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STATISTICAL ANALYSIS
IN MICROBIOLOGY:
STATNOTES
STATISTICAL ANALYSIS
IN MICROBIOLOGY:
STATNOTES

Richard A. Armstrong and Anthony C. Hilton

A John Wiley & Sons, Inc. Publication

Copyright © 2011 by John Wiley & Sons, Inc. All rights reserved

Published by John Wiley & Sons, Inc., Hoboken, New Jersey

Published simultaneously in Canada

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Library of Congress Cataloging-in-Publication Data is available

ISBN 978-0-470-55930-7

Printed in the United States of America

10 9 8 7 6 5 4 3 2 1
 CONTENTS

Preface xv

Acknowledgments xvii

Note on Statistical Software xix

1 ARE THE DATA NORMALLY DISTRIBUTED? 1

1.1 Introduction 1
1.2 Types of Data and Scores 2
1.3 Scenario 3
1.4 Data 3
1.5 Analysis: Fitting the Normal Distribution 3
1.5.1 How Is the Analysis Carried Out? 3
1.5.2 Interpretation 3
1.6 Conclusion 5

2 DESCRIBING THE NORMAL DISTRIBUTION 7

2.1 Introduction 7
2.2 Scenario 8
2.3 Data 8
2.4 Analysis: Describing the Normal Distribution 8
2.4.1 Mean and Standard Deviation 8
2.4.2 Coefficient of Variation 10
2.4.3 Equation of the Normal Distribution 10
2.5 Analysis: Is a Single Observation Typical of the Population? 11
2.5.1 How Is the Analysis Carried Out? 11
2.5.2 Interpretation 11
2.6 Analysis: Describing the Variation of Sample Means 12
2.7 Analysis: How to Fit Confidence Intervals to a Sample Mean 12
2.8 Conclusion 13

3 TESTING THE DIFFERENCE BETWEEN TWO GROUPS 15

3.1 Introduction 15
3.2 Scenario 16
3.3 Data 16
vi CONTENTS

3.4 Analysis: The Unpaired t Test 16

3.4.1 How Is the Analysis Carried Out? 16
3.4.2 Interpretation 18
3.5 One-Tail and Two-Tail Tests 18
3.6 Analysis: The Paired t Test 18
3.7 Unpaired versus the Paired Design 19
3.8 Conclusion 19

4 WHAT IF THE DATA ARE NOT NORMALLY DISTRIBUTED? 21

4.1 Introduction 21
4.2 How to Recognize a Normal Distribution 21
4.3 Nonnormal Distributions 22
4.4 Data Transformation 23
4.5 Scenario 24
4.6 Data 24
4.7 Analysis: Mann–Whitney U test (for Unpaired Data) 24
4.7.1 How Is the Analysis Carried Out? 24
4.7.2 Interpretation 24
4.8 Analysis: Wilcoxon Signed-Rank Test (for Paired Data) 25
4.8.1 How Is the Analysis Carried Out? 25
4.8.2 Interpretation 26
4.9 Comparison of Parametric and Nonparametric Tests 26
4.10 Conclusion 26

5 CHI-SQUARE CONTINGENCY TABLES 29

5.1 Introduction 29
5.2 Scenario 30
5.3 Data 30
5.4 Analysis: 2 × 2 Contingency Table 31
5.4.1 How Is the Analysis Carried Out? 31
5.4.2 Interpretation 31
5.4.3 Yates’ Correction 31
5.5 Analysis: Fisher’s 2 × 2 Exact Test 31
5.6 Analysis: Rows × Columns (R × C) Contingency Tables 32
5.7 Conclusion 32

6 ONE-WAY ANALYSIS OF VARIANCE (ANOVA) 33

6.1 Introduction 33
6.2 Scenario 34
6.3 Data 34
CONTENTS vii

6.4 Analysis 35
6.4.1 Logic of ANOVA 35
6.4.2 How Is the Analysis Carried Out? 35
6.4.3 Interpretation 36
6.5 Assumptions of ANOVA 37
6.6 Conclusion 37

7 POST HOC TESTS 39

7.1 Introduction 39
7.2 Scenario 40
7.3 Data 40
7.4 Analysis: Planned Comparisons between the Means 40
7.4.1 Orthogonal Contrasts 40
7.4.2 Interpretation 41
7.5 Analysis: Post Hoc Tests 42
7.5.1 Common Post Hoc Tests 42
7.5.2 Which Test to Use? 43
7.5.3 Interpretation 44
7.6 Conclusion 44

8 IS ONE SET OF DATA MORE VARIABLE THAN ANOTHER? 45

8.1 Introduction 45
8.2 Scenario 46
8.3 Data 46
8.4 Analysis of Two Groups: Variance Ratio Test 46
8.4.1 How Is the Analysis Carried Out? 46
8.4.2 Interpretation 47
8.5 Analysis of Three or More Groups: Bartlett’s Test 47
8.5.1 How Is the Analysis Carried Out? 47
8.5.2 Interpretation 48
8.6 Analysis of Three or More Groups: Levene’s Test 48
8.6.1 How Is the Analysis Carried Out? 48
8.6.2 Interpretation 48
8.7 Analysis of Three or More Groups: Brown–Forsythe Test 48
8.8 Conclusion 49

9 STATISTICAL POWER AND SAMPLE SIZE 51

9.1 Introduction 51
9.2 Calculate Sample Size for Comparing Two Independent
Treatments 52
9.2.1 Scenario 52
9.2.2 How Is the Analysis Carried Out? 52
viii CONTENTS

9.3 Implications of Sample Size Calculations 53

9.4 Calculation of the Power (P′) of a Test 53
9.4.1 How Is the Analysis Carried Out? 53
9.4.2 Interpretation 54
9.5 Power and Sample Size in Other Designs 54
9.6 Power and Sample Size in ANOVA 54
9.7 More Complex Experimental Designs 55
9.8 Simple Rule of Thumb 56
9.9 Conclusion 56

10 ONE-WAY ANALYSIS OF VARIANCE (RANDOM

EFFECTS MODEL): THE NESTED OR HIERARCHICAL
DESIGN 57
10.1 Introduction 57
10.2 Scenario 58
10.3 Data 58
10.4 Analysis 58
10.4.1 How Is the Analysis Carried Out? 58
10.4.2 Random-Effects Model 58
10.4.3 Interpretation 60
10.5 Distinguish Random- and Fixed-Effect Factors 61
10.6 Conclusion 61

11 TWO-WAY ANALYSIS OF VARIANCE 63

11.1 Introduction 63
11.2 Scenario 64
11.3 Data 64
11.4 Analysis 64
11.4.1 How Is the Analysis Carried Out? 64
11.4.2 Statistical Model of Two-Way Design 65
11.4.3 Interpretation 65
11.5 Conclusion 66

12 TWO-FACTOR ANALYSIS OF VARIANCE 67

12.1 Introduction 67
12.2 Scenario 68
12.3 Data 68
12.4 Analysis 69
12.4.1 How Is the Analysis Carried Out? 69
12.4.2 Interpretation 70
12.5 Conclusion 70
CONTENTS ix

13 SPLIT-PLOT ANALYSIS OF VARIANCE 71

13.1 Introduction 71
13.2 Scenario 72
13.3 Data 72
13.4 Analysis 73
13.4.1 How Is the Analysis Carried Out? 73
13.4.2 Interpretation 74
13.5 Conclusion 75

14 REPEATED-MEASURES ANALYSIS OF VARIANCE 77

14.1 Introduction 77
14.2 Scenario 78
14.3 Data 78
14.4 Analysis 78
14.4.1 How Is the Analysis Carried Out? 78
14.4.2 Interpretation 78
14.4.3 Repeated-Measures Design and Post Hoc Tests 80
14.5 Conclusion 80

15 CORRELATION OF TWO VARIABLES 81

15.1 Introduction 81
15.2 Naming Variables 82
15.3 Scenario 82
15.4 Data 83
15.5 Analysis 83
15.5.1 How Is the Analysis Carried Out? 83
15.5.2 Interpretation 83
15.6 Limitations of r 85
15.7 Conclusion 86

16 LIMITS OF AGREEMENT 87
16.1 Introduction 87
16.2 Scenario 88
16.3 Data 88
16.4 Analysis 88
16.4.1 Theory 88
16.4.2 How Is the Analysis Carried Out? 89
16.4.3 Interpretation 90
16.5 Conclusion 90
x CONTENTS

17 NONPARAMETRIC CORRELATION COEFFICIENTS 91

17.1 Introduction 91
17.2 Bivariate Normal Distribution 91
17.3 Scenario 92
17.4 Data 92
17.5 Analysis: Spearman’s Rank Correlation (ρ, rs) 93
17.5.1 How Is the Analysis Carried Out? 93
17.5.2 Interpretation 94
17.6 Analysis: Kendall’s Rank Correlation (τ) 94
17.7 Analysis: Gamma (γ) 94
17.8 Conclusion 94

18 FITTING A REGRESSION LINE TO DATA 95

18.1 Introduction 95
18.2 Line of Best Fit 96
18.3 Scenario 97
18.4 Data 98
18.5 Analysis: Fitting the Line 98
18.6 Analysis: Goodness of Fit of the Line to the Points 98
18.6.1 Coefficient of Determination (r 2) 98
18.6.2 Analysis of Variance 99
18.6.3 t Test of Slope of Regression Line 100
18.7 Conclusion 100

19 USING A REGRESSION LINE FOR PREDICTION AND

CALIBRATION 101
19.1 Introduction 101
19.2 Types of Prediction Problem 101
19.3 Scenario 102
19.4 Data 102
19.5 Analysis 102
19.5.1 Fitting the Regression Line 102
19.5.2 Confidence Intervals for a Regression Line 103
19.5.3 Interpretation 104
19.6 Conclusion 104

20 COMPARISON OF REGRESSION LINES 105

20.1 Introduction 105
20.2 Scenario 105
20.3 Data 106
CONTENTS xi

20.4 Analysis 106

20.4.1 How Is the Analysis Carried Out? 106
20.4.2 Interpretation 107
20.5 Conclusion 108

21 NONLINEAR REGRESSION: FITTING AN EXPONENTIAL

CURVE 109
21.1 Introduction 109
21.2 Common Types of Curve 110
21.3 Scenario 111
21.4 Data 111
21.5 Analysis 112
21.5.1 How Is the Analysis Carried Out? 112
21.5.2 Interpretation 112
21.6 Conclusion 112

22 NONLINEAR REGRESSION: FITTING A GENERAL

POLYNOMIAL-TYPE CURVE 113
22.1 Introduction 113
22.2 Scenario A: Does a Curve Fit Better Than a Straight Line? 114
22.3 Data 114
22.4 Analysis 114
22.4.1 How Is the Analysis Carried Out? 114
22.4.2 Interpretation 115
22.5 Scenario B: Fitting a General Polynomial-Type Curve 115
22.6 Data 116
22.7 Analysis 117
22.7.1 How Is the Analysis Carried Out? 117
22.7.2 Interpretation 117
22.8 Conclusion 118

23 NONLINEAR REGRESSION: FITTING A LOGISTIC

GROWTH CURVE 119
23.1 Introduction 119
23.2 Scenario 119
23.3 Data 120
23.4 Analysis: Nonlinear Estimation Methods 120
23.4.1 How Is the Analysis Carried Out? 120
23.4.2 Interpretation 121
23.6 Conclusion 122
xii CONTENTS

24 NONPARAMETRIC ANALYSIS OF VARIANCE 123

24.1 Introduction 123
24.2 Scenario 123
24.3 Analysis: Kruskal–Wallis Test 124
24.3.1 Data 124
24.3.2 How Is the Analysis Carried Out? 124
24.3.3 Interpretation 125
24.4 Analysis: Friedmann’s Test 125
24.4.1 Data 125
24.4.2 How Is the Analysis Carried Out? 126
24.4.3 Interpretation 126
24.5 Conclusion 126

25 MULTIPLE LINEAR REGRESSION 127

25.1 Introduction 127
25.2 Scenario 128
25.3 Data 128
25.4 Analysis 129
25.4.1 Theory 129
25.4.2 Goodness-of-Fit Test of the Points to the Regression
Plane 131
25.4.3 Multiple Correlation Coefficient (R) 131
25.4.4 Regression Coefficients 131
25.4.5 Interpretation 132
25.5 Conclusion 132

26 STEPWISE MULTIPLE REGRESSION 135

26.1 Introduction 135
26.2 Scenario 136
26.3 Data 136
22.4 Analysis by the Step-Up Method 136
26.4.1 How Is the Analysis Carried Out? 136
26.4.2 Interpretation 137
26.4.3 Step-Down Method 137
26.5 Conclusion 138

27 CLASSIFICATION AND DENDROGRAMS 139

27.1 Introduction 139
27.2 Scenario 140
27.3 Data 140
CONTENTS xiii

27.4 Analysis 140

27.4.1 Theory 140
27.4.2 How Is the Analysis Carried Out? 142
27.4.3 Interpretation 142
27.5 Conclusion 144

28 FACTOR ANALYSIS AND PRINCIPAL COMPONENTS ANALYSIS 145

28.1 Introduction 145
28.2 Scenario 146
28.3 Data 146
28.4 Analysis: Theory 147
28.5 Analysis: How Is the Analysis Carried Out? 148
28.5.1 Correlation Matrix 148
28.5.2 Statistical Tests on the Correlation Coefficient Matrix 148
28.5.3 Extraction of Principal Components 149
28.5.4 Stopping Rules 149
28.5.5 Factor Loadings 149
28.5.6 What Do the Extracted Factors Mean? 149
28.5.7 Interpretation 150
28.6 Conclusion 152

References 153

Appendix 1 Which Test to Use: Table 157

Appendix 2 Which Test to Use: Key 159

Appendix 3 Glossary of Statistical Terms and

Their Abbreviations 163

Appendix 4 Summary of Sample Size Procedures for

Different Statistical Tests 167

Index of Statistical Tests and Procedures 169

 PREFACE

This book is aimed primarily at microbiologists who are undertaking research and who
require a basic knowledge of statistics to analyze their experimental data. Computer
software employing a wide range of data analysis methods is widely available to experi-
mental scientists. The availability of this software, however, makes it essential that inves-
tigators understand the basic principles of statistics. Statistical analysis of data can be
complex with many different methods of approach, each of which applies in a particular
experimental circumstance. Hence, it is possible to apply an incorrect statistical method
to data and to draw the wrong conclusions from an experiment. The purpose of this book,
which has its origin in a series of articles published in the Society for Applied Microbiology
journal The Microbiologist, is an attempt to present the basic logic of statistics as clearly
as possible and, therefore, to dispel some of the myths that often surround the subject.
The 28 statnotes deal with various topics that are likely to be encountered, including the
nature of variables, the comparison of means of two or more groups, nonparametric
statistics, analysis of variance, correlating variables, and more complex methods such as
multiple linear regression and principal components analysis. In each case, the relevant
statistical method is illustrated with examples drawn from experiments in microbiological
research. The text incorporates a glossary of the most commonly used statistical terms,
and there are two appendices designed to aid the investigator in the selection of the most
appropriate test.

Richard Armstrong and Anthony Hilton

 ACKNOWLEDGMENTS

We thank the Society for Applied Microbiology (SFAM) for permission to publish mate-
rial that originally appeared in The Microbiologist. We would also like to acknowledge
Dr. Lucy Harper, the editor of The Microbiologist, for help in commissioning this book,
supporting its production, and for continuing encouragement.
We thank Tarja Karpanen and Tony Worthington (both of Aston University) for the
use of data to illustrate Statnotes 15, 18, and 20 and Dr. Steve Smith (Aston University)
for the data to illustrate Statnote 13.
We thank Graham Smith (Aston University) for drawing the figures used in Statnotes
25 and 28.
This book benefits from the teaching, research data, critical discussion, and especially
the criticism of many colleagues: Dr. T. Bradwell (British Geological Survey), Dr. N. J.
Cairns (Washington University, St Louis), Dr. M. Cole (Aston University), Dr. R. Cubbidge
(Aston University), Dr. C. Dawkins (University of Oxford), Dr. M. C. M. Dunne (Aston
University), Dr. F. Eperjesi (Aston University), Professor B. Gilmartin (Aston University),
Dr. I. Healy (King’s College London), Dr. E. Hilton (Aston University), Dr. P. D. Moore
(King’s College London), Dr. S. N. Smith (Aston University), and Dr. K. M. Wade
(University of Oxford).
We dedicate the book to our families.
 NOTE ON STATISTICAL SOFTWARE

There are nearly 100 commercially available software packages for statistical analysis
known to the authors at the time of this writing. At the present time, an authoritative review
and comparison of all the available packages is not available and is beyond the scope of
this book and its authors. However, the following points need to be considered. First, not
all of the statistical tests most useful to microbiologists are likely to be available in a single
package. Second, different packages may not use the same terminology when referring to
various statistical tests. This problem is especially acute in describing the different forms
of analysis of variance (ANOVA). A particular example of the confusion that can arise is
discussed in Statnote 11 with reference to the terminology for the two-way ANOVA in
randomized blocks. Third, it is better to become familiar with one or two packages than
to have a superficial knowledge of many. Finally, although the authors do not offer any
specific recommendations, the major software packages, for example, GRAPHPAD
PRISM, MINITAB, SPSS, STATISTICA, MEDCALC, SYSTAT, UNISTAT, and
STATVIEW will carry out most of the statistical procedures described in this book, includ-
ing all the basic tests, most of the common variations of ANOVA (one way, two way,
factorial, split plot, and repeated measures), contingency tables, nonparametric statistics
including the comparison of more than two groups, correlation, and regression analyses
including multiple regression. Despite the proliferation of statistical software and their
accompanying manuals, sound advice from a statistician with knowledge of microbiology
is likely to remain the best protection against the incorrect application of statistical
procedures.
 Statnote 1
ARE THE DATA NORMALLY
DISTRIBUTED?

Why is knowledge of statistics necessary?

The role of statistics in an experimental investigation.
Types of data and scores.
Testing the degree of normality of the data: chi-square (χ 2) goodness-of-fit test or
Kolmogorov–Smirnov (KS) test.

1.1 INTRODUCTION

Knowledge of statistical analysis is important for four main reasons. First, it is necessary
to understand statistical data reported in increasing quantities in articles, reports, and
research papers. Second, to appreciate the information provided by a statistical analysis
of data, it is necessary to understand the logic that forms the basis of at least the most
common tests. Third, it is necessary to be able to apply statistical tests correctly to a range
of experimental problems. Fourth, advice will often be needed from a professional statisti-
cian with some experience of research in microbiology. Therefore, it will be necessary to
communicate with a statistician, that is, to explain the problem clearly and to understand
the advice given.
The scientific study of microbiology involves three aspects: (1) collecting the evi-
dence, (2) processing the evidence, and (3) drawing a conclusion from the evidence.
Statistical analysis is the most important stage of processing the evidence so that a sound

Statistical Analysis in Microbiology: Statnotes, Edited by Richard A. Armstrong and Anthony C. Hilton
Copyright © 2010 John Wiley & Sons, Inc.
2 ARE THE DATA NORMALLY DISTRIBUTED?

conclusion can be drawn from the data. Two types of question are often posed by scientific
studies. The first type of question is a test of a hypothesis, for example, does adding a
specific supplement to a culture medium increase the yield of a microorganism? The
answer to this question will be either yes or no, and an experiment is often designed to
elicit this answer. By convention, hypotheses are usually stated in the negative, or as null
hypotheses (often given the symbol H0), that is, we prefer to believe that there is no effect
of the supplement until the experiment proves otherwise. The second type of question
involves the estimation of a quantity. It may be established that a particular supplement
increases the yield of a bacterium, and an experiment may be designed to quantify this
effect. Statistical analysis of data enables H0 to be tested and the errors involved in
estimating quantities to be determined.

1.2 TYPES OF DATA AND SCORES

There are many types of numerical data or scores that can be collected in a scientific
investigation, and the choice of statistical analysis will often depend on the form of the
data. A major distinction between variables is to divide them into parametric and nonpara-
metric variables. When a variable is described as parametric, it is assumed that the data
come from a symmetrically shaped distribution known as the normal distribution, whereas
nonparametric variables have a distribution whose shape may be markedly different from
normal and are referred to as distribution free, that is, no assumptions are usually made
about the shape of the distribution.
In this book, three types of data are commonly collected:

1. Attribute data in which the data are frequencies of events, for example, the
frequencies of males and females in a hospital with a particular infectious disease.
In addition, frequency data can be expressed as a proportion, for example, the
proportions of patients who are resistant to various antibiotics in a hospital or
community-based environment.
2. Ranked data in which a particular variable is ranked or scored on a fixed scale, for
example, the abundance of fungi in different soil environments might be expressed
on a scale from 0 (none) to 5 (abundant).
3. Measurements of variables that fulfill the requirements of the normal distribution.
Many continuous biological variables are normally distributed and include many
measurements in microbiology. Not all measurements, however, can be assumed
to be normally distributed, and it may be difficult to be certain in an individual
case. The decision may not be critical, however, since small departures from nor-
mality do not usually affect the validity of many of the common statistical tests
(Snedecor & Cochran, 1980). In addition, many parametric tests can be carried out
if the sample size is large enough. It is worth noting that tests designed to be used
on normally distributed data are usually the most sensitive and efficient of those
available.

Statnote 1 is concerned with the basic question of whether the data depart significantly
from a normal distribution and, hence, whether parametric or nonparametric tests would
be the most appropriate form of statistical analysis.
ANALYSIS: FITTING THE NORMAL DISTRIBUTION 3

1.3 SCENARIO

The domestic kitchen is increasingly recognized as an important reservoir of pathogenic

microorganisms, with dishcloths and sponges providing an ideal environment for their
growth, survival, and dissemination. Given the intrinsic structural and compositional dif-
ferences between these two material types, a study was envisaged to investigate if one
provided a more favorable environment for bacterial survival than the other, the hypothesis
being that there would be a quantitative difference between the number of microorganisms
recovered from dishcloths compared to sponges.
A total of 54 “in-use” dishcloths and 46 sponges were collected from domestic kitch-
ens, and the aerobic colony count of each was determined in the laboratory. Microbiological
data from environmental sources usually have very large counts and associated standard
deviations (SD) (see Statnote 2) and may not be normally distributed. Hence, the first stage
of the analysis, illustrated by the sponge data in this statnote, is to determine the degree
to which, if at all, the data depart from normality. Having established the distribution of
the data, parametric or nonparametric statistical tests may be applied as appropriate to
compare the difference between the cloth and sponge data.

1.4 DATA

The data comprise the aerobic colony counts of bacteria on 46 sponges and therefore
represent several measurements of a single variable.

1.5 ANALYSIS: FITTING THE NORMAL DISTRIBUTION

1.5.1 How Is the Analysis Carried Out?

To fit the normal distribution, the variable (aerobic colony count on sponges) is first
divided into frequency classes describing the range of the variable in the population. In
the present case, 10 classes were used (Table 1.1). The limits that define these classes are
then converted so that they are members of the standard normal distribution, that is, a
distribution that has a mean of zero and a SD of unity. To carry out this calculation, the
mean and SD of the observations are first calculated. The sample mean is then subtracted
from each class limit and divided by the SD, which converts the original measurements
to those of the standard normal distribution. Tables of the standard normal distribution are
then used to determine the expected number of observations that should fall into each class
if the data are normally distributed. The observed and expected values (Fig. 1.1) are then
compared using either a chi-square (χ2) “goodness-of-fit” or a Kolmogorov–Smirnov (KS)
test. This statistical analysis is available in most of the popular statistical analysis software
packages.

1.5.2 Interpretation
The χ test (χ2 = 38.99) for the sponge data is significant at the 1% level of probability
2

(P < 0.01), suggesting that the data deviate significantly from a normal distribution. The
KS test (KS = 0.0895), however, is not significant (P > 0.05), a not uncommon result
since this test is less sensitive than χ2 and only indicates gross deviations from the normal
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