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This page intentionally left blank
U N B I A S E D S T E R E O LO G Y
A Concise Guide

P E T E R R . M O U TO N

The Johns Hopkins University Press

Baltimore
© 2011 Peter R. Mouton
All rights reserved. Published 2011
Printed in the United States of America on acid-free paper
9 8 7 6 5 4 3 2 1

The Johns Hopkins University Press

2715 North Charles Street
Baltimore, Maryland 21218-4363
www.press.jhu.edu

Library of Congress Cataloging-in-Publication Data

Mouton, Peter R.
Unbiased stereology : a concise guide / Peter R. Mouton.
p. cm.
Includes bibliographical references and index.
ISBN-13: 978-0-8018-9984-3 (hardcover : alk. paper)
ISBN-10: 0-8018-9984-2 (hardcover : alk. paper)
ISBN-13: 978-0-8018-9985-0 (pbk. : alk. paper)
ISBN-10: 0-8018-9985-0 (pbk. : alk. paper)
1. Stereology. 2. Microstructure—Measurement. I. Title.
Q175.M8778 2011
516.00113—dc22 2010050256

A catalog record for this book is available from the British Library.

Special discounts are available for bulk purchases of this book. For more information, please
contact Special Sales at 410-516-6936 or [email protected].

The Johns Hopkins University Press uses environmentally friendly book materials, including
recycled text paper that is composed of at least 30 percent post-consumer waste, whenever
possible.
...
To D. C. Sterio, whose inspiration, intellect, and resolve to “do it right
or don’t do it at all” ensured a great deal of scientific progress
This page intentionally left blank
 CO N T E N T S

Preface ix

1. . . E L I A S CO I N S A W O R D 1

2. . . S O L I D 3  D O B J E C T S 5

3. . . R E G I O N A L V O LU M E E S T I M AT I O N 9

4. . . A R E A E S T I M AT I O N B Y P O I N T CO U N T I N G 15

5. . . P R O B E  O B J E C T I N T E R S E C T I O N S 22

6. . . V O LU M E B Y C AVA L I E R I P O I N T CO U N T I N G 26

7. . . A CC U R A C Y A N D P R E C I S I O N 33

8. . . F R O M 2  D TO 3  D 47

9. . . S U R FA C E A R E A A N D L E N G T H 62

10. . . TOTA L O B J E C T N U M B E R 71

11. . . R A R E E V E N T S 90

12. . . LO C A L S I Z E E S T I M ATO R S 96

vii
13. . . D O M O R E , L E S S W E L L 105

14. . . U N C E R TA I N T Y 120

15. . . CO M P U T E R I Z E D S T E R E O LO G Y S Y S T E M S 133

16. . . A S U R V E Y O F T I S S U E 142

17. . . P E E R R E V I E W CO N S I D E R AT I O N S 147

Appendix: Conceptual Framework for Organic Stereology 153

Glossary 155
Bibliography 161
Index 171

viii CO N T E N T S
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 P R E FA C E

The term stereology came to life, so to speak, in May 1961 at a meet-

ing organized by Professor Hans Elias at the The Feldberg, a moun-
taintop retreat in Germany’s Black Forest. The modifier unbiased
gradually entered the vernacular sometime in the 1980s to differenti-
ate new assumption- and model-free techniques, developed by Hans
Jørgen G. Gundersen of Aarhus, Denmark, and colleagues in the Inter-
national Society for Stereology, from older assumption- and model-based
methods in Euclidean geometry, known as biased stereology. Since
unbiased carries both colloquial and mathematical connotations, un-
biased stereology has been replaced in many circles by the term design-
based stereology. Over the past four decades, the theoretical concepts
that underlie design-based stereology have been developed, tested, re-
fined, and published by members of the International Society for Ste-
reology under a strong peer-review process in a variety of journals
that specialize in stereology, including the Journal of Microscopy.
Today, the terms unbiased and design-based refer to the theoretical
basis for stereology approaches to estimate first-order parameters,
such as number (N), length (L), surface area (S), and volume (V), and
several second-order parameters, including variation, spatial distribu-
tion, and so on.
Design-based stereology is unbiased in theory, because applica-
tions to biological material carry the potential for all manner of as-
sumptions, uncertainties, and artifacts to skew results from expected
values. Obtaining unbiased data from design-based stereology is what
Luis Cruz-Orive refers to as “a committed task.” Every investigator’s
study design must be firm in identifying and avoiding the stereological

ix
bias and uncertainty that arise from a wide variety of tissue-processing
and microscopy-related sources. These issues differ considerably from
stereology applications in other fields, such as materials sciences, soil
sciences, engineering, metallurgy, and geology. The term organic ste-
reology is introduced here to highlight biological applications of design-
based stereology. Hence, this book is intended to address researchers’
problems in the biosciences with applying theoretical principles to
biological tissue in an accurate, precise, and efficient manner.
My involvement with stereology began in perhaps the most ordi-
nary way—as a means to an end. I was involved in collaborative re-
search projects in the laboratory of Lars Olson as a predoctoral fel-
low at the Karolinska Institute in Stockholm, Sweden. One field of
study involved transplantation of stem cells into the brains of adult
rats. The survival of transplanted stem cells could be demonstrated
through staining and microscopy, but progress required reliable mor-
phometric techniques. We needed a morphometric approach to deter-
mine whether certain molecules delayed or enhanced the growth of
these undifferentiated cells. I had some experience using “biased ste-
reology,” that is, clicking with a hand-counter to count hundreds of
cell profiles on dozens of thin tissue sections at low magnification—
one click for each cell profile. Following the application of a so-called
correction factor, this approach generates biased data for the number
of cells per unit area (areal density). Besides being tedious, this ap-
proach is also labor and cost intensive, and based on numerous faulty,
model-based assumptions (e.g., assume the cell is a sphere).
Hoping for a more accurate and efficient approach, I waded into
the stacks of journals at Den Karolinska Bibliotek, the revered library
at the Karolinska Institute. This research turned up various morpho-
metric approaches for sampling and counting cells, with the most
highly cited papers reporting data based on thousands and even hun-
dreds of thousands of clicks on cell profiles. One study that took years
to finish reported “complete counts” based on clicks of more than
400,000 cell profiles on literally hundreds of tissue sections. Notwith-
standing the tremendous work and dedication of this effort, this ap-
proach suffered from the same weaknesses as my own. The counting
method assumed that the neurons of interest were spheres of uniform
size, shape, and orientation, an assumption violated by not only the

x P R E FA C E
cells in that study but also all cells in the fields of bioscience in general
and neuroscience in particular. Despite the faulty assumptions, mod-
els, and correction factors in such studies, these approaches were
highly regarded for their enormous investment of material and per-
sonnel resources. Those were the days before books on unbiased ste-
reology and commercially available computerized stereology systems.
I found a recently published article in the Journal of Microscopy by
D. C. Sterio entitled, “The Unbiased Estimation of Number and Sizes
of Arbitrary Particles Using the Disector.” This theoretical work pro-
posed a method for counting the number of cells on tissue sections,
without any further assumptions about the size, shape, or other char-
acteristics of the cells. To my novice eye, this seemed like the way to go.
After listening to the outcome of my literature survey, Lars Olson
suggested that I attend a stereology course offered by Hans Jørgen
Gundersen at the nearby University of Aarhus in Denmark. I met an
international team of dedicated stereologists from a wide variety of
scientific disciplines, including Mark J. West, Bente Pakkenberg, Eva
Jensen, and Arne Møller (Denmark), Vivian Howard (Great Britain),
Luis Cruz-Orive (Spain), Terry Mayhew (Scotland), and Adrian Bad-
deley (Australia), all dedicated to helping bioscientists quantify organic
tissue. Although I never met Dr. Sterio at that meeting (or did I?*), I
learned that standard histological sections were biased for number;
that is, accurate counts of the number of neurons could never be ob-
tained from them, no matter how many thousands of clicks on cell
profiles were carried out; that greater numbers of clicks on cell pro-
files actually produced less accurate data; and that the number of
surviving stem cells in the brains of my rats could be accurately quan-
tified using the disector method. I also learned that Gundersen’s stu-
dents nicknamed him “Indiana Jones of Anatomy” for his ubiquitous
leather jacket, unrelenting travel to far-flung places, and fervent dedi-
cation to design-based approaches in stereology.
After this course, I accepted Gundersen’s invitation to join his
research group as a postdoctoral fellow after completing my PhD de-
fense. After two years of studying stereology principles and practices

* D. C. Sterio is the nom de plume of a stereologist who does not wish his or her name
to be associated with the disector method.

P R E FA C E xi
and living the Danish way of life, I received an overseas phone call from
Donald L. Price, head of the Neuropathology Laboratory at the Johns
Hopkins University School of Medicine in Baltimore, Maryland. Dr.
Price told me that, while he did not fully understand stereology, “every-
one is telling me that it’s important.” I accepted his invitation to join
his research group at Johns Hopkins as a National Institutes of Health
Fellow in experimental neuropathology, where I spent much of the
next two years informing U.S. bioscientists about the principles and
practices of stereology. I typically faced skepticism, resistance, and
aggressive questioning about why my stereology was better than the
assumption- and model-based methods used for decades to quantify
biological structure.
After the neuropathology fellowship, I joined the faculty in the
Department of Pathology at Johns Hopkins and spent the next six
years working to promote applications of design-based stereology to
the biological sciences. Together with Arun M. Gokhale (Georgia
Tech, Atlanta) and Mark J. West (University of Aarhus, Denmark), I
started a long-running training program, Applications of Unbiased
Stereology to Neural Systems, to train bioscientists in the theory and
practice of state-of-the-art design-based stereology. To increase the
throughput of research projects, we incorporated design-based stere-
ology into integrated hardware-software computerized systems with
support from the Johns Hopkins University School of Medicine and
in collaboration with Joel Durgavich at Systems Planning and Analysis
in Alexandria, Virginia. To help disseminate stereology-related infor-
mation to the international biomedical research community, in 2000,
we established the Stereology Resource Center (SRC) with a singular
mission, “to bring state-of-the-art stereology to the biosciences.”
Among the important changes in stereology during the past two
decades, I have identified the following three as perhaps the most im-
portant. First, concerns about design-based stereology have shifted
from opposition (“Why is design-based stereology better than my cur-
rent methods?”) to support (“Since design-based stereology can pro-
duce reliable results, why accept the results of biased approaches?”).
Second, efforts from members of the International Society for Stereol-
ogy to promote unbiased approaches have attracted the attention of
editors and reviewers of bioscience journals, as well as federal and

xii P R E FA C E
private funding agencies in many countries, which, in turn, have
changed the priorities for funding and publishing bioscience research.
Third, and perhaps most significant, I have seen the application of
design-based stereology to organic material, that is, organic stereol-
ogy, become the dominant method for quantifying the biological
structure in organic tissue.

This book celebrates the 50-year anniversary of the first stereology

meeting in the Black Forest of Germany. The opinions expressed here
are my own. I wish to express my appreciation to Vincent J. Burke
and the editorial and production staff at the Johns Hopkins Univer-
sity Press, and to my wife, Sammie, for her inspired dedication to
prepare images and continued support throughout the long ordeal of
processing words into sentences, sentences into paragraphs, and so
on. I welcome positive and negative feedback from readers whom I
trust will appreciate this text as I would have as a graduate student
many years ago.

P R E FA C E xiii
This page intentionally left blank
U N B I A S E D S T E R E O LO G Y
This page intentionally left blank
 1...
E L I A S CO I N S A W O R D

In the years leading up to 1961, an interesting point occurred to Ger-

man histologist Hans Elias. He realized that researchers in a wide
variety of scientific disciplines, including geology, materials sciences,
engineering, and natural sciences, struggled with a ubiquitous prob-
lem: how to quantify structural parameters of three-dimensional ob-
jects based on their two-dimensional representations on cut sections.
Several innovations in the late 1950s and early 1960s provided the
stimulus for biologists and histologists to acquire reliable methods to
quantify biological objects in tissue sections. Antibody-based probes to
label specific populations of biological objects based on the presence of
specific proteins (antigens), a technique called immunocytochemistry,
arose in the 1960s from the research of A. H. Coons. This approach
spurred the development of other immunohistochemical techniques
to quantify the amount of biological substances in tissue. Together,
these histological techniques allowed histologists to distinguish, for
the first time, new and discrete populations of cells, fibers, and blood
vessels from one another, leading to questions about relative quanti-
ties and changes in these structures during disease and aging and fol-
lowing experimental treatments.
In concert with these methodological breakthroughs in histology,
the availability of affordable, high-quality, mass-produced glass and
electromagnetic lenses in the late 1950 and early 1960s provided biol-

1
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