The Laryngoscope
C 2011 The American Laryngological,
V
Rhinological and Otological Society, Inc.
Contemporary Review
Revisiting Human Nose Anatomy: Phylogenic and Ontogenic
Perspectives
Roger Jankowski, MD
This review suggests revisiting nose anatomy by considering the ethmoidal labyrinths as part of the olfactory
nose and not as paranasal sinuses.
Phylogenetically, the olfactory and respiratory organs of the most primitive vertebrates are separated. Exaptation, a mechanism of evolution, may explain the fusion of the olfactory and respiratory organs in dipnoi. The respiratory and olfactory noses remain anatomically separated by the transverse lamina in most mammals, whose olfactory labyrinth is a blind recess housing the ethmoturbinates. In humans, the partitioning between the olfactory cleft
and the ethmoid labyrinth seems to be a consequence of ethmoid bone remodeling induced by the acquisition of an
upright posture. The ethmoid bone is derived from the cartilaginous nasal capsule of primitive vertebrates and considered to be a highly conserved region among the bony elements of the skull base. It appears to be involved only in
housing and protecting the olfactory function.
During the early stages of human fetal development, rupture of the oronasal membrane leads to the integration
of the primary olfactory sac in the future respiratory organ. The cartilaginous nasal capsule appears in the tissue
under the brain and around the olfactory channels. Its early fetal development is classically regarded as the beginning
of paranasal sinus formation. From phylogenic and ontogenic perspectives, it may be regarded as the development of
the olfactory labyrinth as modified by the remodeling process of the human face and skull base. The endochondral
bony origin of the ethmoid labyrinths makes them substantially different from the other paranasal sinuses.
Key Words: Ethmoid, olfaction, olfactory cleft, embryology, phylogeny, cartilaginous nasal capsule, nasal
turbinate, ethmoturbinal, paranasal sinus
Level of Evidence: N/A.
Laryngoscope, 121:2461–2467, 2011
INTRODUCTION
Currently, the nose and sinuses are considered as
one organ. However, examination of the nose and
sinuses from a phylogenic and development perspective
illustrates that the nose is primarily an olfactory organ.
The nose was secondarily integrated into the respiratory
apparatus by exaptation, a major mechanism of evolution, ultimately evolving toward our rhinosinusal organ.
Olfaction and respiration are the primary functions
of the nose, but the role of paranasal sinuses is still
under debate. Despite recent works demonstrating proFrom the Département d’Otorhinolaryngologie et Chirurgie CervicoFaciale, Hôpital Central, Centre Hospitalier Universitaire, Université
Henri Poincaré, Nancy, France.
Editor’s Note: This Manuscript was accepted for publication
September 9, 2010.
The author has no funding, financial relationships, or conflicts of
interest to disclose.
Send correspondence to Dr. Roger Jankowski, O.R.L. et Chirurgie
Cervico-Faciale,C.H.U.–Hôpital Central, 29 Avenue du Maréchal de
Lattre de Tassigny, F-54035 Nancy Cedex, France.
E-mail: [email protected]
DOI: 10.1002/lary.21368
Laryngoscope 121: November 2011
duction of nitric oxide in the paranasal sinuses, it
nevertheless remains possible that they arose as an aid
to facial growth and architecture, or persist as residual
remnants of an evolutionary structure with an as yet
unknown purpose.1
The ethmoid labyrinths are currently considered as
sinuses. However, examination of their development
shows that the ethmoid bone is derived from the cartilaginous nasal capsule, which phylogenetically emerges
and evolves to house and protect the olfactory function.2
Despite being described as sinuses for centuries, the ethmoid labyrinths may be regarded instead as remnants of
the olfactory nose.
The aim of this review is to illustrate that the integration of phylogenic and ontogenetic perspectives may
refine and shed new light on our understanding of
human nose anatomy.
PHYLOGENY
Vertebrates arose from a group of simple aquatic
organisms called protochordates. As the simple sense
organs of the protochordates gave way to the more
Jankowski: Phylo-ontogenic Anatomy of the Nose
2461
Fig. 1. Two primitive vertebrates
illustrating exaptation of the olfactory function by the respiratory
organ. (A, B) Lampetra fluviatilis (a
modern-day agnathan) presents a
blind uneven olfactory tube through
which the olfactory pouch is irrigated. Respiration works apart by
swallowing water through branchia.
(C, D) Protopterus africanus (a lungfish still living in African marshes)
presents branchia and primitive
alveoli and shows olfactory channels
that open posteriorly into the mouth,
allowing the passage from aquatic to
aerial life. [Color figure can be
viewed in the online issue, which is
available at wileyonlinelibrary.com.]
sophisticated olfactory, ocular, and audio-vestibular systems of the aquatic vertebrates, the brains of the most
primitive vertebrates (agnathans, a class of jawless
fishes) became protected in a cartilaginous chondrocranium, formed by paired prechordal, hypophyseal, and
parachordal cartilages. The prechordal cartilages evolved
into the cartilaginous nasal capsule to house and protect
the olfactory function.2
Exaptation of the Olfactory Organ by the
Respiratory Organ3
Exaptation is a mechanism of evolution by which a
functional structure of an organ is coopted by another.4
This mechanism explains the olfactory organ’s integration in the respiratory apparatus.
The most primitive vertebrates (agnathans)
appeared 500 million years ago.5 Lamprey and hagfishes
are modern-day representatives of this lineage.2 Their
primitive olfactory organ is a blind cartilaginous tube
through which the olfactory pouch is irrigated. Respiration occurs in a separate structure by swallowing water
through branchia3 (Fig. 1A and 1B).
The passage from aquatic to aerial life occurred 400
million years ago. Dipnoi, represented today by species
such as protopterus (an African lungfish), show both
branchia and primitive alveoli that allow them to
breathe in both water and air. Their olfactory channels
are no longer blind structures; they open posteriorly into
the mouth, i.e., into the respiratory apparatus of the fish
(Fig. 1C and 1D).3,5
From this evolutionary point forward, the olfactory
and respiratory noses remain fused and adapted to aerial life, ultimately evolving through different species
toward our rhinosinusal organ.
Laryngoscope 121: November 2011
2462
Olfactory and Respiratory Noses in
Macrosmatic Mammals3
The fundamental configuration of the nasal fossa is
remarkably constant throughout the great majority of
mammalian groups. Two exceptions are the Cetacea
(whales, dolphins, and porpoises), where highly specialized
respiratory requirements prevail, and the Anthropoidea
(humans and higher primates), where olfaction has
become less important.6
In macrosmatic mammals, the respiratory nose is
separated from the olfactory nose by the transverse lamina3,6 (Fig. 2), a bony plate that projects medially from the
lateral ethmoidal plates and articulates with the wings
projecting laterally from the vomer. It thus divides the
nose posteriorly into upper and lower compartments.6
The lower compartment is the respiratory nose: air
enters through the nostril, is warmed and humidified by
a large anterior turbinate called the nasal turbinate,
then reaches the pharynx and trachea by passing under
the transverse lamina.
The upper compartment, or olfactory nose, is a
blind olfactory recess, housing the ethmoturbinals and
lying in front of the cribriform plate. Ethmoturbinals
increase enormously the area of olfactory mucosa,6 forming an olfactory labyrinth.7 Each ethmoturbinal consists
of a bony lamella projecting medially from the lateral
and superior ethmoidal plates into the superior chamber.
The lamellae may undergo repeated branching and
undergo some degree of inrolling to form olfactory folds
toward their free extremities. Ethmoturbinals are usually arranged into two or more rows, depending on how
far they project medially into the olfactory chamber. The
elements forming the more lateral rows are termed exoturbinals, and those situated more medially are called
endoturbinals (Fig. 2B).
Jankowski: Phylo-ontogenic Anatomy of the Nose
Fig. 2. Respiratory and olfactory
nose in macrosmatic mammals. (A)
Sagittally sectioned skull of a fox
(right nasal fossa). (B) Schematic
representation of the ethmoturbinals
on a coronal section of a dog
(adapted from Flottes et al.3). [Color
figure can be viewed in the online
issue, which is available at
wileyonlinelibrary.com.]
As illustrated by extensive studies, variations in
the number and form of ethmoturbinals across different
species can be readily correlated with the importance of
the olfactory sense in the life of the animal.6
From Mammalian Olfactory Labyrinths to
Human Ethmoid Labyrinths
In humans, the mammalian olfactory labyrinth has
transformed into an ethmoid labyrinth lacking olfactory
mucosa. Human olfactory mucosa is restricted to a very
narrow portion of the ethmoid bone, called the olfactory
fossa (Fig. 6).8,9
One hypothesis for this transformation is related
to the upright posture of humans: bipedal locomotion
freed the hands, increased the role of vision, and
decreased the role of olfaction. As a result, the snout
retracted and the orbits migrated anteriorly.3 The
remodeling of the head forced the ethmoid bone to
migrate between the paranasal sinuses, displacing the
frontal sinus upwards and disconnecting this latter from
the maxillary sinus.10 In parallel, the remodeling of the
ethmoid bone resulted in the formation of two vertical
compartments on each side of the perpendicular plate:
the olfactory cleft and ethmoid labyrinth.
Phylogenetically, the ethmoid bone, which is part of
the cranial base, appears to be involved only in housing
and protecting the olfactory function.10 It is considered
to be a highly phylogenetically conserved region among
the bony elements of the skull.11 Some authors have suggested that the ethmoid labyrinths cannot be considered
‘‘true’’ paranasal sinuses.10 According to Cave,12 the sole
guide to the morphologic identity of a sinus is provided
not by the bone(s) it may ultimately pneumatize, but by
the bone(s) that circumscribe(s) its ostium, or point of origin. No such points are known in the formation of the
ethmoidal cells. Moreover, there is no clear definition of
what ethmoidal ‘‘cells’’ are and no description of their
ostia; the ethmoidal air spaces are mostly irregular in
shape and their drainage openings cannot really be
called ostia.10
Despite being described as sinuses for centuries,
from a phylogenic perspective, the ethmoid labyrinths
may be regarded as remnants of the olfactory
labyrinth.
Laryngoscope 121: November 2011
ONTOGENY
From Olfactory Placodes to Oronasal
Communication
According to Haeckel’s theory, some phylogenic
steps may be recapitulated during ontogeny.13
Indeed, the developmental phenomena that occur in
the tissue that separates the olfactory organ from the
oral cavity are well known (Fig. 3) and seem to recapitulate the phylogenic exaptation of the olfactory function
by the primary respiratory nose (Fig. 1).
The olfactory (nasal) placodes appear during the fifth
week of human embryonic development on the frontonasal
process. In the sixth week, they invaginate to form the
nasal pits (Fig. 3A and 3B). At the end of the sixth week,
the deepening nasal pits fuse posteriorly to form a nasal
sac, which is separated from the oral cavity by the nasal
fin (Fig. 3C). At the beginning of the seventh week, the fin
thins to a fine membrane (the oronasal membrane), which
ruptures during the seventh week to form an opening with
the oral cavity called the primitive choana. The floor of the
primary nasal fossa is called the primary palate (Fig. 3D).
From olfactory placodes to the cartilaginous
nasal capsule
The developmental phenomena in the tissue that separates the primary olfactory cavities from the brain
structures (Fig. 4A) have recently been investigated indepth in more than 300 serially sectioned embryos.14 This
study demonstrated that the cartilaginous nasal capsule
develops in close connection with the olfactory structures
during embryogenesis, thus supporting the phylogenetic
housing function of the cartilaginous nasal capsule. The cartilaginous nasal capsule becomes distinct at 6.5 weeks,
when the oronasal membrane breaks down.14 Its typical
‘‘m’’ shape is well identified at 8 weeks of embryonic life.14,15
From the cartilaginous nasal capsule to
ethmoidal labyrinths
The formation of the cartilaginous nasal capsule is
well described in the human embryo.2,14–19 Its development
is classically regarded as the beginning of paranasal sinus
formation. However, from phylogenic and ontogenic perspectives, it may be regarded as the development of the
Jankowski: Phylo-ontogenic Anatomy of the Nose
2463
Fig. 3. From the olfactory placode to oronasal communication in a human embryo. The first steps of embryonic development seem to reproduce the exaptation of the olfactory function by the respiratory organ. (A) Cephalic portion of a human embryo at the end of the fifth week of
development; (B) end of the fifth week (parasagittal section); (C) sixth week (parasagittal section); and (D) seventh week (parasagittal section).
Fig. 4. Cartilaginous nasal capsule.
(A) The nasal capsule is an emanation of the chondrocranium around
the primitive olfactory organ. It will
ultimately develop into the ethmoid
bone. (B) Furrows and ridges form
in the lateral nasal capsule (third
month of fetal life). Palatal shelves
and inferior turbinates originate from
the maxillary processes.
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2464
Jankowski: Phylo-ontogenic Anatomy of the Nose
Fig. 5. Lateral wall of the right
human nasal fossa. NVe ¼ nasal
vestibule; NVa ¼ nasal valve; NCh
¼ nasal chamber; Ch ¼ choana;
RPh ¼ rhinopharynx; Na ¼ nasal
attic; SEr ¼ spheno-ethmoidal
recess. [Color figure can be viewed
in the online issue, which is available at wileyonlinelibrary.com.]
olfactory labyrinth as modified by the remodeling process
of the human face and skull base. Currently, reliable
embryologic observations suggest strongly that the ethmoid
labyrinth is made of turbinates and interturbinal meatus
with correlations with mammalian ethmoturbinals.20
Thus, during weeks 9 to 10 of human fetal development, six major furrows, separated by ridges and resembling
ethmoturbinals, appear on each lateral branch of the cartilaginous nasal capsule (Fig. 4B). The first ethmoturbinal
regresses, leaving only the uncinate process as a remnant.
The middle turbinate develops from the second ethmoturbinal, the superior turbinate from the third, and the supreme
turbinate from the fusion of the fourth and fifth. The middle
meatus and hiatus semilunaris develop from the first primary furrow, the superior meatus from the second, and the
supreme meatus from the third. The formation of ethmoidal
cells is attributed to further formation of more or less developed transverse septa (which may be derivates of the
smallest ectoturbinates) in the interturbinal meatus. All this
development is completed before birth and thus the role of
pneumatization in the formation of the ethmoid labyrinths
is questionable. Moreover, the endochondral bony origin of
the ethmoid labyrinths makes them substantially different
from the other paranasal sinuses.
Paranasal Sinuses
The development of paranasal sinuses is only
observed after birth in aerial conditions. The maxillary,
frontal, and sphenoid sinuses are the result of epithelial
diverticula that escape the bounds of the cartilaginous
nasal capsule to pneumatize the surrounding bones of
membranous origin.3,10,21,22 The maxillary sinuses
expand at birth and throughout childhood within the
maxillary bones. The sphenoid sinuses first appear five
months after birth and continue to enlarge throughout
infancy and childhood. The frontal sinuses do not appear
until the age of five or six years, then continue to
expand throughout childhood and adolescence. They
mainly seem to arise as an aid to facial growth and
architecture.1 It has been suggested that, although the
extent of the ethmoid is inherently fixed and constrained, the size of paranasal sinuses is highly variable,
as paranasal recesses are not predictable.10
Laryngoscope 121: November 2011
REVISITING NOSE AND SINUS PHYSIOLOGY
AND ANATOMY
According to phylogeny and ontogeny, the classical
nose and sinus organ is the result of the fusion of three
entities: the respiratory nose, the olfactory nose including the ethmoidal labyrinths and olfactory clefts, and
the paranasal sinuses (Figs. 5 and 6).
Respiratory Nose
Physiologic studies in humans have shown that the
primary respiratory airstream passes through the inferior half of the nasal fossa in normal conditions, thus
bypassing the olfactory cleft, the ethmoidal labyrinths,
and the paranasal sinuses.23–27
The respiratory nose can be described as a channel,
roughly quadratic in section, with limen nasi as anterior
and choana as posterior openings. The inferior wall is
the floor of the nasal fossa. As the transverse lamina
has disappeared, the superior wall is a virtual plane
joining, posterior to anterior, the roof of the rhinopharynx, the inferior edge of the middle turbinate, the tip of
the nasal valve, and the vestibule (Fig. 5). The lateral
wall is the turbinate wall of the maxillary sinus,28 with
the inferior turbinate resembling the nasal turbinate
in the fox. The medial wall is the corresponding portion
of the nasal septum.
The respiratory nose presents, ventral to dorsal, four
regions (Fig. 5): the nasal vestibule, the nasal valve, the
nasal chamber, and the choana. The rhinopharynx may
sometimes be included as part of the respiratory nose.
Olfactory Nose
The olfactory nose has been partitioned by the facial remodeling of evolution into four vertical
compartments: the two medial compartments are the olfactory clefts, and the two lateral compartments are the
ethmoid labyrinths (Fig. 6).
According to histologic studies, human olfactory
mucosa is limited to the roofs of the olfactory clefts,
although its exact surface and distribution are not well
established.8,9,29 The ethmoid labyrinths are completely
free of olfactory mucosa.
Jankowski: Phylo-ontogenic Anatomy of the Nose
2465
Fig. 6. Coronal computed tomography scan of the human nasosinusal
organ.
Ethmoid Labyrinth
The turbinate wall of the ethmoid labyrinth
(TWEL) represents the limit between the olfactory cleft
and the ethmoid labyrinth (Fig. 6).28 The TWEL is
attached to the ethmoid roof above the level of the cribriform plate by the lateral lamella of the olfactory groove,
the medial face of which is endocranial and the lateral
face ethmoidal. The lateral lamella of the olfactory
groove classically continues under the level of the cribriform plate with a rectangular, bony plate—the conchal
lamina as named by Mouret30,31—to which the middle,
superior, and possibly supreme turbinates are attached,
ventrally to dorsally (Fig. 5).
If the ethmoid labyrinth is considered from a developmental point of view, it becomes apparent that the
TWEL is made of bony structures, known as the turbinates, which traverse the entire ethmoid labyrinth to
extend laterally to the lamina papyracea and superiorly
to the lamina cribrosa (Fig. 6). They are separated by
air spaces, the interturbinal meatus, which are secondarily partitioned by smaller transverse septa, leading to
the formation of ethmoidal cells. Together, these observations make it clear that the number of cells depends on
the development of the septa in the interturbinal meatus
and is highly variable in the ethmoids.
by a virtual plane at the inferior limit of the conchal
lamina (Figs. 5 and 6). Studies on airflow in the human
nose show that the olfactory cleft appears as a zone of
very slow airflow, probably affording greater residence
time to facilitate olfactory sensing.24
Paranasal Sinuses
The paranasal sinuses comprise the maxillary, frontal, and sphenoid sinuses. They form hollow, air-filled
cavities lined by a thin respiratory mucosa with virtually no glands or vascularization. A simple contact with
the atmospheric environment is maintained through a
small ostium.
It is well established that air composition in the
sinuses is stable (17.5% O2, 2.2% CO2, 100% relative humidity, 34 C) and that the best model to explain air
exchange between the nose and sinuses through the
ostium is passive diffusion.3,35 Most studies on mucous
drainage were done on maxillary or frontal sinuses36,37
and extrapolated to the sphenoid sinus, as well as the
ethmoid labyrinth. In fact, neither ventilation nor mucous drainage has been specifically studied in any
ethmoidal cell.
Olfactory Cleft
CONCLUSIONS
Although its location is obvious, the anatomy of the
olfactory cleft is not well described, even in major anatomy textbooks.32–34 The olfactory cleft can be described
as a narrow air space located above the respiratory nose
and below the olfactory groove; it is medial to the ethmoid labyrinth and lateral to the nasal septum. As the
olfactory epithelium is restricted to the upper part of the
olfactory cleft, this latter can be subdivided into an
upper chamber, the olfactory fossa, which is the true
sensory cavity, and a lower chamber, the olfactory vestibule. The limit between the two chambers is represented
This contemporary review has examined nasal
anatomy via phylogeny and ontogeny. Considered from
this evolutionary and development perspective, it can be
concluded that the ethmoidal labyrinth is better considered phylogenetically as part of the olfactory organ; its
classical inclusion in the paranasal sinuses is thus fundamentally imprecise.
Laryngoscope 121: November 2011
2466
Acknowledgment
The author thanks Mr. Kevin L. Erwin, biomedical
translator, for proofreading this article.
Jankowski: Phylo-ontogenic Anatomy of the Nose
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