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Proximity of Vascular Bone Channel in the Lateral Sinus Wall to Root Apices of Maxillary First Molars: A Cone-beam Computed Tomographic Analysis
CLINICAL RESEARCH
Proximity of Vascular Bone Channel in the Lateral Sinus Wall to Root Apices of Maxillary First Molars: A Cone-beam Computed Tomographic Analysis ABSTRACT Introduction: Apical surgery is frequently indicated in maxillary first molars. Occasionally, a vascular anastomosis in the lateral maxillary sinus wall can be observed during surgery. The aim of this study was to examine the distance between the vascular bone channel (VBC) and the root apices of maxillary first molars using cone-beam computed tomographic imaging. Methods: Cone-beam computed tomographic images of 104 maxillary first molars were oriented in the coronal plane to evaluate the distance between the roots and the VBC. The measurements were only recorded in relation to the buccal roots. In addition, demographic parameters and further measurements such as the diameter of the VBC and the proximity to the periapical pathology were evaluated. Results: A total of 210 VBCs were assessed. The mean distance from the VBC to the apices of the buccal roots of the maxillary first molars was 6.18 mm 6 3.84 mm. The VBC was mostly located intrasinusally (74.3%) and only rarely superficially (0.5%). The diameter of the VBC was on average 0.88 6 0.32 mm. Conclusions: In this study, the VBC was usually found closer to the mesiobuccal than to the distobuccal root apex. During preparation of the access window, the existence of the VBC should be kept in mind because the mesiobuccal roots of maxillary first molars undergo apical surgery to the buccally positioned roots only. (J Endod 2019;-:1–7.)
KEY WORDS
Frank M. Bischof, DMD,* Michael M. Bornstein, DMD,† Valerie G.A. Suter, DMD,* Ryan I.E. Lello, DMD,* and Thomas von Arx, DMD*
SIGNIFICANCE Distances between the VBC and its surrounding anatomic structures were generally shorter in females than in males, and the VBC was located closer to mesiobuccal roots than to distobuccal roots of maxillary first molars. During preparation of the access window, the existence of the VBC should be kept in mind because mesiobuccal roots of maxillary first molars often need apical surgery because of their complex root canal anatomy.
Apical surgery; cone-beam computed tomography; maxillary first molar; vascular bone channel
One of the signs of root canal treatment failure is the presence of microbial infection and, as an objectivized symptom, a fistula and/or the persistence of pain. Failures of root canal treatment can be categorized as anatomic (isthmus, apical ramifications, and accessory canals), iatrogenic (perforations and fractured instruments), pathological (pulp canal obliteration, cysts, and neoplasia), or technical (orthograde access blocked by a post and/or a crown). To preserve teeth with failing endodontic treatment, apical surgery is an established treatment option1. A frequent tooth to be treated with apical surgery is the first maxillary molar because of its complex root canal anatomy, in particular of the mesiobuccal root. An important issue to consider in apical surgery is the risk of potentially jeopardizing or injuring adjacent anatomic structures. The root apices of teeth in the posterior maxilla are located close to the floor of the maxillary sinus. The apex of the first premolar is the furthest from the sinus floor. Posteriorly, the distances constantly decrease until the mesiobuccal root of the second molar2. Because the surgical access and room for microsurgical instruments in the posterior maxilla are limited, knowledge about periapical bone dimensions is of interest3. Four branches of the maxillary artery perfuse the lateral maxillary sinus wall: the posterior superior alveolar artery (PSAA), the anterior superior alveolar artery, the descending palatine artery, and the infraorbital artery4. A cadaver study reported the existence of an extraosseous and an intraosseous
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From the *Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Bern, Bern, Switzerland; and † Oral and Maxillofacial Radiology, Applied Oral Sciences, Faculty of Dentistry, The University of Hong Kong, Prince Philip Dental Hospital, Sai Ying Pun, Hong Kong SAR, China Address requests for reprints to Dr Frank M. Bischof, Department of Oral Surgery and Stomatology, University of Bern, Freiburgstrasse 7, CH-3010, Bern, Switzerland. E-mail address: frank.bischof@zmk. unibe.ch 0099-2399/$ - see front matter Copyright © 2019 American Association of Endodontists. https://doi.org/10.1016/ j.joen.2019.09.004
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anastomosis between the PSAA and the anterior superior alveolar artery5. The intraosseous anastomosis, running inside a vascular bone channel (VBC), supplies the teeth and the periodontium in the posterior maxilla as well as the Schneiderian membrane lining the lateral sinus wall5. Surgical interventions such as apical surgery in the posterior maxilla or sinus floor elevation procedures can entail several risks, including the rupture of the Schneiderian membrane or damage to the VBC with subsequent hemorrhage6. The use of cone-beam computed tomographic (CBCT) imaging for diagnosis and treatment planning of apical surgery is becoming increasingly accepted as a standard imaging procedure because of its lower radiation dose and better resolution than conventional computed tomographic (CT) imaging7,8. CBCT imaging enables a better understanding of the root position and its surrounding anatomic structures compared with 2-dimensional radiography9. The primary objective of the present study was to examine the distance from the VBC to the root apices of maxillary first molars scheduled for apical surgery using CBCT imaging. Secondary outcomes included demographic parameters and additional measurements such as the diameter of the VBC, the relationship between the VBC and adjacent anatomic structures including the maxillary sinus floor and the buccal cortical wall, and the distance from the VBC to the apical radiolucency when present.
MATERIALS AND METHODS Patient Selection The CBCT images were selected from patients who underwent radiologic assessment of the maxillary sinus and posterior maxilla before apical surgery between March 2006 and May 2017. Patients were excluded from this study if they were younger than 18 years old or had a history of maxillary sinus trauma, surgery, or orthognathic intervention; patients with supernumerary teeth, impacted teeth, foreign bodies, previous apical surgery, artifacts hindering image interpretation, or root resorptions within the region of interest were also excluded. The local ethics committee approved the study protocol (KEK-BE 2018-00387).
Radiographic Assessment The CBCT images were all recorded with a 3D Accuitomo 80 or 170 unit (J Morita Corp, Kyoto, Japan). The exposure parameters were 5–7 mA and 80–90 kV, and the exposure time was 17.5 seconds with a full scan rotation (360 ). The field of view was chosen according to the indication and the diagnostic requirements but always following the “as low as diagnostically acceptable” principle10. The different field of views used included 40 ! 40 mm, 60 ! 60 mm, 80 ! 80 mm, or 100 ! 100 mm with corresponding voxel sizes between 0.08 mm and 0.25 mm, respectively. All measurements were made with the corresponding software (iDixel, version 2.0.4, J Morita Corp). A calibrated observer (F.B.), not involved in any surgery, performed the
measurements on a 19-inch Eizo Flexscan monitor with a resolution of 1280 ! 1024 pixels (Eizo Nanao AG, W€adenswil, Switzerland). To assess the intraobserver reliability, the measurements of 20 randomly selected (https://www.randomizer.org) cases were repeated after a washout period of 4 weeks. For an optimal depiction of the root apices and the VBC, the CBCT images were manipulated in all 3 anatomic planes. If roots were curved, the CBCT slice was oriented along the apical root portion. The study sites were examined in the coronal plane. The following parameters were analyzed in the mesiobuccal and distobuccal roots of maxillary first molars: A: the shortest distance between the VBC and the root apex (Fig. 1A and B) B: the largest diameter of the VBC (Fig. 1) C: the horizontal distance from the VBC to the lateral cortical wall (Fig. 1) D: the shortest distance from the VBC to the apical radiolucency (when present) (Fig. 1) E: the vertical distance from the lower border of the VBC to the floor of the maxillary sinus using a horizontal auxiliary line; when the VBC was located below the floor of the maxillary sinus, the value for the distance was negative (Fig. 1) F: assessment of the location of the VBC relative to the root apex (palatal, above, or buccal) (Fig. 2A–F) G: assessment of the location of the VBC within the lateral wall of the maxillary sinus (intrasinusal/intraosseous/superficial)11 (Fig. 2)
FIGURE 1 – (A ) A schematic illustration and (B ) CBCT image of the VBC (*) and its shortest distance to the root apex (A, 3.37 mm); its diameter (B, 1.38 mm); and its distance to the buccal bone wall (C, 5.87 mm), the apical radiolucency (D, 0.20 mm), and the maxillary sinus floor (E, 3.63 mm).
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FIGURE 2 – Locations of the VBC relative to the root apex were classified as (A ) palatal, (B ) above, or (C ) buccal. Locations relative to the lateral border of the maxillary sinus were classified as (D ) intrasinusal, (E ) intraosseous, or (F ) superficial. Additionally, the side (right/left) as well as patient-related data (age and sex) were evaluated.
Statistical Analysis All data were first analyzed using descriptive statistics. The detailed differences between mesiobuccal and distobuccal roots were then compared using paired t tests. If the differences between mesiobuccal and distobuccal roots were significant in at least 1 parameter, then separated analyses for each type of roots were performed with Bonferroni adjustment. The teeth were assumed as
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independent within the same person. Age was dichotomized by a median split, yielding 2 age groups for further statistical analysis. The effects of the binary independent variables (sex, side, and age) on the linear measurements were separately evaluated with 2-sample t tests. The effects of the binary independent variables (sex, side, and age) on VBC location were evaluated with the Pearson chi-square test (or the Fisher exact test if .20% of the cells had an expected count ,5). The significance level chosen for all statistical tests was set at P , .05. Statistical
procedures were all performed SPSS Version 25.0 (IBM Corp, Armonk, NY).
RESULTS This retrospective study evaluated 104 first maxillary molars resulting in 208 buccal roots with a nearly equal distribution of 48 women (46.2%) and 56 men (53.9%). The mean age of the patients was 52.7 years (median 5 52 years) with a range of 22–79 years. The VBC was identified in all 104 scans; however, it was only detected in 203 of 208 roots (97.6%) that met the inclusion criteria. In 5 coronal slice
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TABLE 1 - The Mean Distances between the Vascular Bone Channel (VBC) and the Measured Surrounding Anatomic Structures A–E at the Mesiobuccal (MB)/Distobuccal (DB) Roots and Pooled per Tooth in Millimeters MB
DB
P value
Pooled per tooth
6.02 6 3.75 (n 5 105) 0.88 6 0.29 (n 5 105) 1.38 6 1.16 (n 5 105) 4.46 6 3.70 (n 5 98) 5.95 6 4.12 (n 5 105)
6.34 6 3.95 (n 5 105) 0.89 6 0.36 (n 5 105) 1.51 6 1.00 (n 5 105) 5.06 6 3.79 (n 5 93) 6.88 6 4.02 (n 5 105)
.06 .80 .62 .00* .00*
6.18 6 3.84 (N 5 210) 0.88 6 0.32 (N 5 210) 1.44 6 1.08 (N 5 210) 4.75 6 3.75 (N 5 191) 6.41 6 4.08 (N 5 210)
Distances VBC to root apex (A) Diameter of VBC (B) VBC to lateral bone surface (C) VBC to apical radiolucency (D) VBC to maxillary sinus floor (E) Values are mean 6 standard deviation. *P , .05, significant difference.
images, the VBC could not be located because of its course through the apical radiolucency. Five individuals (4.81%) showed the presence of a bifid VBC. In 3 cases, the bifid VBC was identified either at the mesiobuccal or the distobuccal root, whereas in 2 cases it was found at both roots. Therefore, a total of 210 VBCs were analyzed. The repetition of the measurements in 20 cases for parameters A to G showed an excellent intraobserver reliability (intraclass correlation coefficient values between 0.980– 1.000 and all kappa values as 1.000). The mean distances between the VBC and its surrounding anatomic structures are listed in Table 1. The mean proximity of the VBC to the root apex (A) was 6.18 mm 6 3.84 mm (N 5 210). The VBC lay mostly within 4.01–10 mm (51%) to the root apex but also frequently occurred 4 mm or closer (34.3%). The mean diameter of the VBC (B) measured as 0.88 mm 6 0.32 mm (N 5 210) (Table 1). The frequency analysis showed that the diameter of the VBC was greater than 1 mm in 31.4% of the roots evaluated. The mean shortest distance to an apical radiolucency (D) was 4.75 mm 6 3.75 mm (n 5 191); 19 roots were not evaluated for category D because they had no periapical pathology. The mean distance between the VBC and the lateral bone surface (C) was 1.44 mm 6 1.08 mm (N 5 210), and the vertical distance between
the VBC and the floor of the maxillary sinus (E) was 6.41 mm 6 4.08 mm (N 5 210) on average. The VBC was mostly located buccally (53.8%) but was also found above (38.1%) or palatally (8.1%) in relation to the apices (F). Most frequently, the VBC was found intrasinusally (74.3%). Intraosseous (25.2%) and, rarely, superficial positions (0.5%) were also observed (G). The detailed differences between the mesiobuccal and distobuccal roots are presented in Table 1, and significant differences were found for VBC in relation to the apical radiolucency (D) and VBC to the maxillary sinus floor (E) (both P 5 .00). In general, women showed lower values for parameters A–E (Table 2) compared with men. Statistically significant differences were detected for diameter (B) in both mesiobuccal and distobuccal roots (P 5 .00) and for the distance from the VBC to the lateral bone surface (C) in distobuccal roots (P , .03). The distance between the VBC and the lateral cortical wall (C) was shorter in the older than in the younger age group (P , .02) in mesiobuccal roots. The distance between the VBC and the maxillary sinus floor (E), the distance from the VBC to the root apices (A), the diameter of the VBC (B), and the distance to periapical radiolucencies (D) were similar for both age groups (all P . .05) (Table 3). When comparing the right and left side, only minor
but not statistically significant differences were found (all P . .05). Sex significantly affected the distribution with regard to VBC location to the root apex (F). In mesiobuccal roots, the VBC was located in a buccal position more often in women than in men (P , .05) (Table 4). The side affected the distribution with regard to VBC location in relation to the lateral sinus wall (G), with the left side having a significantly higher rate of VBCs intrasinusally and a lower rate in intraosseous position than the right side (P 5 .02) in mesiobuccal roots (Table 4). For distobuccal roots, no significant different proportion distributions were found for VBC location with regard to the root apex (F) and lateral sinus wall (G) when assessed for the influencing factors of sex, age, and side.
DISCUSSION This radiographic analysis assessed the VBC in the lateral maxillary sinus wall and its relation to the buccal roots of the maxillary first molars using reoriented CBCT images. The VBC was present in 97.6% of the root apices, which is comparable with data from former cadaver studies that described a VBC in 100% of the root apices5,12,13. The discrepancy might be explained by the fact that the presence of a periapical lesion may inhibit the identification of a nearby VBC in CBCT images.
TABLE 2 - The Mean Distances between the Vascular Bone Channel (VBC) and the Measured Structures A–E Regarding Sex at the Mesiobuccal (MB)/Distobuccal (DB) Roots in Millimeters MB
VBC to root apex (A) Diameter of VBC (B) VBC to lateral bone surface (C) VBC to apical radiolucency (D) VBC to maxillary sinus floor (E)
DB
Female
Male
P value
Female
Male
P value
5.72 6 3.38 (n 5 49) 0.74 6 0.23 (n 5 49) 1.19 6 0.82 (n 5 49)
6.29 6 4.06 (n 5 56) 1.01 6 0.28 (n 5 56) 1.54 6 1.37 (n 5 56)
.88 .00* .24
6.16 6 3.48 (n 5 49) 0.74 6 0.25 (n 5 49) 1.25 6 0.82 (n 5 49)
6.50 6 4.34 (n 5 56) 1.02 6 0.39 (n 5 56) 1.73 6 1.10 (n 5 56)
1.00 .00* .03*
4.32 6 3.28 (n 5 46)
4.58 6 4.07 (n 5 52)
1.00
5.05 6 3.38 (n 5 43)
5.06 6 4.15 (n 5 50)
1.00
5.88 6 3.75 (n 5 49)
6.01 6 4.45 (n 5 56)
1.00
6.34 6 3.30 (n 5 49)
7.36 6 4.53 (n 5 56)
.39
Distances
Values are mean 6 standard deviation. *P , .05, significant difference.
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TABLE 3 - The Mean Distances between the Vascular Bone Channel (VBC) and the Measured Structures A–E Regarding Age at the Mesiobuccal (MB)/Distobuccal (DB) Roots in Millimeters MB Distances VBC to root apex (A) Diameter of VBC (B) VBC to lateral bone surface (C) VBC to apical radiolucency (D) VBC to maxillary sinus floor (E)
DB
22–52 years
53–79 years
P value
22–52 years
53–79 years
P value
6.07 6 3.58 (n 5 51) 0.90 6 0.31 (n 5 51) 1.69 6 1.47 (n 5 51)
5.98 6 3.93 (n 5 54) 0.86 6 0.27 (n 5 54) 1.08 6 0.64 (n 5 54)
1.00 .93 ,.02*
6.11 6 3.64 (n 5 53) 0.92 6 0.39 (n 5 53) 1.70 6 1.05 (n 5 53)
6.59 6 4.26 (n 5 52) 0.86 6 0.32 (n 5 52) 1.30 6 0.91 (n 5 52)
1.00 .88 .08
4.44 6 3.63 (n 5 46)
4.47 6 3.80 (n 5 52)
1.00
4.95 6 3.58 (n 5 47)
5.16 6 4.04 (n 5 46)
1.00
5.256 3.71 (n 5 51)
6.60 6 4.40 (n 5 54)
.19
6.34 6 3.59 (n 5 53)
7.44 6 4.37 (n 5 52)
.33
Values are mean 6 standard deviation. *P , .05, significant difference.
Nevertheless, CBCT imaging is an appropriate tool for the anatomic evaluation of bony structures as well as for planning of complex surgical interventions such as apical surgery. The mean shortest distance from the VBC to the root apex was 6.18 mm. This is in contrast to a previous study14 in which it was located a greater distance away (8.3 mm 6 3.3 mm). In the literature, a small number of CT studies15–17, 1 cadaver study5, and several CBCT studies11,14,18–20 assessed the topographic relationship between the VBC and the surrounding anatomic structures. However, only a few used a methodology
similar to the present study. When comparing the distance between the VBC and the maxillary sinus floor, the anatomic plane in which the images are analyzed is crucial. Only 2 CBCT studies with a comparable methodology were identified that assessed CBCT images in the coronal plane11,14. Kang et al14 analyzed 150 CBCTs of a Korean population. Generally, higher values were reported in their study (Table 5), and ethnicity might be a possible explanation for these differences. Another study examined 860 sinuses in 430 patients of a white population11. The detection rate of the VBC (anastomosis of
the PSAA) was 60.6%, which is substantially lower than in the present study (97.6%). The diameter (1.17 mm) and the distance to the sinus floor (8.09 mm) were greater than in the present study. The use of different CBCT machines and settings might be a possible explanation. Furthermore, Danesh-Sani et al11 do not mention where exactly the diameter of the VBC was measured. Regarding the diameter of the VBC, the findings in the present study (0.88 6 0.32 mm) were generally a little lower than the data described in previous studies that also evaluated reoriented CBCT images (Table 5).
TABLE 4 - The Location of the Vascular Bone Channel (VBC) in Relation to the Root Apex and the Lateral Sinus Wall in Mesiobuccal (MB) Roots MB Location Relative to root apex (F) Total Sex Female Male Age group 22–52 years 53–79 years Side Left side Right side Location Relative to lateral sinus wall (G) Total Sex Female Male Age group 22–52 years 53–79 years Side Left side Right side
P value
Palatal, %
Above, %
Buccal, %
9.5 (n 5 10)
47.6 (n 5 50)
42.9 (n 5 45)
4.1 (n 5 2) 14.3 (n 5 8)
38.8 (n 5 19) 55.4 (n 5 31)
57.1 (n 5 28) 30.4 (n 5 17)
.03*
13.7 (n 5 7) 5.6 (n 5 3)
47.1 (n 5 24) 48.1 (n 5 26)
39.2 (n 5 20) 46.3 (n 5 25)
.68
13.1 (n 5 8) 4.5 (n 5 2)
45.9 (n 5 28) 50.0 (n 5 22)
41.0 (n 5 25) 45.5 (n 5 20)
.67
P value
Inside, %
Central, %
Outside, %
65.7 (n 5 69)
33.3 (n 5 35)
1.0 (n 5 1)
59.2 (n 5 29) 71.4 (n 5 40)
40.8 (n 5 20) 26.8 (n 5 15)
0.0 (n 5 0) 1.8 (n 5 1)
.30†
68.6 (n 5 35) 63.0 (n 5 34)
29.4 (n 5 15) 37.0 (n 5 20)
2.0 (n 5 1) 0.0 (n 5 0)
.94†
75.4 (n 5 46) 52.3 (n 5 23)
23.0 (n 5 14) 47.7 (n 5 21)
1.6 (n 5 1) 0.0 (n 5 0)
.02*†
*P , .05, significant difference. † Fisher exact test.
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TABLE 5 - An Overview of Studies (in Chronologic Order) Assessing the Distance between the Vascular Bone Channel (VBC) and the Maxillary Sinus Floor (mm) and the Diameter of the VBC (mm)
Authors
Study material 19
Ilguy et al, 2013 Kang et al, 201314 Apostolakis et al, 201520 Danesh-Sani et al, 201711 Present study
135 patients 150 patients 156 patients 430 patients 104 patients
Methodology
Distance between VBC and sinus floor
Diameter of VBC
CBCT (coronal plane) CBCT (coronal plane)* CBCT (axial plane) CBCT (coronal plane) CBCT (coronal plane)
— 8.3 6 3.3 — 8.09 (0.43–30.90) 6.41 6 4.08
0.94 6 0.26 \ 1.07 6 0.43, _ 1.24 6 0.44 1.1 6 0.4 1.17 (0.4–2.8) 0.88 6 0.32 \ 0.74 6 0.25 _ 1.01 6 0.33
—, distance was not measured in this study. *Distances were measured at 6 different sites.
Different ethnicities and/or evaluation in a different plane could be possible reasons for this. An earlier CT study observed a positive correlation between age and diameter15. The data of the 2 age groups in this study (22–52 years old and 53–79 years old) did not differ substantially. Therefore, such a correlation could not be confirmed for the present population (Table 3). A case report described the intraoperative finding of a vessel of approximately 3 mm in diameter21. The present study detected a diameter of the VBC greater than 2 mm in 0.5% of the sites analyzed. To prevent peri- or postoperative complications, the ligation of unusually large VBCs was suggested. Although harming the intraosseous vascular anastomosis is not lifethreatening, it may influence the local bone healing and the vascularization of a possible graft material13. Regarding the frequency of the proximity between the VBC and the root apex lying within 4 mm (34.3%) as well as the prevalence of a VBC lying in a buccal position (pooled percentage 5 53.8%), the intraoperative appearance of the VBC may be expected during osteotomy and apicectomy by assessing the CBCT images preoperatively. In case of intraoperative perforation of the VBC, the hemorrhage can limit the surgeon’s sight11,22 and/or complicate establishing dry
conditions for the retrograde root canal filling. Furthermore, almost 3 of 4 VBCs were located as being inside the maxillary sinus (pooled percentage 5 74.3%). This finding contradicts recent studies11,14,19 but could be explained by focusing only on first molars in the present study. The frequent intrasinusal position may cause an intra- or postoperative complication during sinus floor elevation. When elevating the Schneiderian membrane from the sinus walls, the delicate border of the VBC, and thus the vascular anastomosis, can be harmed and result in bleeding. Impaired vision and an increased risk of membrane perforation can be possible consequences11,22. A local hematoma or, in case of a rupture of the Schneiderian membrane, a hematosinus are possible sequelae. Both situations entail the risk of a severe infection22 or treatment failure23. Therefore, knowledge of the local anatomy and adequate surgical planning is mandatory; 3-dimensional radiographic imaging using CBCT scans before the intervention might be beneficial.
CONCLUSIONS With regard to the findings of the present study, the following clinically relevant conclusions can be drawn and might help to
avoid damage to the VBC with subsequent hemorrhage during surgical interventions such as apical surgery in the posterior maxilla on the basis of an adequate assessment of CBCT images: 1. Distances between the VBC and its surrounding anatomic structures were generally shorter in women than in men. 2. The VBC was located closer to mesiobuccal roots than distobuccal roots of maxillary first molars. 3. During preparation of the access window, the existence of the VBC should be kept in mind because mesiobuccal roots of maxillary first molars often need apical surgery because of their complex root canal anatomy.
ACKNOWLEDGMENTS The authors thank Ms Bernadette Rawyler, Graphical Department of the School of Dental Medicine, University of Bern, Bern, Switzerland, for the graphic illustrations and Ms Kar Yan Li, Centralised Research Lab, Faculty of Dentistry, The University of Hong Kong, for her valuable assistance regarding the statistical analysis. The authors deny any conflicts of interest related to this study.
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Katranji A, Fotek P, Wang HL. Sinus augmentation complications: etiology and treatment. Implant Dent 2008;17:339–49.
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Proximity of Vascular Bone Channel in the Lateral Sinus Wall to Root Apices of Maxillary First Molars: A Cone-beam Computed Tomographic Analysis ABSTRACT Introduction: Apical surgery is frequently indicated in maxillary first molars. Occasionally, a vascular anastomosis in the lateral maxillary sinus wall can be observed during surgery. The aim of this study was to examine the distance between the vascular bone channel (VBC) and the root apices of maxillary first molars using cone-beam computed tomographic imaging. Methods: Cone-beam computed tomographic images of 104 maxillary first molars were oriented in the coronal plane to evaluate the distance between the roots and the VBC. The measurements were only recorded in relation to the buccal roots. In addition, demographic parameters and further measurements such as the diameter of the VBC and the proximity to the periapical pathology were evaluated. Results: A total of 210 VBCs were assessed. The mean distance from the VBC to the apices of the buccal roots of the maxillary first molars was 6.18 mm 6 3.84 mm. The VBC was mostly located intrasinusally (74.3%) and only rarely superficially (0.5%). The diameter of the VBC was on average 0.88 6 0.32 mm. Conclusions: In this study, the VBC was usually found closer to the mesiobuccal than to the distobuccal root apex. During preparation of the access window, the existence of the VBC should be kept in mind because the mesiobuccal roots of maxillary first molars undergo apical surgery to the buccally positioned roots only. (J Endod 2019;-:1–7.)
KEY WORDS
Frank M. Bischof, DMD,* Michael M. Bornstein, DMD,† Valerie G.A. Suter, DMD,* Ryan I.E. Lello, DMD,* and Thomas von Arx, DMD*
SIGNIFICANCE Distances between the VBC and its surrounding anatomic structures were generally shorter in females than in males, and the VBC was located closer to mesiobuccal roots than to distobuccal roots of maxillary first molars. During preparation of the access window, the existence of the VBC should be kept in mind because mesiobuccal roots of maxillary first molars often need apical surgery because of their complex root canal anatomy.
Apical surgery; cone-beam computed tomography; maxillary first molar; vascular bone channel
One of the signs of root canal treatment failure is the presence of microbial infection and, as an objectivized symptom, a fistula and/or the persistence of pain. Failures of root canal treatment can be categorized as anatomic (isthmus, apical ramifications, and accessory canals), iatrogenic (perforations and fractured instruments), pathological (pulp canal obliteration, cysts, and neoplasia), or technical (orthograde access blocked by a post and/or a crown). To preserve teeth with failing endodontic treatment, apical surgery is an established treatment option1. A frequent tooth to be treated with apical surgery is the first maxillary molar because of its complex root canal anatomy, in particular of the mesiobuccal root. An important issue to consider in apical surgery is the risk of potentially jeopardizing or injuring adjacent anatomic structures. The root apices of teeth in the posterior maxilla are located close to the floor of the maxillary sinus. The apex of the first premolar is the furthest from the sinus floor. Posteriorly, the distances constantly decrease until the mesiobuccal root of the second molar2. Because the surgical access and room for microsurgical instruments in the posterior maxilla are limited, knowledge about periapical bone dimensions is of interest3. Four branches of the maxillary artery perfuse the lateral maxillary sinus wall: the posterior superior alveolar artery (PSAA), the anterior superior alveolar artery, the descending palatine artery, and the infraorbital artery4. A cadaver study reported the existence of an extraosseous and an intraosseous
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From the *Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Bern, Bern, Switzerland; and † Oral and Maxillofacial Radiology, Applied Oral Sciences, Faculty of Dentistry, The University of Hong Kong, Prince Philip Dental Hospital, Sai Ying Pun, Hong Kong SAR, China Address requests for reprints to Dr Frank M. Bischof, Department of Oral Surgery and Stomatology, University of Bern, Freiburgstrasse 7, CH-3010, Bern, Switzerland. E-mail address: frank.bischof@zmk. unibe.ch 0099-2399/$ - see front matter Copyright © 2019 American Association of Endodontists. https://doi.org/10.1016/ j.joen.2019.09.004
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anastomosis between the PSAA and the anterior superior alveolar artery5. The intraosseous anastomosis, running inside a vascular bone channel (VBC), supplies the teeth and the periodontium in the posterior maxilla as well as the Schneiderian membrane lining the lateral sinus wall5. Surgical interventions such as apical surgery in the posterior maxilla or sinus floor elevation procedures can entail several risks, including the rupture of the Schneiderian membrane or damage to the VBC with subsequent hemorrhage6. The use of cone-beam computed tomographic (CBCT) imaging for diagnosis and treatment planning of apical surgery is becoming increasingly accepted as a standard imaging procedure because of its lower radiation dose and better resolution than conventional computed tomographic (CT) imaging7,8. CBCT imaging enables a better understanding of the root position and its surrounding anatomic structures compared with 2-dimensional radiography9. The primary objective of the present study was to examine the distance from the VBC to the root apices of maxillary first molars scheduled for apical surgery using CBCT imaging. Secondary outcomes included demographic parameters and additional measurements such as the diameter of the VBC, the relationship between the VBC and adjacent anatomic structures including the maxillary sinus floor and the buccal cortical wall, and the distance from the VBC to the apical radiolucency when present.
MATERIALS AND METHODS Patient Selection The CBCT images were selected from patients who underwent radiologic assessment of the maxillary sinus and posterior maxilla before apical surgery between March 2006 and May 2017. Patients were excluded from this study if they were younger than 18 years old or had a history of maxillary sinus trauma, surgery, or orthognathic intervention; patients with supernumerary teeth, impacted teeth, foreign bodies, previous apical surgery, artifacts hindering image interpretation, or root resorptions within the region of interest were also excluded. The local ethics committee approved the study protocol (KEK-BE 2018-00387).
Radiographic Assessment The CBCT images were all recorded with a 3D Accuitomo 80 or 170 unit (J Morita Corp, Kyoto, Japan). The exposure parameters were 5–7 mA and 80–90 kV, and the exposure time was 17.5 seconds with a full scan rotation (360 ). The field of view was chosen according to the indication and the diagnostic requirements but always following the “as low as diagnostically acceptable” principle10. The different field of views used included 40 ! 40 mm, 60 ! 60 mm, 80 ! 80 mm, or 100 ! 100 mm with corresponding voxel sizes between 0.08 mm and 0.25 mm, respectively. All measurements were made with the corresponding software (iDixel, version 2.0.4, J Morita Corp). A calibrated observer (F.B.), not involved in any surgery, performed the
measurements on a 19-inch Eizo Flexscan monitor with a resolution of 1280 ! 1024 pixels (Eizo Nanao AG, W€adenswil, Switzerland). To assess the intraobserver reliability, the measurements of 20 randomly selected (https://www.randomizer.org) cases were repeated after a washout period of 4 weeks. For an optimal depiction of the root apices and the VBC, the CBCT images were manipulated in all 3 anatomic planes. If roots were curved, the CBCT slice was oriented along the apical root portion. The study sites were examined in the coronal plane. The following parameters were analyzed in the mesiobuccal and distobuccal roots of maxillary first molars: A: the shortest distance between the VBC and the root apex (Fig. 1A and B) B: the largest diameter of the VBC (Fig. 1) C: the horizontal distance from the VBC to the lateral cortical wall (Fig. 1) D: the shortest distance from the VBC to the apical radiolucency (when present) (Fig. 1) E: the vertical distance from the lower border of the VBC to the floor of the maxillary sinus using a horizontal auxiliary line; when the VBC was located below the floor of the maxillary sinus, the value for the distance was negative (Fig. 1) F: assessment of the location of the VBC relative to the root apex (palatal, above, or buccal) (Fig. 2A–F) G: assessment of the location of the VBC within the lateral wall of the maxillary sinus (intrasinusal/intraosseous/superficial)11 (Fig. 2)
FIGURE 1 – (A ) A schematic illustration and (B ) CBCT image of the VBC (*) and its shortest distance to the root apex (A, 3.37 mm); its diameter (B, 1.38 mm); and its distance to the buccal bone wall (C, 5.87 mm), the apical radiolucency (D, 0.20 mm), and the maxillary sinus floor (E, 3.63 mm).
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FIGURE 2 – Locations of the VBC relative to the root apex were classified as (A ) palatal, (B ) above, or (C ) buccal. Locations relative to the lateral border of the maxillary sinus were classified as (D ) intrasinusal, (E ) intraosseous, or (F ) superficial. Additionally, the side (right/left) as well as patient-related data (age and sex) were evaluated.
Statistical Analysis All data were first analyzed using descriptive statistics. The detailed differences between mesiobuccal and distobuccal roots were then compared using paired t tests. If the differences between mesiobuccal and distobuccal roots were significant in at least 1 parameter, then separated analyses for each type of roots were performed with Bonferroni adjustment. The teeth were assumed as
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independent within the same person. Age was dichotomized by a median split, yielding 2 age groups for further statistical analysis. The effects of the binary independent variables (sex, side, and age) on the linear measurements were separately evaluated with 2-sample t tests. The effects of the binary independent variables (sex, side, and age) on VBC location were evaluated with the Pearson chi-square test (or the Fisher exact test if .20% of the cells had an expected count ,5). The significance level chosen for all statistical tests was set at P , .05. Statistical
procedures were all performed SPSS Version 25.0 (IBM Corp, Armonk, NY).
RESULTS This retrospective study evaluated 104 first maxillary molars resulting in 208 buccal roots with a nearly equal distribution of 48 women (46.2%) and 56 men (53.9%). The mean age of the patients was 52.7 years (median 5 52 years) with a range of 22–79 years. The VBC was identified in all 104 scans; however, it was only detected in 203 of 208 roots (97.6%) that met the inclusion criteria. In 5 coronal slice
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TABLE 1 - The Mean Distances between the Vascular Bone Channel (VBC) and the Measured Surrounding Anatomic Structures A–E at the Mesiobuccal (MB)/Distobuccal (DB) Roots and Pooled per Tooth in Millimeters MB
DB
P value
Pooled per tooth
6.02 6 3.75 (n 5 105) 0.88 6 0.29 (n 5 105) 1.38 6 1.16 (n 5 105) 4.46 6 3.70 (n 5 98) 5.95 6 4.12 (n 5 105)
6.34 6 3.95 (n 5 105) 0.89 6 0.36 (n 5 105) 1.51 6 1.00 (n 5 105) 5.06 6 3.79 (n 5 93) 6.88 6 4.02 (n 5 105)
.06 .80 .62 .00* .00*
6.18 6 3.84 (N 5 210) 0.88 6 0.32 (N 5 210) 1.44 6 1.08 (N 5 210) 4.75 6 3.75 (N 5 191) 6.41 6 4.08 (N 5 210)
Distances VBC to root apex (A) Diameter of VBC (B) VBC to lateral bone surface (C) VBC to apical radiolucency (D) VBC to maxillary sinus floor (E) Values are mean 6 standard deviation. *P , .05, significant difference.
images, the VBC could not be located because of its course through the apical radiolucency. Five individuals (4.81%) showed the presence of a bifid VBC. In 3 cases, the bifid VBC was identified either at the mesiobuccal or the distobuccal root, whereas in 2 cases it was found at both roots. Therefore, a total of 210 VBCs were analyzed. The repetition of the measurements in 20 cases for parameters A to G showed an excellent intraobserver reliability (intraclass correlation coefficient values between 0.980– 1.000 and all kappa values as 1.000). The mean distances between the VBC and its surrounding anatomic structures are listed in Table 1. The mean proximity of the VBC to the root apex (A) was 6.18 mm 6 3.84 mm (N 5 210). The VBC lay mostly within 4.01–10 mm (51%) to the root apex but also frequently occurred 4 mm or closer (34.3%). The mean diameter of the VBC (B) measured as 0.88 mm 6 0.32 mm (N 5 210) (Table 1). The frequency analysis showed that the diameter of the VBC was greater than 1 mm in 31.4% of the roots evaluated. The mean shortest distance to an apical radiolucency (D) was 4.75 mm 6 3.75 mm (n 5 191); 19 roots were not evaluated for category D because they had no periapical pathology. The mean distance between the VBC and the lateral bone surface (C) was 1.44 mm 6 1.08 mm (N 5 210), and the vertical distance between
the VBC and the floor of the maxillary sinus (E) was 6.41 mm 6 4.08 mm (N 5 210) on average. The VBC was mostly located buccally (53.8%) but was also found above (38.1%) or palatally (8.1%) in relation to the apices (F). Most frequently, the VBC was found intrasinusally (74.3%). Intraosseous (25.2%) and, rarely, superficial positions (0.5%) were also observed (G). The detailed differences between the mesiobuccal and distobuccal roots are presented in Table 1, and significant differences were found for VBC in relation to the apical radiolucency (D) and VBC to the maxillary sinus floor (E) (both P 5 .00). In general, women showed lower values for parameters A–E (Table 2) compared with men. Statistically significant differences were detected for diameter (B) in both mesiobuccal and distobuccal roots (P 5 .00) and for the distance from the VBC to the lateral bone surface (C) in distobuccal roots (P , .03). The distance between the VBC and the lateral cortical wall (C) was shorter in the older than in the younger age group (P , .02) in mesiobuccal roots. The distance between the VBC and the maxillary sinus floor (E), the distance from the VBC to the root apices (A), the diameter of the VBC (B), and the distance to periapical radiolucencies (D) were similar for both age groups (all P . .05) (Table 3). When comparing the right and left side, only minor
but not statistically significant differences were found (all P . .05). Sex significantly affected the distribution with regard to VBC location to the root apex (F). In mesiobuccal roots, the VBC was located in a buccal position more often in women than in men (P , .05) (Table 4). The side affected the distribution with regard to VBC location in relation to the lateral sinus wall (G), with the left side having a significantly higher rate of VBCs intrasinusally and a lower rate in intraosseous position than the right side (P 5 .02) in mesiobuccal roots (Table 4). For distobuccal roots, no significant different proportion distributions were found for VBC location with regard to the root apex (F) and lateral sinus wall (G) when assessed for the influencing factors of sex, age, and side.
DISCUSSION This radiographic analysis assessed the VBC in the lateral maxillary sinus wall and its relation to the buccal roots of the maxillary first molars using reoriented CBCT images. The VBC was present in 97.6% of the root apices, which is comparable with data from former cadaver studies that described a VBC in 100% of the root apices5,12,13. The discrepancy might be explained by the fact that the presence of a periapical lesion may inhibit the identification of a nearby VBC in CBCT images.
TABLE 2 - The Mean Distances between the Vascular Bone Channel (VBC) and the Measured Structures A–E Regarding Sex at the Mesiobuccal (MB)/Distobuccal (DB) Roots in Millimeters MB
VBC to root apex (A) Diameter of VBC (B) VBC to lateral bone surface (C) VBC to apical radiolucency (D) VBC to maxillary sinus floor (E)
DB
Female
Male
P value
Female
Male
P value
5.72 6 3.38 (n 5 49) 0.74 6 0.23 (n 5 49) 1.19 6 0.82 (n 5 49)
6.29 6 4.06 (n 5 56) 1.01 6 0.28 (n 5 56) 1.54 6 1.37 (n 5 56)
.88 .00* .24
6.16 6 3.48 (n 5 49) 0.74 6 0.25 (n 5 49) 1.25 6 0.82 (n 5 49)
6.50 6 4.34 (n 5 56) 1.02 6 0.39 (n 5 56) 1.73 6 1.10 (n 5 56)
1.00 .00* .03*
4.32 6 3.28 (n 5 46)
4.58 6 4.07 (n 5 52)
1.00
5.05 6 3.38 (n 5 43)
5.06 6 4.15 (n 5 50)
1.00
5.88 6 3.75 (n 5 49)
6.01 6 4.45 (n 5 56)
1.00
6.34 6 3.30 (n 5 49)
7.36 6 4.53 (n 5 56)
.39
Distances
Values are mean 6 standard deviation. *P , .05, significant difference.
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TABLE 3 - The Mean Distances between the Vascular Bone Channel (VBC) and the Measured Structures A–E Regarding Age at the Mesiobuccal (MB)/Distobuccal (DB) Roots in Millimeters MB Distances VBC to root apex (A) Diameter of VBC (B) VBC to lateral bone surface (C) VBC to apical radiolucency (D) VBC to maxillary sinus floor (E)
DB
22–52 years
53–79 years
P value
22–52 years
53–79 years
P value
6.07 6 3.58 (n 5 51) 0.90 6 0.31 (n 5 51) 1.69 6 1.47 (n 5 51)
5.98 6 3.93 (n 5 54) 0.86 6 0.27 (n 5 54) 1.08 6 0.64 (n 5 54)
1.00 .93 ,.02*
6.11 6 3.64 (n 5 53) 0.92 6 0.39 (n 5 53) 1.70 6 1.05 (n 5 53)
6.59 6 4.26 (n 5 52) 0.86 6 0.32 (n 5 52) 1.30 6 0.91 (n 5 52)
1.00 .88 .08
4.44 6 3.63 (n 5 46)
4.47 6 3.80 (n 5 52)
1.00
4.95 6 3.58 (n 5 47)
5.16 6 4.04 (n 5 46)
1.00
5.256 3.71 (n 5 51)
6.60 6 4.40 (n 5 54)
.19
6.34 6 3.59 (n 5 53)
7.44 6 4.37 (n 5 52)
.33
Values are mean 6 standard deviation. *P , .05, significant difference.
Nevertheless, CBCT imaging is an appropriate tool for the anatomic evaluation of bony structures as well as for planning of complex surgical interventions such as apical surgery. The mean shortest distance from the VBC to the root apex was 6.18 mm. This is in contrast to a previous study14 in which it was located a greater distance away (8.3 mm 6 3.3 mm). In the literature, a small number of CT studies15–17, 1 cadaver study5, and several CBCT studies11,14,18–20 assessed the topographic relationship between the VBC and the surrounding anatomic structures. However, only a few used a methodology
similar to the present study. When comparing the distance between the VBC and the maxillary sinus floor, the anatomic plane in which the images are analyzed is crucial. Only 2 CBCT studies with a comparable methodology were identified that assessed CBCT images in the coronal plane11,14. Kang et al14 analyzed 150 CBCTs of a Korean population. Generally, higher values were reported in their study (Table 5), and ethnicity might be a possible explanation for these differences. Another study examined 860 sinuses in 430 patients of a white population11. The detection rate of the VBC (anastomosis of
the PSAA) was 60.6%, which is substantially lower than in the present study (97.6%). The diameter (1.17 mm) and the distance to the sinus floor (8.09 mm) were greater than in the present study. The use of different CBCT machines and settings might be a possible explanation. Furthermore, Danesh-Sani et al11 do not mention where exactly the diameter of the VBC was measured. Regarding the diameter of the VBC, the findings in the present study (0.88 6 0.32 mm) were generally a little lower than the data described in previous studies that also evaluated reoriented CBCT images (Table 5).
TABLE 4 - The Location of the Vascular Bone Channel (VBC) in Relation to the Root Apex and the Lateral Sinus Wall in Mesiobuccal (MB) Roots MB Location Relative to root apex (F) Total Sex Female Male Age group 22–52 years 53–79 years Side Left side Right side Location Relative to lateral sinus wall (G) Total Sex Female Male Age group 22–52 years 53–79 years Side Left side Right side
P value
Palatal, %
Above, %
Buccal, %
9.5 (n 5 10)
47.6 (n 5 50)
42.9 (n 5 45)
4.1 (n 5 2) 14.3 (n 5 8)
38.8 (n 5 19) 55.4 (n 5 31)
57.1 (n 5 28) 30.4 (n 5 17)
.03*
13.7 (n 5 7) 5.6 (n 5 3)
47.1 (n 5 24) 48.1 (n 5 26)
39.2 (n 5 20) 46.3 (n 5 25)
.68
13.1 (n 5 8) 4.5 (n 5 2)
45.9 (n 5 28) 50.0 (n 5 22)
41.0 (n 5 25) 45.5 (n 5 20)
.67
P value
Inside, %
Central, %
Outside, %
65.7 (n 5 69)
33.3 (n 5 35)
1.0 (n 5 1)
59.2 (n 5 29) 71.4 (n 5 40)
40.8 (n 5 20) 26.8 (n 5 15)
0.0 (n 5 0) 1.8 (n 5 1)
.30†
68.6 (n 5 35) 63.0 (n 5 34)
29.4 (n 5 15) 37.0 (n 5 20)
2.0 (n 5 1) 0.0 (n 5 0)
.94†
75.4 (n 5 46) 52.3 (n 5 23)
23.0 (n 5 14) 47.7 (n 5 21)
1.6 (n 5 1) 0.0 (n 5 0)
.02*†
*P , .05, significant difference. † Fisher exact test.
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TABLE 5 - An Overview of Studies (in Chronologic Order) Assessing the Distance between the Vascular Bone Channel (VBC) and the Maxillary Sinus Floor (mm) and the Diameter of the VBC (mm)
Authors
Study material 19
Ilguy et al, 2013 Kang et al, 201314 Apostolakis et al, 201520 Danesh-Sani et al, 201711 Present study
135 patients 150 patients 156 patients 430 patients 104 patients
Methodology
Distance between VBC and sinus floor
Diameter of VBC
CBCT (coronal plane) CBCT (coronal plane)* CBCT (axial plane) CBCT (coronal plane) CBCT (coronal plane)
— 8.3 6 3.3 — 8.09 (0.43–30.90) 6.41 6 4.08
0.94 6 0.26 \ 1.07 6 0.43, _ 1.24 6 0.44 1.1 6 0.4 1.17 (0.4–2.8) 0.88 6 0.32 \ 0.74 6 0.25 _ 1.01 6 0.33
—, distance was not measured in this study. *Distances were measured at 6 different sites.
Different ethnicities and/or evaluation in a different plane could be possible reasons for this. An earlier CT study observed a positive correlation between age and diameter15. The data of the 2 age groups in this study (22–52 years old and 53–79 years old) did not differ substantially. Therefore, such a correlation could not be confirmed for the present population (Table 3). A case report described the intraoperative finding of a vessel of approximately 3 mm in diameter21. The present study detected a diameter of the VBC greater than 2 mm in 0.5% of the sites analyzed. To prevent peri- or postoperative complications, the ligation of unusually large VBCs was suggested. Although harming the intraosseous vascular anastomosis is not lifethreatening, it may influence the local bone healing and the vascularization of a possible graft material13. Regarding the frequency of the proximity between the VBC and the root apex lying within 4 mm (34.3%) as well as the prevalence of a VBC lying in a buccal position (pooled percentage 5 53.8%), the intraoperative appearance of the VBC may be expected during osteotomy and apicectomy by assessing the CBCT images preoperatively. In case of intraoperative perforation of the VBC, the hemorrhage can limit the surgeon’s sight11,22 and/or complicate establishing dry
conditions for the retrograde root canal filling. Furthermore, almost 3 of 4 VBCs were located as being inside the maxillary sinus (pooled percentage 5 74.3%). This finding contradicts recent studies11,14,19 but could be explained by focusing only on first molars in the present study. The frequent intrasinusal position may cause an intra- or postoperative complication during sinus floor elevation. When elevating the Schneiderian membrane from the sinus walls, the delicate border of the VBC, and thus the vascular anastomosis, can be harmed and result in bleeding. Impaired vision and an increased risk of membrane perforation can be possible consequences11,22. A local hematoma or, in case of a rupture of the Schneiderian membrane, a hematosinus are possible sequelae. Both situations entail the risk of a severe infection22 or treatment failure23. Therefore, knowledge of the local anatomy and adequate surgical planning is mandatory; 3-dimensional radiographic imaging using CBCT scans before the intervention might be beneficial.
CONCLUSIONS With regard to the findings of the present study, the following clinically relevant conclusions can be drawn and might help to
avoid damage to the VBC with subsequent hemorrhage during surgical interventions such as apical surgery in the posterior maxilla on the basis of an adequate assessment of CBCT images: 1. Distances between the VBC and its surrounding anatomic structures were generally shorter in women than in men. 2. The VBC was located closer to mesiobuccal roots than distobuccal roots of maxillary first molars. 3. During preparation of the access window, the existence of the VBC should be kept in mind because mesiobuccal roots of maxillary first molars often need apical surgery because of their complex root canal anatomy.
ACKNOWLEDGMENTS The authors thank Ms Bernadette Rawyler, Graphical Department of the School of Dental Medicine, University of Bern, Bern, Switzerland, for the graphic illustrations and Ms Kar Yan Li, Centralised Research Lab, Faculty of Dentistry, The University of Hong Kong, for her valuable assistance regarding the statistical analysis. The authors deny any conflicts of interest related to this study.
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Proximity of Vascular Bone Channel
7