3 Physiology of the Nose and Paranasal Sinuses

Physiology of the Nose and Paranasal Sinuses 29 3 Physiology of the Nose and Paranasal Sinuses

Davide Tomenzoli

CONTENTS source of suffering for patients and a focus of atten- 3.1 Introduction 29 tion for clinicians. 3.2 Breathing 29 “Physiologic” breathing occurs through the nose; 3.3 Mucociliary System 30 it may be supplemented by oral respiration under 3.4 Filtration 30 demanding conditions of exercise or of severe nasal 3.5 Heating and Humidifi cation 31 3.6 Antimicrobial Defense 31 obstruction. Nasal fossae may not only be considered 3.7 Refl ex Action 31 the front door of the respiratory system, but are also 3.8 Recovery of Water 31 characterized by peculiar and signifi cant functions 3.9 Resonance 32 other than breathing: conditioning and moistening 3.10 Olfactory Function 32 of the nasal air-fl ow, fi ltration of inspired noxious 3.11 The Role of Paranasal Sinuses 32 3.11.1 Lighten the Skull for Equipoise of the Head 32 materials, specifi c and non-specifi c antibacterial and 3.11.2 Impart Resonance to the Voice 32 antiviral activities, refl ex action, collection of water 3.11.3 Increase the Olfactory Area 33 from expired airfl ow, olfactory function. 3.11.4 Thermal Insulation of Vital Parts 33 3.11.5 Secretion of Mucus to Moisten the Nasal Cavity 33 3.11.6 Humidify and Warm the Inspired Air 33 3.11.7 Absorption of Stress with Possible Avoidance of Concussion 33 3.2 3.11.8 Infl uence on Facial Growth and Architecture 33 Breathing References 34 Every day 10,000 l of ambient air reach lower respiratory airways for pulmonary ventilation. Air enters the nose through the nostrils, as a consequence of a pressure gradient existing between external ambi- 3.1 ent and pulmonary alveoli, and converges through Introduction the so-called nasal valve, positioned in the anterior part of the nasal fossa just behind the nasal vestibu- Many papers and investigations on nasal physiol- lum. The term “nasal valve” refers to an area lying ogy have been published in the last 40 years; as a on a perpendicular plane to the anteroposterior axis consequence, knowledge of nasal functions has now of the nasal fossa, which is bordered medially by the been well established. In contrast, however, the role nasal septum, laterally by the head of the inferior of the human paranasal sinuses remains as much turbinate and superiorly by the posterior margin of an enigma today as it was nearly two millennia ago the lateral crus of the alar cartilage. This restricted (Blaney 1990). According to Cole (1998), the con- area accounts for about 50% of the total resistance clusive evidence of a functional relevance of the of the respiratory system and gives rise to a laminar paranasal sinuses has yet to be found. Even though airfl ow. As inspiratory air leaves the narrow valvular the existence of the paranasal sinuses may be unex- area and enters the much larger cross-section of plained, their susceptibility to disease is a common the nasal fossa, its velocity decelerates from 18 m/ s to 4 m/s and the laminar airfl ow becomes turbulent. When airfl ow reaches nasal fossa it splits into three air streams, the largest of which fl ows D. Tomenzoli, MD over the superior edge of the inferior turbinate. A Department of Otorhinolaryngology, University of Brescia, second smaller airfl ow (about 5%–10%) runs along Piazzale Spedali Civili 1, Brescia, BS, 25123, Italy the olfactory mucosa localized on the roof of the 30 D. Tomenzoli nasal fossa, the medial surface of the upper and of mucus and an underlying layer of serous fl uid. middle turbinates, and the opposed part of the sep- This fl uid is deep enough to avoid entanglement tum. Finally, a minimal fl ow runs on the fl oor of the of the cilia with the viscoelastic mucus that fl oats nasal fossa (Fig. 3.1). The subdivision of the nasal on its surface enabling the mucus (which contains airfl ow and the presence of a turbulent fl ow allows entrapped contaminants, microorganisms and de- the maximal distribution of inspired air throughout bris) to be propelled along well-established routes the nasal cavity, enabling exchanges of heat, water to the pharynx, where it is swallowed (Fig. 3.2). and contaminants between the inspired air and the Serous and seromucinous glands localized in the respiratory mucosa. intermediate layer of the lamina propria, and the intraepithelial goblet cells are the producers of the periciliary fl uid and the thick viscoelastic mucus (Cole 1998; Nishihira and McCaffrey 1987).

Fig. 3.1. Breathing at rest. Inspired air once it has passed through the nasal valve (red area, 1) divides into three air streams. The main one fl ows along the middle turbinate (2); the second and third fl ow along the ethmoid roof (3) and nasal Fig. 3.2. Prechambers and paths of normal mucous drainage. fossa fl oor (4) Structures are demonstrated after subtotal removal of middle turbinate. Frontal sinus, anterior ethmoid cells, and maxillary sinus drain into the middle meatus (red arrows). The sphenoid sinus and posterior ethmoid cells drain into the superior meatus (blue arrows). Arrowheads indicate the insertion of the 3.3 middle turbinate’s ground lamella on the lateral nasal wall. FS, Mucociliary System frontal sinus; B, bulla ethmoidalis; PEC, posterior ethmoid cells; SS, sphenoid sinus; UP, uncinate process; IT, inferior turbinate Nasal mucosa presents a ciliated columnar pseu- dostratifi ed epithelium that lines the nose and the paranasal sinuses and is bounded by squamous epithelium at the level of the nasal vestibulum. The 3.4 area of the luminal surface of the sinonasal epi- Filtration thelium is greatly expanded by 300–400 microvilli x cell. Also, columnar cells bear about a hundred The inspired air contains a great amount of sus- cilia x cell beating 1000 x/min in sequence with pended exogenous particulate material. The upper those of neighboring ciliated cells (Mygind 1978). respiratory tract, especially the nose, must act as the The cilia beat in a serous periciliary fl uid of low fi rst line of defense and plays a signifi cant role as a viscosity. The beat of a single cilium consists of protective fi lter for particles as well as for irritant a rapid forward beat and a slow return beat with gases. Turbulence and impingement cause deposi- a time ratio of 1:3. Within a limited mucosal area tion of particles just behind the constricted area all cilia beat in the same direction; the cilia beat of the nasal valve. Thus, the nose is normally the synchronously in parallel ranks one after another principal site of particle deposition, but the effi cacy forming metachronous waves that transport the ex- of this nasal fi lter depends on the diameter of the ogenous particles toward rhinopharynx. Cilia are particles inhaled (Muir 1972). Few particles greater plunged in a mucus blanket that is made up of than 10 µm are able to penetrate the nose during a double liquid layer: a superfi cial viscous sheet breathing at rest, while particles smaller than 1 µm Physiology of the Nose and Paranasal Sinuses 31 are not fi ltered out, reaching the delicate structures 3.6 of the alveoli. Deposited particles, between 10 and Antimicrobial Defense 1 µm in diameter, are removed from the nasal mucosa within 6–15 min depending on the effi cacy of In addition to physical removal of microorganisms the mucociliary system. and other noxious materials by mucociliary transport, an important line of defense is provided by the surface fl uids that contain macrophages, basophils and mast cells, leucocytes, eosinophils, and antibacte- 3.5 rial/antiviral substances that include immunoglobu- Heating and Humidifi cation lins, lactoferrin, lysozymes and interferon. These cells and substances discourage microbial colonization The blood vessels of the nasal mucosa are of paramount and enhance the protective properties of the sinona- importance for the functions of heating and humidifi - sal mucosa against infections. cation. As reported by detailed studies (Cauna 1970) the arterioles of the nasal mucosa are characterized by the total absence of the internal elastic membrane so that the endothelial basement membrane is con- 3.7 tinuous with the basement membrane of the smooth Refl ex Action muscle cells. In addition, nasal blood vessels are also characterized by porosity of endothelial basement Nasal mucosa is supplied by nerves from the so- membrane so that the subendothelial musculature matic and autonomic systems. The sensory fi bers of these vessels may be rapidly infl uenced by agents travel with the trigeminal nerve, while the parasym- and drugs carried in the blood. Between the capil- pathetic fi bers are derived from the facial nerve and laries and the venules are interposed the cavernous the sympathetic fi bers from the superior cervical sinusoids; these are localized in the lower layer of the ganglion. lamina propria especially on the inferior turbinates. Afferent impulses are transported via the sensory Cavernous sinusoids are regarded as specialized capil- fi bers to the central nervous system giving rise to laries adapted to some of the functional demands of tickling or pain. Efferent impulses are propagated the airway, i.e. moistening and heating of the inspired through autonomic, vasomotor and secretory-mo- air. Nasal blood vessels can be classifi ed according to tor nerve fi bers. The stimulation of nasal mucosa their principal function into capacitance, resistance results in sneezing, watery rhinorrhea and changes and exchange vessels. The amount of sinonasal blood in blood fl ow (Allison and Powis 1971). volume depends on the tone of the capacitance ves- Other than nasal effects, the stimulation of the sels (mainly venous vessels and cavernous sinusoids), nasal mucosa can produce systemic refl exes as the while the blood fl ow on the tone of resistance vessels inhibition of respiration due to an increase in air- (mainly small arteries, arterioles and arteriovenous way resistance or laryngospasm. Furthermore, an anastomoses). Finally, transport through the walls of increase in resistance in vessels of the skin, muscle, vessels takes place in the exchange vessels (mainly splanchnic and kidney circulation can be observed. capillaries). Finally, cardiac output is reduced during nasal Nasal air condition also depends on a number of fac- stimulation as a result of bradycardia (Angell and tors other than nasal blood vessels such as seromucous Daly 1972). glands, goblet cells, plasmatic transudate and lacri- mal secretion. Furthermore, the nose has additional properties that contribute to heating and humidifying inspired air such as: maximum wall contact for the 3.8 mixed fl ow of air (laminar and turbulent, according to Recovery of Water the different areas of the nasal cavities); the ability to change the turbinates cross-section depending on the During expiration warm air coming from the lower variation in temperature and humidity of the ambient airway condenses in the anterior part of the nose, air; the large amount of blood fl owing rapidly through which has a temperature 4°C lower than that of the the arteriovenous anastomoses of the turbinates; the lung. With this mechanism, called the “piggy bank” contribution to the inhaled air of atomized watery se- function, the nose is able to recover about 100 ml of cretion from serous glands. water everyday. Nevertheless, during nasal breath- 32 D. Tomenzoli ing at room temperature the daily total loss is about 3.11 500 ml of water and 300 kcal (Ingelstedt and The Role of Paranasal Sinuses Toremalm 1961). No conclusive theory on the role of paranasal sinuses has been accepted yet. Some authors have suggested a functional role, while others have argued that the 3.9 paranasal sinuses in higher primates are merely non- Resonance functional remnants of a common mammalian an- cestor. The following sections review the different Even though it can not be considered a vital function, theories. the nose acts as a resonance box which gives its contribution, together with paranasal sinuses and pharynx, to the characterization of the tone of the voice. 3.11.1 Lighten the Skull for Equipoise of the Head

This is the oldest of all theories. The fi rst objection 3.10 came from Braune and Clasen (1877), who claimed Olfactory Function that if the sinuses were fi lled with spongy bone the total weight of the head would be increased by only The superior turbinate, the cribriform plate, the 1%. Despite statements that man’s musculature is ad- upper surface of the middle turbinate and the op- equate to maintain head poise regardless of the state posed part of the nasal septum are covered by a of paranasal sinuses (Flottes et al. 1960), it was not specialized epithelium containing receptors cells. until 1969 that an electromyographic investigation The sense of smell is mediated via stimulation was made of the activity of human neck muscles in of these olfactory receptors by volatile chemicals. response to loading the anterior aspect of the head. Five different types of cells form the olfactory epi- It was concluded that the human paranasal sinuses thelium: the bipolar olfactory neuron, which is a are not signifi cant as weight reducers of the skull for primary sensory neuron with an olfactory knob maintenance of equipoise of the head (Biggs and from which several olfactory cilia extend; the basal Blanton 1970). cell, which replaces the bipolar neuron cells every 7 weeks; sustentacular cell, which acts as a support cell supplying nutrients for bipolar neuron cells; 3.11.2 microvillar cell, which have no clearly defi ned role Impart Resonance to the Voice except to perhaps assist olfaction; Bowman’s glands, which provide a serous component to the mucous In the seventeenth century, Bartholinus asserted that layer covering the olfactory epithelium (Rice and paranasal sinuses are important phonatory adjuncts Gluckman 1995). in that they aid resonance. This theory received sup- The exact mechanism of olfaction is somewhat port from Howell (1917), when he stated that the vague. Multiple theories have been proposed but peculiar quality or timbre of the individual voice none have really been supported scientifi cally. There arises from the accessory sinuses and the bony frame- is some suggestion that different odors produce dif- work of the face. This conclusion was related to the ferent patterns of activity across the olfactory mu- observation that Maori – who have a small frontal cosa. Whatever the explanation at the molecular sinus – possess a peculiarly dead voice. Blanton level, depolarization of the bipolar neurons occurs, and Biggs (1969) also supported this theory on the resulting in an action potential that is transmitted basis that the howling monkeys possess particularly along the olfactory nerve, and the information is large paranasal sinuses. Nevertheless, a few authors processed centrally in the olfactory tubercle, pyri- discounted the resonance theory by observing that form cortex, amygdaloid nucleus, and hypothala- animals with loud voices such as the lion can have mus. Interestingly enough, olfactory receptor cells small sinuses (Proetz 1953), or that other animals, are the only nerve cells capable of regeneration, such as the giraffe and rabbit, have small or shrill, allowing for (at least theoretically) the possibility non-resonant voices despite having large sinus cavi- of regeneration after severe injury (Laffort et al. ties (Negus 1958). Finally, Flottes et al. (1960) 1974). reported that the physical properties of paranasal Physiology of the Nose and Paranasal Sinuses 33 sinuses make them poor resonators and added that al. 1960). However, some authors demonstrated that sinus surgery does not modify the voice. exchange of gases between the nose and paranasal sinuses is negligible and thus also the contribution of the sinuses to the conditioning of the inspired air 3.11.3 proves to be insignifi cant (Paulsson et al. 2001). Increase the Olfactory Area

This theory arose when Cloquet (1830) incorrectly 3.11.7 stated that the human maxillary sinus was lined with Absorption of Stress with Possible Avoidance of olfactory epithelium such as in some mammals. On Concussion the contrary, the mucous membrane of the human paranasal sinuses is made up of non-olfactory epithe- This theory originated from Negus’ work on horned lium, but is lined by a thinner, less vascular mucosa ungulates (Negus 1958). He noted that the air which is more loosely fi xed to the bony wall than that spaces which extend over the cranial vault and into of the respiratory region of the nasal cavity. the horns, such as the ox and goat, are sometimes explained as stress distributors. However, in other horned ungulates such as the moose, the horns are 3.11.4 attached directly to the cranium without air spaces. Thermal Insulation of Vital Parts Rui (1960) observed that the sinus complex could be considered as a pyramidal buffer with the base This theory was originally proposed by Proetz (1953) situated anteriorly and the apex at the sphenoid thus who compared the paranasal sinuses to an air-jacket forming an architectural structure suited to a protec- enveloping the nasal fossae. Nevertheless, Eskimos tive function of endocranial structures. often possess no frontal sinus, while African Negroes possess large frontal sinuses (Blaney 1990). 3.11.8 Infl uence on Facial Growth and Architecture 3.11.5 Secretion of Mucus to Moisten the Nasal Cavity According to Proetz (1953) the paranasal sinuses are the result of a plastic rearrangement of the skull This theory is also discounted on the basis of his- as a consequence of a disproportionate growth of the tology. First advocated by Haller (1763, reported face and cranium and associated structures after they by Wright 1914) it proposes that the sinuses are are fully or partly ossifi ed. However, Negus (1958) important for moistening the nasal olfactory mu- documented that individuals with a single frontal cosa. However, Skillen (1920) and Negus (1958) sinus do not show a defective facial growth. Eckel observed that an adequate amount of mucus for this (1963) attributed the presence of sinus cavities to purpose cannot be secreted by the human paranasal strains and stress of the skull created solely by the sinuses lining. In contrast to the nose with its 100,000 pressure exerted by the chewing apparatus. However, submucosal glands, the sinuses have only 50–100 Takahashi (1984) emphasized that the shape of the glands (Dahl and Mygind 1998). neurocranium and cranial base must also be considered important elements. He stated that in the evolu- tion of mammals from primates to humans, sinuses 3.11.6 originally acted as an aid to olfaction, but were infl u- Humidify and Warm the Inspired Air enced by the retraction of the maxillofacial box and by the process of cerebral enlargement. The develop- It has long been known that air exchange takes place ment of human paranasal sinuses is thus the result in the sinuses during respiration. However, a debate of an increase in the angle between the forehead and existed as to whether this exchange occurs to enable frontal cranial base, and decrease in the angle of the humidifi cation and warming of inspired air. Aerated cranial base at the sella turcica. sinuses develop in large swiftly moving mammals In conclusion, according to Blaney (1990), it is with an active respiration, while slow moving mam- becoming apparent that an architectural theory is mals, especially those living in a humid medium like far more likely in that it is known that craniofacial the hippopotamus, have small sinuses (Flottes et form has an important bearing on paranasal sinus 34 D. Tomenzoli morphology. Further research into craniofacial form Cole P (1998) Physyology of the nose and paranasal sinuses. and development needs to be done before the exact Clin Rev Allergy Immunol 16:25-54 role of the paranasal sinuses in humans can be de- Dahl R, Migynd N (1998) Anatomy, physiology and function of the nasal cavities in health and disease. Adv Drug Deliv fi nitively clarifi ed or established. It is encouraging Rev 5:3-12 that the more recent studies have emphasized the Eckel W (1963) Untersuchungen zur Grössenentwicklung der importance of differential sinuses (Takahashi 1984; Kieferhöhlen. Arch Ohren Nasen Kehlkopfheilkd 182:479- Blaney 1986). With the advent of new imaging tech- 484 niques much accurate data about paranasal sinus size Flottes L, Clerc P, Rui R et al (1960) La physiologie des sinus. Libraire Arnette, Paris and morphology can be collected and further differ- Howell HP (1917) Voice production from the standpoint of the ential growth studies performed. laryngologist. Ann Otol Rhinol Laryngol 26:643-655 Ingelstedt S, Toremalm NG (1961) Air fl ow pattern and heat trans- fer within the respiratory tract. Acta Physiol Scand 51:1-4 Laffort P, Patte F, Etcheto M (1974) Olfactory coding on the basis of physiochemical properties. Ann NY Acad Sci References 237:193-208 Muir DCF (1972) Clinical aspects of inhaled particles. 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