- Email: [email protected]
Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology journal homepage: www.elsevier.com/locate/jomsmp
Original Research
Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population Kang Lun Hong a , Raymond C.W. Wong a,b , Asher A.T. Lim a , Fun Chee Loh a , Jin Fei Yeo a,b , Intekhab Islam a,b,∗ a b
Discipline of Oral and Maxillofacial Surgery, University Dental Cluster, National University Hospital Singapore, Singapore Discipline of Oral and Maxillofacial Surgery, Faculty of Dentistry, National University of Singapore, Singapore
a r t i c l e
i n f o
Article history: Received 10 February 2016 Received in revised form 22 August 2016 Accepted 15 September 2016 Available online xxx Keywords: Anastomosis CBCT Maxillary sinus septa Sinus augmentation
a b s t r a c t Objectives: The purpose of the study was to retrospectively investigate the prevalence, location, orientation, origin and height of the maxillary sinus septa as well as the location of anastomosis (of the infra-orbital artery and posterior superior alveolar artery) from the alveolar crest in a sample population of Singapore. Methods: The study was done through the retrospective analysis of cone beam computed tomography (CBCT) images of 224 maxillary sinuses in 139 patients. Results: The prevalence of septa was 38.3% in this study. Septa formation was most commonly seen at the anterior region (i.e. first and second premolar), followed by the posterior (third molar) and middle region (first and second molar). 93% of the septa demonstrated a bucco-lingual orientation. 61.6% of septa were found to be primary septa i.e. located above root apices of maxillary teeth whereas 38.4% of septa were secondary septa i.e. located above an edentulous span. The mean height of the septa was 5.95 mm. The intra-osseous anastomosis between the infra-orbital artery and posterior superior alveolar artery was visible on the coronal view of 100 (45%) maxillary sinuses and the mean height of the intra-osseous anastomosis from the alveolar crest was 17.8 mm. Conclusion: To prevent the occurrence of complications, it is vital to have sufficient pre-operative knowledge of the possible anatomic structures present in the maxillary sinus. Having pre-operative CBCT imaging prior to sinus augmentation is advantageous as it allows for accurate assessment for the presence of septa or other anatomic irregularities that may complicate the surgery. © 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
1. Introduction The maxillary sinus floor elevation with placement of autogenous or synthetic grafting materials (sinus lift bone graft) has enabled endosseous implants to be placed in severely resorbed posterior maxillas and is seen as a predictable treatment modality today. It was first verbally presented by Tatum at the Alabama
夽 Asian AOMS: Asian Association of Oral and Maxillofacial Surgeons; ASOMP: Asian Society of Oral and Maxillofacial Pathology; JSOP: Japanese Society of Oral Pathology; JSOMS: Japanese Society of Oral and Maxillofacial Surgeons; JSOM: Japanese Society of Oral Medicine; JAMI: Japanese Academy of Maxillofacial Implants. ∗ Corresponding author at: Discipline of Oral and Maxillofacial Surgery, National University of Singapore, 11 Lower Kent Ridge Road, Singapore 119083, Singapore. Fax: +65 67732600. E-mail address: [email protected] (I. Islam).
Implant Congress in 1976 and published for the first time in 1980 by Boyne and James [1]. The most frequent complication of sinus floor elevation is perforation of the Schneiderian membrane [2–6]. Prevalence of sinus perforations from the literature ranges from 11% to 44% [4,6–11]. A systematic review of 48 studies by Pjetursson et al. found that the average perforation rate was 19.5% [5]. Perforation usually happens as the lateral wall is being in-fractured or when the membrane is being lifted off the sinus wall and floor. The risk of membrane perforation increases in presence of anatomical variations such as presence of septa or irregular sinus floor [2,12–14]. Maxillary sinus septa are bone ridges inside the sinus. The clinical significance of pre-existing septa during sinus floor elevation procedures is that access from the lateral window is affected. The sinus membrane is adherent to the wall of the septa and this increases the difficulty of membrane elevation as the
http://dx.doi.org/10.1016/j.ajoms.2016.09.005 2212-5558/© 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model
ARTICLE IN PRESS
JOMSMP-557; No. of Pages 6
K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
2
surgeon would need to take into account the altered anatomy. It is also challenging to insert the graft material into both parts of the sinus cavity, anterior and posterior to the septa [2,13]. The prevalence of septa within maxillary sinuses ranges from 16% to 67% whereas prevalence of septa within patients ranges from 22% to 69% (Table 1). In the absence of additional imaging, such septa may not be picked up on a panoramic or intraoral radiograph. Attempts at sinus augmentation without checking the existence of such septa can lead to increased risk of membrane perforation. Besides perforation of the maxillary sinus membrane, another possible complication is profuse bleeding that occurs during osteotomy of the lateral sinus wall, coming from anastomoses between the infra-orbital artery and posterior superior alveolar artery [33]. These anastomoses can give rise to both intra and extraosseous branches, supplying the lateral sinus wall and overlying membranes, with the intra-osseous branches found in all cases about 19 mm from the alveolar ridge crest and the extra-osseous branches found in 50% of all specimens about 23–26 mm from the alveolar ridge crest, according to Solar et al. [33]. These anatomical variations can pose a challenge to clinicians and it is critical to access and know the variations before surgery is attempted. There have been studies on these variations in an ethnic Chinese population in Taiwan. The population of Singapore is much more heterogeneous, with a majority race 70% of Chinese mainly descendants of immigrants from southern China, 25% Malays, 3% Indians, mainly descendants of immigrants from southern India and the rest made up of mixed races and other races. It is unknown what variation exists in the Singapore population. The National University Hospital Singapore serves as one of two tertiary referral hospitals in Singapore. The purpose of this study was to retrospectively investigate the prevalence and location of maxillary sinus septa and arterial anastomoses of a sample of the Singapore population by analyzing cone beam computed tomography images of patients taken in the National University Hospital, Singapore. 2. Materials and methods 2.1. Scan and image collection All cone beam computed tomography (CBCT) scans, performed at the University Dental Cluster, National University Hospital,
Singapore, of patients showing at least one full maxillary sinus, were collected. These patients had undergone scans for implant planning purposes, impacted teeth, orthognathic surgery or pathology. Permission was sought and granted for access to these records from the Institutional Review Board of the hospital. 2.2. Scanner The CBCT scans were taken using the Vatech Pax-Reve3D CBCT machine (Vatech Co Ltd, Korea). Field of view (FOV) chosen ranged from 5 cm × 5 cm, 8 cm × 6 cm, 12 cm × 8 cm, 15 cm × 15 cm depending on requirements of the ordering clinician. Voxel size ranges from 0.12 to 0.2 mm. Slice thickness is 0.1–0.4 mm. Maxillary sinuses with gross pathology were excluded from the study. 2.3. Image analysis The image analysis program – EZ3D Plus (QST Group, Singapore) was used to reconstruct the maxillary sinus into axial, coronal, sagittal planes and reformatted panoramic images. The images were referenced to the occlusal plane. 2.4. Sinus septa The presence of maxillary sinus septa was initially evaluated using axial images and further defined by the sagittal and coronal images. Presence of septa was indicated by bony structures that divide the maxillary sinus cavity into separate compartments. The locations of septa were divided into anterior, middle and posterior regions. The anterior region was defined as the first and second premolar region. The middle region was defined as the first and second molar region. The posterior region was defined as the third molar region [18,28,29,31]. In edentulous areas, the anterior-posterior width was divided into thirds for the purpose of classifying location. Orientation of the septa was evaluated using axial, coronal and sagittal views. Orientation was classified as bucco-lingual, sagittal or transverse [14]. Origin of septa was classified as primary or secondary. When a septum is located superior to roots of maxillary teeth, it is classified as a primary septum. When located above an edentulous span, the septum is termed secondary septum [14,20].
Table 1 Prevalence of septa [9,11,14–32]. Type of study
No. of subjects
Ethnicity
No. of sinuses
Prevalence among subjects (%)
Prevalence among sinuses (%)
Author
Year
In-vivo MSCT MSCT MSCT MSCT DPT MSCT MSCT Cadaveric/MSCT Cadaveric CBCT MSCT MSCT MSCT Cadaveric CBCT MSCT MSCT MSCT MSCT CBCT CBCT
41 – 156 – 100 1024 30 – 75 65 15 111 45 200 30 1029 204 200 30 423 500 –
Austrian Austrian USA Czech Korean Brazilian Spanish Turkish French German Japanese Polish Canadian S. African Italian German Korean Korean Spanish Taiwanese Brazilian Korean
– 200 312 68 200 – 60 330 150 130 30 222 52 400 60 – 236 400 60 846 – 150
31.7 – 32.7 – 38 21.6 – – 39 – – – – 69 – 47 27 37 – 30 44 –
– 16 24 36 26.5 – 25 23 – 27 37 26 40 56 33 33 24.6 27.7 66.7 20.5 – 44
Ulm et al. [15] Krennmair et al. [14] Velasquez-Plata et al. [16] Kasabah et al. [17] Kim et al. [18] Shibli et al. [19] Gonzalez-Santana et al. [20] Selcuk et al. [21] Ella et al. [22] Gosau et al. [23] Naitoh et al. [24] Rysz et al. [34] Malkinson et al. [9] Van Zyl et al. [25] Rosano et al. [26] Neugebauer et al. [27] Lee et al. [28] Park et al. [29] Maestre-Ferrin et al. [30] Shen et al. [31] Lana et al. [32] Kang et al. [11]
1995 1997 2002 2002 2006 2007 2007 2008 2008 2009 2009 2009 2009 2009 2010 2010 2010 2011 2011 2012 2012 2013
DPT: dental panoramic tomography; MSCT: multislice computed tomography; CBCT: cone beam computed tomography.
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
In addition, septa were classified into complete and incomplete depending whether they fully partitioned the maxillary sinus cavity [14]. The height of the septa was evaluated using reformatted panoramic images. Only septa with height of at least 2.5 mm were considered. This is in accordance with other studies [18,30,31]. Statistical analyses were carried out to test for association between gender, presence, location, orientation and completeness of septum.
2.5. Arterial anastomoses The presence of the intra-osseous anastomosis (if any) between the infra-orbital artery and posterior superior alveolar artery was determined on coronal images in the region of the first premolar to second molar. The intervals between successive images were kept small to confirm the presence of a linear structure consistent with the appearance of a vascular canal. The intra-osseous anastomosis that was most clearly visible among the coronal images was chosen for measurement. The vertical distance between the intra-osseous anastomosis and the alveolar crest was measured in a manner that was parallel to the long axis of the tooth and perpendicular to the occlusal plane. The mean distance between the intra-osseous anastomosis and the alveolar crest was calculated.
3. Results Scans from 139 patients met the criteria and the images collected. All the patients that met the criteria were of ethnic Chinese origin of which 50.4% were males and 49.6% were females with a mean age of 44.9 years. A total of 224 maxillary sinuses were examined in 139 patients, 85 of which had bilateral scans and 54 unilateral. The youngest patient was 16 years old and oldest patient was 88 years old. 43.2% (60/139) of the patients were fully dentate, 50.4% (70/139) of the patients were partially edentulous and 6.5% (9/139) patients were fully edentulous.
3
The prevalence of septa within maxillary sinuses was 35.7% in this study. 86 out of 224 maxillary sinuses demonstrated one or more septa while 144 did not have any sinus septa. Septa formation was most commonly seen at the anterior region (36%), followed by the posterior (34.9%) and middle (29.1%) region. The most common orientation (93%) of the septa was buccolingual while 5.8% demonstrated transverse orientation and 1.2% demonstrated sagittal orientation (Fig. 1). 89.5% of the septa were complete and fully partitioned the maxillary sinus cavity and only 10.5% of the septa were incomplete (Figs. 2 and 3). The majority of the septa were primary septa (61.6%) i.e. located above root apices of maxillary teeth and the remaining (38.4%) were secondary septa (located above edentulous span). The primary septa were significantly taller than secondary septa. The median height of primary septa was 6.2 mm and that of secondary septa was 4.87 mm (Fig. 4). The mean height of the measurable septa was 5.95 mm. The septa in transverse orientation (n = 5) were not measurable. Does sex affect the presence of septa? The results showed a significant difference between males and females. 58.6% of males demonstrated presence of septa whereas 33.3% of females demonstrated presence of septa. The number of male patients who had septa was significantly more than female patients with 58.6% of males having septa compared to 33.6% for females. The presence or absence of teeth also seemed to affect the likelihood of septa. Fully edentulous patients were most likely to have septa (55.6%), followed by partially edentulous patients (50%) and fully dentate patients (40%). These differences were not significant. The results are summarized in Table 2. A significant association (P < 0.05) was found between origin of septa and height of septa. However there was no significant association between any of the other variables. The intra-osseous anastomosis between the infra-orbital artery and posterior superior alveolar artery was visible on the coronal view of 100 maxillary sinuses with a mean height of 17.8 mm from
Fig. 1. An illustration of a bucco-lingual septum being displayed in 3 views – axial, coronal and sagittal.
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model
ARTICLE IN PRESS
JOMSMP-557; No. of Pages 6
K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
4 Table 2 Characteristics of maxillary septa. Sinuses examined
Presence of septa
Location of septa
224
38.3% Mean height: 5.95 mm Complete septa: 89.5%
Anterior Middle Posterior
Orientation of septa 36% 29.1% 34.9%
Bucco-lingual Transverse Sagittal
Origin of septa 93 5.8 1.2
Primary Secondary
61.6 38.4
comparing septa found in DPT and that found in CT scans [17]. Gonzalez-Santana et al. reported 11.8% of false-negatives when diagnosing septa using DPT [20]. Maestre-Ferrin et al. also reported that a lower prevalence of septa was detected in DPT when compared to CT scans [30]. To accurately determine the location and morphology of septa, a CBCT scan would be advisable prior to surgery. Wherever CBCT imaging is used, it is advisable to check for presence of septa. Proper planning and access to the sinus cavity reduces the risk of membrane perforation.
Fig. 2. Illustration of an incomplete septum.
the alveolar crest (Table 3) (Fig. 5). If the anastomosis was not visible, it was likely to be extra-osseous. 4. Discussion The purpose of this study was to find out the prevalence and location of maxillary sinus septa and arterial anastomosis in a sample of the patient population in Singapore. A total of 139 patients and 224 maxillary sinuses were examined. All the patients that met the inclusion criteria happened to be from ethnic Chinese background. This probably reflects the reality of the patient demographics around the hospital and the referral pattern to the National University Hospital, Singapore. Perhaps looking at and comparing the data from other centres with majority population of other races would help to further delineate the variances. This is the first study looking at the prevalence in the population of Singapore.
Fig. 4. Illustration of a primary septum (right) and secondary septum (left).
The prevalence of septa within patients is 46% and prevalence of septa within maxillary sinuses is 38.3%. The figures are slightly higher when compared to another study conducted by Shen et al. who reported the prevalence of septa as 29.3% in an ethnic Chinese population in Taiwan [31]. This, however, is comparable to other studies reported in the literature (26–44%) [9,11,17,18,24,27–29,34]. The incidence of maxillary sinus septa was first investigated by Underwood in 1910 and is known as Underwood’s septa [35]. According to Underwood, septa are formed because of different eruption phases of teeth. Septa are the remaining intervening bone partitions when the rest of the bony floor sinks down between the dental roots of adjacent teeth during eruption. He reported a 33% incidence of septa in the maxillary sinus. The function of septa is largely unknown. Van den Bergh et al. postulated that septa act as struts to withstand masticatory forces during the dentate stage of life [2]. As was alluded earlier, a false negative finding can result in surgical complications. Septa formation was most commonly seen at the anterior region (36.0%), followed by the posterior (34.9%) and middle region (29.1%). However, there was no significant difference in distribution of septa between the 3 regions. The results were similar to studies done by Ulm et al. [15], Krennmair et al. [14] and Neugebauer et al. [27], who
Fig. 3. Illustration of a complete septum.
CBCT scans were used to determine the presence of septa. The literature has shown that DPT alone is not accurate in diagnosing presence of septa. Krennmair et al. found that DPT led to false diagnosis of presence or absence of septa in 21.5% of cases after clinically verifying the septa during sinus augmentation surgery [14]. Kasabah et al. reported false diagnosis in 44% of cases after
Table 3 Distance of intra-osseous anastomosis from alveolar crest. Total sinuses examined
224
Total sinuses with intra-osseous anastomosis visible on coronal view Mean distance of intra-osseous anastomosis from alveolar crest
100 (45%) 17.8 mm
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
5
Fig. 5. Illustration of measurement of distance from intra-osseous anastomosis to alveolar crest.
concluded that the anterior region contained the majority of septa. Some studies have reported that more septa are located in the middle region [16,18,20,25,26,28–31]. This could be due to the lack of uniformity in defining the location in different studies, especially in edentulous areas where there is lack of teeth. In terms of orientation, 93% (80/86) of septa demonstrated bucco-lingual direction, which was the most common orientation of the septa in this study and this is in agreement with other studies in the literature [14,18,25,29,31]. Clinically, the septa that would most likely hinder lateral window sinus grafting would be the bucco-lingual septa. When septa are present on the antral floor, Boyne and James suggested cutting them with a narrow chisel and removing them with a hemostat [1]. This allows the bone graft to be placed over the entire antral floor without interruption. Van den Bergh et al. suggested making a W-shaped trap door to reduce risk of perforation when elevating the maxillary sinus membrane [2]. Zijderveld et al. suggested making 2 trap doors – one anterior and one posterior to the septum instead of the classical one trap door design [6]. Whichever technique is adopted, accurate localization of the septa, their orientation and length is important when deciding on the surgical approach to the lateral window. A great majority of the septa (81 out of 88) were measurable. There were 5 transverse septa which were excluded because the height could not be measured. The mean height of the 81 septa was 5.95 mm. The mean height of septa in the literature ranged from 2.5 mm to 9.2 mm [14,16,18,20,25–27,29,30]. Kim et al. [18], Maestre-Ferrin et al. [30] and Shen et al. [31] only considered septa with height of at least 2.5 mm to be clinically relevant. This is likely because the lower border of the lateral window is usually located 3 mm above the level of the sinus floor. In our study, the mean height of the septa was almost 6 mm. This may impede the in-fracture of the lateral window and hinder access during sinus augmentation. In such cases, an out fracture approach may be more advisable. As septa increase in height, the difficulty in elevation of the sinus membrane from the septa surface increases as well. There was a significant difference between males and females in terms of occurrence of septa. 58.6% of males compared to 33.3% of females demonstrated presence of septa. Using Fisher’s Exact Test, the difference was statistically significant (P < 0.05). It is interesting that males demonstrated significantly higher prevalence of septa compared to females in this study. This could possibly be attributed to increased masticatory forces in males leading to an increased formation of septa. Among the different states of dentition, fully edentulous patients were most likely to demonstrate presence of septa (55.6%), followed by partially edentulous patients (50%) and fully dentate patients (40%). Krennmair et al. [14], Kim et al. [18], Van Zyl and Van Heerden [25] and Lee et al. [28] also reported higher incidences of septa in edentulous regions compared to dentate regions. However, there was no significant difference in occurrence of septa between the different states in this study (P > 0.05). Secondary septa
are known to be acquired and develop in edentulous regions due to pneumatization of the maxillary sinus after tooth loss [14]. This could likely be why the prevalence of septa is higher in edentulous regions. Significant differences in the origin of septa were found between patients with different states of dentition. Dentate patients were significantly more likely to have primary septa and fully edentulous patients were more likely to have secondary septa. According to Krennmair et al., primary septa are congenital in nature and evolve during the growth of the middle face whereas secondary septa form as a result of tooth loss and irregular pneumatization of the sinus floor [14]. The ‘bony crests’ formed as a result of atrophy of the alveolar process are what is known as secondary septa. Significant differences in height were found between primary and secondary septa. In this study, primary septa were significantly taller than secondary septa. This is in agreement with Kim et al. who found that primary septa were significantly taller than secondary septa [18]. This is because primary septa are formed congenitally during growth of the middle face and are not subjected to effects of alveolar resorption after tooth loss. Secondary septa are formed as ‘bony crests’ as a result of atrophy of the alveolar process. Thus, primary septa are generally taller than secondary septa. From this study, it was concluded that the state of dentition (i.e. dentate/partially edentulous/fully edentulous) did not influence variables such as location, orientation, completeness and height of septa. Similarly, location of septa (i.e. anterior/middle/posterior) did not influence variables such as orientation, completeness, origin and height of septa. In addition, origin of septa (i.e. primary/secondary) did not influence variables such as orientation and completeness of septa. Profuse bleeding during osteotomy of the lateral window can occur at times. This usually occurs when performing the vertical osteotomy cuts of the lateral window. The anastomosis between the infra-orbital artery and posterior superior alveolar artery was visible on the coronal view of 100 maxillary sinuses (out of a total of 224 sinuses). The blood vessel anastomosis was not always visible as they could be extra-osseous [10,11,33]. In this study, the voxel size of 0.12–0.2 mm and slice thickness of 0.1–0.4 mm was sufficient for identification of the intra-osseous anastomosis. The mean distance of the intra-osseous anastomosis from the alveolar crest is 17.8 mm in this study, which is similar to other studies previously conducted. Solar et al. [33] conducted a cadaveric study on 18 maxillas and found that the intra-osseous anastomosis was 19 mm from the alveolar crest. Guncu et al. [10] and Kang et al. [11] conducted a CT study and found that the intra-osseous anastomosis was also 19 mm from the alveolar crest. A point can be made that after extractions, there will be vertical bony resorption, thus making any measurements from the alveolar crest inaccurate. This is especially true for total edentulism or partially dentate situations whereby the posterior maxillary teeth had been extracted. An alternative reference point of measurement could be from the
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
6
infraorbital foramen. This would then bring up the question of whether the location of the infraorbital foramen is constant both in terms of distance from the orbital rims and also if the location varies between races or sex. We have no information on this and this would make a good point for further study. The other counter point for this would be previous studies all measured the distance from the alveolar crest and using this reference point serves as a point of comparison to other studies and also from a practical point of view during surgery, it is easier to measure the distance from the alveolar crest than from the infraorbital foramen as this would mean more periosteal stripping and consequently, more edema. The position of the lateral window design should be made after analysis of the amount of sub-antral bone height on CBCT. In cases where the superior border of the lateral window is more than 17 mm from the alveolar crest, there may be an increased risk of encountering the blood vessel during osteotomy. Haemostasis may be achieved with methods such as electrocautery. In cases where the blood vessel is not encountered, the anastomosis is likely to be extra-osseous in nature. Both Solar et al. [33] and Kang et al. [11] reported that the extra-osseous anastomosis is located superior to the intra-osseous anastomosis and is usually located around 23 mm away from the alveolar crest. Extraosseous anastomosis may be less commonly encountered as it may be retracted within the mucoperiosteal flap and thus protected from the osteotomy site. 5. Conclusion The prevalence of septa within maxillary sinuses in the ethnic Chinese population in Singapore is found to be 35.7%, which is similar to other studies. Orientation of the septa was most common in a bucco-medial direction. The distance of the arterial anastomosis was at an average of 17.8 mm from the alveolar crest. This prevalence prevails upon the operator to take more detailed scans to detect these structures. The location of septa and anastomosis can be detected quite readily with a CBCT, which can help to clue in the operator to take steps to prevent sinus membrane perforation or bleeding during the procedure. Conflict of interest There is no conflict of interest in this study. References [1] Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980;38:613–6. [2] Van den Bergh JP, Ten Bruggenkate CM, Disch FJ, Tuinzing DB. Anatomical aspects of sinus floor elevations. Clin Oral Implants Res 2000;11:256–65. [3] Shlomi B, Horowitz I, Kahn A, Dobriyan A, Chaushu G. The effect of sinus membrane perforation and repair with Lambone on the outcome of maxillary sinus floor augmentation: a radiographic assessment. Int J Oral Maxillofac Implants 2004;19:559–62. [4] Ardekian L, Oved-Peleg E, Mactei EE, Peled M. The clinical significance of sinus membrane perforation during augmentation of the maxillary sinus. J Oral Maxillofac Surg 2006;64:277–82. [5] Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol 2008;35(Suppl):216–40. [6] Zijderveld SA, Van den Bergh JP, Schulten EA, Ten Bruggenkate CM. Anatomical and surgical findings and complications in 100 consecutive maxillary sinus floor elevation procedures. J Oral Maxillofac Surg 2008;66:1426–38. [7] Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical complications of the sinus graft procedure and their impact on implant survival. J Periodontol 2004;75:511–6.
[8] Hernandez-Alfaro F, Torradeflot MM, Marti C. Prevalence and management of Schneiderian membrane perforations during sinus-lift procedures. Clin Oral Implants Res 2008;19:91–8. [9] Malkinson S, Irinakis T. The influence of interfering septa on the incidence of Schneiderian membrane perforations during maxillary sinus elevation surgery: a retrospective study of 52 consecutive lateral window procedures. J Oral Surg 2009;2:19–25. [10] Guncu GN, Yildirim YD, Wang HL, Tozum TF. Location of posterior superior alveolar artery and evaluation of maxillary sinus anatomy with computerized tomography: a clinical study. Clin Oral Implants Res 2011;22:1164–7. [11] Kang SJ, Shin SI, Herr Y, Kwon YH, Kim GT, Chung JH. Anatomical structures in the maxillary sinus related to lateral sinus elevation: a cone beam computed tomographic analysis. Clin Oral Implants Res 2013;24(Suppl A100):75–81. [12] Tatum OH.Lecture Presented to the Alabama Implant Congress. 1976. [13] Betts NJ, Miloro M. Modification of the sinus lift procedure for septa in the maxillary antrum. J Oral Maxillofac Surg 1994;52:332–3. [14] Krennmair G, Ulm C, Lugmayr H. Maxillary sinus septa: incidence, morphology and clinical implications. J Craniomaxillofac Surg 1997;25:261–5. [15] Ulm CW, Solar P, Krennmair G, Matejka M, Watzek G. Incidence and suggested surgical management of septa in sinus-lift procedures. Int J Oral Maxillofac Implants 1995;10:462–5. [16] Velasquez-Plata D, Hovey LR, Peach CC, Alder ME. Maxillary sinus septa: a 3-dimensional computerized tomographic scan analysis. Int J Oral Maxillofac Implants 2002;17:854–60. [17] Kasabah S, Slezak R, Simunek A, Krug J, Lecaro MC. Evaluation of the accuracy of panoramic radiograph in the definition of maxillary sinus septa. Acta Medica (Hradec Kralove) 2002;45:173–5. [18] Kim MJ, Jung UW, Kim CS, Kim KD, Choi SH, Kim CK, et al. Maxillary sinus septa: prevalence, height, location, and morphology. A reformatted computed tomography scan analysis. J Periodontol 2006;77:903–8. [19] Shibli JA, Faveri M, Ferrari DS, Melo L, Garcia RV, d’Avila S, et al. Prevalence of maxillary sinus septa in 1024 subjects with edentulous upper jaws: a retrospective study. J Oral Implantol 2007;33:293–6. [20] Gonzalez-Santana H, Penarrocha-Diago M, Guarinos-Carbo J, Sorni-Broker M. A study of the septa in the maxillary sinuses and the subantral alveolar processes in 30 patients. J Oral Implantol 2007;33:340–3. [21] Selcuk A, Ozcan KM, Akdogan O, Bilal N, Dere H. Variations of maxillary sinus and accompanying anatomical and pathological structures. J Craniofac Surg 2008;19:159–64. [22] Ella B, Noble Rda C, Lauverjat Y, Sedarat C, Zwetyenga N, Siberchicot F, et al. Septa within the sinus: effect on elevation of the sinus floor. Br J Oral Maxillofac Surg 2008;46:464–7. [23] Gosau M, Rink D, Driemel O, Draenert FG. Maxillary sinus anatomy: a cadaveric study with clinical implications. Anat Rec (Hoboken) 2009;292:352–4. [24] Naitoh M, Suenaga Y, Kondo S, Gotoh K, Ariji E. Assessment of maxillary sinus septa using cone-beam computed tomography: etiological consideration. Clin Implant Dent Relat Res 2009;11(Suppl 1):e52–8. [25] Van Zyl AW, Van Heerden WF. A retrospective analysis of maxillary sinus septa on reformatted computerised tomography scans. Clin Oral Implants Res 2009;20:1398–401. [26] Rosano G, Taschieri S, Gaudy JF, Lesmes D, Del Fabbro M. Maxillary sinus septa: a cadaveric study. J Oral Maxillofac Surg 2010;68:1360–4. [27] Neugebauer J, Ritter L, Mischkowski RA, Dreiseidler T, Scherer P, Ketterle M, et al. Evaluation of maxillary sinus anatomy by cone-beam CT prior to sinus floor elevation. Int J Oral Maxillofac Implants 2010;25:258–65. [28] Lee WJ, Lee SJ, Kim HS. Analysis of location and prevalence of maxillary sinus septa. J Periodontal Implant Sci 2010;40:56–60. [29] Park YB, Jeon HS, Shim JS, Lee KW, Moon HS. Analysis of the anatomy of the maxillary sinus septum using 3-dimensional computed tomography. J Oral Maxillofac Surg 2011;69:1070–8. [30] Maestre-Ferrin L, Galan-Gil S, Rubio-Serrano M, Penarrocha-Diago M, Penarrocha-Oltra D. Maxillary sinus septa: a systematic review. Med Oral Patol Oral Cir Bucal 2010;15:383–6. [31] Shen EC, Fu E, Chiu TJ, Chang V, Chiang CY, Tu HP, et al. Prevalence and location of maxillary sinus septa in the Taiwanese population and relationship to the absence of molars. Clin Oral Implants Res 2012;23:741–5. [32] Lana JP, Carneiro PM, Machado Vde C, de Souza PE, Manzi FR, Horta MC. Anatomic variations and lesions of the maxillary sinus detected in cone beam computed tomography for dental implants. Clin Oral Implants Res 2012;23:1398–403. [33] Solar P, Geyerhofer U, Traxler H, Windisch A, Ulm C, Watzek G. Blood supply to the maxillary sinus relevant to sinus floor elevation procedures. Clin Oral Implants Res 1999;10:34–44. [34] Rysz M, Bakon L. Maxillary sinus anatomy variation and nasal cavity width: structural computed tomography imaging. Folia Morphol (Warsz) 2009;68:260–4. [35] Underwood AS. An inquiry into the anatomy and pathology of the maxillary sinus. J Anat Physiol 1910;44:354–69.
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
ARTICLE IN PRESS Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology journal homepage: www.elsevier.com/locate/jomsmp
Original Research
Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population Kang Lun Hong a , Raymond C.W. Wong a,b , Asher A.T. Lim a , Fun Chee Loh a , Jin Fei Yeo a,b , Intekhab Islam a,b,∗ a b
Discipline of Oral and Maxillofacial Surgery, University Dental Cluster, National University Hospital Singapore, Singapore Discipline of Oral and Maxillofacial Surgery, Faculty of Dentistry, National University of Singapore, Singapore
a r t i c l e
i n f o
Article history: Received 10 February 2016 Received in revised form 22 August 2016 Accepted 15 September 2016 Available online xxx Keywords: Anastomosis CBCT Maxillary sinus septa Sinus augmentation
a b s t r a c t Objectives: The purpose of the study was to retrospectively investigate the prevalence, location, orientation, origin and height of the maxillary sinus septa as well as the location of anastomosis (of the infra-orbital artery and posterior superior alveolar artery) from the alveolar crest in a sample population of Singapore. Methods: The study was done through the retrospective analysis of cone beam computed tomography (CBCT) images of 224 maxillary sinuses in 139 patients. Results: The prevalence of septa was 38.3% in this study. Septa formation was most commonly seen at the anterior region (i.e. first and second premolar), followed by the posterior (third molar) and middle region (first and second molar). 93% of the septa demonstrated a bucco-lingual orientation. 61.6% of septa were found to be primary septa i.e. located above root apices of maxillary teeth whereas 38.4% of septa were secondary septa i.e. located above an edentulous span. The mean height of the septa was 5.95 mm. The intra-osseous anastomosis between the infra-orbital artery and posterior superior alveolar artery was visible on the coronal view of 100 (45%) maxillary sinuses and the mean height of the intra-osseous anastomosis from the alveolar crest was 17.8 mm. Conclusion: To prevent the occurrence of complications, it is vital to have sufficient pre-operative knowledge of the possible anatomic structures present in the maxillary sinus. Having pre-operative CBCT imaging prior to sinus augmentation is advantageous as it allows for accurate assessment for the presence of septa or other anatomic irregularities that may complicate the surgery. © 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
1. Introduction The maxillary sinus floor elevation with placement of autogenous or synthetic grafting materials (sinus lift bone graft) has enabled endosseous implants to be placed in severely resorbed posterior maxillas and is seen as a predictable treatment modality today. It was first verbally presented by Tatum at the Alabama
夽 Asian AOMS: Asian Association of Oral and Maxillofacial Surgeons; ASOMP: Asian Society of Oral and Maxillofacial Pathology; JSOP: Japanese Society of Oral Pathology; JSOMS: Japanese Society of Oral and Maxillofacial Surgeons; JSOM: Japanese Society of Oral Medicine; JAMI: Japanese Academy of Maxillofacial Implants. ∗ Corresponding author at: Discipline of Oral and Maxillofacial Surgery, National University of Singapore, 11 Lower Kent Ridge Road, Singapore 119083, Singapore. Fax: +65 67732600. E-mail address: [email protected] (I. Islam).
Implant Congress in 1976 and published for the first time in 1980 by Boyne and James [1]. The most frequent complication of sinus floor elevation is perforation of the Schneiderian membrane [2–6]. Prevalence of sinus perforations from the literature ranges from 11% to 44% [4,6–11]. A systematic review of 48 studies by Pjetursson et al. found that the average perforation rate was 19.5% [5]. Perforation usually happens as the lateral wall is being in-fractured or when the membrane is being lifted off the sinus wall and floor. The risk of membrane perforation increases in presence of anatomical variations such as presence of septa or irregular sinus floor [2,12–14]. Maxillary sinus septa are bone ridges inside the sinus. The clinical significance of pre-existing septa during sinus floor elevation procedures is that access from the lateral window is affected. The sinus membrane is adherent to the wall of the septa and this increases the difficulty of membrane elevation as the
http://dx.doi.org/10.1016/j.ajoms.2016.09.005 2212-5558/© 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model
ARTICLE IN PRESS
JOMSMP-557; No. of Pages 6
K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
2
surgeon would need to take into account the altered anatomy. It is also challenging to insert the graft material into both parts of the sinus cavity, anterior and posterior to the septa [2,13]. The prevalence of septa within maxillary sinuses ranges from 16% to 67% whereas prevalence of septa within patients ranges from 22% to 69% (Table 1). In the absence of additional imaging, such septa may not be picked up on a panoramic or intraoral radiograph. Attempts at sinus augmentation without checking the existence of such septa can lead to increased risk of membrane perforation. Besides perforation of the maxillary sinus membrane, another possible complication is profuse bleeding that occurs during osteotomy of the lateral sinus wall, coming from anastomoses between the infra-orbital artery and posterior superior alveolar artery [33]. These anastomoses can give rise to both intra and extraosseous branches, supplying the lateral sinus wall and overlying membranes, with the intra-osseous branches found in all cases about 19 mm from the alveolar ridge crest and the extra-osseous branches found in 50% of all specimens about 23–26 mm from the alveolar ridge crest, according to Solar et al. [33]. These anatomical variations can pose a challenge to clinicians and it is critical to access and know the variations before surgery is attempted. There have been studies on these variations in an ethnic Chinese population in Taiwan. The population of Singapore is much more heterogeneous, with a majority race 70% of Chinese mainly descendants of immigrants from southern China, 25% Malays, 3% Indians, mainly descendants of immigrants from southern India and the rest made up of mixed races and other races. It is unknown what variation exists in the Singapore population. The National University Hospital Singapore serves as one of two tertiary referral hospitals in Singapore. The purpose of this study was to retrospectively investigate the prevalence and location of maxillary sinus septa and arterial anastomoses of a sample of the Singapore population by analyzing cone beam computed tomography images of patients taken in the National University Hospital, Singapore. 2. Materials and methods 2.1. Scan and image collection All cone beam computed tomography (CBCT) scans, performed at the University Dental Cluster, National University Hospital,
Singapore, of patients showing at least one full maxillary sinus, were collected. These patients had undergone scans for implant planning purposes, impacted teeth, orthognathic surgery or pathology. Permission was sought and granted for access to these records from the Institutional Review Board of the hospital. 2.2. Scanner The CBCT scans were taken using the Vatech Pax-Reve3D CBCT machine (Vatech Co Ltd, Korea). Field of view (FOV) chosen ranged from 5 cm × 5 cm, 8 cm × 6 cm, 12 cm × 8 cm, 15 cm × 15 cm depending on requirements of the ordering clinician. Voxel size ranges from 0.12 to 0.2 mm. Slice thickness is 0.1–0.4 mm. Maxillary sinuses with gross pathology were excluded from the study. 2.3. Image analysis The image analysis program – EZ3D Plus (QST Group, Singapore) was used to reconstruct the maxillary sinus into axial, coronal, sagittal planes and reformatted panoramic images. The images were referenced to the occlusal plane. 2.4. Sinus septa The presence of maxillary sinus septa was initially evaluated using axial images and further defined by the sagittal and coronal images. Presence of septa was indicated by bony structures that divide the maxillary sinus cavity into separate compartments. The locations of septa were divided into anterior, middle and posterior regions. The anterior region was defined as the first and second premolar region. The middle region was defined as the first and second molar region. The posterior region was defined as the third molar region [18,28,29,31]. In edentulous areas, the anterior-posterior width was divided into thirds for the purpose of classifying location. Orientation of the septa was evaluated using axial, coronal and sagittal views. Orientation was classified as bucco-lingual, sagittal or transverse [14]. Origin of septa was classified as primary or secondary. When a septum is located superior to roots of maxillary teeth, it is classified as a primary septum. When located above an edentulous span, the septum is termed secondary septum [14,20].
Table 1 Prevalence of septa [9,11,14–32]. Type of study
No. of subjects
Ethnicity
No. of sinuses
Prevalence among subjects (%)
Prevalence among sinuses (%)
Author
Year
In-vivo MSCT MSCT MSCT MSCT DPT MSCT MSCT Cadaveric/MSCT Cadaveric CBCT MSCT MSCT MSCT Cadaveric CBCT MSCT MSCT MSCT MSCT CBCT CBCT
41 – 156 – 100 1024 30 – 75 65 15 111 45 200 30 1029 204 200 30 423 500 –
Austrian Austrian USA Czech Korean Brazilian Spanish Turkish French German Japanese Polish Canadian S. African Italian German Korean Korean Spanish Taiwanese Brazilian Korean
– 200 312 68 200 – 60 330 150 130 30 222 52 400 60 – 236 400 60 846 – 150
31.7 – 32.7 – 38 21.6 – – 39 – – – – 69 – 47 27 37 – 30 44 –
– 16 24 36 26.5 – 25 23 – 27 37 26 40 56 33 33 24.6 27.7 66.7 20.5 – 44
Ulm et al. [15] Krennmair et al. [14] Velasquez-Plata et al. [16] Kasabah et al. [17] Kim et al. [18] Shibli et al. [19] Gonzalez-Santana et al. [20] Selcuk et al. [21] Ella et al. [22] Gosau et al. [23] Naitoh et al. [24] Rysz et al. [34] Malkinson et al. [9] Van Zyl et al. [25] Rosano et al. [26] Neugebauer et al. [27] Lee et al. [28] Park et al. [29] Maestre-Ferrin et al. [30] Shen et al. [31] Lana et al. [32] Kang et al. [11]
1995 1997 2002 2002 2006 2007 2007 2008 2008 2009 2009 2009 2009 2009 2010 2010 2010 2011 2011 2012 2012 2013
DPT: dental panoramic tomography; MSCT: multislice computed tomography; CBCT: cone beam computed tomography.
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
In addition, septa were classified into complete and incomplete depending whether they fully partitioned the maxillary sinus cavity [14]. The height of the septa was evaluated using reformatted panoramic images. Only septa with height of at least 2.5 mm were considered. This is in accordance with other studies [18,30,31]. Statistical analyses were carried out to test for association between gender, presence, location, orientation and completeness of septum.
2.5. Arterial anastomoses The presence of the intra-osseous anastomosis (if any) between the infra-orbital artery and posterior superior alveolar artery was determined on coronal images in the region of the first premolar to second molar. The intervals between successive images were kept small to confirm the presence of a linear structure consistent with the appearance of a vascular canal. The intra-osseous anastomosis that was most clearly visible among the coronal images was chosen for measurement. The vertical distance between the intra-osseous anastomosis and the alveolar crest was measured in a manner that was parallel to the long axis of the tooth and perpendicular to the occlusal plane. The mean distance between the intra-osseous anastomosis and the alveolar crest was calculated.
3. Results Scans from 139 patients met the criteria and the images collected. All the patients that met the criteria were of ethnic Chinese origin of which 50.4% were males and 49.6% were females with a mean age of 44.9 years. A total of 224 maxillary sinuses were examined in 139 patients, 85 of which had bilateral scans and 54 unilateral. The youngest patient was 16 years old and oldest patient was 88 years old. 43.2% (60/139) of the patients were fully dentate, 50.4% (70/139) of the patients were partially edentulous and 6.5% (9/139) patients were fully edentulous.
3
The prevalence of septa within maxillary sinuses was 35.7% in this study. 86 out of 224 maxillary sinuses demonstrated one or more septa while 144 did not have any sinus septa. Septa formation was most commonly seen at the anterior region (36%), followed by the posterior (34.9%) and middle (29.1%) region. The most common orientation (93%) of the septa was buccolingual while 5.8% demonstrated transverse orientation and 1.2% demonstrated sagittal orientation (Fig. 1). 89.5% of the septa were complete and fully partitioned the maxillary sinus cavity and only 10.5% of the septa were incomplete (Figs. 2 and 3). The majority of the septa were primary septa (61.6%) i.e. located above root apices of maxillary teeth and the remaining (38.4%) were secondary septa (located above edentulous span). The primary septa were significantly taller than secondary septa. The median height of primary septa was 6.2 mm and that of secondary septa was 4.87 mm (Fig. 4). The mean height of the measurable septa was 5.95 mm. The septa in transverse orientation (n = 5) were not measurable. Does sex affect the presence of septa? The results showed a significant difference between males and females. 58.6% of males demonstrated presence of septa whereas 33.3% of females demonstrated presence of septa. The number of male patients who had septa was significantly more than female patients with 58.6% of males having septa compared to 33.6% for females. The presence or absence of teeth also seemed to affect the likelihood of septa. Fully edentulous patients were most likely to have septa (55.6%), followed by partially edentulous patients (50%) and fully dentate patients (40%). These differences were not significant. The results are summarized in Table 2. A significant association (P < 0.05) was found between origin of septa and height of septa. However there was no significant association between any of the other variables. The intra-osseous anastomosis between the infra-orbital artery and posterior superior alveolar artery was visible on the coronal view of 100 maxillary sinuses with a mean height of 17.8 mm from
Fig. 1. An illustration of a bucco-lingual septum being displayed in 3 views – axial, coronal and sagittal.
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model
ARTICLE IN PRESS
JOMSMP-557; No. of Pages 6
K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
4 Table 2 Characteristics of maxillary septa. Sinuses examined
Presence of septa
Location of septa
224
38.3% Mean height: 5.95 mm Complete septa: 89.5%
Anterior Middle Posterior
Orientation of septa 36% 29.1% 34.9%
Bucco-lingual Transverse Sagittal
Origin of septa 93 5.8 1.2
Primary Secondary
61.6 38.4
comparing septa found in DPT and that found in CT scans [17]. Gonzalez-Santana et al. reported 11.8% of false-negatives when diagnosing septa using DPT [20]. Maestre-Ferrin et al. also reported that a lower prevalence of septa was detected in DPT when compared to CT scans [30]. To accurately determine the location and morphology of septa, a CBCT scan would be advisable prior to surgery. Wherever CBCT imaging is used, it is advisable to check for presence of septa. Proper planning and access to the sinus cavity reduces the risk of membrane perforation.
Fig. 2. Illustration of an incomplete septum.
the alveolar crest (Table 3) (Fig. 5). If the anastomosis was not visible, it was likely to be extra-osseous. 4. Discussion The purpose of this study was to find out the prevalence and location of maxillary sinus septa and arterial anastomosis in a sample of the patient population in Singapore. A total of 139 patients and 224 maxillary sinuses were examined. All the patients that met the inclusion criteria happened to be from ethnic Chinese background. This probably reflects the reality of the patient demographics around the hospital and the referral pattern to the National University Hospital, Singapore. Perhaps looking at and comparing the data from other centres with majority population of other races would help to further delineate the variances. This is the first study looking at the prevalence in the population of Singapore.
Fig. 4. Illustration of a primary septum (right) and secondary septum (left).
The prevalence of septa within patients is 46% and prevalence of septa within maxillary sinuses is 38.3%. The figures are slightly higher when compared to another study conducted by Shen et al. who reported the prevalence of septa as 29.3% in an ethnic Chinese population in Taiwan [31]. This, however, is comparable to other studies reported in the literature (26–44%) [9,11,17,18,24,27–29,34]. The incidence of maxillary sinus septa was first investigated by Underwood in 1910 and is known as Underwood’s septa [35]. According to Underwood, septa are formed because of different eruption phases of teeth. Septa are the remaining intervening bone partitions when the rest of the bony floor sinks down between the dental roots of adjacent teeth during eruption. He reported a 33% incidence of septa in the maxillary sinus. The function of septa is largely unknown. Van den Bergh et al. postulated that septa act as struts to withstand masticatory forces during the dentate stage of life [2]. As was alluded earlier, a false negative finding can result in surgical complications. Septa formation was most commonly seen at the anterior region (36.0%), followed by the posterior (34.9%) and middle region (29.1%). However, there was no significant difference in distribution of septa between the 3 regions. The results were similar to studies done by Ulm et al. [15], Krennmair et al. [14] and Neugebauer et al. [27], who
Fig. 3. Illustration of a complete septum.
CBCT scans were used to determine the presence of septa. The literature has shown that DPT alone is not accurate in diagnosing presence of septa. Krennmair et al. found that DPT led to false diagnosis of presence or absence of septa in 21.5% of cases after clinically verifying the septa during sinus augmentation surgery [14]. Kasabah et al. reported false diagnosis in 44% of cases after
Table 3 Distance of intra-osseous anastomosis from alveolar crest. Total sinuses examined
224
Total sinuses with intra-osseous anastomosis visible on coronal view Mean distance of intra-osseous anastomosis from alveolar crest
100 (45%) 17.8 mm
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
5
Fig. 5. Illustration of measurement of distance from intra-osseous anastomosis to alveolar crest.
concluded that the anterior region contained the majority of septa. Some studies have reported that more septa are located in the middle region [16,18,20,25,26,28–31]. This could be due to the lack of uniformity in defining the location in different studies, especially in edentulous areas where there is lack of teeth. In terms of orientation, 93% (80/86) of septa demonstrated bucco-lingual direction, which was the most common orientation of the septa in this study and this is in agreement with other studies in the literature [14,18,25,29,31]. Clinically, the septa that would most likely hinder lateral window sinus grafting would be the bucco-lingual septa. When septa are present on the antral floor, Boyne and James suggested cutting them with a narrow chisel and removing them with a hemostat [1]. This allows the bone graft to be placed over the entire antral floor without interruption. Van den Bergh et al. suggested making a W-shaped trap door to reduce risk of perforation when elevating the maxillary sinus membrane [2]. Zijderveld et al. suggested making 2 trap doors – one anterior and one posterior to the septum instead of the classical one trap door design [6]. Whichever technique is adopted, accurate localization of the septa, their orientation and length is important when deciding on the surgical approach to the lateral window. A great majority of the septa (81 out of 88) were measurable. There were 5 transverse septa which were excluded because the height could not be measured. The mean height of the 81 septa was 5.95 mm. The mean height of septa in the literature ranged from 2.5 mm to 9.2 mm [14,16,18,20,25–27,29,30]. Kim et al. [18], Maestre-Ferrin et al. [30] and Shen et al. [31] only considered septa with height of at least 2.5 mm to be clinically relevant. This is likely because the lower border of the lateral window is usually located 3 mm above the level of the sinus floor. In our study, the mean height of the septa was almost 6 mm. This may impede the in-fracture of the lateral window and hinder access during sinus augmentation. In such cases, an out fracture approach may be more advisable. As septa increase in height, the difficulty in elevation of the sinus membrane from the septa surface increases as well. There was a significant difference between males and females in terms of occurrence of septa. 58.6% of males compared to 33.3% of females demonstrated presence of septa. Using Fisher’s Exact Test, the difference was statistically significant (P < 0.05). It is interesting that males demonstrated significantly higher prevalence of septa compared to females in this study. This could possibly be attributed to increased masticatory forces in males leading to an increased formation of septa. Among the different states of dentition, fully edentulous patients were most likely to demonstrate presence of septa (55.6%), followed by partially edentulous patients (50%) and fully dentate patients (40%). Krennmair et al. [14], Kim et al. [18], Van Zyl and Van Heerden [25] and Lee et al. [28] also reported higher incidences of septa in edentulous regions compared to dentate regions. However, there was no significant difference in occurrence of septa between the different states in this study (P > 0.05). Secondary septa
are known to be acquired and develop in edentulous regions due to pneumatization of the maxillary sinus after tooth loss [14]. This could likely be why the prevalence of septa is higher in edentulous regions. Significant differences in the origin of septa were found between patients with different states of dentition. Dentate patients were significantly more likely to have primary septa and fully edentulous patients were more likely to have secondary septa. According to Krennmair et al., primary septa are congenital in nature and evolve during the growth of the middle face whereas secondary septa form as a result of tooth loss and irregular pneumatization of the sinus floor [14]. The ‘bony crests’ formed as a result of atrophy of the alveolar process are what is known as secondary septa. Significant differences in height were found between primary and secondary septa. In this study, primary septa were significantly taller than secondary septa. This is in agreement with Kim et al. who found that primary septa were significantly taller than secondary septa [18]. This is because primary septa are formed congenitally during growth of the middle face and are not subjected to effects of alveolar resorption after tooth loss. Secondary septa are formed as ‘bony crests’ as a result of atrophy of the alveolar process. Thus, primary septa are generally taller than secondary septa. From this study, it was concluded that the state of dentition (i.e. dentate/partially edentulous/fully edentulous) did not influence variables such as location, orientation, completeness and height of septa. Similarly, location of septa (i.e. anterior/middle/posterior) did not influence variables such as orientation, completeness, origin and height of septa. In addition, origin of septa (i.e. primary/secondary) did not influence variables such as orientation and completeness of septa. Profuse bleeding during osteotomy of the lateral window can occur at times. This usually occurs when performing the vertical osteotomy cuts of the lateral window. The anastomosis between the infra-orbital artery and posterior superior alveolar artery was visible on the coronal view of 100 maxillary sinuses (out of a total of 224 sinuses). The blood vessel anastomosis was not always visible as they could be extra-osseous [10,11,33]. In this study, the voxel size of 0.12–0.2 mm and slice thickness of 0.1–0.4 mm was sufficient for identification of the intra-osseous anastomosis. The mean distance of the intra-osseous anastomosis from the alveolar crest is 17.8 mm in this study, which is similar to other studies previously conducted. Solar et al. [33] conducted a cadaveric study on 18 maxillas and found that the intra-osseous anastomosis was 19 mm from the alveolar crest. Guncu et al. [10] and Kang et al. [11] conducted a CT study and found that the intra-osseous anastomosis was also 19 mm from the alveolar crest. A point can be made that after extractions, there will be vertical bony resorption, thus making any measurements from the alveolar crest inaccurate. This is especially true for total edentulism or partially dentate situations whereby the posterior maxillary teeth had been extracted. An alternative reference point of measurement could be from the
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005
G Model JOMSMP-557; No. of Pages 6
ARTICLE IN PRESS K.L. Hong et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2016) xxx–xxx
6
infraorbital foramen. This would then bring up the question of whether the location of the infraorbital foramen is constant both in terms of distance from the orbital rims and also if the location varies between races or sex. We have no information on this and this would make a good point for further study. The other counter point for this would be previous studies all measured the distance from the alveolar crest and using this reference point serves as a point of comparison to other studies and also from a practical point of view during surgery, it is easier to measure the distance from the alveolar crest than from the infraorbital foramen as this would mean more periosteal stripping and consequently, more edema. The position of the lateral window design should be made after analysis of the amount of sub-antral bone height on CBCT. In cases where the superior border of the lateral window is more than 17 mm from the alveolar crest, there may be an increased risk of encountering the blood vessel during osteotomy. Haemostasis may be achieved with methods such as electrocautery. In cases where the blood vessel is not encountered, the anastomosis is likely to be extra-osseous in nature. Both Solar et al. [33] and Kang et al. [11] reported that the extra-osseous anastomosis is located superior to the intra-osseous anastomosis and is usually located around 23 mm away from the alveolar crest. Extraosseous anastomosis may be less commonly encountered as it may be retracted within the mucoperiosteal flap and thus protected from the osteotomy site. 5. Conclusion The prevalence of septa within maxillary sinuses in the ethnic Chinese population in Singapore is found to be 35.7%, which is similar to other studies. Orientation of the septa was most common in a bucco-medial direction. The distance of the arterial anastomosis was at an average of 17.8 mm from the alveolar crest. This prevalence prevails upon the operator to take more detailed scans to detect these structures. The location of septa and anastomosis can be detected quite readily with a CBCT, which can help to clue in the operator to take steps to prevent sinus membrane perforation or bleeding during the procedure. Conflict of interest There is no conflict of interest in this study. References [1] Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980;38:613–6. [2] Van den Bergh JP, Ten Bruggenkate CM, Disch FJ, Tuinzing DB. Anatomical aspects of sinus floor elevations. Clin Oral Implants Res 2000;11:256–65. [3] Shlomi B, Horowitz I, Kahn A, Dobriyan A, Chaushu G. The effect of sinus membrane perforation and repair with Lambone on the outcome of maxillary sinus floor augmentation: a radiographic assessment. Int J Oral Maxillofac Implants 2004;19:559–62. [4] Ardekian L, Oved-Peleg E, Mactei EE, Peled M. The clinical significance of sinus membrane perforation during augmentation of the maxillary sinus. J Oral Maxillofac Surg 2006;64:277–82. [5] Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol 2008;35(Suppl):216–40. [6] Zijderveld SA, Van den Bergh JP, Schulten EA, Ten Bruggenkate CM. Anatomical and surgical findings and complications in 100 consecutive maxillary sinus floor elevation procedures. J Oral Maxillofac Surg 2008;66:1426–38. [7] Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical complications of the sinus graft procedure and their impact on implant survival. J Periodontol 2004;75:511–6.
[8] Hernandez-Alfaro F, Torradeflot MM, Marti C. Prevalence and management of Schneiderian membrane perforations during sinus-lift procedures. Clin Oral Implants Res 2008;19:91–8. [9] Malkinson S, Irinakis T. The influence of interfering septa on the incidence of Schneiderian membrane perforations during maxillary sinus elevation surgery: a retrospective study of 52 consecutive lateral window procedures. J Oral Surg 2009;2:19–25. [10] Guncu GN, Yildirim YD, Wang HL, Tozum TF. Location of posterior superior alveolar artery and evaluation of maxillary sinus anatomy with computerized tomography: a clinical study. Clin Oral Implants Res 2011;22:1164–7. [11] Kang SJ, Shin SI, Herr Y, Kwon YH, Kim GT, Chung JH. Anatomical structures in the maxillary sinus related to lateral sinus elevation: a cone beam computed tomographic analysis. Clin Oral Implants Res 2013;24(Suppl A100):75–81. [12] Tatum OH.Lecture Presented to the Alabama Implant Congress. 1976. [13] Betts NJ, Miloro M. Modification of the sinus lift procedure for septa in the maxillary antrum. J Oral Maxillofac Surg 1994;52:332–3. [14] Krennmair G, Ulm C, Lugmayr H. Maxillary sinus septa: incidence, morphology and clinical implications. J Craniomaxillofac Surg 1997;25:261–5. [15] Ulm CW, Solar P, Krennmair G, Matejka M, Watzek G. Incidence and suggested surgical management of septa in sinus-lift procedures. Int J Oral Maxillofac Implants 1995;10:462–5. [16] Velasquez-Plata D, Hovey LR, Peach CC, Alder ME. Maxillary sinus septa: a 3-dimensional computerized tomographic scan analysis. Int J Oral Maxillofac Implants 2002;17:854–60. [17] Kasabah S, Slezak R, Simunek A, Krug J, Lecaro MC. Evaluation of the accuracy of panoramic radiograph in the definition of maxillary sinus septa. Acta Medica (Hradec Kralove) 2002;45:173–5. [18] Kim MJ, Jung UW, Kim CS, Kim KD, Choi SH, Kim CK, et al. Maxillary sinus septa: prevalence, height, location, and morphology. A reformatted computed tomography scan analysis. J Periodontol 2006;77:903–8. [19] Shibli JA, Faveri M, Ferrari DS, Melo L, Garcia RV, d’Avila S, et al. Prevalence of maxillary sinus septa in 1024 subjects with edentulous upper jaws: a retrospective study. J Oral Implantol 2007;33:293–6. [20] Gonzalez-Santana H, Penarrocha-Diago M, Guarinos-Carbo J, Sorni-Broker M. A study of the septa in the maxillary sinuses and the subantral alveolar processes in 30 patients. J Oral Implantol 2007;33:340–3. [21] Selcuk A, Ozcan KM, Akdogan O, Bilal N, Dere H. Variations of maxillary sinus and accompanying anatomical and pathological structures. J Craniofac Surg 2008;19:159–64. [22] Ella B, Noble Rda C, Lauverjat Y, Sedarat C, Zwetyenga N, Siberchicot F, et al. Septa within the sinus: effect on elevation of the sinus floor. Br J Oral Maxillofac Surg 2008;46:464–7. [23] Gosau M, Rink D, Driemel O, Draenert FG. Maxillary sinus anatomy: a cadaveric study with clinical implications. Anat Rec (Hoboken) 2009;292:352–4. [24] Naitoh M, Suenaga Y, Kondo S, Gotoh K, Ariji E. Assessment of maxillary sinus septa using cone-beam computed tomography: etiological consideration. Clin Implant Dent Relat Res 2009;11(Suppl 1):e52–8. [25] Van Zyl AW, Van Heerden WF. A retrospective analysis of maxillary sinus septa on reformatted computerised tomography scans. Clin Oral Implants Res 2009;20:1398–401. [26] Rosano G, Taschieri S, Gaudy JF, Lesmes D, Del Fabbro M. Maxillary sinus septa: a cadaveric study. J Oral Maxillofac Surg 2010;68:1360–4. [27] Neugebauer J, Ritter L, Mischkowski RA, Dreiseidler T, Scherer P, Ketterle M, et al. Evaluation of maxillary sinus anatomy by cone-beam CT prior to sinus floor elevation. Int J Oral Maxillofac Implants 2010;25:258–65. [28] Lee WJ, Lee SJ, Kim HS. Analysis of location and prevalence of maxillary sinus septa. J Periodontal Implant Sci 2010;40:56–60. [29] Park YB, Jeon HS, Shim JS, Lee KW, Moon HS. Analysis of the anatomy of the maxillary sinus septum using 3-dimensional computed tomography. J Oral Maxillofac Surg 2011;69:1070–8. [30] Maestre-Ferrin L, Galan-Gil S, Rubio-Serrano M, Penarrocha-Diago M, Penarrocha-Oltra D. Maxillary sinus septa: a systematic review. Med Oral Patol Oral Cir Bucal 2010;15:383–6. [31] Shen EC, Fu E, Chiu TJ, Chang V, Chiang CY, Tu HP, et al. Prevalence and location of maxillary sinus septa in the Taiwanese population and relationship to the absence of molars. Clin Oral Implants Res 2012;23:741–5. [32] Lana JP, Carneiro PM, Machado Vde C, de Souza PE, Manzi FR, Horta MC. Anatomic variations and lesions of the maxillary sinus detected in cone beam computed tomography for dental implants. Clin Oral Implants Res 2012;23:1398–403. [33] Solar P, Geyerhofer U, Traxler H, Windisch A, Ulm C, Watzek G. Blood supply to the maxillary sinus relevant to sinus floor elevation procedures. Clin Oral Implants Res 1999;10:34–44. [34] Rysz M, Bakon L. Maxillary sinus anatomy variation and nasal cavity width: structural computed tomography imaging. Folia Morphol (Warsz) 2009;68:260–4. [35] Underwood AS. An inquiry into the anatomy and pathology of the maxillary sinus. J Anat Physiol 1910;44:354–69.
Please cite this article in press as: Hong KL, et al. Cone beam computed tomographic evaluation of the maxillary sinus septa and location of blood vessels at the lateral maxillary sinus wall in a sample of the Singaporean population. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.005