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


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.


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


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


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


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


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


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

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