Textbook descriptions of the morphology of the adult maxillary sinus address the volume and the degree of pneumatization of the pyramidal cavity lateral to the zygoma and inferiorly relative to the nasal floor and maxillary dentition (Zuckerkandl, 1892). Alterations in its morphology from a variety of pathologic states is mentioned and collectively attributed to damage to the growth centers in the maxilla, or the demand for marrow production inhibiting pneumatization. It is the purpose of this article to identify and clarify the different mechanisms by which diverse pathologic conditions alter maxillary sinus configuration and volume.
The maxillary sinus is universally described as a pyramidal-shaped cavity in the maxilla. Hypoplasia, which can occur unilaterally or bilaterally, is graded by the authors by the degree of failure of descent below the nasal floor in achieving its position adjacent to the posterior dentition in the adult. Unlike early studies using plain X-rays, which considered pneumatization into the zygomatic recess and dental alveolus as criteria, the authors have adopted the above-cited parameters based on computed tomography (CT) imaging, which reveals that even when smaller the sinus retains a pyramidal configuration, although truncated. Rarely, the sinus is excessively pneumatized in the nonpathologic state. Review of the literature failed to reveal a comprehensive study of the conditions that alter maxillary sinus volume and configuration. Based on a retrospective review of 6,000 high resolution CT scans of the paranasal sinuses, the types and relative incidences of these conditions have been determined, and a classification system proposed. The mixed-sex sample group (= 2,540) was comprised of nonpediatric (adolescent and adult) and was of a polyethnic composition. Results showed that enlargement of the sinus is uncommonly encountered, and is produced by air (pneumocele) and mucus (mucocele) entrapment, or by benign tumors which have arisen in the sinus or adjacent maxilla and have grown intracavitarily, with the sinus walls expanding and remodeling to accommodate them. Reduction in size and volume is more frequent. Heredo-familial syndromic conditions reduce sinus size by impaired facial growth centers, or obliteration by dense osteosclerosis. Irradiation for neoplastic disease in the pediatric population similarly, directly effect growth centers, or impairs pituitary function. Another iatrogenic cause, direct surgical intervention (Caldwell-Luc procedure) almost universally alters sinus volume and shape by osteoneogenesis. Midfacial fractures involving the sinus also produce distortion by sclerosis as well as by malpositioning of bone fragments. The principal systemic disorders, sickle cell anemia and osteopetrosis, which diffusely effect medullary bone, do so either through compensatory marrow proliferation or sclerotic new bone formation, thus serving to produce maxillary enlargement and sinus obliteration. The greatest source of maxillary sinus distortion and destruction are neoplasms. Malignant sinonasal and oral cavity tumors produce bony erosion of the sinus walls, whereas benign odontogenic cysts remain external to the sinuses and compress it as they enlarge. Most odontogenic tumors produce external compression and remodeling. Fibro-osseous disorders similarly produce size and shape distortions by external impingement. Although diverse developmental and pathological conditions influence maxillary sinus morphology, there is a limited range of biologic response. Anat Rec, 291:1554–1563, 2008. © 2008 Wiley-Liss, Inc.
MATERIALS AND METHODS
The source of this retrospective study is based on the examination of 6,000 high resolution, multiplanar computed tomography (CT) scans of the paranasal sinuses from the senior author's practice at a tertiary care medical center encompassing a 10-year period. The mixed-sex sample group (N = 2,540) was comprised of nonpediatric (adolescent and adult) and was of a polyethnic composition. The scans were performed because of complaints suggestive of sinonasal, or maxillary disease. Infections, which comprised the greatest number of the abnormal findings, have been eliminated as mucous membrane thickening reduced the sinus cavity volume, but there was no alteration in the integrity or shape of its walls.
The maxillary sinus has limited methods of morphologic change in response to diverse pathologic processes, namely, enlargement and reduction of its volume. The different mechanisms by which this occurs are summarized in Table 1. The types and incidence of the pathologic processes involving the maxillary sinus encountered in this review are summarized in Table 2. The most common lesions seen were malignant neoplasms, principally squamous cell carcinomas, arising primarily in the sinus, or extending there secondarily from the oral cavity. The hallmark of these tumors is their infiltrative growth which while enlarging the maxilla and sinus by a mass effect, produces extensive bone destruction leaving no recognizable normal architecture. Adenocarcinomas are slower growing tumors permitting sinus wall remodeling in some areas and causing erosion at other sites.
|Mucocele Pneumatocele||Mucus Trapping air trapping|
|Silent sinus syndrome||Atelectasis|
|Zygoma, maxilla||Displaced bone, fat|
|Tumors||Mass ingrowth, invasion|
|Fibro-osseous||Abnormal bone growth|
|Odontogenic lesions||Wall displacement, infiltration|
|Squamous cell carcinoma||36|
|Squamous cell carcinoma||44|
|Silent sinus syndrome||1|
Benign tumors arising in the sinus, or surrounding bone, grow into the sinus cavity and as they enlarge, the sinus expands around them leaving a peripheral rim of air. An enlarged maxillary sinus encasing a central mass, points to the diagnosis of a benign tumor. Notable exceptions to this statement are such aggressive inflammatory lesions as the pseudotumor and giant cell granuloma.
Odontogenic tumors arising from the dentoalveolar apparatus generally enter and expand inside the sinus. The most common type, the ameloblastoma, whereas histologically benign can be locally aggressive, producing extensive bone destruction. The hallmark of these tumors is their involvement of the alveolus, their site of origin. Unlike the mandible, unerupted impacted or displaced teeth were uncommonly found in the maxilla.
Odontogenic cysts have a characteristic appearance. They never invade the maxillary sinus and as they enlarge they displace and constrict the sinus itself. A lamella of bone separates them, often giving the appearance of a septate sinus. The dentigerous cyst arises from the dental follicle of an unerupted tooth and can be identified by the presence of a tooth in the periphery of the cyst.
Developmental, congenital, iatrogenic, traumatic, and systemic disorders also contributed to reduction of the maxillary sinus, albeit with less frequency than neoplastic lesions.
An understanding of the embryology and development of the maxillary sinus is essential in assessing its degree of pneumatization in the adult on an age-related basis. Although the development of the paranasal sinuses begins in the third week of gestation, it continues through early adulthood. At three–and-a-half weeks, ectodermal cells proliferate and migrate medially to form the notochord. Initially formed in the caudal region of the embryonic disc, the notochord soon rotates to lie posterior to the primitive foregut. Adjacent to the notochord lies the paraxial layer of mesenchyme, which eventually differentiates into the somite ridges, intermediate cell mass and lateral plate mesoderm. From these mesodermal structures arise the branchial arches, the first of which, in turn, gives rise to the internal nasal structures.
At 12 weeks, turbinate structures have become established intranasally and palatal fusion has occurred. Ectodermal invagination begins in the middle meatal groove, growing laterally, to reach the proportions of 7 × 4 × 4 mm at birth. The maxillary sinus is filled with fluid until birth, at which point it becomes pneumatized. Growth of the sinus after birth is biphasic, with rapid growth during the first 3 years, and then again from the age of 7 to 12. Growth between the ages of 3 and 7 occurs at a slower pace, and then again after the age of 12, growth slows until early adulthood. At the age of 9–12, the floor of the sinus is usually level with the floor of the nose. After this point, the floor of the sinus descends as permanent teeth begin eruption, and pneumatization can be extensive enough as to expose the tooth roots which may have only a thin covering of soft tissue within the sinus (Wang et al., 1994).
Morphology and Anatomy
When fully pneumatized, the adult maxillary sinus is a pyramidal structure, with the nasal wall as the base and the lateral apex extending into the zygomatic process of the maxillary bone, or into the zygoma. The average volume is 15 ml, with the dimensions of ∼33 mm in height, 23–25 mm in width, and 34 mm in the anteroposterior axis (Karmody et al., 1977).
Frequently encountered variations in antral volume and configuration involve posterior extension toward the zygoma (zygomatic recess), and inferior pneumatization into the dental alveolus about the roots of the posterior teeth, or between them in edentulous areas (Fig. 1). Anteriorly, the maxillary sinus does not extend beyond the first premolar tooth, with the canine and incisor teeth positioned below the nasal cavity (Márquez et al., 2002). Only one instance was found where a fingerlike projection of the sinus extended below the distal portion of the nasolacrimal duct to the pyriform aperture. In two cases, pneumatization of the palatal shelf of the maxilla was encountered. Pneumatization was not seen to extend medial to the lamina papyracea of the ethmoid, or deform the curvature of the orbital floor in nonpathologic states. Extreme hypertrophy of the inferior turbinates has been seen to remodel the medial wall in the inferior meatus into the sinus (Fig. 2).
Enlargement of the maxillary sinus.
There have been multiple reports in the literature of hyperpneumatization of the maxillary sinus. As more cases have come to publication, a terminology has evolved to discuss the types of pneumatization (Trimarchi et al., 2003)
If a patient is asymptomatic and the sinus does not compress structures beyond its borders, it is termed a hypersinus. If the patient has cosmetic, or local pressure symptoms, and the sinus is encroaching on other structures beyond the normal boundary with intact bony walls, it is termed pneumosinus dilitans. When the bony sinus walls are thinned, or have loss of integrity, it is termed a pneumocele. If there exists or develops a structural defect in the bony sinus wall and the air then moves outside of the sinus into surrounding tissues, this is termed a pneumatocele (Fig. 3).
The presence of a defective “valve” at the ostiomeatal complex delaying pressure equilibration has not been demonstrated, and the concept of an air trapping ball valve remains theoretical.
The term mucocele refers to a cystic dilatation produced by progressive mucus formation from a blocked excretory duct (Fig. 4). In the case of the maxillary sinus, it is the result of obstruction of the natural ostium in the middle meatus. With both pneumoceles and mucoceles, the sinus walls expand, producing facial enlargement and elevation of the orbital floor displacing the eye outward.
Reduction of maxillary sinus.
The basis of reduction of the volume of the maxillary sinus is multifactorial and includes congenital and acquired variants. Among the latter are neoplastic, traumatic, iatrogenic, and systemic causes. We only address those disorders which cause a reduction of the actual bony configuration and anatomic borders of the sinus in this discussion section
Although complete aplasia of the maxillary sinus can occur, it is extremely rare, whereas maxillary sinus hypoplasia (MSH) is a well-known clinical entity. There are three types: MSH-Type I is characterized by mild-to-moderate hypoplasia, a normally developed uncinate process and well-defined infundibulum, with varying degrees of mucosal thickening within the sinus. MSH-Type II is characterized by a hypoplastic uncinate process and an ill-defined or absent infundibular passage, marked hypoplasia of the sinus and total opacification of the sinus by soft tissue density on CT scan. MSH-Type III shows an extremely hypoplastic or absent uncinate process with profound hypoplasia of the sinus, only noted as a shallow cleft along the lateral nasal wall (Erdem et al., 2002; Bassiouny et al., 1982). Unilateral and bilateral hypoplasia occurs in less than 10% of patients. Examples of varying degrees of incomplete pneumatization are seen in Figures 5 and 6
Syndromal etiologies of MSH can be broadly divided into lack of development from failure of midfacial skeleton growth and obliteration of the sinus cavities from osteosclerosis. Over 100 forms of craniofacial dysostoses exist. The majority are bilateral and include mandibular dysostosis (Treacher-Collins syndrome), Acrocephalosyndactyly (Apert's syndrome), craniofacial dysostosis (Crouzon's syndrome), and maxillomandibular dysplasia (Binder's syndrome). However, in Goldenhar's syndrome (hemifacial microsomia), the size of the maxillary sinus is reduced by unilateral hyperplasia of the lateral maxilla and zygoma. In Williams syndrome, or Elfin Face syndrome, the diminutive face is secondary to failure in prenatal and post-natal growth and is reflected in the paranasal sinuses being small bilaterally.
In the other group, hereditary dysplasias causing osteosclerosis (e.g., progressive diaphyseal dysplasia, generalized cortical hyperostosis, craniometaphyseal dysplasia, craniodiaphyseal dysplasia), produce changes in the skull and facial bones and also in the axial skeleton by forming dense osteosclerosis, which narrows and partially obliterates the maxillary sinuses (Som et al., 2003).
Silent sinus syndrome.
Whereas MSH is considered to stem from changes in embryologic development, silent sinus syndrome (SSS) is postulated to be the acquired corollary. Classically, an asymptomatic patient develops enopthalmos spontaneously. Radiographically, a small shrunken sinus is seen with remodeling and depression of the orbital floor (Fig. 7). Obstruction of the natural ostium is thought to be the initiating factor, with resorption of gases generating negative pressure and leading to demineralization and bowing of the walls into the sinus, creating an atelectatic sinus (Wise et al., 2007)
The single greatest source of alteration of the maxillary sinus was malignant neoplasms arising in the sinus, principally squamous cell carcinomas. As the tumor proliferates, the cavity is filled and the adjacent walls are invaded and destroyed; with advanced tumors there may be no recognizable sinus, only an irregular soft tissue mass. Malignant tumors arising from the maxillary alveolus may grow into the sinus but generally destroy only its floor, whereas intracavitary tumors have multidirectional growth. The hallmark of malignant tumors is an irregular appearing sinus due to the loss of its bony walls and intrasinal soft tissue
Benign tumors of the maxillary sinus are extremely rare and include salivary gland neoplasms, inverted papillomas (Fig. 8) and osteomas, which produce an intracavitary mass which can expand the sinus if large. Primary benign tumors of the maxilla (neurogenic, vascular tumors), behave like odontogenic lesions and distort the sinus by impingement. They can also enter the sinus causing expansion and remodeling. An exception is the pseudotumor, which is a chronic inflammatory lesion that can produce extensive destruction and distortion of the maxillary sinus (Som et al., 1994)
Odontogenic cysts encroach upon the maxillary sinus by displacing one of its walls, depending on its site of origin. Inflammatory (radicular) cysts arising from the roots of nonvital teeth elevate the antral floor, while developmental (dentigerous, keratocysts) cysts displace the posterior and lateral walls (Figs. 9 and 10). They are noninvasive and can create what appears to be a duplicate sinus. Benign odontogenic tumors (myxoma, cementoma, odontoma) similarly narrow the maxillary sinus by external compression (Fig. 11). Ameloblastomas, although histologically benign, are locally invasive and can infiltrate the sinus. Radiographically, the sinus walls may be remodeled, or destroyed (Fig. 12). The calcifying epithelial odontogenic tumor (Pindborg tumor) presents similarly (Verbin and Barnes, 2000)
Fibro-osseous disorders may broadly be divided into ossifying lesions (osteomas, ossifying fibroma), fibrous dysplasia, and Paget's disease. The ossifying fibroma (also cementifying fibroma) is an encapsulated benign bony neoplasm that encroaches upon the antrum by mass effect. It arises from the alveolar segment of the maxilla and expands internally towards the sinus rather than deform the outer surface bones (Fig. 13)
Fibrous dysplasia is an idiopathic skeletal disorder in which medullary bone is replaced by poorly organized weak fibro-osseous tissue. It occurs in a monostotic (Fig. 14) and polyostotic (Fig. 15) form, both of which can involve the craniofacial bones. In the maxilla, the abnormal “woven” bone gradually replaces the normal medullary bone, enlarging the maxilla and progressively obliterating the maxillary sinus cavity.
By contrast, in Paget's disease, or osteitis deformans, the maxilla is enlarged bilaterally, especially in its posterior aspect, by the formation of abnormal bone formed by both osteoclastic and osteoblastic activity. In the head, it is a polyostotic process effecting principally the calvarium, skull base, and jaws. In replacing the normal medullary bone, both sinus cavities become progressively obliterated (Fig. 16).
Midfacial fractures commonly change maxillary sinus shape and volume by telescoping, or rotation, of bony fragments into the sinus. This is especially true with zygoma fractures which, when rotated medially and posteriorly, truncate the pyramidal configuration of the sinus to create a “microantrum”. Orbital floor “blowout” fractures, if minimal, produce a teardrop of herniated fat in the roof of the maxillary sinus, or if severe, cause lowering of the roof. LeFort fractures of the maxilla acutely produce sinus cavity enlargement by downward displacement of the maxilla. Postreduction, the pre-injury volume is approximated, but there may remain the telltale signs of wall fractures and irregularities and areas of bony sclerosis
Transoral surgical access to the maxillary sinus through the canine fossa is eponymically known as the Caldwell-Luc procedure. The paranasal sinuses possess the idiosyncratic ability to auto-obliterate by osteoneogenesis and fibrosis, following disturbance and removal of their lining. This varies in degree with different sinuses, but is most marked in the maxillary and frontal sinuses. In the maxillary sinus, the process progresses medially from the zygomatic recess in varying degrees, producing lateral narrowing to near total obliteration (Fig. 17). The condition can be distinguished from developmental hypoplasia by the presence of a surgical defect in the lateral wall and the dense bony sclerosis of the remaining walls
Controversy has surrounded the role of endoscopic sinus surgery in the pediatric population in causing sinus hypoplasia secondary to growth center injury. However, no evidence exists for this (Bothwell et al., 2002).
Radiotherapy for malignancy in childhood will damage midface growth centers; the extent of destruction depending on the size of radiation portals, the dosage, and the age at which radiation was delivered. In the midface, the sinuses in the field of radiation will be hypoplastic by developmental arrest in an age-related manner when compared with the untargeted side (Gevorgyan et al., 2007).
Hematologic conditions affecting the marrow space of the facial bones can lead to MSH. This has been reported in sickle cell anemia and thalassemia, principally the former. As with all marrow spaces in the body, the medullary spaces of the maxilla are widened to accommodate the need for increased production of blood cells, leading to a decrease in the volume, or obliteration, of the sinus itself (Som et al., 2003)
Hypoplasia of the maxillary sinus has been reported with primary and acquired hypopituitarism and hypothyroidism (Kornreich et al., 2002, Scharf and Laron, 1972). As discussed before with cranial irradiation, pituitary injury may affect the release of growth hormone and decrease the ability of the facial bony growth centers to develop fully. This is also true of decreases in thyroid hormone as it too plays a central role in growth and metabolism
Osteopetrosis (Albers-Schonberg disease, Brittle Bone disease) is a family of heredo-familial disorder, in which a proliferation of abnormally dense bone replaces the normal medullary bone, resulting in marrow space and sinus cavity obliteration (Fig. 18) (Tolar et al., 2004)
Developmental variability in maxillary sinus morphology is principally limited to varying degrees of hypoplasia arising in a small number of individuals, yet still maintaining its pyramidal configuration. This configuration is present also in pathologic conditions involving growth center arrest, from genetic syndromal conditions, or acquired from interval pressure alterations, or osteonecrosis.
The plasticity of the maxillary sinus is seen in its ability to expand and compress its walls in response to an internal or external slow growing mass. Aggressive infiltrating lesions will produce bone destruction and often reveal a mixed radiological pattern of remodeling and erosion. Lesions involving the medullary spaces (fibro-osseous disorders, hereditary anemias and bone dysplasias) will progressively obliterate the sinus.
The high frequency of variation seen in the normal and abnormal anatomy of the maxillary sinus, and how this sinus preserves its morphology across polyethnic groups, continues to intrigue the authors. While volume differences may vary in diverse populations, there is a relatively uniform response to a multiplicity of stresses across these ethnic boundaries.
Although this retrospective survey encompasses a time period of only 10 years, I wish to acknowledge those individuals that I have greatly benefited from, and whose collegiality made it a pleasure to come to work. Starting with Joseph Goldman and Dr. Max Som who revolutionized diagnosis with the use of imaging, and whose son, Dr. Peter Som, continues that level of excellence, and to Dr. Hugh Biller who, as chair, gave me the opportunity to develop the subspecialty of rhinology. To Dr. Jeffrey T. Laitman, a dear colleague of over 35 years, whose patience for this project is greatly appreciated. Finally, I would like to thank Dr. Samuel Márquez, for inviting the authors to participate in this special issue on paranasal sinuses, who as a graduate student would shadow me during patient examination and observe me during surgery for the purposes of documenting sinus variation, and who continues to do so even after his doctorate.