YEARBOOK OF PHYSICAL ANTHROPOLOGY 44:106 –147 (2001)
Paleohistopathology of Bone: A New Approach to the
Study of Ancient Diseases
Michael Schultz
Zentrum Anatomie der Georg-August-Universität, Göttingen, Germany D-37075
KEY WORDS paleopathology; microscopy; etiology; epidemiology; inflammatory diseases;
porotic hyperostosis
ABSTRACT Light microscopy, particularly the use of
polarized light, has such a high value for the differential
diagnosis of dry bones that it can no longer be neglected.
Alterations caused intra vitam by disease or other living
conditions can clearly be differentiated by this technique
from changes due to postmortem reactions (e.g., pseudo-
pathology). As a reliable diagnosis is the basis not only of
the study of case reports but also of the etiology and
epidemiology of diseases in ancient populations, paleo-
pathologists would be well-advised to employ histological
analysis for their research, to avoid false diagnoses. The
necessary basis for such research is the knowledge of the
general histology, histogenesis, and growth as well as
pathophysiology of bone. Some new techniques which fa-
cilitate the practical use of microscopic analysis, such as
the preparation of thin-ground sections from undecalcified
bone samples and nonrehydrated mummified soft tissues,
are described. Selected examples of mechanisms of patho-
GLOSSARY
Actinomycetes, very small fungus-like bacteria
with mycelia
Autolysis, breakdown of tissues by the action of
enzymes starting directly after death
Basic lamellae, circumferential lamellae, i.e., ex-
ternal (periosteal) internal (endosteal) and basic la-
mellae of the shaft of a long bone
Casuistics, case studies
Cavitas medullaris, medullary cavity, e.g., of long
bones
Chondral ossification, bone originating primarily
as cartilage which is secondarily replaced by bone
(perichondral and endochondral ossification); see in-
tramembranous ossification
Cephalhematoma, swelling filled with blood be-
neath the pericranium, frequently caused during
birth
Compacta, see substantia compacta
Corticalis, cortical bone, thin lamellae of external
bone structure
Cribra cranii externa, descriptive term character-
izing a thickened and porotic external skull vault;
not an independent disease, but a morphological
symptom of various diseases; see porotic hyperosto-
sis
©2001 WILEY-LISS, INC.
DOI 10.1002/ajpa.10024
logical bone changes, particularly the determination of
vestiges of diseases in macerated bones by microscopy, are
presented. Emphasis is placed on the differential diag-
noses of proliferative reactions (e.g., periosteal processes
of long bones and the skull). In this context, the impor-
tance of meningeal reactions on the endocranial lamina of
the skull for morbidity and mortality in ancient popula-
tions is demonstrated. Furthermore, porotic hyperostosis
of the skull vault and the orbital roof, i.e., the cribra cranii
externa and cribra orbitalia, is discussed. Selected exam-
ples of the etiology and epidemiology of ancient diseases
are presented (e.g., anemia, scurvy, rickets, and menin-
geal diseases), and ideas on living conditions and their
implications for the origin and the spread of disease are
given to establish a better understanding of deficiency and
infectious diseases in the past. Yrbk Phys Anthropol 44:
106 –147, 2001. © 2001 Wiley-Liss, Inc.
Cribra orbitalia (⫽ cribra orbitalia), descriptive
term characterizing a porotic orbital roof; not an
independent disease, but a morphological symptom
of various diseases
Decomposition, disintegration of a corpse
Diagenesis, disintegration of a skeleton
Diploë, substantia spongiosa of the flat skull bones
(e.g., skull vault)
Epidemiology, study of the frequencies and the
spread of diseases
Epidural hematoma, hematoma between the inter-
nal lamina of the skull vault and the dura mater
Etiology, study of the causes of diseases
Faserfilz-osteon, an osteon, in which the lamellae
are very irregularly built up like in felt, found; e.g.,
frequently in slowly growing solid-bone tumors
Fossil, fossilized, e.g., in a fossil bone, organic sub-
stances replaced by minerals
Grenzstreifen (⫽ grenzlinie), line or band-like
structure indicating the place of the original exter-
nal surface of the shaft of a long bone separating the
external newly built bone formation (e.g., polsters)
from the deeper (sometimes still compact) bone sub-
stance; characteristic features at the microscopic
level seen in treponemal (and leprous?) periostitis
M. Schultz]
Haversian system, osteon, i.e., system of regular
circular lamellae around a blood vessel canal
(⫽ Haversian canal)
Hemangioma, benign tumor made up of new-
formed blood vessels
Hematogenous, e.g., in infections, distributed or
spread by way of the bloodstream
Hemorrhage, discharge of blood, as from a rupture
of a blood vessel
Hemorrhagic, adj., see hemorrhage
Hilfsobject, a compensator used in polarization mi-
croscopy
Howship’s lacunae, in microscopy, bay-like struc-
ture caused by osteoclasts
Inflammatory, pathology stage (inflammation),
caused by microorganisms or toxins (e.g., infection)
Intracartilaginous ossification, endochondral ossi-
fication
Intramembranous ossification, bone originates
primarily as bone inside the connective tissue; see
chondral ossification
Intra vitam, during life
Lacuna, space of osteocyte
Lamina externa, external lamina of the skull
bones (e.g., skull vault)
Lamina interna, internal lamina of the skull bones
(e.g., skull vault)
“Leichenschatten” (germ), shadow-like remains of
a prehistoric corpse
Macerate, to free a bone of soft tissue and cells, by
various agents; the result is dry bone
Meningioma, tumor developing from the lepto-
meningeal cells which line the arachnoid villi
Meningitis, inflammatory process of the meninges
caused by bacteria or viruses. Bacterial meningitis
can cause characteristic features, such as hemor-
rhage and increased brain pressure. Thus, due to
the dominance of the morphological features, the
observer can differentiate in dry skull bones be-
tween inflammatory-hemorrhagic and hemorrhagic-
inflammatory meningitis. In a specific inflammatory
meningeal disease, e.g., tuberculous meningitis
(Leptomeningitis tuberculosa), additional features,
such as small roundish impressions, are present
Meningo-encephalitis, inflammatory process of the
meninges and brain
Microfilariae, very small (ca. 15 ␮m length)
threadlike parasitic nematode worm of the family
Filariidae
Myositis ossificans, mineralization of muscles (and
PALEOHISTOPATHOLOGY OF BONE 107
tendons) caused by an inflammatory or metabolic
process
Osteitis (⫽ ostitis), inflammatory process of the
compact bone substance of a long bone
Osteoblast, cell of the bony tissue which secretes
osteoid
Osteoblastic, adj., buildup of new bone; see osteo-
blast and productive (proliferative)
Osteoclast, large cell of the bony tissue which
stems from monocytes (hyaline leukocyte) and
resorbs bone (causing Howship’s lacunae)
Osteoclastic, adj., resorption of bone; see osteoclast
and osteolytic
Osteocyte, bone cell
Osteoid, nonmineralized, preosseous substance,
secreted by osteoblasts
Osteolytic, see osteoclastic
Osteomyelitis, inflammatory process in 1) the
medullary cavity (fat or yellow marrow) of a long
bone, or 2) in the cancellous bone substance (red
marrow) of flat, short, and long bones; process af-
fects, as a rule, the complete bone
Osteon, see Haversian system
Perimortem, around the time of death
Periostitis, inflammatory process of the perios-
teum caused, e.g., by infection
Periostosis, noninflammatory process of the peri-
osteum caused, e.g., by hemorrhage or tumor
Plastination, fixation and embedding process de-
veloped by von Hagens [(1979) Anat Rec 194:247–
255], using the epoxy resin Biodur威
Polster, pillow-like structure of newly built bone
formations at the external surface of the shaft of a
long bone; characteristic features at the microscopic
level seen in treponemal and leprous periostitis
Porotic hyperostosis, descriptive term characteriz-
ing a thickened and porotic external skull vault,
sometimes called cribra cranii externa; not an inde-
pendent disease, but rather a morphological symp-
tom of various diseases
Postmortem, after death
Proliferative, productive; see osteoblastic
Recidivation, repeated or relapsed occurrence of a
pathological process
Subfossil, still not fossilized, e.g., archaeological
(medieval) bone
Substantia compacta, thick, i.e., compact sub-
stance of the shaft of a long bone
Substantia spongiosa, cancellous or spongy sub-
stance, exists in all bones

TABLE OF CONTENTS

Introduction ............................................................................................................................................................. 108

Brief summary of the history of microscopic research in paleopathology ...................................................... 108
Why do we need microscopic research in paleopathology? .............................................................................. 109
What diseases can be diagnosed in archaeological bones by microscopy? ...................................................... 110
What might be the effect of microscopic studies in bioarchaeology and sociobiology
of ancient populations? .................................................................................................................................... 110
Available Techniques .............................................................................................................................................. 110
108 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
What materials are investigated by microscopy in paleopathology? ............................................................... 110
Magnifying glass and stereoscopic low-power microscope ............................................................................... 110
Preparation and embedding of specimens for light microscopy ....................................................................... 110
Microscopy using plane light .............................................................................................................................. 112
Microscopy using polarized light ........................................................................................................................ 112
Microradiography ................................................................................................................................................ 114
Scanning-electron microscopy ............................................................................................................................. 114
Other techniques ................................................................................................................................................. 114
Microscopic Structure of Bone ............................................................................................................................... 114
General histology of bone .................................................................................................................................... 114
Histogenesis and growth of bone ........................................................................................................................ 116
Influence of Autolysis, Decomposition, and Diagenesis on Diagnostics ............................................................. 116
Soil and water ...................................................................................................................................................... 118
Plant roots ............................................................................................................................................................ 120
Fungi, algae, and bacteria .................................................................................................................................. 120
Arthropods ............................................................................................................................................................ 120
Crystals ................................................................................................................................................................ 120
Selected Examples of Mechanisms of Pathological Bone Changes: The Determination of the
Vestiges of Diseases in Macerated Bones by Microscopy ............................................................................. 120
General comments ............................................................................................................................................... 120
Proliferative reactions ......................................................................................................................................... 123
Periosteal reaction on long bones ................................................................................................................... 124
Meningeal reactions on the endocranial lamina of the skull ....................................................................... 128
Porotic hyperostosis of the skull vault and the orbital roof: the problem of cribra cranii externa and
cribra orbitalia .............................................................................................................................................. 131
Pseudopathology ...................................................................................................................................................... 137
Conclusions .............................................................................................................................................................. 140
Acknowledgments .................................................................................................................................................... 142
Literature Cited ...................................................................................................................................................... 142

INTRODUCTION second half of the 20th century, using mainly the

Brief summary of the history of microscopic
research in paleopathology
Light microscopy of macerated (dry) bones was
practiced for the first time as a part of routine
medical examination at the end of the 19th cen-
tury. At about the same time, the first publica-
tions dealing with the microscopic structure of
fossil bones (e.g., Schaffer, 1889) also appeared.
Since the 1920s, microscopy has been used in pa-
leopathology. At the very beginning of the devel-
opment of paleohistology, a term which was intro-
duced into the Anglo-Saxon literature by Moodie
(1923), the samples were decalcified, embedded in
paraffin wax, and cut by a microtome, or polished
surfaces of undecalcified bone were examined us-
ing normal (plane) and polarized light. Short re-
views describing the beginnings of paleohistology
and paleohistopathology were given by Garland
(1993), Martin (1991), de Ricqlès (1993), and Stout
(1976). Moodie (1923) published very informative
photomicrographs demonstrating specific struc-
tures in fossil and prehistoric animal and human
bones, and Weber (1927) examined prehistoric hu-
man long bones to diagnose treponemal diseases.
Because archaeological bones are very brittle and,
as a rule, cannot be decalcified to be sectioned
by microtomes without destroying the sample,
ground sections and new techniques of embedding
became the methods of choice. Thus, in the early
technique of ground sections, Ascenzi (1969),
Baud and Morgenthaler (1956), Hackett (1976),
Ortner (1976), Stout (1976), and Stout and Simons
(1979) carried out important research into the pa-
leohistology of dry bones. Particularly in North
America, during recent decades, paleohistopatho-
logical research using light microscopy has been
carried out primarily in connection with the his-
tological morphometrics of compact bone and mea-
surements of bone formation rates (e.g., Frost and
Wu, 1967; Martin and Armelagos, 1979, 1985;
Pfeiffer and King, 1981; Richman et al., 1979;
Stout and Lueck, 1995; Weinstein et al., 1981).
In contrast to the microscopic investigation of
macerated bones, the investigation of mummified
tissues was more popular at the beginning of pa-
leohistopathology (e.g., Ruffer, 1911; Williams,
1927; Wilson, 1927). Later, after World War II,
scientists like Sandison (1957), who represented
one of the leading authorities, carried out paleo-
pathological research in ancient mummified tis-
sues at the microscopic level. Although histology
on mummified soft tissues was carried out rela-
tively frequently (e.g., Brothwell et al., 1969;
Cockburn and Cockburn, 1998; Sandison, 1970;
Zimmerman, 2001; Zimmerman and Kelley, 1982),
the histopathology of archaeological bones has
rarely been a subject of interest (e.g., Kramar et
al., 1983; Largier and Baud, 1980).
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
Why do we need microscopic research
in paleopathology?
Reliable diagnosis is the basis for reconstructing
the etiology and epidemiology of diseases in ancient
populations. However, it is well-known that diag-
noses of diseases in ancient bones are not easily
established. As a rule, paleopathologists can only
examine the vestiges of ancient diseases in dry
bones, and no soft tissues or cells, which play an
important role in pathological investigations on re-
cent materials, can be studied to establish a reliable
diagnosis or for comparative purposes. Therefore, no
cytological and only a limited histological examina-
tion of soft tissues can be carried out (see below).
Many paleopathologists investigate archaeological
bone remains by macroscopy alone or sometimes
additionally by using radiological techniques such
as conventional X-ray images and CT-scans, and the
rate of false diagnoses is still high. Microscopic in-
vestigation of thin-ground sections produces more
reliable results than the use of multislice CT
(MSCT), which is an advanced form of helical com-
puted tomography (Rühli et al., 2000, 2001). Be-
cause diagnostic criteria can be relatively limited in
paleopathology, special methods and techniques,
particularly at the microscopic level, need to be es-
tablished to render such diagnoses more reliable.
Light microscopy (especially with polarized light),
microradiography, and scanning-electron micros-
copy have such high value for differential diagnosis
of dry bones that they can no longer be neglected. As
there are now several reliable techniques (Schultz,
1988; Schultz and Drommer, 1983), paleopatholo-
gists are advised to employ these useful tools for
their research to avoid false diagnoses. Many bone
changes which cannot be observed by macroscopic
analysis are revealed by microscopic techniques
(Schultz, 1988). Thus, many alterations caused intra
vitam by disease can clearly be differentiated from
changes due to postmortem reactions (Schultz, 1986,
1994a, 1997b). The nature of bone tumors and tu-
morous lesions can be detected microscopically, as
well as the different structures occurring through
specific and nonspecific bone inflammations (Hack-
ett, 1976; Schultz, 1986, 1999a; Schultz and Roberts,
2001; Schultz and Teschler-Nicola, 1987b). Also,
changes caused by metabolic diseases, processes of
aging, and decrease or increase in physical activity
are identifiable with the aid of microscopic methods
(Schultz, 1986, 2001a), and initial stages of bone
diseases which are not visible by gross examination
can be clarified by microscopic techniques. Some
diseases cause typical lesions in the bone matrix
that cannot be differentiated from lesions from a
different disease (Schultz, 1993b). The importance of
microscopic investigation of macerated bone speci-
mens for our knowledge of differential diagnoses
and the development of diseases is demonstrated by
the classic article on treponematoses by Hackett
(1976). In this article, figures are published which
109
TABLE 1. Frequencies of diseases observed
by using different techniques
Disease Disease
frequencies after frequencies
macroscopic after additional
examination microscopic
Diseases alone examination
Anemia 7.0% 4.7%
Rickets 0.0% 3.9%
Osteomyelitis 8.5% 4.7%
Irritation of meninges 6.8% 9.5%
describe very clearly the different stages of bony
destruction in the skeleton of people suffering from
yaws and venereal syphilis. The basis for the eluci-
dation of the stages lay in Cecil Hackett’s long years
of experience with the histopathology of dry bones.
The impact of microscopic research on the field of
epidemiology of diseases in ancient populations can
be illustrated by an example (Schultz, 1993b). In the
Early Bronze Age population from İkiztepe, north-
ern Anatolia, 144 infant and child burials were
available for the paleopathological investigation. Of
these, 129 individuals with preserved skulls were
suitable for the study of anemia, rickets, or osteo-
myelitis, and 117 individuals with preserved skulls
were suitable for the study of meningeal irritations
(Schultz, 1990). The materials were examined twice.
The first investigation was carried out at the site of
the excavation, using only macroscopic techniques
(Table 1). After microscopic investigation later car-
ried out at the Department of Anatomy of the Uni-
versity of Göttingen, according to the new diagnoses,
the frequencies of the four diseases were quite dif-
ferent (Table 1). The differences in the frequencies of
these diseases were really striking (cf. Schultz,
1993b). Three cases macroscopically diagnosed as
osteomyelitis were microscopically diagnosed as ir-
ritations of meninges. Three other cases were mac-
roscopically diagnosed as anemia, but diagnosed by
microscopy as osteomyelitis (cf. Fig. 16A,B). Five
cases macroscopically diagnosed as osteomyelitis
were microscopically diagnosed as rickets. Other
similar examples will be given later.
Microscopic analysis in paleopathology not only
allows more reliable diagnoses of ancient diseases,
but also enables improved age determinations (e.g.,
Kerley, 1965; Kerley and Ubelaker, 1978; Schultz,
1986; Stout, 1992; Wolf, 1999). Additionally, a mi-
croscopic investigation can detect changes at the
micro-level, such as inactivity atrophy, which cannot
be observed by macroscopy alone (Schultz, 1986,
1997b). Also, the effects of heat and fire occurring
around the time of death (perimortem), or after
death (postmortem), lead to typical changes in the
microstructure of bones (Grimm and Strauch, 1959;
Piepenbrink and Herrmann, 1988; Schultz, 1986,
1997b; Teschler-Nicola and Schultz, 1984). In the
case of small bone fragments, questions might arise
as to whether these fragments are human or animal
bones. The answer can often be easily clarified
110 YEARBOOK OF PHYSICAL ANTHROPOLOGY
through the histological analysis of a bone sample
(Harsányi, 1978, 1993). Furthermore, the result of
microscopic examination of archaeological bone
samples frequently gives important information
about the state of preservation and the kind of post-
mortem destruction (e.g., Hackett, 1981; Schultz,
1986, 1997b; Stout and Teitelbaum, 1976), which is
highly necessary for someone intending to date ar-
chaeological bones by the radiocarbon technique, or
to do molecular work on ancient bones such as an-
cient DNA and collagenous and noncollagenous bone
proteins, or to examine trace elements and stable
isotopes (Schultz, 1986, 1997b).
What diseases can be diagnosed in
archaeological bones by microscopy?
This is a more interesting and important question
than it would seem at first sight. In paleopathology,
all diseases which produce changes in the bony sys-
tem can be studied by microscopic techniques. Most
of these diseases can be reliably diagnosed by mac-
roscopic analysis in combination with radiology, en-
doscopy, and some of the special techniques used in
biochemistry or molecular biology. However, certain
of these diseases are only diagnosable by micros-
copy. These include, in particular, diseases which
affect the microstructure of the compact bone sub-
stance of the long bones (e.g., hematogenous osteo-
myelitis, treponemal diseases, leprosy) and the cor-
tical and cancellous bone substance of the skull (e.g.,
anemia, scurvy, rickets, meningitis, nonspecific and
specific osteomyelitis). Furthermore, many tumor
and tumor-like skeletal diseases belong to this
group.
What might be the effect of microscopic
studies in bioarchaeology and sociobiology
of ancient populations?
Microscopic methods and techniques can lead to
better and more reliable paleopathological diag-
noses. With the aid of these more reliable diagnoses,
the results of investigations dealing with 1) individ-
ual case studies (casuistics), 2) the causes (etiology)
and distribution and frequency of diseases (epidemi-
ology), and 3) the evolution and history of diseases
enable paleopathologists to expand their knowledge
in the interdisciplinary fields of bioarchaeology and
sociobiology of ancient populations. In these new
fields, paleopathology will play a dominant role in
the future by elucidating the living conditions, in-
cluding the causes of diseases and the ways of life, of
prehistoric and historic populations (e.g., Larsen,
1997; Ortner and Putschar, 1981; Roberts and
Manchester, 1995; Schultz, 1982; Spitery, 1983;
Wood, 1979; Živanović, 1982).
Furthermore, the results of microscopic studies
can provide important controls for molecular biolog-
ical investigations (e.g., DNA, proteins of the extra-
cellular bone matrix) of recent and ancient dry
bones. Thus, various kinds of contamination, such as
[Vol. 44, 2001
different phases and the intensity of diagenesis as
well as changes caused by the excavator, can be
easily checked.
Below, I discuss the available techniques for mi-
croscopic examination of archaeological bone, briefly
review some fundamentals of bone histology, exam-
ine the effects of postmortem change on bone micro-
structure, and present some examples of how these
techniques can be applied in paleopathological re-
search. Finally, some pseudopathologies are pre-
sented and discussed.
AVAILABLE TECHNIQUES
What materials are investigated by
microscopy in paleopathology?
The majority of samples examined in paleohis-
topathology are, without doubt, subfossil skeletal
remains of human beings and other animals and,
only occasionally, fossil remains. To what extent
microscopic analysis, particularly histology, can con-
tribute to establishing a reliable diagnosis depends
on the state of preservation (Schultz, 1997b). Some-
times, preservation is so poor that it is impossible to
present a convincing result of an age determination
or a disease diagnosis using macroscopic methods
alone, and we have no choice but to attempt a mi-
croscopic investigation. In a very extreme situation,
the skeletal remains can be so very poorly preserved
that only a corpse shadow, a “leichenschatten,” is
preserved. Even in this case, microscopic analysis of
the earth containing very small bone fragments can
sometimes give a satisfactory result (Schultz,
1997b).
Magnifying glass and stereoscopic
low-power microscope
In addition to macroscopic examination of archae-
ological skeletal remains, all bone surfaces sus-
pected of having been changed by pathological pro-
cesses while the person was alive should be
examined with a magnifying glass. In this way, very
unobtrusive vestiges can be recognized. Stereoscopic
low-power microscopes allow further studies of fea-
tures that cannot be interpreted by a magnifying
glass only. The advantage of these observations is
that they are not invasive, i.e., the bone will not be
destroyed by these examinations. The disadvantage
is that there is no information about the internal
structure and the composition of newly formed bone,
such as a secondary layer on the original bone sur-
face.
Preparation and embedding of specimens
for light microscopy
Light microscopy can be employed in two ways.
Polished surfaces of bone samples can be observed
using reflected light, or ground sections can be ex-
amined by transmission light. For the latter method,
which is much more efficient, the bone sample has to
be sectioned or ground down to become translucent.
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
Fig. 1. Sampling and preparation of thin-ground sections.
When archaeological or sometimes even forensic
bones are to be examined, the method of choice is the
grinding process (e.g., Hackett, 1976; Stout, 1992;
see Fig. 1). The author has modified these tech-
niques (Schultz, 1988; Schultz and Drommer, 1983),
using a special embedding procedure (see below, and
Fig. 1). After this, thin-ground sections with a thick-
ness ranging between 15–100 ␮m are produced. The
nature of pathological structures can then be rela-
tively easily detected (Blondiaux et al., 1994; Hack-
ett, 1976; Michaelis, 1930; Moodie, 1923; Schultz,
1986, 1987b, 1993a,b; Weber, 1927). For a reliable
diagnosis, it is important to prepare two thin-ground
sections from different levels from each bone sam-
ple, because microscopic structures can also change
in their three-dimensional architecture. Although
light microscopy is a relatively old technique, this
kind of analysis is still one of the most efficient,
whereas regular scanning-electron microscopy (see
below) is only able to check the faces of a bone or the
cut or sawn planes of bone sections.
Excavated skeletal remains are usually lacking in
strength and elasticity, due to decomposition of the
organic matrix, and are therefore fragile and ex-
tremely brittle, no longer having the quality of fresh
bone. Archaeological undecalcified bone, embedded
or not, should not be cut by microtome, because the
procedure may cause serious artifacts (e.g., micro-
fractures, decay) leading to false diagnoses. If the
111
bone sample is decalcified, it is easier to cut. How-
ever, if a poorly preserved bone sample is decalcified,
nothing will remain worth analyzing, and special
techniques must be used for the sampling and pro-
duction of histological specimens (Donath, 1983;
Kaissling, 1973; Schultz, 1988, 1997a; Schultz and
Drommer, 1983). In most cases, the technique of
choice is the preparation of undecalcified thin-
ground sections after embedding, which is highly
suitable even for very poorly preserved bone sam-
ples. To prepare thin-ground sections for light mi-
croscopy, a special technique was established based
on the method of plastination developed by von Ha-
gens (1979), but modified for histological purposes
by M. Schultz and M. Brandt (cf. Schultz, 1988). For
embedding (see Fig. 1), we use a special Epoxy resin.
Before being embedded, the samples are dehydrated
using ascending concentration steps of alcohol solu-
tions (e.g., solutions of 40%, 50%, 60%, 75%, 80%,
85%, 90%, and 95% of alcohol for usually 1 day
each). The next day, the sample is put into methyl
chloride as an intermediate solution for the ex-
change of substances. The sample is then ready to be
embedded. Our experience, which has been gathered
over decades, has shown that the most suitable em-
bedding substance for macerated bone samples is
the Epoxy resin Biodur威, which was developed by
von Hagens (1979). Biodur威 is easy to handle during
the embedding procedure, which takes place under a
112 YEARBOOK OF PHYSICAL ANTHROPOLOGY
relative vacuum (motor vacuum pump). This resin is
highly suitable for organic materials which might
still contain minimal vestiges of moisture. Using
Biodur威, the process takes at least 3 weeks because
the embedding process runs very slowly; however,
the results are excellent. Thus, from the sawing of a
sample from a bone until the moment when the
thin-ground section is viewed by microscope, 4 or
even 6 weeks might pass. The embedded samples
are mounted on a glass slide, cut with a special
circular saw (Dr. Steeg and Reuter, Frankfurt am
Main) and ground down to a thickness of 100 ␮m
(microradiographs), 70 ␮m and 50 ␮m (unstained
thin-ground sections examined in plane or polarized
light), or 15 ␮m (stained thin-ground sections exam-
ined for cells, collagen bundles, and special soft-
tissue structures in plane light) with the same saw,
using a special circular disk. Finally, the polished
ground section is labeled and protected by a thin
cover glass. Such thin-ground sections prepared by
this procedure, from brittle or even rotted bone, can
be examined satisfactorily. Thus, no artifacts pro-
duced by the embedding (such as from the use of
methyl metacrylate) or the grinding process disturb
the microscopic examination of even large speci-
mens.
A final point should be taken into consideration
while assessing possible techniques. A microtome
section of an undecalcified bone sample is, as a rule,
limited to small sizes, e.g., 5 ⫻ 5 or 10 ⫻ 10 mm.
With a Leica sawing-microtome (Innenlochsäge), the
sample size can be larger (ca. 25 ⫻ 25 mm). How-
ever, for thin-ground sections prepared after the
plastination process from an undecalcified bone
sample, the sizes of sections for routine examina-
tions can be 28 ⫻ 48 or 46 ⫻ 76 mm or, in special
cases, even larger (e.g., 120 ⫻ 120 mm). Thus, using
the latter technique, a cross section of a femur can
be examined in its entirety in the same section, even
if the bone is thickened by osteomyelitis to double or
triple its size. As mentioned below, the ways of di-
agnosing macerated bone samples are different from
the schedules used in recent pathology. Further-
more, large samples of bones, such as complete cross
sections, are inevitably necessary. Large sections
from undecalcified bone samples can only be pre-
pared after the embedding of the sample because
archaeological bone is, as a rule, very brittle and
sometimes even disintegrated, and will fall to pieces
when cut without embedding.
Microscopy using plane light
Using transmission microscopy, in plane and po-
larized light, unstained and stained thin-ground sec-
tions of hard tissues (e.g., from bone samples), as
well as unstained and stained sections of soft tissues
(e.g., from muscles, liver, or lungs) prepared by mi-
crotome, can be investigated. In particular, stained
sections made from soft tissues are very clearly ob-
servable in plane light.
[Vol. 44, 2001
Several techniques are available for preparation
of histological sections from mummified soft tissues
for microscopic research (e.g., Sandison, 1955; Zim-
merman, 2001). All these techniques are based on
the rehydration of mummified samples before cut-
ting with a microtome. During the process of rehy-
dration, the original connection between the differ-
ent tissues, particularly the connective tissue, is
sometimes considerably disturbed or even destroyed
by a relative swelling of the tissues. Small parasites
affecting the individual during his lifetime can be
washed out by the rehydration process (Schultz and
Gessler-Löhr, 1992). Therefore, a new technique for
preparing histological specimens of mummified tis-
sues was introduced, using thin-ground sections. A
very efficient procedure for preparing thin-ground
sections of prehistoric and historic skeletal remains
recovered in archaeological excavations or kept
in bone collections has already been described
(Schultz, 1988; Schultz and Drommer, 1983). How-
ever, up to now, this technique has never been used
for mummified specimens. The idea is that soft-
tissue samples are embedded without rehydration,
using a modified plastination process (Schultz,
1997b; Schultz and Gessler-Löhr, 1992). This em-
bedding technique was used to prepare thin-ground
sections from soft tissues of an organ bundle from an
old Egyptian mummy of a boy who died at age 5–7
years. The thin-ground sections demonstrate that
many very small parasites, which were identified as
Microfilariae, were still in place in the soft tissue
(Fig. 2A). Thus, the boy suffered from microfilariasis
(Schultz and Gessler-Löhr, 1992). No Microfilariae
were found in rehydrated samples. Also in other
cases, this technique worked sufficiently well, e.g.,
for studying the debris of arthropods in canals in
mummified tissues (Schultz, 1993b).
Microscopy using polarized light
The use of polarized-light microscopy is very help-
ful in examining ground sections produced from dry
bone samples. The identification of collagen fibers
and the special pattern of mineralized structures in
normal (Fig. 2B) and pathologically changed bones,
as well as in calcified and ossified soft tissues, e.g.,
parts of blood vessels, tendons, muscles, and menin-
ges, can be clearly demonstrated by polarized-light
examination. Thus, structural changes caused by
pathological processes can be classified. Also, the
presentation of various crystals (e.g., cholesterol,
uric acid), which are, for instance, found in gall-
stones and renal calculus, can be detected and clas-
sified (cf. Schultz, 1982). Undecalcified archaeologi-
cal bone samples cut by microtome (i.e., not ground
sections) can, of course, also be studied in polarized
light. However, the result is not very satisfactory
and frequently leads to false diagnoses because of
the artifacts produced by the cutting procedure (e.g.,
microfractures). The examination of decalcified bone
samples in polarized light is, as a rule, also very
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 113

Fig. 2. Demonstration of use of various microscopic techniques in paleopathology. A: Microfilariae (arrows). Mummified tissue
from respiratory system. Egyptian mummy of a 5–7-year-old boy, Ptolemaic-Roman times. Undecalcified, nonrehydrated, stained
thin-ground section (20 ␮m), viewed through the microscope in plane light. Magnification, ⫻640. B: Cross section through compact
bone substance of left femur of a mature individual from Achsheim (southern Germany), burial 3, early Middle Ages, Alamannic.
Haversian systems (osteons). Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light. Magnifi-
cation, ⫻100. C: Cross section through compact bone substance of a femur. Künzing (southern Germany), Late Roman period, burial
32. Haversian systems (osteons) and lines of arrested appositional growth (arrows). Microradiograph of undecalcified thin-ground
section (100 ␮m), viewed through the microscope in plane light. Magnification, ⫻6. D: Howship’s lacunae. Osteoclastic tumor. Sayala
(Egyptian Nubia), Coptic period, individual I3. Scanning-electron microscopic image. Bar, 10 ␮m.

unsatisfactory, because the decalcification proce-
dure affects the collagen structure.
Additionally, polarization microscopy is a useful
tool in paleontology and paleoanthropology to study
the microstructure of fossil bone (e.g., Schultz,
1999c), as well as in forensic anthropology to esti-
mate the time a skeleton has remained in the soil.
This latter can be achieved using quantitative meth-
ods (Berg, 1982, 1997). Another relatively quick
method, in which a portion of undecalcified bone
tissue is filed off, was developed by Berg (1982). The
bone dust is stirred and then quantitatively exam-
ined in polarized light for its amount of anisotropic
particles. This method, however, provides only a
very rough estimation of burial time.
The use of a hilfsobject red first-order (quartz) as
compensator (Schultz, 1988) gives more information
about the structural features of macerated bone and
ossified soft tissues because various structures, e.g.,
orientation of collagen fibers in poorly preserved
bone structure and agents and products of diagen-
esis, such as crystals and floral and faunal remains,
are better observable. Thus, it is possible to obtain
an impression of the three-dimensional structures of
bone. Using such a hilfsobject as compensator, the
microscopic view of an unstained 50-␮m thin-ground
section becomes, in the polarized light, a very color-
ful picture by the physical phenomenon of interfer-
ence. These interference colors originate between
the crossed polarizing filters (Nikols). Thus, the col-
ors are not those of a solar spectrum, but are
grouped in a character sequence called Newton’s
series. The colors are formed in orders that, in bire-
fringent materials, must be interpreted according to
material thickness and birefringence (Delly, 1998).
The background is always a light purple-red. The
course of collagen fibers, e.g., in the Haversian sys-
tems, is colored in yellow (in thicker sections, or-
ange) or in blue (in thicker sections, green). Haver-
sian systems appear as “negative crosses” which are
represented by so-called Maltese crosses. This
means that fibers that run exactly parallel to the
axis of the microscope are inactive in polarized light.
Therefore, they show the same purple-red color as
114 YEARBOOK OF PHYSICAL ANTHROPOLOGY
the background, whereas fibres which run only
slightly oblique have a dim-violet color. Fibers which
run in polarized light parallel to the direction of the
additive position are blue, which those at right an-
gles are yellow (Weber, 1927). An additional point is
the examination of thin-ground sections prepared
from burnt or heated bones in polarized light using
a hilfsobject red first order (quartz) as compensator
(see above). The effects of heat and fire lead to typ-
ical changes in the microstructure of the bony tis-
sues (Grimm and Strauch, 1959; Piepenbrink and
Herrmann, 1988; Schultz, 1986) which are also ex-
pressed in the bone collagen (Schultz, 1986, 1997b;
Teschler-Nicola and Schultz, 1984). Furthermore,
the intensity of staining gives an accurate idea of the
thickness of the thin-ground section (e.g., in a
thicker section, i.e., approximately 75–95 ␮m, struc-
tures are presented in orange and green; in a thin-
ner section, i.e., approximately 50 –70 ␮m, in yellow
and blue), which is an important aid during prepa-
ration of the specimen.
Microradiography
Microradiography can easily detect the stage of
ossification and the degree of calcification of bones
and other tissues (e.g., Jowsey, 1963, 1977). This
technique has been used in paleopathology for many
decades to diagnose diseases (e.g., Schultz, 1986,
1988) and postmortem structural changes at the
microlevel (e.g., Baud and Morgenthaler, 1956) in
subfossil and fossil bones. Microradiography pro-
duces reliable results which can also be used in
paleopathology. As an example, very fine lines found
in the compact substance of long bones (Fig. 2C) give
the paleopathologist information similar to the
transverse linear enamel hypoplasias in the teeth
and Harris lines in the metaphysis of long bones
(Herrmann et al., 1990; Schultz, 1986). Indeed,
these lines represent cement lines, probably due to
arrested appositional growth. These lines should not
be mistaken for the cement lines found in secondary
osteons. The lines presented in Figure 2C are situ-
ated in the compact bone substance represented by
secondary Haversian bone oriented parallel to the
external circumferential lamellae of the shaft of the
long bone. Also, newly built bone formations such as
subperiosteal layers caused by an inflammatory pro-
cess, callus formation after bone fracture, and bone
tumors can be identified and classified using this
technique.
Scanning-electron microscopy
Scanning-electron microscopy (SEM) is a helpful
tool in paleopathology. However, it should be used in
combination with other microscopic methods, be-
cause only surfaces of tissues can be inspected. Us-
ing transmission light microscopy, the observer is
looking through the bony tissue; using regular scan-
ning-electron microscopy, the observer sees only the
bone surface. Furthermore, and this is particularly
[Vol. 44, 2001
the case in viewing sections of bones with the scan-
ning-electron microscope, the microstructure of ar-
chaeological bone such as the lamellar formation of a
bone trabecula is not really visible because it is, as a
rule, very brittle and will crumble away at the cut or
sawn face. However, if the back-scattered electron-
mode (BSE-mode in SEM) of a scanning-electron
microscope is available for investigations, internal
structures of the bone tissue, e.g., the quality of the
lamellae of a bone trabecula or the degree of miner-
alization of the inorganic bone substance, can be
studied in a similar way as in transmission light
microscopy.
Using the high-magnification capability of an
SEM, even very fine details representing intra vitam
changes such as Howship’s lacunae (Fig. 2D), and
postmortem alterations such as plant roots (Fig. 6B)
and fungi (Fig. 6C,D,F), are visible. These features
can sometimes be important in differential diag-
noses. For the diagnosis of perimortem cut marks
and injuries, this technique also produces very good
results (Wakely, 1993).
Other techniques
There are also some other techniques, such as
fluorescence microscopy (e.g., for the detection of the
vestiges of postmortem or intra vitam fungi), phase-
contrast microscopy, and interferential-contrast
microscopy (e.g., examination of soil-living microor-
ganisms), which are sometimes useful in paleopa-
thology. However, these techniques are, as a rule,
not routine and only rarely needed.
Occasionally, close-up endoscopy can also contrib-
ute significantly to the microscopic research of dry
bones. Magnifications up to approximately 50⫻ are
possible. With this technique, the internal surfaces
of the endocranial face of the base and vault of a
skull, the paranasal sinuses, and the middle ear
region, as well as the medullary cavity of long bones,
can be viewed noninvasively by low-power micros-
copy. This kind of examination is very helpful in
establishing reliable differential diagnoses of in-
flammatory and hemorrhagic diseases of the skull.
MICROSCOPIC STRUCTURE OF BONE
The following discussion is only intended to pro-
vide a basis for understanding the microstructure of
bone as it is applied to bone histopathology (cf.
Schultz, 1997a). For in-depth discussion of this sub-
ject, the reader is referred, for example, to Bloom
and Fawcett (1994), Cormack (1987), Hancox (1972),
Junqueira et al. (1998), Martin and Burr (1989),
Pritchard (1972), Schaffer (1930), and Weidenreich
(1930). All the necessary technical terms referred to
below are listed and defined in the glossary.
General histology of bone
The thin external surface of bones is called corti-
cal bone (corticalis). When it is thick, it is called
compact bone substance (substantia compacta). At
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
joint surfaces, the bone is very smooth, is covered by
articular cartilage, and shows no blood-vessel ca-
nals. This bone is called subchondral bone. The in-
terior of bone consists of a spongy, porous substance
called cancellous or trabecular bone (substantia
spongiosa) containing the red bone marrow. In the
bones of the skull vault, the spongy structure is the
diploë (diploë), and the cortical structures are the
external lamina (lamina externa) and the internal
lamina (lamina interna). Long bones have a rela-
tively large, tubular medullary cavity (cavitas med-
ullaris) containing the yellow bone marrow, which
mainly consists of fat cells in older children and
adults.
Characteristic cells called osteoblasts and osteo-
cytes are embedded in the bone matrix. During bone
growth, osteoblasts are mainly concentrated be-
neath the periosteum and other bone surfaces such
as the trabeculae of the spongy bone or the endosteal
lamina of the long bones. They have very thin cyto-
plasmic extensions with which they communicate.
Osteoblasts secrete an amorphous preosseous sub-
stance called osteoid, which is rich in densely packed
collagen fibers. Osteoblasts are responsible for the
synthesis of the organic substances of the bone. Os-
teoid becomes mineralized due to the deposition of
calcium phosphate crystals.
In principle, an osteocyte is an osteoblast that has
become embedded within the bone matrix. Osteo-
cytes lie in oval, flat holes called lacunae and also
have very fine, filopodium-like cytoplasmic pro-
cesses which run through canaliculi. These canalic-
uli spread radially from the lacunae of the bone
cells.
Osteoclasts are mobile, multinucleated giant cells
which vary greatly in size and in their number of
nuclei, and play an active and major role in bone
resorption. They are also responsible for resorption
processes in the ground substance. As a rule, they
are found in sharply defined erosion bays, which are
called Howship’s lacunae (Figs. 2D, 20A).
In routine histological examinations, only two
types of human bone can strictly be differentiated
(cf. Bloom and Fawcett, 1994; Hancox, 1972; Jun-
queira et al., 1998): woven bone and lamellar bone.
Lamellar bone can be further organized into several
recognizable forms, e.g., circumferential or Haver-
sian, as described below.
When bone originates, it will, as a rule, develop
primarily as woven bone (e.g., fetal bone, callus,
newly built bone structures in osteosarcoma). The
woven nature of this type of bone is due to the fact
that the collagen fibers in the ground substance,
which form partly fine and partly coarse bundles, do
not show regular orientation. Thus, there is no la-
mellar structure (Fig. 3). The osteocytes also seem to
be more randomly scattered throughout the ground
substance of woven bone.
Lamellar bone may be compact or cancellous. Typ-
ical features of lamellar bone tissue are lamellae
(layers) and regular lacunae with canaliculi. The
115
Fig. 3. Woven bone. Bone sample from Early Modern times.
Undecalcified thin-ground section (50 ␮m), viewed through the
microscope in polarized light. Magnification, ⫻100.
lamellae are separated from each other very dis-
tinctly, and are characterized by the presence of
osteocytes and collagen fibers. Within each lamella,
the collagen fibers have a typical orientation. The
course and angle of ascent of collagen fibers alter-
nate from lamella to lamella, which is important for
their biomechanical function. The microstructure of
lamellar bone, particularly the course and orienta-
tion of collagen fibers which are birefringent, can be
easily observed in polarized light (Fig. 2B). When
the course of collagen fibers looks bright in polarized
light, they are oriented transversely to the light
beam, i.e., the light beam meets the fibers vertically
(anisotropic). When the collagen fibers look dark,
they are oriented approximately in the direction of
the light beam, i.e., the light beam meets the fibers
orthograde or obliquely (Fig. 2B). The orientations of
the lamellae vary, but in the compact tissue of long
bone diaphyses, the disposition of the lamellae is
very regular (Fig. 2B).
Viewing a cross section of a long bone by low-
power microscope, the basic or circumferential la-
mellae enclose a long bone shaft on the external
(periosteal) and on the internal (endosteal) surfaces.
The number of external lamellae exceeds that of
internal lamellae. As a rule, the internal basic la-
mellae do not represent a closed boundary, because
small bone trabeculae of the cancellous bone of the
metaphysis originate from these lamellae. Between
the external and the internal basic lamellae, the
compact bone substance is situated. The number of
external and internal basic lamellae decreases with
age. During appositional growth in the long bones of
adults, the external circumferential lamellae are re-
placed by secondary Haversian bone, while the in-
ternal circumferential lamellae are resorbed (see be-
low).
The most common type of special lamellae is found
in Haversian systems, which are also called osteons.
An osteon is a system of circular lamellae and is the
predominant structural unit of adult compact bone
substance (Fig. 2B). The Haversian canal, which
116 YEARBOOK OF PHYSICAL ANTHROPOLOGY
contains blood vessels, is situated in the center of an
osteon. The osteon includes a large number of lacu-
nae, each containing an osteocyte. The canaliculi
associated with every bone cell lacuna form a char-
acteristic network. Particularly in compact bone tis-
sue, the irregular angular spaces between the os-
teons are filled with lamellae, called interstitial
lamellae, which are remnants of unremodeled pri-
mary lamellar bone or the remains of osteons that
have perished or have been partly destroyed during
the internal growth and reconstruction of the bone.
The external and internal surfaces of bones are
covered by connective tissue called periosteum and
endosteum, respectively. Surfaces of bone not cov-
ered by these structures are resorbed by osteoclasts.
The periosteum consists of a stratum fibrosum as
external layer, and a stratum osteogenicum as in-
ternal layer.
Histogenesis and growth of bone
There are two different kinds of osteogenesis: in-
tramembranous and chondral ossification. During
intramembranous ossification, bone originates di-
rectly in connective tissue (e.g., bones of the skull
vault). During chondral ossification, the bone origi-
nates indirectly from a primary cartilage model
which secondarily ossifies (most bones of the skele-
ton). There are two kinds of chondral ossification:
either the bone originates at the periphery of the
cartilage model (e.g., at the diaphyses of long bones
representing the periosteal band or collar), which is
called perichondral ossification, or it originates by
intracartilaginous ossification (e.g., center of epiph-
yses), which is called endochondral ossification.
Chondrally ossified bones principally grow in
length at growth or epiphyseal plates oriented
roughly transversely between the diaphysis and the
epiphyses. The increase in diameter of bones is
achieved by appositional growth. Bones originating
intramembranously also grow by apposition.
At fetal and early infant ages, the microscopic
structure of bone is only dependent on its origin,
meaning that primarily woven bone is found. The
characteristic compact bone substance represented
by Haversian systems develops later and depends on
the functional biomechanical stress experienced
during a lifetime (cf. Currey, 1984). The primary
woven bone develops into primitive osteonal bone,
which is built up during various generations of os-
teons. In principle, the same process, which starts in
very early infancy, occurs throughout life and can be
studied microscopically in cross sections of the shaft
of a long bone. The initial step involves bone resorp-
tion. This process, which is associated with the pres-
ence of osteoclasts, affects not only parts of the
newly built primitive Haversian systems, which are
mainly found in the compact bone substance and in
areas that are established by periosteal bone appo-
sition during the growth in diameter of long bones,
but sometimes also in endosteal bone, where the
internal basic lamellae are situated. In this way,
[Vol. 44, 2001
small cavities (⫽ resorption holes or resorptive bays)
filled with blood vessels and embryonic bone marrow
are formed. The destruction then stops, the activity
of the osteoblasts starts, and a new generation of
osteons (⫽ secondary osteons) originates from the
concentric growth of lamellae around the blood ves-
sels. In the same way, the third and fourth genera-
tions of osteons grow. Remains of destroyed osteons
survive as interstitial lamellae. In a very similar
way, the ossification process occurs in cancellous
bone and at the endosteal face of long bones during
reparation processes. However, regular osteons are,
as a rule, not built up at these places.
Occasionally, in some parts of the skeleton, can-
cellous bone is transformed physiologically into com-
pact bone. In this case, the cavities of the cancellous
bone, which are usually filled with bone marrow,
become narrower and narrower, as the osteoblasts
covering the bone surface put down layer after layer
over the primary trabeculae. If this process contin-
ues, the primary marrow cavity containing the blood
vessels of this area becomes so narrow that thin
bone lamellae are concentrically built up around the
blood vessels and a primitive Haversian system
emerges.
Sometimes, vestiges of arrested growth are visible
in microradiographs obtained from cross sections of
the shafts of long bones (see above; Herrmann et al.,
1990; Schultz, 1986). These vestiges are expressed
in microradiographs in the form of very fine, radio-
dense lines representing cement lines that origi-
nated after an arrest of appositional bone growth
(Fig. 2C). A very similar phenomenon is seen in the
growth of the bones of the skull vault. In these cases,
characteristic changes in the form of step-like bor-
derlines can be observed at the endocranial face of
the affected bones (Fig. 4A). In the microscopic view
(Fig. 4B), the arrested growth can affect not only the
internal lamina, but also the external part of the
diploë. As a rule, these vestiges of arrested skull
growth can be interpreted as a particular stress
indicator. To a certain degree, these step-like bor-
derlines are comparable with Harris lines, trans-
verse linear enamel hypoplasias, and the above-
mentioned cement lines in the compact bone
substance of the shafts of long bones. As a rule, the
step-like borderlines are apparently remodeled rel-
atively shortly after their origin. However, if a child
dies within a few days or weeks of their origin, they
can be satisfactorily studied. Probably these step-
like borderlines frequently have something to do
with the immediate cause of death.
INFLUENCE OF AUTOLYSIS, DECOMPOSITION,
AND DIAGENESIS ON DIAGNOSTICS
A corpse disintegrates in various ways. Autolysis
is the breakdown of tissues by the action of enzymes
contained in the tissues affected immediately after
death. As a rule, the autolytic process does not
change the microstructure of mineralized or calcified
components of bone. However, autolysis may destroy
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 117

Fig. 4. Evidence of arrested growth of skull bones demonstrated in an approximately 4-month-old infant from İkiztepe (northern
Turkey), burial 220, Early Bronze Age. A: Step-like borderlines (arrow) at endocranial face of a fragment of parietal bone. B: Same as
A, but microscopic view. Arrested growth has affected not only the internal lamina, but also the external part of the diploë. a, external
lamina; b, diploë; c, d, levels of internal lamina between the step-like structure. Undecalcified thin-ground section (50 ␮m), viewed
through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25.

cells and soft tissues. This is important to keep in
mind for someone working on special problems at
the molecular biological level. Further disintegra-
tion of soft tissues occurs through decomposition.
During this process, the soft tissues are separated or
resolved into constituent parts or elements, partic-
ularly by bacteria, fungi, and arthropods. This pro-
cess usually takes months or even years. Mineral-
ized or calcified tissues are, as a rule, not affected.
The term “diagenesis” characterizes the disintegra-
tion of mineralized or calcified tissues.
Archaeological bone is known to be affected under
the earth by various factors (e.g., roots of plants,
fungi, algae, bacteria, arthropods and their larvae,
worms, protozoa, and mechanical agents such as
water and crystals). This process, diagenesis, is
characterized by the destruction of bones by physical
and chemical agents produced by the factors de-
scribed above. Diagenesis occurs in the soil after the
process of decomposition. Unfortunately, even to-
day, relatively little is known about the physiology
of the fauna and flora of cadavers, represented by
the various organisms living over many centuries on
and in a corpse causing decomposition and diagen-
esis (cf. Bass, 1997; Hall, 1997; Haskell et al., 1997;
Rodriguez, 1997; Stout, 1987). All these postmortem
factors produce damage that can falsely be diag-
nosed by paleopathologists as lesions caused intra
vitam by diseases (pseudopathology; see below). As a
rule, many of the changes cannot be differentiated
by macroscopic or radiological analysis, but are eas-
ily diagnosed by microscopic techniques (cf. Schultz,
1986). For instance, compact bone can be destroyed
by characteristic tunnel-like canals caused by the
postmortem growth of fungi or algae (Hackett,
1981). Due to intensive growth of fungi, these tun-
nels can flow together and produce relatively large
destruction holes that can be macroscopically mis-
taken for intra vitam osteoporosis or vestiges of a
metastasizing tumor. A seemingly thickened newly
built bone formation on the external surface of a
bone, which is macroscopically thought to be the
product of an inflammatory periosteal reaction, can
be diagnosed microscopically in a thin-ground sec-
tion as a postmortem layer due to the aggregation of
crystals (brushit) having originated during diagen-
esis. Net-like impressions on the internal lamina of
the skull vault, which seem macroscopically suspi-
cious of the vestiges of a hemorrhagic meningeal
reaction, may be shown by light or scanning-electron
microscopic analysis to be the result of postmortem
growth of plant roots. Snake-like, irregular grooves
on the external skull vault that have a coarse bottom
can be caused by an inflammatory process of the
scalp and the adjoining bone (e.g., nonspecific osteo-
myelitis, treponemal diseases). However, in such a
case, microscopic examination must be carried out to
exclude postmortem changes due to soil and water
erosion.
Furthermore, it should be kept in mind that these
postmortem factors can affect the results of immu-
nohistochemical and molecular biological investiga-
tions (e.g., DNA, bone proteins) as well as the exam-
ination of trace elements and stable isotopes
(Schultz, 1986, 1997b; Schwartz and Schultz, 1994).
Therefore, microscopic investigation is indispens-
able before examination of archaeological remains
by chemical and physical techniques can be carried
out (Hanson and Buikstra, 1987; Schultz, 1986).
Sometimes bones are preserved in the ground by
protective surroundings. Thus, the process of di-
agenesis works very slowly and incompletely or is
even suspended. This has, for instance, happened
when a bone has become a fossil. In such a case, the
bone could have been preserved over many thou-
sands of years in a cave or in a rock shelter. How-
ever, subfossils such as prehistoric bones have a
good chance of not being affected by diagenesis if
elements such as copper (Cu), manganese (Mn), and
even iron (Fe) are present in the soil. Microscopic
investigation in combination with element analysis
makes a demonstration of the causes and processes
118 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
of preservation feasible. It is well-known that Cu-
ions preserve organic materials very well, even at
the microlevel, because of their bactericidal efficacy
(Schultz, 1997b). If archaeological bones are found
in close contact with bronze jewelry or bronze weap-
ons, the neighboring bone surfaces will be stained
greenish over hundreds or thousands of years. In
most cases, the histological analysis of these green-
ish-stained bone samples reveals very well-pre-
served bone substance which is sometimes almost in
the same state as fresh bone. The Göttingen re-
search group consisting of S. Berg, W. Bonte, H.
Kijewski, and M. Schultz studied bone samples col-
lected from different prehistoric and early historic
sites in Europe, the Near East, and North America
by morphological and physical techniques. The re-
sults are striking. Manganese (Mn) is able to pre-
serve bone almost as well as copper (Cu), and even
iron (Fe) is able to protect bone structures to a cer-
tain degree (Fig. 20B). It is interesting that the
degree of morphological preservation of the bone
substance actually correlates with the concentration
of soil minerals that have invaded the bone. The
following is a good example. An Alamannic skeleton
from the early Middle Ages (5th–7th century AD)
from Mertingen (Southern Germany) was relatively
well-preserved. A bone sample taken from the femur
shaft revealed not only very good preservation mi-
croscopically, but also a remarkable concentration of
the elements manganese (Mn) and iron (Fe), partic- Fig. 5. Results of element analysis (atomic absorption spec-
ularly in the external narrow zone of the cross sec- troscopic technique). Concentrations of manganese (Mn), iron
tion (Fig. 5, zone 1), checked by atomic absorption (Fe), and copper (Cu) measured in three different morphological
spectroscopic technique. The concentration of these zones of the cross section through the femur of a mature Alaman-
two elements, especially iron, was exceedingly high nic warrior from Mertingen (southern Germany), burial 13, Early
Middle Ages.
in this narrow external zone (Fig. 5, zone 1) and not
so high in the middle zone (Fig. 5, zone 2). The very
high concentration of iron (1,110 mg/100 g) can be structures of bone in a relatively characteristic man-
explained by the fact that at the funeral, an iron ner, as in the following example. During the Late
sword was placed by the funeral across the upper leg Bronze Age of Western Anatolia, burials were laid
of this Germanic warrior. During the disintegration down at a small cemetery into the sand of the shore
process of the sword, iron-oxide coated the bone
shaft, protecting the bony tissue from further di-
agenesis. Additionally, the increased concentration Fig. 6. Various factors of diagenesis. A: Fragment of skull
of manganese caused by ground water that flooded vault. Beşik Tepe (Western Anatolia), Late Bronze Age, burial 1.
Vestiges of erosion caused by soil and water. a, bone substance; b,
the burial ground many times, and washed manga- sand crystals. Undecalcified thin-ground section (50 ␮m), viewed
nese from the soil into the bone, had a strong pro- through the microscope in polarized light using a hilfsobject red
tective effect. These processes lasted many decades. first order (quartz) as compensator. Magnification, ⫻25. B: Re-
Therefore, the external zone of the bone (Fig. 5, zone mains of plant roots. Tetelpan (Mexico), Preclassic period. Scan-
1, represented morphologically by Fig. 20C) was ning-electron microscopic image. Sporangium and spores. Bar, 40
␮m. C: Fungus in historic bone sample: sporangium and spores in
slightly affected by diagenesis before the protective spongy bone substance of tibia, Klosterneuburg, Lower Austria,
effect of iron and manganese stopped the disintegra- Early Modern times. Scanning-electron microscopic image. Bar, 4
tion of the bone substance (Fig. 20C). The concen- ␮m. D: Fungus (probably Aspergillus flavus) in Haversian canal
tration of iron and manganese exceeds the normally of compact bone substance of left tibia (E-4), Klosterneuburg,
Lower Austria, Early Modern times. Undecalcified thin-ground
observed level of these elements in archaeological section (50 ␮m), viewed through the microscope in plane light.
bones by approximately 5–10 times. Magnification, ⫻160. E: Algae growing on bone surface. Micro-
photograph taken by Dr. B. Süssmann-Bertozzi. F: Haversian
Soil and water canal with vestiges of growth of actinomycetes (a) and fungal
Vestiges of destruction in archaeological bones are hyphae (b), Tetelpan (Mexico), Preclassic period. Scanning-elec-
tron microscopic image. Bar, 2 ␮m. G: Remains of a mite in
often caused by the mechanical influence of the soil prehistoric bone sample. Scanning-electron microscopic image.
in which the corpse has been buried. Water and sand Bar, 20 ␮m. H: Remains of exuvia of a mite in prehistoric bone
are able to change bone surfaces or even the internal sample. Scanning-electron microscopic image. Bar, 10 ␮m.
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 119

Fig. 6.
120 YEARBOOK OF PHYSICAL ANTHROPOLOGY
of Beşik Bay, which was one of the ancient harbors
of Troy. Some of these skeletons showed character-
istic vestiges of erosion (Fig. 6A), which were caused
by weathering due to sand crystals in the mud that
were moved by the power of seawater (Wittwer-
Backofen et al., 2000).
Furthermore, the microscopic examination of
skeletal remains can prove where a burial was pri-
marily placed. As a rule, in the spaces of cancellous
bone, small particles of the soil in which the burial
was primarily laid can be detected by the microscope
(Fig. 20D). Using polarized light, principally, the
microscopic analysis is able to reconstruct the qual-
ity and the composition of soil (e.g., sand, loess,
humus). Thus, there is probable evidence of a sec-
ondary burial if the soil particles from the interior of
the bone are different from the soil particles from
the burial pit.
Plant roots
Plant roots are one of the most common causes of
postmortem bone destruction (Fig. 6B). Large roots
create distinctive traces on bone surfaces which are,
as a rule, not difficult to diagnose (Schultz, 1997b).
However, very small, hair-like roots are able to pro-
duce fine defects, which can be mistaken for the
vestiges of diseases, e.g., a sulcus representing a
blood vessel impression on the internal lamina of the
skull vault, or an intra vitam cut mark (Schultz,
1986, 1997b). It is important to know that these fine
roots can also grow into the paranasal sinuses and
the medullary cavities and produce pseudopathol-
ogy.
Fungi, algae, and bacteria
A large group of organisms that destroy archaeo-
logical skeletal remains include fungi, algae and
bacteria (Schultz, 1986, 1994a, 1997b). Fungi (Fig.
6C,D,F) and algae (Fig. 6E), in particular, create
small holes, cavities, and channel-like structures
(Fig. 20E). The latter are called bohrkanäle (Wedl,
1864) or tunnels (Hackett, 1981). Such traces are
found in the majority of archaeological bones and
can be observed in plane light. Using fluorescence
microscopy or phase-contrast microscopy and scan-
ning-electron microscopy, not only the specimens
but also the vestiges and the products of the organ-
isms’ growth can be studied (e.g., Basset et al., 1980;
Keith and Armelagos, 1982, 1988, 1991; Piepen-
brink, 1984; Schultz, 1986, 1997b). Sometimes the
growth traces of Actinomycetes, very small bacteria
that grow like mycelia, can be observed (Fig. 6F).
Arthropods
Remains of arthropods are frequently seen in
bones or mummified tissues recovered in archaeo-
logical excavations, when microscopic techniques
are used (Fig. 6G,H). In many cases, the origin of
these small intruders is uncertain, because of the
poor preservation of the findings. Therefore, partic-
[Vol. 44, 2001
ularly in the case of remains of insects, it is difficult
to decide whether these specimens parasitized the
body during its lifetime, or whether they appeared
immediately after death in the cadaver, or the used
the macerated bones during their time under the
ground as a habitation (Schultz, 1986, 1997b). For
differential diagnoses, it is necessary to identify the
remains of insects and their larvae, worms, proto-
zoa, spores of fungi, and bacteria. Sometimes para-
sites affecting the living resemble specimens that
live in the cadaver or belong to the fauna and flora of
the ground. Only reliable diagnoses (see below) es-
tablished by microscopic research make the study of
infectious diseases of past populations feasible.
Thus, exact knowledge of these faunal and floral
specimens is still a requirement.
Crystals
Under certain conditions of diagenesis, new crys-
tals can develop within the bone originating from
natural bone apatite, e.g., brushit, which is acidic
calcium phosphate (Herrmann and Newesely, 1982).
These newly crystallized structures can aggregate
and almost completely break up interior structures
of a bone (Fig. 20F), in the same way that frozen
water can burst a full, stoppered bottle (Schultz,
1986, 1997b).
SELECTED EXAMPLES OF MECHANISMS OF
PATHOLOGICAL BONE CHANGES: THE
DETERMINATION OF VESTIGES OF DISEASES
IN MACERATED BONES BY MICROSCOPY
General comments
It is well-known that caries, fractures, genetically
caused malformations of bones, osteoarthritis, myo-
sitis ossificans, and various inflammatory bone pro-
cesses, such as nonspecific osteomyelitis and perios-
titis, as well as many osteoblastic and osteoclastic
bone tumors, can frequently be diagnosed macro-
scopically in ancient bones. Additionally, some defi-
ciency diseases, such as scurvy, rickets, and anemia,
often produce characteristic changes in bone tissue
that can be observed without a microscope. How-
ever, in many cases, reliable diagnoses are difficult
to establish (see above). Therefore, it is fortunate
that many of these diseases cause specific changes
not only at the macroscopic, but also at the micro-
scopic level. The results of microscopy can provide
reliable differential diagnoses and, in many cases,
exact diagnoses.
The diseases which can be diagnosed by micros-
copy are, as a rule, put into different classes accord-
ing to their specific features. There are numerous
books and articles dealing with pathological bone
changes in recent pathology that could help in diag-
nosing ancient bones (e.g., Adler, 1998; Jaffe, 1972;
Resnick and Niwayama, 1981; Revell, 1986; Scha-
jowicz, 1981). However, we have to be aware that in
the paleohistopathology of dry bones, the diagnostic
criteria can be quite different from those used in
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
recent pathology, where soft tissues and cells are
available as important diagnostic markers. There-
fore, the classification of diseases investigated by
paleohistopathologists does not necessarily conform
in all ways to that used by recent pathologists. In
paleohistopathology, we must first classify morpho-
logical features before establishing a final diagnosis.
For instance, a porotic skull vault can be due to
various diseases (see below) such as anemia, scurvy,
rickets, osteomyelitis, periostitis, inflammatory pro-
cesses of the scalp, or even postmortem changes.
Therefore, the term “porotic hyperostosis,” which
describes only a morphological feature, is not char-
acteristic of a single but of several diseases. In the
end, the final diagnosis must be made using the
results of a microscopic analysis.
It is striking that in the paleopathological litera-
ture (e.g., Tyson, 1997), contributions dealing with
microscopic research on archaeological skeletal re-
mains are relatively rare. Even in comprehensive
books, such as Aufderheide and Rodrı́guez-Martı́n
(1998), Brothwell and Sandison (1967), Dastugue
and Gervais (1992), Jarcho (1966), Ortner and
Aufderheide (1991), Ortner and Putschar (1981),
Steinbock (1976), and Živanović (1982), light micro-
scopic research on ancient bone is not at all or not
very well represented. Therefore, in this contribu-
tion, the emphasis is laid on the microscopic diagno-
sis of diseases that can only be diagnosed reliably by
light microscopy, using thin-ground sections pre-
pared from dry bone tissue. Table 2 gives an outline
and classification of various disease types diagnos-
able by light and scanning-electron microscopy ac-
cording to traditional pathology criteria.
As mentioned above, the main problem in the
microscopic investigation of archaeological skeletal
remains is that soft tissues and cells, which play an
important role in pathological investigations on re-
cent materials, cannot be studied to establish a re-
liable diagnosis. Therefore, no cytological investiga-
tion can be carried out, and a true histological
examination of archaeological skeletal remains in
the primary sense of the term “histology” (i.e., the
study of tissues) is not really possible in all aspects.
However, the mineralized components and some or-
ganic features, such as bone collagen, can be studied
by histology. The most important role in diagnosing
pathological changes in ancient skeletons at the mi-
crolevel is played by the nature of the architecture of
the cortical, compact, and spongy bone structures,
and in particular the newly built bone formations
(Schultz, 1986, 1993a,b). There is a current opinion
that bone tissue always acts in the same way when
affected by inflammatory diseases. It is correct to
say that at the macroscopic level, different diseases
can sometimes produce similar or almost the same
morphological changes in bone. This means that an
inflammatory process affecting the periosteum (e.g.,
hematogenous osteomyelitis or treponemal dis-
eases) produces changes that cannot be differenti-
ated by macroscopic investigation. However, micro-
121
TABLE 2. Classification of disease types following traditional
pathology criteria, with relevant references (diagnoses using
light microscopy and thin-ground sections prepared from
archaeological specimens)
Skeletal dysplasias: abnormal development or inborn
biochemical disorders
Osteogenesis imperfecta
Osteopetrosis
Pfaundler-Hurler’s disease (Schultz et al., 1984)
Osteopoikilosis (Götz, 1988; Wapler, 1998)
Infantile cortical hyperostosis
Metabolic bone diseases
General view (Martin and Armelagos, 1985)
Osteomalacia and rickets (Schultz, 1990; Teegen and
Schultz, 1999; Teichmann, 2000)
Scurvy (Carli-Thiele, 1996; Kreutz, 1997; Schultz, 1990;
Teichmann, 2000)
Fluorosis
Osteoporosis and bone atrophy
Metabolic or due to endocrine disorders (Martin and
Armelagos, 1985; Schultz, 1986, 1997b)
Infectious diseases of bone
Osteomyelitis, osteitis, or periostitis, as follow
Hematogenous osteomyelitis (Hackett, 1976; Schultz, 1986,
1987a; Schultz and Teschler-Nicola, 1987b)
Osteomyelitis after trauma (Teschler-Nicola and Schultz,
1985)
Treponemal infections (Hackett, 1976; Schultz, 1986, 1994b;
Schultz and Teschler-Nicola, 1987b)
Leprosy (Blondiaux et al., 1994; Schultz and Roberts, 2001)
Tuberculosis
Fungi and actinomycosis
Meningitis: nonspecific (Carli-Thiele, 1996; Kreutz, 1997;
Schultz, 1987b, 1989, 1990, 1993a,b, 1999a; Schultz and
Kunter, 1999; Schultz and Teschler-Nicola, 1987a;
Teichmann, 2000; Teschler et al., 1986) and specific, i.e.,
Leptomeningitis tuberculosa (Jankauskas and Schultz,
1999; Schultz, 1994; Templin, 1993; Templin and Schultz,
1994)
Pleurisy: nonspecific (Schultz, 1987a, 1989) and specific
Myositis ossificans (Schultz and Teschler-Nicola, 1987d)
Circulatory disorders
Ideopathic (primary) necrosis
Osteochondrosis dissecans (Konstantinou, 2000)
Perthes disease
Hypertrophic osteoarthropathy or Bamberger-Marie disease
(Schultz, 1987a; Teschler-Nicola and Schultz, 1984)
Hematological disorders
Anemias (Carli-Thiele, 1996; Faerman et al., 2000a; Götz,
1988; Kreutz, 1997; Schultz, 1984, 1986, 1990, 1993b,
1999b; Schultz et al., 2001; Teichmann, 2000; Wapler,
1998; Wapler and Schultz, 1997)
Multiple myeloma
Lymphoma (Schultz, 1986)
Histiocytosis-X
Bone tumors and tumor-like conditions
Osteochondroma
Chondrosarcoma (Schultz, 1986)
Osteoma (Schultz, 1986)
Osteoid osteoma (Schultz, 1986)
Fibro-osseous tumors (Schultz, 1978, 1986)
Osteosarcoma
Primary carcinoma (Schultz, 1991)
Metastatic skeletal lesions (Grupe, 1988; Schultz, 1986,
1993c)
Miscellaneous conditions
Paget’s disease of bone
Hyperostosis frontalis interna (Schultz and Kunter, 1999)
Healing in bone
Healing of fractures, i.e., callus (Schultz and Teschler-
Nicola, 1984, 1987c; Szilvássy et al., 1984)
scopic analysis demonstrates that there is almost
always a pattern of features represented by the ar-
chitectural elements of the cortical, compact, and
122 YEARBOOK OF PHYSICAL ANTHROPOLOGY
spongy bone substances associated with a particular
disease. As a rule, such a pattern is not found in its
exact constellation in any other disease. The classi-
fication and the interpretation of these morphologi-
cal features, particularly found in the newly built
bone formations of a florid, but frequently also of a
slowly developing chronic process, make diagnoses
more reliable. Thus, the pattern of changes is an
efficient key to a diagnosis. These problems of dif-
ferential diagnosis emphasize the need to consider
the total distribution pattern of abnormal lesions in
the skeleton, rather than each one in isolation. Fur-
thermore, there are special indications or better,
specific morphological features at the microlevel,
such as faserfilz-osteons (described by Knese et al.,
1954) in nonpathologically changed adult long
bones, although this kind of osteon is also found
frequently in slowly growing primary osteoblastic
bone tumors; Schultz, 1978, 1986), polsters, and
grenzstreifen (in treponemal diseases; see Glossary),
which are, as a rule, not relevant in recent pathol-
ogy, or which have been neglected but which enable
the paleopathologist to make relatively reliable di-
agnoses. Also, the number and distribution of How-
ship’s lacunae give a relevant impression of the na-
ture of an osteoclastic or osteolytic process (cf. Fig.
20A). Bone pathologists from the end of the 19th and
the first half of the 20th century often diagnosed
macerated bone in a way similar to paleopatholo-
gists of today (e.g., Beitzke, 1934; Gruber, 1938;
Konschegg, 1934; Lauche, 1939). Sometimes an ex-
act diagnosis is not possible, but in almost all cases
the group of diseases characterized by the various
bone reactions (e.g., proliferative, osteolytic), or at
least the nature of the disease, can be determined (e.g.,
inflammatory, hemorrhagic). Thus, the paleohis-
topathologist should try to become very familiar not
only with the microarchitecture, but also with the
pathophysiology of bone.
During microscopic examination, we primarily see
proliferative (productive or osteoblastic) and osteo-
lytic (osteoclastic) processes that reflect bone behav-
ior (cf. Little, 1973). Specific features at the mic-
rolevel enable the observer to group the changes
(e.g., inflammatory or hemorrhagic; see below) into a
pattern that characterizes the process (e.g., perios-
titis or periostosis; see below) by its specific charac-
teristics.
If characteristic vestiges of periosteal bone reac-
tions are macroscopically and microscopically very
similar or even identical, there is a high probabil-
ity that the changes were caused by similar or the
same affecting noxa. A final diagnosis should only
be made using the sum of the results of all diag-
nostics such as macroscopic, radiological, endo-
scopic, and light and scanning-electron micro-
scopic techniques.
Up to now, very little has been achieved in com-
parative histopathological research on ancient skel-
etal remains. As a rule, it should not be too difficult
to differentiate microscopically in ancient bones be-
[Vol. 44, 2001
tween the bony products of an inflammatory process
(inflammation, e.g., caused by an infection) and a
hemorrhagic process (hemorrhage, e.g., caused by
the rupture of a blood vessel) (Carli-Thiele, 1996;
Kreutz, 1997; Schultz, 1987b, 1993a,b; Schultz and
Teschler-Nicola, 1987a; Templin, 1993). However,
the two kinds of processes frequently occur together,
and this makes diagnoses difficult. Thus, basic med-
ical knowledge is required if histopathological work
is to be successful.
In many diseases, the same mechanisms of bone
behavior can be observed. Thus, when we go through
Table 2, which presents a classification of the most
important groups of diseases affecting the skeleton,
we frequently find in various diseases the same
basic reactions of bone behavior represented by a
characteristic morphological pattern of bone archi-
tecture. This morphological pattern persistently in-
fluences the gross morphology of a bone, and this is
what the paleopathologist first observes in a patho-
logically affected bone. Therefore, especially for pa-
leopathologists who are, as a rule, not practicing
bone pathologists but anthropologists, a special, al-
ternate categorization is recommended, shown in
Table 3, that is based on characteristic morphologi-
cal patterns. This categorization follows the macro-
scopic investigation and allows a step-by-step diag-
nosis, using the characteristic morphological features
observed in the microscope, leading to a final diag-
nosis. This categorization does not follow the tradi-
tional pathology criteria leading to the classification
presented in Table 2; however, in combination with
the results of the macroscopic and radiological in-
vestigation, the diagnosis is highly reliable.
As an example of one of the most important basic
reactions, proliferative changes are described and
discussed (see Table 3). Proliferative changes as a
characteristic trait of bone behavior are observed in
some metabolic diseases, in infectious bone diseases,
sometimes in circulatory disorders, in bone tumors
and tumor-like conditions, and in miscellaneous
other conditions, as well as in healing of bone after
fracture (cf. Table 2). Proliferative changes are
found in all parts of the skeleton and not only in long
bones and the skull. Another basic reaction of bone
behavior is represented by osteoclastic changes
which are observed in various groups of diseases
(e.g., inflammatory and tumorous diseases). Fur-
thermore, the porotic changes in the skull vault and
orbital roof that are frequently associated with a
marked thickening of the affected bone structure
and represent a morphological syndrome will be ex-
plained (see Table 4). To clarify how microscopic
diagnosis usually works in paleopathology, exam-
ples from some of those categories presented in
Tables 3 and 4 are given below. Finally, some
groups of morphological patterns (cf. Tables 3 and
4) as well as cases of various diseases (cf. Table 2)
are demonstrated, describing the most important
morphological features of macerated tissue at the
microlevel. Finally, there is technical information
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 123
TABLE 3. Proliferative reactions: a classification of characteristic morphological patterns, with relevant references (diagnoses using
light microscopy and thin-ground sections prepared from archaeological specimens)
Proliferative reactions (characterized by addition of new bone to external and endocranial surfaces)
A) External periosteal reactions (e.g., long bones, skull vault)
Hemorrhagic, i.e., in subperiosteal hematoma, e.g., caused by trauma (e.g., Schultz, 1987a); in scurvy (e.g., Schultz, 1986,
1988b; Schultz and Teschler-Nicola, 1987b,d). In contrast to inflammatory processes, changes due to hemorrhagic processes
are only found external to the original bone surface. The original bone substance is not affected by the pathological process.
Changes are expressed by
a) Small hemorrhage or peripheral region of large hemorrhage: thin layer in form of a slip-like cover of newly built bone,
b) Center of large hemorrhage: relatively short, bulky bone trabeculae showing extensive bridging. Rarely, in recidivation,
several layers can be developed.
Inflammatory, i.e., in nonspecific and specific periostitis, e.g., caused by unspecific osteitis or hematogenous osteomyelitis,
treponemal osteitis, or osteomyelitis (e.g., Schultz, 1986, 1988b; Schultz and Teschler-Nicola, 1987b,d). In contrast to
hemorrhagic processes, inflammatory processes always affect the bone surface and outer layer, and frequently also the deeper
structures of the original bone substance.
Changes are expressed by
a) Small area or extremely peripheral region of large area affected: thin layer in form of a slip-like cover of newly built bone,
b) Middle-sized or large area affected: relatively long and thin bone trabeculae which are mainly oriented slightly irregular in
parallel order. There is only slight bridging. Relatively frequently, several layers can be developed (recidivation). In this
case, there is extensive bridging, in particular just at the level of an episode.
Tumorous, i.e., as periostosis, e.g., caused by primary or secondary bone tumors (e.g., Schultz, 1986, 1993c). Tumorous
processes may affect the bone surface, and also in advanced stages the deeper structures of the original bone substance.
Changes are expressed by structures very similar to the inflammatory changes described before. However, as a rule, the
trabeculae show a more regular development.
Circulatory, i.e., as periostosis, e.g., caused by hypertrophic osteoarthropathy or Bamberger-Marie disease (e.g., Schultz,
1987a; Teschler-Nicola and Schultz, 1984). There are relatively thick secondary layers at original bone surfaces. Sometimes,
short and bulky trabeculae are developed, which are similar to changes observed in hemorrhagic processes. Vestiges of
recidivation in the form of stratified formations are frequently seen.
B) Endocranial meningeal reactions (skull vault and base)
Hemorrhagic, i.e., in epidural hematoma, e.g., caused by trauma; scurvy; or “pachymeningeosis haemorrhagica interna” (e.g.,
Carli-Thiele, 1996; Kreutz, 1997; Schultz, 1987a,b, 1990, 1993a). In contrast to inflammatory processes, changes due to
hemorrhagic processes are only found external to the original bone surface. The original bone substance of the internal
laminae can be affected by pressure atrophy due to the pathological process.
Changes are expressed by
a) Beginning stage of organization (remodeling): small, patch-like areas of narrow, branching blood-vessel impressions;
b) Slightly advanced stage of organization (remodeling): porotic plates which can become relatively thick (large hematoma),
covering the blood-vessel impressions mentioned before; or
c) More advanced stage of organization (remodeling): groups of tongue-like smooth plates which are separated by an
extensively net-like aggregation of small blood-vessel impressions.
These lesions are mainly situated in the digital impressions but can also spread over larger areas of the skull vault.
Inflammatory, i.e., in nonspecific (bacterial) and specific (tuberculous) meningitis, meningo-encephalitis, and pachymeningitis.
In contrast to hemorrhagic processes, inflammatory processes always affect the bone surface, and frequently also the deeper
structures of the original bone substance (particularly in tuberculous meningitis).
a) Relatively fresh, i.e., florid process:
1) In nonspecific (bacterial) and specific (tuberculous) meningitis, changes are expressed by smooth and flat plate-like
newly built bone formations, which are, as a rule, oriented tangentially to the endocranial surface. There are isolated
plates which can also be confluent as one layer. Several layers are possible (recidivation). These lesions are frequently
found in digital impressions but also spread over larger areas in an advanced stage (e.g., Carli-Thiele, 1996; Kreutz,
1997; Schultz, 1990, 1993a,b).
2) In specific (tuberculous) meningitis, changes are expressed as described before. However, additionally, particularly at
the skull base and the basal regions of the vault, there are small impressions, which can be isolated or grouped together
(e.g., Jankauskas and Schultz, 1999; Kreutz, 1997; Schultz, 1999a; Templin, 1993; Templin and Schultz, 1994).
b) Nonspecific and specific lesions: in more advanced organization stages, the contours become indistinct, and the plate-like
character will be lost by the remodeling process. In specific lesions only: the small impressions become organized, i.e., they
start to be filled by newly built bone formations (remodeling) (e.g., Schultz, 1999a; Templin, 1993).
Tumorous, e.g., in meningioma. Tumorous processes may affect the bone surface, and also in advanced stages the deeper
structures of the original bone substance.
Changes are expressed by irregular bulging of relatively dense newly built bone formations, with no typical trabecular growth.

dealing with the Figures demonstrating light mi-
croscopic results. The magnification indicated for
photomicrographs of thin-ground sections is calcu-
lated for 35-mm film.
Proliferative reactions
Proliferative (productive) reactions in bony tis-
sue can be best observed on the external and in-
ternal surfaces of bones. Thus, in this paper, se-
lected examples of these reactions are presented
in two different topographic areas of the human
skeleton: the periosteal, i.e., the external surface
of the shaft of long bones, and the meningeal, i.e.,
the endocranial surface of the skull. Of course,
there are also various other regions of the skeleton
where proliferative processes of the periosteum
can be observed, such as at the internal surfaces of
ribs (Fig. 7A), where pleurisy and empyema of the
costal pleura affect the periosteum. The suspicion
that these changes are in general a symptom of
tuberculosis (TB) of the lungs and even character-
istic of TB cannot be universally accepted, al-
though such changes can accompany a tubercu-
lous process (Pfeiffer, 1991; Wakely, 1991).
124 YEARBOOK OF PHYSICAL ANTHROPOLOGY
TABLE 4. Phenomenon of porotic hyperstosis: what
pathological processes can contribute to a morphological
syndrome (diagnoses using light microscopy and thin-ground
sections prepared from archaeological specimens)
Porotic hyperostosis (characterized by a thickened bone
structure and a porotic surface)
A) Skull vault
Inflammatory processes:
a) Inflammatory processes of the scalp
b) Periostitis of the external skull vault
c) Nonspecific and sometimes also specific osteitis and
osteomyelitis of the skull vault. The characteristic
changes of porotic hyperostosis can occur after healing.
As a rule, the thickening of the skull vault and the
porosity are not very well-pronounced.
Hemorrhagic processes:
a) Subperiosteal hematoma caused by trauma (e.g., birth),
relatively frequently seen in infants and children. In
infants, the changes can be relatively well-developed.
b) Subperiosteal hematoma caused by scurvy (see below),
frequently seen in infants and children. The changes
can be very well-pronounced and reach sometimes an
enormous size. Macroscopically, changes are very
similar to those found in cavernous hemangioma and
anemia.
Tumors and tumorous processes:
a) Cavernous hemangioma. This is a rare tumor.
Macroscopically, the changes are very similar to the
changes found in hemorrhagic (hematoma) and anemic
processes.
b) Meningioma. Not a very rare tumor. However, newly
built bone formations at the external skull surfaces
representing porotic hyperostosis are very rare.
Macroscopically, the changes are very similar to the
changes found in hemorrhagic (hematoma) and anemic
processes.
Dietary disorders:
a) Various kinds of anemia (see below), such as
nutritionally caused iron-deficiency anemia. The well-
known changes range from slight to extremely severe.
Macroscopically, the changes are very similar to the
changes found in hemorrhagic processes (hematoma)
and cavernous hemangioma.
b) Scurvy (see above), frequently seen in infants and
children. The changes due to hemorrhagic processes can
be very well-pronounced and sometimes reach an
enormous size. Macroscopically, the changes are very
similar to those found in anemia and cavernous
hemangioma.
c) Rickets, relatively rarely seen (depending on
geographical region and nutritional situation). As a rule,
the changes are very discrete, what means that a very
fine porosity can be well-pronounced. However, the
thickening is only slightly developed.
Genetic causes:
E.g., some kinds of anemia (see above), such as sickle-cell
anemia and thalassemia. The changes ranges from slight
to extremely severe. Macroscopically, the changes are very
similar to those found in hemorrhagic processes
(hematoma) and cavernous hemangioma.
Other causes:
E.g., other kinds of anemia that are not due to nutritional
stress, i.e., caused by parasites (e.g., worms, plasmodia).
B) Orbital roof
Porotic hyperostosis of the orbital roof is called cribra
orbitalia. In general, all kinds of diseases listed in A can be
responsible for this morphological phenomenon.
Additionally, some inflammatory diseases that are of no
importance for the development of porotic hyperostosis of
the skull vault but can result in cribra orbitalia are listed
here: inflammation of the frontal, maxillary, and ethmoidal
sinuses, inflammation of the lacrimal gland, and meningeal
reactions.
[Vol. 44, 2001
Periosteal reactions on long bones (see table 3).
On the surfaces of ancient long bones, newly built
bone formations, so-called bone appositions, can be
frequently observed by microscopic analysis. A wide
range of diseases can be responsible for such
changes, e.g., hematogenous osteomyelitis, trepone-
mal diseases, leprosy, tuberculosis, and even non-
specific periosteal reactions such as inflammatory
processes of the deep veins, primary and secondary
hypertrophic osteoarthropathy (Bamberger-Marie
disease; cf. Fig. 7F), soft-tissue and bone tumors
(e.g., Fig. 7E), scurvy, external trauma, and overly-
ing soft-tissue infections (e.g., Carli-Thiele, 1996;
Kreutz, 1997; Schultz, 1986, 1987a,b, 1990, 1993a,b,
2001a; Templin, 1993; Zink, 1999). Particularly in
subadults, periosteal reactions on long bones caused
by scurvy (cf. Fig. 7B) and inflammatory processes
(Fig. 7C,D) are relatively frequently seen, whereas
chronic heart-lung diseases (e.g., deformed heart)
are rare (Fig. 7F).
In principle, there are morphologically only four
groups of proliferative processes which can be ob-
served on the periosteal surfaces of long bones in
ground sections made from a macerated sample (cf.
Table 3). As a rule, these processes are accompanied
by newly built bone formations. Thus, the product of
hemorrhagic (i.e., subperiosteal hematoma) and in-
flammatory processes (i.e., periostitis), as well as of
a tumorous process, can be differentiated. The diag-
nosis of a periosteal bone formation due to circula-
tory problems (e.g., Bamberger-Marie disease) is dif-
ficult. The changes are relatively similar to what is
observed in hemorrhagic processes. However, the
new bone formations are relatively dense (cf. Fig. 7F).
An organized, remodeled subperiosteal hema-
toma, which can originate in scurvy, is characterized
by a newly built spongy bone formation that is
found, e.g., on the external surface of the bone shaft.
Thus, the external basic lamellae are still intact and
there are no evident changes in the compact bone
substance (Fig. 7B). The short bony trabeculae of
this subperiosteal formation are relatively coarse
and bulky, building, as a rule, short-bridged struc-
tures (Fig. 7B). Subperiosteal hematoma is rela-
tively frequently found after trauma in subadults
suffering from scurvy.
It is well-known that scurvy, particularly in
subadults, is accompanied by widespread subperios-
teal bleeding, which frequently can occur after slight
trauma or even without trauma. The vestiges of
such a hematoma can also be diagnosed in archaeo-
logical skeletal remains because of the characteristic
newly built bone formations. In dry bones, the main
features caused by chronic scurvy are subperiosteal
new bone formations representing mineralized hem-
orrhagic processes. Such alterations are frequently
found on the shaft of long bones, on the ectocranial
and also sometimes on the endocranial surface of the
skull vault, and in the jaw area. In subadults, all
these pathological changes are usually much better
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 125

Fig. 7. Vestiges of nonspecific periosteal reactions in postcranial skeleton. A: Cross section through rib of a 35– 49-year-old male
from Boğazkale (central Turkey), burial 61B/85, Early Byzantine period. Vestiges of pleurisy: a, original cortex of rib; b, fissural gap
between external bone surface and newly built bone formation (c), noxa-affected periosteum from pleura. Undecalcified thin-ground
section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator.
Magnification, ⫻25. B: Cross section through left fibula of 25–39-year-old, probable female from Pergamon (western Turkey), Late
Byzantine period. Vestiges of organized subperiosteal hematoma, which became built up to woven bone: a, original compact bone of
shaft; b, newly built bone formation. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using
a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. C: Cross section through tibia of 2– 4 -year-old child from
Bettingen (Switzerland), individual 2/K-2, Late Middle Ages. Vestiges of acute periostitis: a, original compact bone of shaft; b, newly
built bone formation. Up to time of death, no pathological changes occurred in compact bone substance. Undecalcified thin-ground
section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator.
Magnification, ⫻25. D: Cross section through right fibula of 35– 49-year-old male from Boğazkale (central Turkey), burial 37/83, Early
Byzantine period. Vestiges of chronic, relapsing periostitis (at least three wave-like processes) due to osteomyelitis: a, original compact
bone of the shaft; 1–3, vestiges of relapsing periostitis. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in
polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. E: Cross section through left clavicle of
adult female from Sayala (Egyptian Nubia), burial K-68/2, Coptic period. Metastasizing carcinoma. Relapsing tumor periostosis: a,
original compact bone of shaft; 1, 2, vestiges of relapsing periostosis. Undecalcified thin-ground section (50 ␮m), viewed through the
microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻100. F: Cross section through
left tibia of a young baby from Bettingen (Switzerland), burial 35/43. Periostosis caused by Bamberger-Marie disease: a, original
compact bone of shaft; b, fissural gap between external bone surface and newly built bone formation (c). Undecalcified thin-ground
section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator.
Magnification, ⫻25.
126 YEARBOOK OF PHYSICAL ANTHROPOLOGY
expressed because in this age group, bone metabo-
lism is more active.
Periostitis in all its appearances creates charac-
teristic changes that can be grouped into different
morphological pictures. As a rule, in a florid inflam-
matory process of the periosteum, the bone trabec-
ulae evidently have a different shape from those in a
hemorrhagic process as described above. The rela-
tively thin, often parallel trabeculae are radially
oriented to the bone surface (Fig. 7C). The basic
lamellae, if still in place because of their age depen-
dence, and the neighboring compact bone substance
are, as a rule, affected by the inflammatory process.
Only at the beginning of an inflammatory process,
and if it is caused by an external noxa, could the
basic lamellae and the compact bone substance
partly be more or less free of pathological changes
(Fig. 7C). In chronic periostitis, the periosteal reac-
tion is only one of the patho-morphological symp-
toms. In this stage of disease, there is not only
periostitis, but also osteitis (i.e., the inflammatory
process has affected the compact bone substance)
and osteomyelitis (i.e., the inflammatory process has
affected the medullary cavity). In hematogenous os-
teomyelitis, the process starts from the medullary
cavity and in the end reaches, as a rule, the perios-
teum. When a bone is affected by an inflammatory
process, its character will be altered macroscopically
and radiologically, e.g., becoming sclerotic, but it
will also start remodeling, and thus typical morpho-
logical features can be observed at the microlevel.
Organized (remodeled) structures produced during a
nonspecific inflammatory process by the periosteum
have a characteristic morphology. As a rule, the
periosteal products of nonspecific inflammatory pro-
cesses in ancient bones such as hematogenous osteo-
myelitis, or of specific inflammatory processes such
as treponemal diseases, bone tuberculosis, and lep-
rosy, look different upon microscopic examination
(e.g., Schultz, 1994b, 2001a; Schultz and Roberts,
2001; Schultz and Teschler-Nicola, 1987b). Thus,
microscopic differential diagnoses in inflammatory
diseases in archaeological remains can indeed be
successful.
Mainly in chronic osteomyelitis, the periosteal re-
action can recur. In ground sections, various perios-
teal formations observed at the same place on the
bone surface represent the wave-like progress of the
inflammatory process (Fig. 7D), which can charac-
terize a recidivation. Such changes will be found in
archaeological specimens relatively frequently in
hematogenous osteomyelitis, but sometimes also in
treponemal and lepromatous periostitis (e.g., Be-
itzke, 1934; Hackett, 1976; Schultz, 1986, 2001a;
Schultz and Roberts, 2001; Schultz and Teschler-
Nicola, 1987b).
Regarding treponemal diseases, Hackett (1976)
described the different stages of typical syphilitic
bone changes in the skull and long bones very ex-
actly. Unfortunately, bone lesions caused by syphilis
are frequently very similar to alterations caused by
[Vol. 44, 2001
nonspecific bone diseases, particularly in long bones.
Using polarized light in light microscopy, the inter-
nal bone structure, especially the arrangement of
collagenous fibers, is detected, and structures typi-
cally built up by different disease processes become
visible. Thus, the results of microscopic investiga-
tion provide, in combination with the results of the
macroscopic, radiological, and scanning-electron mi-
croscopic research, a reliable diagnosis. As men-
tioned above, there are special telltale signs at the
microlevel such as 1) polsters and 2) grenzstreifen,
which are obviously characteristic in treponemal
diseases. These are now considered in more detail.
Polsters are characteristic features at the micro-
scopic level (Fig. 8A,B) that are frequently found in
chronic treponemal diseases of the long bones
(Michaelis, 1930; Schultz, 1994b; Schultz and Te-
schler-Nicola, 1987b; Weber, 1927). They consist of
parallel lamellae arranged at the periosteal level in
the form of pillow-like newly built bone formations
demarcated by periosteal blood vessels developed
during the course of the inflammatory process (hy-
pervascularization). As the growth of this patholog-
ical superficial bone formation, as a rule, progresses
relatively slowly, the polsters show a regular and
relatively homogeneous structure. In contrast, in
hematogenous osteomyelitis, the periosteal newly
built bone formation is irregular and shows various
structures that are the result of relatively rapid
growth associated with a relatively high remodeling
rate. Particularly well-developed polsters are a good
indicator of treponemal diseases (Schultz, 1994b).
However, in lepromatous periostitis, polster-like
structures that are rudimentarily developed and rel-
atively flat (Fig. 8E,F) can also be observed (Blondi-
aux et al., 1993, 1994; Schultz and Roberts, 2001).
As a rule, a grenzstreifen or grenzlinie (Fig. 8C,D)
can be observed in chronic treponemal diseases
(Schultz, 1994b; Schultz and Teschler-Nicola, 1987b).
This is never found in hematogenous osteomyelitis
of the long bones (Schultz, 1994b; Schultz and
Teschler-Nicola, 1987b; Weber, 1927). At first sight,
the grenzstreifen and older unremodeled bone ma-
terial embedded by a nonspecific inflammatory pro-
cess are the same. However, the grenzstreifen is, as
a rule, a very fine line or a narrow, band-like struc-
ture that represents the original external surface of
the bone shaft (remains of external circumferential
lamellae) and newly built lamellae that originate
during the first infection of the periosteum due to
the pathological process, e.g., Periostitis syphilitica
(Weber, 1927). Thus, the grenzstreifen is conclu-
sively caused by the relatively slow transmigration
of a specific inflammatory process in the primary
periosteal region. Externally from the grenzstreifen,
the newly built bone formation is present as a solid
mass. However, in nonspecific inflammatory bone
disease, e.g., hematogenous osteomyelitis, the pro-
cess is very aggressive and grows rapidly. Therefore,
the destruction is extensive. While bone is rapidly
eaten away, new bone formation also builds up rap-
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 127

Fig. 8. Vestiges of periosteal reactions in shafts of long bones caused by venereal syphilis and leprosy. A: Cross section through
right tibia of adult individual (E-6) from Klosterneuburg (Lower Austria), Early Modern times. Vestiges of venereal syphilis in form
of small polsters: a, primary (older) newly built formation of pathologically changed bone; b, polster; c, secondary external surface of
bone shaft. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light. Magnification, ⫻25. B: Cross
section through right tibia of adult individual (E-6) from Klosterneuburg (Lower Austria), Early Modern times. Vestiges of venereal
syphilis in the form of pronounced polsters: a, primary (older) newly built formation of pathologically changed bone; b, polster; c,
secondary external surface of bone shaft. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light
using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. C: Cross section through left tibia of adult individual
(E-4) from Klosterneuburg (Lower Austria), Early Modern times. Vestiges of venereal syphilis representing Periostitis syphilitica: a,
area of original compact bone substance predominantly consisting of Haversian systems; b, newly bone formation built up by
periosteum; c, narrow grenzstreifen. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light. Magni-
fication, ⫻25. D: Cross section through left tibia of adult individual (E-4) from Klosterneuburg (Lower Austria), Early Modern times.
Vestiges of venereal syphilis representing Periostitis syphilitica: a, area of original compact bone substance predominantly consisting of
Haversian systems; b, newly bone formation built up by periosteum; c, well-developed grenzstreifen. Undecalcified thin-ground section (50
␮m), viewed through the microscope in polarized light. Magnification, ⫻25. E: Cross section through right tibia of adult individual from
Chichester (England), burial 202, Middle Ages. Vestiges of leprosy: a, area of original compact bone substance predominantly consisting of
Haversian systems; b, polster-like newly bone formation built up by periosteum. Undecalcified thin-ground section (50 ␮m), viewed through
the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. F: Cross section through
right tibia of adult individual from Chichester (England), burial 148, Middle Ages. Vestiges of leprosy: a, area of original compact bone
substance predominantly consisting of Haversian systems; b, newly bone formation built up by periosteum; c, grenzstreifen-like
structure represented by flat blood-vessel canals. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in
polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25.
128 YEARBOOK OF PHYSICAL ANTHROPOLOGY
idly. Therefore, large pieces of the old bone shaft can
still be in place but embedded in the newly built
bone formation. This structure is not a grenzstrei-
fen. Thus, a grenzstreifen can be a useful indicator
to diagnose chronic treponematoses by microscopy.
In chronic leprosy, no characteristic grenzstreifen
(Fig. 8F) can be observed (Schultz and Roberts,
2001). In contrast to the findings in leprosy, in trepo-
nemal diseases including endemic syphilis, there are
not only alterations in the subperiosteal bone, but
also osteoclastic changes in the endosteal bone and
the bony trabeculae of the medullary cavity, as well
as in the compact bone substance of the shafts of the
long bones affected (Kuhnen et al., 1999; Schultz,
1994b; Schultz and Roberts, 2001; Schultz and
Teschler-Nicola, 1987b). This means that the osteo-
lytic changes in the shafts of long bones correspond
to the findings described by Hackett (1976). There-
fore, the microscopist will not only see resorption
holes and corroded structures, such as incomplete
trabeculae, but also vestiges of an extensive remod-
eling process. The latter is, as a rule, not found to
this extent in hematogenous osteomyelitis.
The last group of periosteal newly built bone for-
mations is observed in tumorous diseases and in the
healing of bones after fracturing, processes involv-
ing the deep veins as well as primary and secondary
hypertrophic osteoarthropathy (cf. Fig. 7F). Since in
these processes the resulting structures are not pro-
duced by an inflammatory process, the term perios-
titis is, strictly speaking, incorrect. Such a process
should instead be called periostosis, because in
Latin terminology, the suffix “osis” characterizes a
noninflammatory process, and the suffix “itis” an
inflammatory process.
In general, a spindle-shaped enlargement of the
bone shaft is characteristic of various periosteal re-
actions, such as periostosis in bone tumors (cf. Fig.
7E), but also as periostitis in treponemal diseases
(e.g., Periostitis syphilitica). However, at the begin-
ning of a tumorous periosteal reaction, the lesions
usually resemble flat layers. The compact bone sub-
stance is not affected at this stage. At an advanced
stage, the external area of the newly built bone
formation is frequently structured in spicula and the
compact bone substance can be severely affected by
sclerotic or osteoclastic changes. As a rule, tumor
periostosis looks different (cf. Fig. 7E and cover-
photograph) from the product of an inflammatory
process (periostitis, cf. Fig. 7C,D).
The newly built bone induced by the periosteum
during the healing process following a fracture is
called callus. This kind of periosteal bone appears in
various shapes, because muscles inserting (area of
Sharpey’s fibers) close to the fracture line and the
affected periosteum influence its development. Sim-
ilar conditions of initiation and morphology are
found in the new periosteal bone formations ob-
served in processes of the deep veins as well as in
primary and secondary hypertrophic osteoarthropa-
[Vol. 44, 2001
thy. However, as a rule, the new periosteal bone is
more moderately developed.
Meningeal reactions on the endocranial lam-
ina of the skull (see table 3). On the endocranial
lamina of the skulls of subadults, vestiges of menin-
geal reactions are frequently observable (Carli-
Thiele, 1996; Kreutz, 1997; Schultz, 1987b, 1990,
1993a,b, 2001a; Schultz and Teschler-Nicola, 1987a;
Templin, 1993). Various kinds of meningeal dis-
eases, such as epidural hematoma, meningitis, and
meningo-encephalitis, produce characteristic ves-
tiges on the endocranial lamina of the skull bones.
Indeed, in every case in which newly built bone
formations are visible, the pathological process rep-
resents a pachymeningitis. In subadults, particu-
larly in babies and infants, the dura mater has the
properties of the periosteum and is able to react in a
similar way. Thus, the products of meningeal reac-
tions (cf. Fig. 10) can be differentiated by micro-
scopic investigation into hemorrhagic, inflamma-
tory, and mixed forms of meningeal disease
(hemorrhagic-inflammatory or inflammatory-hem-
orrhagic). As a rule, the internal lamina of the skull
bones is relatively rarely affected. However, in hem-
orrhagic processes and areas of the skull vault
affected by a relatively large focus of meningeal
inflammation, the characteristic impressions of
atypical blood vessels can occur. Frequently, symp-
toms of increased brain pressure induced by cerebro-
spinal fluid are observed. Furthermore, other men-
ingeal diseases can also be, as a rule, reliably
diagnosed, such as tuberculous meningitis (Lepto-
meningitis tuberculosa), subdural empyema, and
hemorrhagic and inflammatory processes of the si-
nuses of the dura mater (Schultz, 1987b, 1993a,
1999a).
The origin of an epidural hematoma is frequently
connected with trauma (cf. Campillo, 1977). In ba-
bies, infants, and young children, scurvy is also a
cause of a hemorrhagic process of the meninges. As
a characteristic example, the case of a 5–7-year-old
child from the early Byzantine cemetery of Boğaz-
kale, Central Anatolia, is presented (Figs. 9, 20G). A
small, plate-like newly built formation of porotic
character is situated at the bottom of the sulcus of
the sagittal sinus, at the opening of a small diploic
vein (cf. Schultz, 1987a). The microscopic analysis
reveals woven bone (Schultz, 1987b). Thus, the child
died probably only a few weeks after this process,
which could have been caused by trauma.
The majority of cases dealing with meningeal re-
actions are represented by a disease group of inter-
mingled hemorrhagic and inflammatory compo-
nents. Vestiges of this kind of meningeal disease are
usually characterized by fine, very short sinuous
blood vessel impressions and very small, flat,
stalked plates (Figs. 10, 20H). By examining thin-
ground sections that demonstrate the latter changes
responsible for an inflammatory process, polarized
light enables the paleohistopathologist to diagnose
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
Fig. 9. Endocranial face of frontal bone of 5–7-year-old child
from Boğazkale (central Turkey), burial 37/83, Early Byzantine
period. In the impression of the sagittal sulcus, there are porotic
plates (arrows) representing vestiges of a hemorrhage. One of the
plates (a) covers the opening of a blood-vessel canal (diploic vena).
Fig. 10. Endocranial face of right parietal bone of 3–5-year-
old child from Franzhausen (Lower Austria), burial 338, Early
Bronze Age. In digital impressions, there are small, flat, stalked
plates representing vestiges of an inflammatory process (menin-
gitis).
primitive or coarse-woven bone (Fig. 20H). Addition-
ally, scanning-electron microscopic investigation re-
veals the stage of organization, i.e., of remodeling,
which allows an estimate of healing at time of death
(Fig. 11A,B). However, the advancement of healing
can also be estimated by light microscopy, using
polarized light (Fig. 21A).
Vestiges of tuberculous meningitis are character-
ized not only by the changes described above, but
also by relatively small, granular impressions whose
diameter varies between 0.5–1.0 mm (Fig. 11C–F).
Microscopically, the lesions are very characteristic
and a reliable indicator of Leptomeningitis tubercu-
losa, because in polarized light, the intra vitam ori-
gin of these impressions can be easily differentiated
(Fig. 21B,C). It is striking that these lesions could
apparently be organized (remodeling) after a while
(Fig. 21C) if the child survived long enough. The
localization of these impressions, which are gener-
ally grouped in clusters, is very characteristic. They
129
are situated at the endocranial face of the base,
sometimes also at the lateral wall of the skull, espe-
cially in the middle and the posterior cranial fossa,
and occasionally also in the cerebral fossa of the
occipital bone (Schultz, 1999a; Templin, 1993; Tem-
plin and Schultz, 1994; Teschler-Nicola et al., 1994,
1996). These lesions are caused by pressure atrophy
of the tuberculars. They represent specific features
and are characteristic of this kind of tuberculous
disease. It is not correct to diagnose tuberculous
meningitis if only vestiges mainly characteristic of
nonspecific meningeal reactions (e.g., inflammatory-
hemorrhagic meningitis) are present.
Infant mortality in prehistoric and early historic
populations often reached 40 – 60% or even more.
Until recently, it was only possible to speculate on
the causes of this exceedingly high mortality rate.
Now, the results of a large project in paleopathologi-
cal research, using extensive microscopic investiga-
tions, demonstrated that inflammatory and hemor-
rhagic reactions of the meninges are among the most
important factors leading to death in infancy
(Schultz, 1993a). The role of meningeal disease in
the mortality of infants and children in prehistoric
and historic populations is frequently underesti-
mated.
The frequency of meningeal reactions in prehis-
toric and historic infant populations is striking (cf.
Schultz, 2001b). In the Early Bronze Age, frequen-
cies vary between 9 –22%. Thus, in northern Anato-
lia (Fig. 12), at İkiztepe, 11 of 117 children (9.4%)
show vestiges of meningeal reactions (Schultz, 1990,
1993a). In Central Europe, frequencies are similar
(Fig. 12). In Franzhausen-I, 22 of 99 children
(22.2%) suffered from meningeal diseases. And in
Gemeinlebarn-F, 2 of 20 children (10.0%), in Hain-
burg, 6 of 35 children (17.1%) (Schultz, 1988/1989,
1990, 1993a; Schultz and Schmidt-Schultz, 1999), in
Jelšovce, in the Nitra Culture, 5 of 43 children
(11.6%), and in the Aunjetitz Culture, 6 of 29 chil-
dren (20.7%) show vestiges of meningeal diseases
(Schultz, 2001b; Schultz and Schmidt-Schultz,
1999). However, in the Middle Ages in Central Eu-
rope and Anatolia (Fig. 12), the frequencies were
significantly higher. In Barbing, 11 of 22 children
(50.0%), and in Harting, 10 of 22 children (45.5%)
suffered from meningeal diseases (Schultz, 1993a).
In Straubing, 107 of 176 children (60.8%) (Kreutz,
1997), in Bettingen, 21 of 30 children (70%) (Temp-
lin, 1993), in Boğazkale, 16 of 64 children (25.0%)
(Schultz, 1993a), and in Pergamon-B, 19 of 31 chil-
dren (61.3%) demonstrate vestiges of meningeal re-
actions (Schultz and Schmidt-Schultz, 1995).
Although the sample size is not very large, there is
a trend to be seen in the evolution of meningeal
diseases. In Central Europe and Anatolia, this group
of diseases increased dramatically from the Bronze
Age to the Middle Ages, apparently caused by con-
tinuous population growth and the change in eco-
nomic and political situations.
130 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001

Fig. 11. Evidence of hemorrhagic and tuberculous diseases of meninges. A: Remains of hemorrhagic-inflammatory meningeal
reaction in a 5–9-year-old child. Relatively advanced organization stage. Alytus (Lithuania), Late Middle Ages—Early Modern times,
burial 593. Scanning-electron microscopic image. Bar, 200 ␮m. B: Remains of hemorrhagic-inflammatory meningeal reaction in
5–9-year-old child. Advanced organization stage. Alytus (Lithuania), Late Middle Ages—Early Modern times, burial 593. Scanning-
electron microscopic image. Bar, 200 ␮m. C: Group of granular impressions in endocranial lamina of skull of 9 –15-year-old child
caused by leptomeningitis tuberculosa. Alytus (Lithuania), Late Middle Ages—Early Modern times, burial 302. Scanning-electron
microscopic image. Bar, 200 ␮m. D: Group of granular impressions in endocranial lamina of skull of 22-year-old male caused by
leptomeningitis tuberculosa (individual 59). Weisbach-Collection, Vienna (Austria), end of 19th century (1877). In this case, tubercu-
losis was clinically diagnosed. Scanning-electron microscopic image. Bar, 1 mm. E: Granular impression in endocranial lamina of skull
of 22-year-old male caused by leptomeningitis tuberculosa (individual 59). Weisbach-Collection, Vienna (Austria), end of 19th century
(1877). In this case, tuberculosis was clinically diagnosed. Scanning-electron microscopic image. Bar, 200 ␮m. F: Granular impression
in endocranial lamina of skull of 22-year-old male caused by leptomeningitis tuberculosa (individual 59) Weisbach-Collection, Vienna
(Austria), end of 19th century (1877). In this case, tuberculosis was clinically diagnosed: a, granular impression caused by tubercular
(specific feature), with intra vitam origin proved by course of collagen fibers; b, product of inflammatory process of meninges
(nonspecific feature). Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject
red first order (quartz) as compensator. Magnification, ⫻25.
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 131

Fig. 12. Frequencies of meningeal reactions in prehistoric and historic subadult populations. Early Bronze Age: Franz, Franz-
hausen (Lower Austria); Gem, Gemeinlebarn-F (Lower Austria); Hainb, Hainburg (Lower Austria); Jel-N, Jelšovce-N (Slovakia); Jel-A,
Jelšovce-A (Slovakia); Ikiz, İkiztepe (Turkey). Middle Ages: Barb, Barbing (Lower Bavaria); Hart, Harting (Lower Bavaria); Strau,
Straubing (Lower Bavaria), Kreutz, 1997; Bett, Bettingen (Switzerland); Bog, Boğazkale (Turkey); Perg, Pergamon (Turkey); Indiv.,
complete sample size (diseased and nondiseased individuals).

Porotic hyperostosis of the skull vault and the
orbital roof: the problem of cribra cranii
externa and cribra orbitalia
Porotic hyperostosis of the skull vault (cribra cra-
nii externa) and the orbital roof (cribra orbitalia) is
relatively frequently seen in prehistoric infant
skulls all around the world. As a rule, these changes
are much more frequently seen in subadults than in
adults. Regarding differential diagnoses and the eti-
ology of diseases, we now know that porotic changes
on the external surface of the skull vault can be
associated with porotic changes on the orbital sur-
face of the eye socket. In the North American liter-
ature, many scientists agree with the idea that po-
rotic hyperostosis of the skull vault and the orbital
roof can be caused by anemia, especially by iron-
deficiency anemia (e.g., El-Najjar et al., 1976; Tay-
lor, 1985; Ubelaker, 1992). However, recent investi-
gations in the field of paleohistopathology yielded
the result (Schultz, 1993a) that these morphological
features can also be due to various other diseases
(see Table 4). Thus, inflammatory processes of the
skull bones, e.g., periostitis, osteitis, and osteomy-
elitis (Kreutz, 1997; Schultz, 1986, 1987b, 1990,
1993a; Schultz et al., 2001), as well as inflammatory
processes of the scalp (Schultz, 1993a), can produce
after healing a porotic external surface of the skull
vault, which is usually thickened. Causes of these
diseases could be local primary inflammatory pro-
cesses, frequently after head trauma, or secondarily,
a spread of inflammatory processes of the nasal cav-
ity, the paranasal sinuses, or the orbit. In these
cases, the primary focus can be detected by endo-
scopic investigation without difficulty. Hemorrhagic
processes on the external lamina, such as ectocra-
nial hematoma (Schultz and Merbs, 1995; Schultz et
al., 1998; Teegen and Schultz, 1999; Wadsworth,
1992), can also involve the external skull surface
when the vestiges of such a hemorrhage are remod-
eled and show a porotic nature. In these cases,
which are more frequently observed in subadults,
the skull vault is in general thicker than in healed
inflammatory processes. In babies, the most com-
mon cause of ectocranial hematoma is trauma (e.g.,
cephalhematoma, caused by birth). Subadults suf-
fering from scurvy generally show a higher fre-
quency of hemorrhagic processes. Additionally, other
diseases, such as tumors (e.g., hemangioma, menin-
gioma) or even rickets (e.g., Carli-Thiele, 1996;
Kreutz, 1997; Schultz, 1987b, 1993a; Schultz et al.,
1998, 2001; Teegen and Schultz, 1999), can be re-
sponsible for the morphological appearance of po-
rotic hyperostosis. Thus, the epidemiology of ancient
diseases with respect to the frequency of anemia,
scurvy, rickets, inflammatory processes of the skull,
and tumorous lesions must be reconsidered. In this
context, it should be remembered that the etiology of
these processes and their dependence on each other
are very important for a reliable reconstruction of
the state of health and disease and the physical
condition of people from ancient times (Schultz,
1982, 1996, 1999b).
It is important to keep in mind that porotic hyper-
ostosis of the skull vault and cribra orbitalia are not
characteristic of a specific disease, but rather they
represent a morphological feature. Therefore, a very
careful investigation of these alterations is of the
utmost importance in order to obtain reliable diag-
132 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
noses. Macroscopic and radiological investigation
alone are not sufficient, because the structures of
hyperostotic and porotic newly built bone formations
due to different diseases are really very similar in
their macroscopic morphology. Furthermore, it
should not be forgotten that sometimes a molecular
biological investigation is able to provide a special
diagnosis in the scope of anemic diseases (Faerman
et al., 2000a,b).
The phenomenon of porotic hyperostosis in
chronic anemia is characterized by two morphologi-
cal features that are usually seen at the same time
and reflect the development of the following changes:
1) thinning of the external lamina, which creates
porosity because the cancellous bone (diploë) be-
comes visible, and 2) enlargement of the cancellous
bone by radial growth of the bone trabeculae, which
reduces the external lamina by something like pres-
sure atrophy. During the early stages of this process,
only the external lamina becomes porotic (Fig. 16A),
and the growth of the diploë cannot be observed by
macroscopic analysis. To demonstrate the elucida-
tion of different stages in the development of porotic
hyperostosis caused by anemia (Schultz, 1982, 1986,
1993b), some line-drawings and selected micropho-
tographs are presented (Fig. 13). Characteristically,
such lesions are found in the skulls of subadults.
One of the five skulls described represents a recent
case; the other four skulls represent archaeological
cases.
A drawing of the normal anatomy of the skull
vault in cross section of an approximately 5-year-old Fig. 13. Line drawings true to original undecalcified ground
child from the Late Neolithic cemetery of Alburg- sections (sagittal or frontal sections), demonstrating development
Straubing/Lerchenheid (southern Germany, first of porotic hyperostosis in chronic anemia (stages 0 –3). Magnifi-
half of the 3rd millennium BC, culture of the cation, approximately ⫻1.75. A: Stage 0, skull vault of 5-year-old
child from Alburg-Straubing (southern Germany), Neolithic Age.
Schnurkeramik) is shown in Figure 13A (stage 0). No pathological changes. B: Stage 1, right parietal bone of a 121
Both the external and the internal lamina of the – 2-year-old infant from İkiztepe (northern Turkey), burial 190,
vault bone are in place, and the diploë has developed Early Bronze Age. Slightly porotic changes caused by onset of
as is normal in a child of this age. This case is of reduction of external lamina in right part of sample. Although the
special interest because this child suffered from ane- skull vault is relatively thick, there is no real thickening of vault
bones but a relatively slight enlargement of modules of red bone
mia (cf. Fig. 13D). However, the sample demon- marrow. C: Stage 2, skull vault of 2–3-year-old child from İkiz-
strated in Figure 13A was taken from the part of the tepe (northern Turkey), burial 246, Early Bronze Age. Slight to
skull vault where no vestiges of porotic hyperostosis moderate porosity in left part of sample (cf. Fig. 16A). Skull vault
could be observed. is only slightly thicker in affected regions. Diploic trabeculae
To illustrate the onset of anemia, the right pari- start to orient themselves in radial direction (left part of sample,
1 cf. Fig. 21E). D: Stage 3, skull vault of 5-year-old child from
etal bone of a 12 –2-year-old infant from the Early Alburg-Straubing (southern Germany), Neolithic Age (cf. Fig.
Bronze Age settlement of İkiztepe (northern Turkey, 13A). Advanced changes represented by coarsely porotic surface
first half of the 3rd millennium BC) is presented in due to complete disintegration of skull vault, which shows pro-
Figure 13B (stage 1). Macroscopically, the external nounced thickening in affected areas. Diploic trabeculae are sig-
nificantly oriented in a radial direction, causing so-called “hair-
surface of the skull vault demonstrates a slightly on-end” phenomenon. E: Transitional stage between stages 2–3,
porotic change (Fig. 16A). These changes are fre- parietal bone of recent child (age group Infant II) from collection
quently situated in the area close to the lambdoid of Department of Pathology, University of Göttingen. Surfaces
suture of the parietal bones or, less frequently, in are coarsely porotic and show some irregular, short clefts. Skull
the corresponding area of the occipital squama or vault is significantly thickened and shows vestiges of remodeling
process (middle and right part of sample). Hair-on-end phenom-
even in the region of the parietal eminence. It is enon is still visible. F: Well-developed stage 3, skull of 9 –12-year-
important to realize that the macroscopic morphol- old child from Santa Maria de Yamasee, Spanish Florida, Mission
ogy of these alterations is very similar in various Period, has an extremely thickened and coarsely porotic vault.
diseases, such as anemia, scurvy, rickets, inflamma- Changes are characterized by parallel, extremely long, and grac-
ile bone trabeculae, situated at right angles to original surface of
tory diseases (e.g., inflammatory processes of the external lamina of skull vault (extremely pronounced hair-on-end
scalp, periostitis, osteitis, or osteomyelitis of the phenomenon). No vestiges of bone remodeling.
skull vault), and rarely hemangioma. Microscopi-
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
cally, the thin-ground section (Fig. 13B) shows that
the external lamina is starting to be resorbed and
shows very few slightly enlarged secondary cavities,
which are situated at the level of the original exter-
nal lamina and become confluent with the primary
modules of the red bone marrow (⫽ diploic spaces),
which are, as a rule, also slightly enlarged in this
area. The skull vault is not thickened.
The next case, of a slightly more advanced stage,
is seen in Figure 13C (stage 2). This child also lived
at İkiztepe (northern Turkey, first half of the 3rd
millennium BC) and died at the age of 2–3 years.
Macroscopically, the porosity is more pronounced.
Thus, in contrast to the stage described above, there
is a slight to moderate porosity. As a rule, the lesions
spread over the same areas described above (stage
1). Frequently, however, the skull vault is only
slightly thicker in the affected regions. Again, the
macroscopic morphology of these alterations is very
similar in various diseases, such as anemia, scurvy,
rickets, inflammatory diseases (e.g., inflammatory
processes of the scalp, periostitis, osteitis, or osteo-
myelitis of the skull vault), and rarely hemangioma.
Microscopically (Figs. 13C, 21E), the external lam-
ina of the skull vault is disintegrated over a rela-
tively large area. The orientation and size of the
secondary cavities are regular. Between these cavi-
ties, there are secondarily built, relatively short and
bulky bone trabeculae that grow out of the primary
diploë, forming a characteristic pattern. In the af-
fected areas of the skull vault, the bone mainly
grows in the external half of the diploë, causing the
slight thickening of the skull bone.
The next example involves a different section
through the skull vault of the same 5-year-old child
from Alburg-Straubing/Lerchenheid described above
(cf. stage 0). Here, the characteristic changes of
stage 3 can be observed. The changes are expressed
by a pronounced thickening and a coarsely porotic
surface of the affected skull region, both of which are
found in the areas of the parietal and frontal emi-
nences, the lambdoid areas of the parietals, and the
upper part of the occipital squama. In the porotic
structure, there can also be a few irregular, short
clefts in the center of the hypertrophic regions,
which sometimes give the structure a star-like ap-
pearance. In general, the macroscopic alterations
characteristic of such an advanced stage of porotic
hyperostosis caused by anemia are very similar to
changes due to scurvy or occasionally hemangioma.
However, the alterations observed in advanced
stages of rickets and inflammatory diseases (e.g.,
inflammatory processes of the scalp, periostitis, os-
teitis, or osteomyelitis of the skull vault) are, as a
rule, different in their morphology. Thus, a reliable
diagnosis should not be very difficult. Microscopi-
cally (Fig. 13D), the external lamina is completely
disintegrated and the skull vault is significantly
thickened in the affected areas (compare with non-
affected areas in Fig. 13A). The trabeculae in the
external half of the diploë are relatively thick and
133
take on a parallel orientation, which is responsible
for their radial arrangement, producing the typical
“hair-on-end” phenomenon (cf. Steinbock, 1976).
These three stages of porotic hyperostosis in ane-
mia have been demonstrated in children (age group
Infans Ia, i.e., newborn–2-year-old) and a young
child (age group Infans Ib, i.e., 2– 6-year-old). How-
ever, in older children (age group Infans II, i.e.,
6 –14-year-old), the morphological structure of the
skull vault in hypertrophic areas looks slightly dif-
ferent due to age-dependent bone growth. Addition-
ally, the characteristic changes due to anemia that
represent hypertrophy, i.e., the growth of modules of
red bone marrow in the direction of the external
bone surface, can be secondarily remodeled. This is
illustrated by the example of a recent child (age
group Infans II) from the collection of the Depart-
ment of Pathology of the University of Göttingen
(Fig. 13E). Macroscopically, the skull vault is signif-
icantly thickened in the areas of skull eminences.
The surfaces are coarsely porotic and there are some
irregular, short clefts in the center of the hypertro-
phic regions. The microscopic illustration shows the
complete loss of the external lamina and relatively
gracile bone trabeculae that form a characteristic
pattern which is not so well-developed as in stage 3
(Fig. 13E; please note that this is a child of age group
Infans II; therefore, the skull vault is thicker than in
the cases presented in Fig. 13C,D). Thus, the char-
acteristic features of stages 2 and 3 are observable.
Therefore, this case represents a transition stage
(stage 2–3). However, in the periphery of the porotic
areas, vestiges of a remodeling process can be ob-
served (Fig. 13E), which represent a secondary
change in the bone structure of the vault and which
can be interpreted as the result of a kind of partly
local healing. Nevertheless, characteristic features
of the hair-on-end phenomenon are still observable.
The last case in this series again involves an ar-
chaeological specimen. The extremely thickened and
coarsely porotic skull vault of a 9 –12-year-old child
from Santa Maria de Yamasee, Spanish Florida
(Mission Period), indicates a more or less regularly
porotic surface which touches the left and extends
slightly over the right temporal line (Schultz et al.,
2001). Microscopic investigation of a sample taken
from the skull vault demonstrates that the newly
built bone formation is characterized by parallel,
relatively long, and gracile bone trabeculae situated
at right angles to the original surface of the external
lamina of the skull vault (Fig. 13F). These trabecu-
lae are extremely enlarged in the vertical plane and
are responsible for the hair-on-end phenomenon.
The region of the original diploë shows a more or less
normal morphology. Thus, this case represents
stage 3 (please note that this is a child of age group
Infants II; therefore, the skull vault is thicker than
in the cases presented in Fig. 13D). There are no
vestiges of bone remodeling such as in the case pre-
viously described (Fig. 13E). This case thus repre-
134 YEARBOOK OF PHYSICAL ANTHROPOLOGY
Fig. 14. Line drawings true to original undecalcified ground
sections (sagittal or frontal sections), demonstrating development
of porotic hyperostosis in scurvy, rickets, and osteomyelitis. A and
C, magnification approximately ⫻3.5. B, magnification approxi-
mately ⫻5. A: Frontal bone of child from pre-Columbian Sun-
down Site, burial 3 (also see Fig. 15A,B). Large, ossified subperi-
osteal hematoma on external skull surface due to scurvy. Newly
built bone formations, seen as horizontal layers, are situated on
external lamina, which is still in place. Diploë is not affected (cf.
Fig. 15B). B: Fragment of parietal bone of newborn–3-month-old
infant from İkiztepe (northern Turkey), burial 53, Early Bronze
Age (Fig. 15C,D). Completely changed skull bone due to rickets:
external lamina is built up of squamous plates, spongy substance
is completely irregular, and internal lamina is splintered (cf. Fig.
15D). C: Vault fragment of 6 –12-month-old infant from pre-Co-
lumbian Sundown Site, burial 12, (cf. Figs. 15E,F, 21D). Skull
vault was severely destroyed by nonspecific osteomyelitis. Peri-
ostitis on ectocranial and endocranial surfaces caused new bone
formations represented by gracile, more or less irregularly ori-
ented bone trabeculae that branch frequently. Most of the diploic
trabeculae were eaten away by inflammatory process (cf. Figs.
15F, 21D).
sents one of the very rare cases of extremely pro-
nounced florid chronic anemia.
For comparative purposes, a characteristic case of
an ectocranial subperiosteal hematoma due to
chronic scurvy is demonstrated. The skull vault of a
child from the pre-Columbian Sundown Site, Ari-
zona, USA, macroscopically shows the phenomenon
of pronounced porotic hyperostosis (Figs. 14A, 15A).
Therefore, anemia is a reasonable tentative diagno-
sis. However, microscopic examination reveals fea-
tures (Fig. 15B) that clearly demonstrate that the
changes are due to a hemorrhage that was first
organized from a hematoma to fibrous connective
tissue and then built up to woven bone. For differ-
ential diagnoses, it is very important to be aware
that a subperiosteal hematoma is situated on the
original bone surface without affecting the external
lamina (see proliferative reactions, above) and that
the diploë has a normal structure (Fig. 15B). Fur-
thermore, as a rule, a typical hair-on-end phenome-
non, as pronounced as in long-existent chronic ane-
mia, is not seen in a subperiosteal hematoma of the
skull bones. However, in relatively slightly devel-
oped cases, porotic hyperostosis in scurvy and ane-
[Vol. 44, 2001
mia are very similar. Here, the criteria described
above (structures dealing with the morphology of
the external lamina and diploë) help to establish the
correct diagnosis. As chronic vitamin C-deficiency is
the most frequent cause of subperiosteal hematoma
in subadults, the reliable diagnosis is scurvy (for
additional criteria, see Schultz, 1988/1989, 1990;
Schultz and Schmidt-Schultz, 1995; Schultz et al.,
1998).
As mentioned above, chronic rickets is also able to
produce porotic hyperostosis. A typical case is briefly
demonstrated. The skull of a newborn–3-month-old
infant macroscopically presents a porotic vault,
which is only slightly enlarged (Figs. 14B, 15C). The
results of microscopic investigation suggest rickets
and clearly exclude anemia, scurvy, and an inflam-
matory process (Fig. 15D).
Additionally, a case of osteomyelitis of the skull
vault is presented for comparative purposes. The
skull of a young infant from the pre-Columbian Sun-
down Site (Arizona) shows enormous bone apposi-
tion on its external surfaces (Figs. 14C, 15E). Micro-
scopically, all features support the diagnosis, of
osteomyelitis of the skull vault (Figs. 15F, 21D).
Finally, the difficulty in diagnosing porotic changes
of the external surfaces of the skull vault is demon-
strated. Figure 16 shows porotic changes which are
due to intra vitam processes (differential diagnosis,
postmortem destruction). Macroscopically, no reli-
able diagnosis is possible. However, microscopically
the correct diagnosis is easy to obtain. The 2–3-year-
old child from burial 246 of the İkiztepe cemetery
(Fig. 16A; cf. Fig. 13C) suffered from anemia (Fig.
21E), while the 6 –12-month-old infant from burial
78 of the same cemetery (Fig. 16B) suffered from
osteomyelitis of the skull vault (Fig. 21F). The case
is also very interesting because this inflammatory
process of the skull vault was accompanied by a
hemorrhagic-inflammatory process of the meninges
(Fig. 21F).
All that has been described above for porotic
changes of the skull vault can also be observed in a
very similar way in the orbital roof. As a rule, only
histological examination produces reliable results
(Schultz, 1987b, 1993a,b; Schultz et al., 2001;
Wapler, 1998; Wapler and Schultz, 1997). This may
sometimes be difficult to accept for the paleopatholo-
gist working macroscopically, but the macroscopic
study of the external morphology of porotic orbital
roofs will only rarely lead to a reliable diagnosis.
Thus, if microscopic analysis is not carried out, pa-
leopathologists should restrict their assessment to
stress indicators if studying porotic hyperostosis of
the skull vault and the orbital roof, and not try to
diagnose specific diseases, such as iron-deficiency
anemia (Schultz, 1993b; Schultz et al., 2001).
Here, as characteristic examples, two cases of po-
rotic hyperostosis of the orbital roof are described.
The porotic and thickened orbital roof of a 9 –12-
year-old child from Santa Maria de Yamasee (Flor-
ida), shows, in a thin-ground section, the classic
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 135

Fig. 15. Porotic hyperostosis caused by different diseases. A: External view of right frontal bone of child from pre-Columbian
Sundown Site who suffered from external subperiosteal hematoma caused by scurvy, burial 3 (Fig. 14A). B: Sagittal section through
fragment of right frontal bone of child described in A: a, external lamina; b, newly built formation (“bone apposition”) on external
lamina; c, diploë. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red
first order (quartz) as compensator. Magnification, ⫻25. C: External view of fragment of parietal bone of newborn–3-month-old infant
from İkiztepe (northern Turkey) who suffered from rickets, burial 53, Early Bronze Age (Fig. 14B). D: Sagittal section through
fragment of right frontal bone of infant described in C. Completely changed microstructure. External and internal lamellae are
splintered, and modules of red bone marrow are irregularly shaped: a, external lamina; b, diploë; c, internal lamina. Undecalcified
thin-ground section (50 ␮m), viewed through the microscope in plane light. Magnification, ⫻25. E: External view of left frontal bone
of 6 –12-month-old infant from pre-Columbian Sundown Site, burial 12, who suffered from osteomyelitis of skull vault (cf. Fig. 14C).
F: Sagittal section through fragment of left frontal bone of infant described in E. Very severe inflammatory reactions: a, external
lamina; b, diploë, partly eaten away by osteoclastic reactions; c, internal lamina; d, new bone formation (“bone apposition”) on external
lamina; e, new bone formation (“bone apposition”) on internal lamina. Undecalcified thin-ground section (50 ␮m), viewed through the
microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25 (cf. Fig. 21D).
136 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001

Fig. 16. Differential diagnosis in porotic skull bones. A: Fragment of parietal bone of 2–3-year-old child from İkiztepe (northern
Turkey), burial 246, Early Bronze Age. Porotic surface due to anemia. B: Fragment of frontal bone of 6 –12-month-old infant from
İkiztepe (northern Turkey), burial 78, Early Bronze Age. Surface is porotic due to inflammatory process (osteomyelitis).

Fig. 17. Frequencies of anemia in Bronze Age subadult populations diagnosed in skull vault. Franzh-I, Franzhausen-I (Lower
Austria); Gemeinl-F, Gemeinlebarn-F (Lower Austria); Hainburg, Hainburg (Lower Austria); Jelsovce-N, Jelšovce-N (Slovakia);
Jelsovce-A, Jelšovce-A (Slovakia); Ikiztepe, İkiztepe (Turkey).

features of hypertrophy of the red bone marrow. The
modules of red bone marrow are longitudinally en-
larged, the bone trabeculae are oriented parallel
(i.e., the hair-on-end phenomenon), and the orbital
lamina has, intra vitam, been completely reduced
(Fig. 21G). The other case represents a 4 – 6-year-old
child who lived in the early Middle Ages at Hailfin-
gen (southern Germany). In this case, the orbital
roof is only slightly thickened, but has a porotic
surface. These features were produced by a hemor-
rhage, but may also have been due to a hemorrhagic-
inflammatory process in the orbit that created new
bone formation (Fig. 21H), similar to the process
already described above for the proliferative reac-
tions on the surfaces of long bones.
Some practical applications are now presented,
demonstrating the advantage of reliable diagnoses
based on microscopic techniques. There are various
reasons why subadults suffered from anemia. The
most frequent etiologies are parasitic disease (e.g.,
Reinhard, 1992; Larsen and Sering, 2000), chronic
iron deficiency, such as caused by iron-poor diets
(e.g., El-Najjar et al., 1976), thalassemia (e.g., As-
cenzi et al., 1991), or chronic malnutrition, such as
chronic deficiency of the amino acid tryptophan
(Schultz, 1982). More detailed information is given
by Garn (1992).
In prehistoric subadults, different frequencies of
anemia have been documented. For instance, from
the Neolithic Age, in the population from Wan-
dersleben (central Germany), belonging to the cul-
ture of the Bandkeramik (corded ware) who were the
earliest agriculturists in Central Europe, anemia
was observed in 13 of 30 children (43.3%; Fig. 17),
diagnosed by examining the skull vaults and orbital
roofs (Carli-Thiele, 1996).
M. Schultz] PALEOHISTOPATHOLOGY OF BONE
Fig. 18. Frequencies of scurvy in prehistoric and early historic subadult populations diagnosed in the skeleton. Franzh-I,
Franzhausen-I (Lower Austria); Hainburg, Hainburg (Lower Austria); Jelsovce-N⫹A, Jelšovce-N and Jelšovce-A (Slovakia); Ikiztepe,
İkiztepe (Turkey); Straubing (Kreutz, 1997), Straubing (Lower Bavaria).
In the Early Bronze Age of Central Europe, the
frequencies of anemia were relatively different (Fig.
17). Thus, in the valley of the River Traisen (Lower
Austria), from the sites of Franzhausen-I and Ge-
meinlebarn-F, as well as from Hainburg, no convinc-
ing case of anemia could be diagnosed, taking skull
vaults and orbital roofs into account (Schultz, 1993a,
2001b; Schultz and Schmidt-Schultz, 1999). How-
ever, at Early Bronze Age Jelšovce (Slovakia), which
is only approximately 200 km northeast of the
Traisental, anemia was present. At this site, two
different cultural traditions could be proved by the
archaeological findings. In the Nitra Culture, only 8
of 47 children (17%), and in the Aunjetitz Culture,
12 of 31 children (38.7%) suffered from anemia
(Schultz et al., 1998; Schultz and Schmidt-Schultz,
1999). From the Early Bronze Age settlement of
İkiztepe (northern Turkey), 6 of 129 children (4.7%)
suffered from anemia diagnosed in the skull vault
(Schultz, 1990, 1993a, 2001b; Schultz and Schmidt-
Schultz, 1999). The cause for the cases of anemia in
the population from İkiztepe was probably malaria,
which was endemic in this geographical area since
at least the Early Bronze Age (Schultz, 1990, 1993a,
2001b,c; Schultz and Schmidt-Schultz, 1999; cf. An-
gel, 1966, 1978).
Chronic vitamin C deficiency (scurvy) is an impor-
tant factor contributing to morbidity and mortality
in prehistoric populations (e.g., Aufderheide and Ro-
drı́guez-Martı́n, 1998; Holck, 1984; Maat, 1982; Ort-
ner and Putschar, 1981; Steinbock, 1976). There is a
close connection between scurvy and other diseases,
such as posthemorrhagic anemia. Scurvy is also able
to create immunodeficiency, and infectious diseases
are often seen in association with scurvy. With re-
gard to nutrition, prehistoric populations were
137
strongly dependent on their environment. In Neo-
lithic times, subsistence was mainly based on agri-
culture. Cereals such as corn or wheat provide no
vitamin C, and fruits and vegetables were available
only at certain times of the year. During winters, an
adequate supply of fresh food was probably difficult.
Thus, a seasonal deficiency of vitamin C must be
considered. In Neolithic populations from Central
Europe (Fig. 18), vestiges of chronic scurvy were
observed, with a maximum of 14 of 35 children
(40.0%) (Carli-Thiele, 1996; Carli-Thiele and Schultz,
1999). In adults, the frequency was lower. In
subadult populations of the Early Bronze Age from
Central Europe and northern Anatolia (Fig. 18), fre-
quencies were found to range between 0.0 –21.4%. In
Franzhausen-I, 7 of 110 children (6.4%), in Hain-
burg, none of 38 children (0.0%), in Jelšovce, of the
Nitra and Aunjetitz Culture, 15 of 89 children
(16.9%), and in İkiztepe, 17 of 123 (13.8%) suffered
from chronic scurvy (Schultz, 1990, 2001b,c; Schultz
et al., 1998; Schultz and Schmidt-Schultz, 1999).
Obviously, in the Middle Ages (Fig. 18), the nutri-
tional situation became worse, as an example from
Straubing (southern Germany) demonstrates. In
this Germanic population, 57 of 159 subadults
(35.8%) show vestiges of chronic scurvy (Kreutz,
1997).
PSEUDOPATHOLOGY
Now that we have discussed examples of specific
morphological features characteristic of particular
diseases and some basic bone reactions with which
we can elucidate the mechanisms of bone behavior
during pathological processes, an understanding of
pseudopathological changes may be much easier. We
have briefly discussed pseudopathology in terms of
138 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001

Fig. 19. Pseudopathology. A: Internal view of left part of mandibula of 8 –10-year-old child from İkiztepe (northern Turkey), Early
Bronze Age, burial 199. Mandibular surface is covered by porotic bone apposition (arrows) which appears to be the product of an
inflammatory process. B: Same specimen as in A. Cross section through body of mandible (a) and “bone apposition” (b, c). Microscopic
view demonstrates that small bone trabeculae (b) did not develop in this area but consists of other very small fragments of skull,
probably from the visceral cranium, and were sintered postmortem at internal face of mandibula (c: postmortem crystals), simulating
periostitis. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in plane light. Magnification, ⫻25. C: Endocra-
nial surface of skull fragment of adult female from Lentia (Upper Austria), Roman period. Coarse porotic surface seems to be due to
postmortem soil erosion (diagenesis). D: Same specimen as in C. Small holes were not caused by diagenesis but by a metastasizing
carcinoma (osteoclasia) simulating pseudopathology. Scanning-electron microscopic image. Bar, 500 ␮m.

Fig. 20. Diagnosing ancient bones by light microscopy. A: Section through fragment of skull vault. Metastasizing carcinoma. Sayala
(Egyptian Nubia), Coptic period, individual K-68/2, adult female. Masses of Howship’s lacunae (arrows). Undecalcified thin-ground
section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator.
Magnification, ⫻25. B: Cross section through compact bone substance of femur. Manching (southern Germany), Iron Age, Celtic, adult
individual 1959/73. Haversian systems (osteons). Bone relatively well-preserved, secondarily, by protection due to manganese ions
causing yellowish staining. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a
hilfsobject red first order (quartz) as compensator. Magnification, ⫻100. C: Cross section through femur of Alamannic warrior from
Mertingen (southern Germany), Early Middle Ages. Remarkably good preservation (a), particularly caused by iron ions. External
narrow zone (b) was first slightly affected by diagenesis. Later, during the disintegration process of an iron sword, the bone shaft was
coated with iron-oxide which permanently preserved the bone. Undecalcified thin-ground section (50 ␮m), viewed through the
microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻100. D: Cross section through
compact bone substance of long bone fragment of Kelsterbach mammoth (central Germany). Cancellous bone of metaphysis excellently
preserved. In modules of red bone marrow, there are small crystals from sand of the bank of the River Main. Undecalcified thin-ground
section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator.
Magnification, ⫻25. E: Cross section through compact bone substance of long bone fragment from Tetelpan (Mexico), Preclassic period.
Vestiges of growth of fungus (bohrkanäle). Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light
using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻160. F: Cross section through fragment of skull vault from
adult individual from Maysar (Oman), Bronze-Iron Age. Blood vessel canal in diploë burst by postmortem crystal growth (arrows),
probably brushit. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject red
first order (quartz) as compensator. Magnification, ⫻200. G: Transverse section through frontal bone of 5–7-year-old child from
Boğazkale (central Turkey), Early Byzantine period, burial 1/83. Ossified vestige of small epidural hematoma, consisting of woven bone
(arrows) at bottom of sagittal sinus at opening of a diploic vena (Fig. 9), internal lamina (a). Undecalcified thin-ground section (50 ␮m),
viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. H:
Sagittal section through frontal bone of 2–3-year-old child from İkiztepe (northern Turkey), Early Bronze Age, burial 145. Internal
lamina and diploë (a) are intact. Endocranial, ribbon-like skull bone consists of woven bone (b). Small ossified plates (woven bone) are
product of an inflammatory meningeal reaction (c). Undecalcified thin-ground section (50 ␮m), viewed through the microscope in
polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25.
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 139

Fig. 20.
140 YEARBOOK OF PHYSICAL ANTHROPOLOGY
decomposition and diagenesis (see above). Since we
have now described the mechanisms of intra vitam
proliferative reactions, we can easily differentiate
between these lesions and postmortem changes that
simulate pathological alterations. The term “pseu-
dopathology” was introduced to paleopathology by
Wells (1967). In general, it is not easy to differenti-
ate macroscopically between the vestiges of diseases
and postmortem changes in archaeological bones,
especially when the skeletal remains are only poorly
preserved (Schultz, 1986, 1997b). Additionally, the
histopathological analysis of poorly preserved bones
can create serious problems in disease diagnosis.
The causes were mentioned above, particularly dur-
ing the process of diagenesis where the resulting
structures simulate intra vitam changes. The char-
acteristic case of an 8 –10-year-old child buried at
the Early Bronze Age cemetery from İkiztepe, north-
ern Turkey, is presented. The lingual face of the left
part of the mandible of this child displays a newly
built bone formation that appears to be a periosteal
reaction due to an inflammatory process (Fig. 19A).
However, microscopic analysis in polarized light
(Fig. 19B) reveals a postmortem apposition which
consists of broken bone trabeculae, probably from
the visceral cranium, which had been agglomerated
by the buildup of secondary crystals (cf. Fig. 20F) at
the lingual surface of the mandible.
Occasionally, traces are observed which, at first
sight, macroscopically appear to be caused by post-
mortem erosion (Fig. 19C), and which only after
[Vol. 44, 2001
microscopic study can be recognized as vestiges of
intra vitam processes, such as vestiges of metasta-
sizing carcinoma (Fig. 19D). In such a case, the
eroded structures suggestive of postmortem changes
can be diagnosed as the result of osteoclastic resorp-
tion by scanning-electron microscopic analysis and
light-microscopic examination of thin-ground sections.
These typical features of intra vitam resorption are
characterized by masses of Howship’s lacunae on bone
surfaces, the irregular shape of bone trabeculae, and
the margins and edges of resorption holes, where os-
teoclasts have eaten away the bony substance.
CONCLUSIONS
In the interdisciplinary field of paleopathology,
not only macroscopic, radiological, and endoscopic
methods are required, but microscopy is also needed.
In this paper, the effect and usefulness of micro-
scopic study of skeletal remains in paleopathology
and its implication for the causes (etiology), but es-
pecially for the frequencies and the spread of se-
lected diseases (epidemiology) during the Neolithic
Age, the Bronze Age, and the Middle Ages in Central
Europe and Anatolia, are underlined by specific ex-
amples, such as anemia, scurvy, and meningeal re-
actions. Selected examples of mechanisms of patho-
logical bone changes have been presented, dealing
mainly with proliferative reactions in the periosteal
area of long bones, the meningeal reactions of the
endocranial surface of the skull, and porotic hyper-
ostosis of the skull vault and corresponding changes

Fig. 21. Diagnosing ancient bones by light microscopy. A: Sagittal section through occipital bone of 12–18-year-old individual from
Stillfried (Lower Austria), Late Bronze Age. Diploë (a) and internal lamina (b) are intact. New bone formation (c) on endocranial
lamina as a result of hemorrhagic-inflammatory meningeal reaction. Structures are well-organized, i.e., healing stage (partly woven,
partly already lamellar bone). Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a
hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. B: Sagittal section through skull vault of 22-year-old male
(individual 59). Weisbach-Collection, Vienna (Austria), end of 19th century (1877). In this case, tuberculosis was clinically diagnosed
(cf. Fig. 11D–F). Small granular impression caused by pressure atrophy of a tubercule (a). Undecalcified thin-ground section (50 ␮m),
viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. C:
Sagittal section through frontal bone of a 6 –10-year-old child from Bettingen (Switzerland), individual 20/76-1, Late Middle Ages.
Leptomeningitis tuberculosa. Small granular impression caused by pressure atrophy of a tubercule. Wall of intra vitam-originated
impression (a). Impression is in stage of remodeling (healing process not finished because child died), which took place in two different
episodes: first episode (b) followed by second (c). Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized
light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. D: Sagittal section through skull vault of
6 –12-month-old infant from pre-Columbian Sundown Site, burial 12 (cf. Figs. 14C, 15E,F). Severe nonspecific osteomyelitis of skull
vault accompanied by periostitis. On external lamina (a) there are new bone formations (d). On internal lamina (c), there are extremely
well-developed bone formations (e). Diploë is almost completely lysed (b). Undecalcified thin-ground section (50 ␮m), viewed through
the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. E: Sagittal section
through skull vault of a 2–3-year-old child from İkiztepe (northern Turkey), burial 246, Early Bronze Age (Figs. 13C, 16A). Anemia,
stage 2. Internal lamina (a) and diploë (b) are not affected. External lamina is completely disintegrated. External trabeculae of diploë
(c) lie at right angles to internal lamella (onset of hair-on-end phenomenon). Undecalcified thin-ground section (50 ␮m), viewed
through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. F: Sagittal
section through fragment of parietal bone of 6 –12-month-old infant from İkiztepe (northern Turkey), burial 78, Early Bronze Age (cf.
Fig. 16B). Nonspecific osteomyelitis of skull vault: a, external lamina, partly destroyed (porotic); b, diploë, in disintegration due to
osteoclasia; c, internal lamina, partly reduced; d, newly built bone formation due to hemorrhagic-inflammatory process of meninges
caused by osteomyelitis. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a
hilfsobject red first order (quartz) as compensator. Magnification, ⫻25. G: Sagittal section through right orbital roof of 9 –12-year-old
child from Santa Maria de Yamasee (Florida), Early Spanish period, burial 106. Porotic hyperostosis of orbital roof caused by chronic
anemia (cribra orbitalia II/III). Parallel bone trabeculae presenting hair-on-end phenomenon (arrows). In modules of red bone marrow,
small sand crystals. Undecalcified thin-ground section (50 ␮m), viewed through the microscope in polarized light using a hilfsobject
red first order (quartz) as compensator. Magnification, ⫻25. H: Sagittal section through right orbital roof of 4 – 6-year-old child from
Hailfingen (southern Germany), Early Middle Ages, Alamannic, burial 2190. Porotic orbital roof caused by hemorrhagic or hemor-
rhagic-inflammatory process. On original lamellae of orbital roof (a), diploic trabeculae (c) which are covered by a secondary layer (b)
are found. Only macroscopically does the morphology simulate porotic hyperostosis due to anemia. Undecalcified thin-ground section
(50 ␮m), viewed through the microscope in polarized light using a hilfsobject red first order (quartz) as compensator. Magnification,
⫻25.
M. Schultz] PALEOHISTOPATHOLOGY OF BONE 141

Fig. 21.
142 YEARBOOK OF PHYSICAL ANTHROPOLOGY
on the orbital roof (cribra orbitalia). It was shown
that the histological examination of archaeological
skeletal remains provides improved reliability in the
establishment of diagnoses. The patterning of archi-
tectural changes in the cortical, compact, and
spongy bone substances, particularly in newly built
bone formations, is an efficient key in attempting to
diagnosis. Therefore, special categorizations were
developed to make the process of diagnosis easier.
Thus, we have morphological features at the mic-
rolevel, such as faserfilz-osteons (in slowly growing
primary osteoblastic bone tumors), grenzstreifen,
and polsters (in chronic treponemal diseases and
apparently also in chronic leprosy in only a slight
modification), which are important indicators of par-
ticular diseases or groups of diseases. Furthermore,
there is evidence of basic bone reactions that char-
acterize bone behavior also at the microlevel, such
as proliferative (productive, osteoblastic) and osteo-
lytic (osteoclastic) reactions. Finally, we can observe
morphological symptoms (e.g., thinning or thicken-
ing of the external lamellae of the skull vault, en-
largement of the diploë), which can be grouped into
morphological syndromes, such as porotic hyperos-
tosis or cribra orbitalia. These syndromes do not
represent or characterize one particular disease, but
can be caused by various diseases.
The basis of any microscopic analysis of ancient
bones is a good working knowledge of the microscopic
structure of bone, including the histogenesis and
growth of bone, as well as the influences of decompo-
sition and diagenesis, which help to avoid false diag-
noses due to pseudopathology. The method of choice is
the study of dry bone samples by thin-ground sections.
To investigate thin-ground sections using plane or po-
larized transmission light, a special technique is re-
quired for embedding the usually brittle and some-
times poorly preserved bone samples. Additionally, the
production of thin-ground sections must be efficient.
For these purposes, special techniques have been de-
veloped (Schultz, 1988; Schultz and Drommer, 1983).
However, not only suitable techniques, but also expe-
rience and a collection for comparative purposes, are
necessary to establish reliable diagnoses. False diag-
noses can be avoided that could easily be caused by
postmortem changes such as those due to diagenesis.
Additionally, microradiography and scanning-electron
microscopy are powerful tools for diagnosing ancient
bones.
It is important to know that it is possible to
establish general and differential diagnoses from
archaeological bone samples by microscopic study,
even though soft tissues and cells, which are the
most important features in recent pathology, are
not present. The etiology and epidemiology of an-
cient diseases require reliable diagnoses as the
basis of further research. The paleohistopathologi-
cal investigation of archaeological skeletal re-
mains should be part of the arsenal of every pa-
leopathologist.
[Vol. 44, 2001
ACKNOWLEDGMENTS
The author thanks Michael Brandt and Ingrid
Hettwer-Steeger (Department of Anatomy, Univer-
sity of Göttingen, Göttingen, Germany) for prepar-
ing the ground sections, Ingrid Hettwer-Steeger for
preparing the samples for scanning-electron micros-
copy, Dr. Peter Schwartz (Department of Anatomy,
University of Göttingen) for taking some of the
SEM-photos (Fig. 6B,F,G,H), Prof. Dr. Dr. Harald
Kijewski (Department of Forensic Medicine, Univer-
sity of Göttingen), and Prof. Dr. Steffen Berg
(München) for analyzing the concentration of ele-
ments in compact bone samples by atomic absorp-
tion spectroscopic technique, Dr. Barbara Süss-
mann-Bertozzi (Göttingen) for a microphotograph
(Fig. 6E), Egbert von Bischoffshausen (Department
of Anatomy, University of Göttingen) for line draw-
ings, Sascha Dessi (Department of Anatomy, Uni-
versity of Göttingen) for computer work, and Cyrilla
Maelicke (Department of Histology, University of
Göttingen) for reading the English-language text.
Furthermore, the author thanks for bone samples
Dr. Jozef Bátora (Nitra, Slovakia), Prof. Dr. Önder
Bilgi (Istanbul, Turkey), Dr. Alfred Czarnetzki (Tü-
bingen, Germany), Dr. Marcella Frangipane (Rome,
Italy), Dr. Beatrix Gessler-Löhr (Heidelberg, Ger-
many), Prof. Dr. Bernd Herrmann (Göttingen, Ger-
many), Prof. Dr. Rimantas Jankauskas (Vilnius,
Lithuania), Dr. Bruno Kaufmann (Aesch, Switzer-
land), Prof. Dr. Manfred Korfmann (Tübingen, Ger-
many), Dr. Herbert Kritscher (Vienna, Austria),
Prof. Dr. Manfred Kunter (Giessen, Germany), Prof.
Dr. Ekkehard Kunze (Göttingen, Germany), Dr.
Günter Lange (Frankfurt am Main, Germany), Prof.
Dr. Clark S. Larsen (Columbus, MO), Prof. Dr. Jo-
sefina Mansilla Lory (Mexico City, Mexico), Prof. Dr.
Charles F. Merbs (Tempe, AZ), Dr. Peter Neve
(Malente, Germany), Prof. Dr. Dr. Reiner R.R.
Protsch (Frankfurt am Main, Germany), Prof. Dr.
Carmen M. Pijoan Aguade (Mexico City, Mexico),
Dr. Wolfgang Radt (Istanbul, Turkey), Dr. Bruce
Ragsdale (San Luis Obispo, CA), Dr. Charlotte Rob-
erts (Durham, England), Dr. Peter Schröter
(München, Germany), Prof. Dr. J. Szilvássy, Prof.
Dr. Maria Teschler-Nicola (Vienna, Austria), Dr.
Rose Tyson (San Diego, CA), and Prof. Dr. Phillip L.
Walker (Santa Barbara, CA). Additionally, the au-
thor especially thanks the reviewers who helped in
establishing this contribution.
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