Growth pattern of the maxillary sinus in the Japanese ...
Transcript of Growth pattern of the maxillary sinus in the Japanese ...
Dentistry
Dentistry fields
Okayama University Year 1996
Growth pattern of the maxillary sinus in
the Japanese macaque (Macaca fuscata) :
reflections on the structural role of the
paranasal sinuses
Thomas Koppe Hiroshi NagaiOkayama University Okayama University
This paper is posted at eScholarship@OUDIR : Okayama University Digital InformationRepository.
http://escholarship.lib.okayama-u.ac.jp/dentistry general/2
J. Anat. (1997) 190, pp. 533–544, with 5 figures Printed in Great Britain 533
Growth pattern of the maxillary sinus in the Japanese
macaque (Macaca fuscata) : reflections on the structural role
of the paranasal sinuses
THOMAS KOPPE AND HIROSHI NAGAI
Department of Anatomy, Okayama University School of Dentistry, Japan
(Accepted 12 December 1996)
To investigate the claim that the primate paranasal sinuses possess not a functional but a structural role
associated with the skull architecture (Blaney, 1990), the relationship between the maxillary sinus and the
skull architecture was studied ontogenetically in 30 skulls of male and female Japanese macaques (Macaca
fuscata). Coronal CT scan series and computerised 3-dimensional images served to evaluate the maxillary
sinus. The definitive hemispherical shape of the sinus was already achieved after the completion of the primary
dentition. Sinus volume increased with a trend indicating positive allometry. When compared with an
ontogenetic data set of orang-utan (Koppe et al. 1995), however, the growth rate of the maxillary sinus of
M. fuscata was significantly less. The maxillary sinus both of male and female macaques enlarged according
to a common growth pattern. However, no sexual dimorphism could be established for the maxillary sinus
size. Although the volume of the right maxillary sinus was normally bigger than that of the left side, the
results suggested that asymmetry in maxillary sinus volume is related neither to skull size nor sex. Whereas a
correlation analysis showed close relationships between the maxillary sinus volume and external cranial
dimensions, the partial correlation coefficients revealed that these relationships were highly influenced by
skull size. Although it cannot be ruled out that the paranasal sinuses are to some extent linked to the skull
architecture, this study does not support a solely structural role for these air cavities.
Key words : Craniofacial growth; sexual dimorphism; computed tomography.
The actual function of the paranasal sinuses, as well as
the factors involved in the pneumatisation of the
facial skeleton, are still largely uncertain. Numerous
authors have suggested that the development and
growth of the air cavities are directly linked to both
growth of the skull and dentition (e.g. Sperber, 1980;
Wolf et al. 1993). Consequently, it is widely believed
that the morphology of the paranasal sinuses in adults
depends on the skull architecture and that the air
cavities are designed to replace functionless bone
between the bony pillars of the facial skeleton
(Weidenreich, 1924; Lund, 1988).
The degree of pneumatisation, however, varies
considerably among primate species. Furthermore,
Correspondence to Dr Th. Koppe, Department of Anatomy, Okayama University School of Dentistry, Shikata-cho 2–5–1, Okayama, 700
Japan. Fax: 81-86-222-4572; e-mail:koppe!dent.okayama-u.ac.jp.
there is evidence that the difference in the maxillary
sinus size between the Hominoidea and Old World
monkeys cannot be explained only by a single factor
such as body size (Koppe & Nagai, 1995). This also
holds true for the morphology of the floor of the
maxillary sinus. Although the relationships between
the floor of the sinus and the posterior maxillary teeth
tend to become closer in the large-sized hominoids
(Ward & Pilbeam, 1983), root apices of the maxillary
molars exposed into the sinus floor can also be found
in relatively small-sized macaques such as M. mulatta
(Koppe & Nagai, 1995).
While numerous authors have increased our under-
standing about the development, growth and varia-
bility of the human paranasal sinuses (e.g., Schaeffer,
1920; Leicher, 1928; Negus, 1958; Takahashi, 1983;
534 T. Koppe and H. Nagai
Lang, 1989; Anon et al. 1996), the knowledge about
the primate paranasal sinuses is still incomplete. Even
though the morphology of the paranasal sinuses of the
great apes and of certain Old and New World monkey
species has been described in detail (Seydel, 1891;
Paulli, 1900; Wegner, 1936; Cave & Haines, 1940;
Cave, 1968, 1973), quantitative analyses of the
primate paranasal sinuses are rare and mostly re-
stricted to adult samples (Blaney, 1986; Lund, 1988;
Koppe & Schumacher, 1992). As to our knowledge,
except for a single report of the maxillary sinus in
growing Bornean orang-utans (Koppe et al. 1995),
there are no studies on the growth pattern of the air
cavities in primates. This knowledge, however, is
necessary to illuminate the role of the primate
paranasal sinuses.
Thus the present study was performed to analyse
the postnatal growth pattern of the maxillary sinus in
a species of Old World monkey. The maxillary sinus
is the only true air cavity of Old World monkeys
(Koppe & Nagai, 1995). For this study, the Japanese
macaque was chosen because the postnatal cranio-
facial growth as well as the dentition of this macaque
is quite well known (Ikeda & Watanabe, 1966;
Iwamoto et al. 1984, 1987; Mouri, 1994, 1995).
Moreover, a preliminary study of adult Japanese
macaques (Koppe et al. 1996a) revealed a relatively
small degree of sexual dimorphism in the maxillary
sinus size and suggested that both the size and shape
of the maxillary sinus are less related to the external
architecture of the skull than in hominoids. Therefore,
this study may also verify whether the obvious
differences in the morphology of the maxillary sinus
between the Old World monkeys and Hominoidea are
also reflected by differences in the postnatal growth
pattern of this sinus.
Thirty skulls of the Japanese macaque (Macaca
fuscata) of both sexes and of different ages were
studied. The samples comprise skulls from both
captive and wild animals. Because the age of death of
none of these monkeys was known, their age was
estimated from the tooth eruption sequence (Iwamoto
et al. 1984, 1987; Mouri, 1994). The samples were
divided into 4 age groups. Each age group was
comprised of an equal number of male and female
skulls : (1) deciduous dentition and fully erupted
permanent 1st molar (6 animals) ; (2) fully erupted
permanent incisors, as well as the permanent 2nd
molar (6 animals) ; (3) fully erupted premolars (8
animals) ; and (4) complete secondary dentition (10
animals). According to Iwamoto et al. (1984, 1987)
and Mouri (1994) these age groups range approxi-
mately as follows: (1) from birth to 2 y; (2) from 2 y
to 4 y; (3) from 4 y to 4±5 y (female) and 4±75 y (male) ;
(4) older than 4±5 and 4±75 y, respectively.
The skulls were scanned by CT in the coronal plane
using a HiSpeed Advantage RP computed tomograph
(General Electric Medical Systems, Milwaukee, USA).
The slice thickness ranged from 0±5 to 1±0 mm, and the
scanning parameters were 120 kV and 150 mA. The
smaller slice thickness was applied to the skulls of the
age group 1 in order to increase the accuracy of the
following 3-dimensional (3D) reconstructions (Lofchy
et al. 1994). In addition, a number of broken skulls of
newborn and infant monkeys, showing the maxillary
sinus, were examined visually.
The serial coronal CT images were analysed with
the ALLEGRO software program (ISG Technologies,
Toronto). The ALLEGRO workstation was used to
reformat the original coronal CT images of the skull
to view the air cavities also in the sagittal and
horizontal planes. This procedure also permits evalu-
ation of the maxillary sinus and its relationship to
neighbouring structures from a different perspective
without the need to rescan the skulls. Furthermore,
the ALLEGRO workstation served to perform 3D
image reconstructions of the maxillary sinus and
corresponding bony structures as well as for cal-
culation of the maxillary sinus volume (Koppe et al.
1996a).
In addition, to determine the relationship between
the maxillary sinus and skull architecture, the fol-
lowing linear measurements of external cranial para-
meters were recorded with a sliding caliper (Mitutoyo,
Tokyo): basicranial length (basion to nasion) ; facial
length (basion to prosthion), palatal length (prosthion
to staphylion), biorbital width (frontomalare tem-
porale to frontomalare temporale) ; and bimaxillary
width (zygomaxillare to zygomaxillare) (Fig. 1).
Dean & Wood (1981) emphasised that cross-
sectional data of any kind do not permit the
demonstration of individual differences in the rate of
growth or the timing of particular events within the
growth period. Thus, because the exact ontogenetic
ages of the samples were not known and in view of the
small sample size, the relative growth of the maxillary
sinus was described using the basicranial length as an
independent variable. The basicranial length is con-
sidered to be a valuable measure of overall skull size
(Leutenegger & Masterson, 1989). The relationship
between the logarithmic transformed data was
analysed using a simple regression analysis, and the
difference in the slope of the regression lines between
Maxillary sinus growth 535
Fig. 1. Inferior (a) and anterior (b) aspects of a skull as well as a line tracing of a sagittal CT scan (c) of an adult Japanese macaque showing
the measurements used in this study. BL, basicranial length; FL, facial length; PL, palatal length; OW, biorbital width; MW, bimaxillary
width.
the male and female samples was tested by employing
the 2-tailed t test (P! 0±05).
The least-squares regression model was also applied
to describe the growth changes of the external
measurements of the skull. The sexes were pooled for
this analysis. Differences in the relative growth
between the external measurements of the skull and
the maxillary sinus size were detected by testing the
differences in slope of the regression lines using the 2-
tailed t test. To verify whether the relations between
the maxillary sinus volume and the external measures
of the skull were influenced by the skull size factor, in
addition to Pearson’s correlation coefficients, the
partial correlation coefficients were also calculated.
In order to demonstrate possible differences in the
growth pattern of the air cavities between the Old
World monkeys and Hominoidea, the relative growth
of the maxillary sinus of the Japanese macaque was
compared with that of the maxillary sinus of the
orang-utan (Koppe et al. 1995). The basicranial length
again served as an independent variable in both
species and least-squares regression was applied to
describe the relationship between the data sets.
There are numerous discussions regarding which
regression model is appropriate to describe the
relationship between 2 variables, especially for com-
parisons between species (Leutenegger & Larson,
1985; McKinney, 1988; Martin & Barbour, 1989;
Martin, 1990). In this study the least-squares re-
gression model was applied, because it regards X as an
independent variable. The basicranial length was used
as an independent variable mainly to describe the
proportional enlargement of the maxillary sinus rather
than to explain the sinus growth (e.g. Martin, 1990).
On the other hand, however, there is also reason to
treat the measure of body}skull size as an independent
variable because body size itself is an important
determinant of numerous physiological and ecological
parameters (McKinney, 1988; Smith et al. 1995).
Regarding the interspecies comparison of maxillary
sinus growth, it is noteworthy to draw attention to the
fact that the relationship between the maxillary sinus
536 T. Koppe and H. Nagai
Fig. 2. Coronal CT scans through the maxillary first molar (a, b) in male Japanese macaques and reconstructed CT images from direct
coronal CT scans of female Japanese macaques (c, d ) in different age groups; (c) horizontally reconstructed CT scan through the zygomatic
arch (arrowhead) ; (d ) sagittally reconstructed CT scan through the right maxillary 1st molar. The right maxillary sinus is always marked by
an asterisk. Note the relationship between the maxillary sinus and the tooth germ of the maxillary second molar (black asterisk). Although
the tooth germ of the maxillary second molar is in close proximity to the sinus floor, the tooth germ is not exposed as bulge in the sinus
wall. Bar, 1 cm.
volume and age in the orang-utan is most appro-
priately described by a nonlinear regression model
(Koppe et al. 1995). The curvilinear pattern of the
plotted data did not change significantly after the
logarithmic transformation of the raw values. Thus
the orang-utan’s data set was divided into 2 groups
according to the growth pattern as described by
Koppe et al. (1995) : group 1, samples with age of less
than 16 y; and group 2, samples older than 15 y of
age. The differences in the slopes of the regression
lines of the maxillary sinus of M. fuscata and the
orang-utan were tested using the 2-tailed t test (P!0±05).
The paranasal sinuses are subject of considerable
variation in size and shape. Although prominent
developmental anomalies of the maxillary sinus may
occur either as hypoplasia or as aplasia (Bassiouny et
al. 1982), asymmetry in the sinus usually arises as
small random deviations from symmetry. This kind of
asymmetry can be considered as so-called fluctuating
asymmetry (Manning & Chamberlain, 1993). To
reveal whether the observed asymmetry in maxillary
sinus volume of M. fuscata is related to age or to sex,
the absolute asymmetrywas calculatedas thedifference
in the volume of the left and right maxillary sinus
(Manning & Chamberlain, 1993). Because there was a
significant relationship between the absolute asym-
metry and skull size of the males, the relative
asymmetry between the right and the left maxillary
volume was also calculated and expressed by an
asymmetry index. As asymmetry index we adopted
the size dimorphism index that was initially proposed
by Lovich & Gibbons (1992) to express sexual size
dimorphism. The asymmetry index (AI) used in this
study is based on the size of the larger maxillary sinus
(LMS) divided by the size of the smaller maxillary
sinus (SMS). To exhibit directionality, the asymmetry
index was calculated with the formula AI¯[LMS}SMS]1 when the right maxillary sinus was
larger or AI¯ [LMS}SMS]®1 when the left maxil-
lary sinus was larger. Arbitrarily the asymmetry index
was defined as positive when the left maxillary sinus
was larger and negative when the right maxillary sinus
was larger.
Maxillary sinus growth 537
The examination of a few isolated maxillary bones
and broken skulls revealed that the maxillary sinus
has already invaded the maxillary bone at the age of
3–5 mo. At this stage the maxillary sinus appeared as
a bean-like cavity 5–7 mm in length, 3–4 mm in width
and 3–4 mm in height. After completion of the
Fig. 3. Three-dimensional images based on computerized reconstructions of coronal CT scans of Macaca fuscata in different age groups
showing a part of the facial skeleton (grey) from the lateral aspect with the right maxillary sinus (red) and its relation to the developing
permanent teeth viewed from laterally. The tooth roots of already erupted teeth are shown in red, whereas the tooth germs and the tooth
roots of erupting permanent teeth are indicated in yellow. The 1st maxillary molar is always marked by an arrowhead. (a, b) Male macaques;
(c, d ), female macaques.
primarydentition the pairedmaxillary sinuses emerged
in the coronal CT scans as a nearly hemispherical
cavity with the base towards the nasal cavity. At this
stage the maxillary sinus was seen in the region of the
2nd maxillary deciduous molar and the tooth germ of
the 1st maxillary molar. Only the latter, however, was
in close relation to the maxillary sinus floor (Figs 2, 3).
As the permanent molars erupted the maxillary
538 T. Koppe and H. Nagai
Fig. 4. Bivariate logarithmic plot of the maxillary sinus volume
against the basicranial length in male and female Macaca fuscata.
Note that the values of both male and female monkeys form a
common cluster.
sinus gradually enlarged mainly in an anteroposterior
direction. The growth laterally towards the zygo-
maticomaxillary suture was less pronounced. Thus
in coronal CT scans the hemispherical form of the
maxillary sinus, which was already evident with the
completion of the primary dentition, did not change
Table 1. Means and standard deviations of the maxillary sinus volume* of male and female Japanese macaques in different age
groups
Males Females
Right sinus Left sinus Right sinus Left sinus
Age group n Mean .. Mean .. AS n Mean .. Mean .. AS
1 3 0±07 0±03 0±06 0±03 0±009 3 0±07 0±02 0±06 0±02 0±004
2 3 0±24 0±13 0±12 0±11 0±066 3 0±17 0±04 0±14 0±03 0±037
3 4 0±38 0±17 0±40 0±17 0±054 4 0±30 0±24 0±29 0±22 0±051
4 5 0±99 0±48 0±90 0±24 0±257 5 0±77 0±46 0±77 0±42 0±069
* In cm$ ; n, sample size ; the 2-tailed t test revealed no sex difference in maxillary sinus volume in any of these age groups; AS, absolute
asymmetry, i.e. mean difference in the volume of the left and right maxillary sinuses.
Table 2. Means and standard deviations for right maxillary sinus volume* of Macaca fuscata and Pongo satyrus borneensisa
in different age groups, sexes are pooled. The relative increase of maxillary sinus volume is expressed as percentage from the age
group 4 (adult)
Macaca fuscata Pongo satyrus borneenis
Age group n Mean .. P n Mean .. P
1 6 0±07 0±02 7±8 6 2±52 3±65 9±82 6 0±18 0±11 20±3 6 6±95 4±83 34±33 8 0±35 0±19 39±3 6 15±63 3±36 61±04 10 0±88 0±46 100±0 22 25±61 7±66 100±0
* In cm$ ; a taken from Koppe et al. (1995) ; n, sample size ; P, percentage.
markedly. During the eruption of the secondary
dentition the maxillary sinus came in contact with the
crypts of the developing 2nd maxillary molar (Figs 2,
3). After the eruption of the permanent 2nd molar the
maxillary sinus shared a wall with the crypt of the
tooth germ of the 3rd maxillary molar (Fig. 3).
Although the maxillary sinus was seen frequently in
close proximity to the developing molars during the
eruption of the secondary dentition, the tooth germs
were not exposed as bulges into the sinus floor. After
the completion of the secondary dentition, only the
palatal root of the 1st maxillary molar occasionally
reached the maxillary sinus floor (Fig. 3).
The maxillary sinus volume (pooled sexes) increased
from 0±07 cm$ in age group 1 to 0±88 cm$ in age group
4 (adult) (Table 2). Although male monkeys tended to
have a bigger sinus than female monkeys, there was
no significant sexual dimorphism in sinus size. The
plot of the log-transformed data against the basi-
cranial length indicated that both male and female
macaques follow the same growth pattern. Moreover
the statistical analysis revealed no significant difference
in the slope of the regression lines of male and female
samples (Fig. 4).
Asymmetry between the right and left maxillary
sinus volume also occurs in M. fuscata. Although
Maxillary sinus growth 539
Table 3. Regression coefficients for log-transformed right maxillary sinus volume and external cranial dimensions against
basicranial length in Macaca fuscata ; sexes are pooled. Asterisks mark slopes, significantly different from the slope of maxillary
sinus volume
Dimensions (n) Intercept Slope 95% CI r t value
Maxillary sinus volumea (30) ®2±158 2±449 (1±806, 3±092) 0±828 —
Facial length (30) ®0±459 1±662 (1±566, 1±759) 0±989 2±483*
Palatal length (30) ®0±906 1±852 (1±510, 2±193) 0±903 1±677ns
Bimaxillary width (30) ®0±109 1±059 (0±917, 1±200) 0±945 4±330**
Biorbital width (30) 0±119 0±725 (0±574, 0±876) 0±882 5±345**
n, Sample size ; a cube root value; 96% CI, 95% confidence interval for slope estimate; *P! 0±05; **P! 0±01; nsnot significant.
Table 4. Correlation matrix among the measurement items of the right maxillary sinus and external cranial measurement in
growing Japanese macaques; sexes are pooled (n¯ 30)
1 2 3 4 5
1 Maxillary sinus volume — — — — —
2 Basicranial length 0±696 — — — —
3 Facial length 0±736 0±987 — — —
4 Palatal length 0±701 0±906 0±926 — —
5 Bimaxillary width 0±737 0±940 0±944 0±894 —
6 Biorbital width 0±677 0±870 0±874 0±770 0±885
For all results P! 0±01; n, sample size.
Fig. 5. The relationship between log basicranial length and
asymmetry index in male and female Japanese macaques. Although
the right maxillary sinus of both male and female animals tended to
be larger than the left maxillary sinus, correlation analysis revealed
that the degree of asymmetry was not associated with basicranial
length, either in males or females.
there was no clear consistency with regard to the
direction of asymmetry, in both male and female
monkeys the larger maxillary sinus volume was
generally observed on the right side. The absolute
asymmetry, however, was more pronounced in male
monkeys and tended to increase from age group 1 to
age group 4 (Table 1). We found for males that the
absolute asymmetry was significantly correlated with
Table 5. Pearson’s correlation coefficients (r) and partial
correlation coefficients (r«) among the maxillary sinus volume
and external cranial dimensions. (Sexes are pooled, n¯ 30)*
Dimensions r r«
Maxillary sinus volume (right)
Maxillary sinus volume (left) 0±954** 0±908**
Facial length 0±736** 0±423*
Palatal length 0±701** 0±046ns
Bimaxillary width 0±737** 0±335ns
Biorbital width 0±677** 0±201ns
* Basicranial length¯ constant ; *P! 0±05, **P! 0±01; nsnot
significant ; n, sample size.
the basicranial length (r¯ 0±652; P! 0±01). There
was no significant correlation between the absolute
asymmetry and basicranial length in female monkeys.
To obtain an asymmetry pattern that is independent
from the skull size factor, the relative asymmetry was
calculated and expressed by the asymmetry index
(Fig. 5). A correlation analysis revealed no significant
association between the basicranial length and the
asymmetry index either for males (r¯ 0±335) or
females (r¯ 0±214), suggesting that asymmetry in
maxillary sinus volume is related neither to sex nor
age.
Comparing the relative growth of the maxillary
sinus with the growth of different external measure-
ments of the skull, it became evident that maxillary
sinus volume increased with a steeper slope than most
540 T. Koppe and H. Nagai
Table 6. Comparison of the regression coefficients for log-transformed right maxillary sinus volume against basicranial length
between Macaca fuscata and Pongo satyrus borneensis ; sexes are pooled. Asterisks mark slopes of Pongo satyrus borneenisa,
significantly different from Macaca fuscata
Species (n) Intercept Slope 95% CI r t value
Macaca fuscata ®6±427 7±284 (5±344, 9±225) 0±824 —
Pongo satyrus—Group 1 (24) ®8±132 9±889 (8±232, 11±546) 0±938 2±081*
Pongo satyrus—Group 2 (16) ®2±567 1±852 (0±956, 4±177) 0±675 2±246ns
aData from Koppe et al. (1995) ; n, sample size ; Group 1, age 0–15 y, Group 2 age" 15 y; 95% CI, 95% confidence interval for slope
estimate; *P! 0±05; nsnot significant.
of the cranial measurements. However, there was no
significant difference in the slopes of the regression
lines between maxillary sinus volume and palatal
length (Table 3). While the Pearson’s correlation
coefficients indicated significant associations between
maxillary sinus volume and the external measures of
the skull, the calculation of the partial correlation
coefficients proved that most of the correlations were
influenced by the basicranial length (Tables 4, 5).
Regarding the interspecies comparison of the
relative growth pattern of the maxillary sinus, this
study showed different results depending on the
treatment of the raw data for the orang-utan. In the
case when the orang-utan data set was treated as a
single group, regardless of the curvilinear plot of the
log-transformed values, no differences in the slopes of
the regression lines between M. fuscata and the orang-
utan could be found. However, the division of the
orang-utan’s values into 2 groups as indicated above
revealed obvious differences in the growth patterns
between these species. Although the relative growth of
maxillary sinus volume of both the Japanese macaque
and orang-utan (group 1) showed positive allometry,
maxillary sinus volume of the orang-utan increased
within the 1st group with a significantly steeper slope.
Because group 2 comprises mainly adult and mature
samples of orang-utan, the increase of the maxillary
sinus volume within group 2 was significant smaller
when compared with the growth series of the Japanese
macaque, and the slope of the regression line indicated
isometry, i.e. the increase of maxillary sinus volume
proportionally to basicranial length (Tables 2, 6).
Maxillary sinus growth
Regarding the known variation in size and shape of
the paranasal sinuses it is interesting to note that the
definitive shape of the maxillary sinus is achieved in
the Japanese macaque relatively early in postnatal
development with the completion of the primary
dentition. The finding that the characteristic pyr-
amidal shape of the human maxillary sinus does not
emerge before the eruption of the 2ndmolar (Schaeffer,
1910) may point to species differences in the re-
lationship of the maxillary sinus to the developing
teeth. Indeed, Ward & Brown (1986) held that in
cercopithecoids the development of the maxillary
sinus is not closely synchronised with dental matu-
ration as in man. The present study seems to support
this claim.
Although the maxillary sinus floor of the Japanese
macaque was always in close proximity to the tooth
germs of the maxillary molars during postnatal
growth, contrary to the condition found in the
hominoids (Underwood, 1910; Schaeffer, 1920;
Runge, 1928; Koppe et al. 1995), the crypts of the
developing tooth germs of M. fuscata were not
exposed as bulges in the walls of the maxillary sinus.
When the eruption of the permanent teeth is com-
pleted, the differences between M. fuscata and the
hominoids regarding the relationship of the maxillary
sinus floor to the tooth roots are much clearer.
Whereas in the hominoids the tooth roots of the
maxillary posterior teeth are in close proximity to the
floor of the maxillary sinus also after completion of
the primary dentition, the sinus floor in adult Japanese
macaques is usually seen quite far from the root apices
of the molars (Koppe & Nagai, 1995). Numerous
studies have highlighted the fact that the enlargement
of the human maxillary sinus into the maxilla is
restrained by the developing teeth (e.g. Anon et al.
1996). However, it is important to recall that also in
man the influence of the primary dentition on the
growth of the maxillary sinus is not conspicuous
(Schaeffer, 1920; Runge, 1928).
At first glance the results of the morphological
analysis seem to support the view of the maxillary
sinus of Old World monkeys as a structure which, if
present at all, expands very slowly and not to any
great extent (Ward & Brown, 1986; Benefit &
McCrossin, 1993). The results of this study showed,
however, that the maxillary sinus volume increased
with a trend indicating positive allometry, i.e. the
Maxillary sinus growth 541
sinus grew faster postnatally than did basicranial
length. Although comparable data are rare, this
growth pattern is similar to that of the maxillary sinus
of man and the orang-utan (Libersa et al. 1981;
Koppe et al. 1995). Moreover, the fact that frontal
sinus volume in the African great apes also shows
positive allometry when scaled relative to skull length
(Blaney, 1986), suggests that this trend is a common
pattern within higher primates. However, although
the maxillary sinus both of the Japanese macaque and
the orang-utan tended to increase with increasing
skull size, this present study confirms an earlier report
(Koppe & Nagai, 1995) which showed evidence that
this relationship may differ in the hominoids and Old
World monkeys.
Variation in size and shape of the paranasal sinuses
is a common finding. In humans the maxillary sinuses
are subject to fewer variations than the other
paranasal sinuses (Dodd & Jing, 1977). The present
study showed a significant correlation between the
absolute asymmetry in maxillary sinus volume and
skull size, but only for males. At first glance results
seem to support the view (Manning & Chamberlain,
1983) that structures under stronger sexual selection
tend to show a higher level of asymmetry. However,
the asymmetry index (Fig. 5) revealed that neither
skull size nor sex is correlated with asymmetry.
Despite numerous studies concerning asymmetry in
the size of the human maxillary sinus which differ
mainly in whether the left (Anagnostopoulou et al.
1991; Nowak & Mehlis, 1975) or right maxillary sinus
(Schu$ rch, 1906; Schumacher et al. 1972) is larger, it
has been suggested that asymmetry in the human
maxillary sinus is usually very small (Ariji et al. 1994).
Moreover Ariji et al. demonstrated that missing teeth
did not affect the differences between the volume of
the right and left maxillary sinuses. Although more
studies are necessary to explore the influence both of
environmental and genomic stress on the asymmetry
in maxillary sinus size, the present study supports the
assumption (Livshits & Smouse, 1993) that fluctuating
asymmetry such as in maxillary sinus size might be
considered merely as a ‘measure of noise ’ in de-
velopment.
Sexual dimorphism in maxillary size is well docu-
mented for both man and the great apes (Schaeffer,
1920; Nowak & Mehlis, 1975; Koppe et al. 1995).
Recently Koppe et al. (1995) have suggested that
sexual dimorphism in the maxillary sinus volume of
the orang-utan results from prolonged growth in
males. This pattern is the ontogenetic basis of sexual
dimorphism of most external cranial traits of the Old
World monkeys (Shea, 1986; Ravosa, 1991), including
M. fuscata (Mouri, 1994). In the latter, sexual di-
morphism of numerous cranial dimensions occurs in
early stages of postnatal development (Mouri, 1994).
The present study, however revealed a lack of sexual
dimorphism in the maxillary sinus size. If both male
and female Japanese macaques exhibit a common
growth pattern in most of the external cranial
dimensions as well as in the maxillary sinus, the
question arises why does the growth of the maxillary
sinus stop so early in males?
Blaney (1986), studying the sexual dimorphism of
frontal sinus volume in African great apes, held that
the external cranial morphology also has a con-
siderable influence on the degree of sexual dimorphism
in sinus size, i.e. the smaller the degree of sexual
dimorphism in external cranial dimensions the smaller
the dimorphism in sinus size. Although further studies
on related species such as M. mulatta and
M. fascicularis, which exhibit a stronger sexual di-
morphism in most cranial dimensions than M. fuscata
(Mouri, 1995), are necessary to evaluate the validity of
Blaney’s (1986) approach for M. fuscata, the results of
the present study suggest that the relationship between
the morphology of the maxillary sinus of M. fuscata
and the external cranial architecture is obviously
weak. All calculated partial correlation coefficients
betweenmaxillary sinus volume anddifferentmeasures
of the skull were clearly below the Pearson’s cor-
relation coefficients (Table 5). The lack of sexual
dimorphism in the maxillary sinus size of M. fuscata
as well as the weak relationship between the sinus and
the external dimensions of the skull strengthen the
assumption that the influence of facial growth on the
development of the maxillary sinus is smaller than had
been previously suggested (e.g. McGowan et al. 1993).
These findings support earlier studies in man sug-
gesting that the maxillary sinus possesses a devel-
opmental potential of its own (Schaeffer, 1920;
Libersa et al. 1981).
The ‘structural ’ role of the paranasal sinuses
Among primates, the maxillary sinus tends to enlarge
with increasing skull}body size (Ward et al. 1982;
Lund, 1988). Furthermore, in addition to a maxillary
sinus that pneumatises virtually the whole maxillary
bone, the African apes and man have the ethmoidal,
frontal and sphenoidal sinuses. This high degree of
skull pneumatisation seems to support Blaney’s (1986)
claim that the paranasal sinuses do not have a
functional but only a structural role, i.e. to eliminate
unnecessary bone between the pillars of the facial
skeleton. The lack of sexual dimorphism in sinus size
542 T. Koppe and H. Nagai
as well as the weak relationship between the external
cranial architecture and the maxillary sinus in
M. fuscata suggests, however, that a solely structural
role of the maxillary sinus is questionable at least for
this species. On the other hand, recent clinical studies
indicate that the influence of external cranial mor-
phology on pneumatisation in man is also obviously
smaller than is usually indicated in common textbooks
on human anatomy. Robinson et al. (1982) and
Francis et al. (1990) have demonstrated that in
patients with cleft palate neither size and shape nor
the growth rate of the air cavities differed significantly
from a normal population. Furthermore, recent
investigations on Bornean orang-utans (Koppe et al.
1996b) strengthen the assumption that the influence
of palatal form on the maxillary sinus is not
conspicuous.
The numerous theories about the significance of the
paranasal sinuses explain the air cavities either on a
structural or a functional basis (for review see,
Blanton & Biggs, 1969; Takahashi, 1983; Blaney,
1990). Although none of these theories have been
convincingly proved, arguments supporting a struc-
tural role for the paranasal sinuses dominate the
literature. With regard to biomechanical analysis of
the skull morphology of different mammalian species
(Demes et al. 1986; Preuschoft et al. 1986), Preuschoft
(1989) claimed that the changes of skull shape during
human evolution can be explained as an adaptation to
the mechanical necessities caused by alterations of
bite force. Moreover, he held that the widening of the
maxillary sinus in hominoids can be understood as a
possibly effective way to increase bending strength.
Recent studies of in vivo bone strains in cercopithe-
coids (Hylander et al. 1991; Hylander & Johnson,
1992) have demonstrated, however, that not all bony
structures of the face are designed to optimize strength
according to the masticatory loads.
It is important to recall that the morphology of the
skull as seen in adults is the result of complex
interactions between its numerous skeletal subunits in
the course of ontogenesis (Moss & Greenberg, 1967;
McAlarney et al. 1992; Zelditch et al. 1992; Emerson
& Bramble, 1993). Most of the growth-related
allometric changes in size and shape of these subunits
have functional consequences, which are also im-
portant in terms of phylogenesis (Dean & Wood,
1984; Emerson & Bramble, 1993). Thus with regard to
the fact that the maxillary sinus is probably a primitive
eutherian feature (Moore, 1981), it is unlikely that the
primate air cavities have developed only because of
alterations in skull morphology. Conversely, we
hypothesise that the already present paranasal sinuses
served during the evolution of hominoids as structures
to optimise the skull architecture (e.g. Preuschoft,
1986).
Regarding the function of the paranasal sinuses, it
should be stressed here that the sinus spaces have to be
considered as part of the upper respiratory tract.
Although there is considerable scepticism regarding a
significant contribution of the paranasal sinuses, e.g.
for air conditioning, it is interesting to note that the
sinus mucosa shows a number of peculiarities such as
a high regenerative capacity (McGowan et al. 1993)
and a relatively high venous blood flow (Drettner &
Aust, 1974). This blood flow is similar to that of the
nasal mucous membrane and greater than in muscles,
brain and liver (Drettner & Aust, 1974). It has been
suggested that cooling of the nasal mucous membrane
through ventilation may be important for the regu-
lation of brain temperature (e.g. Baker & Chapman,
1977; Dean, 1988; Zenker & Kubik, 1996). In a recent
paper, Zenker & Kubik (1996) claimed that among
others the veins of the paranasal sinuses are involved
in this process. Thus although it cannot be ruled out
that the paranasal sinuses are in some way linked to
skull architecture, we suppose that the paranasal
sinuses are functional. These functions, however, may
differ between different orders of mammals (Moore,
1981) and also among different taxonomic groups of
primates.
This study was supported by the Cooperative Re-
search Program of the Primate Research Institute of
Kyoto University, Japan. We are grateful to Prof. T.
Kimura (Tokyo), Dr Y. Hamada, Dr T. Mouri and
Dr Y. Kunimatsu (Inuyama) for valuable advice and
support. Prof. Y. Hiraki (Okayama) kindly provided
examination time on the CT scanner of his department
and allowed us to use the workstation to produce the
3D images. We thank Mr Y. Ohkawa (Okayama) for
his kind assistance in running the CT scanner. We
would like to thank Linda E. Curtis for preparing Fig.
1. Dr Christopher Dean (London), Dr Todd C. Rae
(Durham) as well as Dr Valerie Lee and Dr Jens C.
Tu$ rp (Ann Arbor) offered helpful comments on this
paper.
A S, V D, S N. (1991)
Classification of human maxillary sinuses according to their
geometric features. Anatomischer Anzeiger 173, 121–130.
A JB, R M, Z SJ (1996) Anatomy of the Paranasal
Sinuses. Stuttgart : Georg Thieme.
A Y, K T, M S, A E, K S (1994) Age
changes in the volume of the human maxillary sinus: a study
Maxillary sinus growth 543
using computed tomography. Dentomaxillofacial Radiology 23,
163–168.
B MA, C LW (1977) Rapid brain cooling in exercising
dogs. Science 195, 781–783.
B A, N WJ, A H, Z Y (1982) Maxillary
sinus hypoplasia and superior orbital fissure asymmetry.
Laryngoscope 92, 441–448.
B BR, MC M (1993) Facial anatomy of Victoria-
pithecus and its relevance to the ancestral cranial morphology of
Old World monkeys and apes. American Journal of Physical
Anthropology 92, 329–370.
B SPA (1986) An allometric study of the frontal sinus in
gorilla, pan and pongo. Folia Primatologica 47, 81–96.
B SPA (1990) Why paranasal sinuses? Journal of Laryngology
and Otology 104, 690–693.
B PI, B NL (1969) Eighteen hundred years of
controversy: the paranasal sinuses. American Journal of Anatomy
124, 135–148.
C AJE (1968) Observations on the platyrrhine nasal fossa.
American Journal of Physical Anthropology 26, 277–288.
C AJE (1973) The primate nasal fossa. Proceedings of the
Linnean Society of London 5, 377–387.
C AJE, H RW (1940) The paranasal sinuses of the
anthropoid apes. Journal of Anatomy 72, 493–523.
D MC (1988) Another look at the nose and the functional
significance of the face and the nasal mucous membrane for
cooling the brain in fossil hominids. Journal of Human Evolution
17, 715–718.
D MC, W BA (1981) Developing pongid dentition and its
use for ageing individual crania in comparative cross-sectional
growth studies. Folia Primatologica 36, 111–127.
D MC, W BA (1984) Phyologeny, neotony and growth of
the cranial base in hominoids. Folia Primatologica 43, 157–180.
D B, C N, P H (1986) Functional significance of
allometric trends in the hominoid masticatory apparatus. In
Primate Evolution (ed. Else JG, Lee PC), pp. 229–238. Cambridge:
Cambridge University Press.
D GD, J BO (1977) Radiology of the Nose, Paranasal
Sinuses and Nasopharynx. Baltimore: Williams & Wilkins.
D B, A R (1974) Plethysmographic studies of the blood
flow in the mucosa of the human maxillary sinus. Acta Oto-
Laryngologica 78, 259–263.
E SB, B DM (1993) Scaling, allometry, and skull
design. In The Skull, vol. 3 (ed. Hanken J, Hall BK), pp. 384–421.
Chicago: University of Chicago Press.
F P, R R, K P, K I (1990) Pneumatization
of the paranasal sinuses (maxillary and frontal) in cleft lip and
palate. Archives of Otolaryngology—Head Neck and Surgery 116,
920–922.
H WL, P PG, J KR (1991) Function of the
supraorbital region of primates. Archives of Oral Biology 36,
273–281.
H WL, J KR (1992) Strain gradients in the
craniofacial region of primates. In The Biological Mechanisms of
Tooth Movement and Craniofacial Adaptation (ed. Davidovitch
Z), pp. 559–569. Columbus: Ohio State University, College of
Dentistry.
I J, W T (1966) Morphological studies of Macaca
fuscata. III. Craniometry. Primates 7, 271–288.
I M, H Y, W T (1984) Eruption of the
deciduous teeth in Japanese monkeys (Macaca fuscata). Journal
of the Anthropological Society Nipponica 92, 273–279.
I M, W T, H Y (1987) Eruption of
permanent teeth in Japanese monkeys (Macaca fuscata). Primate
Research 3, 18–28.
K T, S KU (1992) Untersuchen zum Pneumatisa-
tionsgrad des Viscerocranium beim Menschen und bei den
Pongiden. Acta Anatomica Nipponica 67, 725–734.
K T, N H (1995) On the morphology of the maxillary
sinus floor in Old World monkeys—a study based on three-
dimensional reconstructions of CT scans. In Proceedings of the
10th International Symposium on Dental Morphology (ed.
Radlanski RJ, Renz H), pp. 423–427. Berlin: C. & M. Bru$ nne.
K T, R$ -E O, H D, R R, N, H (1995)
Growth pattern of the maxillary sinus in orang-utan based on
measurements of CT scans. Okajimas Folia Anatomica Japonica
72, 37–43.
K T, I Y, H Y, N H (1996a) The pneumatiza-
tion of the facial skeleton in the Japanese macaque (Macaca
fuscata)—a study based on computerized three-dimensional
reconstructions. Anthropological Science 104, 31–41.
K T, R$ -E O, H D, R R, N H (1996b)
The relationship between the palatal form and the maxillary sinus
in orang-utan. Okajimas Folia Anatomica Japonica 72, 297–306.
L J (1989) Clinical Anatomy of the Nose, Nasal Cavity and
Paranasal Sinuses. Stuttgart : G. Thieme.
L H (1928) Vererbung anatomischer Variationen der Nase,
ihrerNebenhoX hlenunddesGehoX rgangs.Mu$ nchen: J. F. Bergmann.
L W, L S (1985) Sexual dimorphism in the
postcranial skeleton of New World primates. Folia Primatologica
4, 82–95.
L W, M TJ (1989) The ontogeny of sexual
dimorphism in the cranium of Bornean orang-utans (Pongo
pygmaeus pygmaeus) : II.Allometry andheterochrony.Zeitschrift
fuX r Morphologie und Anthropologie 78, 15–24.
L C, L M, L JC (1981) The pneumatization of the
accessory cavities of the nasal fossae during growth. Anatomica
Clinica 2, 265–273.
L G, S PE (1993) Multivariate fluctuating asymmetry
in Israeli adults. Human Biology 65, 547–578.
L N, S J, T J (1994) Three-dimensional
reconstruction imaging of the paranasal sinsues. In An Atlas of
Imaging of the Paranasal Sinuses (ed. Shankar L, Evans K,
Hauke M, Stammberger H), pp. 172–178. London: Martin
Dunitz.
L JE, G JW (1992) A review of techniques for
quantifying sexual size dimorphism. Growth, Development &
Aging 56, 269–281.
L VJ (1988) The maxillary sinus of higher primates. Acta Oto-
Laryngologica 105, 163–171.
M JT, C AT (1993) Fluctuating asymmetry,
sexual selection and canine teeth in primates. Proceedings of the
Royal Society of London. Series B : Biological Sciences 251, 83–87.
M RA (1990) Estimating body mass and correlated variables
in extinct mammals : travels in the fourth dimension. In Body Size
in Mammalian Paleobiology (ed. Damuth J, MacFadden BJ), pp.
49–68. Cambridge: Cambridge University Press.
M RD, B AD (1989) Aspects of line-fitting in bivariate
allometric analyses. Folia Primatologica 53, 65–81.
MA ME, D G, M ML, M-S L
(1992) Anatomical macroelements in the study of craniofacial rat
growth. Journal of Craniofacial Genetics and Developmental
Biology 12, 3–12.
MG DA, B PB, J J (1993) The Maxillary Sinus
and its Dental Implications. Oxford: Wright.
MK ML (1988) Classifying heterochrony allometry, size and
time. In Heterochrony in Evolution. A Multidisciplinary Approach
(ed. McKinney ML), pp. 17–34. New York: Plenum Press.
M WJ (1981) The Mammalian Skull. Cambridge: Cambridge
University Press.
M ML, G SN (1967) Functional cranial analysis of the
human maxillary bone: I, basal bone. Angle Orthodontist 37,
151–164.
M T (1994) Postnatal growth and sexual dimorphism in the
skull of the Japanese macaque (Macaca fuscata). Anthropological
Science 102 (Suppl.), 43–56.
544 T. Koppe and H. Nagai
M T (1995) Sex differences of the cranial size in macaque
species. Primate Research 11, 187–196.
N V (1958) The Comparative Anatomy and Physiology of the
Nose and the Paranasal Sinuses. Edinburgh: E. & S. Livingstone.
N R, M G (1975) Untersuchungen zum Verhalten der
Pneumatisation des Sinus maxillaris. Anatomischer Anzeiger 138,
143–151.
P S (1900) U> ber die Pneumaticita$ t des Scha$ dels bei den
Sa$ ugethieren. Eine morphologische Studie. I, II, III. Gegenbaurs
Morphologisches Jahrbuch 28, 147–178, 179–251, 483–564.
P H (1989) Biomechanical approach to the evolution of
the facial skeleton of hominoid primates. In Trends in Vertebrate
Evolution, Fortschritte der Zoologie Band 35 (ed. Splechtna H,
Hilgers H), pp. 421–431. Stuttgart : Gustav Fischer.
P H, D B, M M, B$ HF (1986) The
biomechanical principles realised in the upper jaw of long-
snouted primates. In Primate Evolution, vol. 1 (ed. Else JG, Lee
PC), pp. 249–264. Cambridge: Cambridge University Press.
R MJ (1991) The ontogeny of cranial sexual dimorphism in
two Old World monkeys: Macaca fascicularis (Cercopithecinae)
and Nasalis larvatus (Colobinae). International Journal of
Primatology 12, 403–426.
R HE, Z GK, P V (1982) Maxillary sinus
development in patients with cleft palates as compared to those
with normal palates. Laryngoscope 92, 183–187.
R H (1928) Die Beziehungen der Zahnkeime und Zahnwurzeln
zur Oberkieferho$ hle wa$ hrend des Kindesalters. Zeitschrift fuX rAnatomie und Entwicklungsgeschichte 85, 734–761.
S JP (1910) The sinus maxillaris and its relations in the
embryo, child, and adult man. American Journal of Anatomy 10,
313–368.
S JP (1920) The Nose, Paranasal Sinuses, Nasolacrymal
Passageways, and Olfactory Organ in Man. Philadelphia: P.
Blakiston.
S$ O (1906) Ueber die Beziehugen der Gro$ ssenvariationen
der Highmorsho$ hlen zum individuellen Scha$ delbau und
deren praktische Bedeutung fu$ r die Therapie der
Kieferho$ hleneiterungen. Archiv fuX r Laryngologie 18, 229–257.
S GH, H HJ, F$ R (1972) Zur Anatomie
der menschlichen Nasennebenho$ hlen. 2. Mitteilung. Volumetrie.
Anatomischer Anzeiger 130, 143–157.
S O (1891) U> ber die Nasenho$ hle der ho$ heren Sa$ ugethiere
und des Menschen. Gegenbaurs Morphologisches Jahrbuch 17,
44–99.
S BT (1986) Ontogenetic approaches to sexual dimorphism in
anthropoids. Human Evolution 1, 97–110.
S FA, B JL, B JH (1995) Evolution of body
size in the woodrat over the past 25,000 years of climate change.
Science 270, 2012–2014.
S GH (1980) Applied anatomy of the maxillary sinus.
Journal of the Canadian Dental Association 6, 381–386.
T R (1983) The formation of the human paranasal
sinuses. Acta Oto-Laryngologica (Suppl. 408), 1–28.
U AS (1910) An inquiry into the anatomy and pathology
of the maxillary sinus. Journal of Anatomy and Physiology 14,
354–369.
W SC, J DC, C Y (1982) Subocclusal mor-
phology and alveolar process relationships of hominid gnathic
elements from the Hadar formation: 1974–1977 collections.
American Journal of Physical Anthropology 57, 605–630.
W SC, P DR (1983) Maxillofacial morphology of
miocene hominoids from Africa and Indo-pakistan. In New
Interpretations of Ape and Human Ancestory (ed. Cichion RL,
Corruccini RS), pp. 211–238. New York: Plenum Press.
W SC, B B (1986) The facial skeleton of Sicapithecus
indicus. In Comparative Primate Biology, vol. 1 (ed. Swindler
DR, Erwin J), pp. 413–452. New York: Alan R. Liss.
W RN (1936) Sonderbildungen der Kieferho$ hle bei
Anthropoiden. Anatomischer Anzeiger 83, 161–193.
W F (1924) U> ber pneumatische Nebenra$ ume des
Kopfes. Ein Beitrag zur Kenntnis des Bauprinzips der Knochen,
des Scha$ dels und des Ko$ rpers. (Knochenstudien: III. Teil).
Zeitschrift fuX r Anatomie und Entwicklungsgeschichte 72, 55–93.
W G, A W, K F (1993) Development of the
paranasal sinuses in children: implications for paranasal sinus
surgery. Annals of Otology, Rhinology and Laryngology 102,
705–711.
Z ML, B FL, L BL (1992) Ontogeny of
integrated skull growth in the cotton rat Sigmodon fulviventer.
Evolution 46, 1164–1180.
Z W, K S (1996) Brain cooling—anatomical considera-
tions. Anatomy and Embryology 193, 1–13.