Development of a decision support tool to compare diagnostic strategies for establishing the herd status for infectious diseases - An example with Salmonella Dublin infection in dairies

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Preventive Veterinary Medicine 228 (2024) 106234

Contents lists available at ScienceDirect

Preventive Veterinary Medicine


journal homepage: www.elsevier.com/locate/prevetmed

Development of a decision support tool to compare diagnostic strategies for


establishing the herd status for infectious diseases: An example with
Salmonella Dublin infection in dairies
Maryse Michèle Um a, b, c, Simon Dufour a, b, c, *, Luc Bergeron d, Marie-Lou Gauthier d, Marie-
Ève Paradis b, e, Jean-Philippe Roy b, f, Myriam Falcon g, Elouise Molgat h, André Ravel a
a
Department of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, Canada
b
Op+lait FRQNT Research Group, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, Canada
c
Research Group in Epidemiology of Zoonoses and Public Health, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, Canada
d
Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec, Canada
e
Association des Médecins Vétérinaires Praticiens du Québec, Saint-Hyacinthe, Québec, Canada
f
Department of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, Canada
g
Les Producteurs de lait du Québec, Longueuil, Canada
h
Lactanet, Sainte-Anne-de-Bellevue, Canada

A R T I C L E I N F O A B S T R A C T

Keywords: The diagnosis of infectious diseases at herd level can be challenging as different stakeholders can have conflicting
Multi-criteria decision analysis priorities. The current study proposes a “proof of concept” of an approach that considers a reasonable number of
Diagnostic criteria to rank plausible diagnostic strategies using multi-criteria decision analysis (MCDA) methods. The
Infectious disease
example of Salmonella Dublin diagnostic in Québec dairy herds is presented according to two epidemiological
Dairy herd
Salmonella Dublin
contexts: (i) in herds with no history of S. Dublin infection and absence of clinical signs, (ii) in herds with a
previous history of infection, but absence of clinical signs at the moment of testing. Multiple multiparty ex­
changes were conducted to determine: 1) stakeholders’ groups; 2) the decision problem; 3) solutions to the
problem (options) or diagnostic strategies to be ordered; 4) criteria and indicators; 5) criteria weights; 6) the
construction of a performance matrix for each option; 7) the multi-criteria analyses using the visual preference
ranking organization method for enrichment of evaluations approach; 8) the sensitivity analyses, and 9) the final
decision. A total of nine people from four Québec’s organizations (the dairy producers provincial association
along with the DHI company, the ministry of agriculture, the association of veterinary practitioners, and experts
in epidemiology) composed the MCDA team. The decision problem was “What is the optimal diagnostic strategy
for establishing the status of a dairy herd for S. Dublin infection when there are no clinical signs of infection?”.
Fourteen diagnostic strategies composed of the three following parameters were considered: 1) biological
samples (bulk tank milk or blood from 10 heifers aged over three months); 2) sampling frequencies (one to three
samples collection visits); 3) case definitions to conclude to a positive status using imperfect milk- or blood-ELISA
tests. The top-ranking diagnostic strategy was the same in the two contexts: testing the bulk tank milk and the
blood samples, all samples collected during one visit and the herd being assigned a S. Dublin positive status if one
sample is ELISA-positive. The final decision favored the top-ranking option for both contexts. This MCDA
approach and its application to S. Dublin infection in dairy herds allowed a consensual, rational, and transparent
ranking of feasible diagnostic strategies while taking into account the diagnostic tests accuracy, socio-economic,
logistic, and perception considerations of the key actors in the dairy industry. This promising tool can be applied
to other infectious diseases that lack a well-established diagnostic procedure to define a herd status.

* Corresponding author at: Department of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, Canada.
E-mail address: simon.dufour@umontreal.ca (S. Dufour).

https://doi.org/10.1016/j.prevetmed.2024.106234
Received 13 March 2024; Received in revised form 26 April 2024; Accepted 18 May 2024
Available online 24 May 2024
0167-5877/© 2024 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

1. Introduction qualitative and quantitative indicators are used for criteria along with
mathematical equations, which improves rationality; (iv) all judgements
Infectious diseases continue to represent a threat to dairy production of stakeholders are emphasized through weights that are attributed to
in terms of animal health, public health, and economic losses (Ras­ each criterion; (v) mathematical optimization, algorithms and advanced
mussen et al., 2021; Drewe et al., 2023). Determining herd-level status scientific computing are used to rank the potential solutions (Dodgson
for certain diseases plays a key role in deciding the prevention and et al., 2009). The MCDA methods have been widely used in management
control measures to put in place (e.g. on the occasion of animal trade, science and various areas of engineering (Wiecek et al., 2008). Their
herd management, organization of pasteurization circuits, biosecurity application in the field of animal or public health has been increasing
measures, etc.); it relies on effective diagnostic approaches. However, over the last decade, notably for ranking pathogens or diseases in certain
for some diseases, diagnostic challenges persist even where efforts for contexts (Cox et al., 2013; Hongoh et al., 2017) or for identifying and
implementing surveillance and control programs have been put in place assessing options for surveillance and control programs (e.g. Lyme dis­
for decades (Nielsen et al., 2021; Nobrega et al., 2023). These challenges ease, foot-and-mouth disease, bovine tuberculosis) (Aenishaenslin et al.,
are often associated with the availability of only imperfect tests (anti­ 2013; Corbellini et al., 2020). Its application to compare diagnostic tests
bodies-, culture-, PCR-based approaches on aggregated or individual in human medicine or potential diagnostic strategies for establishing the
samples), the chronic nature of some diseases and absence of clear herd status for infectious diseases is more recent (Sayan et al., 2020;
clinical signs, the pathogenesis of the agent involved and the difficulty to Guetin-Poirier et al., 2022). The MCDA methods allow the conception of
sometimes define the “carrier state” of an infected individual. These frameworks that are reusable and updatable according to the
difficulties have considerable consequences (direct costs to the pro­ decision-making context. There is clearly a need for such reproducible
ducers, impacts due to misclassification errors like “culling false-positive and transparent decision-making process in the field of diagnostic of
animals”, compromised trades, disruption in milk collection associated animal infectious diseases.
with false-positive results; or risky trades, herds escaping authorities’ The objectives of the study were: 1) to develop a MCDA tool that
interventions due to false-negative results). could be used to compare diagnostic strategies aiming at establishing the
The implementation of a diagnostic strategy aiming at establishing herd status for infectious diseases in dairies and in different epidemio­
the herd-level status for an infectious disease requires an optimal se­ logical contexts (e.g. herds with or without history of known previous
lection of: the age of tested animals, the number of animals tested, the infection); and 2) to compare, using that latter tool, diagnostic strategies
optimal timing with regards to the infection curve, the type of biological for establishing the herd status for S. Dublin infection in the two
samples collected, the tests used, and the epidemiological contexts of the different contexts.
disease (Um et al., 2022). Salmonella Dublin infection in dairy cattle
exemplifies all the latter challenges. In young animals, the infection 2. Materials and methods
often causes non-specific enteric signs, respiratory signs, and sudden
death due to septicemia. In adults, it can lead to abortion. In many herds, This study, hereafter named the MCDA project, was conducted be­
however, the disease is mostly subclinical. The bacteria is host-adapted, tween June 2021 and April 2023. The study was part of a larger project
and thus, generates subclinical carriers among cows, making their entitled “Validation of bulk tank milk sampling strategies and identifi­
identification more complicated for veterinary practitioners and pro­ cation of risk factors for Salmonella Dublin in dairies” hereafter called S.
ducers (Nielsen, 2013). Dublin project with the overall objectives of suggesting a diagnostic
In the Québec province, Canada, the S. Dublin emerged in 2011 in strategy for determination of the herd-level S. Dublin status in dairies
dairy cattle and continues to spread in dairy herds (RAIZO, 2022). The and identifying farm-level risk factors for S. Dublin infections (Um et al.,
diagnosis of S. Dublin can be carried out by demonstrating the presence 2020, 2022, 2023). The current part of that larger study received the
of the bacteria in clinical or necropsy samples by culture or PCR or, in approval of the Université de Montréal’s Science and Health Research
the absence of clinical signs in the herd, with the measurement of an­ Ethics Committee (or Comité d’éthique de la recherche en science et en
tibodies for S. Dublin using an ELISA test performed on bulk tank milk santé de l’Université de Montréal), project number 2022–1629.
and/or individual animals blood samples (MAPAQ, 2023), as it is done MCDA actually encompasses a variety of methods with different
in other countries where the disease is endemic (Agren et al., 2018; approach and technical features (Greco et al., 2016). For this project, we
Holschbach and Peek, 2018). However, both ELISA tests (i.e. on milk chose the preference ranking organization method for enrichment of
and blood) are imperfect (Um et al., 2022). It appears that all the evaluations (PROMETHEE) because of its simplicity in conception, its
aforementioned considerations to select a diagnostic strategy could clearness, and its user-friendly features (Brans et al., 1986; Behzadian
represent divergent issues for the potential parties dealing with the et al., 2010). This outranking method consists in pairwise comparisons
disease (i.e. economic losses for dairy producers, false positive and/or of the options to solve a problem according to evaluation criteria and
false negative results for animal health authorities, etc.). For example, preferences of the stakeholders, which is more intuitive than defining
for dairy producers, the preference could go to one bulk tank milk “what is good” and “what is bad” (Mareschal, 2013). We followed and
testing every six months as it is a less costly, and time-saving approach. adapted the steps proposed to guide the MCDA process (Aenishaenslin
While, for animal health authorities, the preference could be a combi­ et al., 2019). Table 1 lists these steps whereas the following sections
nation of blood testing from non-milking animals (heifers) and bulk tank detail each of them.
milk testing with a requirement that at least one test should be positive
to consider the herd S. Dublin-positive, even though, this strategy could 2.1. Identifying the participating stakeholders
be more expensive and logistically more demanding than the latter.
To aid decision-makers in adopting a compromise for the diagnostic The initial concern of the S. Dublin project participants that led to
strategy to be implemented, methods such as multi-criteria decision undertake the MCDA was about recommending a diagnostic strategy for
analysis (MCDA) can be used. It considers various and sometimes con­ establishing the status of a dairy herd for S. Dublin infection when there
flicting perspectives. It originates from the field of operational research are no clinical signs of infection and in a context where no nationwide
(Keeney and Raiffa, 1976) and allows comparing and ranking potential surveillance for such infection had been planned. The goal was to help
solutions to a problem without an obvious solution according to several the veterinarians in using a common and optimal strategy when their
defined criteria. Its advantages are that: (i) stakeholders from all sectors dairy clients want to know their herd’s status for this infection.
with different ideas and preferences about a solution can present their To identify the relevant stakeholders, the MCDA project coordinator
views, which brings transparency in decision-making; (ii) measurable (i.e. the first author) invited all S. Dublin project participants to a
criteria are used to compare solutions favoring reliability; (iii) meeting. During that meeting, they used the rainbow diagram tool

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Table 1 order to come up by consensus with a more specific statement of the


Steps for a multi-criteria decision analysis and the main outputs of its application decision problem that was at stake. More specifically, the context
for recommending a diagnostic strategy in Québec, Canada for establishing the included the epidemiology of the disease in Québec dairy herds as
status of a dairy herd for Salmonella Dublin (S. Dublin) infection when there are known from the surveillance of clinical cases and the findings of the
no clinical signs of infection. larger S. Dublin project. Of interest, those sources of information esti­
Steps Outputs mated the herd-level S. Dublin prevalence at 6.8% in a convenience
1. Identifying the participating Four organizations: sample of dairy herds in Québec, but at 25% in herds with a previous
stakeholders 1) the dairy producers of Québec along with history of this latter infection (Um et al., 2022), suggesting at least two
the private dairy herd improvement epidemiological contexts for the disease in Québec.
company in charge of individual and bulk
milk analyses and diagnostic in dairy cattle
sector (PLQ); 2.3. Defining the options
2) the ministry of agriculture. fisheries and
food of Québec (MAPAQ); The MCDA team brainstormed on the potential diagnostic strategies
3) the association of veterinary practitioners that could be used in these two contexts for establishing the herd status
of Québec (AMVPQ);
4) epidemiologists from the veterinary faculty
for S. Dublin infection in the absence of clinical signs. The discussion
(FMV) was informed by practical aspects, by the findings of the ongoing S.
With 2 representatives for each organization + Dublin project (Um et al., 2020, 2022, 2023), the availability of labo­
1 coordinator ratory tests in Québec, the testing procedures already used by the pro­
2. Refining the decision problem One general question: what is the optimal
vincial animal health authorities in case of clinical signs of S. Dublin
diagnostic strategy for establishing the status
of a dairy herd for S. Dublin infection when infection in dairy cattle (MAPAQ, 2023), and the S. Dublin surveillance
there are no clinical signs of infection? programs in place in northern European countries that have been
Two contexts: dealing with S. Dublin infection for decades (Jordan et al., 2008; Niel­
sen, 2013; Agren et al., 2018). Full consensus was the rule for deciding
1) herds with no previous history of S. Dublin
infection
on the diagnostic strategies to include into the MCDA.
2) herds with history of S. Dublin infection
3. Defining the options for the 14 diagnostic strategies (Fig. 1) 2.4. Defining criteria and indicators
diagnostic strategy
4. Defining the criteria and their 10 criteria and their indicator (Table 2 and
The MCDA team brainstormed on the main issues and concerns they
indicators Table S1)
5. Weighting the criteria The criteria weights determined by each had about the future diagnostic strategy, i.e. what could bother the
participating stakeholder and those reached by stakeholders, what feature the strategy should have or avoid for facili­
consensus (Table S2) tating the implementation and the usefulness of the strategy. For
6. Assessing the performance of The performance matrix (Table 3) example, cost, delay, and diagnostic precision are usual concerns when
each option on each criterion The preference functions (Table S3)
7. Multicriteria analysis based on The option profiles (Fig. 2)
selecting a diagnostic strategy. Each MCDA team member had the op­
PROMETHEE The option net outranking flow and their portunity to express its concerns and perceptions on the features that the
ranking by participating stakeholders (Table 4) diagnostic strategy should fulfill. Through discussion, a set of common
Map of the relative positioning of criteria and and shared general issues and concerns was defined by full consensus.
options (GAIA) (Fig. 3)
Then the MCDA team further defined these general issues and concerns
Map of the relative positioning of participating
stakeholders and the options (Fig. 4) into a number of potential criteria (usually a few criteria per issue) that
8. Sensitivity analysis No important differences within and between would be the basis for comparing the diagnostic strategies. All proposed
the participating stakeholders were identified ( criteria were explained, discussed, and appraised according to three
Figs. 3 and 4). rules: 1) each criterion must be relevant to the decision problem, which
9. Decision on the optimal Two diagnostic strategies recommended and
diagnostic strategy another one found interesting under certain
was comparing diagnostic strategies; 2) each criterion must be associ­
circumstances (see text). ated with a measurable (quantitatively or qualitatively) characteristic of
the diagnostic strategies; and 3) the value for the criterion should differ
for at least two diagnostic strategies. Every general issue or concern
(Chevalier and Buckles, 2008) for the collective identification of the needed to have at least one criterion, and the team aimed at limiting the
relevant stakeholders to participate into the MCDA. Stakeholders were total number of criteria to 10–15. The decision about the final list of
defined as key collective actors (i.e. not individual but organization or general issues or concerns and the final list of criteria had to be
group of actors sharing the same interest and stake) who could be consensual.
affected by the decision (e.g. those applying the diagnostic strategy or The MCDA team then defined the indicator (i.e. how the criterion is
dealing with the herd status resulting from the diagnostic strategy, or measured precisely) for each criterion and determined its measurement
who could influence its development). The meeting participants iden­ scale, which had to be specific, measurable, applicable, realistic, and
tified all potential stakeholders and used the rainbow diagram to char­ timely. Full consensus was, again, used to finalize all indicators and
acterize each along two dimensions: the most, the moderately or the scales. The MCDA team also determined whether the value of each in­
least affected stakeholders, and the most or the least influential stake­ dicator should be maximized or minimized (i.e. the desirable outcome
holders. The coordinator then invited all identified organizations as the for the indicator) in the subsequent MCDA analysis.
most influential and either the most or moderately affected stakeholders
to participate into the MCDA project. The participating stakeholders 2.5. Weighting the criteria
plus the MCDA coordinator are referred as to the MCDA team. The
MCDA team then participated to each of the next steps by holding The fixed-point allocation method was used to quantify the criteria
meetings and sharing documents. weights according to a two-step hierarchical process (Aenishaenslin
et al., 2019). It was applied for each context separately. First, each pair
2.2. Refining the decision problem of representatives of a given participating stakeholder distributed 100
points over the general issues or concerns identified. Second, they
The MCDA team reflected on the problem as initially stated, ac­ distributed 100 points over the criteria included within each issue. The
cording to the context of S. Dublin dairy herd infections in Québec, in final criterion weight for each stakeholder was the multiplication of each

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

criterion weight within the issue by the corresponding issue weight. detected whether the ranking of the five top options changed using the
Then, the whole MCDA team met, evaluated and compared the different Walking Weights tool in Visual PROMETHEE. In addition, we assessed
stakeholder’s weighting proposal, and reached a consensus on an overall whether the range of weights of an option, within which the five top
weighting scheme. The subjective weighting method was selected outranking options stayed the same, was below 4 points using the Sta­
among the various weighting methods available because of its easiness bility Intervals tools. The threshold of 4 points was set by considering a
to implement (Nemeth et al., 2019) and because it provides similar re­ 20% uncertainty in the weight value for a uniform distribution of weight
sults to more objective or more sophisticated methods (van Til et al., (i.e. - and +20% of the 100 total allocated points/10 criteria means a
2014). range of 8–12 points). All this was undertaken for each criterion and for
each participating stakeholder plus the consensual weighting. Finally,
2.6. Assessing the performance of each option on each criterion we used the GAIA Decision-Maker-Brain for each stakeholder partici­
pant to assess the sensitivity of its decision axis to the criterias’ weights
The performance was assessed diversely depending on the indicators. (Brans and De Smet, 2016). This tool automatically computes the deci­
The value for each option was directly computed for some indicators, sion axis based on a range of weights instead of a single value and
computed based on the findings of the S. Dublin project for others, or projects them as an ellipse on the GAIA plane. The outranking is robust
appraised through specifically designed research tools (e.g. survey). This when the ellipse does not include the origin of the plane. The range for
step yielded all the information needed for the performance matrix, i.e. a the varying weights was set at 25% of its value (e.g. if the weight is 8%,
grid summarizing the value of each diagnostic strategy on each criterion. the range was set to vary between 6% and 10%).

2.7. Multi-criteria analyses 2.9. Final decision

Basically, the multi-criteria analysis with PROMETHEE first consists Informed by the numerous outputs of the results, the MCDA team
in comparing each pair of diagnostic strategies on all criteria yielding met and discussed about the optimal diagnostic strategy to recommend
unicriterion scores based on the values in the performance matrix. Those and decide on the optimal diagnostic strategy, again by full consensus.
pairwise comparisons require the definition of the preference function
for each criterion. The preference function determines the extent of the 3. Results
preference of one diagnostic strategy over another by setting the mini­
mal difference between the two values to state that one diagnostic 3.1. Problem, stakeholders, criteria, performance matrix
strategy is preferred over another, the shape of the relation between the
difference and the degree of outranking, and the maximal difference 3.1.1. The participating stakeholders
between two values for considering that the maximum degree of out­ Results from the stakeholders’ identification exercise are provided as
ranking is reached. A unicriterion score can be positive, indicating that supplementary materials (https://doi.org/10.5683/SP3/87HRGH).
overall, the diagnostic strategy outranked most of the others; it can be Initially, the rainbow diagram led to consider 18 different stakeholders.
negative, indicating that, overall, the diagnostic strategy is outranked by Four were identified as “the most influent and the most affected”: the
most of the others. Second, the analysis aggregates all unicriterion scores dairy producers of Québec or les Producteurs de Lait du Québec - PLQ;
of a given diagnostic strategy into an overall net outranking flow using the beef producers of Québec or les Producteurs de Bovins du Québec -
the criteria weights. The diagnostic strategies can then be ranked ac­ PBQ; the ministry of agriculture, fisheries and food of Québec or Min­
cording to their net outranking flow values. More details of the com­ istère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec -
putations behind the analysis have been well described (Brans and De MAPAQ; the association of veterinary practitioners of Québec or Asso­
Smet, 2016). We used Visual PROMETHEE (software package Academic ciation des Médecins Vétérinaires Praticiens du Québec - AMVPQ. Four
version 1.9) (Mareschal, 2013) to perform all analyses. In addition, this were identified as “the most influent, but moderately affected”: the
software allows displaying the analysis outputs in a variety of tabular private DHI company in charge of individual and bulk milk analyses and
and graphical formats, which are helpful to interpret the results mean­ diagnostics in dairy cattle sector or Lactanet; epidemiologists from the
ingfully. One interesting tool is the Geometrical Analysis for Interactive veterinary faculty of the Université de Montréal or Faculté de Médecine
Aid (GAIA). It allows, among other things, projecting the options and the Vétérinaire - FMV; the Québec dairy breeds council or Conseil Québécois
criteria values after a principal component analysis of the performance des Races Laitières - CQRL; and the cattle auctions of the province of
values, yielding a bi or tri dimensional plane with the greatest variance, Québec. After further discussions, the dairy producers of Québec and the
and is helpful to explore the proximity between diagnostic strategies, the DHI company were considered as stemming on the same group of in­
independence between the criteria, and the relationship between the terest, that of the dairy industry, and were kept together under the same
diagnostic strategies and the criteria. In addition, GAIA allows the vector stakeholder’s name PLQ. All those identified organizations were offi­
of the weighted criteria (referred as to the decision axis) to be shown on cially invited to be part of the MCDA project. Three declined the invi­
the same plane, thus highlighting toward which diagnostic strategy the tation: PBQ, CQRL, and the cattle auctions. Therefore, eight
decision points out. Note that, except for the decision axis, the GAIA representatives from four organizations plus the MCDA project coordi­
plane is the same for any stakeholder. Finally, with GAIA, the net out­ nator were included as part of the MCDA team (Table 1).
ranking flows of the various stakeholders can be aggregated and dis­
played on another plane showing the extent of divergence between 3.1.2. The decision problem refined
stakeholders on their ranking of the options under evaluation. To make The decision problem was refined as “What is the optimal diagnostic
our results reproducible, the completed Visual PROMETHEE files (n=2; strategy for establishing the status of a dairy herd for S. Dublin infection
one per context) are available at https://doi.org/10.5683/S when there are no clinical signs of infection?”. The term diagnostic
P3/87HRGH. strategy represented the combination of sampling strategies (i.e. bio­
logical material collected, number of tests, number of animals, animals’
2.8. Sensitivity analyses categories, frequency of sampling) and the tests to be used (i.e. type,
interpretation, thresholds, case definition). In addition, the MCDA team
Since the preference flows are linear functions of the weights of emphasized two different contexts for which the decision problem had
criteria, sensitivity analyses on the criteria’s weights are critical. to be worked out (Table 1): the “No S. Dublin history” context (i.e. for
Focusing on the top five diagnostic strategies, we modified the weight of herds without a known history of S. Dublin infection), and the “With S.
one criterion at a time (by adding -5–5 points to its value) and visually Dublin history” context (i.e. for herds with a previously confirmed

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

history of infection, but still in absence of obvious clinical signs at the considerations (two criteria), and perception of producers and veteri­
moment of testing). narians (two criteria). Their corresponding indicators, measurement
scales, direction relative to the decision (maximization or minimiza­
3.1.3. The options included tion), and computation methods or source are presented in supple­
The options for the diagnostic strategies were composed of three key mentary Table S1. Eight indicators were measurable on a quantitative
elements: 1) the biological sample (i.e. either bulk tank milk or blood continuous scale, while two were measurable on a categorical ordinal
from 10 heifers aged over three months); 2) the sampling frequency (i.e. scale.
from one to three samples collection visits); 3) the case definition The weight for the criteria varied between the participant stake­
required to classify a herd as S. Dublin-positive (i.e. the number of test- holders and differed between the two disease-diagnostic contexts (sup­
positive bulk tank samples and/or seropositive heifers to consider a herd plementary Table S2). Overall, most of the weight was attributed to the
as positive). Only one type of laboratory test was considered for both diagnostic considerations (range: 30–55%) and least to the logistic
milk and blood samples: the ELISA test (PrioCHECK™ Salmonella Ab consideration (range: 5–25%). At the criterion level, the following
Bovine Dublin) with the same cut-off set at PP% ≥ 35. The MCDA team criteria received the largest consensual weight when the diagnosis
identified 14 options for the diagnostic strategies (Fig. 1). They were the strategies were applied to herds without a previous history of S. Dublin:
same for both disease contexts. For strategies relying on multiple visits, impacts of diagnostic error (15%) and value of a negative diagnostic
the time intervals between two successive sampling visits were set to be (13.5%). When the diagnostic strategies were applied to herds with a
one month for strategies involving only bulk milk samples or six months previous history of S. Dublin, then the largest consensual weights were
whenever two blood samples visits were encompassed. obtained for impacts of diagnostic error (17.5%) and the representa­
tivity of the sampling (12.5%).
3.1.4. The criteria proposed and their weighting
The MCDA team agreed upon 10 criteria grouped into four general 3.1.5. The performance of each diagnostic strategy
issues or concerns. The criteria were similar for the two contexts The value of each diagnosis strategy for each criterion is displayed in
(Table 2). The identified issues were: diagnostic considerations (four the performance matrix (Table 3). Some performances obviously were
criteria), socio-economics considerations (two criteria), logistics identical for some criteria between the diagnosis strategies that shared a

Fig. 1. The 14 diagnostic strategies evaluated in a MCDA analysis for establishing the dairy herd status for Salmonella Dublin infection.

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Table 2
Concerns, criteria, and indicators proposed for a multicriteria analysis in order to compare diagnostic strategies and ultimately establish the dairy herd status for an
infectious disease (Salmonella Dublin in this case).
Issue or concern Criteria (code) Definition Indicator

Diagnostic Value of a positive diagnostic Probability that a positive result is correct Positive predictive value (PPV)
considerations (1_VD+)
Value of a negative diagnostic Probability that a negative result is correct Negative predictive value (NPV)
(2_VD-)
Credibility of predictive values Level of certainty in the two preceding parameters Sum of the width of the 95% credibility interval of the PPV and
(3_Credibility) NPV
Representativity of the sampling The extent to which the sampling strategy A categorical variable defined by the biological samples collected
(4_Representativity) represents different groups of animals in the herd (milk vs. blood vs. milk and blood) and the number of sampling
vs. a fraction of the animals visits (1 vs. 2 vs. 3 visits)
Socio-economic Operational costs The costs associated with the sampling strategy Costs in $ for producer time, veterinarian fees, and laboratory
considerations (5_Costs) analyses
Impact of diagnostic errors Societal and economic consequences associated Misclassification cost terms according to the epidemiological
(6_Impacts) with diagnostic errors context (Um et al., 2023)
Logistic Delay before final results Time needed to obtain the diagnostic Number of days before obtaining the diagnostic
considerations (7_Delay)
Mobilization of human resources Human resources needed in the field to collect A categorical variable representing the human resources
(8_Resources) samples involved (producers vs. veterinarians vs. both)
Perception Level of producers’ acceptability The extent to which the veterinarian will get the Veterinarian’s perception regarding the acceptability of the
(9_Acceptability) buy-in from the producers regarding the diagnostic diagnostic strategy by producers
strategy
Level of simplicity of results’ Ease for the veterinarian to determine and Acceptability by veterinarians of the diagnostic strategy’s case
interpretation by veterinarians communicate results to the producer definition
(10_Simplicity)

diagnostic strategy feature (e.g. the number of visits, the type of sample maximal for the strategies based on milk and blood samples (M+B).
tested). Briefly, the value of a positive diagnostic varied between 28.1% Conversely, strategies based on one or two milk sample collection visits
and 92.6% (mean 49.4%) for herds with no previous S. Dublin infection performed very well on the other three issues (i.e. socio-economic
history and between 71.2% and 98.7% (mean 84.5%) for herds with a consideration, logistic consideration, and perception) compared to
previous S. Dublin history. Similarly, the value of a negative diagnostic strategies based on milk and blood samples. After taking into consid­
ranged between 95.4% and 99.3% (mean 96.9%) for herds with no eration the criteria weight and the relative performance of each option,
previous S. Dublin infection history and between 76.5% and 95.5% four options clearly ranked amongst the top options for almost all
(mean 83.5%) for herds with a previous S. Dublin history. The credi­ participating stakeholders: 1(M+B):1or1, 1(M+B):1or2, 3 M:1, and
bility of predictive values criteria varied from 31.2% to 94.3% (mean 1 M:1 by decreasing order of their net outranking flows (Table 4).
67.5%) for herds with no previous S. Dublin infection history and from The GAIA plane has a good representativity (76% on the first two
22.9% to 87.6% (mean 56.1%) for herds with a previous S. Dublin his­ axes) and was clearly split into two groups (Fig. 3A). The strategies
tory. Five scores (from very poor to very good) were possible for the based on milk samples were spread out in the left part, whereas the other
representativity of the sampling criteria, and three scores (low, moder­ (blood samples or combinations of bulk milk and blood samples) were
ate, and high) were possible for the mobilization of human resources on the right part with the exception of option 1(M+B):1or2. Three
criteria. Seven different values were obtained for the operational costs criteria relative to the diagnostic issue (value of a negative diagnostic,
criteria (13.50, 27.00, 40.50, 297.90, 311.40, 598.80, and 622.80 CAD), credibility of predictive values, and representativity of the sampling)
while four different values were obtained for the delay before final re­ were clustered together and were in opposition with the impact of
sults criteria (7, 37, 67, and 187 days). Impact of diagnostic errors diagnostic errors and mobilization of human resources criteria. The two
ranged from 0.031 to 0.101 (mean 0.057) for herds with no previous S. perception criteria (level of producers’ acceptability and level of
Dublin infection history and from 0.15 to 1.147 (mean 0.729) for herds simplicity of results’ interpretation by veterinarians) were clustered
with a previous S. Dublin history. Level of producers’ acceptability together on the GAIA plane and they pointed, with the delay before final
varied between -0.9 and 4.9 (mean 2.3) for herds with no previous S. results criterion, in the opposite direction as compared to the value of a
Dublin infection history and between 0.0 and 6.0 (mean 3.3) for herds positive diagnostic criterion.
with a previous S. Dublin history. Level of simplicity of results’ inter­ According to the sensitivity analysis, the ranking of the five top
pretation by veterinarians ranged from -0.9–6.2 (mean 3.3) for herds outranking options was very robust to changes in the weights stake­
with no previous S. Dublin infection history while it ranged from holders attributed to the criteria. There were no major divergent views
-2.5–6.0 (mean 1.8) for herds with a previous S. Dublin history. between the participating stakeholders on the best options (Fig. 4A).

3.2. The multi-criteria analyses 3.2.3. Results when testing herds with a previous S. Dublin infection history
The performances of the strategies for this context were slightly
3.2.1. The preference functions different compared to those for herds with no previous S. Dublin
The preference functions used were linear or V-shaped with small infection history (Fig. 2B). Taking into account the weight, the same
preference thresholds whereas the indifference thresholds were set to strategies ranked amongst the top four options for all participating
cover the full range of the criterion values (Supplementary Table S3). stakeholders: 1(M+B):1or1, 2(M+B):(1or1)OR(1or1), 1(M+B):1or2,
and 1B:1 (Table 4). The GAIA map has a good representativity (75% on
3.2.2. Results when testing herds with no previous S. Dublin infection the first two axes). It suggested that strategies based on milk testing only
history tend to cluster together and were aligned with lower costs and less
According to the pairwise comparisons, the performances of the 14 resource (Fig. 3B). Strategies based on two visits of blood testing were
diagnostic strategies on the 10 criteria varied considerably (Fig. 2). aligned with greater delay and lower acceptability, and possibly lower
Worth noting, the performances related to the diagnostics issue were simplicity. The four criteria related to the diagnostic consideration and
relatively minimal for the strategies based on bulk milk samples (M) and the criterion impact of diagnostic errors were almost aligned and in the

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Table 3
Performance matrix comparing the 14 options against the 10 criteria for the two contexts of interest (herd with or without history of known previous infection by
Salmonella Dublin).
Diagnostic strategiesa Context Diagnostic considerations Socio-economic Logistic considerations Perception
considerations

1_VD+ 2_VD- 3_Credi- 4_Repre- 5_Costs 6_Im- 7_De- 8_Resources 9_Accep- 10_Sim-
bility sentati- pacts lay tability plicity
vity

% % %Points Score CAD Score Days Score Score Score

1 M:1 No History 46.1 96.1 74.1 Very poor 13.5 0.052 7 Low 4.9 4.4
With 84.4 79.4 46.2 Very poor 13.5 0.969 7 Low 6.0 4.3
History
2 M:1 No History 34.4 96.4 86.2 Poor 27 0.064 37 Low 4.9 3.8
With 76.9 80.9 87.6 Poor 27 0.881 37 Low 5.8 4.0
History
2 M:2 No History 50.8 95.6 92.0 Poor 27 0.050 37 Low 3.3 3.8
With 86.7 77.4 76.2 Poor 27 1.095 37 Low 5.0 0.3
History
3 M:1 No History 38.1 96.8 82.8 Moderate 40.5 0.062 67 Low 3.8 6.2
With 79.6 82.5 77.5 Moderate 40.5 0.792 67 Low 5.5 5.3
History
3 M:3 No History 40.9 95.4 93.3 Moderate 40.5 0.052 67 Low -0.9 -0.9
With 81.4 76.5 85.6 Moderate 40.5 1.147 67 Low 3.0 -2.5
History
1B:1 No History 49.2 97.4 75.2 Very poor 297.9 0.051 7 Moderate 1.3 4.0
With 86 85.5 53.2 Very poor 297.9 0.150 7 Moderate 3.0 1.3
History
1B:2 No History 77.4 96.1 66.3 Very poor 297.9 0.042 7 Moderate 2.7 3.8
With 95.6 79.7 31.2 Very poor 297.9 0.954 7 Moderate 4.5 2.3
History
2B:1 or 1 No History 28.1 98.1 55.9 Poor 595.8 0.101 187 Moderate 0.7 3.1
With 71.2 88.9 75.8 Poor 595.8 0.495 187 Moderate 0.0 1.8
History
2B:2 and 2 No History 49.9 95.5 94.3 Poor 595.8 0.050 187 Moderate -0.9 1.3
With 86.3 76.9 84.2 Poor 595.8 1.121 187 Moderate 0.5 -0.3
History
1(M+B):1 or 1 No History 44.8 98.1 44.6 Good 311.4 0.057 7 High 3.8 4.7
With 83.7 88.8 38.4 Good 311.4 0.482 7 High 4.0 3.5
History
1(M+B):1 or 2 No History 54.6 97.0 56.7 Good 311.4 0.046 7 High 3.8 4.2
With 88.4 83.8 33.0 Good 311.4 0.726 7 High 5.3 3.0
History
2(M+B):(1 or 1) No History 35.7 99.3 36.8 Very good 622.8 0.085 187 High 3.1 3.6
OR(1 or 1) With 77.9 95.5 36.3 Very good 622.8 0.224 187 High 0.8 3.0
History
2(M+B):(1 or 1) AND(1 No History 92.6 97.0 31.2 Very good 622.8 0.031 187 High -0.4 1.1
or 1) With 98.7 83.5 22.9 Very good 622.8 0.741 187 High 1.0 -1.8
History
2(M+B):(1 or 2) No History 48.6 98.3 55.8 Very good 622.8 0.052 187 High 1.8 3.3
OR(1 or 2) With 85.7 89.9 37.5 Very good 622.8 0.433 187 High 2.0 0.9
History
a
The code used for the diagnostic strategies is: the number and the letter prior to the colon give the number of sample collection visits and the type of sample (blood
of 10 young animals (B), bulk milk (M) or both sample types (M+B)), respectively; the number of tests that has to be positive to attribute a positive status to the herd
depending on the diagnostic strategy is after the colon (i.e. 1 bulk milk tests and/or 1 or 2 seropositive animals out of 10 tested per visit).

opposite direction of the strategies based on milk testing only. The in the absence of clinical signs of the disease, we can expect that one out
ranking of the options by the participating stakeholders was very robust of two positive results will be a false positive (positive predictive value
to changes in the weights they attributed to the criteria and there were of 44.8%; Um et al., 2023).
no major divergent views between the participating stakeholders on the For testing herds with a previous S. Dublin history, the MCDA team
best strategies (Fig. 4B). concluded that the diagnostic strategy 1(M+B):1or1 was the most
relevant. However, the MCDA team also concluded that the diagnostic
strategy 2(M+B):(1or1)OR(1or1) (an approach similar to the previous
3.3. Final decisions one but requiring a repetition of the tests with the same samples
collected during a second visit carried out 6 months later, with a case
When testing herds with no previous S. Dublin infection history, the definition of 1 positive test to define a herd status as positive) could be
MCDA team concluded that the most preferable diagnostic strategy was useful under certain conditions. The main advantage of the latter
1(M+B):1or1 (i.e. testing the bulk tank milk and the blood of 10 heifers strategy was the greater confidence in the result for herds testing
>3-month-old, all samples taken during a single farm visit, and the herd negative. In the latter case, when testing negative, only 1 out of 20 herds
being assigned a positive status whenever the milk sample or one of the (negative predictive value of 95.5%) would possibly be a false negative.
blood samples is positive to the PrioCHECK™ ELISA test). The MCDA As a comparison, with the 1(M+B):1or1 strategy, among the herds with
team further made the caution that this diagnostic strategy should be a negative result, 2 out of 20 would be expected to be false negative
recommended as a “screening test” to rule out the presence of S. Dublin. results. The 2(M+B):(1or1)OR(1or1) strategy could, therefore, be
In a herd with no history of S. Dublin and using this diagnostic strategy

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Fig. 2. Stacked unicriterion scores of the 14 diagnostic strategy options assessed on the 10 criteria proposed resulting of all pairwise comparisons of the strategies
without weight or preference functions. A/ Diagnostic strategies for herds with no previous history of Salmonella Dublin infection. B/ Diagnostic strategies for herds
with a previous history of Salmonella Dublin infection. The code for the diagnostic strategies is as followed: the number and letter prior to the colon give the number
of visits and the type of sample (i.e. blood of 10 young animals (B), bulk milk (M) or both sample types (M+B)), respectively. The number of tests that must be
positive to attribute a positive status to the herd depending on the diagnostic strategy is after the colon (i.e. 1 bulk milk test, and/or 1 or 2 seropositive animals out of
10 tested per visit).

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Table 4
Rank and net outranking flow of the 14 diagnostic strategy options for the two contexts (herds with or without history of known previous infection by Salmonella
Dublin). The strategies are ordered according to their rank obtained with the consensus-built weights.
FMV MAPAQ PLQ AMVPQ Consensus

Diagnostic strategiesa Rank Flow Rank Flow Rank Flow Rank Flow Rank Flow

Herds with no previous S. Dublin history


1(M+B):1or1 1 0.161 1 0.204 1 0.140 2 0.173 1 0.177
1(M+B):1or2 4 0.136 3 0.124 4 0.110 5 0.123 2 0.111
3 M:1 3 0.137 5 0.068 2 0.131 3 0.148 3 0.081
1 M:1 2 0.137 8 0.007 3 0.129 1 0.177 4 0.078
2 M:1 5 0.108 9 -0.016 6 0.088 4 0.135 5 0.047
1B:2 7 0.065 7 0.031 5 0.093 7 0.081 6 0.045
2(M+B):(1or1)OR(1or1) 8 -0.002 2 0.179 9 -0.032 9 -0.065 7 0.041
2 M:2 6 0.081 11 -0.052 7 0.077 6 0.101 8 0.019
1B:1 9 -0.040 10 -0.021 8 0.014 8 0.051 9 0.013
2(M+B):(1or2)OR(1or2) 11 -0.055 4 0.106 11 -0.058 11 -0.114 10 -0.008
2(M+B):(1or1)AND(1or1) 10 -0.041 6 0.065 10 -0.053 12 -0.162 11 -0.010
3 M:3 12 -0.127 13 -0.305 12 -0.147 10 -0.090 12 -0.125
2B:1or1 13 -0.228 12 -0.080 13 -0.204 13 -0.214 13 -0.164
2B:2and2 14 -0.331 14 -0.308 14 -0.287 14 -0.343 14 -0.307
Herds with a previous S. Dublin history
1(M+B):1or1 1 0.210 1 0.177 1 0.167 1 0.181 1 0.191
2(M+B):(1or1)OR(1or1) 3 0.141 2 0.163 4 0.083 4 0.107 2 0.149
1(M+B):1or2 2 0.161 3 0.114 2 0.128 3 0.121 3 0.132
1B:1 5 0.088 4 0.108 3 0.114 2 0.122 4 0.100
2(M+B):(1or2)OR(1or2) 7 0.060 5 0.083 8 0.037 7 0.030 5 0.070
3 M:1 4 0.089 6 0.042 7 0.045 6 0.052 6 0.061
1 M:1 6 0.060 8 0.020 5 0.068 5 0.053 7 0.034
1B:2 9 0.002 7 0.029 6 0.052 8 0.030 8 0.002
2 M:1 8 0.026 10 -0.035 10 -0.020 9 -0.003 9 -0.005
2(M+B):(1or1)AND(1or1) 11 -0.082 9 0.007 9 0.003 10 -0.041 10 -0.036
2 M:2 10 -0.065 11 -0.087 11 -0.038 11 -0.043 11 -0.067
2B:1or1 12 -0.151 12 -0.132 13 -0.195 13 -0.158 12 -0.142
3 M:3 13 -0.173 13 -0.192 12 -0.119 12 -0.123 13 -0.153
2B:2and2 14 -0.365 14 -0.298 14 -0.325 14 -0.328 14 -0.336
a
The code for the diagnostic strategies is as followed: the number and letter prior to the colon give the number of visits and the type of sample (i.e. blood of 10 young
animals (B), bulk milk (M) or both sample types (M+B)), respectively. The number of tests that must be positive to attribute a positive status to the herd depending on
the diagnostic strategy is after the colon (i.e. 1 bulk milk test, and/or 1 or 2 seropositive animals out of 10 tested per visit).

preferable in situations where the level of certainty in relation to a Moreover, the current framework has the additional advantage of
negative result must be very high. allowing a final brainstorming at the last step (consensual final deci­
sion). This highlights the fact that the objective of the MCDA exercise is
4. Discussion not a direct single recommendation, but a full consensual decision-
making process, helped and informed by the outputs of the analyses.
4.1. Multi-criteria analyses results Interestingly, the main final decision that was adopted and consid­
ered the most relevant (1(M+B):1or1; i.e. testing the bulk tank milk and
The objectives of this study were to develop a MCDA tool to compare the blood of 10 heifers >3-month-old, all samples taken during a single
diagnostic strategies aiming at defining a herd-level status for infectious farm visit and the herd being assigned a positive status if one sample is
diseases in dairy herds, and to use that tool in the case of S. Dublin ELISA-positive) happened to be already applied by the Québec’s au­
infection in two epidemiological contexts. The various MCDA methods thorities (except for the milk-ELISA cut-off: set at PP% ≥ 35 in the
have already been applied in animal health and veterinary public health, current study vs PP% ≥ 15 in the authorities policy) (MAPAQ, 2023).
but, so far, mainly to prioritize diseases or risks or to inform disease Thus, this MCDA process provides consensual and rational bases to
prevention and control (Mourits et al., 2010; Corbellini et al., 2020; support the diagnostic strategy already in place. It should be noted that
Zhao et al., 2022; Amenu et al., 2023). Its use to inform decision on a these multi-criteria results only apply to the defined options, criteria,
diagnostic strategy seems newer: we found one application to COVID-19 and disease contexts that were determined by the MCDA team. In case of
diagnosis in humans (Sayan et al., 2020) and another one for the peri­ a new option (e.g. one including a different diagnostic test), the per­
odic screening of tuberculosis in bovine herds (Guetin-Poirier et al., formance matrix exercise should be carried out again. Moreover, an
2022). additional diagnostic strategy (2(M+B):(1or1)OR(1or1)) was proposed
The current study has shown how in a non-mandatory and complex for the “with previous history of infection” context, notably in situations
screening context for infectious diseases in dairies, a decision on diag­ where the decision-maker would like to minimize false negative results,
nostic strategy can still be successfully informed by applying the MCDA which demonstrates that final decision is not always unique and simple.
methodology. Here, we provided a transparent and documented 9-step
process, in the case of S. Dublin infection, starting with the working 4.2. Method
team. The rigorous rainbow diagram tool allowed a balanced selection
for the MCDA team, which required all the S. Dublin project participants Our MCDA team determined 10 criteria falling under four main is­
to define the relevant stakeholders who must participate to the exercise sues for comparing the diagnostic strategies. Guetin-Poirier et al. (2022)
(from 18 to 7 stakeholders’ groups). In this manner, all the diagnostic worked in a similar way (i.e. the same MCDA steps and PROMETHEE II
strategies included in the framework to define the herd status would tool were used) to inform decision on the periodic screening of tuber­
have the assent of the most impacted actors and actors who could in­ culosis in French bovine herds (Guetin-Poirier et al., 2022). Our two
fluence the most their implementation in the field. studies had unique set of criteria and indicators. Nevertheless, they

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Fig. 3. GAIA plane showing the relative localization of the 14 diagnostic strategies and of the 10 criteria on the first two projection axes (UV plane). A/ For herds
with no previous Salmonella Dublin infection history (the representativity of the plane is 76%). B/ For herds with a previous Salmonella Dublin infection history (the
representativity of the plane is 75%). The diagnostic strategies are shown by red, pale blue and pink squares for the strategies based on blood (B), milk (M) or both
sample types (M+B), respectively. The code for the diagnostic strategies is as followed: the number and letter prior to the colon give the number of visits and the type
of sample, respectively. The number of tests that must be positive to attribute a positive status to the herd depending on the diagnostic strategy is after the colon (i.e.
1 bulk milk test, and/or 1 or 2 seropositive animals out of 10 tested per visit). The arrows ending with a diamond indicate the criteria, the color corresponding to their
issues of concern (gray: Diagnostic considerations; green: Socio-economic considerations; black: Logistics considerations; blue: Perception). The diamond indicates
the wanted optimal direction (i.e. minimizing or maximizing) for the criterion. The red stick highlights the decision axis for the consensus. The red ellipse shows the
location that the tip of the decision axis would cover if the weight of each criterion varied up to +/- 25% of its initial value. This allows assessing the sensitivity of the
decision axis to the weight of the criterion: the larger the ellipse, the more sensitive the decision axis is to the criteria weight.

share the similar main concerns about the decision. Regarding diag­ tuberculosis is a notifiable disease with plan for culling positive animal.
nostic considerations, the same authors (Guetin-Poirier et al., 2022) The same authors considered the impact through their criterion “Per­
used the diagnostic strategy’s sensitivity and specificity while we centage of animals culled for nothing” while we propose a more so­
included the probability of positive and of negative diagnostics (whose phisticated yet validated approach (misclassification costs). They had
computation includes the diagnostic sensitivity and specificity plus the three criteria on the easiness of implementing the diagnostic strategy
expected herd prevalence of disease). We chose those probabilities over (for the farmers, for the veterinarians, and for the authorities) which
sensitivity and specificity because they are more informative regarding partially overlap our criteria on resources and on farmers’ acceptability.
the reliability of the test result when applied in a given epidemiological Sayan et al. (2020) in their multi-criteria evaluation of diagnostic tests
context. This latter fact becomes obvious when comparing the varying for COVID-19 in humans used 15 criteria, which were minimally defined
values for these criteria, within a same diagnostic strategy, but across (Sayan et al., 2020). Nevertheless, one of them was about costs, four
the two epidemiological contexts (i.e. in herds with vs without a previ­ about the diagnostics validity (sensitivity, specificity, false positivity,
ous S. Dublin history). As a comparison, the sensitivity and specificity of false negativity), and one about the equipment, all being aligned to our
a given diagnostic strategy, the criteria used by other authors would not criteria. Although limited, these comparisons argue for the application
be modified by the epidemiological context. These latter parameters are of MCDA methods in the choice of a diagnostic strategy to determine a
intrinsic characteristics of the test and they do not provide insights on herd infection status when there is no obvious procedure. They also
the test’s behavior when applied in a given population (Buczinski et al., indicate that such analyses should include criteria relating to the validity
2023). of the diagnosis, but also criteria focusing on socio-economic impacts, on
In addition, we added credibility as another criterion regarding the logistical considerations, and on the perception by the different
validity of the test strategy to weigh for the uncertainty around the es­ stakeholders.
timates of the probabilities of positive and negative diagnostics. Finally, Given the relative repeatability of the issues and criteria across
we proposed and used a criterion on the sampling representativeness to studies, we hypothesize that an important part of the work conducted in
take into consideration the complex physiopathology of the disease. We our study could be reused in future studies comparing diagnostic stra­
can find in the study by Guetin-Poirier et al. (2022) the same other tegies for establishing the herd status for a given disease, when clinical
concerns about the socio-economics impacts, the logistics, and about signs are not readily observable, and when a gold standard test is not
perception by farmers and veterinarians of the diagnostic strategy. available and/or when it is impossible to sample all animals in the herd.
However, they are differently organized and defined. For example, two For such usage, one could use the issues, criteria, and indicators devel­
criteria were used for the cost: one for the farmers and one for the au­ oped in our study. The development of those criteria and indicators (the
thorities (Guetin-Poirier et al., 2022). And their cost criteria encompass 4th step of the MCDA process) was one of the most demanding part of
not only the cost of the testing, as we included, but also the cost of the the MCDA exercise. The identification of the stakeholders (the first step),
control in case of positive animal, all of which being relevant because as well as refining the decision problem (the 2nd step) and defining the

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Fig. 4. GAIA plane of the multicriteria preferences for the 14 diagnostic strategies by participating stakeholder. The red stick shows the decision axis: a) for herds
with no previous Salmonella Dublin infection history; b) for herds with a previous Salmonella Dublin infection history. The blue dots indicate the participating
stakeholders: the association of veterinary practitioners of Québec (AMVPQ); epidemiologists from the veterinary faculty (FMV); the ministry of agriculture. fisheries
and food of Québec (MAPAQ); the dairy producers of Québec combined with the private dairy herd improvement company in charge of individual and bulk milk
analyses and diagnostic in dairy cattle sector (PLQ). The options are shown by red, pale blue and pink squares for the strategies based on blood (B), milk (M) or both
sample types(M+B), respectively. The code for the diagnostic strategies is: the number and the letter prior to the colon give the number of visits and the type of
sample, respectively; the number of tests that has to be positive to attribute a positive status to the herd depending on the diagnostic strategy is after the colon (i.e. 1
bulk milk test and/or 1 or 2 seropositive animals out of 10 tested per visit).

options for the diagnostic strategies (the 3rd step) would, of course, have 9_Acceptability, 10_Simplicity). Overall, it should be stressed that the
to be disease and study-specific. In addition, the weights attributed to current proposed MCDA tool could be adapted for other situations, it
each indicator (the 5th step) would also have to be determined to fit the would have, however, to be modified according to the specific disease
context of that new study. This latter matter is clearly illustrated by the and epidemiological context studied.
different weights that were attributed to the various indicators in our
study, when investigating the same disease (S. Dublin), but in different 5. Conclusion
contexts (herds with vs without previous S. Dublin history).
The present research proposed a multi-criteria decision analysis tool
that could be used to compare diagnostic strategies (i.e. combinations of:
4.3. Limitations biological samples, repetitions, and diagnostic test interpretations)
aiming at defining the herd status for infectious diseases in dairies. The
The MCDA framework that was developed in the current study tool was then used in the case of S. Dublin infection in two contexts: (i)
resulted from the application of already well-described techniques herds with no history, and (ii) herds with previous history of infection.
(Dodgson et al., 2009; Mareschal, 2013). With regards to the partici­ The identified decision problem was “What is the optimal diagnostic
pants, a number of two key actors was selected by each stakeholders’ strategy for establishing the status of a dairy herd for S. Dublin infection
organization. Even though no fix number of stakeholders’ representa­ when there are no clinical signs of infection?”. Fourteen options of
tives is recommended, we could have considered including more than diagnostic strategies were defined to help solving the problem. Ten
two representatives by organization. Our choice of options and contexts criteria grouped in diagnostic, socio-economic, logistic, and perception
can also be debated. Here, fourteen options were developed according to considerations were selected to appraise the 14 diagnostic strategies.
Québec’s context, and to what is already in place in the province and in The consensual final decision was 1(M+B):1or1 i.e. testing the bulk tank
northern European countries where the disease is endemic. Obviously, milk and the blood of 10 heifers over 3-month-old, all samples taken
this list is not exhaustive. Future studies should broaden the type of tests during a single farm visit and the herd being assigned a positive status if
and samples to be included in the diagnostic strategies (e.g. PCR, envi­ one sample is ELISA-positive. These results are a first step in efforts to
ronmental samples, etc.). Other epidemiological contexts could also help stakeholders with divergent priorities (e.g. dairy producers, vet­
comprise the presence or absence of biosecurity measures in dairy herds. erinarians, and authorities) overcoming diagnostic challenges with
Finally, another limitation to this study is the differences in the type regards to the screening of herds, notably for host-adapted diseases and
of variables that were used for criteria measurements. Most criteria (6/ when the only available tests are imperfect.
10) were measured with strong indicators that are well known, repro­
ducible, and already published or well sourced (1_VD+, 2_VD-, Funding
3_Credibility, 5_Costs, 6_Impacts, 7_Delay). However, the remaining
criteria were measured with terms that could be considered as “the This work was supported by funding from Les Producteurs de Lait du
result of subjective interpretation” (4_Representativity, 8_Resources,

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M.M. Um et al. Preventive Veterinary Medicine 228 (2024) 106234

Québec and a Collaborative Research and Development grant from the api/core/bitstreams/9c4fe1f8-24b9-47a0-852a-a5bed717a927/content. Seen on
November, 2023. SAGE Publications India Pvt Ltd New Delhi, India.
Natural Sciences and Engineering Research Council of Canada (Grant
Corbellini, L.G., Fernandez, F., Vitale, E., Moreira Olmos, C., Charbonnier, P., Iriarte
No. # CRDPJ: 518064-17) and the second author Natural Sciences and Barbosa, M.V., Riet-Correa, F., 2020. Shifting to foot-and-mouth disease-free status
Engineering Research Council of Canada Discovery grant (Grant No. # without vaccination: application of the PROMETHEE method to assist in the
RGPIN-2020-05237). development of a foot-and-mouth national program in Uruguay. Prev. Vet. Med. 181,
105082.
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Simon Dufour: Writing – review & editing, Writing – original draft, Available here: https://eprints.lse.ac.uk/12761/1/Multi-criteria_Analysis.pdf.
Visualization, Validation, Supervision, Resources, Project administra­ London School of Economics and Political Science, Department of Economic
tion, Methodology, Investigation, Funding acquisition, Formal analysis, History..
Drewe, J.A., Snary, E.L., Crotta, M., Alarcon, P., Guitian, J., 2023. Surveillance and risk
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Declaration of Competing Interest Available on: https://cdn-contenu.quebec.ca/cdn-contenu/adm/min/agriculture-
pecheries-alimentation/sante-animale/surveillance-controle/raizo/reseau-bovin/
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