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Practical Clinical Epidemiology
for the Veterinarian
Practical Clinical
Epidemiology for
the Veterinarian
Aurora Villarroel
This edition first published 2015 © 2015 by John Wiley & Sons, Inc
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Library of Congress Cataloging‐in‐Publication Data
Villarroel, Aurora, author.
Practical clinical epidemiology for the veterinarian / Aurora Villarroel. – First edition.
   p. ; cm.
Includes bibliographical references and index.
ISBN 978-1-118-47206-4 (pbk.)
1. Veterinary epidemiology. I. Title.
[DNLM: 1. Epidemiologic Methods–veterinary. 2. Disease Outbreaks–veterinary.
3. Evidence-Based Practice. SF 780.9]
SF780.9.V55 2015
636.089′44–dc23
2014047527
A catalogue record for this book is available from the British Library.
Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not
be available in electronic books.
Cover images: Vet and Cat © elenaleonova/iStockphoto
Set in 9.5/13pt Meridien by SPi Publisher Services, Pondicherry, India

1 2015
Dedicated to all (present and future) members of this great profession
Contents

Preface, xi
Acknowledgments, xiii
About the companion website, xiv

1 Describing health and disease, 1

Case definition, 1
What is the problem?, 2
Who is affected?, 4
Where is the disease concentrated?, 5
When does disease occur?, 5
Types of measurements, 5
Counts, 5
Proportions, 7
Ratios, 8
Rates, 9
Specific measurements of disease, 10
Prevalence, 10
Incidence, 13
Morbidity, 16
Mortality, 16
Disease‐specific mortality, 16
Case‐fatality, 17

2 Basic epidemiology concepts, 19

Outcome, 19
Risk factor, 21
Unit of analysis, 22

vii
viii   Contents

Variables, 23
Types of variables, 26
Appropriate statistical analyses for continuous/parametric
variables, 27
Appropriate statistical analyses for categorical/nonparametric
variables, 29
Appropriate statistical analyses for multiple samples taken from the same
animal, 30
Control groups, 33
Sample size and P‐value, 34
Error and bias, 35
Confounding, 41
Interaction, 42

3 Evidence‐based medicine for the veterinarian, 44

Evaluation of a research paper, 49
Data presentation in the results, 53
Interpretation of results, 57
Statistical significance, 58
Biological significance, 60

4 Study designs, 62
Retrospective studies, 63
Case–control studies, 64
Surveys, 65
Cross‐sectional studies, 68
Prospective studies, 70
Cohort studies, 70
Clinical trials, 72
Sampling strategies, 73

5 Causation versus association, 77

Hill’s criteria to determine causation, 78
Temporal association, 78
 Contents   ix

Strength of association, 78
Consistency of association, 79
Specificity of association, 79
Dose–response (biological gradient), 80
Biologic plausibility, 81
Analogy, 81
Measures of association, 82
Odds ratio, 84
Relative risk, 89
Attributable risk, 92

6 Diagnostic tests, 94
Test quality, 95
Accuracy, 95
Precision, 95
Discrimination ability, 98
Test performance, 99
Sensitivity, 100
Specificity, 102
Positive predictive value, 104
Negative predictive value, 105
Screening, 107
Parallel testing, 107
Serial testing, 107
Gold standard, 108

7 Outbreak investigations, 109

Definitions, 110
Steps in an outbreak investigation, 110
Case definition/diagnosis verification, 110
Determine the magnitude of the problem, 111
Describe the spatial and temporal patterns of disease, 112
x   Contents

Analyze potential risk factors, 116

Follow‐up, 119

Glossary, 120
Formulas, 125
Final word, 128
References, 129
Index, 134
Preface

The intention of this book is to open your eyes to the tools that epidemiology
provides in the daily work of a clinician working with any animal species. This
book will not help you become an epidemiologist; it is only a glimpse into what
you can do with epidemiology.
So, what is epidemiology? The definition of epidemiology is the study of
­diseases in a population. Maybe due to the population term, most people think
that epidemiology is only suited to veterinarians working with cattle or food
animals in general. However, companion animal veterinarians use epidemiology
every day; they do not work with individual animals in a vacuum because their
patients are part of a population that interacts at the dog park, at shows, at
parties, on the street, and also at the vet clinic—that is your vet clinic! We all
deal with animal populations and we use epidemiological methods every day.
Being aware of how to use these methods to our advantage will enable us to
become better practitioners to improve the health of our patients, prevent disease,
and provide the best therapeutic options.
Throughout this book, you will notice the use of the terms “disease” and
“condition” interchangeably. This is because the same epidemiological methods
can be used to determine the risk of a disease such as lameness or a condition
such as twin pregnancies in mares, which is not a disease per se but a problem.
Other “conditions” that can be studied with the same epidemiological methods
are not problems but positive outcomes such as “cure,” “positive response to a
treatment,” or “extended life,” as happens with cancer treatments.
The book starts by describing the most common measurements of disease
and some of the most commonly used terms in epidemiology in Chapters 1 and 2.
There is a minimal part on statistics, simply to point out what are the appropriate
statistical tests to be used. These tests are not explained and there are no formulas;
for that you need to look into statistics books. The book continues in Chapter 3
with what I consider to be the most important part of the book: how to read and
interpret research papers. Research papers are the “point of the spear” for new
knowledge; however, just because something is published does not mean that it
is good work, accurate, or true. My hope is that after applying the knowledge in
this chapter, you will realize that you can determine whether a study warrants
the conclusions that are published or not and whether you can use that
information to help your patients. Chapter 4 covers in a simple straightforward
manner examples of the different epidemiologic study designs to show the pros
and cons, as well as the information obtained from each. Chapter 5 covers a core

xi
xii   Preface

distinction in epidemiology: association does not mean causation. If you have

ever spoken in length with an epidemiologist, you would have probably noticed
that epidemiologists are very careful in the use of each term. This chapter will
explain why. The final two chapters of the book will cover two of the most
common uses of epidemiology encountered on the daily work at a veterinary
clinic, that is, diagnostic tests (Chapter 6) and outbreak investigations (Chapter 7).
In the chapter about diagnostic tests, you will learn how to evaluate the strengths
and weaknesses of a test and properly interpret the results. In the chapter on
outbreak investigations, you will learn how to determine the transmission
pattern of a disease or condition so you can help your patients by preventing
disease spread and future disease occurrence. At the end of the book, there is a
section that collects all formulas in one place, as well as a glossary of the most
important epidemiologic terms used throughout the book.
This book is intended to provide concise and straightforward information on
how to apply epidemiological concepts in daily practice. Only the most necessary
formulas and calculations will be presented, with real‐life examples from all
animal species, but especially focused on companion animals. Most reference
articles are “open access,” which means they can be downloaded for free from
the Internet. My hope is that this book will help make you a better clinician.
Acknowledgments

I want to sincerely thank everyone who has made this book possible. Among
them are the veterinary students who I have had the privilege to guide over the
years and have taught me so much during that time. Special gratitude is due
to my dear mentor Dr. V. Michael Lane, who helped me grow when I was a
fledgling epidemiologist and did plant the seed for this book in my mind. He has
also graciously helped me make it better with his reviews. Finally, I have to
thank my family (two‐ and four‐legged) for always allowing me to follow my
dreams. Thank you all.

xiii
About the companion website

Practical Clinical Epidemiology for the Veterinarian is accompanied by a

companion website:
www.wiley.com/go/villarroel/epidemiology

The website includes:

•• Exercises for self‐study and review

xiv
 1 Describing health
and disease

Disease does not occur at random; if it were we would not have a job! There is a
pattern for every disease; we just need to find it.
To find how disease behaves we need to answer the following questions:
•• What is the problem?
•• Who gets diseased?
•• Where is the disease concentrated?
•• When does disease occur?
Answering all these questions (the essence of epidemiology is describing
disease in populations) should lead us to the answer of the ultimate question
we have about a certain disease (why does it happen?) and enable us to
­prevent it.

Case definition

The best explanation of the true substance of the word “definition” in matters
pertinent to epidemiology comes from combining two of the meanings of the
“definition”: (i) an exact statement or description of the nature, scope, or
meaning of something, and (ii) the degree of distinctness in outline of an object
(Oxford Dictionaries online).1 Therefore, the more carefully we describe things,
the more distinctness we achieve. In defining words, it is important to avoid
using another word with the same root as the one we are defining. When
defining a case, it tends to be more complete and accurate when following the
same rule of not using words with the same root.

Practical Clinical Epidemiology for the Veterinarian, First Edition. Aurora Villarroel.
© 2015 John Wiley & Sons, Inc. Published 2015 by John Wiley & Sons, Inc.
Companion website: www.wiley.com/go/villarroel/epidemiology

1
2    Practical Clinical Epidemiology for the Veterinarian

Example

When asked to define a diarrheic patient, simply stating it is a dog with diarrhea does not give
much distinction to the case. However, if we define a diarrheic patient as a dog with feces that
are not well‐formed and cannot be picked up without leaving a mark on the ground gives a
clear‐cut characteristic that allows anyone to categorize a patient as having diarrhea or not.

What is the problem?

Before we start looking into who is diseased or where it is, we need to define
what we are going to consider a diseased individual looks like; in other words,
we need a case definition. This seems silly at first, but it is the most important
step in any study or investigation and is not so clear‐cut if you look deeper.

Example

Let us suppose we want to investigate if there is a problem of parvovirus in a kennel. How

would you define a case of parvovirus? Most people would say a puppy with diarrhea. The
problems with this simple definition of a case of parvovirus are as follows:
• There are other causes of diarrhea in puppies, so you may be overestimating how much
parvovirus infection there truly is.
• Parvovirus may have asymptomatic infections, so you may be underestimating infection.
• Parvovirus can have other clinical signs without diarrhea, such as lethargy, anorexia,
fever, vomiting, and severe weight loss, so you may be underestimating infection by
looking only at puppies with diarrhea.
• How old can a dog be while still being considered a puppy? In other words, what is the
“case definition” of a puppy?
To get the best estimate of truly infected dogs in a population, we would have to better
define a case of parvovirus infection. An example could be “dogs less than 9 months old
with a positive fecal ELISA test for parvovirus.” This definition would minimize the number of
dogs with diarrhea due to other causes (because they have to have a positive ELISA test), and
it would also minimize the number of dogs excluded because they did not have diarrhea.

The importance of case definition becomes paramount when comparing

research studies about a certain disease. If two studies do not have the same case
definition, the results of both studies cannot be compared directly.

Example

A study on hip dysplasia in dogs (Paster et al. 2005) showed that inclusion of the caudal
curvilinear osteophyte in the definition of canine hip dysplasia significantly altered the
diagnosis of a large proportion of dogs, usually toward a higher score but sometimes to
a lower score (Figure 1.1).
 120 Scoring without CCO
100

80
68
60
46 48
40 34

20

Frequency
0 1 3
0
120
Scoring with CCO 118
100

80

60
38
40
24
20 15
2 3
0
0
l

ir

rd

HD

HD

HD
ce

oo

Fa

Bo
Ex

ild

od

v
G

Se
M

M
Subjective score

Figure 1.1 Distribution (frequency [no.]) of subjective hip scores for dysplasia using
two different definitions (Paster, E.R., LaFond, E., Biery, D.N., Iriye, A., Gregor, T.P.,
Shofer, F.S., and Smith, G.K. (2005). Estimates of prevalence of hip dysplasia in golden
retrievers and Rottweilers and the influence of bias on published prevalence figures.
Journal of the American Veterinary Medical Association, 226(3):387–392. © AVMA).

Another example is from a study on diagnosis of staphylococcal infections in a veterinary

hospital (Geraghty et al. 2013). In this study, phenotypic appearance of cultured bacteria or
genotypic analysis was used to determine which staphylococcal species was isolated from
each animal. Figure 1.2 shows a summary of the data presented in the published paper,
showing large mismatch in the results using one method versus the other.

Phenotypic Genotypic
Kocuria rosea
S. xylosus
S. warneri/pasteuri
S. succinus
S. simulans
S. saprophyticus
S. pseudintermedius
S. felis
S. equorum
S. epidermidis
S. chromogenes
S. carnosus/simulans
S. carnosus
S. aureus
No result
0 2 4 6 8 10 12 14 0 2 4 6 8 10 12 14

Figure 1.2 Distribution of isolation of staphylococcal species defined via phenotypic

or genotypic methods (data source Geraghty, L., Booth, M., Rowan, N., and Fogarty, A.
(2013). Investigations on the efficacy of routinely used phenotypic methods compared
to genotypic approaches for the identification of staphylococcal species isolated from
companion animals in Irish veterinary hospitals. Irish Veterinary Journal, 66(1):7–15).
4    Practical Clinical Epidemiology for the Veterinarian

Case definition is of paramount importance in situations where a range of

outcomes is possible. This is typical of outcomes that are measured by scores,
which are used to establish a relative degree of the outcome when there is no
directly measurable factor.

Example

In a study on gastric ulcers in pleasure horses (Niedzwiedz et al. 2013), the authors used a
scoring system to determine the severity of the lesion. The scoring system they described is
shown in Figure 1.3. Notice that with this description it would be possible to replicate the
study using the same scoring system and therefore comparing results across studies. There
could be only a potential problem in determining what “small” and what “large” lesions
are—that is, a diameter threshold that would qualify a lesion as small or large. Therefore,
it is better to always use objective characteristics to define cases or scores.

Lesion severity score Description

0 No lesions

I Lesions appear superficial (only mucosa

missing)

II Small, single, or multifocal erosions or ulcers

III Large, single, or multifocal ulcers, or

extensive erosions and sloughing

IV Active hemorrhage or adherent blood clot

Figure 1.3 Lesion severity score description for a study on gastric lesions in pleasure
horses (Niedzwiedz, A., Kubiak, K., & Nicpon, J. (2013). Endoscopic findings of the
stomach in pleasure horses in Poland. Acta Veterinaria Scandinavica, 55:45–55).

Who is affected?
Remember we are looking for patterns of disease, so the question is whether the
entire population is affected or there are some specific subgroups more affected
than others? Any type of subgrouping can be investigated: age, gender, breed, envi-
ronment, disposition (mainly used for companionship, racing, hunting, or other),
diet, etc. To continue with the parvovirus example, we know that most affected
animals are puppies and young dogs. Among the young dogs it is mostly males, in
theory reflecting their higher tendency to roam lose compared with females.
An example for the environmental differences can be found in feline leu-
kemia, a disease more common in multicat households and in cats that are
allowed access to the outdoors.
You can surely find an example for different diets, breeds, etc.
 Chapter 1 Describing health and disease    5

Where is the disease concentrated?

Defining the spatial distribution of disease may help identify risk factors and the
behavior of infection. A risk factor is any characteristic that increases the risk of an
animal for a certain condition. For example, which horses get infected, those in
pasture or those in the barn? Is the disease spreading to adjacent stalls or are appar-
ently “random” stalls involved? Are neighboring farms affected too? Do affected
animals live in specific areas such as downtown (smog), or close to wet areas?

When does disease occur?

Is there a pattern in time? How many animals are affected in winter versus summer,
spring, and fall? Is there a difference in the number of diseased individuals before
and after a given event (change in disinfectant, vaccination event, etc.)? Is there a
cyclical nature to the disease that could coincide with mosquito season or freezing?
Evaluate the epidemic curve–temporal distribution of cases. The first case
diagnosed in an outbreak is called the “index case.” A representation of the
number of cases by days will show the type of epidemic curve of a disease
(Figure 1.4). A “point‐source” curve shows a high number of affected animals
initially, which fades over time. This is typical of situations where many animals
are exposed at the same time, like in outbreaks of food‐borne diseases. A
“­propagated” epidemic curve shows a slow increase in the number of cases and a
slow decrease too. This curve is typical of epidemics of infectious (contagious) dis-
eases, where animals get exposed at different points in time (i.e., one animal gets
infected and spreads the infection to a few others, which in turn infect others).

Answering the who, what, where, and when of a disease leads to the why and how.

Types of measurements

Following are the most common ways to measure events in epidemiology, and
then we will look into specific measurements of disease.

Counts
A count of individuals is used to establish the size of the population. However,
when evaluating how important a disease is, simply reporting the count of sick
animals does not give much useful information.

Example

If someone says they have two sick dogs, is that a little or a lot? Obviously, it depends on
how many dogs they have in total. If they have two dogs, it means all of their dogs are
diseased, but if it is a kennel that has 50 dogs, 2 out of 50 dogs is not a lot.
6    Practical Clinical Epidemiology for the Veterinarian

40

35

30

25
Number of cases

20

15

10

0
1 3 5 7 9 11 13 15 17 19 21
Days

40

35

30

25
Number of cases

20

15

10

0
1 3 5 7 9 11 13 15 17 19 21
Days

Figure 1.4 Epidemic curves: point‐source (top) and propagated (bottom).

Everything has to be studied in context, in the case of epidemiology, in refer-

ence of the total population. Some may be thinking now that if we are dealing
with a terrible disease that can spread very fast and kill the animals, even 2 out
of 50 animals is too much. Agreed, but it is not a lot compared with 2 out of 2.
We are simply looking at numbers right now; we will add meaning or signifi-
cance to these numbers later in Chapter 5. The point is that, to give a sense of
 Chapter 1 Describing health and disease    7

how big the number of diseased animals is, it needs to be put in context in
­reference of the size of the total population.

Proportions
A proportion is the most normal way of looking at the magnitude of the number
of animals affected with a disease. It puts the count of sick animals in perspective
of the number of total animals in the population.
The formula to calculate a proportion is as follows:

A
(1.1)
A B

where A is the number of sick animals and B is the number of healthy animals.
Together A and B make the total population.
Note that the numerator is ALWAYS included in the denominator. Therefore,
proportions compare a subgroup with the whole group of animals under study. They are
usually expressed as percentages.

Example

Two sick dogs would represent 100% for the client that has two dogs total:

Sick 2
1 100%
Sick Healthy 2 0

While in a kennel that has 50 dogs, they would represent only 4%:

Sick 2
0 .4 4%
Sick Healthy 2 48

When calculating and reporting proportions, it is paramount to report what

population is included in the denominator, as this may not always be clear, and
simply reporting a percentage can lead to confusion as to how that proportion
was calculated.

Example

In a study about risk factors for dystocia in Boxers (Linde Forsberg and Persson 2007), the
authors show a graph (Figure 1.5) with two different proportions calculated using the
same animals in the numerator but different denominator. The light bars represent
the proportion of bitches within each age group (numerator) among all whelpings
(denominator, n = 253), while the dark bars represent the proportion of bitches within
each age group (numerator) among whelpings that resulted in dystocia (denominator,
n = 70). This is not clear from the graph itself but becomes evident when reading
the text.
8    Practical Clinical Epidemiology for the Veterinarian

100

80

Percentage (%) 60

40

20

0
1 2 3 4 5 6 7
Age (years)

Figure 1.5 Proportion of whelpings by age group in a study on Boxers (Linde Forsberg, C.
& Persson, G. (2007). A survey of dystocia in the boxer breed. Acta Veterinaria
Scandinavica, 49:8).

In contrast, in a study on the incidence of vaccine‐induced sarcomas in cats (Dean et al.

2013), the authors specify that they used three different denominators to calculate the
incidence of this type of tumors in their study (Figure 1.6).

Denominator 1. The total number of cats registered at the selected

practices at the end of 2007.
Denominator 2. The total number of consultations/examinations,
for which a code was in the system (e.g. primary
consultation, repeat consultation etc.) recorded for
cats by the selected practices during 2007.
Denominator 3. The total number of vaccinations visits for which
there was a code in the system for vaccination
visit (e.g. booster vaccination, primary vaccination
courses etc.), recorded for cats by the selected
practices during 2007.

Figure 1.6 Description of denominators used for the calculation of incidence of

vaccine‐induced sarcomas in cats (Dean, R.S., Pfeiffer, D.U., & Adams, V.J. (2013).
The incidence of feline injection site sarcomas in the United Kingdom. BMC Veterinary
Research, 9:17–19).

Ratios
A ratio shows the relationship between two mutually exclusive groups. This means
that the numerator cannot be included in the denominator. In other words, an
animal cannot be part of both groups that are being compared. It is like com-
paring apples and oranges.
The formula to calculate a ratio is as follows:

A
B (1.2)
 Chapter 1 Describing health and disease    9

where A is the number of animals in one group and B is the number of animals
in the other group.
A typical example of a ratio you can see in the literature is the ratio of males
to females. Obviously, an animal cannot be both. It is usually expressed in print
with figures as A : B and with text as A/B or A‐to‐B. Verbally, it is expressed as
“ratio of A to B.” It does not matter which one of the two groups goes first,
although there seems to be a tendency to put the lowest number last.

Example

A typical veterinary clinic may be expected to have a 5 : 1 dog‐to‐cat visits. This means that
for each cat they see, the clinic will see five dogs. Again, it is obvious that an animal cannot
be both a dog and a cat, so this is a ratio.
In another example, it has been shown that a higher adult/young ratio decreases
aggression among young horses. This means that the more adult horses there are for each
young horse, the better they all get along. Horses are either young or old; they cannot be
both at the same time.

However, it is not always easy to determine where to draw the line to include
an animal into one group or another when the characteristic that is used to clas-
sify them changes over time, as opposed to gender or breed, which are fixed.
With the example of the horses, we could consider that a horse is young until
3 years of age. So a horse that is 2 years and 11 months old (35 months) will be
considered “young,” while a horse that is 3 years and 1 month old (37 months)
will be considered old. Do we really expect much difference in behavior between
these two horses? Should they be included when studying horse aggression?
Should we use a different cutoff point for this study? These are some of the most
common questions that arise when dealing with ratios. Notice the importance of
definitions of age in this case.

Rates
A rate represents the speed of something developing. A rate compares a sub-
group with the whole group of animals during a specific time. Therefore, it is like
looking at a proportion including the time each individual is at risk.
The formula to calculate a rate is as follows:

A
(1.3)
(A B) time

The most important feature of a rate, which makes it different from a

proportion, is that it directly accounts for the time that each individual is at risk.
Exploring the Variety of Random
Documents with Different Content
[102] The mabeyn lies between the selamlik (general reception
room for men) and the haremlik; and is the living apartment for
men.
[103] The sluice which was supposed to have been used for this
purpose is still seen at Old Seraglio Point.
[104] According to Knowles, this was a part of Scanderbeg's reply
to Amurath II.
[105] The firman of Sultan Mahomet was never revoked, and
from his time until the extinction of the order of Janizaries by
Sultan Mahmoud, in 1834, the Padishah always appointed the
Chief Aga.
[106] The word Drakul signifies in Servian "the Devil."
[107] Vide Knowles, History of the Turks, and Albanian
Chronicles.
[108] Modern Alessio.
[109] Koran, Chapter VI.
[110] The price of blood, generally 1000 piastres among the
poorer classes, which was paid by the culprit to the village where
the crime was committed, and by it paid to the general
government.
[111] Castriot married late in life.
 *** END OF THE PROJECT GUTENBERG EBOOK THE CAPTAIN OF
THE JANIZARIES ***

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