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Differential diagnosis of mastoid hypocellularity in human skeletal remains.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:442–453 (2009)
Differential Diagnosis of Mastoid Hypocellularity in
Human Skeletal Remains
Stefan Flohr,1,2* Uwe Kierdorf,1 and Michael Schultz2
1
2
Department of Biology, University of Hildesheim, 31141 Hildesheim, Germany
Department of Anatomy, Georg-August-University, 37075 Göttingen, Germany
KEY WORDS
mastoid process; otitis media; paleopathology; temporal bone pneumatization
ABSTRACT
Mastoid hypocellularity is frequently
used as an indicator of chronic otits media in paleopathological investigations. The condition can be caused by a
poor development of air cells during infancy and early
childhood (primary hypocellularity) or by obliteration of
air cells with bone during later life (secondary hypocellularity). We performed a macroscopic, radiographic, and
microscopic study of pneumatization patterns in 151 mastoid processes of individuals from an early-medieval cemetery in Germany, with emphasis on the architecture of
the nonpneumatized portion of hypocellular mastoid processes. Two types of primary mastoid hypocellularity were
distinguished. The first was characterized by a poorly
defined boundary between the pneumatized portion and
the nonpneumatized portion and a trabecular thickening
in the spongy bone of the latter. The second showed a
well-defined boundary between the pneumatized portion
and the nonpneumatized portion and normal spongy
Today infectious middle ear diseases are among the
most frequently observed medical conditions in humans.
Also in prehistoric human populations otitis media (OM)
was a very frequent disease (Schultz, 1979). It is
assumed that, compared with today’s societies with an
advanced health care system and the availability of antibiotics, severe complications of infectious middle-ear diseases have occurred more often in prehistoric and historic times. Thus far, relatively few paleopathological
studies focused on middle-ear diseases. One reason for
this could be that many osseous manifestations of pathological processes in the middle ear region are difficult to
identify and to interpret in archaeological bone (Qvist
and Grøntved, 2001).
In general, the more developed the osseous manifestations are in archaeological bone the more accurately
they can be assigned to a specific disease. Consequently,
many studies describe very obvious changes in the middle-ear region like stapedial footplate fixation or ankylosis within the ossicle chain (Holzhueter et al., 1965;
Birkby and Gregg, 1975; Arensburg et al., 1977;
Ziemann-Becker et al., 1994) as well as severe destruction caused by cholesteatoma (Mann, 1992; Mays and
Holst, 2006).
The mastoid process of the human temporal bone
shows a variable degree of pneumatization, with the air
cells varying in number, form, and size. Thus, the aircell system may pervade the complete mastoid process
and also extend into other parts of the temporal bone or
even into the jugular process of the occipital bone. On
the other hand, the mastoid process may be acellular,
C 2009
V
WILEY-LISS, INC.
bone architecture in the latter. The key feature for the
diagnosis of secondary hypocellularity was the recognition of the walls of former air cells. Our observations
closely match the histopathological findings by Wittmaack (Wittmaack: Über die normale und die pathologische Pneumatisation des Schläfenbeins. Jena: Gustav
Fischer [1918]), who developed a concept of the normal
pneumatization process of the temporal bone and the
pathogenesis of aberrant pneumatization. We agree with
Wittmaack’s view that two types of primary mastoid
hypocellularity can be distinguished morphologically.
Regarding the pathogenesis of these types, we, however,
conclude that Wittmaack’s concept needs to be revised and
updated. Further studies are required to establish the relationship between morphological findings in cases of mastoid hypocellularity and the health status of individuals.
Am J Phys Anthropol 140:442–453, 2009. V 2009 Wiley-Liss,
C
Inc.
i.e., have no air cells at all. The observed variability in
the degree of pneumatization of the mastoid process
raises the question of whether a poorly developed or
missing mastoid air-cell system can be viewed as a pathological condition (e.g. Wittmaack, 1918, 1932; Link and
Handl, 1954; Tos et al., 1984; Aoki et al., 1990) or
whether hypocellular mastoid processes should be considered ‘‘normal’’ variants (e.g. Schwarz, 1929; Albrecht
and Schwarz, 1933; Schulter-Ellis, 1979; Sadé et al.,
2006). It has been argued that unilateral hypocellularity
in a cranium supports the hypothesis that the condition
was caused by a disease process in the middle ear
(Wittmaack, 1932; Virapongse et al., 1985). However, the
causes underlying the occurrence of mastoid hypocellularity are still a matter of controversy (Todd, 1994). In
principle, mastoid hypocellularity, i.e., an incomplete
pneumatization of the mastoid process or even a total
lack of the mastoid air-cell system (5acellular mastoid
process), can be caused either by a poor development of
air cells during infancy and early childhood, i.e., during
the first 5–6 years of life (primary hypocellularity) or by
*Correspondence to: Stefan Flohr, Department of Biology, University of Hildesheim, Marienburger Platz 22, D-31141 Hildesheim,
Germany. E-mail: flohrs@uni-hildesheim.de
Received 25 November 2008; accepted 13 March 2009
DOI 10.1002/ajpa.21087
Published online 28 May 2009 in Wiley InterScience
(www.interscience.wiley.com).
MASTOID HYPOCELLULARITY
an obliteration of existing air cells with newly formed
bone (secondary hypocellularity).
In paleopathology, a poor or absent pneumatization of
the mastoid region is often used as a criterion for diagnosing chronic otitis media (COM) in human skeletal
remains. Gregg et al. (1965) studied 417 temporal bones
from South Dakota burials using radiographs. Following
clinical/radiological usage, they distinguished a pneumatic condition (well-developed air-cell system) from a
diploic, a mixed, and a sclerotic condition, which they
considered as deviant forms. However, the authors provided no explanation for the causes underlying these different deviant forms or the processes leading to their formation. The same method and the same categories were
used by Titche et al. (1981) who investigated 1,296 temporal bones from 742 skulls of prehistoric Arizona Indians. Again, the causes of the deviant forms of pneumatization and the development of these conditions were not
addressed. In their study on a prehistoric Iranian sample Rathbun and Mallin (1977) diagnosed several cases
of what they described as ‘‘depneumatization,’’ which in
our view could be suggestive of a secondary filling of previously existing air cells.
An attempt to distinguish between different forms of
mastoid hypocellularity with respect to the underlying
etiology was undertaken by Gregg and Steele (1982,
p 460). They linked the diploic condition to ‘‘OM early in
life’’ and the sclerotic condition to ‘‘frequent or severe
OM.’’ Similar interpretations of the different categories
were also given by Loveland et al. (1990).
Comprehensive investigations on pneumatization patterns in recent and historical Inuit populations were performed by Homøe and colleagues (Homøe and Lynnerup,
1991; Homøe et al., 1994, 1995, 1996, 2001). Based on
their results in living people, these authors developed a
model that allowed them to infer the presence or absence
of COM based on pneumatization patterns in dried
skulls. Their studies focused on the planimetric analysis
of the pneumatized part of the temporal bone while
the condition of the nonpneumatized part was not
considered.
Two comments need to be made with respect to the
above-mentioned studies. First, a frequent cooccurrence
of COM and mastoid hypocellularity has been observed
in preantibiotic as well as recent times (Albrecht, 1924;
Hanse, 1930; Stix, 1935; Weber, 1943; Schätzle and Haubrich, 1975; Fleischer, 1979). Therefore, it seems justified
to conclude that diagnosing hypocellularity on radiographs is a nondestructive method providing valid data
on the frequency of COM. However, COM that occurs
first during adult life can of course not be the underlying
cause of primary mastoid hypocellularity, because this
condition is the result of a poor pneumatization during
infancy and early childhood. Rather, primary hypocellularity and COM can be viewed as two symptoms of a disease process that started early in life and persisted into
adult age. Second, the term ‘‘chronic middle ear diseases’’ as used by different authors certainly comprises a
number of different conditions and consequently, the
diagnosis ‘‘COM’’ is a very general one. To the best of
our knowledge, thus far, no attempts have been undertaken to distinguish between different causes of mastoid
hypocellularity in archaeological bone.
Sectioned hypocellular mastoid processes show a variety of morphological pictures. It is often difficult or even
impossible to unambiguously assign these pictures to
one of the broad radiologic categories diploic, mixed, or
443
sclerotic. On the basis of the premise that a well-developed air-cell system represents the ‘‘normal’’ condition, it
could be hypothesized that in the case of primary hypocellularity these different morphologies represent different diseases or at least different courses, stages, or
severities of one and the same disease or disease complex during childhood.
Basic research into the anatomy, histology, and pathology of the middle ear region was conducted in the late
19th and early-20th centuries (e.g. Bezold, 1906; Panse,
1912; Wittmaack, 1918). The anatomical descriptions in
these works are helpful for the interpretation of osseous
structures in archaeological bone since—in contrast to
modern studies—they cover both gross morphological
and microscopic aspects. Furthermore, these early studies present disease conditions from preantibiotic times,
which make the findings more comparable with archaeological cases than do more recent observations. It is well
known that some clinical pictures have changed dramatically with the availability of antibiotic treatments
(Rudberg, 1954).
The aims of the present study were to (1) relate the
huge structural variability visible in sectioned mastoid
processes from archaeological bone to the already existing descriptions and etiological considerations in the otological literature, especially the works by Wittmaack
(1918, 1926), (2) study the prevalence of symmetrically
and asymmetrically developed mastoid air cell systems
in human crania, and (3) discuss the possibilities and
limits of this approach for a differential diagnosis of
mastoid hypocellularity in archaeological skeletal
remains.
MATERIALS AND METHODS
We investigated 151 temporal bones from 99 individuals of the early-medieval (Merovingian period) linear
cemetery of Dirmstein, located in the state of RhinelandPalatinate, Germany (Table 1). In 52 crania, both temporal bones were present and could be diagnosed. Archaeological findings indicate that the cemetery was in use
between the middle of the sixth century and the middle
of the eighth century AD (Leithäuser, 2006). The study
was restricted to individuals of at least juvenile age,
because we wanted to include only those individuals in
which the process of pneumatization of the mastoid process had already been finished. The material from Dirmstein had previously been analyzed for the presence of
osseous changes caused by mastoiditis (Flohr and
Schultz, 2009a,b).
Sex determination was performed on the skeletons
based on gross morphological characteristics of the pelvis
and the skull (Ferembach et al., 1979; Buikstra and
Ubelaker, 1994). Age at death estimation was also based
on gross morphological features, including closure of
cranial sutures (Acsádi and Nemeskéri, 1970; Meindl
and Lovejoy, 1985), changes to the auricular surface of
the ilium (Lovejoy et al., 1985), to the symphyseal face of
the pubis (McKern and Stewart, 1957), and to the ster_can et al., 1984). The individuals were
nal rib ends (Is
grouped into age classes ‘‘juvenile’’ (12–20 years), ‘‘adult’’
(21–40 years), and ‘‘mature/senile’’ (>40 years).
The temporal bones were X-rayed (Faxitron, Hewlett–
Packard) and thereafter sectioned in the frontal plane
with a band saw. Specimens, which on radiologic and
macroscopic inspection demonstrated marked mastoid
hypocellularity, were chosen for microscopic investigaAmerican Journal of Physical Anthropology
444
S. FLOHR ET AL.
TABLE 1. Distribution of sex and age class for the temporal bones analyzed in this studya
Male
Juvenile
Adult, mature/senile
Total
a
Temporal
bones
1
87
88
Female
Individuals
Temporal
bones
1
54
55
3
49
52
Sex indeterminable
Individuals
Temporal
bones
3
34
37
0
11
11
Total
Individuals
Temporal
bones
Individuals
0
7
7
4
147
151
4
95
99
Age estimation and sex determination were performed by M. Lebschy, J. Kauppert, and one of the authors (SF).
TABLE 2. Frequencies of different types of pneumatization of the mastoid process according to sex
Fully
pneumatized
Male
Female
Sex indeterminable
Total
52
39
9
100
(59.1%)
(75.0%)
(81.8%)
(66.2%)
Hypocellular
Type 1
12
7
0
19
(13.6%)
(13.5%)
(0.0%)
(12.6%)
Hypocellular
Type 2
22
5
2
29
tions to obtain more detailed information on their morphology. For this, the bones were embedded in epoxy resin
(Biodur1 E12/E1, Biodur Products, Heidelberg) following
the protocol of Schultz (1988). The blocks were sectioned in a
plane following that of the first section, using a rotary saw
with a water-cooled diamond blade (Woko 50, Conrad Apparatebau, Clausthal-Zellerfeld, Germany). The cut surface
was ground and polished using a series of silicon carbide
papers (grades 600; 1,000; 1,200; 2,400; and 4,000). The polished block faces of selected specimens were viewed in a lowvacuum scanning electron microscope (FEI Quanta 600
FEG) operated in the backscattered electron (BSE) mode to
evaluate the degree of bone mineralization. Thereafter, each
block was mounted with its polished face down to a glass
slide. The block was then removed from the slide using the
rotary saw, leaving behind a 1-mm thick section. This was
ground and polished to a thickness of about 70 lm, again
using a series of graded silicon carbide papers. The ground
sections were studied in a light microscope (Axioskop 2 Plus,
Zeiss, Jena) using bright and dark field illumination, polarized light with and without a red first-order retardation
plate (hilfsobject), as well as phase contrast.
The following morphological characteristics were documented and formed the basis for a classification of mastoid hypocellularity:
Extension of the air cell system within the mastoid
process
Configuration of the boundary between the pneumatized portion and the nonpneumatized portion of the
mastoid process
Bone architecture in the nonpneumatized portion of
the mastoid process
Frequency differences between the two sexes with
regard to the mode of pneumatization of the mastoid
process were analyzed with the v2-test, applying Yates’
correction for continuity. Only crania with both temporal
bones present and diagnosable were included in the
analysis. Statistical analyses were performed using the
software package Statistica 8.0 (StatSoft, Tulsa, OK). A
P-value <0.05 was considered to indicate significance. In
crania in which both temporal bones could be subjected
American Journal of Physical Anthropology
(25.0%)
(9.6%)
(18.2%)
(19.2%)
Hypocellular
Type 3
1
1
0
2
(1.1%)
(1.9%)
(0.0%)
(1.3%)
Hypocellular
Type 2 1 3
1
0
0
1
(1.1%)
(0.0%)
(0.0%)
(0.7%)
Total
88
52
11
151
(100.0%)
(100.0%)
(100.0%)
(100.0%)
Fig. 1. Sectioned right temporal bone of a female (age group
adult) from grave 80 showing a normal extension of the mastoid
air cell system. [Color figure can be viewed in the online issue,
which is available at www.interscience.wiley.com.]
to diagnosis it was further studied whether the mastoid
processes were pneumatized in a symmetric or asymmetric fashion.
RESULTS
Fully pneumatized mastoid process
In most temporal bones (100 of 151; 66.2%; Table 2),
the air-cell system pervaded the complete mastoid region
down to the apex of the mastoid process (see Fig. 1).
These mastoid processes were classified as fully pneumatized. The remaining 51 mastoid processes were classified as hypocellular. In 52 crania, both mastoid processes
445
MASTOID HYPOCELLULARITY
TABLE 3. Distribution of primary pneumatization patterns in crania in which both mastoid processes could be
subjected to diagnosis
Bilaterally fully
pneumatized
Male
Female
Sex indeterminable
Total
a
b
13
10
3
26
One side fully pneumatized;
the other side showing
primary hypocellularity
a
(39.4%)
(66.7%)
(75.0%)
(50.0%)
9
2
1
12
(27.3%)
(13.3%)a
(25.0%)
(23.1%)
Bilateral occurrence of
primary hypocellularity
11
3
0
14
b
(33.3%)
(20.0%)
(0.0%)
(26.9%)
Total
33
15
4
52
(100.0%)
(100.0%)
(100.0%)
(100.0%)
Including one case of unilateral Type 3 (secondary) hypocellularity.
Including one case of unilateral combination of Types 2 and 3 hypocellularity.
TABLE 4. Distribution of primary pneumatization types in crania in which both mastoid processes could be subjected to diagnosis
Fully pneumatized
(bilaterally)
Male
Female
Sex indeterminable
Total
13
10
3
26
a
(39.4%)
(66.7%)
(75.0%)
(50.0%)
Hypocellular
Type 1 (uni- or bilaterally)
7
2
0
9
(21.2%)
(13.3%)
(0.0%)
(17.3%)
Hypocellular
Type 2 (uni- or bilaterally)
13
3
1
17
b
(39.4%)
(20.0%)c
(25.0%)
(32.7%)
Total
33
15
4
52
(100.0%)
(100.0%)
(100.0%)
(100.0%)
a
Including one case of unilateral Type 3 (secondary) hypocellularity (Fig. 8).
Including one case of unilateral combination of Types 2 and 3 hypocellularity (Fig. 10). The contralateral mastoid process of this
individual exhibited Type 2 hypocellularity.
c
Including one case of unilateral Type 3 (secondary) hypocellularity. The contralateral mastoid process of this individual exhibited
Type 2 hypocellularity.
b
were present in a condition allowing diagnosis of the
degree of pneumatization. Twenty-five of these crania
exhibited bilateral full pneumatization of the mastoid
process. A further cranium (from a male individual) was
diagnosed as exhibiting a unilateral secondary hypocellular condition, caused by obliteration of air cells during
later life (see below). Because this cranium had originally possessed two fully pneumatized mastoid processes, the number of crania originally exhibiting bilateral full pneumatization was raised to 26 (Table 3). In
the remaining 26 crania, either one mastoid process or
both processes were diagnosed to show primary hypocellularity (see below). In males, 13 of 33 individuals
(39.4%) showed originally bilaterally fully pneumatized
mastoid processes, whereas in females this condition was
found in 10 of 15 individuals (66.7%). The difference
between the sexes was not statistically significant (v2 5
2.08, df 5 1, P 5 0.15).
Sometimes, a small rim of nonpneumatized bone was
present at the apex of the mastoid process. Formation of
this bone rim was attributed to traction by the sternocleidomastoid muscle. In addition to the pneumatization
process, this traction is considered to influence the size
and shape of the mastoid process (Saternus and
Schmitt, 1970). This condition was considered normal
and was not regarded as representing an incomplete
pneumatization.
Hypocellular condition—Type 1
A rather frequently found pattern in our material was
characterized by two main features. First, there was no
clear boundary between the pneumatized portion and
the nonpneumatized portion of the mastoid process. The
two portions were connected via openings of different
size and a clear distinction between air-cell lumina and
marrow spaces was sometimes not possible. Second, the
nonpneumatized portion exhibited clear deviations from
the normal spongy bone pattern in that its marrow
spaces were variably reduced due to trabecular thickening. This Type 1 hypocellular condition was present in
19 of 151 mastoid processes (12.6%; Table 2). Frequency
of the Type 1 condition (either uni- or bilaterally) was
21.2% (7 of 33) in male crania and 13.3% (2 of 15) in
female ones (Table 4). The difference between the sexes
was not statistically significant (v2 5 0.06, df 5 1, P 5
0.80).
A distinct Type 1 condition was present in the right
temporal bone of a male (age class mature/senile) from
grave 255. The radiograph showed a poor pneumatization of the temporal bone (Fig. 2a). Some periantral air
cells had developed and a massively enlarged air cell
was present in the superior–posterior part of the system
(Citelli’s triangle). The complete mastoid process seemed
to consist of normal spongy bone. The boundary between
the pneumatized portion and the nonpneumatized portion was poorly defined.
The sectioned bone provided further information
(Fig. 2b). Again, the boundary between the pneumatized
portion and the nonpneumatized portion was only poorly
defined. Moreover, the bone architecture of the nonpneumatized portion showed deviations from the normal
spongy bone morphology. Although the trabeculae in the
apex of the mastoid process were almost normal, they
were thicker and irregularly shaped closer to the pneumatized portion, giving this region of the spongiosa a
sclerotic appearance.
A similar condition was present in the right temporal
bone of a male (age class adult or mature/senile) from
grave 225 (see Fig. 3). Because of the poor preservation
of the skeleton, a more accurate age estimation was not
possible. Compared to the first case, the air cells were
smaller but supposedly still within the normal range of
variation. However, the boundary between the air-cell
system and the nonpneumatized portion below was
American Journal of Physical Anthropology
446
S. FLOHR ET AL.
Fig. 2. (a) Lateral radiograph of the isolated right temporal
bone of a male (age class mature) from grave 255 showing a hypocellular condition of Type 1. Some of the existing air cells are slightly
enlarged (arrow). The mastoid process consists of diploic bone
(arrowhead); the boundary between the pneumatized and the nonpneumatized portion is diffuse. (b) Sectioned mastoid process from
the same individual showing that the trabeculae near the pneumatized portion are thickened (asterisk), whereas they are normal near
the tip of the mastoid process. [Color figure can be viewed in the
online issue, which is available at www.interscience.wiley.com.]
Fig. 4. More advanced stage of the Type 1 hypocellular condition in the form of a sclerotic right mastoid process in a male (age
class mature) from grave 244. [Color figure can be viewed in the
online issue, which is available at www.interscience.wiley.com.]
senile). The pneumatized portion appeared to be more
clearly delimited from the nonpneumatized portion.
However, the two portions were still connected via several openings. Also, some spaces located deeper in the
sclerotic portion were most likely connected to the pneumatized portion. They might have been secondarily
enlarged spaces in the formerly existing diploic bone.
Regular spongy bone was not present.
In this case, BSE imaging demonstrated only relatively minor differences in mineral content within the
thickened bone mass (Fig. 5a). Histologically, this mass
consisted predominantly of woven bone, but there were
also some lamellar formations and even osteon-like
structures (Fig. 5b). The overall lower mineral density of
the osteon-like structures compared with the surrounding woven bone (Fig. 5a) suggests a younger age of the
former.
Hypocellular condition—Type 2
Fig. 3. Sectioned mastoid process of a male (age class adult
or mature) from grave 225 showing an advanced stage of a
hypocellular condition of Type 1. The trabeculae of the nonpneumatized portion are thickened; normal trabeculae are not
present. [Color figure can be viewed in the online issue, which
is available at www.interscience.wiley.com.]
again poorly defined. The trabecular bone of the nonpneumatized portion was grossly thickened. In contrast
to the first case, normal spongy bone did not exist in this
case and the trabecular thickening was more marked.
The sclerotic mastoid process shown in Figure 4 is
regarded to represent a more advanced stage of the
same condition (male from grave 244, age class mature/
American Journal of Physical Anthropology
A second type of hypocellularity was characterized by
a well-defined boundary between the pneumatized portion and the nonpneumatized portion of the mastoid process, the latter consisting of spongy bone. The boundary
between the two portions was sometimes slightly sclerotic. In contrast to the first type, the bone structure in
the nonpneumatized portion was not altered. The trabeculae of the spongy bone were of normal thickness and
regular configuration.
Type 2 hypocellularity was present in 29 of 151
mastoid processes (19.2%; Table 2). It was found, either
uni- or bilaterally, in 13 of 33 (39.4%) male crania and in
3 of 15 (20.0%) female ones (Table 4). The difference
between the sexes was again not statistically significant
(v2 5 0.98, df 5 1, P 5 0.32).
MASTOID HYPOCELLULARITY
447
Fig. 5. (a) BSE image of the
sclerotic bone mass shown in
Figure 4. The degree of mineralization is rather homogeneous. (b) Light microscopic
image of the same specimen in
polarized light using a red-one
plate. The sclerotic bone substance consists almost completely of woven bone.
Fig. 6. (a) Lateral radiograph of the isolated temporal bone
of a male (age class adult) from grave 174A showing a Type 2
hypocellular condition. The boundary between the pneumatized
and the nonpneumatized portion is clearly visible (arrow).
(b) Same specimen, sectioned. The diploic bone in the nonpneumatized portion exhibits normal trabecular architecture. [Color
figure can be viewed in the online issue, which is available at
www.interscience.wiley.com.]
A Type 2 hypocellularity was present in a characteristic way in the right temporal bone of a male (age class
adult) from grave 174A. The radiograph showed an overall well-pneumatized temporal bone with a lack, however, of air cells in the mastoid process (Fig. 6a). The
boundary between the air-cell system and the spongy
bone was distinct. In the sectioned bone, these findings
could be observed in more detail (Fig. 6b). The spongy
bone within the mastoid process exhibited a normal configuration with no signs of trabecular thickening.
The variability in this type of hypocellularity was
small. Variations were found only in the position of the
boundary between the pneumatized portion and the
nonpneumatized portion, this position most probably
reflecting the growth stage at which the pneumatization
process had stopped.
Hypocellular condition—Type 3
A third type of hypocellularity was found in only two
mastoid processes (Table 2). The characteristics of this
type of hypocellularity are described for the left temporal
bone of a male individual (age class adult or mature/senile) from grave 274. Because of the poor preservation of
the skeleton, a more accurate age estimation based on
macromorphological features was again not possible. A
third specimen presented a combined form (Types 2 and
3, see below).
Fig. 7. Lateral radiograph of the isolated temporal bone of a
male individual (age class adult or mature) from grave 274
showing Type 3 mastoid hypocellularity. A dense bone mass fills
the lower part of the mastoid process, while the walls of the
former air cells are clearly visible (arrows). The small rim of
normal spongy bone might be due to the traction of the sternocleidomastoid muscle.
The radiograph of the left temporal bone of the individual from grave 274 showed an almost regular
pneumatization of large parts of the temporal bone (see
Fig. 7). The configuration of the air cells was quite
normal. Again, however, the mastoid process was hypocellular, with air cells limited to its upper portion. The
nonpneumatized portion exhibited a nonuniform architecture. There was a clear boundary between a dense
bone formation in the upper part of the nonpneumatized
portion and an apically located diploic part.
The sectioned bone also illustrated this tripartite
structure (Fig. 8a). The upper portion consisted of air
cells, extending to about the height of the mastoid notch.
The most apically located air cell was enlarged, and
some irregular bone formations could be seen along its
wall. The middle portion consisted of dense bone. The
borders with the air cells above and the spongy bone
below were well defined. The apical-most spongy portion
was quite small and might have been formed due to traction of the sternocleidomastoid muscle. Bone architecture within this spongy part was almost normal.
Comparison with the opposite side of the cranium suggested that the hypocellular condition was caused by the
American Journal of Physical Anthropology
448
S. FLOHR ET AL.
Fig. 8. (a) Same specimen as shown in Figure 7. The outline
of the formerly existing air cells that had been filled with a dense
bone mass (arrowhead) can be traced. (b) Contralateral mastoid
process from the same cranium. Comparison of the two-sectioned
mastoid processes demonstrates that the pneumatization pattern
would be very similar on both sides if the dense bone mass present
on the left side were removed. [Color figure can be viewed in the
online issue, which is available at www.interscience.wiley.com.]
Fig. 10. Sectioned right mastoid of a mature male from
grave 1 showing a combination of Types 2 and 3 hypocellularity.
[Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]
fine, densely packed trabeculae. Histologically, these
trabeculae consisted predominantly of woven bone
with only little lamellar bone and only few osteon-like
structures.
Combined type of mastoid hypocellularity
Fig. 9. Microscopic image of the dense bone mass shown in
Figures 7 and 8a. The densely packed trabecular bone formation
(asterisk) consists predominantly of woven bone. The new bone
is attached to the wall of the former air cell (W) by small stalks,
leaving small gaps (arrowheads) between the air cell wall and
the newly formed bone mass. [Color figure can be viewed in the
online issue, which is available at www.interscience.wiley.com.]
secondary filling of air cells. Thus, the course of the
boundary of the pneumatized portion on the right side
was very similar to the course of the boundary between
the dense bone portion and the small spongy portion on
the left side (Fig. 8b). The findings suggest that the
boundary in the left mastoid process traced the extension of its former air-cell system.
On a microscopic level, the dense bone mass present
on the left side was incompletely separated from the surrounding bone and attached to what was regarded as
the walls of the former air cells by small pinlike trabeculae (see Fig. 9). The dense bone mass was not composed
of compact bone, as might have been concluded based on
radiographic examination alone, but instead consisted of
American Journal of Physical Anthropology
One specimen (right temporal bone of a male, age
class mature/senile, from grave 1) was diagnosed as presenting features of both Types 2 and 3 (see Fig. 10). As
in Type 2, the lower part of the mastoid process consisted of spongy bone that was clearly delimited from the
upper part. Air cells were, however, missing from the
complete upper part, which instead consisted of a macroscopically dense bone mass.
The microscopic structure of this bone mass was similar
to the formations described for Type 3. Again, there were
small gaps between what was regarded to be the former
air cell walls and the dense bone formation that was
attached to these walls by small pinlike trabeculae. Moreover, the bone formation itself consisted of densely packed
slender trabeculae. Comparison of the mineralization
between the dense bone formation and the compact bone of
the wall of the mastoid process demonstrated interesting
differences. While the wall of the mastoid process exhibited a rather homogenous mineralization, the dense bone
formation in the interior of the mastoid process showed a
more varying mineralization pattern (see Fig. 11).
Symmetric versus asymmetric pneumatization
Of the 52 crania in which both mastoid processes could
be studied, 26 (50.0%) exhibited either unilateral or
MASTOID HYPOCELLULARITY
Fig. 11. BSE image of same case as depicted in Figure 10.
The dense bone mass in the upper part of the mastoid region
exhibits features regarded as indicative of filling of former air
cells by new bone. Note the variation in the degree of mineralization between the wall of the mastoid process (W) and the new
bone formation (asterisk). Arrowhead: gap between the two components.
bilateral primary hypocellularity (Table 3). In 12 of the
52 crania (23.1%), only one mastoid process exhibited
primary hypocellularity (either Type 1 or Type 2),
whereas the contralateral one was fully pneumatized.
When both mastoid processes exhibited primary hypocellularity, which was the case in 14 of the 52 crania
(26.9%), the condition was always of the same type on
both sides. A combination of Type 1 on one side and
Type 2 on the other side was not observed in our material.
DISCUSSION
The present study demonstrated that different types of
mastoid hypocellularity can be distinguished based on a
combination of macroscopic, radiological, and histomorphological analysis. This approach enables a more
detailed description of the architecture and relationship
of the pneumatized and nonpneumatized portions of
mastoid processes than is possible on the basis of a
purely radiological study. In consequence, it is often difficult and sometimes even impossible to unambiguously
apply the radiologic terms ‘‘diploic,’’ ‘‘sclerotic,’’ and
‘‘mixed’’ to our findings. Thus, a sclerotic condition could
correspond to either a Type 1 or a Type 3 hypocellularity
according to our classification.
Generally, mastoid hypocellularity can be caused either by incomplete pneumatization during infancy and
early childhood (primary hypocellularity) or by a filling
of already existing air cells with new bone (secondary
hypocellularity) during later life. It has been debated for
many years but is widely accepted today that the latter
condition can occur as a consequence of mastoiditis
(Krainz, 1926; Ziegler, 1936; Friedmann, 1957). With
regard to the primary hypocellular condition, there is a
449
controversy about whether this represents genetically
based (normal) variation in the extent of pneumatization
(e.g. Schwarz, 1929; Albrecht and Schwarz, 1933;
Schulter-Ellis, 1979; Sadé et al., 2006) or whether it is
the consequence of a disease process (e.g. Wittmaack,
1918, 1932; Link and Handl, 1954; Tos et al., 1984; Aoki
et al., 1990).
Given the two possible modes leading to mastoid hypocellularity, the question arises whether it is possible to
distinguish between primary and secondary hypocellularity on the basis of features present in dry bone. Such
a distinction would be important, because secondary
hypocellularity is said to be associated with mastoiditis
occurring as a sequel to acute otitis media (AOM) or
COM at higher age.
Minor bone proliferations due to mastoiditis that
extend into the air-cell lumen can be diagnosed in sectioned bones (Flohr and Schultz, 2009a). More extensive
bone proliferation can lead to a more or less-complete
obliteration of air cells. This had apparently been the
case in the Type 3 hypocellular condition of the present
study in which the walls of the former air cells were still
discernable. We therefore conclude that Type 3 hypocellularity represents a secondary hypocellular condition.
Diagnostic features for secondary hypocellularity are the
discernability of the former air-cell walls, the presence of
a small gap between the wall of the (former) air cell and
the new bone formation, the presence of pinlike connections between the wall and the new bone, and a densely
packed trabecular structure of the latter. Only three
cases of secondary hypocellularity (including one mastoid
process exhibiting both primary (Type 2) and secondary
hypocellularity) were observed in our material, suggesting that it is a much rarer phenomenon than primary
mastoid hypocellularity. On first sight, this may appear
to be in contrast to the finding that mastoiditis has been
a common disease in this population (Flohr and Schultz,
2009b). However, the Type 3 condition constitutes an
advanced stage of bone proliferation that has led to
extensive filling of the air cell lumen. Earlier stages of
this proliferation process in the form of frequently
observed pin or platelike structures extending from the
air-cell wall into the air-cell lumen would not be diagnosed as Type 3 hypocellularity although they are also
attributable to mastoiditis (Flohr and Schultz, 2009a).
BSE imaging showed that, compared with the wall the
former air cell, the trabecular bone that filled the air-cell
lumen was characterized by a higher variability in the
degree of mineralization. This finding is consistent with
the view that the trabecular filling of the former air cell
was formed later than the bone constituting the air-cell
wall.
Contrary to Type 3 hypocellularity, no traces of former
air cells could be observed in the nonpneumatized portions of mastoid processes assigned to Types 1 and 2.
This suggests that Type 1 and Type 2 hypocellularity are
primary conditions resulting from incomplete pneumatization of the mastoid process during development in
infants and young children up to the age of 5–6 years.
Our findings and interpretations on the three types of
mastoid hypocellularity are summarized in Table 5.
It may be asked, however, if the bone architecture
observed in these two types of mastoid hypocellularity
could also be a result of the remodeling of obliterated air
cells from mastoid processes showing secondary hypocellularity. In our view, it is very unlikely that a remodeling process in a secondary hypocellular mastoid can lead
American Journal of Physical Anthropology
450
S. FLOHR ET AL.
TABLE 5. Overview of the different types of mastoid hypocellularity with the assigned morphological characters and
their possible etiology
Type 1
Type 2
Type 3
Morphological features
Poorly defined boundary
between the pneumatized
portion and the
nonpneumatized portion
Trabecular thickening in
the spongy bone of the
nonpneumatized portion
Distinct boundary between the
pneumatized portion and the
nonpneumatized portion
(sometimes slightly sclerotic)
Almost normal spongy bone
structure in the
nonpneumatized portion
Mode of formation
Incomplete pneumatization
during development ?
primary hypocellular
condition
Genetic variation or
developmental
disturbances during
growth (environmental
factors)
Hyperplastic mucous
membrane
Incomplete pneumatization
during development ?
primary hypocellular
condition
Genetic variation or
developmental disturbances
during growth
(environmental factors)
Walls of former air cells can be
traced
Lumen of reconstructed former
air cells filled by slender and
densely packed trabeculae
Microscopic inspection shows
that the bone filling the
former air cells is attached to
the former air cell walls by
pinlike trabeculae bridging
the small gap between the air
cell walls and the trabecular
bone inside.
Obliteration of existing air cells
during later life ? secondary
hypocellular condition
Possible origin
Proximate cause according
to Wittmaack
Fibrotic mucous membrane
to the formation of regular spongy bone architecture as
seen in Type 2 hypocellularity.
In the case of Type 1 hypocellularity, the mastoid process presented trabecular thickening of different extent,
affecting smaller or larger areas of the nonpneumatized
portion (Figs. 2–4). The findings could be grouped in a
sequence of increasing severity regarding both the
amount and the extension of trabecular thickening. This
is suggestive of a bone proliferative process spreading
through the nonpneumatized portion of the mastoid process, with the process starting at the boundary between
the pneumatized and the nonpneumatized portion.
This leads us to assume that also Type 1 hypocellularity is in fact a primary condition, i.e., the result of an
incomplete pneumatization during infancy and early
childhood. The fact that the dense bone of the nonpneumatized portion showed a rather homogeneous mineralization is consistent with the view that it was formed
early during development and remained largely
unchanged thereafter. In case of major remodeling processes within the nonpneumatized portion, we would
expect to find a patchier mineralization pattern with
areas of higher and lower mineral density. Thus, it is
assumed that, in this case, woven bone persisted for longer periods of time without being replaced by lamellar
bone. There may, however, be cases in which a distinction between an advanced form of Type 1 hypocelluarity
and Type 3 hypocelluarity is difficult or even impossible.
In the case of primary mastoid hypocellularity, it can be
asked whether the condition represents a genetically
based (normal or abnormal) variation or whether it is indicative of a disturbed development caused by external
factors. Although symmetric hypocellularity is consistent
with both genetic and environmental causation, asymmetric pneumatization patterns point to the condition being
caused by external factors, such as a disease process
(Wittmaack, 1932). In our sample, 12 of 26 of the individuals with primary mastoid hypocellularity exhibited asymAmerican Journal of Physical Anthropology
Bone proliferation due to
mastoiditis
–
metrical pneumatization, i.e., one fully pneumatized and
one hypocellular mastoid process. In these cases, it may
therefore be concluded that environmental factors played
a causative role in the formation of hypocellularity. In
case of symmetrically developed primary hypocellularity,
the explanation of the condition as being caused either by
genetic or by environmental factors may be misleading.
Rather, it can be hypothesized that there exists a genetically based variation in the susceptibility of individuals to
factors causing disturbances of the pneumatization process. This suggests that the same environmental factor
can probably cause mastoid hypocellularity in more susceptible individuals, whereas, in less susceptible individuals, it does not interfere with normal development.
Views on pathological processes in the middle-ear
region underwent major changes during the last century,
not the least due to advances in microscopic and biochemical techniques that allowed more detailed analyses. However, although recent studies using these techniques are relevant for clinical practice, they are often of
little help for interpreting osseous structures present in
the sectioned mastoid process of human skeletons from
archaeological sites. For example, experimental animal
studies reported changes in the mucosa under pathological conditions (Nell and Grote, 1999; Vicente et al.,
2007). However, the mucosa is not preserved in archaeological bone and information on the osseous structure
underneath the mucosa that could be of help for paleopathological diagnosis was not provided by the recent studies. Impaired development of the air-cell system following experimental obstruction of the Eustachian tube in
pigs has been demonstrated (e.g. Aoki et al., 1990). The
morphology of the incompletely pneumatized temporal
bones was, however, not addressed. Also, inflammations
caused by microorganisms during infancy and early
childhood can lead to primary mastoid hypocellularity
(Mey et al., 2006). Again, information on the morphological structure of the incompletely pneumatized temporal
MASTOID HYPOCELLULARITY
bones was not provided. These studies are therefore not
helpful for the interpretation of the morphological variability observed in primary hypocellular mastoids.
It may be asked whether the two different types of primary hypocellularity can be related to different patterns
of alteration of the pneumatization process. This question was largely neglected for several decades, as most
studies focused on the structure and extension of the
pneumatized portion of the mastoid process and did not
address the structure of the nonpneumatized portion
that forms the basis of the distinction between Type 1
and Type 2 hypocellularity. To find information of relevance for the above question, one must go back to work
performed in the first decades of the 20th century.
According to the seminal studies by Wittmaack (1918,
1926, 1932), the mucous membrane is the ‘‘key structure’’ for the pneumatization process of the temporal
bone. Normal pneumatization depends on a normal mucous membrane structure. This normal structure (‘‘constitution’’ according to Wittmaack) can be altered by various disease conditions. His idea was that, depending on
the kind and severity of the disease, the mucous membrane is altered in a specific way, and the process of
pneumatization in consequence becomes disturbed in a
specific manner. Accordingly, Wittmaack stated that the
morphological picture of the (primary) hypocellular mastoid process provides evidence on the underlying disease
(Wittmaack, 1926). To understand the process of disturbed pneumatization on a morphological level, it is
necessary to first consider the normal situation.
On the basis of the findings of Wittmaack (1918,
1926), Eckert-Möbius (1926) gave a detailed description
of the normal pneumatization process. He divided the
process of pneumatization into three steps. Starting with
birth, the process is promoted by an epithelium-lined
and air-filled space that extends from the Eustachian
tube into the middle-ear cavity. The first step of pneumatization is characterized by infiltration of the subepithelial embryonic connective tissue, which usually fills the
middle-ear spaces in the newborn, into the adjacent
spongy bone, replacing the bone marrow in this region.
At the same time, osteoclastic resorption of the trabeculae of the spongiosa forms preliminary spaces within the
spongiosa. In the second step, the epithelium grows into
these preliminary spaces, forming small air cells. The
third step is characterized by regression of the subepithelial connective tissue and the development of the final
mucous membrane that together with the periosteum
forms the so-called mucoperiosteum that covers the bone
surface. Usually, the process of pneumatization is almost
finished at the age of 5 or 6 years. However, minor
changes may still occur in old age.
According to Wittmaack, a pathological alteration of
the mucous membrane during infancy and early childhood will lead to a disturbance of the pneumatization
process. He distinguished a ‘‘hyperplastic’’ from a
‘‘fibrotic’’ (hypoplastic) form of alteration. A mixed form
is also possible when a hyperplastic form is changed to a
fibrotic one. According to Wittmaack (1926, 1932), a
main difference between a hyperplastic mucous membrane and a fibrotic one is whether only the epithelium
or both the epithelium and the subepithelial connective
tissue are affected. In the hyperplastic form, in which
only the mucosal epithelium is altered, the processes
driven by the connective tissue take place in a normal
way. Consequently, step one of the pneumatization process occurs, whereas steps two and three do not. In other
451
Fig. 12. (a) Illustration from Wittmaack (1918) showing a
sectioned temporal bone of a 28-year-old individual with a
severe inhibition of the pneumatization caused by a ‘‘hyperplastic’’ mucous membrane. (b) Illustration from the same book
showing a sectioned temporal bone of a 2-year-old child with a
‘‘fibrotic’’ mucous membrane. Reproduced from Wittmaack K.
1918. Über die normale und die pathologische Pneumatisation
des Schläfenbeins. Jena: Gustav Fischer.
words, connective tissue infiltrates the spongy bone and
replaces the bone marrow. However, contrary to the normal development, this connective tissue does not regress,
and bone formation produces thickened trabecular structures that extend into the former marrow spaces. A clear
boundary is not present between the nonpneumatized
and the pneumatized portions. Wittmaack published
drawings of such cases that show striking similarities to
what we described as the Type 1 condition in our medieval material (Fig. 12a).
In the fibrotic (hypoplastic) form according to Wittmaack (1926) not only the epithelium is affected but also
the connective tissue underneath the epithelium. In this
case, also the first step of the normal pneumatization
process is inhibited. Consequently, there is no infiltration
of connective tissue into and no bone formation within
the spongiosa, which therefore retains a normal trabecular structure. Wittmaack (1918) presented a drawing of
a mastoid process affected by the fibrotic form that
closely resembles our findings in the case of the Type 2
condition in the sectioned archaeological bone (Fig. 12b).
In the view of Wittmaack (1918, 1926), the two forms
of primary hypocellularity reflect different alterations of
the mucous membrane. But what does this tell us about
the underlying disease and the clinical picture in an
affected individual? Wittmaack’s comments on this are
scanty. In his 1926 book, he states that a fibrotic form is
associated with a ‘‘manifest-exudative’’ OM in children,
which may correspond to an AOM in today’s clinical parlance. Regarding the hyperplastic form, Wittmaack himself had difficulties in finding an explanation. He associated it with a ‘‘latent-hyperplastic’’ OM, a condition that
most probably corresponds to a mild chronic form of OM
in today’s terminology. In a later publication, Wittmaack
(1932), however, admits that even one and the same
pathological condition might affect either only the epithelium or both epithelium and underlying connective
tissue. Possible factors affecting the reaction of the
mucous membrane include genotype (‘‘hereditary theory’’
according to Albrecht (1924) and Albrecht and Schwarz
(1933)), a person’s immunocompetence, and the kind,
intensity, and duration of the pathogenic insult.
American Journal of Physical Anthropology
452
S. FLOHR ET AL.
From a pathophysiological point of view, Wittmaack’s
concept of an affection of either only the epithelium or
both the epithelium and the underlying connective tissue
seems problematic. It can be doubted that the epithelium
alone can be affected while the adjacent connective tissue is not. We, however, agree with Wittmaack that
there are two different types of primary mastoid hypocellularity that can be distinguished by detailed morphological analysis.
CONCLUSIONS
In archaeological skeletons, it is possible to distinguish
a primary hypocellular condition of the mastoid process,
caused by an incomplete pneumatization, from a secondary hypocellular condition, caused by obliteration of air
cells with new bone in the course of an inflammatory
process (mastoiditis). The distinction is of importance for
the reconstruction of health conditions in individuals
and paleoepidemiological studies based on these findings.
Primary mastoid hypocellularity develops during the
first 5–6 years of life, whereas secondary mastoid hypocellularity is indicative of mastoiditis during later life.
Assuming that primary mastoid hypocellularity is at
least in most cases indicative of a chronic disease process
starting during infancy and early childhood (or even prenatally, e.g. by aspiration of amniotic fluid), it may be
concluded that individuals exhibiting this condition had
been exposed to an unfavorable environment at young
age.
An association between OM in infancy and early childhood and mastoid hypocellularity was repeatedly documented (e.g. Diamant, 1940; Lindeman and Shea, 1980).
Lubianca Neto et al. (2006) identified major risk factors
for the development of middle-ear diseases in present
populations. Important factors related to the environment
included infections of the upper air ways, presence of siblings/family size, passive smoking, and age at weaning.
In prehistoric and historic times, indoor air pollution
from open-fire places probably constituted an additional
major risk factor for air-way infections that today is still
present in developing countries (Roberts, 2007).
Today, male infants and children are more frequently
affected by middle-ear diseases than female ones
(Lanphear et al., 1997; Paradise et al., 1997). Consistent
with this, in the material from Dirmstein primary mastoid hypocellularity (Types 1 and 2) was more frequently
observed in males than in females, although the differences between the sexes were not statically significant.
This may, however, be due to the small sample size in
our study.
Mastoiditis, as the cause of secondary hypocellularity,
is also linked to infection of the air ways, however, at an
older age (Schätzle and Haubrich, 1975). In the sample
from Dirmstein, secondary mastoid hypocellularity was
much less frequent than primary mastoid hypocellularity. This might be taken to suggest that OM occurs more
often during early than later life, as has been repeatedly
stated in the otological literature (e.g. Klein, 2000;
Boenninghaus and Lennarz, 2005). It must be cautioned,
however, that secondary mastoid hypocellularity is only
one of several possible manifestations of mastoiditis in
the course of OM in later life (Krainz, 1926; Ziegler,
1936; Friedmann, 1957; Flohr and Schultz, 2009a).
Thus, the frequency of secondary mastoid hypocellularity
is in our view not a suitable indicator of the prevalence
of mastoiditis in archaeological skeletons.
American Journal of Physical Anthropology
The observed structural variation in the nonpneumatized portion of the mastoid process could be related to
the histopathological findings by Wittmaack (1918, 1926)
who also proposed a concept for the formation of the different types (Table 5). However, in a paleopathological
context, the relationship between otological disease conditions distinguished in today’s clinical practice and the
morphological findings observed in sectioned mastoid
processes remains problematic. For a deeper understanding of the variety of the morphological manifestations in
cases of mastoid hypocellularity, further anatomical and
histological research on specimens from individuals with
a known course of disease is therefore required. Such a
deeper understanding of the causes underlying the
observed morphological variation would allow more specific diagnoses than those possible in radiology-based
paleootological studies.
ACKNOWLEDGMENTS
The authors thank D. Klosa from Geozentrum Hannover for the opportunity to use the SEM, and Melanie
Lebschy and Joachim Kauppert for help with age at
death and sex determination on the skeletons. The helpful comments by our colleagues Horst Kierdorf and Carsten Witzel and those by the associate editor were greatly
appreciated.
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