section 5 details a simulation exercise using Danish data; Section 6 discusses the results; Section 7 presents the policy implications; and the final section concludes the paper.</p><p>Several approaches can be used to address the complexity of the relationship between SDB and economic outcomes at the farm level. Previous studies have shown that large parts of the variations in data are farm-specific and therefore should not be attributed to changes in ODC levels but to farm specific characteristics (Nielsen et al. <span>2012a</span>, <span>2013</span>). Therefore, we include farm fixed effects as they control for any time-invariant factors leading to unobserved heterogeneity across individual farms. Examples of farm-fixed effects could include the size of the house of operation, location, breed of cattle, management practices, and so forth.</p><p>This study hypothesizes that SDB infections in dairy herds adversely affect economic performance across several dimensions. First, we expect that SDB will reduce milk yield, as infections likely impair the health and productivity of dairy cows. Second, we hypothesize that “newly” infected herds will experience more significant reductions in milk yield and calf mortality compared to herds with no infections. Third, we anticipate that SDB infections will increase calf mortality, as compromised cow health and SDB infections in newborn calves are expected to reduce calf survival. Finally, we expect that SDB will raise variable production costs, particularly those related to veterinary and medical services, and biosecurity measures.</p><p>All model specifications include farm fixed effect, <span></span><math>\n <semantics>\n <msub>\n <mi>α</mi>\n <mi>i</mi>\n </msub>\n <annotation>${\\alpha _i}$</annotation>\n </semantics></math>, which accounts for time-invariant unobserved differences between farms due to, for example, management differences. The quarter fixed effects <span></span><math>\n <semantics>\n <msub>\n <mi>η</mi>\n <mi>q</mi>\n </msub>\n <annotation>${\\eta _q}$</annotation>\n </semantics></math> accounts for any secular trends that affect all farms similarly in each quarter (e.g., environmental regulations, credit constraints, or technological progress similar for all cattle farms). To capture potential non-linearities in the fixed effects, almost all specifications include the interaction term “year-of-sample by farm fixed effects”, <span></span><math>\n <semantics>\n <msub>\n <mi>ω</mi>\n <mrow>\n <mi>z</mi>\n <mi>t</mi>\n </mrow>\n </msub>\n <annotation>${\\omega _{zt}}$</annotation>\n </semantics></math>, that is, allowing for interactions between farm and year fixed effects. The interaction captures any year varying farm-specific systematic change, for example, yearly change in size of a farm, yearly disease outbreak in each farm, and so forth. The natural choice for the interaction effect in a model with farm and quarter-fixed effects would be to interact farm-fixed effects with quarter-fixed effects. However, due to insufficient degrees of freedom, we opted to use farm-fixed effects interacted with year-fixed effects instead. In addition, as robustness checks, we include results using farm-fixed effects interacted with quarter of the year to capture seasonal farm level unobservable as component yield may not just be a function of breed but also changes with weather and feed and throughout the cow's biological cycle. Finally, the error term <span></span><math>\n <semantics>\n <msub>\n <mi>ε</mi>\n <mrow>\n <mi>i</mi>\n <mi>q</mi>\n </mrow>\n </msub>\n <annotation>${\\varepsilon _{iq}}$</annotation>\n </semantics></math> accounts for unobserved random variations in farms’ economic or production performance across quarters.</p><p>As described in the data section above, the quarterly herd-level panel data is used to estimate various specifications of Equation (1). To estimate different specifications of Equation (2), observations are aggregated annually and at the farm level. Both regression equations are estimated using STATA 17.0 software.</p><p>The following section presents the major findings from our study on the economic consequences of SDB infection on dairy farms. We present its impact on milk production, calf mortality rates, and farm production costs.</p><p>The significant relation between SDB in bulk tank milk and milk yield found in Table 5 can be used to assess the overall income foregone and the results from Table 9 can be used to assess the costs due to SDB. Given the development in SDB prevalence, the most recent of the 10 years is used to assess the industry income foregone and costs presented in Table 9. In total, there were 569,000 dairy cows in Denmark in 2020 with the majority having an ODC equal to zero. The total income foregone is EUR 7.5 million and the total cost for the industry is EUR 5.1 million. The average price for milk is found to be 36.1 Eurocent per kg of milk in 2020, with 90 percent being conventional milk and the remaining 10 percent being organic milk.</p><p>The industry costs found in Table 9 can be assessed to specify the contribution from different cost components. The contribution from the cost components presented in Figure 3 shows that the increase in feed costs is making up the largest share of the increase in costs related to SDB. The 95 percent confidence interval is presented with the vertical lines in the bars and represents an indication of statistically significant parameter estimate at 5 percent level, but in the industry costs in Table 9, the costs are included if the correlation is significant at the 10 percent level.</p><p>If the industry costs are assessed by the non-linear (binary) model based on the same number of cows in 2020 the total income foregone is 6.2 million EUR, that is, the estimated income foregone would be slightly lower in the non-linear model but still in the same range, whereas the total costs would be 6.1 million EUR per year and hence higher than in the model with discrete ODC levels (Table 9).</p><p>From a regulatory perspective, understanding the economic impact of SDB on dairy production is key to determining appropriate measures. If the disease causes significant losses, information on its burden and eradication strategies could be effective. If losses are minimal, stronger incentives may be needed to address its broader One Health implications. This paper presents the first comprehensive empirical estimates of SDB's economic impact on dairy farms using a unique panel dataset of Salmonella antibodies from milk deliveries across all Danish dairy farms.</p><p>The study finds that milk yield, calf mortality, and total variable costs are associated with SDB at the herd level. We estimate that herds infected with SDB may experience a reduction in milk yield of up to 13 kg per cow per month, which represents a 1.6% loss based on an average milk yield of 833 kg per cow per month. This decrease in milk yield translates into a financial loss of EUR 5 per cow per month, or EUR 58 per cow annually. For a herd of 200 milking cows, this could amount to a monthly loss of EUR 970. Moreover, if a herd experiences 25 &lt; ODC &lt; 40 for a period of 6 months, it is estimated to reduce income by EUR 5600. These findings underscore the importance of preventing and controlling SDB in dairy herds to ensure farmers can maintain stable incomes. However, the financial impact might not be immediately noticeable to farmers due to the variability of production factors, as well as differences in how the effects manifest between individual farms. Although the magnitude is less significant compared to earlier studies (e.g., Peters <span>1985</span>; Velasquez-Munoz et al. <span>2024</span>), the study also finds a strong correlation between higher ODC levels and increased calf mortality. This may provide one explanation for why farmers often fail to act when ODC levels are low. Since calf mortality is the most visible and immediate concern for farmers, the absence of this effect at lower ODC levels could delay intervention, even though reduced milk yield is already affecting farm profitability.</p><p>The study also estimates that the increased variable costs associated with SDB infections can be significant for farmers. Our simulation results indicate that the lower and upper bounds for economic burden estimates expand at higher ODC counts. For a typical farm with 200 milking cows, a small level of ODC (between 0 and 10) is estimated to result in increased variable costs of EUR 6700 per year, compared to a herd without SDB. A larger level of ODC (between 25 and 40) is estimated to be associated with an additional variable costs of EUR 11,300 per year, compared to a herd without SDB. These increased variable costs correspond to 1%–3% of the total variable costs per cow per year, which is estimated to be EUR 2800. This highlights the importance of taking measures to prevent and control SDB infections to minimize the additional variable costs for farmers. However, it is important to note that these estimates should be interpreted with caution, as the causal relationship between SDB infections and production outcomes has yet to be precisely determined.</p><p>Direct comparisons with other studies are challenging, but the closest study by Nielsen et al. (<span>2012a</span>) differs from our findings for several reasons. (i) Our study uses data from 2011 to 2020, while Nielsen et al. (<span>2012a</span>) analyzed data from 2005 to 2009. (ii) Nielsen et al. (<span>2012a</span>) analyzed cow-level milk yield data, while our study emphasizes herd-level data encompassing a broader range of economic outcomes. This approach enables us to explore the complexities of farm management and production behavior (Seegers et al. <span>2003</span>). (iii) Their study examined a small sample of Holstein herds with a sharp rise in ODC levels, compared to a control group with stable ODC levels, which may explain some of the differences. Although we also analyze “newly” infected herds, we find no significant differences in milk yield compared to other (potentially non) infected herds. Another possible explanation is that farmers may have adopted more mitigation measures over time, resulting in lower production losses but higher costs, as reflected in our findings. Unlike Nielsen et al. (<span>2012a</span>), we also estimate link between SDB infections with calf mortality and production costs. On the other hand, Nielsen et al. (<span>2013</span>) predicted higher production costs from SDB infection using a simulation model. However, unlike our study, they relied on simulations rather than statistical analysis of empirical data, which may reduce the reliability of their estimates.</p><p>Compared to other animal diseases, SDB is associated with statistically and economically significant reductions in milk production even at low infection levels, where cows act as carriers without necessarily exhibiting acute symptoms. Other diseases, such as paratuberculosis (caused by Mycobacterium avium), require higher infection rates at advanced stages to produce similar economic impacts (Garcia and Shalloo <span>2015</span>). Mastitis primarily causes milk yield reductions at later stages or during severe outbreaks, with economic losses escalating with the severity of the infection (Seegers et al. <span>2003</span>; Hadrich et al. <span>2018</span>), and none of these are zoonotic. Diseases like Bovine Leukemia Virus and Foot-and-Mouth Disease also result in significant losses, but typically at more advanced stages of infection (Knight-Jones &amp;Rushton <span>2013</span>; Norby et al. <span>2016</span>). Interestingly, Bovine Leukemia Virus may even unexpectedly increase milk yield (Yang et al. <span>2022</span>). However, the early impact of SDB underscores the critical need for early detection and control strategies to minimize both production losses and its significant public health threat, as the disease kills 12% of human infections (Helms et al. <span>2003</span>).</p><p>Even with access to a considerable amount of high-quality data, capturing the relationship between SDB infection in cows and production losses is challenging for several reasons. First, we use SDB antibodies in tank milk (a herd-level observation) as an indicator of SDB infections (a cow-level observation), which makes establishing the time lag between SDB introduction into a herd and the rise in ODC in tank milk complex. Although ODC is a useful proxy for infection rates, it is not a perfect measure. For example, bulk milk testing rarely produces false positives, though cross-reactivity or contamination can lead to misleading results. On the other hand, dilution from the herd's milk and weak antibody responses in chronic carriers may result in false negatives (Cummings et al. <span>2018</span>). Therefore, ODC should ideally be used alongside other diagnostic and biosecurity measures for a more complete understanding of herd health. Moreover, SDB may not infect all animals in the herd simultaneously, meaning that the ODC rise in tank milk could occur before all cows are infected. There may also be a delay between cows being infected with SDB and an increase in ODC levels, as initial infections may involve only a few cows, making herd-level declines in milk yield less noticeable.</p><p>We tested several lag and lead models, but none resulted in better model fits than the model without these variables. Furthermore, because we lacked daily milk yield records, we relied on monthly deliveries to the dairy. Our initial monthly data analysis found no evidence of a lead or lag relationship between changes in ODC and milk yield, consistent with Nielsen et al. (<span>2012a</span>). However, the relationship between ODC and production output could be uncertain and may not be fully captured by our herd-level models. We also explored potential links between “new” SDB infections and production outcomes, but defining new infections proved challenging and beyond the scope of this study. Thus, the production loss figures are rough estimates of the impact of actual infection levels in herds.</p><p>Second, the study could analyze the ODC using either monthly or quarterly data, each with its advantages and disadvantages. Monthly data offers greater precision in time correlations but may introduce uncertainty in data collection, such as variations in milk delivery frequency. Since ODC data are only available quarterly, the study uses the same frequency to maintain compatibility between the two variables and reduce uncertainty around milk delivery frequency. However, this approach loses some information on month-to-month variation due to the aggregation into quarterly data.</p><p>Third, using the fixed effects model provides strong evidence of the explanatory power of ODC on economic outcomes. However, it has limitations, such as not identifying which farm-specific factors, like farmhouse age, farm size, breed, or the use of automated milking machines, most influence milk yield loss, as these are included in the farm fixed effect term. Since this analysis focuses on the relationship between ODC and farm economic outcomes, future studies could explore other approaches to investigate the impact of other factors on farm economic outcomes, in addition to ODC.</p><p>This study provides new evidence on the effects of SDB on farm economics, but future research is needed to establish causality, enhance the robustness of the findings, and offer more detailed insights at the cow level for a deeper understanding of the effects.</p><p>The study underscores the economic challenges posed by SDB infections in dairy farming, affecting milk yield, mortality rates, and operating costs. Although impacts vary across herds and may not be immediately noticeable, there is an urgent need for early management of SDB, even at low prevalence levels. The asymptomatic nature of SDB often leads farmers to underestimate its economic consequences, diminishing their incentives to comply with national eradication efforts. Farmers may overlook low infection levels for other management priorities, leading to higher costs in the long run.</p><p>To tackle these challenges, we propose the following measures: (i) Farms experiencing significant losses from SDB should receive targeted information on the economic impacts and effective eradication strategies. For those with minimal losses, considering that some farmers may not perceive the economic burden of SDB, policy initiatives should offer substantial incentives, such as subsidies for prevention efforts and early herd testing, or adjusted milk pricing for farms with prolonged SDB infections. (ii) Existing arbitrary ODC threshold-based regulations should be reassessed, as even low levels of SDB can are associated with significant loss of milk yield. Last, implementing a comprehensive monitoring system that includes regular testing is crucial for effective SDB eradication. This system should gather both herd-level and individual cow data to ensure a complete understanding of disease dynamics and accurate estimation of the sectoral burden. The policy implications can be wrapped up by stating that, although significant correlations are found at the herd/farm level between ODC and milk yield, the magnitude of the associations with calf mortality and variable costs is too low to effectively incentivize farmers to prevent and eradicate SDB infections and curb human infections.</p><p>This study uses a long panel dataset on production statistics and levels of SDB antibodies in tank milk (represented by ODC levels). By applying high dimensional fixed effects models, the study minimizes endogeneity concerns and finds a statistically significant correlation between milk yield and SDB infections. Specifically, herds with non-zero ODC levels in tank milk experience a monthly milk yield loss of approximately 8 kg per cow compared to herds with ODC of 0. For herds with ODC levels above 55, the estimated milk yield loss increases to 13 kg per cow per month, which corresponds to an income loss of EUR 58 per cow per year, assuming a milk price of 40 Eurocents per kg. These losses, while smaller than those found in previous studies by Nielsen et al. (<span>2012a, 2013</span>), highlight that even small increases in ODC are associated with productivity loss.</p><p>Interestingly, the study did not find a significant association between ODC and milk yield for “newly” infected herds, contrary to Nielsen et al. (<span>2012a</span>) findings. This suggests that SDB is associated with milk yield loss as soon as ODC levels are positive, such as below 10 ODC, not only at higher thresholds, which indicates the need for more stringent rules than existing arbitrary threshold-based regulations. This finding has policy implications because the current Danish surveillance scheme is implicitly built on the notion that “newly” infected herds are going to be incentivized by the economic consequences of having an ODC above 25, whereas we find a correlation for ODC &gt; 0.</p><p>In addition to milk yield losses, the study also documents small increases in calf mortality, particularly among bull calves, correlated with ODC levels above 0. For example, herds with ODC above 55 experienced 14 extra dead heifer calves per 1000 live-born calves compared to herds with ODC of 0. Although this increase is small, the correlation with higher ODC levels, including “new infections”, may explain farmers’ delays in taking action when ODC levels are low. Since calf mortality is the most visible concern, its absence at lower ODC levels may delay intervention, even though reduced milk yield is already affecting profitability.</p><p>Moreover, the results suggest that “new” SDB infections are associated with increased calf mortality, but not with milk yield, indicating that calves may be more vulnerable to “new” SDB infections than cows. In addition to herd-wide preventive measures, targeted interventions such as vaccination are recommended to reduce calf mortality (Cummings et al. <span>2019</span>).</p><p>It is important to note that this study does not isolate the effect of SDB from other changes that are implemented at the same time at herd level. For instance, if farmers are successful in mitigating the milk yield loss due to changes in hygiene level or increased overall management performance, then the isolated effect of SDB in a herd could be larger than the estimates provided.</p><p>Ultimately, although the herd/farm level correlations between ODC and milk yield, calf mortality and variable costs are attributed to SDB infections, the magnitudes of the economic losses are too small to be easily detected by farmers or to sufficiently incentivize them to effectively prevent and eradicate SDB infections and curb human infections. Stronger incentives need to be implemented to drive effective actions.</p><p>DB and JVO conceptualized the study. JVO acquired the data. DB developed the empirical strategy, curated and visualized the data, and conducted the formal econometric analysis, while JVO performed the simulation study. DB drafted the manuscript, while JVO contributed through editing, validation, and critical review. Both authors discussed and validated the empirical results and approved the final version of the manuscript.</p><p>The authors declare they have no competing interests.</p>","PeriodicalId":50837,"journal":{"name":"Agricultural Economics","volume":"56 4","pages":"666-693"},"PeriodicalIF":4.0000,"publicationDate":"2025-04-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/agec.70016","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Agricultural Economics","FirstCategoryId":"96","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/agec.70016","RegionNum":3,"RegionCategory":"经济学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"AGRICULTURAL ECONOMICS & POLICY","Score":null,"Total":0}
引用次数: 0

Abstract

Zoonotic1 livestock diseases, such as Salmonella Dublin (SDB), have become a major public health concern in recent decades due to their potential to affect animal protein production, trade, human health, livelihoods, and food security (Hennessy and Marsh 2021). The increased globalization, expansion of human populations, intensification of animal production systems, and changes in land use and climate increase the risk of zoonotic diseases spreading as epidemics and pandemics (Leal et al. 2022). This calls for the need for effective surveillance and monitoring systems to mitigate their impact as highlighted during the COVID-19 pandemic. SDB, a strain commonly found in cattle, is one of the most important zoonotic diseases, with rising incidence and widespread antibiotic resistance, which makes it difficult to treat and deadly, killing up to 12% of human infections (Helms et al. 2003; Harvey et al. 2017; Srednik et al. 2021; Velasquez-Munoz et al. 2024; do Amarante et al. 2025). It can remain latent in herds for extended periods in healthy-appearing animals, spreading through infected animal trade, animal contact, or manure, which complicates control and eradication efforts (Nielsen et al. 2004; Velasquez-Munoz et al. 2024). Despite the high prevalence of SDB in cattle (e.g., 60% in Great Britain (APHA 2022) and 18% in the US (Frye 2021)), its role as the main source of human Dublin infections (Helms et al. 2003; Harvey et al. 2017, Velasquez-Munoz et al. 2024) and its capacity to cause severe illness and death in cattle, particularly in calves (Peters 1985; Holschbach and Peek 2018; SEGES 2022), regulatory bodies worldwide have yet to implement adequate measures to control or eradicate SDB in cattle farming.

The absence of effective monitoring systems and the growing issue of multidrug antibiotic resistance in SDB infections present significant challenges for controlling the disease (Harvey et al. 2017). These factors, coupled with the lack of comprehensive farm-level economic estimates, undermine efforts to convince policymakers and farmers to implement stronger regulations and interventions. For instance, while society may aim to reduce human Dublin infections originating from cattle, as seen with initiatives like Denmark's SDB eradication plan in 2008, empirical evidence does not indicate significant farmer participation in SDB reduction efforts, contrary to predictions based solely on cow-level milk yield outcomes (Nielsen et al. 2012a, 2012b; Nielsen et al. 2013), which often fail to account for the complexities of farm management and production behavior (Seegers et al. 2003). Understanding the economic impacts of SDB at the farm level is crucial for identifying farmers' incentives to engage in eradication efforts and for designing effective regulatory policies aimed at mitigating SDB in cattle farming (Velasquez-Munoz et al. 2024). This paper aims to provide the first comprehensive empirical estimates of the economic burden of SDB infections on dairy farms, leveraging a unique panel dataset of SDB antibody test results from all dairy farms in Denmark.

Two strands of literature are relevant for the present study. First, unlike much of the existing literature that primarily focuses on the public health costs of salmonellosis, our study contributes to the agricultural economics literature by specifically investigating the economic impact on farm operations, which has received relatively little attention. Other studies have largely focused on the effects of surveillance schemes not estimating the economic burden and did not focus on SDB specifically (e.g., Ollinger and Bovay 2018, 2020; Ollinger and Houser 2020). Moreover, existing studies on animal farming have been limited by small sample sizes, lack of data on farmers' production and managerial behavior, failure to examine standard measures of economic performance, and reliance on cost-benefit analysis, computer-based simulation models, and optimization methods (Bergevoet et al. 2009; Nielsen et al. 2012a; Nielsen et al. 2013; Ågren et al. 2015; Rasmussen et al. 2024). The study aims to address these limitations by using unique long farm-level panel data covering all Danish dairy herds that contain detailed information on production and economic statistics and registered SDB antibodies in tank milk (Optical Density Counts [ODC]) to approximate SDB infections in dairy cows (Cummings et al. 2018). SDB transmits through feces and the infection with SDB bacteria can cause Salmonellosis with clinical signs of the disease or the cow can be infected without being clinically ill (Nielsen et al. 2004; Holschbach and Peek 2018). If a cow has been infected by the bacteria, it develops antibodies detectable in milk samples when the concentration is high enough. The duration from the first infection until a high ODC can be found in the tank milk samples depends on the epidemiological development in the herd (Nielsen et al. 2004). The eradication of the bacteria depends on biosecurity measures preventing newborn calves and heifers from being infected (Nielsen et al. 2012b).

Specifically, the paper's key contributions are: (i) it utilizes a unique panel dataset of tests for SDB antibodies for the entire population of Danish dairy farms; (ii) it employs rigorous high-dimensional fixed effects regression models, including farm, quarter, and farm by year fixed effects for quarterly analysis, and farm and year fixed effects for annual analysis, that help address all time-invariant and most time-varying unobservable confounding variables, along with other relevant covariates that account for observable confounders; (iii) it analyzes milk yield at the farm/herd level over a long period; (iv) it takes into account farmers' management and production behavior; (v) in addition to milk yield, the most common outcome in previous studies (e.g., Nielsen et al. 2012a); it examines additional range of outcomes, including calf mortality and production costs; (vi) it utilizes more recent data from 2011 to 2021, enabling the analysis of changes in adaptation to and costs of SDB infections since earlier studies; and (vii) in contrast to previous studies, we also conduct a simulation study to estimate the sectoral economic burden of SDB using the lower and upper bounds of the econometric estimates, thereby providing a confidence interval for the reliability of our burden estimation. These factors make the results directly relevant to policy decisions (Seegers et al. 2003).

Second, this study enhances the existing literature on the economic impacts of livestock diseases by incorporating asymptomatic chronic infections into the estimation of disease economic burdens, an area that has been relatively underexplored. Previous research has predominantly concentrated on one-time disease outbreaks (Caskie et al. 1999; Bennett 2003; Pendell et al. 2007; Park et al. 2008; Saghaian et al. 2008; Ihle et al. 2012; Knight-Jones &Rushton 2013; Cairns et al. 2017) and has primarily examined epizootic2 and enzootic3 diseases within the beef (Pendell et al. 2007; Park et al. 2008; Ihle et al. 2012; Knight-Jones and Rushton 2013; Cairns et al. 2017) and poultry sectors (Saghaian et al. 2008; Antunes et al. 2016). These studies have primarily analyzed data on symptomatic individuals or herds, where the visible impacts of disease on health and production are more easily measurable. In contrast, this study emphasizes the significant yet often-overlooked effects of asymptomatic life-long infections on production behavior and decision-making in the dairy sector by utilizing data on both symptomatic and asymptomatic infections (Harvey et al. 2017; Cummings et al. 2018). This dimension is particularly important for SDB due to its One Health implications, as its high prevalence in cattle and antibiotic resistance pose a public health threat, potentially leading to outbreaks and pandemics (Harvey et al. 2017; Velasquez-Munoz et al. 2024).

Incorporating asymptomatic infections into our data improves our understanding of the economic burden of zoonotic diseases. First, despite lacking visible symptoms, asymptomatic carriers can act as reservoirs for pathogens, facilitating disease spread and potential outbreaks (Nielsen et al. 2004; Harvey et al. 2017; Cummings et al. 2018). Second, these infections can significantly affect management practices and economic outcomes; farmers unaware of them may neglect crucial biosecurity measures, leading to unexpected productivity losses, increased veterinary costs, and potentially significant human health impact (Helms et al. 2003; Harvey et al. 2017). We argue that recognizing the prevalence of asymptomatic cases and their potential economic impacts could shift farmers’ perceptions of overall herd health, leading to more effective management strategies and ultimately reducing the economic risks associated with zoonotic diseases. This study specifically examines the impact of SDB infections on farmers' production behavior in the dairy sector, utilizing a unique panel dataset that includes test results for SDB antibodies—including asymptomatic infections—and production statistics from all dairy farms in Denmark.

The remainder of the paper is organized as follows: Section 2 describes the data; Section 3 outlines the empirical strategy; Section 4 presents the main results, including robustness tests; Section 5 details a simulation exercise using Danish data; Section 6 discusses the results; Section 7 presents the policy implications; and the final section concludes the paper.

Several approaches can be used to address the complexity of the relationship between SDB and economic outcomes at the farm level. Previous studies have shown that large parts of the variations in data are farm-specific and therefore should not be attributed to changes in ODC levels but to farm specific characteristics (Nielsen et al. 2012a, 2013). Therefore, we include farm fixed effects as they control for any time-invariant factors leading to unobserved heterogeneity across individual farms. Examples of farm-fixed effects could include the size of the house of operation, location, breed of cattle, management practices, and so forth.

This study hypothesizes that SDB infections in dairy herds adversely affect economic performance across several dimensions. First, we expect that SDB will reduce milk yield, as infections likely impair the health and productivity of dairy cows. Second, we hypothesize that “newly” infected herds will experience more significant reductions in milk yield and calf mortality compared to herds with no infections. Third, we anticipate that SDB infections will increase calf mortality, as compromised cow health and SDB infections in newborn calves are expected to reduce calf survival. Finally, we expect that SDB will raise variable production costs, particularly those related to veterinary and medical services, and biosecurity measures.

All model specifications include farm fixed effect, α i ${\alpha _i}$ , which accounts for time-invariant unobserved differences between farms due to, for example, management differences. The quarter fixed effects η q ${\eta _q}$ accounts for any secular trends that affect all farms similarly in each quarter (e.g., environmental regulations, credit constraints, or technological progress similar for all cattle farms). To capture potential non-linearities in the fixed effects, almost all specifications include the interaction term “year-of-sample by farm fixed effects”, ω z t ${\omega _{zt}}$ , that is, allowing for interactions between farm and year fixed effects. The interaction captures any year varying farm-specific systematic change, for example, yearly change in size of a farm, yearly disease outbreak in each farm, and so forth. The natural choice for the interaction effect in a model with farm and quarter-fixed effects would be to interact farm-fixed effects with quarter-fixed effects. However, due to insufficient degrees of freedom, we opted to use farm-fixed effects interacted with year-fixed effects instead. In addition, as robustness checks, we include results using farm-fixed effects interacted with quarter of the year to capture seasonal farm level unobservable as component yield may not just be a function of breed but also changes with weather and feed and throughout the cow's biological cycle. Finally, the error term ε i q ${\varepsilon _{iq}}$ accounts for unobserved random variations in farms’ economic or production performance across quarters.

As described in the data section above, the quarterly herd-level panel data is used to estimate various specifications of Equation (1). To estimate different specifications of Equation (2), observations are aggregated annually and at the farm level. Both regression equations are estimated using STATA 17.0 software.

The following section presents the major findings from our study on the economic consequences of SDB infection on dairy farms. We present its impact on milk production, calf mortality rates, and farm production costs.

The significant relation between SDB in bulk tank milk and milk yield found in Table 5 can be used to assess the overall income foregone and the results from Table 9 can be used to assess the costs due to SDB. Given the development in SDB prevalence, the most recent of the 10 years is used to assess the industry income foregone and costs presented in Table 9. In total, there were 569,000 dairy cows in Denmark in 2020 with the majority having an ODC equal to zero. The total income foregone is EUR 7.5 million and the total cost for the industry is EUR 5.1 million. The average price for milk is found to be 36.1 Eurocent per kg of milk in 2020, with 90 percent being conventional milk and the remaining 10 percent being organic milk.

The industry costs found in Table 9 can be assessed to specify the contribution from different cost components. The contribution from the cost components presented in Figure 3 shows that the increase in feed costs is making up the largest share of the increase in costs related to SDB. The 95 percent confidence interval is presented with the vertical lines in the bars and represents an indication of statistically significant parameter estimate at 5 percent level, but in the industry costs in Table 9, the costs are included if the correlation is significant at the 10 percent level.

If the industry costs are assessed by the non-linear (binary) model based on the same number of cows in 2020 the total income foregone is 6.2 million EUR, that is, the estimated income foregone would be slightly lower in the non-linear model but still in the same range, whereas the total costs would be 6.1 million EUR per year and hence higher than in the model with discrete ODC levels (Table 9).

From a regulatory perspective, understanding the economic impact of SDB on dairy production is key to determining appropriate measures. If the disease causes significant losses, information on its burden and eradication strategies could be effective. If losses are minimal, stronger incentives may be needed to address its broader One Health implications. This paper presents the first comprehensive empirical estimates of SDB's economic impact on dairy farms using a unique panel dataset of Salmonella antibodies from milk deliveries across all Danish dairy farms.

The study finds that milk yield, calf mortality, and total variable costs are associated with SDB at the herd level. We estimate that herds infected with SDB may experience a reduction in milk yield of up to 13 kg per cow per month, which represents a 1.6% loss based on an average milk yield of 833 kg per cow per month. This decrease in milk yield translates into a financial loss of EUR 5 per cow per month, or EUR 58 per cow annually. For a herd of 200 milking cows, this could amount to a monthly loss of EUR 970. Moreover, if a herd experiences 25 < ODC < 40 for a period of 6 months, it is estimated to reduce income by EUR 5600. These findings underscore the importance of preventing and controlling SDB in dairy herds to ensure farmers can maintain stable incomes. However, the financial impact might not be immediately noticeable to farmers due to the variability of production factors, as well as differences in how the effects manifest between individual farms. Although the magnitude is less significant compared to earlier studies (e.g., Peters 1985; Velasquez-Munoz et al. 2024), the study also finds a strong correlation between higher ODC levels and increased calf mortality. This may provide one explanation for why farmers often fail to act when ODC levels are low. Since calf mortality is the most visible and immediate concern for farmers, the absence of this effect at lower ODC levels could delay intervention, even though reduced milk yield is already affecting farm profitability.

The study also estimates that the increased variable costs associated with SDB infections can be significant for farmers. Our simulation results indicate that the lower and upper bounds for economic burden estimates expand at higher ODC counts. For a typical farm with 200 milking cows, a small level of ODC (between 0 and 10) is estimated to result in increased variable costs of EUR 6700 per year, compared to a herd without SDB. A larger level of ODC (between 25 and 40) is estimated to be associated with an additional variable costs of EUR 11,300 per year, compared to a herd without SDB. These increased variable costs correspond to 1%–3% of the total variable costs per cow per year, which is estimated to be EUR 2800. This highlights the importance of taking measures to prevent and control SDB infections to minimize the additional variable costs for farmers. However, it is important to note that these estimates should be interpreted with caution, as the causal relationship between SDB infections and production outcomes has yet to be precisely determined.

Direct comparisons with other studies are challenging, but the closest study by Nielsen et al. (2012a) differs from our findings for several reasons. (i) Our study uses data from 2011 to 2020, while Nielsen et al. (2012a) analyzed data from 2005 to 2009. (ii) Nielsen et al. (2012a) analyzed cow-level milk yield data, while our study emphasizes herd-level data encompassing a broader range of economic outcomes. This approach enables us to explore the complexities of farm management and production behavior (Seegers et al. 2003). (iii) Their study examined a small sample of Holstein herds with a sharp rise in ODC levels, compared to a control group with stable ODC levels, which may explain some of the differences. Although we also analyze “newly” infected herds, we find no significant differences in milk yield compared to other (potentially non) infected herds. Another possible explanation is that farmers may have adopted more mitigation measures over time, resulting in lower production losses but higher costs, as reflected in our findings. Unlike Nielsen et al. (2012a), we also estimate link between SDB infections with calf mortality and production costs. On the other hand, Nielsen et al. (2013) predicted higher production costs from SDB infection using a simulation model. However, unlike our study, they relied on simulations rather than statistical analysis of empirical data, which may reduce the reliability of their estimates.

Compared to other animal diseases, SDB is associated with statistically and economically significant reductions in milk production even at low infection levels, where cows act as carriers without necessarily exhibiting acute symptoms. Other diseases, such as paratuberculosis (caused by Mycobacterium avium), require higher infection rates at advanced stages to produce similar economic impacts (Garcia and Shalloo 2015). Mastitis primarily causes milk yield reductions at later stages or during severe outbreaks, with economic losses escalating with the severity of the infection (Seegers et al. 2003; Hadrich et al. 2018), and none of these are zoonotic. Diseases like Bovine Leukemia Virus and Foot-and-Mouth Disease also result in significant losses, but typically at more advanced stages of infection (Knight-Jones &Rushton 2013; Norby et al. 2016). Interestingly, Bovine Leukemia Virus may even unexpectedly increase milk yield (Yang et al. 2022). However, the early impact of SDB underscores the critical need for early detection and control strategies to minimize both production losses and its significant public health threat, as the disease kills 12% of human infections (Helms et al. 2003).

Even with access to a considerable amount of high-quality data, capturing the relationship between SDB infection in cows and production losses is challenging for several reasons. First, we use SDB antibodies in tank milk (a herd-level observation) as an indicator of SDB infections (a cow-level observation), which makes establishing the time lag between SDB introduction into a herd and the rise in ODC in tank milk complex. Although ODC is a useful proxy for infection rates, it is not a perfect measure. For example, bulk milk testing rarely produces false positives, though cross-reactivity or contamination can lead to misleading results. On the other hand, dilution from the herd's milk and weak antibody responses in chronic carriers may result in false negatives (Cummings et al. 2018). Therefore, ODC should ideally be used alongside other diagnostic and biosecurity measures for a more complete understanding of herd health. Moreover, SDB may not infect all animals in the herd simultaneously, meaning that the ODC rise in tank milk could occur before all cows are infected. There may also be a delay between cows being infected with SDB and an increase in ODC levels, as initial infections may involve only a few cows, making herd-level declines in milk yield less noticeable.

We tested several lag and lead models, but none resulted in better model fits than the model without these variables. Furthermore, because we lacked daily milk yield records, we relied on monthly deliveries to the dairy. Our initial monthly data analysis found no evidence of a lead or lag relationship between changes in ODC and milk yield, consistent with Nielsen et al. (2012a). However, the relationship between ODC and production output could be uncertain and may not be fully captured by our herd-level models. We also explored potential links between “new” SDB infections and production outcomes, but defining new infections proved challenging and beyond the scope of this study. Thus, the production loss figures are rough estimates of the impact of actual infection levels in herds.

Second, the study could analyze the ODC using either monthly or quarterly data, each with its advantages and disadvantages. Monthly data offers greater precision in time correlations but may introduce uncertainty in data collection, such as variations in milk delivery frequency. Since ODC data are only available quarterly, the study uses the same frequency to maintain compatibility between the two variables and reduce uncertainty around milk delivery frequency. However, this approach loses some information on month-to-month variation due to the aggregation into quarterly data.

Third, using the fixed effects model provides strong evidence of the explanatory power of ODC on economic outcomes. However, it has limitations, such as not identifying which farm-specific factors, like farmhouse age, farm size, breed, or the use of automated milking machines, most influence milk yield loss, as these are included in the farm fixed effect term. Since this analysis focuses on the relationship between ODC and farm economic outcomes, future studies could explore other approaches to investigate the impact of other factors on farm economic outcomes, in addition to ODC.

This study provides new evidence on the effects of SDB on farm economics, but future research is needed to establish causality, enhance the robustness of the findings, and offer more detailed insights at the cow level for a deeper understanding of the effects.

The study underscores the economic challenges posed by SDB infections in dairy farming, affecting milk yield, mortality rates, and operating costs. Although impacts vary across herds and may not be immediately noticeable, there is an urgent need for early management of SDB, even at low prevalence levels. The asymptomatic nature of SDB often leads farmers to underestimate its economic consequences, diminishing their incentives to comply with national eradication efforts. Farmers may overlook low infection levels for other management priorities, leading to higher costs in the long run.

To tackle these challenges, we propose the following measures: (i) Farms experiencing significant losses from SDB should receive targeted information on the economic impacts and effective eradication strategies. For those with minimal losses, considering that some farmers may not perceive the economic burden of SDB, policy initiatives should offer substantial incentives, such as subsidies for prevention efforts and early herd testing, or adjusted milk pricing for farms with prolonged SDB infections. (ii) Existing arbitrary ODC threshold-based regulations should be reassessed, as even low levels of SDB can are associated with significant loss of milk yield. Last, implementing a comprehensive monitoring system that includes regular testing is crucial for effective SDB eradication. This system should gather both herd-level and individual cow data to ensure a complete understanding of disease dynamics and accurate estimation of the sectoral burden. The policy implications can be wrapped up by stating that, although significant correlations are found at the herd/farm level between ODC and milk yield, the magnitude of the associations with calf mortality and variable costs is too low to effectively incentivize farmers to prevent and eradicate SDB infections and curb human infections.

This study uses a long panel dataset on production statistics and levels of SDB antibodies in tank milk (represented by ODC levels). By applying high dimensional fixed effects models, the study minimizes endogeneity concerns and finds a statistically significant correlation between milk yield and SDB infections. Specifically, herds with non-zero ODC levels in tank milk experience a monthly milk yield loss of approximately 8 kg per cow compared to herds with ODC of 0. For herds with ODC levels above 55, the estimated milk yield loss increases to 13 kg per cow per month, which corresponds to an income loss of EUR 58 per cow per year, assuming a milk price of 40 Eurocents per kg. These losses, while smaller than those found in previous studies by Nielsen et al. (2012a, 2013), highlight that even small increases in ODC are associated with productivity loss.

Interestingly, the study did not find a significant association between ODC and milk yield for “newly” infected herds, contrary to Nielsen et al. (2012a) findings. This suggests that SDB is associated with milk yield loss as soon as ODC levels are positive, such as below 10 ODC, not only at higher thresholds, which indicates the need for more stringent rules than existing arbitrary threshold-based regulations. This finding has policy implications because the current Danish surveillance scheme is implicitly built on the notion that “newly” infected herds are going to be incentivized by the economic consequences of having an ODC above 25, whereas we find a correlation for ODC > 0.

In addition to milk yield losses, the study also documents small increases in calf mortality, particularly among bull calves, correlated with ODC levels above 0. For example, herds with ODC above 55 experienced 14 extra dead heifer calves per 1000 live-born calves compared to herds with ODC of 0. Although this increase is small, the correlation with higher ODC levels, including “new infections”, may explain farmers’ delays in taking action when ODC levels are low. Since calf mortality is the most visible concern, its absence at lower ODC levels may delay intervention, even though reduced milk yield is already affecting profitability.

Moreover, the results suggest that “new” SDB infections are associated with increased calf mortality, but not with milk yield, indicating that calves may be more vulnerable to “new” SDB infections than cows. In addition to herd-wide preventive measures, targeted interventions such as vaccination are recommended to reduce calf mortality (Cummings et al. 2019).

It is important to note that this study does not isolate the effect of SDB from other changes that are implemented at the same time at herd level. For instance, if farmers are successful in mitigating the milk yield loss due to changes in hygiene level or increased overall management performance, then the isolated effect of SDB in a herd could be larger than the estimates provided.

Ultimately, although the herd/farm level correlations between ODC and milk yield, calf mortality and variable costs are attributed to SDB infections, the magnitudes of the economic losses are too small to be easily detected by farmers or to sufficiently incentivize them to effectively prevent and eradicate SDB infections and curb human infections. Stronger incentives need to be implemented to drive effective actions.

DB and JVO conceptualized the study. JVO acquired the data. DB developed the empirical strategy, curated and visualized the data, and conducted the formal econometric analysis, while JVO performed the simulation study. DB drafted the manuscript, while JVO contributed through editing, validation, and critical review. Both authors discussed and validated the empirical results and approved the final version of the manuscript.

The authors declare they have no competing interests.

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都柏林沙门氏菌对奶牛场的经济影响:来自丹麦的专家组证据
细菌的根除取决于防止新生牛犊和小母牛被感染的生物安全措施(Nielsen等人,2012b)。具体来说,该论文的主要贡献是:(i)它为丹麦奶牛场的整个人口使用了一个独特的SDB抗体测试面板数据集;(ii)采用严格的高维固定效应回归模型,包括农场、季度和农场按年固定效应用于季度分析,农场和年固定效应用于年度分析,这有助于解决所有时不变和大多数时变不可观察的混杂变量,以及其他相关协变量,这些协变量可以解释可观察的混杂因素;(iii)分析长期农场/牧群水平的产奶量;(四)兼顾农民经营和生产行为;(v)除了产奶量之外,在以前的研究中最常见的结果(例如,Nielsen et al. 2012a);它考察了其他一系列结果,包括小牛死亡率和生产成本;(vi)它利用了2011年至2021年的最新数据,能够分析自早期研究以来SDB感染的适应变化和成本;(7)与以往的研究相比,我们还进行了模拟研究,利用计量经济学估计的下界和上界来估计深发展的行业经济负担,从而为我们的负担估计的可靠性提供了一个置信区间。这些因素使结果与政策决定直接相关(Seegers et al. 2003)。其次,本研究通过将无症状慢性感染纳入疾病经济负担的估计,加强了现有文献对牲畜疾病经济影响的研究,这一领域的研究相对较少。以前的研究主要集中在一次性疾病暴发(Caskie等人,1999年;班尼特2003;Pendell et al. 2007;Park et al. 2008;Saghaian et al. 2008;Ihle et al. 2012;Knight-Jones &Rushton 2013;Cairns等人,2017年),并主要检查了牛肉中的动物传染病和动物传染病(Pendell等人,2007年;Park et al. 2008;Ihle et al. 2012;Knight-Jones and Rushton 2013;Cairns et al. 2017)和家禽业(Saghaian et al. 2008;Antunes et al. 2016)。这些研究主要分析了有症状的个体或畜群的数据,在这些个体或畜群中,疾病对健康和生产的可见影响更容易衡量。相比之下,本研究通过利用有症状和无症状感染的数据,强调了无症状终身感染对乳制品行业生产行为和决策的重要但经常被忽视的影响(Harvey等人,2017;Cummings et al. 2018)。由于SDB的“同一个健康”含义,这一维度对SDB尤其重要,因为它在牛中的高流行率和抗生素耐药性构成了公共卫生威胁,可能导致爆发和大流行(Harvey等人,2017;Velasquez-Munoz et al. 2024)。将无症状感染纳入我们的数据可以提高我们对人畜共患疾病的经济负担的理解。首先,尽管没有明显的症状,但无症状携带者可以作为病原体的宿主,促进疾病传播和潜在的暴发(Nielsen et al. 2004;Harvey et al. 2017;Cummings et al. 2018)。其次,这些感染会严重影响管理实践和经济成果;没有意识到这一点的农民可能会忽视关键的生物安全措施,导致意外的生产力损失、兽医成本增加,并可能对人类健康产生重大影响(Helms等人,2003年;Harvey et al. 2017)。我们认为,认识到无症状病例的流行及其潜在的经济影响,可以改变农民对整体畜群健康的看法,从而产生更有效的管理策略,并最终降低与人畜共患疾病相关的经济风险。本研究利用一个独特的面板数据集,包括SDB抗体的检测结果(包括无症状感染)和丹麦所有奶牛场的生产统计数据,专门研究了SDB感染对乳制品行业农民生产行为的影响。论文的其余部分组织如下:第2节描述数据;第3节概述了实证策略;第4节给出了主要结果,包括稳健性检验;第5节详细介绍了使用丹麦数据的模拟练习;第6节讨论了结果;第7节介绍政策影响;最后一部分是对本论文的总结。在农场层面上,有几种方法可以用来解决深发展与经济成果之间关系的复杂性。先前的研究表明,数据中的大部分变化是农场特有的,因此不应归因于ODC水平的变化,而应归因于农场特有的特征(Nielsen et al. 2012a, 2013)。 因此,我们纳入了农场固定效应,因为它们控制了导致个体农场未观察到的异质性的任何时不变因素。农场固定效应的例子包括经营房屋的大小、地点、牛的品种、管理方法等等。本研究假设,在奶牛群中感染SDB会在多个维度上对经济表现产生不利影响。首先,我们预计SDB会降低产奶量,因为感染可能会损害奶牛的健康和生产力。其次,我们假设“新”感染的畜群与未感染的畜群相比,产奶量和小牛死亡率将出现更显著的下降。第三,我们预计SDB感染会增加小牛的死亡率,因为奶牛健康受损和新生小牛的SDB感染预计会降低小牛的存活率。最后,我们预计深发展将提高可变生产成本,特别是与兽医和医疗服务以及生物安全措施有关的成本。所有的模型规格都包括农场固定效应,α i ${\alpha _i}$,它解释了农场之间的时不变的未观察到的差异,例如,管理差异。季度固定效应η q ${\eta _q}$解释了每个季度影响所有农场的任何长期趋势(例如,环境法规,信贷限制或所有养牛场类似的技术进步)。为了捕捉固定效应中的潜在非线性,几乎所有规范都包括相互作用项“农场固定效应的样本年”,ω z t ${\omega _{zt}}$,即允许农场和年固定效应之间的相互作用。这种相互作用捕捉到任何年份不同的农场特有的系统变化,例如,农场规模的年度变化,每个农场每年爆发的疾病,等等。在农场固定效应和四分之一固定效应的模型中,相互作用效应的自然选择将是农场固定效应与四分之一固定效应相互作用。然而,由于自由度不足,我们选择使用农场固定效应与年固定效应相互作用来代替。此外,作为鲁棒性检查,我们包括使用农场固定效应与一年中的季度相互作用的结果,以捕捉季节性农场水平,这是不可观察的,因为组成产量可能不仅是品种的函数,而且还随着天气和饲料以及奶牛的整个生物周期而变化。最后,误差项ε i q ${\varepsilon _{iq}}$解释了各季度农场经济或生产表现中未观察到的随机变化。如上文数据部分所述,我们使用季度畜群水平面板数据来估计式(1)的各种规格。为了估计公式(2)的不同规格,观测值按年和农场水平汇总。使用STATA 17.0软件对两个回归方程进行估计。以下部分介绍了我们对SDB感染对奶牛场的经济后果的研究的主要发现。我们介绍了它对牛奶产量、小牛死亡率和农场生产成本的影响。表5中发现的散罐奶中SDB与产奶量之间的显著关系可用于评估放弃的总体收入,表9的结果可用于评估SDB带来的成本。考虑到SDB患病率的发展,我们使用最近10年的数据来评估表9所示的行业收入和成本。到2020年,丹麦共有56.9万头奶牛,其中大多数奶牛的ODC为零。放弃的总收入为750万欧元,整个行业的总成本为510万欧元。研究发现,到2020年,牛奶的平均价格为每公斤36.1欧分,其中90%是传统牛奶,其余10%是有机牛奶。可以评估表9中的行业成本,以指定不同成本组成部分的贡献。图3所示的成本组成部分的贡献表明,饲料成本的增加在与SDB相关的成本增加中所占的份额最大。 95%置信区间用竖线表示,表示在5%水平上统计上显著的参数估计,但在表9中的行业成本中,如果相关性在10%水平上显著,则包括成本。如果行业成本通过非线性(二元)模型评估,基于2020年相同数量的奶牛,放弃的总收入为620万欧元,也就是说,在非线性模型中,放弃的估计收入略低,但仍在相同的范围内,而总成本为每年610万欧元,因此高于具有离散ODC水平的模型(表9)。从监管的角度来看,了解深发展对乳制品生产的经济影响是确定适当措施的关键。如果该疾病造成重大损失,有关其负担和根除战略的信息可能是有效的。如果损失很小,可能需要更强有力的激励措施来解决其更广泛的“同一个健康”影响。本文采用丹麦所有奶牛场的牛奶中沙门氏菌抗体的独特面板数据集,首次对SDB对奶牛场的经济影响进行了全面的实证估计。研究发现,产奶量、小牛死亡率和总可变成本在畜群水平上与SDB相关。我们估计,感染SDB的畜群可能会经历每头奶牛每月最多13公斤的产奶量减少,根据每头奶牛每月833公斤的平均产奶量计算,这意味着1.6%的损失。产奶量的减少意味着每月每头奶牛的经济损失为5欧元,或每年每头奶牛的经济损失为58欧元。对于一群200头奶牛来说,这相当于每月损失970欧元。此外,如果兽群经历25 &lt;ODC & lt;40,为期6个月,预计将减少收入5600欧元。这些发现强调了预防和控制奶牛群SDB的重要性,以确保农民能够保持稳定的收入。然而,由于生产因素的可变性,以及各个农场之间的影响表现方式的差异,农民可能不会立即注意到这种财政影响。尽管与早期的研究(例如,Peters 1985;Velasquez-Munoz et al. 2024),该研究还发现较高的ODC水平与小牛死亡率增加之间存在很强的相关性。这或许可以解释为什么农民在ODC水平较低时往往不采取行动。由于小牛死亡率是农民最明显和最直接的担忧,在较低的ODC水平下缺乏这种影响可能会推迟干预,即使产奶量减少已经影响到农场的盈利能力。该研究还估计,与SDB感染相关的可变成本增加对农民来说可能是重大的。我们的模拟结果表明,经济负担估计的下限和上限在较高的ODC计数时扩大。对于一个拥有200头奶牛的典型农场来说,与没有SDB的奶牛相比,ODC的低水平(在0到10之间)估计会导致每年增加6700欧元的可变成本。与没有SDB的牧群相比,较大的ODC水平(在25至40之间)估计与每年11,300欧元的额外可变成本相关。这些增加的可变成本相当于每年每头奶牛总可变成本的1%-3%,估计为2800欧元。这凸显了采取措施预防和控制SDB感染的重要性,以尽量减少农民的额外可变成本。然而,需要注意的是,这些估计应该谨慎解释,因为SDB感染与生产结果之间的因果关系尚未精确确定。与其他研究的直接比较是具有挑战性的,但尼尔森等人(2012a)的最接近的研究与我们的发现不同,原因有几个。(i)我们的研究使用了2011年至2020年的数据,而Nielsen et al. (2012a)分析了2005年至2009年的数据。(ii) Nielsen等人(2012a)分析了奶牛水平的产奶量数据,而我们的研究强调了包含更广泛经济成果的畜群水平数据。这种方法使我们能够探索农场管理和生产行为的复杂性(Seegers et al. 2003)。(iii)他们的研究检查了一小部分ODC水平急剧上升的荷斯坦牛群样本,与ODC水平稳定的对照组相比,这可能解释了一些差异。虽然我们也分析了“新”感染的畜群,但我们发现产奶量与其他(可能未感染的)畜群相比没有显著差异。另一种可能的解释是,正如我们的研究结果所反映的那样,随着时间的推移,农民可能采取了更多的缓解措施,导致生产损失减少,但成本增加。不像Nielsen等人。 (2012a),我们还估计了SDB感染与小牛死亡率和生产成本之间的联系。另一方面,Nielsen et al.(2013)使用模拟模型预测深发展感染会导致更高的生产成本。然而,与我们的研究不同,他们依赖于模拟而不是对经验数据的统计分析,这可能会降低他们估计的可靠性。与其他动物疾病相比,即使在感染水平较低的情况下,SDB也会导致产奶量的显著减少,在这种情况下,奶牛作为携带者而不一定表现出急性症状。其他疾病,如副肺结核(由鸟分枝杆菌引起),在晚期需要更高的感染率才能产生类似的经济影响(Garcia和Shalloo, 2015)。乳腺炎主要在后期或严重疫情期间导致产奶量减少,经济损失随着感染的严重程度而增加(Seegers等,2003年;Hadrich et al. 2018),这些都不是人畜共患的。牛白血病病毒和口蹄疫等疾病也会造成重大损失,但通常是在感染的晚期阶段(Knight-Jones &Rushton 2013;Norby et al. 2016)。有趣的是,牛白血病病毒甚至可能出乎意料地增加产奶量(Yang et al. 2022)。然而,深发展的早期影响强调了早期发现和控制策略的迫切需要,以尽量减少生产损失及其重大的公共卫生威胁,因为该疾病导致12%的人类感染(Helms等,2003年)。即使可以获得大量高质量的数据,由于几个原因,捕获奶牛SDB感染与产量损失之间的关系仍然具有挑战性。首先,我们使用罐奶中的SDB抗体(群体水平观察)作为SDB感染的指标(奶牛水平观察),从而建立了SDB进入群体与罐奶复合物中ODC上升之间的时滞。尽管ODC是感染率的一个有用的指标,但它并不是一个完美的衡量标准。例如,散装牛奶检测很少产生假阳性,尽管交叉反应性或污染可能导致误导性结果。另一方面,牛乳的稀释和慢性携带者的弱抗体反应可能导致假阴性(Cummings et al. 2018)。因此,理想情况下,ODC应与其他诊断和生物安全措施一起使用,以更全面地了解畜群健康。此外,SDB可能不会同时感染牛群中的所有动物,这意味着在所有奶牛被感染之前,罐奶中的ODC可能会上升。奶牛感染SDB和ODC水平增加之间也可能存在延迟,因为最初的感染可能只涉及几头奶牛,使得牛群产奶量的下降不那么明显。我们测试了几个滞后和领先模型,但没有一个模型比没有这些变量的模型更适合模型。此外,由于我们缺乏每日产奶量记录,我们依赖于每月向奶牛场发货。我们最初的月度数据分析没有发现ODC变化与产奶量之间存在领先或滞后关系的证据,这与Nielsen等人(2012a)的结论一致。然而,ODC和生产产出之间的关系可能是不确定的,并且可能无法被我们的群体级模型完全捕获。我们还探索了“新”SDB感染与产量之间的潜在联系,但新感染的定义被证明具有挑战性,超出了本研究的范围。因此,生产损失数字是对畜群实际感染水平影响的粗略估计。其次,研究可以使用月度或季度数据来分析ODC,每种数据都有其优点和缺点。每月数据在时间相关性方面提供了更高的精度,但可能在数据收集中引入不确定性,例如产奶频率的变化。由于ODC数据仅按季度提供,因此该研究使用相同的频率来保持两个变量之间的兼容性,并减少有关送奶频率的不确定性。然而,由于汇总成季度数据,这种方法丢失了一些关于月度变化的信息。第三,使用固定效应模型为ODC对经济结果的解释力提供了强有力的证据。然而,它也有局限性,例如没有确定哪些农场特定因素(如农舍年龄、农场规模、品种或自动挤奶机的使用)对牛奶产量损失的影响最大,因为这些因素都包含在农场固定效应期限中。由于本分析侧重于ODC与农场经济成果之间的关系,未来的研究可以探索其他方法来调查除了ODC之外的其他因素对农场经济成果的影响。 该研究为SDB对农业经济的影响提供了新的证据,但未来的研究需要建立因果关系,增强研究结果的稳健性,并在奶牛层面提供更详细的见解,以更深入地了解这些影响。该研究强调了SDB感染给奶牛养殖场带来的经济挑战,影响牛奶产量、死亡率和运营成本。尽管对畜群的影响各不相同,可能不会立即引起注意,但即使在低患病率水平下,也迫切需要对SDB进行早期管理。深发展的无症状性往往导致农民低估其经济后果,降低了他们遵守国家根除努力的动力。农民可能会因为其他管理重点而忽视低感染水平,从而导致长期成本增加。为了应对这些挑战,我们建议采取以下措施:(i)遭受深发展严重损失的农场应获得有关经济影响和有效根除策略的针对性信息。对于那些损失最小的农户,考虑到一些农民可能没有意识到深发展的经济负担,政策措施应该提供实质性的激励措施,例如为预防工作和早期牛群检测提供补贴,或者为长期感染深发展的农场调整牛奶价格。(ii)应重新评估现有的基于ODC阈值的任意法规,因为即使低水平的SDB也可能与产奶量的显著损失有关。最后,实施包括定期检测在内的全面监测系统对于有效根除SDB至关重要。该系统应收集牛群和个体牛的数据,以确保完全了解疾病动态并准确估计部门负担。政策含义可以概括为,尽管在畜群/农场水平上发现ODC与产奶量之间存在显著相关性,但与小牛死亡率和可变成本的关联程度太低,无法有效激励农民预防和根除SDB感染并遏制人类感染。本研究使用了一个关于生产统计数据和储罐奶中SDB抗体水平的长面板数据集(以ODC水平表示)。通过应用高维固定效应模型,该研究最大限度地减少了内生性问题,并发现产奶量与SDB感染之间存在统计学上显著的相关性。具体而言,与ODC为0的奶牛相比,罐乳中ODC非为零的奶牛每月的产奶量损失约为8公斤。对于ODC水平高于55的畜群,估计产奶量损失增加到每头奶牛每月13公斤,相当于每头奶牛每年58欧元的收入损失,假设牛奶价格为每公斤40欧分。这些损失虽然比Nielsen等人(2012a, 2013)之前的研究发现的要小,但突出表明,即使ODC的小幅增加也与生产力损失有关。有趣的是,该研究并未发现“新”感染畜群的ODC与产奶量之间存在显著关联,这与Nielsen等人(2012a)的发现相反。这表明,只要ODC水平为正值,例如低于10 ODC, SDB就与产奶量损失相关,而不仅仅是在较高的阈值下,这表明需要制定更严格的规则,而不是现有的基于任意阈值的法规。这一发现具有政策意义,因为目前丹麦的监测计划隐含地建立在这样一种观念之上,即“新”感染的畜群将受到ODC高于25的经济后果的激励,而我们发现ODC和ODC之间存在相关性;0.除了产奶量减少之外,该研究还记录了犊牛死亡率的小幅上升,尤其是公牛犊牛,这与ODC水平高于0有关。例如,与ODC为0的牧群相比,ODC超过55的牧群每1000头活产小牛中有14头额外死亡。虽然这一增幅很小,但与较高的ODC水平(包括“新感染”)的相关性可能解释了当ODC水平较低时农民采取行动的延迟。由于犊牛死亡率是最明显的问题,即使产奶量减少已经影响到盈利能力,但在较低的ODC水平上缺乏犊牛死亡率可能会推迟干预。此外,研究结果表明,“新的”SDB感染与犊牛死亡率增加有关,但与产奶量无关,这表明犊牛可能比奶牛更容易受到“新的”SDB感染。除了整个牛群的预防措施外,还建议有针对性的干预措施,如接种疫苗,以降低小牛死亡率(Cummings等人,2019)。值得注意的是,这项研究并没有将SDB的影响与同时在畜群水平上实施的其他变化隔离开来。 例如,如果农民由于卫生水平的改变或整体管理绩效的提高而成功地减轻了牛奶产量损失,那么SDB在畜群中的孤立影响可能比提供的估计更大。最终,尽管ODC与产奶量、小牛死亡率和可变成本之间的畜群/农场水平相关性归因于SDB感染,但经济损失的规模太小,农民无法轻易发现,也无法充分激励他们有效预防和根除SDB感染并遏制人类感染。需要实施更强有力的激励措施来推动有效的行动。db和JVO对这项研究进行了概念化。JVO获得了数据。DB制定实证策略,对数据进行整理和可视化,并进行正式的计量经济学分析,JVO进行模拟研究。DB起草了手稿,而JVO通过编辑、验证和关键审查做出了贡献。两位作者讨论并验证了实证结果,并批准了手稿的最终版本。作者宣称他们没有竞争利益。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Agricultural Economics
Agricultural Economics 管理科学-农业经济与政策
CiteScore
7.30
自引率
4.90%
发文量
62
审稿时长
3 months
期刊介绍: Agricultural Economics aims to disseminate the most important research results and policy analyses in our discipline, from all regions of the world. Topical coverage ranges from consumption and nutrition to land use and the environment, at every scale of analysis from households to markets and the macro-economy. Applicable methodologies include econometric estimation and statistical hypothesis testing, optimization and simulation models, descriptive reviews and policy analyses. We particularly encourage submission of empirical work that can be replicated and tested by others.
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