Chapter 38 Maxillary Sinus Anatomy, Pathology, and Graft Surgery

Carl E. Misch, Randolph R. Resnik, Francine Misch-Dietsh

Maxillary posterior partial or complete edentulism is one of the most common conditions in dentistry.¹ Thirty million people in the United States, or 17.5% of the adult population, are missing all of their maxillary teeth. In addition, 20% to 30% of the adult partially edentulous population older than 45 years is missing maxillary posterior teeth in one quadrant, and 15% of this age group is missing the maxillary dentition in both posterior regions. In other words, approximately 40% of adult patients are missing at least some maxillary posterior teeth. This chapter addresses the treatment concepts specific to the maxillary posterior partial or complete edentulous regions.

The maxillary posterior edentulous region presents many unique and challenging conditions in implant dentistry. Most noteworthy surgical methods include sinus grafts to increase available bone height, onlay grafts to increase bone width, and modified surgical approaches to insert implants in areas with poorer bone density.² Grafting of the maxillary sinus to overcome the problem of reduced vertical available bone has become a very popular and predictable procedure over the last decades. After the initial introduction by Tatum in the mid 1970s and the initial publication of Boyne and James in 1980, many studies have been published about sinus grafting with positive results.³–³⁸ In 1983, Misch² observed the most predictable intraoral region to grow bone height is on the maxillary sinus floor, once the sinus mucosa has been elevated. This statement still holds true today.

ANATOMICAL CONSIDERATIONS OF THE POSTERIOR MAXILLA

The maxilla has a thinner cortical plate on the facial compared with any region of the mandible. In addition, the trabecular bone in the posterior maxilla is finer than other dentate regions. The loss of maxillary posterior teeth results in an initial decrease in bone width at the expense of the labial bony plate. The width of the posterior maxilla decreases at a more rapid rate than in any other region of the jaws.³⁹ The resorption phenomenon is accelerated by the loss of vascularization of the alveolar bone and the existing fine trabecular bone type. However, because the initial residual ridge is so wide in the posterior maxilla, even with a 60% decrease in the width of the ridge, adequate-diameter root form implants usually can be placed. However, the ridge progressively shifts toward the palate until the ridge is resorbed into a medially positioned narrower bone volume.⁴⁰ The posterior maxilla continues to progressively remodel toward the midline as the bone resorption process continues. This results in the buccal cusp of the final restoration often being cantilevered facially to satisfy esthetic requirements at the expense of biomechanics in the moderate to severe atrophic ridges.⁴¹

DENTAL CONTRAINDICATIONS FOR IMPLANT TREATMENT OF THE POSTERIOR MAXILLA

A rule in traditional prosthodontics is that a fixed prosthesis is contraindicated when the canine and two adjacent teeth are missing. Therefore, when the canine and both premolars are missing, a fixed restoration is contraindicated. A removable prosthesis that has no movement under function is considered a fixed prosthesis and therefore should follow the rules of treatment planning for a fixed prosthesis in relation to implant number and position. A minimum of a healthy natural canine tooth or an implant abutment in the canine region is required before posterior implants are considered in the quadrant.

Abnormal intraoral conditions may compromise the final outcome of sinus-grafting procedures and/or the survival rates of dental implants placed in the grafted sinuses. These contraindications are similar to those reported for standard implant treatment of edentulous patients and may be summarized as follows:

• Inadequate oral hygiene

• Untreated periodontal disease of the residual dentition

• Severe malocclusion

• Severe bruxism with loss of incisal guidance

• Active infection

Decreased Crown Height Space

The crown height space (CHS) should be evaluated before implant placement. Once the occlusal plane is properly restored or modified, the CHS should be greater than 8 mm (Figure 38-1). If less space is available for prosthodontic reconstruction, then a gingivectomy is first considered because it is not uncommon for excess tissue thickness to be present in this region. However, if tissue reduction cannot correct the CHS problem, then osteoplasty and/or vertical osteotomy of the maxillary posterior alveolar process are indicated to improve the vertical ridge orientation before implant surgery.

Figure 38-1 The crown height space (CHS) in the posterior maxilla should be at least 8 mm for prosthetic reconstruction. Reduced CHS requires osteoplasty before implant insertion, which reduces the existing available bone height.

Poor Bone Density

In general, the bone quality is poorest in the posterior maxilla compared with any other intraoral region.⁴² A literature review of clinical studies from 1981 to 2001 reveals the poorest bone density may decrease implant loading survival by an average of 16%, and it has been reported as low as 40%.⁴³ The cause of these failures is related to several factors. Bone strength is directly related to its density, and the poor-density bone of this region is often five to 10 times weaker compared with bone found in the anterior mandible.⁴⁴ Bone densities directly influence the bone-implant contact percent (BIC), which accounts for the force transmission to the bone. The BIC is least in D4 bone, and the stress patterns in this bone migrate farther toward the apex of the implant (Figure 38-2). As a result, bone loss is more pronounced and occurs also along the implant body, rather than only crestally as in other denser bone conditions. D4 bone also exhibits the greatest biomechanical elastic modulus difference when compared with titanium under load.⁴⁴ As such, strategic choices to increase BIC are suggested.

Figure 38-2 The bone-implant contact percent is often reduced in the posterior maxilla, because the quality of bone is poorer than other regions of the mouth.

In the posterior maxilla, the deficient osseous structures and an absence of cortical plate on the crest of the ridge is often observed, which further compromises the initial implant stability at the time of insertion. The labial cortical plate is thin, and the ridge is often wide. As a result, the lateral cortical BIC to stabilize the implant is often insignificant. Implant surgery more often uses bone compression rather than bone extraction to create the implant osteotomy to compensate for these deficiencies. As a consequence, initial healing of an implant in D4 bone is often compromised.

Implant Size

The ideal length of the implant is directly related to the implant width, the design, the amount of the forces, and the bone density. Because implant success after loading is reduced in implants shorter than 10 mm, it is logical to treatment plan longer implants in the region. In general, 4-mm threaded root form implants should be at least 12 mm in length when the bone density is poor. This usually provides adequate BIC to dissipate the loads applied to the prosthesis. Implants longer than 16 mm are not necessary, even in the softest bone type, because the stress transfer is not dissipated beyond this length. Therefore the implant most often should be 12 to 16 mm long in this region of the mouth. Sinus grafting is usually required before or in conjunction with implant placement to gain adequate bone height for implants of adequate length in this region. The poor bone density requires implants of a larger size, including length. The implant length requirement is greater because the transmission of stress is expressed farther down the implant length.

MAXILLARY SINUS

The anatomy of the maxillary sinuses was first illustrated and described by Leonardo da Vinci in 1489 and later documented by the English anatomist Nathaniel Highmore in 1651.⁴⁵ The maxillary sinus (or antrum of Highmore) lies within the body of the maxillary bone and is the largest of the paranasal sinuses, as well as the first to develop (Figure 38-3).

Figure 38-3 The maxillary sinuses (1) are the largest of the paranasal sinuses, followed by the frontal (2), ethmoid (3), and sphenoid sinuses (4).

Maxillary Sinus Development

A primary pneumatization of the maxillary sinus occurs at about 3 months of fetal development by an out-pouching of the nasal mucosa within the ethmoid infundibulum. At this time the maxillary sinus is a bud situated at the infralateral surface of the ethmoid infundibulum between the upper and middle meatus.⁴⁶ Prenatally, a secondary pneumatization occurs. At birth, the sinuses are filled with fluid and the maxillary sinus is still an oblong groove on the mesial side of the maxilla, just above the germ of the first deciduous molar.⁴⁷

Postnatally and until the child is 3 months of age, the growth of the maxillary sinus is closely related to the pressure exerted by the eye on the orbit floor, the tension of the superficial musculature on the maxilla, and the forming dentition. As the skull matures, these three elements influence its three-dimensional (3D) development. At 5 months, the sinus appears as a triangular area medial to the infraorbital foramen.⁴⁸

During the child’s first year, the maxillary sinus expands laterally underneath the infraorbital canal, which is protected by a thin bony ridge. The antrum grows apically and progressively replaces the space formerly occupied by the developing dentition. The growth in height is best reflected by the relative position of the sinus floor. At 12 years of age, pneumatization extends to the plane of the lateral orbital wall, and the sinus floor is level with the floor of the nose. The main development of the antrum occurs as the permanent dentition erupts and pneumatization extends throughout the body of the maxilla and the maxillary process of the zygomatic bone. Extension into the alveolar process lowers the floor of the sinus about 5 mm (Figure 38-4). Anteroposteriorly, the sinus expansion corresponds to the growth of the midface and is completed only with the eruption of the third permanent molars when the young person is about 16 to 18 years of age.⁴⁶–⁴⁸

Figure 38-4 The maxillary sinus development increases in size during the growth of the midface of the maxilla and is also related to the eruption of the deciduous teeth, followed by the permanent dentition.

In the adult, the sinus appears as a pyramid of five thin, bony walls. The base of this pyramid faces the lateral nasal wall and often measures 33 × 33 mm; its apex extends approximately 23 mm toward the zygomatic bone.^49,⁵⁰ The dentate adult maxillary sinus has an average volume of 15 mL, although the range is 9.5 to 20 mL.⁵¹ The floor of the maxillary sinus cavity is reinforced by bony or membranous septa joining obliquely or transversely from the medial and/or lateral walls with buttresslike webs. They may be genetic or develop as a result of stress transfer within the bone over the roots of teeth. These have the appearance of reinforcement webs in a wooden boat and rarely divide the antrum into separate compartments. These elements are present from the canine to the molar region, and Misch⁴¹ has observed they tend to disappear in the maxilla of the long-term edentulous patient when stresses to the bone are reduced. Karmody et al.⁵² found that the most common oblique septum is located in the superior anterior corner of the sinus or infraorbital recess (which may expand anteriorly to the nasolacrimal duct). The medial wall is juxtaposed with the middle and inferior meatus of the nose.

Although the adult maxillary sinus maintains its overall size while the teeth are present, a rather rapid expansion phenomenon of the maxillary sinus occurs with the loss of posterior teeth. In fact, even with the loss of a single molar, the sinus expands between the adjacent tooth roots. In the edentulous maxilla, the antrum expands in both inferior and lateral dimensions and may even invade the canine eminence region and proceed to the lateral piriform rim of the nose. This results in a lack of available bone in the posterior maxilla and a greatly decreased height from both the sinus expansion and the crestal resorption. Frequently, less than 10 mm remains between the alveolar ridge crest and the floor of the maxillary sinus in the edentulous posterior maxilla. This limited dimension is compounded by the problem of bone of reduced quality and the resultant medial posterior position of the ridge after resorption of bone width. As a result, compromises in the long-term prognosis of many endosteal implant systems are reported.⁴³

Maxillary Sinus Anatomy

Maxillary sinus grafts have become a predictable procedure before or in conjunction with implant insertion. However, infections of the maxillary sinus are common and may not only cause implant failure but also may be life-threatening to the patient. As a result, the dentist should be knowledgeable of both the macroscopic and microscopic anatomy, as well as the pathologic conditions that may occur before or postoperative to the sinus graft procedure.

Six bony walls that contain many structures of concern during sinus graft surgery surround the maxillary sinus.^45,⁵³ Knowledge of these structures is crucial for both preoperative assessment and postsurgical complications.

Anterior Wall

The anterior wall of the maxillary sinus consists of thin, compact bone extending from the orbital rim to just above the apex of the cuspid. With the loss of the canine, the anterior wall of the atrum may approximate the crest of the residual ridge. Within the anterior wall and approximately 6 to 7 mm below the orbital rim, with anatomic variants as far as 14 mm from the orbital rim, is the infraorbital foramen (Figure 38-5). The infraorbial nerve runs along the roof of the sinus and exits through the foramen. The infraorbital blood vessels and nerves lie directly on the superior wall of the interior and within the sinus mucosa. Tenderness to pressure over the infraorbital foramen or redness of the overlying skin may indicate inflammation of the sinus membrane from infection or trauma. The anterior wall of the maxillary sinus may serve as surgical access during Caldwell-Luc procedures to treat a preexisting or post–sinus graft, pathologic condition.

Figure 38-5 The infraorbital foramen is located approximately 10 mm below the orbital rim. The anterior wall of the maxillary sinus in this skull has a horizontal cut just below the infraorbital foramen. The thin anterior wall is often used for surgical access to the maxillary sinus for Caldwell-Luc procedures.

Superior Wall

The superior wall of the maxillary sinus is shared with the thin orbital floor (Figure 38-6). The orbital floor slants inferiorly in a mediolateral direction and is convex into the sinus cavity. A bony ridge is usually present in this wall that houses the infraorbital canal containing the infraorbital nerve and associated blood vessels. Dehiscence of the bony chamber may be present, resulting in direct contact between the infraorbital structures and the sinus mucosa. Ocular symptoms may result from infections or tumors in the superior aspects of the sinus region and may include proptosis (bulging of the eye) and diplopia (double vision). When these problems occur, the patient is closely supervised and a medical consult is advised to decrease the risk of severe complications that may result from the spread of infection in a superior direction. Superior spreading infections may lead to a brain abscess and death. As a result, when these symptoms appear, aggressive therapy to decrease the spread of infection is indicated. Overpacking the maxillary sinus with bone graft material during a sinus graft may result in pressure against the superior wall if a sinus infection develops.

Figure 38-6 A frontal section of a head demonstrates the frontal sinus above and between the orbits and the maxillary sinuses directly below the orbits. A thin bony wall acts as the floor of the orbit and superior wall of the maxillary sinus. On the left, the infraorbital canal is in the outer third of the superior wall. On the right, the infraorbital canal is located at the junction of the apex of the superior and lateral-wall connection. The lateral wall of the sinus in this edentulous adult is the thickest wall but is only 1 mm thick. The medial wall of the maxillary sinus is thin, separates the maxillary sinus from the nares, and houses the inferior meatus in the bottom half of the sinus. Located in the superior-most aspect of this wall is the primary ostium that connects the maxillary sinus to the nares. The inferior wall represents the base of the existing posterior available bone and is the floor of the maxillary sinus.

Posterior Wall

The posterior wall of the maxillary sinus corresponds to the pterygomaxillary region, which separates the antrum from the infratemporal fossa. The posterior wall usually has several vital structures in the region of the pterygomaxillary fossa, including the internal maxillary artery, pterygoid plexus, sphenopalatine ganglion, and greater palatine nerve. The posterior wall should always be identified on the radiograph. When lack of a posterior wall is present, a pathologic condition (including neoplasms) is to be suspected.

It should be noted that pterygoid implants placed through the posterior sinus wall and into this region might approach vital structures, including the maxillary artery. Therefore a blind surgical technique to place a pterygoid implant through the posterior wall may have increased surgical risk. Because pterygoid implants are often positioned in the third or fourth molar region, they are of benefit primarily when third or fourth molars are needed for prosthetic reconstruction or sinus grafts are contraindicated and available bone posterior to the antrum is present.

Medial Wall

The medial wall of the antrum coincides with the lateral wall of the nasal cavity and is the most complex of the various walls of the sinus (see Figure 38-6). On the nasal aspect, the lower section of the medial wall corresponds to the lower meatus and floor of the nasal fossa; the upper aspect corresponds to the middle meatus. The medial wall is vertical and smooth on the antral side. Located in the superior aspect of the medial wall is the maxillary or primary ostium. This structure is the main opening through which the maxillary sinus drains its secretions via the ethmoid infundibulum through the hiatus semilunaris into the middle meatus of the nasal cavity. The infundibulum is approximately 5 to 10 mm long and drains via ciliary action in a superior and medial direction. This opening corresponds to the initial site of embryonic evagination from the nasal chamber. The ostium diameter averages 2.4 mm in health; however, pathologic conditions may alter the size to vary from 1 to 17 mm. Smaller, accessory or secondary ostia may be present that are usually located in the middle meatus posterior to the main ostium. These additional ostia are usually the result of chronic sinus inflammation and mucous membrane breakdown. They are present in approximately 30% of skulls, range from a fraction of a millimeter to 0.5 cm, and are commonly found within the membranous fontanelles of the lateral nasal wall.⁵⁴ Fontanelles are usually classified either as anterior fontanelles (AFs) or posterior fontanelles (PFs) and termed by their relation to the uncinate process. These weak areas in the sinus wall are sometimes used to create additional openings into the sinus for treatment of chronic sinus infections. Primary and secondary ostia may, on occasion, combine and form a large ostium within the infundibulum.

Lateral Wall

The lateral wall of the maxillary sinus forms the posterior maxilla and the zygomatic process (see Figure 38-6). This wall varies greatly in thickness from several millimeters in a dentate patient to less than 1 mm in an edentulous patient. The lateral wall houses an endosseous anastamosis of the infraorbital and posterior superior alveolar artery. The Tatum lateral-wall approach sinus graft procedure uses this area for entrance into the maxillary sinus (Figure 38-7).

Figure 38-7 The lateral wall of the maxillary sinus most often extends from the second premolar region to the posterior wall of the maxilla. This wall serves as the surgical access to the sinus floor and medial wall for the sinus graft procedure. In this intraoral view, the lateral sinus wall has been infractured and now serves as part of the ceiling of the sinus graft or as the floor of the smaller maxillary sinus.

Inferior Wall

The inferior wall or floor of the maxillary sinus is in close relationship with the apices of the maxillary molars and premolars (see Figure 38-6). The teeth usually are separated by the sinus mucosa by a thin layer of bone; however, on occasion, teeth may perforate the floor of the sinus and be in direct contact with the sinus lining. Studies have shown that the first molar has the most common dehiscent tooth root, occurring approximately 2.2% of the time. In dentate patients, the floor is approximately at the level of the nasal floor. In edentulous posterior maxillae, the sinus floor is often 1 cm below the level of the nasal floor. Complete or incomplete bony septa may exist on the floor in a vertical or horizontal plane. Almost 30% of the dentate maxillae have septa, with three fourths appearing in the premolar region.^55,⁵⁶ Complete septa separating the sinus into compartments are very rare, occurring in only 1.0% to 2.5% of maxillary sinuses.

Maxillary Sinus: Vascular Supply and Innervation

The blood supply to the maxillary sinus comes directly from the maxillary artery, which emanates from the external carotid artery. The maxillary artery supplies the bone surrounding the sinus cavity and also the sinus membrane. Branches of the maxillary artery, which most often include the posterior superior alveolar artery and infraorbital artery, form endosseous and extraosseous anastomoses that encompass the maxillary sinus. The endosseous anastomosis is found within the lateral wall of the sinus and supplies this structure and the lateral aspect of the sinus membrane. A posterior lateral nasal artery (a branch of the sphenopalatine artery that also rises from the maxillary artery) also supplies this region from the medial aspect of the sinus.

The formation of the endosseous and extraosseous anastomoses in the maxillary sinus is termed the double arterial arcade. The extraosseous anastomosis is less common (present in 44% of the population) and is found near the periosteum of the lateral wall. The extraosseous anastomosis is superior to the endosseous unit, which is approximately 15 to 20 mm from the dentate alveolar crest. In addition to the double arterial arcade, a blood supply from the sphenopalatine artery supplies the central and medial parts of the sinus membrane. This artery is also a branch of the maxillary artery and enters the maxillary sinus on the medial aspect via the maxillary ostium ⁵⁷(Box 38-1).

In an edentulous maxilla with posterior vertical bone loss, the endosseous anastamosis may be 5 to 10 mm from the edentulous ridge. The endosseous artery was able to be observed on computed tomography (CT) scans in approximately one half of the patients requiring a sinus graft.⁵⁸ In a long-term edentulous patient with a thin lateral wall, the artery may be atrophied and almost nonexistent. On rare occasions, this anatomical structure may be a concern for arterial bleeding complications during lateral-approach sinus elevation surgery.

Most often, implants of 12 to 16 mm in length should be used to support prostheses in the posterior maxilla, because the bone quality is poor and the occlusal force factors are high. Because the endosseous anastomosis is often present and ranges from 5 to 20 mm from the residual crest of the ridge, the lateral-access window for the sinus graft procedure often violates this arterial supply. However, this is usually of little concern during the surgical procedure and may even be of benefit postsurgery to provide a blood supply to the graft.

The size of the lateral-wall arterial anastomoses usually approximates 1.5 mm in a dentate patient and has little arterial pressure. Although the artery is often in the pathway of surgery for the Tatum lateral-wall approach to sinus grafting, endosseous bleeding is rarely observed as a pulsating rhythm and may be easily arrested by the following: (1) cutting the bone and vessel with a high-speed diamond and no irrigation (which cauterizes the vessel), (2) using electrosurgery on the vessel, and/or (3) elevating the head and using a surgical sponge (gauze) and slight pressure over the region for a few minutes. A hemostat may also be used to clamp the vessel, because it is readily observed; however, fracture of the lateral wall may occur.

The medial and posterior aspects of the maxillary sinus mucosa receive their blood supply from the posterior lateral nasal artery. The sphenopalatine artery is the third or fourth branch of the maxillary artery and enters the nasal cavity through the sphenopalatine foramen, which is near the posterior portion of the superior meatus of the nose. Once through the foramen, the sphenopalatine artery branches into the posterior lateral nasal artery and the posterior septal artery. The posterior lateral nasal artery supplies the medial and posterior walls of the antrum (nasal cavity).

The entire circulatory system in the maxillary sinus is a vital part of the healing and regeneration of bone after a sinus graft. Different factors can alter the vascularization in this area. With increasing age, the number and size of blood vessels in the maxilla decrease. As bone resorption increases, the cortical bone becomes thin, resulting in less vascularization. As the lateral wall becomes thinner, the blood supply to the lateral wall and lateral aspect of the bone graft comes primarily from the periosteum, resulting in a compromised vascularization to the region (Figure 38-8). After surgery the arterial supply in the lateral outer wall (in spite of being severed during the procedure) may help vascularize the sinus graft, because the anastomoses may vascularize the graft from both the posterior region and anterior region.

Figure 38-8 A maxillary ridge with advanced resorption results in a thinner lateral wall with no endosseous anastomosis. In this histologic cross section of a posterior edentulous maxilla, the available bone below the antrum is 2 mm in height and the lateral wall is 0.5 mm thick; a lack of endosseous anastomosis is evident.

The venous drainage of the maxillary sinus originates from a vascular plexus near the maxillary ostium that drains anteriorly into the facial vein and posteriorly into the maxillary and jugular veins.

The nerve supply to the maxillary sinus is via numerous branches of the second division of the trigeminal nerve, including the posterior alveolar nerves, anterior palatine, and infraorbital nerves. The infraorbital nerve is of concern in sinus elevation surgery because of its anatomical position. This nerve enters the orbit via the inferior orbital fissure and continues anteriorly; the nerve lies in a groove in the orbital floor (which is also the maxillary sinus superior wall) before exiting the infraorbital foramen. Anatomical variants have been reported to include a dehiscence and malpositioned infraorbital foramen, along with the nerve transversing the lumen of the maxillary sinus rather than coursing through the bone within the sinus ceiling (orbital floor).

Maxillary Sinus Mucosa: Microscopic Anatomy

The microscopic primary epithelial cells of the maxillary sinus are a continuation of the nasal mucosa and classified as a pseudostratified, ciliated columnar epithelium. However, the epithelial lining of the maxillary sinus is much thinner and contains fewer blood vessels compared with the nasal epithelium. This accounts for the membrane’s paler color and bluish hue. Five primary cell types exist in this tissue: (1) ciliated columnar epithelial cells, (2) nonciliated columnar cells, (3) basal cells, (4) goblet cells, and (5) seromucinous cells. The ciliated cells contain approximately 50 to 200 cilia per cell. In a healthy patient, they help to clear mucus from the sinus and into the nose. The nonciliated cells comprise the apical aspect of the membrane, contain microvilli, and serve to increase surface area. These cells have been theorized to facilitate humidification and warming of inspired air. The basal cell’s function serves most likely as a stem cell that can differentiate as needed. The goblet cells produce glycoproteins that are responsible for the viscosity and elasticity of the mucus produced. The maxillary sinus has the highest concentration of goblet cells in comparison with the other paranasal sinuses.

Although the sinus mucosa has been called a mucoperiosteum, Sharawy and Misch ⁵⁹ suggested that the periosteal portion of this membrane is not similar to the periosteum covering the cortical plates of the maxillary or mandibular residual ridges of the jaws and should not be considered a mucoperiosteum (Figure 38-9). The very minimal and usual absence of osteoblasts in this tissue and, instead, the presence of osteoclasts, may account for the enlargement of the antrum after tooth loss. The maxillary sinus membrane also exhibits few elastic fibers attached to the bone,⁵⁹ which simplifies elevation of this tissue from the bone. The thickness of the sinus mucosa varies, but is generally 0.3 to 0.8 mm.⁶⁰ In smokers, it varies from very thin and almost nonexistent to very thick, with a squamous type of epithelium.

Figure 38-9 A histologic section of the maxillary sinus mucosa demonstrates cilia to the left. An absence of blood vessels and elastic fibers exists in the tissue adjacent to the surrounding bone. No osteoblasts are evident between the sinus mucosa and the surrounding walls of bone.

Maxillary Sinus Mucous Clearance

The mucus of the maxillary sinuses is produced from serous and goblet cells, which produce 1 L of mucus each day in healthy conditions. The cilia in the maxillary sinus beat toward the ostium. A blanket of mucus is propelled toward the ostium by the beating motion of the ciliated lining cells. The mucous material of the sinus in health has two layers: (1) a top mucoid layer and (2) a bottom serous layer (Figure 38-10). The top layer is sticky and collects bacteria and other debris, whereas the serous layer is thin and acts as a lubricant. The cilia of the columnar epithelium beat toward the ostium at 15 cycles per minute, with a stiff stroke through the serous layer, reaching into the mucoid layer. The cilia recover with a limp reverse stroke within the serous layer. This mechanism slowly propels the mucoid layer toward the ostium at a rate of 9 mm per minute and into the middle meatus of the nose.⁶⁰

Figure 38-10 The pseudostratified columnar epithelium cells have 50 to 200 cilia per cell that beat toward the ostium to help clear 1L of mucus from goblet and mucous glands each day from the sinus. In health, the mucous has two layers: a bottom serous layer and top mucoid layer. The cilia beat with a stiff stroke in the mucoid layer toward the ostium and a relaxed recovery stroke within the serous layer.

Various elements may decrease the number of cilia and slow their beating efficiency. Viral infections, pollution, allergic reactions, and certain medications may affect the cilia in this way.⁶¹–⁶³ Genetic disorders (e.g., dyskinetic cilia syndrome) and factors such as long-standing dehydration, anticholinergic medications and antihistamines, cigarette smoke, and chemical toxins also can affect ciliary action. Certain pathogens (Haemophilus influenzae, Streptococcus pneumoniae, Pseudomonas aeruginosa) associated with sinusitis have been shown to release a compound that slows and disorganizes ciliary beating along with affecting mucous transport. Various medications have also been shown to affect ciliary action. Decongestant medications may alter the various layers of the sinus membranes, thus interrupting normal ciliary activity. On the other hand, long-term antibiotic medications have been shown to have a significant increase in ciliary beat frequency.⁶¹

In a healthy sinus, an adequate system of mucus production, clearance, and drainage is maintained. The key to normal sinus physiologic condition is the proper function of the cilia, which are the main component of the mucociliary transport system. These cilia work to move contaminants toward the natural ostium and then to the nasopharynx. The flow of mucus is toward the ostium, which leads to the infundibulum, through the hiatus semilunaris, into the middle meatus of the nose, and ultimately into the nasopharynx (Figure 38-11). An alteration in the sinus ostium patency or the quality of secretions can lead to disruption in ciliary action resulting in sinusitis. For clearance to be maintained, adequate ventilation is necessary. Ventilation and drainage is dependent on the osteomeatal unit, which is the main sinus opening. Ciliary movements of ciliated epithelial cells dictate clearance of the maxillary sinus.

Figure 38-11 A, Normal paranasal anatomy. B, Paranasal pathology and anatomical variants.

The maxillary ostium and infundibulum are part of the anterior ethmoid middle meatal complex, the region through which the frontal and maxillary sinuses drain, which is primarily responsible for mucociliary clearance of the sinuses to the nasopharynx.⁶⁴ As a result, pathogenesis of sinusitis is usually the development of obstruction in one or more areas of this complex.⁶⁵ Symptomatic sinusitis corresponds to the blockage of the osteomeatal complex that drains the paranasal sinuses. Symptoms of sinusitis may be minimal, even in the presence of extensive radiographic findings, as long as the patency of the ostium is maintained.⁶⁶

Mucoid fluid is transported toward the ostium of the maxillary sinus and drained into the nasal cavity, eliminating inhaled small particles and microorganisms. This mucociliary transport system is an active transport system that relies heavily on oxygen. The amount of oxygen absorbed from the blood is not adequate to maintain this drainage system. Additional oxygen has to be absorbed from the air in the sinus; this is why the patency of the ostium is pivotal in maintaining this transport system. Mucociliary transport may be compromised by abnormalities in the cilia, which include a decrease in the number and poor coordination of movement. After sinus infections, the quantitative loss of cilia is reversed except when severe empyema with scarring occurs, which results in the ciliated epithelium being replaced by squamous epithelium.

Maxillary Sinus Bacterial Flora

Much debate concerns the bacterial flora of the maxillary sinus. Maxillary sinuses have been considered to be sterile in health; however, bacteria can colonize within them without producing symptoms. In theory, the mechanism by which a sterile environment is maintained includes the mucociliary clearance system, immune system, and the production of nitrous oxide within the sinus cavity. In a study of patients who underwent surgical repositioning of the maxilla, Cook and Haber ⁶⁷ reported that 80% of the patients showed no bacterial growth. The remaining 20% had some bacterial growth but in negligible numbers. All specimens showed some degree of inflammatory cell infiltrate, more acute in the presence of microorganisms. They concluded that the asymptomatic adult maxillary sinus is usually sterile, but a few transient bacteria may exist in a clinically asymptomatic antrum.

However, recent endoscopically normal sinuses were shown to be nonsterile, with 62.3% exhibiting bacterial colonization. The most common bacteria cultured were Streptococcus viridans, Staphylococcus epidermidis, and Streptococcus pneumoniae.⁶⁸ The culture findings for secretions in acute maxillary sinusitis yielded high numbers of leukocytes, S. pneumoniae, or Streptococcus pyogenes, and Haemophilus influenzae was recovered from the purulent exudates with lower numbers of staphylococci. In fact, the macroscopic appearance of the secretion should not be used to screen samples, because several cases with H. influenzae grew also from nonpurulent samples. Other reports have indicated the bacterial flora of the maxillary sinus consists of nonhemolytic and α-hemolytic streptococci, as well as Neisseria spp. Additional microorganisms identifiable in various quantities belong to the staphylococci, Haemophilus spp., pneumococci, Mycoplasma spp., and Bacteroides spp. This is important to note because the sinus graft procedure often violates the sinus mucosa, and bacteria may contaminate the graft site.

Maxillary Sinus: Clinical Assessment

To establish an adequate osseous morphologic condition for the placement of endosteal implants in the resorbed maxillary posterior region, various grafting techniques have been developed to increase bone volume. In 1987, Misch ⁶⁹ developed four different categories for the treatment of the posterior maxilla (termed subantral [SA]), as SA-1 through SA-4 (Figure 38-12). The SA-1 posterior maxilla allows implant placement inferior to the sinus cavity without sinus manipulation, thus not altering the sinus floor or membrane. As such, if the patient has a preexisting maxillary sinus condition or develops a sinus infection after implant placement, then implants are not at risk of becoming contaminated. However, the SA-2 to SA-4 surgical procedures do alter the sinus membrane and sinus floor. With these treatment options, a thorough preoperative evaluation is completed to rule out existing pathologic condition in the maxillary sinus. In this way, the risk of mucus and bacteria contaminating the graft and creating a bacterial smear layer on the implant, which results in impaired bone formation during healing, is reduced. In addition, because of the proximity of the maxillary sinus to numerous vital structures, postoperative complications can be very severe and even life threatening.

Figure 38-12 Misch classified the subantral (SA) region of the posterior maxilla in four categories: SA-1 has adequate vertical bone for endosteal implants (>12 mm), SA-2 has 0 to 2 mm less than ideal height of bone (10 to 12 mm), SA-3 has 5 to 10 mm of bone below the antrum, and SA-4 has less than 5 mm of vertical bone below the maxillary sinus.

Pathologic conditions associated with the paranasal sinuses are common ailments and afflict more than 31 million people each year. Approximately 16 million people will seek medical assistance related to sinusitis; yet sinusitis is one of the most commonly overlooked diseases in clinical practice.⁷⁰ Potential infection in the region of the sinuses may result in severe complications. Infections in this area have been reported to result in sinusitis, orbital cellulitis, meningitis, osteomyelitis, and cavernous sinus thrombosis. In fact, paranasal sinus infection accounts for approximately 5% to 10% of all brain abscesses reported each year.⁷⁰

A physical examination of the maxillary sinus evaluates the middle third of the face for the presence of asymmetry, deformity, swelling, erythema, ecchymosis, hematoma, or facial tenderness (Table 38-1). Nasal congestion or obstruction, prevalent nasal discharge, epistaxis (bleeding from the nose), anosmia (the loss of the sense of smell), and/or halitosis (bad breath) are noted.

Table 38-1 Preoperative and Postoperative Physical Examination

SITE	SIGNS OF INFECTION
Inferior wall	Bulge in hard palate, ill-fitting denture, loose teeth, hypesthesia or nonvital teeth, bleeding, palatal erosion, oroantral fistula
Medial wall	Nasal obstruction, nasal discharge, epistaxis, cacosmia, visible mass in nostril
Anterior wall	Swelling, pain, skin changes
Lateral wall	Trismus, bulging mass, exudate from incision line
Posterior wall	Midface pain, hypesthesia of one half of face, loss of function of lower cranial nerves
Superior wall	Diplopia (double vision), proptosis (eye bulging out), chemosis, pain or hypesthesia, decreased visual acuity

The clinical examination for maxillary sinusitis concerns the regions surrounding the maxillary antrum. The examination is conducted to assess each wall surrounding the maxillary sinus separately. The infraorbital foramen on the facial wall of the antrum is palpated through the soft tissue of the cheeks or intraorally to determine whether tenderness or discomfort is present. The intraoral examination assesses the floor of the antrum by alveolar ulceration, expansion, tenderness, paresthesia, and oroantral fistulae. The eyes are examined to evaluate the superior wall of the sinus for proptosis, pupillary level, lack of eye movement, and diplopia. The nasal fluids may be used to evaluate the medial wall of the sinus by asking the patient to blow the nose in a waxed paper. The mucus should be clear and thin in nature. A yellow or greenish tint or thickened discharge indicates infection. Infected maxillary sinuses typically are symptomatic, which can exhibit exudate in the middle meatus and may be inspected with a nasal speculum and headlight (rhinoscopy) through the nares.

Other methods of examination of the infected maxillary sinus may include transillumination, nasoendoscopy, bacteriology, cytology, fiber optic antroscopy, and radiography (conventional, CT, or magnetic resonance imaging [MRI]).

Maxillary Sinus Radiographic Evaluation

The maxillary sinus is often pneumatized in partial or completely edentulous patients and requires grafting. Therefore visualization of the maxillary sinus and surrounding structures are crucial for the proper diagnosis and treatment planning of the partial or complete edentulous posterior maxilla. Numerous preoperative radiographic modalities are available to evaluate the posterior maxilla and maxillary sinuses.

Maxillary Sinus: Computed Tomography Radiographic Anatomy

Over the years, preoperative CT scan evaluation has become the standard method for evaluating the pathologic condition of the sinuses before sinus graft procedures. Therefore the practitioner should have an understanding of the CT radiographic anatomy and the pathologic conditions associated with the posterior maxilla and maxillary sinus regions.

Maxillary Sinus Membrane

A CT scan of normal, healthy paranasal sinuses reveal a completely radiolucent (dark) maxillary sinus. Any radiopaque (whitish) area within the sinus cavity is abnormal, and a pathologic condition should be suspected. The normal sinus membrane is radiographically invisible, whereas any inflammation or thickening of this structure will be radiopaque. The density of the diseased tissue or fluid accumulation will be proportional to varying degrees of gray values.

Ostiomeatal Complex

The ostiomeatal unit is composed of the maxillary ostium, ethmoid infundibulum, anterior ethmoid cells, and the frontal recess. The main drainage avenue of the maxillary sinus is through the ostium. The maxillary ostium is bounded superiorly by the ethmoid sinuses and inferiorly by the uncinate process. The uncinate process is a bony knifelike projection that is attached inferiorly to the inferior turbinate and posteriorly has a free margin. Drainage continues through the ostium into the infundibulum, which is a narrow passageway leading into the middle meatus. The middle meatus is the radiolucent space bounded by the middle and inferior turbinates.

Within the nasal cavity, three nasal turbinates or conchae (superior, middle, inferior) exist that are small downward projections of bone. Between the turbinates is a space or recess termed a meatus. The respiratory epithelium covers the turbinates and meatus and warms, moistens, and cleans the air that is respirated into the lungs.

The nasal septum is the bony partition that creates a barrier between the right and left sides of the nasal cavity (see Figure 38-11, A). Obstructions within any aspect of the nasal system predispose the area to pathologic conditions (see Figure 38-11, B).

Maxillary Sinus: Anatomical Variants

Numerous anatomical variants arise that can predispose a patient to postsurgical complications. When these conditions are noted, a pharmacologic discipline may be altered and/or implants may be placed after the sinus graft has matured, rather than predisposing them to an increased risk by inserting them at the same time as the sinus graft. As stated previously, patency of the ostium is paramount to maintain drainage. Preexisting skeletal and bony abnormalities of the osteomeatal complex may compromise the unit, leading to maxillary sinusitis.

Nasal Septum Deviation

A nasal septum deviation is a very common anatomical variant, occurring in as much as 70% of the population older than 14 years. This bony variant in extremes may cause obstruction of the ostiomeatal unit, which results in inflammation from air turbulence, causing increased mucosal drying and particle deposition. If the deviation is long standing, then atrophy of the middle turbinate may occur, resulting in narrowing of the ostiomeatal complex (Figure 38-16).⁷⁵

Figure 38-16 A nasal septum deviation is a common variant. Extreme cases may obstruct the ostiomeatal unit and increase the risk of sinusitis after a sinus graft.

Timmenga et al.⁷⁶ evaluated 45 patients who received 85 sinus grafts with endoscopy postsurgery. Of the 45 patients, five were found to have sinusitis postsurgery; all five of those patients had a nasal deviation or oversized turbinate. Therefore when these conditions are observed, the implant should not be placed at the same time as the sinus graft, and the recommended preoperative and postoperative pharmacologic protocol is especially warranted.

Middle Turbinate Variants

The middle turbinate plays a significant role in proper drainage of the maxillary sinus. A concha bullosa is a pneumatization within the middle turbinate and may occlude the osteomeatal complex, thus compromising adequate drainage. This variant is seen in approximately 4% to 15% of the population (see Figure 38-11).⁷⁷ Another variant in this anatomical structure is a paradoxically curved middle turbinate, which presents a concavity toward the septum, thus decreasing the size of the meatus. This also predisposes the patient to sinus disease.

Uncinate Process Variants

A deflected uncinate process (either laterally or medially) can narrow the ethmoid infundibulum, thus affecting the osteomeatal complex. Perforations may also be present within the uncinate process, leading to communication between the nasal cavity and ethmoid infundibulum. In addition, the uncinate process may be pneumatized. Although this is rare, it may compromise adequate clearance and drainage.

Supplemental Ostia

A supplemental ostium or secondary ostia may occur between the maxillary sinus and the middle meatus, which is often found in the posterior fontanelles (PFs). This may be found in approximately 18% to 30% of individuals. Because these secondary openings are usually located posterior and inferior to the natural ostium, they may predispose the patient to sinusitis by the recirculation of infected secretions from the primary meatus back into the sinus cavity. On occasion, these secondary ostia may be encountered during the elevation of the medial wall of the antrum, before placement of the sinus graft. When observed, a piece of collagen is placed over the site to prevent graft material from entering the nasal cavity.

Maxillary Hypoplasia

Hypoplasia of the maxillary sinus may be a direct result from trauma, infection, surgical intervention, or irradiation to the maxilla during the development of the maxillary bone. These conditions interrupt the maxillary growth center, thus producing a smaller-than-normal maxilla. A malformed and positioned uncinate process is associated with this disorder, leading to chronic sinus drainage problems. Most often, these patients have adequate bone height for endosteal implant placement, and a sinus graft is not required to gain vertical height.

Inferior Turbinate and Meatus Pneumatization (Big-Nose Variant)

Misch has observed, on rare occasion, the inferior third of the nasal cavity pneumatizes within the maxilla and resides over the alveolar residual ridge. An evaluation of 550 CT scans of complete or partially edentulous maxillae found this condition in 18 patients (3% incidence). When the patient has this condition, the maxillary sinus is lateral to the edentulous ridge. When inadequate bone height is present below this structure, a sinus graft does not increase available bone height for an implant. This condition is difficult to observe on a panoramic radiograph. If unaware, then the implant can be placed into the nasal cavity above the residual ridge and even penetrate the inferior turbinate. A sinus graft is contraindicated with this patient condition, because the sinus is lateral to the position of the implants. Instead, an onlay graft is required to increase bone height.

MAXILLARY SINUS PATHOLOGY

A preexisting, pathologic, maxillary sinus condition is a contraindication for many procedures that alter the sinus floor before or in conjunction with sinus grafting and/or implant insertion. The risk of postoperative infection is elevated and may compromise the health of the implant and the patient. Therefore pathologic conditions, either preoperative or postoperative, of a maxillary sinus should be evaluated, diagnosed, and treated.

Pathologic conditions of the maxillary sinus may be divided into four categories: (1) inflammation, (2) cystic conditions, (3) neoplasms, and (4) antroliths and foreign bodies. Studies have shown that 20% to 45% of the asymptomatic population has a subclinical pathologic condition in the maxillary sinus. A study completed at the Misch International Implant Institute evaluated 350 consecutive prospective candidates for maxillary sinus augmentations. The results concluded 30.7% of asymptomatic patients had maxillary sinus pathologic condition on CT scan evaluation. Because of this high incidence, it is highly recommended that a thorough radiographic evaluation be completed on all prospective sinus elevation patients.

INFLAMMATION

Inflammatory conditions can affect the maxillary sinus from odontogenic and nonodontogenic causes.

Odontogenic Sinusitis (Periapical Mucositis)

The close proximity of the roots of the maxillary posterior teeth to the floor of the sinus means that any inflammatory changes in the periodontium or surrounding alveolar bone may cause pathologic conditions in the maxillary sinus.

Etiology

Odontogenic sinusitis is caused by a periapical abscess, cyst, granuloma, or periodontal disease that causes an expansile lesion within the floor of the sinus. Other causes include sinus perforations during extractions and foreign bodies (e.g., gutta-percha, root tips, amalgam). Odontogenic sinusitis is often polymicrobial, with anaerobic streptococci, Bacteroides spp., Proteus spp., and coliform bacilli being involved. Studies have reported that approximately 25% of chronic sinusitis cases may have some odontogenic origin when teeth are present in the posterior maxilla.^78,⁷⁹

Radiographic Appearance

Periodontitis may produce generalized sinus mucosal hyperplasia, which is seen as a radiopaque band that follows the contours of the sinus floor. A localized periapical mucositis reveals a thickening of the mucosal membrane adjacent to the offending tooth and, on occasion, that perforates the floor of the sinus. This radiographic appearance has been termed a halo effect. In the author’s opinion, smoking may be the influencing factor, causing an increased risk of periodontitis, a decrease in immune response, and a decrease in the healthy flow of the mucus within the antrum.

Differential Diagnosis

This condition may be confused with acute sinusitis or mild mucosal thickening. However, in odontogenic sinusitis, the patient has teeth in the posterior maxilla and will usually exhibit symptoms related to the teeth (i.e., pain from a posterior tooth or a recent extraction, exudate around the existing natural posterior teeth).

Treatment

Before sinus augmentation or implant placement, the tooth or teeth involved should be treated periodontally, endodontically, or extracted. After intraoral soft tissue healing and resolution of the pathologic condition, the sinus graft procedure may be performed with little risk of postoperative complications.

Acute Rhinosinusitis

A nonodontogenic pathologic condition may also result in inflammation in the form of sinusitis. The most common type of sinusitis is acute rhinosinusitis. The signs and symptoms of acute rhinosinusitis are rather nonspecific, making it difficult to differentiate from the common cold, influenza type of symptoms, and allergic rhinitis. However, the most common symptoms include purulent nasal discharge, facial pain and tenderness, nasal congestion, and possible fever.

Acute maxillary rhinosinusitis results in 22 to 25 million patient visits to a physician in the United States each year, with a direct or indirect cost of 6 billion U.S. dollars. Although four paranasal sinuses exist in the skull, the most common involved in sinusitis are the maxillary and frontal sinuses.⁷⁰

Etiology

An inflammatory process that extends from the nasal cavity after a viral upper respiratory infection often causes acute maxillary sinusitis. Microbiological cultures have shown the most common pathogens causing acute rhinosinusitis are Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis. These pathogens include approximately 20% to 27% β-lactamase–resistant bacteria. Staphylococcus aureus has also been cited with the microbiology of acute rhinosinusitis. However, this pathogen is usually only seen in nosocomial (hospital induced) sinusitis and is unlikely to be seen in an elective sinus graft patient.

The most important factor in the pathogenesis of acute rhinosinusitis is the patency of the ostium.^80,⁸² Local predisposing causes of sinusitis include inflammation and edema associated with a viral upper respiratory tract infection or allergic rhinitis. As a consequence, mucous production within the sinus may be abnormal in quality or quantity, along with a compromised mucociliary transport. In an occluded sinus, an accumulation of inflammatory cells, bacteria, and mucus exists. Phagocytosis of the bacteria is impaired with immunoglobulin (Ig)-dependent activities decreased by the low concentration of IgA, IgG, and IgM found in infected secretions.

The oxygen tension inside the maxillary sinus has significant effects on pathologic conditions. When the oxygen tension in the sinus is altered, resultant sinusitis occurs. Growth of anaerobic and facultative organisms proliferate in this environment.⁸³ Many factors may alter the normal oxygen tension within the sinuses. A direct correlation exists between the ostium size and the oxygen tension in the sinus. In patients with recurrent episodes of sinusitis, oxygen tension is often reduced, even when infection is not present. As a consequence, a history of recurrent acute rhinosinusitis is relevant to determine whether an implant may be at increased risk when inserted at the same time as the sinus graft.