revisiting human nose anatomy: phylogenic and …€¦ · revisiting human nose anatomy: phylogenic...

The LaryngoscopeVC 2011 The American Laryngological,Rhinological and Otological Society, Inc.

Contemporary Review

Revisiting Human Nose Anatomy: Phylogenic and OntogenicPerspectives

Roger Jankowski, MD

This review suggests revisiting nose anatomy by considering the ethmoidal labyrinths as part of the olfactorynose and not as paranasal sinuses.

Phylogenetically, the olfactory and respiratory organs of the most primitive vertebrates are separated. Exapta-tion, a mechanism of evolution, may explain the fusion of the olfactory and respiratory organs in dipnoi. The respi-ratory and olfactory noses remain anatomically separated by the transverse lamina in most mammals, whose olfac-tory labyrinth is a blind recess housing the ethmoturbinates. In humans, the partitioning between the olfactory cleftand the ethmoid labyrinth seems to be a consequence of ethmoid bone remodeling induced by the acquisition of anupright posture. The ethmoid bone is derived from the cartilaginous nasal capsule of primitive vertebrates and con-sidered to be a highly conserved region among the bony elements of the skull base. It appears to be involved only inhousing and protecting the olfactory function.

During the early stages of human fetal development, rupture of the oronasal membrane leads to the integrationof the primary olfactory sac in the future respiratory organ. The cartilaginous nasal capsule appears in the tissueunder the brain and around the olfactory channels. Its early fetal development is classically regarded as the beginningof paranasal sinus formation. From phylogenic and ontogenic perspectives, it may be regarded as the development ofthe olfactory labyrinth as modified by the remodeling process of the human face and skull base. The endochondralbony 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, nasalturbinate, ethmoturbinal, paranasal sinusLevel of Evidence: N/A.

Laryngoscope, 121:2461–2467, 2011

INTRODUCTIONCurrently, the nose and sinuses are considered as

one organ. However, examination of the nose andsinuses from a phylogenic and development perspectiveillustrates that the nose is primarily an olfactory organ.The nose was secondarily integrated into the respiratoryapparatus by exaptation, a major mechanism of evolu-tion, ultimately evolving toward our rhinosinusal organ.

Olfaction and respiration are the primary functionsof the nose, but the role of paranasal sinuses is stillunder debate. Despite recent works demonstrating pro-

duction of nitric oxide in the paranasal sinuses, itnevertheless remains possible that they arose as an aidto facial growth and architecture, or persist as residualremnants of an evolutionary structure with an as yetunknown purpose.1

The ethmoid labyrinths are currently considered assinuses. However, examination of their developmentshows that the ethmoid bone is derived from the carti-laginous nasal capsule, which phylogenetically emergesand evolves to house and protect the olfactory function.2

Despite being described as sinuses for centuries, the eth-moid labyrinths may be regarded instead as remnants ofthe olfactory nose.

The aim of this review is to illustrate that the inte-gration of phylogenic and ontogenetic perspectives mayrefine and shed new light on our understanding ofhuman nose anatomy.

PHYLOGENYVertebrates arose from a group of simple aquatic

organisms called protochordates. As the simple senseorgans of the protochordates gave way to the more

From the Departement d’Otorhinolaryngologie et Chirurgie Cervico-Faciale, Hopital Central, Centre Hospitalier Universitaire, UniversiteHenri Poincare, Nancy, France.

Editor’s Note: This Manuscript was accepted for publicationSeptember 9, 2010.

The author has no funding, financial relationships, or conflicts ofinterest to disclose.

Send correspondence to Dr. Roger Jankowski, O.R.L. et ChirurgieCervico-Faciale,C.H.U.–Hopital Central, 29 Avenue du Marechal deLattre de Tassigny, F-54035 Nancy Cedex, France.E-mail: [email protected]

DOI: 10.1002/lary.21368

Laryngoscope 121: November 2011 Jankowski: Phylo-ontogenic Anatomy of the Nose

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sophisticated olfactory, ocular, and audio-vestibular sys-tems of the aquatic vertebrates, the brains of the mostprimitive vertebrates (agnathans, a class of jawlessfishes) became protected in a cartilaginous chondrocra-nium, formed by paired prechordal, hypophyseal, andparachordal cartilages. The prechordal cartilages evolvedinto the cartilaginous nasal capsule to house and protectthe olfactory function.2

Exaptation of the Olfactory Organ by theRespiratory Organ3

Exaptation is a mechanism of evolution by which afunctional structure of an organ is coopted by another.4

This mechanism explains the olfactory organ’s integra-tion in the respiratory apparatus.

The most primitive vertebrates (agnathans)appeared 500 million years ago.5 Lamprey and hagfishesare modern-day representatives of this lineage.2 Theirprimitive olfactory organ is a blind cartilaginous tubethrough which the olfactory pouch is irrigated. Respira-tion occurs in a separate structure by swallowing waterthrough branchia3 (Fig. 1A and 1B).

The passage from aquatic to aerial life occurred 400million years ago. Dipnoi, represented today by speciessuch as protopterus (an African lungfish), show bothbranchia and primitive alveoli that allow them tobreathe in both water and air. Their olfactory channelsare no longer blind structures; they open posteriorly intothe mouth, i.e., into the respiratory apparatus of the fish(Fig. 1C and 1D).3,5

From this evolutionary point forward, the olfactoryand respiratory noses remain fused and adapted to aer-ial life, ultimately evolving through different speciestoward our rhinosinusal organ.

Olfactory and Respiratory Noses inMacrosmatic Mammals3

The fundamental configuration of the nasal fossa isremarkably constant throughout the great majority ofmammalian groups. Two exceptions are the Cetacea(whales, dolphins, and porpoises), where highly specializedrespiratory requirements prevail, and the Anthropoidea(humans and higher primates), where olfaction hasbecome less important.6

In macrosmatic mammals, the respiratory nose isseparated from the olfactory nose by the transverse lam-ina3,6 (Fig. 2), a bony plate that projects medially from thelateral ethmoidal plates and articulates with the wingsprojecting laterally from the vomer. It thus divides thenose posteriorly into upper and lower compartments.6

The lower compartment is the respiratory nose: airenters through the nostril, is warmed and humidified bya large anterior turbinate called the nasal turbinate,then reaches the pharynx and trachea by passing underthe transverse lamina.

The upper compartment, or olfactory nose, is ablind olfactory recess, housing the ethmoturbinals andlying in front of the cribriform plate. Ethmoturbinalsincrease enormously the area of olfactory mucosa,6 form-ing an olfactory labyrinth.7 Each ethmoturbinal consistsof a bony lamella projecting medially from the lateraland superior ethmoidal plates into the superior chamber.The lamellae may undergo repeated branching andundergo some degree of inrolling to form olfactory foldstoward their free extremities. Ethmoturbinals are usu-ally arranged into two or more rows, depending on howfar they project medially into the olfactory chamber. Theelements forming the more lateral rows are termed exo-turbinals, and those situated more medially are calledendoturbinals (Fig. 2B).

Fig. 1. Two primitive vertebratesillustrating exaptation of the olfac-tory function by the respiratoryorgan. (A, B) Lampetra fluviatilis (amodern-day agnathan) presents ablind uneven olfactory tube throughwhich the olfactory pouch is irri-gated. Respiration works apart byswallowing water through branchia.(C, D) Protopterus africanus (a lung-fish still living in African marshes)presents branchia and primitivealveoli and shows olfactory channelsthat open posteriorly into the mouth,allowing the passage from aquatic toaerial life. [Color figure can beviewed in the online issue, which isavailable at wileyonlinelibrary.com.]


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As illustrated by extensive studies, variations inthe number and form of ethmoturbinals across differentspecies can be readily correlated with the importance ofthe olfactory sense in the life of the animal.6

From Mammalian Olfactory Labyrinths toHuman Ethmoid Labyrinths

In humans, the mammalian olfactory labyrinth hastransformed into an ethmoid labyrinth lacking olfactorymucosa. Human olfactory mucosa is restricted to a verynarrow portion of the ethmoid bone, called the olfactoryfossa (Fig. 6).8,9

One hypothesis for this transformation is relatedto the upright posture of humans: bipedal locomotionfreed the hands, increased the role of vision, anddecreased the role of olfaction. As a result, the snoutretracted and the orbits migrated anteriorly.3 Theremodeling of the head forced the ethmoid bone tomigrate between the paranasal sinuses, displacing thefrontal sinus upwards and disconnecting this latter fromthe maxillary sinus.10 In parallel, the remodeling of theethmoid bone resulted in the formation of two verticalcompartments on each side of the perpendicular plate:the olfactory cleft and ethmoid labyrinth.

Phylogenetically, the ethmoid bone, which is part ofthe cranial base, appears to be involved only in housingand protecting the olfactory function.10 It is consideredto be a highly phylogenetically conserved region amongthe bony elements of the skull.11 Some authors have sug-gested that the ethmoid labyrinths cannot be considered‘‘true’’ paranasal sinuses.10 According to Cave,12 the soleguide to the morphologic identity of a sinus is providednot by the bone(s) it may ultimately pneumatize, but bythe bone(s) that circumscribe(s) its ostium, or point of or-igin. No such points are known in the formation of theethmoidal cells. Moreover, there is no clear definition ofwhat ethmoidal ‘‘cells’’ are and no description of theirostia; the ethmoidal air spaces are mostly irregular inshape and their drainage openings cannot really becalled ostia.10

Despite being described as sinuses for centuries,from a phylogenic perspective, the ethmoid labyrinthsmay be regarded as remnants of the olfactorylabyrinth.

ONTOGENY

From Olfactory Placodes to OronasalCommunication

According to Haeckel’s theory, some phylogenicsteps may be recapitulated during ontogeny.13

Indeed, the developmental phenomena that occur inthe tissue that separates the olfactory organ from theoral cavity are well known (Fig. 3) and seem to recapitu-late the phylogenic exaptation of the olfactory functionby the primary respiratory nose (Fig. 1).

The olfactory (nasal) placodes appear during the fifthweek of human embryonic development on the frontonasalprocess. In the sixth week, they invaginate to form thenasal pits (Fig. 3A and 3B). At the end of the sixth week,the deepening nasal pits fuse posteriorly to form a nasalsac, which is separated from the oral cavity by the nasalfin (Fig. 3C). At the beginning of the seventh week, the finthins to a fine membrane (the oronasal membrane), whichruptures during the seventh week to form an opening withthe oral cavity called the primitive choana. The floor of theprimary nasal fossa is called the primary palate (Fig. 3D).

From olfactory placodes to the cartilaginousnasal capsule

The developmental phenomena in the tissue that sepa-rates the primary olfactory cavities from the brainstructures (Fig. 4A) have recently been investigated in-depth in more than 300 serially sectioned embryos.14 Thisstudy demonstrated that the cartilaginous nasal capsuledevelops in close connection with the olfactory structuresduring embryogenesis, thus supporting the phylogenetichousing function of the cartilaginous nasal capsule. The car-tilaginous 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 toethmoidal labyrinths

The formation of the cartilaginous nasal capsule iswell described in the human embryo.2,14–19 Its developmentis classically regarded as the beginning of paranasal sinusformation. However, from phylogenic and ontogenic per-spectives, it may be regarded as the development of the

Fig. 2. Respiratory and olfactorynose in macrosmatic mammals. (A)Sagittally sectioned skull of a fox(right nasal fossa). (B) Schematicrepresentation of the ethmoturbinalson a coronal section of a dog(adapted from Flottes et al.3). [Colorfigure can be viewed in the onlineissue, which is available atwileyonlinelibrary.com.]


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Fig. 3. From the olfactory placode to oronasal communication in a human embryo. The first steps of embryonic development seem to repro-duce the exaptation of the olfactory function by the respiratory organ. (A) Cephalic portion of a human embryo at the end of the fifth week ofdevelopment; (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 emana-tion of the chondrocranium aroundthe primitive olfactory organ. It willultimately develop into the ethmoidbone. (B) Furrows and ridges formin the lateral nasal capsule (thirdmonth of fetal life). Palatal shelvesand inferior turbinates originate fromthe maxillary processes.


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olfactory labyrinth as modified by the remodeling processof the human face and skull base. Currently, reliableembryologic observations suggest strongly that the ethmoidlabyrinth is made of turbinates and interturbinal meatuswith correlations with mammalian ethmoturbinals.20

Thus, during weeks 9 to 10 of human fetal develop-ment, six major furrows, separated by ridges and resemblingethmoturbinals, appear on each lateral branch of the carti-laginous nasal capsule (Fig. 4B). The first ethmoturbinalregresses, leaving only the uncinate process as a remnant.The middle turbinate develops from the second ethmoturbi-nal, the superior turbinate from the third, and the supremeturbinate from the fusion of the fourth and fifth. The middlemeatus and hiatus semilunaris develop from the first pri-mary furrow, the superior meatus from the second, and thesupreme meatus from the third. The formation of ethmoidalcells is attributed to further formation of more or less devel-oped transverse septa (which may be derivates of thesmallest ectoturbinates) in the interturbinal meatus. All thisdevelopment is completed before birth and thus the role ofpneumatization in the formation of the ethmoid labyrinthsis questionable. Moreover, the endochondral bony origin ofthe ethmoid labyrinths makes them substantially differentfrom the other paranasal sinuses.

Paranasal SinusesThe development of paranasal sinuses is only

observed after birth in aerial conditions. The maxillary,frontal, and sphenoid sinuses are the result of epithelialdiverticula that escape the bounds of the cartilaginousnasal capsule to pneumatize the surrounding bones ofmembranous origin.3,10,21,22 The maxillary sinusesexpand at birth and throughout childhood within themaxillary bones. The sphenoid sinuses first appear fivemonths after birth and continue to enlarge throughoutinfancy and childhood. The frontal sinuses do not appearuntil the age of five or six years, then continue toexpand throughout childhood and adolescence. Theymainly seem to arise as an aid to facial growth andarchitecture.1 It has been suggested that, although theextent of the ethmoid is inherently fixed and con-strained, the size of paranasal sinuses is highly variable,as paranasal recesses are not predictable.10

REVISITING NOSE AND SINUS PHYSIOLOGYAND ANATOMY

According to phylogeny and ontogeny, the classicalnose and sinus organ is the result of the fusion of threeentities: the respiratory nose, the olfactory nose includ-ing the ethmoidal labyrinths and olfactory clefts, andthe paranasal sinuses (Figs. 5 and 6).

Respiratory NosePhysiologic studies in humans have shown that the

primary respiratory airstream passes through the infe-rior half of the nasal fossa in normal conditions, thusbypassing 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 anteriorand choana as posterior openings. The inferior wall isthe floor of the nasal fossa. As the transverse laminahas disappeared, the superior wall is a virtual planejoining, posterior to anterior, the roof of the rhinophar-ynx, the inferior edge of the middle turbinate, the tip ofthe nasal valve, and the vestibule (Fig. 5). The lateralwall is the turbinate wall of the maxillary sinus,28 withthe inferior turbinate resembling the nasal turbinatein the fox. The medial wall is the corresponding portionof the nasal septum.

The respiratory nose presents, ventral to dorsal, fourregions (Fig. 5): the nasal vestibule, the nasal valve, thenasal chamber, and the choana. The rhinopharynx maysometimes be included as part of the respiratory nose.

Olfactory NoseThe olfactory nose has been partitioned by the fa-

cial remodeling of evolution into four verticalcompartments: the two medial compartments are the ol-factory clefts, and the two lateral compartments are theethmoid labyrinths (Fig. 6).

According to histologic studies, human olfactorymucosa is limited to the roofs of the olfactory clefts,although its exact surface and distribution are not wellestablished.8,9,29 The ethmoid labyrinths are completelyfree of olfactory mucosa.

Fig. 5. Lateral wall of the righthuman nasal fossa. NVe ¼ nasalvestibule; NVa ¼ nasal valve; NCh¼ nasal chamber; Ch ¼ choana;RPh ¼ rhinopharynx; Na ¼ nasalattic; SEr ¼ spheno-ethmoidalrecess. [Color figure can be viewedin the online issue, which is avail-able at wileyonlinelibrary.com.]


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Ethmoid LabyrinthThe turbinate wall of the ethmoid labyrinth

(TWEL) represents the limit between the olfactory cleftand the ethmoid labyrinth (Fig. 6).28 The TWEL isattached to the ethmoid roof above the level of the cribri-form plate by the lateral lamella of the olfactory groove,the medial face of which is endocranial and the lateralface ethmoidal. The lateral lamella of the olfactorygroove classically continues under the level of the cribri-form plate with a rectangular, bony plate—the conchallamina 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 devel-opmental point of view, it becomes apparent that theTWEL is made of bony structures, known as the turbi-nates, which traverse the entire ethmoid labyrinth toextend laterally to the lamina papyracea and superiorlyto the lamina cribrosa (Fig. 6). They are separated byair spaces, the interturbinal meatus, which are second-arily partitioned by smaller transverse septa, leading tothe formation of ethmoidal cells. Together, these observa-tions make it clear that the number of cells depends onthe development of the septa in the interturbinal meatusand is highly variable in the ethmoids.

Olfactory CleftAlthough its location is obvious, the anatomy of the

olfactory cleft is not well described, even in major anat-omy textbooks.32–34 The olfactory cleft can be describedas a narrow air space located above the respiratory noseand below the olfactory groove; it is medial to the eth-moid labyrinth and lateral to the nasal septum. As theolfactory epithelium is restricted to the upper part of theolfactory cleft, this latter can be subdivided into anupper chamber, the olfactory fossa, which is the truesensory cavity, and a lower chamber, the olfactory vesti-bule. The limit between the two chambers is represented

by a virtual plane at the inferior limit of the conchallamina (Figs. 5 and 6). Studies on airflow in the humannose show that the olfactory cleft appears as a zone ofvery slow airflow, probably affording greater residencetime to facilitate olfactory sensing.24

Paranasal SinusesThe paranasal sinuses comprise the maxillary, fron-

tal, and sphenoid sinuses. They form hollow, air-filledcavities lined by a thin respiratory mucosa with virtu-ally no glands or vascularization. A simple contact withthe atmospheric environment is maintained through asmall ostium.

It is well established that air composition in thesinuses is stable (17.5% O2, 2.2% CO2, 100% relative hu-midity, 34�C) and that the best model to explain airexchange between the nose and sinuses through theostium is passive diffusion.3,35 Most studies on mucousdrainage were done on maxillary or frontal sinuses36,37

and extrapolated to the sphenoid sinus, as well as theethmoid labyrinth. In fact, neither ventilation nor mu-cous drainage has been specifically studied in anyethmoidal cell.

CONCLUSIONSThis contemporary review has examined nasal

anatomy via phylogeny and ontogeny. Considered fromthis evolutionary and development perspective, it can beconcluded that the ethmoidal labyrinth is better consid-ered phylogenetically as part of the olfactory organ; itsclassical inclusion in the paranasal sinuses is thus fun-damentally imprecise.

AcknowledgmentThe author thanks Mr. Kevin L. Erwin, biomedical

translator, for proofreading this article.

Fig. 6. Coronal computed tomogra-phy scan of the human nasosinusalorgan.


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revisiting human nose anatomy: phylogenic and …€¦ · revisiting human nose anatomy: phylogenic...

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