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The Maxillary Sinus in Three Genera of New World MonkeysFactors That Constrain Secondary Pneumatization.

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THE ANATOMICAL RECORD 293:91–107 (2010)
The Maxillary Sinus in Three Genera of
New World Monkeys: Factors That
Constrain Secondary Pneumatization
School of Physical Therapy, Slippery Rock University, Slippery Rock, Pennsylvania
Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Anthropology, SUNY Stony Brook, Stony Brook, New York
Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
Department of Oral Biology, University of Pittsburgh, Pittsburgh, Pennsylvania
Aquatic and Physical Rehabilitation Center/Health Campus, Lancaster General Hospital,
Lancaster, Pennsylvania
Cleveland Metroparks Zoo, Cleveland, Ohio
The air filled cavities of paranasal sinuses are thought by some to
appear opportunistically in spatial ‘‘gaps’’ within the craniofacial complex.
Anthropoid primates provide excellent natural experiments for testing
this model, since not all species possess a full complement of paranasal
sinuses. In this study, two genera of monkeys (Saguinus and Cebuella)
which form maxillary sinuses (MS) as adults were compared to squirrel
monkeys (Saimiri spp.), in which a MS does not form. Using microCT
and histomorphometric methods, the spatial position of paranasal spaces
was assessed and size of the adjacent dental sacs was measured. In
Saguinus, secondary pneumatization is underway perinatally, and the
sinus extends alongside deciduous premolars (dp). The MS overlaps all
permanent molars in the adult. In Saimiri, the homologous space (maxillary recess) extends no farther posterior than the first deciduous premolar at birth and extends no farther than the last premolar in the adult.
Differences in dental size and position may account for this finding. For
example, Saimiri has significantly larger relative dp volumes, and
enlarged orbits, which encroach on the internasal space to a greater
degree when compared to Saguinus. These factors limit space for posterior expansion of the maxillary recess. These findings support the hypothesis that secondary pneumatization is a novel, opportunistic growth
mechanism that removes ‘‘unneeded’’ bone. Moreover, paranasal spaces
occur in association with semiautonomous skeletal elements that border
more than one functional matrix, and the spatial dynamics of these units
can act as a constraint on pneumatic expansion of paranasal spaces. Anat
C 2009 Wiley-Liss, Inc.
Rec, 293:91–107, 2010. V
Key words: craniofacial; nasal cavity; paranasal; pneumatization; primate
Grant sponsor: National Science Foundation; Grant numbers:
BCS-0820751, BCS-0610514.
*Correspondence to: Timothy D. Smith, PhD, School of Physical Therapy, Slippery Rock University, Slippery Rock, PA 16057.
Fax: 724-738-2113. E-mail:
Received 8 May 2009; Accepted 23 July 2009
DOI 10.1002/ar.21017
Published online in Wiley InterScience (www.interscience.wiley.
TABLE 1. Age and sexes of the sample under study
Specimen number
USNM #306848
MM105 (SG1)
Saguinus oedipus
Saguinus oedipus
Saguinus oedipus
Saguinus oedipus
Saguinus oedipus
Saguinus oedipus
Saguinus geoffroyi
Saguinus geoffroyi
Saguinus geoffroyi
Saguinus geoffroyi
Saimiri boliviensis
Saimiri boliviensis
Saimiri boliviensis
Saimiri boliviensis
Saimiri boliviensis
Saimiri boliviensis
Saimiri boliviensis
Saimiri sciureus
Cebuella pygmaea
Cebuella pygmaea
Cebuella pygmaea
Adult (3.5 years)
Infant (1 month, 23 days)
Perinatal (stillborn)
Perinatal (stillborn)
Perinatal (P0)
Perinatal (P0)
Perinatal (P10)
Perinatal (P0)
Perinatal (P0)
Adult (1 year, 1 month)
Infant (one month, 11 days)
serial sections (every 10th–20th section) of these specimens may be viewed as movie files
at or at
TABLE 2. Quantitative results on perinatal primates
PNI: dp4
Species (N)
Mean SEM
Mean SEM
Mean SEM
Mean SEM
Mean SEM
Mean SEM
Saguinus oedipus (4)
Saimiri boliviensis (6)
Cebuella pygmaea (1)
0.123 0.008
0.145 0.004
0.072 0.008
0.112 0.005
0.034 0.002
0.032 0.001
0.019 0.002
0.025 0.002
1.56 0.033
1.34 0.085
1.54 0.034
1.35 0.040
PNI, palatonasal index; SEM, standard error of the mean; ?, cranial length was unavailable for this specimen.
All ratios calculated as cube root of dental sac volume relative to palatal or cranial length.
Paranasal sinuses are mucosa-lined, air-filled sacs
that are associated with intracranial cavities. The function or biological role of the paranasal sinuses has been
a subject of investigation for centuries (Blanton and
Biggs, 1969; Rae and Koppe, 2004). Although no consensus has been reached, a recent flurry of research, fueled
in part by the availability of noninvasive imaging methods, has renewed progress (see Rae and Koppe, 2004).
Recent attempts to explain paranasal sinus function
can be crudely divided into ‘‘physiological’’ versus ‘‘structural’’ or ‘‘architectural’’ hypotheses (Rae and Koppe,
2004; Márquez and Laitman, 2008a). The latter have
fared particularly badly in recent years, but this may
be partly due to the difficulty of devising valid tests. The
notion that sinuses play an architectural or structural
role rather than performing an active physiological function has been espoused many times (Proetz, 1922; Weidenreich, 1924; Moss and Young, 1960), but the precise
meaning of the proposition is not always clear. For
example, the sinus spaces may develop as an incidental
byproduct of cranial growth, or they may actually play a
more active role in facilitating the growth. In either
case, the proposed structural role of the sinuses relates
to the growth of the skull, and attempts to test it with
recourse to adult morphology may be at a disadvantage.
Recent inferences on the relationship between paranasal sinuses and primate craniofacial form have been
drawn mainly from comparative samples of adults
(Koppe et al., 1999b; Rae and Koppe, 2000), while only a
few postnatal growth studies have been conducted
(Koppe et al., 1995, 1999c; Koppe and Nagai, 1997; Rossie, 2006). Because the ‘‘structural’’ or ‘‘architectural’’
hypotheses are explicitly developmental, it is necessary
to improve our understanding of sinus formation within
the context of the developing cranium. A thorough documentation of this relationship requires study of the cranium from the earliest phases of sinus growth, that is,
when the sinuses first expand beyond the limits of the
nasal capsule (i.e., secondary pneumatization). This
time-frame is well documented in humans, where secondary pneumatization begins prenatally, in the maxillary sinus (Sperber, 2000). Its onset marks the
beginning of an exponential increase in sinus cavity volume (Koppe et al., 1994; Smith et al., 1997, 1999). Moreover, studies of human fetuses with cartilaginous
dysmorphologies, such as in cleft lip and palate, clearly
Fig. 1. Anteroposterior position of the maxillary sinus in the tamarin
(Saguinus geoffroyi) at three ages. The graphs are standardized with a
start point at the anterior end of the deciduous or permanent canine
and end at the posterior limit of M1. Light blue indicates the portion of
the sinus that opens into the nasal fossa; dark blue indicates levels at
which the sinus is an enclosed sac. Note that in the fetal specimen,
the sinus was completely surrounded inferolaterally by cartilage (see
Smith et al., 2008). Thus, the sinus in this specimen has not undergone secondary pneumatization.
illustrate that neighboring elements affect at least sinus
symmetry in these early stages (Smith et al., 1997). Prenatally, sinuses develop ‘‘within the constraints of adjacent growing tissues’’ that may influence their shape
(Smith et al., 1997, p 488).
With few exceptions (Rossie, 2006; Smith et al., 2008)
it is uncertain how much of the time frame of secondary
pneumatization has been captured in previous studies on
nonhuman primates. Thus, a comparative perspective on
this formative stage of sinus development may be lacking. This is particularly true for the most precocious paranasal space, the maxillary sinus. Indeed, growth studies
of the maxillary sinus in macaques have assessed development beginning at the emergence of the first permanent molar (M1; Koppe and Nagai, 1997; Koppe et al.,
1999c), which could be far too late to assess influences on
the sinus by growth of neighboring structures.
Using a comparative sample of nonhuman primates,
our ultimate aim is to illuminate the dynamic spatial
Fig. 2. Drawings based on computer three-dimensional reconstructions of the teeth (blue) and the sinus mucosa (beige) of three specimens of the tamarin (Saguinus geoffroyi) at different ages (the
perinatal specimen is a different individual than that shown graphically
in Fig. 1). Structures are seen on their medial surface. Dental sacs are
illustrated for fetal and perinatal specimens. In the 53-day old, a mixed
set of erupted teeth and dental sacs are illustrated.
relationships among the sinuses and the other functional
units of the skull (e.g., orbital contents, dentition, oral
cavity, brain). In the present study, we take a first step
in this direction by investigating the spatial relationship
between the developing dentition and maxillary recess
and sinus in three monkey genera. The specific aims of
the present study are twofold. First, the development of
paranasal spaces from fetal (Saguinus) or perinatal
(Cebuella, Saguinus, Saimiri) to adults stages is compared among two genera that do undergo pneumatization of the maxillary bone (Saguinus, Cebuella) and one
that does not (Saimiri). Second, a perinatal sample of
two species of primates is used to test the hypothesis
Fig. 3. Anteroposterior position of the maxillary sinus in the tamarin
(Saguinus oedipus) and maxillary recess in the squirrel monkey (Saimiri
boliviensis) at perinatal and adult ages. Spatial overlap with dentition
is emphasized. The graphs are standardized with a start point at the
anterior end of the deciduous or permanent canine and end at the
posterior limit of M1. Note that the sinus continues beyond the posterior end of M1 in the adult tamarin (see text). Light blue indicates the
portion that opens into the nasal fossa; dark blue indicates levels at
which the sinus or recess is an enclosed sac.
that size and position of the deciduous dentition explains
the magnitude of paranasal pneumatization.
males and females of each genus were acquired. However, only male perinatal Saimiri (and one of unknown
sex) were available for study. As adults of the genus Saimiri are described to have only minimal dimorphism
(Corner and Richtsmeier, 1992) it is not expected that
Saimiri boliviensis is dimorphic at birth.
Excluding the fetal Saguinus, the earliest aged specimens represent a mix of body sizes. They are not all
assumed to be neonatal in stage of somatic maturity,
and likely represent a mix of premature and early postnatal stages (thus, these are referred to as the ‘‘perinatal’’ sample). Perinatal specimens of known age died at
P0 except one of the Saimiri boliviensis, which died at
P10. As this specimen fell within the length range of
both the cranium and palate of P0 specimens, it was
treated as part of the perinatal sample. The 1-month-old
Cebuella and 53-day-old Saguinus are referred to as
‘‘infants’’ throughout the text.
Eight of the perinatal specimens (4 Saimiri boliviensis; 4 Saguinus oedipus) were scanned using micro CT
(19 lm voxel size; VivaCT40 scanner, Scanco Medical).
High resolution X-ray and CT scans of two adult monkeys (previously acquired by Rossie, 2006) were also analyzed. Fetuses, perinatal specimens, infants, and two
adults were dissected and processed for paraffin embedding. Before embedding, cranial length (prosthion-inion)
and palatal length (prosthion-posterior mid-palatal
point) were measured with digital calipers to the nearest
0.01 mm. Paraffin blocks were serially sectioned at 10–
12 lm and stained with hematoxylin-eosin and Gomori
trichrome procedures for histomorphometric analysis
using Scion Image or ImageJ software (NIH). All heads
were sectioned in the coronal plane except one of each
In this study, three genera of New World primates
were examined. In two of these genera, Saguinus and
Cebuella, a maxillary sinus is present postnatally (Nishimura et al., 2005; Rossie, 2006). In the third, Saimiri,
no secondary pneumatization occurs, and no maxillary
sinus develops (Rossie, 2006). Twenty-one specimens
were studied (Table 1), including 10 tamarins (Saguinus
geoffroyi: 1 fetal, 2 perinatal, 1 53-day old; S. oedipus: 4
perinatal; 2 adults); three pygmy marmosets (Cebuella
pygmaea: 1 perinatal, 1 one-month old, 1 adult); eight
squirrel monkeys (Saimiri boliviensis: 6 perinatal, 1
adult; Saimiri sciureus: 1 adult). The fetal Saguinus
geoffroyi was previously estimated to be in a fetal stage
based on body size relative to ‘‘perinatal’’ specimens (see
below) and based on maturation of the nasal capsule
(Smith et al., 2008). Other subadult specimens ranged
from P0 to P53 in age.
Except for two skeletal specimens [Table 1, United
States National Museum(USNM)], all specimens were
acquired from cadaveric remains preserved in 10% formalin. The ‘‘perinatal’’ sample included animals that
were stillborn or died within 10 days of birth in captivity
at the New England Primate Center, the University of
South Alabama Primate Research Center, or the Cleveland Metroparks zoo. Two adult cadaveric heads were
acquired after the animals were euthanized at the New
England Primate Center and the University of South
Alabama Primate Research Center. When possible, both
genus. In the latter specimens, half the head was sectioned coronally while the contralateral head was sectioned in the sagittal plane. Every 10th section, at least,
was mounted on glass slides with serial numbers for
staining. Intervening sections were saved for future histochemical and immunohistochemical analysis.
The perinatal sample of Saguinus and Saimiri was
analyzed in two dental regions regarding palatal, nasal,
and dental variables (Table 2). Following Rossie’s (2006)
analysis of adult monkeys, we selected the mid-level of
dp4 to measure variables related to palatal and nasal
cavity breadth. These variables were also measured at
M1, as the maxillary sinus extends beyond this in postnatal Saguinus (Rossie, 2006). To acquire data, each
stained section in the regions from dp4 to M1 was photographed using a Leica DMLB microscope and Cat-Eye
digital camera. Measurements were then taken from digital micrographs of histological sections using ImageJ
software (NIH). First, palatonasal index was measured.
As per Rossie (2006), nasal width was measured as the
distance between the right and left sides of lateral nasal
wall at the base of the nasal fossa (at P4 this corresponds to the wall of the inferior meatus). As the medial
margin of alveolar bone was difficult to isolate from the
palatine process of the maxillary bone in perinatal animals, alternative landmarks were used: the medial margin of the right and left dental follicles. The distance
between right and left sides was measured as palatal
width. Average palatonasal indices for each species were
calculated as interdental width/nasal width. In specimens where only half of the face was sectioned in the
coronal plane, the ratio was calculated by measuring distances from the dental sac or lateral limit of the nasal
fossa to the midline (using the center of the vomer as
the midline).
Using ImageJ software, dental sac volumes were
measured for dp4 and M1 on the right side of the nasal
fossa, except in two specimens where dp4 or M1 were
damaged. Among specimens in which right and left sides
were both well-preserved for measurement, asymmetry
was not biased toward one side (in about half of the
specimens the right dental sacs were larger, and in the
other half the left sacs were larger). Therefore, the left
side was used for analysis in the two specimens where
the right side was damaged. Volumes were acquired by
tracing the cross-sectional area of the dental sac as estimated by the outer edge of the outer enamel epithelium.
Once all sections containing a cross-section of the tooth
were measured, the cross-sectional areas in mm2 were
multiplied by the distance between sections for a segmental volume of the tooth. This was repeated for each
section of the tooth up to the penultimate section (the
last section containing the tooth was regarded as the
end). Then, all segmental volumes were summed to
obtain total volume of the tooth. The cube root of these
tooth volumes was divided by palatal and cranial lengths
to obtain relative size of the dp4 and M1 (Table 2).
In Saguinus oedipus and Saimiri boliviensis, one perinatal and one adult specimen of each species was
selected for measurement of the mucosal surface area
(mm2) in the nasal and paranasal spaces. Using ImageJ
software, the data were obtained by tracing the perimeter of the nasal fossa and paranasal spaces in each section beginning at the first coronal section in which the
right nasal fossa was enclosed, and ending at the
Fig. 4. Anteroposterior position of the maxillary sinus in the pygmy
marmoset (Cebuella pygmaea) at three ages. The graphs are standardized with a start point at the anterior end of the deciduous or permanent canine and end at the posterior limit of M1. Light blue indicates
the portion of the sinus that opens into the nasal fossa; dark blue indicates levels at which the sinus is an enclosed sac.
choana. A linear distance was obtained in mm, and this
was multiplied by the distance between sections to
obtain a segmental surface area. Segmental surface
areas were summed to estimate total surface areas for
nasal and paranasal mucosa. These data were used for a
preliminary evaluation of age related changes in these
dimensions in the two species.
SPSS 15.0 (SPSS) was used to analyze the data. Data
were compared between groups using a Mann-Whitney
U test. All differences were considered significant at P 0.05.
Position of the Maxillary Sinus Relative to
Dentition in Fetal and Early Postnatal
Geoffroy’s Tamarins (Saguinus geoffroyi)
The anteroposterior spatial relationship of the maxillary sinus to the dentition in Saguinus geoffroyi is
shown in Figs. 1, 2. In the fetal specimen the primordial
Fig. 5. The position of the maxillary sinus or recess (open arrows)
is shown in three perinatal primates. Each plate shows the approximate anteroposterior mid-level of a tooth in the coronal plane. In the
tamarin (Saguinus oedipus; 5a–c), the sinus cavity completely overlaps
dp3 and is found between the tooth and nasal fossa (NF) at this level.
The sinus ends before the mid-point of dp4. Note the relatively small
size of M1. In the pygmy marmoset (Cebuella pygmaea; 5d–f), a rela-
tively small sinus is found superomedial to dp3 (add arrow) and does
not overlap dp4. Note the close proximity of dp4 to the NF in the marmoset compared to the tamarin. In the squirrel monkey (Saimiri boliviensis; 5g–i), the maxillary recess does not reach the anteroposterior
midpoint of dp3. Note the relatively large size of the dentition in the
squirrel monkey, and close proximity to the nasal fossa. Or, orbit.
Scale bars ¼ 1 mm.
maxillary sinus runs the mesiodistal length of dp2 and
most of the length of dp3 (Figs. 1, 2). In the perinatal
S. geoffroyi, the maxillary sinus extends posteriorly to
overlap all of dp2 and dp3 and a portion of dp4 (Figs. 1,
2). The MS extends over more than one-half the length
of dp4 in the 53-day-old S. geoffroyi (Figs. 1, 2).
In dorsoventral space, the primordial maxillary sinus
is well separated from the developing dental sacs in the
fetus (Fig. 2). In the perinatal S. geoffroyi the mucosal
lining of the maxillary sinus is dorsoventrally larger and
is more closely adjacent to the deciduous premolars,
though this is largely due to the growth of the teeth. In
the 53-day old, the maxillary sinus is positioned medial
to dp2 and dp3, and overlaps a portion of dp4 (Fig. 2).
The roots of the deciduous premolars lie lateral to the
maxillary sinus once they develop.
most of the ensuing text. Figures 3–7 show the position of
the maxillary sinus, specifically the mucosal sac, relative
to dental level in Saguinus, Cebuella, and Saimiri at different postnatal ages. In all species, the maxillary sinus
or recess overlaps more posterior teeth in adults than in
perinatal specimens (Figs. 3, 4). The most extreme posterior expansion of the sinus relative to the teeth is in the
adult Saguinus, where the sinus completely overlaps M1
(Fig. 3; the sinus actually extends posterior to M1). In
Cebuella and Saimiri, the sinus/recess does not extend
beyond the level of P4 in adults. However, in Cebuella the
sinus extends more anteriorly compared to the recess of
the adult Saimiri (Figs. 3, 4). In all species, the anterior
limit of the maxillary sinus or recess shifts posteriorly
relative to the maxillary tooth row in adults compared to
perinatal specimens (Figs. 3, 4).
In perinatal specimens, the anterior part of the sinus or
recess is open to the middle meatus via an ostium. Posteriorly, the mucosal sac of the sinus or recess is an enclosed
cul-de-sac. In adults, an enclosed portion of the sinus or
recess also extends anterior to the ostium (Figs. 3, 4).
Figure 5 shows the nasal fossa at coronal mid-levels of
deciduous premolars and M1 in perinatal specimens.
Saguinus is distinguished by a broad separation of the
dental sacs from the nasal fossa and by a comparatively
Perinatal and Postnatal Position of the
Maxillary Sinus or Recess Relative to Dentition
in the Tamarin (Saguinus), Pygmy Marmoset
(Cebuella), and Squirrel Monkey (Saimiri)
As the findings on the position of the sinus or recess
were similar within genera, the genus alone is used in
Fig. 6. The position of the maxillary sinus (open arrows) is shown in
two infant monkeys. Each plate shows the approximate anteroposterior mid-level of a tooth in the coronal plane. In the tamarin (Saguinus
geoffroyi; 6a–c), the sinus cavity overlaps dp4 but does not extend
alongside M1 (see Fig. 1). Note the dorsoventrally expansive sinus
cavity adjacent to dp3. In the pygmy marmoset (Cebuella pygmaea;
6d–f), a relatively small sinus is found superomedial to dp3 and overlaps most of dp4. Note the relatively large size of M1 and it close
adjacency to the nasal fossa. NF, nasal fossa; Or, orbit; double arrows,
dental sacs of permanent teeth. Scale bars ¼ 1 mm.
diminutive M1. Cebuella possesses larger dp4 and M1
compared to dp3 (Fig. 5d–f). In Saimiri, all dental sacs
are cross-sectionally large and closely approximated to
the nasal fossa (Fig. 5g–i). In both Saguinus and
Cebuella, the sinus is directly adjacent to or posterior to
the mid-point of dp3, whereas in Saimiri the maxillary
recess ends anterior to this level (Fig. 5). The cul-de-sac
of the sinus ends at or anterior to the mid-point of dp4
in Saguinus, and does not overlap dp4 at all in the perinatal Cebuella under study (Figs. 3–5).
The 53-day-old Saguinus geoffroyi and 1-month-old
Cebuella reveal positional differences of the sinus compared to perinatal specimens (Figs. 1, 4, 6). In both species, the sinus extends to partially overlap dp4. A
prominent difference between the infant primates is
observed in terms of the secondary dentition. In Saguinus the dental sacs of I1, I2, and the permanent canine
are prominently visible (Fig. 2) whereas postcanine teeth
(not shown) are relatively small and undifferentiated,
without a clear enamel organ. In the 1-month-old
Cebuella, posterior permanent premolars at the cap
stage are prominently positioned adjacent to the maxillary sinus (Fig. 6).
In the adult Saguinus, the mucosal boundaries of the
maxillary sinus or recess completely overlap (and pass
posterior to) M1 (Figs. 3, 7). In the adult Cebuella and
Saimiri, the sinus/recess completely overlaps P4 but
does not reach the level of M1 (Figs. 3, 4, 7). The mucosal boundaries of the maxillary sinus in Saguinus and
maxillary recess in Saimiri are shown at higher
Fig. 7. The position of the maxillary sinus or recess (open arrows)
is shown in three adult primates. Each plate shows the approximate
anteroposterior mid-level of a tooth in the coronal plane. In the tamarin (Saguinus oedipus; 7a–c), the sinus overlaps all permanent premolars and molars in anteroposterior space. Note the relatively greater
magnitude of inferior expansion of the sinus at P3 in Saguinus com-
pared to Cebuella (7d–f). The sinus of Cebuella overlaps P4, but does
not extend alongside M1 (see Fig. 4). In the squirrel monkey (Saimiri
boliviensis; 7g–i), the maxillary recess overlaps P3 and P4. The recess
is an enclosed sac posteriorly, but is separated from the nasal fossa
by mucosa, not bone. NF, nasal fossa; Or, orbit. Scale bars ¼ 1 mm.
magnification in Fig. 8. In each, there is an enclosed mucosal pocket anterior to the ostium. Medially, this region
is enclosed by bone in Saguinus (Fig. 8a) but is bounded
by mucosa alone in Saimiri (Fig. 8d). The ostium opens
into the middle meatus in both monkeys (Fig. 8b,e). The
posterior extension of the maxillary sinus in Saguinus is
medially bordered by bone. In Saimiri the enclosed posterior portion of the mucosal sac is bordered medially by
mucosa alone (Fig. 8f).
The position of the sinus or recess cavity is emphasized in Fig. 10b,d. In each monkey the cavity of the
sinus or recess is wedged between the orbit and deciduous premolars. Fig. 11a–b shows the maxillary sinus
extending ventral to the orbit in Saguinus. The deciduous premolars are positioned lateral to the sinus
(Fig. 11c). In Saimiri, the maxillary recess is more restricted to the region anterior to dp3 (Fig. 11d,e). Figure
11f emphasizes the extreme proximity of the relatively
large orbit and posterior maxillary teeth (dp3-M1) in
Saimiri (also see Fig. 10d).
Figure 12 shows the position of the maxillary sinus or
recess in an adult Saguinus oedipus and Saimiri sciureus relative to the orbit and dentition. The spatial relationship of the paranasal cavities to the maxillary
dentition agrees with results based on histology (Fig. 3).
The maxillary sinus of Saguinus lies medial to all teeth
from P2 to M2 (Fig. 12a–e), whereas the maxillary
recess lies medial to only P3 and P4 in Saimiri
(Fig. 12g,h).
In both adult monkeys, the orbits are highly approximated and encroach on the dorsal part of the nasal fossa
at posterior levels (Fig. 12c–e,h–j). Figure 12c,h emphasize the relatively broader palate in Saguinus (as discussed by Rossie, 2006). This disparity is equally
pronounced at M1 (Fig. 12d,i). The proximity of the orbit
Interrelationship of the Orbit, Nasal Fossa, and
Dentition in Tamarins (Saguinus) and Squirrel
Monkeys (Saimiri)
Figures 9–11 show the spatial relationship of the orbit,
nasal fossae, and dentition relative to the maxillary
sinus or recess in perinatal Saguinus and Saimiri.
Based on three-dimensional reconstructions in the frontal view, inter-orbital distance is relatively wider in
Saguinus at all maxillary tooth levels. In both primates,
the orbits encroach on the superior portion of the nasal
fossa, especially at posterior levels (Figs. 9, 10a,b). The
palate appears proportionally wider relative to bizygomatic width at all levels in Saguinus (Fig. 9). The orbits
appear to be more convergent in Saimiri compared to
Saguinus (Fig. 10a,c).
significant difference at the level of M1 (P < 0.05) but
not at the level of dp4 (P > 0.05).
Age comparisons of mucosal surface areas between
individual adult and perinatal specimens indicate
marked species differences. In a perinatal Saguinus,
total nasal fossa area measures 78.12 mm2, and the
maxillary sinus is 9.81 mm2 in surface area. Total nasal
fossa surface area in the adult Saguinus is 336.7 mm2.
For this specimen, the maxillary sinus measures 66.85
mm2, and the frontal sinus surface area is 51.98 mm2.
In a perinatal Saimiri, total nasal fossa area is 160.11
mm2, and the maxillary recess mucosal surface area
measures 2.12 mm2 in surface area. In the adult Saimiri, the nasal fossa area is 530.0 mm2, and the maxillary recess is 9.74 mm2. An age/species comparison of
internal nasal surface area (nasal fossa and sinus or
recess areas), expressed in percentages, is shown in
Fig. 14. Compared to the perinatal specimen, sinus area
in the adult Saguinus comprises 15% more mucosal
area. In contrast, the percentage surface area of the
maxillary recess is nearly equal when comparing adult
and perinatal Saimiri.
Fig. 8. The mucosal boundaries of the maxillary sinus in the tamarin (Saguinus Oedipus; 8a–c) and the maxillary recess in the squirrel
monkey (Saimiri boliviensis; 8d–f). In Saguinus, the sinus is enclosed
by bone anterior to the ostium (8a). The ostium is shown in 8b. Posteriorly, the sinus is enclosed by bone (8c). In Saimiri, although there are
enclosed portions of the recess anterior (8d) and posterior (8f) to the
ostium (8e), these regions are not enclosed medially by bone. IM, inferior meatus; NA, nasal airway; Or, orbit; double arrows, medial bony
wall of maxillary sinus. Scale bars: a, c, d, f ¼ 0.5 mm, b, d ¼ 1 mm.
to the maxillary teeth and hard palate is greater in
Saimiri compared to Saguinus (Fig. 12a–j).
Quantitative Results
Relative to palatal length, dp4 and M1 are larger in
Saimiri and Cebuella compared to Saguinus (Fig. 13;
Table 2). MannWhitney U tests show that the ratio of
cube root of tooth volumes to palatal length is significantly different between species for both dp4 (P < 0.05)
and M1 (P < 0.05). In both cases, Saimiri has significantly larger dental volume relative to palatal length.
Relative to cranial length, dp4 is not significantly different between species (P > 0.05), but M1 was significantly
(P < 0.05) larger in Saimiri.
Palatonasal indices are lower in Saimiri at both dp4
and M1 levels (Fig. 13). Mann Whitney U tests reveal a
Debates concerning the function of the sinuses have
yielded little consensus (e.g., Koppe et al., 1999a; Preuschoft et al., 2002; Rae and Koppe, 2008). Several
authors have suggested an alternative explanation for
paranasal sinuses which treats the sinus cavities as
‘‘spandrels,’’ or by-products of craniofacial growth processes (Rae and Koppe, 2008; Zollikofer and Weissman,
2008). Such a concept has roots in Weidenreich’s view
that sinuses have an ‘‘architektonisch und funktionell
passiven Charakter’’ (1924, p 91). Zollikofer and Wiessman (2008) pair the spandrel hypothesis with the ‘‘invasive tissue hypothesis.’’ The latter hypothesis invokes
properties of the mucosal lining of sinus cavities as an
explanation for their expansion, and relates to Witmer’s
(1997) conception of sinus expansion as an ‘‘opportunistic’’ process. The invasive tissue hypothesis pairs equally
well with the notion that the growth of the sinuses
actually aids in the growth of the skull (e.g., Proetz,
1922), and this might begin to address the reason for
the expansive tendencies of the sinus mucosa.
As secondary pneumatization is a prolonged process
spanning prenatal and postnatal periods; the exploration
of these concepts demands examination of a broad age
range. To that end, the present study explores the spatial relationships of paranasal maxillary spaces within
the midface in a sample that spans prenatal and postnatal stages. Recently, it was demonstrated that in
Saguinus geoffroyi, the onset of secondary pneumatization is a perinatal event (Smith et al., 2008). Thus, our
study centers on the earliest formative stages of a ‘‘true’’
sinus in at least one genus. Cartilaginous remnants
observed in all perinatal specimens suggest that capsule
breakdown is occurring at this time in other marmosets
and tamarins as well (Smith et al., 2005; unpublished
Computer modeling supports the view that sinus form
is largely dictated by the form of the space available for
pneumatization (Zollikofer and Weissman, 2008).
Although individual cranial bones are pneumatized by
sinus cavities, these bones are formed from ossification
Fig. 9. Micro CT reconstruction of the perinatal tamarin (Saguinus oedipus) and squirrel monkey (Saimiri boliviensis) at different dental levels in a frontal view. The position of the sinus or recess cavity is indicated (red arrows). Top: inferior view of the specimens with dental levels indicated. Scale bars ¼ 1 mm.
centers that abut more than one craniofacial region,
such as soft tissue (‘‘functional’’) matrices, dental follicles, or the developing sinus itself (Fig. 15; Moss and
Young, 1960; Moss and Greenberg, 1967). The potential
influence of neighboring elements on the maxillary sinus
or recess is assessed and discussed below.
Patterns of Pneumatic Expansion
Current researchers appear to agree on the definition
of a paranasal sinus (Witmer, 1999; Rae and Koppe,
2000; Rossie, 2006). The identification of sinuses can be
complicated by the presence of recesses that may persist
Fig. 10. Micro CT reconstruction of the perinatal tamarin (Saguinus
oedipus) and squirrel monkey (Saimiri boliviensis) from a superior perspective (a,c) and a posterior-oblique view (b,d). The position of the
sinus or recess cavity is indicated (arrows). Top: inferior view of the
specimens with dental levels indicated. ET1, first ethmoturbinal; N,
nasal bone; NC, nasal cavity; V, vomer bone; Z, zygomatic bone.
Scale bars ¼ 1 mm.
even in absence of secondary pneumatization. Thus, the
very definition of a sinus is critical (Rae et al., 2003;
Rossie, 2006). ‘‘Recesses’’ of the nasal cavity are most
clearly defined prenatally, when they are still encapsulated by nasal capsule cartilage (much of which later
ossifies into the ethmoid). ‘‘True’’ paranasal sinuses form
by an invasive process wherein mucosa-lined recesses of
the nasal fossae escape the confines of these recesses
and expand within the body of the maxillary, palatine,
ethmoid, frontal, or sphenoid bones (Witmer, 1999). This
expansion is termed secondary pneumatization, in contrast to primary pneumatization. The latter is an unfortunate misnomer referring to the formation of recesses
via growth and folding of prenatal cartilaginous walls of
the nasal cavity (e.g., recessus maxillaris).
Primates that lack maxillary sinuses postnatally, such
as most cercopithecoids, nonetheless possess the natal
maxillary recess (Maier, 2000). The failure of secondary
pneumatization to occur results in the absence of a paranasal cavity outside the limits of the nasal capsule. This
is also the case in at least two New World monkeys,
including Saimiri (Rossie, 2006). The posterior portion of
the maxillary recess in Saimiri is separated from the
nasal cavity by mucosa alone. This mucosal sac also
typifies the primordial maxillary sinus of other taxa
prior to pneumatization, after which it is mostly
enclosed by bone (Fig. 1; Smith et al., 2008).
Preliminary data on internal nasal surface areas provided herein, if typical for the species, emphasizes the
different magnitude of growth in paranasal spaces that
do pneumatize versus those that do not. The proportional difference in sinus mucosal area between the perinatal and adult Saguinus is striking, especially when
compared to the same age comparison in Saimiri. In the
latter, preliminary data (Fig. 14) suggest that the mucosa of the maxillary recess simply follows a growth
Fig. 11. Parasagittal sections of the nasal fossa of a perinatal tamarin (S. oedipus) and squirrel monkey (Saimiri boliviensis). Insets are
the contralateral side of the head, sectioned in the coronal plane. The
position of the maxillary sinus or recess (red arrows) is indicated.
Three different cross-sectional levels are shown. At the top (a,d) the
parasagittal plane which crosses the middle of the sinus or recess
cavity at dp2 is shown. 11b and 11e show a parasagittal plane that
transects the lateral limit of the sinus (11b) and recess (11e). 11c and
11f show a parasagittal plane through the entire maxillary tooth row to
show its relationship to the orbit. The insets show the approximate
location of the parasagittal plane relative to a coronal section through
dp2. c, deciduous canine; NLD, nasolacrimal duct; Or, orbit. Scale
bars ¼ 1 mm. Serial sections (every 10th–20th section) of these specimens may be viewed as movie files at http://www.interscience.wiley.
com/jpages/1932-8486/suppmat or at
trajectory in common with the remainder of the nasal
fossa. In Saguinus, expansion of ‘‘pneumatic’’ mucosa
outpaces that of the nasal fossa.
Rossie (2006) noted the presence of diplöic bone adjacent to the maxillary recess in adult Saimiri. In this
study, such bone is seen posterior to the enclosed mucosal recess (e.g., Fig. 7i). Our findings support Rossie’s
hypothesis that size-related crowding by alveolar skeletal units limits potential space of pneumatization; the
maxilla of perinatal Saimiri is relatively crowded by
dental sacs compared to Saguinus (see Figs. 10, 11). A
critical question is why the diplöic bone that persists adjacent to the maxillary recess is not subject to ‘‘opportunistic’’ pneumatic expansion. Elsewhere in the cranium,
Fig. 12. CT slices, in the coronal plane, of an adult tamarin (a–e
S. oedipus) and squirrel monkey (f–j Saimiri sciureus). Cross-sectional
levels from P2 to M2 are shown. Note that the extent of the maxillary
recess cavity (open arrows) in the squirrel monkeys concurs with find-
ings on the adult Saimiri boliviensis (see Fig. 3). Similarly, the cavity of
the maxillary sinus (open arrows) in the tamarin agrees with results
seen in the serially sectioned adult (Fig. 7). Scale bars ¼ 5 mm.
diplöic bone scales positively in relation to age and body
mass in humans (Lynnerup et al., 2005; Hatipoglu et al.,
2008). These regions of bone may be physiologically or
architecturally essential in the context of dental crowding within the maxilla. It may be that there is a temporal window within which secondary pneumatization can
commence if conditions permit, and only the spatial relations during this time are relevant. In this light, it is
worth noting that the diplöic space found adjacent to the
maxillary recess in adult Saimiri specimens is occupied
by the developing permanent premolars in younger
specimens (see Fig. 9b in Rossie, 2006).
The small sample of adults and infants available in
this study indicate subtle species differences in pneumatic expansion between Saguinus and Cebuella. In
S. geoffroyi, three-dimensional reconstructions of the fetal specimen provide the initial context of sinus/dental
spatial relationships. The mucosal sac of the primordial
sinus is spatially separated from the dental follicles,
although the ostium bears the same anteroposterior
position relative to dp2. Older specimens suggest that
the sinus expands posteriorly at a greater rate than the
deciduous premolars grow in mesiodistal length. This
expansion is accompanied by a posterior displacement of
the sinus ostium, which may relate to displacement by
anterior teeth. An increase in vertical dimensions of the
sinus is evidenced in the perinatal specimen (Fig. 2). In
the infant, the sinus is expanded vertically and posteriorly relative to the deciduous premolars (Fig. 2).
Cebuella shows less evidence of early vertical expansion, by comparison. The small sample studied suggests
that mesiodistal expansion may be completed early in
postnatal ontogeny, since pneumatization does not
extend beyond P4. Cebuella, like Saguinus, has a pneumatic diverticulum that expands anterior to the level of
the ostium.
Interrelationship of Sinus and Adjacent
Midfacial Structures and Spaces
On the basis of patterns of osteoclastic activity, Smith
et al. (2005) asserted that deciduous dentition have
‘‘morphogenetic primacy’’ over the developing maxillary
sinus. In marmosets and tamarins, the alveolar wall of
the maxillary sinus drifts medially in locations where a
single plate of bone separates the sinus from deciduous
premolars. The findings of the present study are consistent with this view and strongly suggest that the
Fig. 12. (Continued from the previous page)
posterior dentition can limit the extent of posterior
pneumatization. The lack of expansion of the maxillary
recess in Saimiri coincides with the significantly larger
relative size of dp4 and M1 in these monkeys compared
to Saguinus at birth. The even larger relative size of M1
in the single perinatal specimen of a Cebuella is suggestive of the same size-related constraint as seen in
Saimiri, especially given the absence of pneumatization
beyond P4 in the older Cebuella. The wide-set palate
presumably mitigates this effect, and allows space for
pneumatic expansion anterior to M1. This emphasizes
that competing factors may dictate the course and extent
of pneumatization in a species.
The influence of these competing factors requires a
clear understanding of the position of the maxillary
sinus before secondary pneumatization. Figure 15
Fig. 14. Surface areas of the nasal mucosa, expressed as percentages, in the tamarin (Saguinus oedipus) and squirrel monkey (Saimiri
boliviensis). Note that the sinus mucosa areas in Saguinus show an
increase in proportions relative to the remainder of the nasal fossa (NF),
whereas the maxillary recess surface area of Saimiri increases isommetrically with the nasal fossa. FS, frontal sinus; MS, maxillary sinus.
Fig. 13. (a) Comparison of the ratio of cube root of dental volumes
to palatal length in the tamarin (Saguinus oedipus) and squirrel monkey (Saimiri boliviensis). (b) Comparison of the ratio of cube root of
dental volumes to cranial length in Saguinus oedipus and Saimiri boliviensis. (c) Palatonasal index interdental width/nasal width) in Saguinus
oedipus and Saimiri boliviensis.
illustrates the position of the primordium of the maxillary sinus relative to adjacent structures in a fetal
Saguinus. The primordial sinus orients in a postero-inferior direction and ends at about the level of dp3. This is
a level at which pneumatization proceeds parallel to the
palate in perinatal Saguinus (see Fig. 11a,b). In perinatal Saimiri, the orbit appears relatively larger than in
Saguinus and is more closely adjacent to the posterior
dentition (dp3-M1). This is consistent with Hartwig’s
(1995) observation that orbital approximation is extreme
in newborn and adult Saimiri, and also emphasizes that
the encroachment of the nasal and paranasal spaces by
highly convergent orbits increases posteriorly. Together,
the contents of the orbit and maxillary dentition from
dp3 to M1 conspire to limit potential for posterior extension of the maxillary recess in the perinatal period (Figs.
10d, 11e illustrate this constraint).
In summary, observations on the primates under
study support the hypothesis that the size and position
of the deciduous dentition constrains secondary pneumatization of the maxillary sinus (Smith et al., 2005).
Observations on the position of the developing dentition
relative to the nasal fossae and orbits prompt the following hypothesis that must be tested on a broader range of
primates: large relative size of the posterior maxillary
dentition, a high degree of orbital approximation, and
low palatonasal indices each act to constrain pneumatization from the maxillary recess. Examining the combination of these measurements in individual species may
afford a nuanced view of the ultimate extent of
An ontogenetic approach to such comparisons will be
beneficial to account for effects of the transient deciduous dentition. While dental constraint appears to easily
explain sinus extent at birth, the deciduous teeth are
transient elements. A noteworthy difference between the
1-month-old Cebuella and 53-day-old Saguinus is the
more advanced development of permanent premolars in
Cebuella (Fig. 6). The dental sacs for the replacement
that surround them) to the sinus during growth of the
anthropoid face. Noteworthy in this regard is the
increasing depth of the growing midface in Saimiri (Corner and Richtsmeier, 1992) which may underlie the positional change in the maxillary recess relative to the
dentition in the adult.
Fig. 15. Top: Three-dimensional reconstruction of a fetal tamarin
(Saguinus geoffroyi) in a postero-oblique view, with the septum
removed. The position of the primordial maxillary sinus (gold) before
secondary pneumatization is emphasized. Note the position of the deciduous premolars (dp) and eye relative to the sinus, which is still surrounded by an inferior scroll of the nasal capsule. Bottom: A serial
section of the same specimen, just posterior to the maxillary sinus (*,
glands at posterior limit of sinus). The cutting plane, at the posterior
end of dp3, is indicated to the left of the section. Pneumatization proceeds posteriorly between the orbit, dentition, and nasal fossa in this
species. Dc, deciduous canine; Di1, deciduous central incisor; dp2,
deciduous premolar 2 (or 1st deciduous molar); ET1, ethmoturbinal I;
F, frontal bone; M, maxilla; M1, 1st permanent molar; NA, nasal airway; OB, olfactory bulb; ONL, orbitonasal lamina; TN, tectum nasi.
Scale ¼ 1 mm.
premolars emerge lingually (e.g., Fig. 6d,e), directly adjacent to the sinus. Variation in the schedule of development of the replacement dentition in relation to
pneumaticity requires further study. An ontogenetic
approach will also be needed to assess the changing
proximity of soft tissue matrices (and the skeletal units
Rossie (2006) revealed major ontogenetic variations in
secondary pneumatization of the maxillary sinus in New
World monkeys. Our results provide a glimpse of variation beginning at the earliest formative stages of a
‘‘true’’ sinus, as compared to an unpneumatized recess.
Magnitude is the single most distinguishing aspect of
the postnatal trajectory of these paranasal spaces in
Saguinus and Cebuella compared to Saimiri. Our results
indicate that the maxillary sinus grows anteroposteriorly, and probably in surface area, at a disproportionately higher rate compared to the nasal fossa. In
contrast, the maxillary recess in Saimiri appears to
grow at a rate similar to the nasal cavity itself. These
observations support the hypothesis that secondary
pneumatization is an opportunistic growth mechanism
(Witmer, 1997) that may be constrained by adjacent elements (Smith et al., 1997, 1999, 2005). While the reasons for maxillary sinus suppression in Saimiri may be
complex, the present data strongly suggest that the size
and position of the postcanine dentition, as well as the
encroachment of the orbits play a substantial role (cf.
Rossie, 2006).
During facial morphogenesis, paranasal sinus expansion may provide a mechanism for resolving spatial
shifts among skeletal elements of the nasal capsule,
orbit, and dentition (Proetz, 1922; Shea, 1985; Enlow
and Hans, 1996; Zollikofer and Weissman, 2008). In this
view, variations in the nature of sinus expansion are
related to specific craniofacial growth patterns (Enlow
and Hans, 1996). Even if the occurrence of paranasal
sinuses is best explained by such a ‘‘structural’’ hypothesis, this does not preclude the acquisition of secondary
functions such as those affected by climate (e.g., Rae
et al., 2003; Márquez and Laitman, 2008b). If secondary
functions reshape sinuses to physiological demands,
inferences drawn from adult crania may fail to ascertain
the validity of any ‘‘structural’’ hypothesis. In other
words, if the process of pneumatization serves to remove
unneeded bone (Proetz, 1922; Weidenreich, 1924; Blaney,
1986), evidence of this is better sought during, rather
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