Introduction
The paranasal sinuses comprise the frontal, maxillary, ethmoid and sphenoid sinuses. They have caused consternation and debate over their true function over the course of nearly two millennia. As stated by Wright,Reference Wright1 VesaliusReference Vesalius2 and Fallopius,Reference Fallopius, Righi Riva and Di Pietro3 GalenReference Galen and Tallamadge4 (130–201 AD) is credited with the first acknowledgement of their existence. However, WrightReference Wright1 himself found no direct reference to the sinuses in Galen's De Usu Partium.Reference Galen and Tallamadge4 Flottes et al. Reference Flottes, Clere, Rui and Devilla5 attribute their discovery to Leonardo Da VinciReference Da Vinci6 (1452–1519). Both KempReference Kemp and Da Vinci7 and PevsnerReference Pevsner8 note that in Da Vinci's classic illustrations ‘Two views of the skull’, circa 1489, the frontal and maxillary sinuses are identified (see Figure 1). These sinuses may also be seen in Da Vinci's ‘View of a skull’, circa 1489 (see Figure 2). Da Vinci even proposed his own theory that the maxillary sinus ‘contains the humor which nourishes the teeth’.Reference O'Malley, Saunders and de9
Fig. 1 ‘Two views of the skull’ by Leonardo Da Vinci, circa 1489.
Fig. 2 ‘View of a skull’ by Leonardo Da Vinci, circa 1489.
WrightReference Wright1 considered that FallopiusReference Fallopius, Righi Riva and Di Pietro3 made the first contribution to paranasal sinus ontogeny with his observation that the sinuses were not present in the neonatal skull. Nathaniel Highmore (1614–1685) made further progress in understanding sinus development with a detailed description of the maxillary sinuses, in 1651; he also advanced the concept of their pneumatisation.Reference Highmore10
Blanton and BiggsReference Blanton and Biggs11 document the fact that, throughout history, speculation over the role of the paranasal sinuses has been numerous and diverse. They recognised that much of this speculation arose from a ‘basis of opinion rather than rigorous scientific investigation’. BlaneyReference Blaney12 considered that no conclusive theory to explain their raison d'être had yet been found.
Materials and methods
In order to define the current evidence for the role of the paranasal sinuses and to attempt to propose an answer to the question ‘why do we have paranasal sinuses?’, a literature review was conducted, searching Medline (1966–2007), Embase (1988–2007), the Cochrane Library and Ovid (1966–2007). Combinations of the following search terms were used: ‘paranasal sinuses’, ‘physiology’, ‘anatomy’, ‘function’, ‘evolution’ and ‘rhinology’. Any relevant references were cascaded to increase detection of pertinent information. The current, tenable theories identified in the literature review are discussed below and the evidence for them examined.
Results and analysis
Imparting resonance to the voice
The paranasal sinuses' function of imparting resonance to the voice was first proposed by BartholinusReference Bartholinus13 in the seventeenth century; he noted that they were not present in those of ‘faulty voice’. Several authorsReference Voltine14, Reference Zuckerkandl15 supported this theory; HowellReference Howell16 studied the Maori people of New Zealand and observed ‘peculiarly dead voices’ in those with ‘an underdevelopment of their accessory sinuses’. He therefore proposed that ‘the peculiar quality or timbre of the individual voice arises from the accessory sinuses and the bony framework of the face’. WegnerReference Wegner17 also supported this theory, observing that howling monkeys had large sinuses.
However, ProetzReference Proetz18 questioned this theory, noting that lions had small sinuses but comparatively loud voices. Furthermore, the guinea pig and giraffe, with their relatively quiet or shrill, irresonant voices, were noted to have large sinus cavities.Reference Montandon19 NegusReference Negus20 demonstrated, through a comparative anatomy study, that there was no relation between the presence or absence of the paranasal sinuses and the voice. Flottes et al. Reference Flottes, Clere, Rui and Devilla5 and SchaefferReference Schaeffer21 also remarked on the physical qualities of the paranasal sinuses which made them poor resonators, noting: the limited size of the ostia; the covering of the ostia by the turbinates; the closed nature of the cavities; and the covering of the sinus walls, dampening any vibration. It has also been observed that, following sinus surgery, no modification of the voice occurs.Reference Flottes, Clere, Rui and Devilla5 Flottes et al.,Reference Flottes, Clere, Rui and Devilla5 Blanton and BiggsReference Blanton and Biggs11 and BlaneyReference Blaney12 all concur that this theory is unsound.
Humidifying and warming inspired air
Air exchange is known to take place in the sinuses during respiration.Reference Braune and Clasen22, Reference Proetz23 However, the amount of exchange that is thought to occur is negligible.Reference Flottes, Clere, Rui and Devilla5, Reference Proetz18, Reference Negus20, Reference Proetz23 NegusReference Negus20 considered the process of humidification and warming of inspired air in species requiring the greatest degree of warming ‘takes the form of an elaborately branching maxillo-turbinal body’ rather than depending on the paranasal sinuses. He noted that ‘it is more profitable to have large maxillo-turbinal bodies, filling the anterior part of the snout, than hollow air spaces’. Levine and ClementeReference Levine and Clemente24 note that, during a single respiratory act, only one-thousandth of the air volume of the sinuses is exchanged, and that the air in the maxillary sinuses is not exchanged even after five minutes of normal breathing.Reference Aust, Stierna and Drettner25 Given the lack of any meaningful air exchange into the sinuses, several authors have doubted that this process occurs and have considered this theory flawed.Reference Flottes, Clere, Rui and Devilla5, Reference Blanton and Biggs11, Reference Blaney12, Reference Proetz18, Reference Negus20
Increasing the olfactory area
CloquetReference Cloquet26 proposed in 1830 that human maxillary sinuses were lined with olfactory epithelium, and therefore suggested that their role might be to increase the area of the olfactory membrane. However, this mucous membrane was later found to be lined by non-olfactory epithelium,Reference Williams and Warwick27 and this theory has been roundly dismissed.Reference Blanton and Biggs11, Reference Blaney12
Providing thermal insulation to vital parts
The possible role of the paranasal sinuses in providing thermal insulation to vital parts was originally proposed by Proetz.Reference Proetz18 He likened the sinuses to ‘an air-jacket about the nasal fossae closely resembling the water jacket of a combustion engine’. However, Eskimos often possess no frontal sinuses,Reference Koertvelyessy28, Reference Tillier29 while Africans possess large frontal sinuses.Reference Brothwell, Molleson, Metreweli and Brothwell30, Reference Wolfowitz31 Rae et al. Reference Rae, Hill, Hamada and Koppe32 demonstrated that Japanese macaques, which show intraspecies variability, have smaller sinuses in individuals from colder areas. Thermal insulation as a primary role for the paranasal sinuses therefore seems unlikely.
Absorbing trauma to protect the sensory organs
NegusReference Negus20, Reference Negus33 first proposed that the sinuses might absorb trauma in order to aid protection of the sensory organs, after noting air spaces extending over the cranial vault and into the hollowed horns of ungulates. However, he also noted that some ungulates, notably the elk and moose, did not possess these air spaces but nevertheless sustained high impact trauma without obvious damage. Riu et al. Reference Riu34 viewed the sinuses as a pyramid, with the base situated anteriorly and the apex at the sphenoid sinus, producing an architectural structure suited to protecting the endocranium. BlaneyReference Blaney12 considered the proposal significantly weakened due to interspecies variability, whereby those species appearing to suffer high impact trauma to this area had very small sinuses.
Aiding facial growth and architecture
ProetzReference Proetz35 proposed that the human frontal and maxillary sinuses might be designed to assist forward and downward growth of the face; ‘in consideration of the rearrangement of the face structure it becomes apparent that the formation of the sinuses is necessary for the surrounding parts’. He also stated that the ‘frontal sinuses develop… along with advancement of the face; the maxillary grows… with the growth of the jaw; the sphenoid… with the broadening of adjacent parts’, such that the development of the sinuses ceases when an adult age is attained, at which time the craniofacial structures acquire a definitive form. However, NegusReference Negus20 noted that individuals with a single frontal sinus of minute volume did not show deficient facial growth. GalperinReference Galperin36 attributed the presence of the sinuses to strains and stresses on the skull due solely to the chewing apparatus, while EckelReference Eckel37 considered that ‘the bite and chewing function are the forces which determine the size and development of the maxillary sinus’. This would not however explain the presence of other paranasal sinuses, and in vivo experiments using strain gauges in primates suggest that little stress reaches the frontal sinus region.Reference Bookstein, Schafer, Prossinger, Seidler, Fieder and Stringer38, Reference Prossinger, Bookstein, Schafer and Seidler39
TakahashiReference Takahashi40 considered that the sinuses originally developed as an aid to olfaction and subsequently altered following the evolution of mammals from primate to human, with consequent retraction of the maxillo-facial massif and cerebral enlargement. It was further proposed that the paranasal sinuses in humans arose as the result of an increase in the angle between the forehead and the frontal cranial base and a decrease in the angle of the cranial base at the sella turcica.
Evolutionary remnants
NegusReference Negus20 stated that ‘there does not appear to be any functional reason for the appearances of air spaces, and the irregularity of their distribution, often with complete absence, suggests that they are only unwanted residual spaces’. Rae and KoppeReference Rae and Koppe41 observe that the maxillary sinuses are ‘the taxonomically most widespread paranasal pneumatisation’. They note that they are present in many groups of mammalsReference Moore42 and were probably present in the last common ancestor of eutherians.Reference Novacek, Hanken and Hall43 The maxillary sinuses were then retained in many anthropoids,Reference Hershkovitz44–Reference Rossie47 including humans. Rae and Koppe suggest finally that their presence requires ‘no additional explanation; these organisms possess the sinus because their ancestors did’.
Lightening the skull bones to maintain equipoise of the head
The theory that the sinuses developed as an aid to maintaining balance of the head has been proposed by several authors.Reference Vesalius2, Reference Galen and Tallamadge4, Reference Da Vinci6, Reference Highmore10 However, Braune and ClasenReference Braune and Clasen22 calculate that if the sinuses were instead composed of spongy bone, then a 1 per cent increase in the weight of the head would result; they consider this a negligible amount. Furthermore, an electromyographic investigation of the neck musculature's response to loading of the anterior aspect of the head concluded that the paranasal sinuses are not significant as weight reducers of the skull for the maintenance of equipoise.Reference Biggs and Blanton48
Flotation device
Both HardyReference Hardy49 and EvansReference Evans50 have suggested that the sinuses may act as a flotation device. HardyReference Hardy49 proposed that Australopithecus represented the link between Homo habilis and Homo sapiens and anthropomorphic monkeys. Australopithecus was thought to be cut off from the African mainland 6.5 million years ago. Forced to adapt by natural selection, the monkeys developed the paranasal sinuses as flotation devices to allow maintenance of the cephalic part and therefore to maintain the nasal cavities out of water. However, Rae and KoppeReference Rae and Koppe41 note that the same group of sinuses occur in all African apes, and they consider it extremely unlikely that an aquatic way of life was the selective evolutionary pressure behind this. The same authors,Reference Rae and Koppe41 citing Gould and Vrba,Reference Gould and Vbra51 comment that an important distinction needs to be drawn in the study of ‘function’ between utility and evolutionary origin. They state that ‘while a structure may permit a particular behaviour in an extant organism, this is no guarantee that this function was responsible for the original evolution of the trait’.
Secreting mucus to moisten the nasal cavity
This theory, advocated by Haller,Reference Haller52 has now been dismissed on the basis of histology,Reference Mygind and Winther53 which shows that the sinuses have only 50–100 submucosal glands, in contrast to the nose with its 100 000 glands. It is therefore suggested that the sinuses cannot secrete a meaningful amount of mucus. BallengerReference Ballenger54 noted that the mucus from the sinuses is ‘uncontaminated’, and proposed an alternative role whereby the sinus mucus might dilute inspired contaminants in the nasal mucus.
Aiding nasal cavity immune defence and production of nitric oxide
The paranasal sinuses are known to play a role in strengthening immune nasal function, with the additional production of immunoglobulins and lythic enzymes (such as lisozyme) which destroy peroxidases and the peptidoglycans of bacterial cell walls.Reference Levine and Clemente24 Mucociliary clearance into the nasal cavity could then bolster nasal immune defences.
Nitric oxide has been proven to be generated by both the paranasal sinuses and the nasal cavity.Reference Haight, Djupesland, Qjan, Chatkin, Furlott and Irish55, Reference Lundberg, Farkas-Szallasi, Weitzberg, Rinder, Lidholm and Anggard56 Furthermore, the sinuses are capable of generating high concentrations of NO, of greater than 20 parts per million,Reference Lundberg, Farkas-Szallasi, Weitzberg, Rinder, Lidholm and Anggard56 and higher concentrations still are generated in the nasal cavity.Reference Menzel, Hess, Bloch, Michel, Schuster and Gabler57 The importance of NO in this area is thought to be twofold, involving both inhibition of viral and bacterial growth and upregulation of ciliary beat frequency.Reference Haight, Djupesland, Qjan, Chatkin, Furlott and Irish55 It may therefore be that the paranasal sinuses act as an adjunct in providing the nasal cavity with NO.
Discussion
Theories of the possible role of the paranasal sinuses generate both controversial and complex issues. While some of the older theories may be easily dismissed, others seem frustratingly difficult to either confirm or refute, partially due to a lack of relevant, hard evidence. The most recently proposed theories have at least been exposed to the rigour of scientific investigation, allowing us perhaps to edge towards a possible, acceptable explanation of paranasal sinus function.
Levine and ClementeReference Levine and Clemente24 believe that the paranasal sinuses may act simply to improve nasal function; certainly, it has been demonstrated that they may act as an adjunct in the production of NO and in aiding the immune defences of the nasal cavity. While this would give the paranasal sinuses a role, and proves at least that they are not, as was once thought, without function,Reference Negus20 it might not necessarily answer the question ‘why do we have paranasal sinuses?’ As previously stated, when considering function there is a distinction between utility and evolutionary origin.Reference Gould and Vbra51 It may still be that the sinuses arose as an aid to facial growth and architecture, or that they persist as residual remnants of an evolutionary structure with an as yet unknown purpose, and in doing so have found an additional role as an adjunct to the nasal cavity.
