DOI: https://doi.org/10.21203/rs.3.rs-2740603/v1
This study aimed to introduce a minimally invasive technique for maxillary sinus floor elevation using the lateral approach (lSFE) and to determine the factors that influence the stability of the grafted area in the sinus cavity. Thirty patients (30 implants) treated with lSFE using minimally invasive techniques from 2015 to 2019 were included in the study. Five aspects of the implant (central, mesial, distal, buccal, and palatal bone heights [BHs]) were measured using cone-beam computed tomography (CBCT) before implant surgery, immediately after surgery (T0), 6 months after surgery (T1), and at the last follow-up visit (T2). Patient characteristics were collected. A small bone window (height, 4.40 ± 0.74 mm; length, 6.26 ± 1.03 mm) was prepared. No implant failed during the follow-up period (3.67 ± 1.75 years). Three of the 30 implants exhibited perforations. Changes in BH, defined as the distance between the implant platform level and the uppermost level of bone graft, of the five aspects of implants showed strong correlations with each other and decreased dramatically before second-stage surgery. RBH did not significantly influence BH changes, whereas smoking status and type of bone graft material were potentially influential factors. During the 3-year observation period, lSFE with a minimally invasive technique demonstrated high implant survival and limited bone reduction in grafted area. In conclusion, patients who were nonsmoker and whose sinus cavity was filled with deproteinized bovine bone mineral (DBBM) had significantly limited bone resorption in grafted area.
Alveolar bone resorption and maxillary sinus expansion are common phenomena following tooth loss in the maxillary posterior region. Proper implant placement in this region is frequently full of challenges owing to the limited available bone height (BH)1–3. Maxillary sinus floor elevation with a lateral (lSFE) or transcrestal (tSFE) approach is adopted to elevate Schneiderian membrane and create sufficient BH for implants4–6. The clinical security and efficacy of tSFE and lSFE have already been demonstrated by plenty of studies7–9. As the most widely used and conventional technique, lSFE is conducted to prepare a bone window in the lateral sinus wall and lift its membrane for placement of the bone graft material and implant10. Compared with tSFE, although lSFE provides direct intraoperative vision and unrestricted instrument operation, it is more invasive, with longer surgical duration, and more postoperative morbidity11,12.
In order to overcome these drawbacks, the lSFE procedures are continuously modified. A conservative strategy with a less-invasive window design has lately been put forward by a couple of researchers. It has been demonstrated that lSFE with a small window is as clinically successful as that with a large window for achieving bone augmentation and implants survival13,14. During lSFE surgery with small bone window, opening the bone window and filling the graft materials require a shorter duration, and shorter surgery duration and smaller flap size can lead to less oedema and pain in patients14,15. Visual analog scales (VAS) diagrams were utilized to analyze patients’ post-surgical discomforts every 7 days after surgery, and patients with a small lateral bone window reported pain relief at 7, 14 and 30-day follow-up14. Moreover, the small bone window plays a critical role in managing and preventing intraoperative complications16. As the most frequent intraoperative complication, membrane perforation is closely related to a larger window area.
Not only can lSFE be performed as pre-implantation surgery (two-stage surgery), but implants can also be placed at the same time (one-stage surgery), if the primary stability can be achieved. A recent systematic review revealed that the 5-year implant survival rate ranged from 88.6–100%, with no significant differences between one- and two- stage surgeries17. Undoubtedly, compared with two-stage surgery, one-stage surgery can be treated as a less invasive, time-saving and cost-effective clinical option. Thus, a novel minimally invasive technique for lSFE that combines small bone access with simultaneous implant placement is proposed.
One possible focus of maxillary sinus floor elevation is the long-term stability of the bone grafts18. Autogenous bone is generally considered the gold standard graft material due to its superb osteoinductive, osteoconductive and osteogenic features19. However, a major concern is that autogenous bone grafts require donor site surgery and have a high and unpredictable resorption rate20–22. To overcome the drawbacks, different forms of biomaterials are proposed, including allogenic, xenogeneic, and synthetic bones. In particular, deproteinized bovine bone mineral (DBBM) is likely to be one of the most promising candidates, owing to its slow substitution rate, superior space maintenance capability and high osteoconductive properties23–25. A study has demonstrated that a composite of autogenous bone and DBBM achieved clinical success in peri-implant bone augmentation26–28. To assess the peri-implant bone augmentation, various imaging approaches have been utilized29. Lately, cone-beam computed tomography (CBCT) has been considered as a promising three-dimensional (3D) option in evaluating the extent of peri-implant bone augmentation surrounding the implant14,23,27,30. However, 3D analysis of the grafted area of lSFE with a small window and minimally invasive techniques for lSFE are scant and have short follow-up periods14,30,31. In the consistence of these studies, authors verified that the stability of implants and excellent osteogenic capacities were detected 6 months after small antrostomy surgery.
The primary objective of the present retrospective study was to meticulously introduce a minimally invasive technique for lSFE in terms of minimal lateral bone access and simultaneous implant placement. The long-term stability of the bone graft area was analyzed by circumferentially evaluating the peri-implant BH from CBCT images, furthermore, the potential influencing factors related to bone resorption in the maxillary sinus were investigated.
The schematic diagram of the retrospective study is shown in Fig. 1, and schematic diagram of radiographic assessment is shown in Fig. 2. The mean follow-up period was 44.36 months (SD = 21.31, ranging from 17 to 72). No significant complications were detected during follow-up. The participants’ characteristics are present in Table 1. Thirty participants (8 males and 22 females), average age 45.13 years (SD = 15.49, ranging from 18 to 70 years) who underwent maxillary sinus floor elevation using a minimally invasive technique were included in the study. Among the participants, 5 were smokers and 25 were non-smokers. Eleven participants had a history of periodontitis, and 19 did not. One participant was placed at 24, 5 participants were placed at 25, 24 participants were placed at 26, and 3 participants were placed at 27. The participants’ mean RBH was 3.39 (SD = 1.30), ranging from 1.13 to 6.24 mm. The vast majority of participants had ITI implants with an insertion torque of 35N∙cm. The mean LIPSC was 5.41 (SD = 1.43) and ranged from 1.66 to 8.50. Perforation of the Schneiderian membrane occurred in 3 patients (incidence, 10%). During overall follow-up period, none of the implants failed.
| Characteristics | |
|---|---|
| Male/Female | 8/22 |
| Mean age (years old) | 45.13 (15.49) |
| Smokers/Non-smokers | 5/25 |
| Number of patients with periodontitis/non-periodontitis | 11/19 |
| Number of patients with sinus membrane thickness of 1–2 mm/less than 1 mm | 11/19 |
| Implanting site of 24/25/26/27 | 1/5/24/3 |
| Mean RBH | 3.39 (1.30) |
| Implant system of ITI-BL/DENTIUM/Nobel | 27/2/1 |
| Implant diameter of 3.3 mm/4.1 mm/≥ 4.8 mm | 2/7/21 |
| Number of patients with implant length of 8 mm/10 mm | 18/12 |
| Initial stability of 15 N/20 N/25 N/30 N/35 N | 2/2/6/4/16 |
| Number of patients with bone meal brand of DBBM/β-TCP | 22/8 |
| Amount of bone meal of 0.25 g/0.50 g/0.75 g | 8/19/3 |
| Number of patients with collagen membrane/ without collagen membrane | 23/7 |
| Mean LIPSC | 5.41(1.43) |
| Number of patients with membrane perforation/without membrane perforation | 3/27 |
| Number of implants placed/lost | 30/0 |
| RBH, residual bone height; LIPSC, length of the implant protruding into the sinus cavity; β-TCP, β-tricalcium phosphate. | |
A small rectangular lateral bone access was prepared to elevate Schneiderian membrane (Fig. 3). The dimensions of lateral bone window prepared in the study were 4.40 ± 0.74 mm in height and 6.26 ± 1.03 mm in length (Fig. 4a).
All patients in the study were examined with radiation analysis of CBCT at T0 (immediately after implant surgery), T1 (before second-stage surgery) and T2 (at the last follow-up visit). Bone height (BH) was defined as the distance between the implant platform and the uppermost level of bone graft. BH was measured at five aspects of each implant: central (BHC), mesial (BHM), and distal (BHD), buccal (BHB), and palatal (BHP) aspects (Fig. 2). To analyze the stability of grafted area in the sinus cavity, BH changes from T0 to T1 (ΔBHT0−T1) and from T0 to T2 (ΔBH T0−T2) were performed.
As shown in Fig. 4 and Table 2, from T0 to T1, the changes in BH all showed a significant difference, whereas form T1 to T2, the BH was relatively stable. The vertical bone gain was 8.07 mm (SD = 1.63, ranging from 5.56 from 11.54 mm). Specifically, the mean BHCs were 11.46 ± 1.40 mm, and that was 10.9 ± 1.52 mm at T1. Thus, from T0 to T1, the mean BHC decreased significantly by 0.54 ±\(\text{ }\)0.97 mm (p < 0.01). Moreover, ΔBHMT0−T1, ΔBHDT0−T1, ΔBHBT0−T1, and ΔBHPT0−T1 significantly decreased to 0.64 ± 1.40 (p < 0.05), 0.55 ±\(\text{ }\)1.17 (p < 0.05), 0.22 ± 1.96 (p < 0.05), and 0.70 ± 0.92 mm (p < 0.01), respectively.
| Outcome | T0 | T1 | ΔBHT0−T1 | T0-T1 (p value) |
|---|---|---|---|---|
| BHC | 11.46 (1.40) | 10.92 (1.52) | -0.54 (0.97) | 0.00*** |
| BHM | 10.78 (1.43) | 10.14 (1.47) | -0.64 (1.40) | 0.01** |
| BHD | 11.30 (1.61) | 10.75 (1.92) | -0.55 (1.17) | 0.01** |
| BHB | 10.92 (2.50) | 10.70 (1.57) | -0.22 (1.96) | 0.01** |
| BHP | 10.82 (1.60) | 10.12 (1.51) | -0.70 (0.92) | 0.00*** |
| *** p < 0.01, ** p < 0.05. Standard deviations are in the parentheses; T0, immediately after bone grafting; T1, 6 months after implant surgery; ΔBHT0−T1 represents the bone height changes from T0-T1. Given the small sample, an alpha level of .1 was used as the cutoff for statistical significance. | ||||
The results of the Pearson correlation analysis showed that all the correlating coefficients of the BH changes were positive and statistically significant, indicating that significant correlations among ΔBHCT0−T1, ΔBHMT0−T1, ΔBHDT0−T1, ΔBHBT0−T1 and ΔBHPT0−T1 (Table 3).
| Outcome | ΔBHCT0−T1 | ΔBHMT0−T1 | ΔBHDT0−T1 | ΔBHBT0−T1 | ΔBHPT0−T1 |
|---|---|---|---|---|---|
| ΔBHCT0−T1 | 1.00 | ||||
| ΔBHMT0−T1 | 0.81*** | 1.00 | |||
| (0.00) | |||||
| ΔBHDT0−T1 | 0.78*** | 0.530*** | 1.00 | ||
| (0.00) | (0.00) | ||||
| ΔBHBT0−T1 | 0.86*** | 0.78*** | 0.70*** | 1.00 | |
| (0.00) | (0.00) | (0.00) | |||
| ΔBHPT0−T1 | 0.63*** | 0.60*** | 0.54*** | 0.70*** | 1.00 |
| (0.00) | (0.00) | (0.00) | (0.00) | ||
| *** p < .01; p values are in the parentheses. | |||||
Scatter plots with fitted value lines (Fig. 5) showed a linear relationship between pre-surgery RBH and ΔBHCT0−T1, ΔBHMT0−T1, ΔBHDT0−T1, ΔBHBT0−T1 and ΔBHPT0−T1. As Fig. 5 displayed, the trends of fitting value lines were relatively smooth, which indicates that no correlations were detected between the ΔBHT0−T1 of the five aspects and RBH (p > 0.05).
BH changes were compared among different groups according to patient characteristics. The ΔBHC T0−T1, ΔBHM T0−T1, ΔBHB T0−T1 and ΔBHP T0−T1 of the smoker group were significantly greater than those of the non-smoker group. Compared with the group that used DBBM, the β-TCP group showed significantly greater changes in ΔBHCT0−T1, ΔBHMT0−T1, ΔBHDT0−T1, ΔBHBT0−T1, and ΔBHPT0−T1 (Table 4).
| Characteristics | Mean bone height change (mm) | ||||
|---|---|---|---|---|---|
| ΔBHC T0−T | ΔBHM T0−T1 | ΔBHD T0−T1 | ΔBHB T0−T1 | ΔBHP T0−T1 | |
| Gender | |||||
| Male | -0.26 (0.76) | 0.04 (1.51) | -0.38 (0.78) | 0.20 (1.41) | -0.29 (0.86) |
| Female | -0.65 (1.03) | -0.88 (1.31) | -0.61 (1.30) | -0.83 (1.21) | -0.85 (0.91) |
| p value | 0.34 | 0.11 | 0.64 | 0.06* | 0.15 |
| Smoking | |||||
| Smoker | -1.22 (0.66) | -1.86 (1.31) | -1.30 (0.65) | -1.58 (1.11) | -1.80 (0.87) |
| Non-smoker | -0.41 (0.97) | -0.39 (1.30) | -0.40 (1.20) | -0.35 (1.28) | -0.48 (0.77) |
| p value | 0.09* | 0.03** | 0.12 | 0.06* | 0.00*** |
| Periodontitis | |||||
| With periodontitis | -0.58 (1.00) | -0.83 (1.49) | -0.64 (0.71) | -0.62 (1.75) | -0.69 (1.04) |
| Non-periodontitis | -0.52 (0.98) | -0.53 (1.37) | -0.50 (1.39) | -0.52 (1.05) | -0.70 (0.87) |
| p value | 0.86 | 0.58 | 0.75 | 0.84 | 0.96 |
| Sinus membrane thickness | |||||
| Less than 1 mm | -0.59 (0.98) | -0.83 (1.33) | -0.38 (1.32) | -0.48 (1.41) | -0.72 (0.98) |
| 1–2 mm | -0.46 (0.99) | -0.30 (1.52) | -0.84 (0.84) | -0.68 (1.21) | -0.66 (0.84) |
| p value | 0.72 | 0.32 | 0.31 | 0.70 | 0.88 |
| Residual bone height | |||||
| \(<\)4 mm | -0.70 (1.05) | -0.82 (1.47) | -0.60 (1.40) | -0.83 (1.24) | -0.78 (0.95) |
| \(\ge\)4 mm | -0.31 (0.81) | -0.36 (1.30) | -0.47 (0.74) | -0.14 (1.38) | -0.58 (0.89) |
| p value | 0.29 | 0.39 | 0.76 | 0.17 | 0.57 |
| Implant length | |||||
| 8 mm | -0.46 (0.99) | -0.48 (1.20) | -0.45 (1.38) | -0.65 (1.14) | -0.60 (0.84) |
| 10 mm | -0.66 (0.96) | -0.87 (1.69) | -0.70 (0.81) | -0.42 (1.60) | -0.85 (1.04) |
| p value | 0.59 | 0.47 | 0.58 | 0.65 | 0.48 |
| Type of bone graft material | |||||
| DBBM | -0.22 (0.83) | -0.17 (1.23) | -0.30 (1.13) | -0.20 (1.28) | -0.53 (0.86) |
| β-TCP | -1.42 (0.77) | -1.92 (1.00) | -1.24 (1.06) | -1.53 (0.91) | -1.17 (0.97) |
| p value | 0.00*** | 0.00*** | 0.05** | 0.01** | 0.08* |
| Collagen membrane | |||||
| With collagen membrane | -0.63 (0.98) | -0.64 (1.46) | -0.75 (0.94) | -0.60 (1.41) | -0.88 (0.97) |
| Without collagen membrane | -0.26 (0.95) | -0.63 (1.28) | 0.11 (1.65) | -0.40 (1.03) | -0.10 (0.29) |
| p value | 0.40 | 0.99 | 0.08* | 0.74 | 0.05** |
| Membrane perforation | |||||
| With membrane perforation | -0.98 (0.07) | -0.42 (0.15) | -0.64 (0.24) | -0.96 (0.66) | -1.11 (0.68) |
| Without membrane perforation | -0.49 (1.01) | -0.66 (1.47) | -0.54 (1.24) | -0.51 (1.38) | -0.65 (0.94) |
| p value | 0.42 | 0.78 | 0.89 | 0.58 | 0.43 |
| RBH, residual bone height; LIPSC, length of the implant protruding into the sinus cavity; β-TCP, β-tricalcium phosphate. * p < 0.1; Standard errors are in the parentheses. Standard deviations are in the parentheses. *** p < 0.01, ** p < 0.05, * p < 0.1. | |||||
Considering the effects of multiple factors on BH changes, linear mixed models were employed. The results in Table 5 estimated by the linear mixed model suggest that smoking had a higher possibility of decreasing BH, which was significantly different among ΔBHCT0−T1 (p < 0.1), ΔBHBT0−T1 (p < 0.1), and ΔBHPT0−T1. (p < 0.1). However, the effects of smoking in the changes of ΔBHMT0−T1 and ΔBHDT0−T1 were insignificant. Furthermore, the Bio-Oss bone graft material was significantly associated with ΔBHCT0−T1 (p < 0.1) and ΔBHBT0−T1 (p < 0.1). Overall, except for smoking and bone-filling material, no other factors were found to be significantly correlated with changes in BH.
| Variables | ΔBHCT0−T1 | ΔBHMT0−T1 | ΔBHDT0−T1 | ΔBHBT0−T1 | ΔBHPT0−T1 |
|---|---|---|---|---|---|
| Female as reference | |||||
| Gender | -0.61 | 0.59 | -0.96 | -0.55 | 0.62 |
| (0.45) | (0.91) | (0.76) | (0.54) | (0.60) | |
| Age | -0.03 | -0.03 | -0.03 | -0.02 | -0.03 |
| (0.02) | (0.04) | (0.04) | (0.03) | (0.03) | |
| Non-smoker as reference | |||||
| Smoking | -1.11* | -1.43 | -0.98 | -1.44* | -1.49* |
| (0.51) | (1.03) | (0.87) | (0.61) | (0.67) | |
| Non-periodontitis as reference | |||||
| Periodontitis | -0.46 | -1.67 | -0.47 | -0.76 | -0.47 |
| (0.49) | (0.99) | (0.83) | (0.58) | (0.65) | |
| 1–2 mm as reference | |||||
| Sinus membrane thickness less than 1mm | 0.18 | -0.23 | 0.55 | 0.48 | -0.87 |
| (0.49) | (0.99) | (0.83) | (0.58) | (0.64) | |
| Implanting site 24 as reference | |||||
| 25 | 0.78 | 0.00 | 1.81 | -2.40 | 1.85 |
| (1.24) | (2.51) | (2.10) | (1.48) | (1.64) | |
| 26 | 1.54 | 0.30 | 1.82 | -1.33 | 0.94 |
| (1.12) | (2.26) | (1.89) | (1.33) | (1.47) | |
| 27 | 0.98 | 0.88 | 1.01 | -1.47 | -0.62 |
| (1.27) | (2.56) | (2.14) | (1.51) | (1.67) | |
| RBH | 0.30 | 0.81 | -0.25 | 0.69 | -0.13 |
| (0.33) | (0.67) | (0.56) | (0.40) | (0.44) | |
| ITI implant as reference | |||||
| DENTIUM | 2.13 | 2.16 | 3.27 | 3.00* | 0.85 |
| (1.21) | (2.44) | (2.05) | (1.44) | (1.60) | |
| Nobel | 1.18 | -1.27 | 2.40 | 0.52 | 2.14 |
| (1.50) | (3.02) | (2.53) | (1.79) | (1.97) | |
| Implant diameter of 3.3mm as reference | |||||
| 4.1 diameter | 2.17* | 3.00 | 1.61 | 1.98 | 1.45 |
| (0.90) | (1.81) | (1.52) | (1.07) | (1.18) | |
| 4.8 diameter | 1.62 | 2.57 | 0.46 | 1.93 | 0.51 |
| (1.25) | (2.52) | (2.11) | (1.49) | (1.64) | |
| Initial stability of 15N as reference | |||||
| 20N | -2.12 | -0.04 | -1.34 | -1.34 | -1.43 |
| (1.09) | (2.21) | (1.85) | (1.31) | (1.44) | |
| 25N | 0.63 | 1.10 | 1.44 | 1.30 | 0.81 |
| (0.80) | (1.61) | (1.35) | (0.95) | (1.05) | |
| 30N | -1.28 | 0.04 | -1.41 | -0.62 | -0.79 |
| (0.89) | (1.80) | (1.51) | (1.06) | (1.18) | |
| 35N | -1.42 | 0.76 | -1.46 | -0.28 | -0.90 |
| Bone filling material of β-TCP as reference | (0.84) | (1.69) | (1.42) | (0.10) | (1.10) |
| Bio-Oss | 1.33* | 1.82 | 0.50 | 1.46* | 0.24 |
| (0.59) | (1.18) | (0.99) | (0.70) | (0.77) | |
| Bone graft of 0.25g as reference | |||||
| 0.5g | 0.50 | 0.43 | 0.93 | 0.78 | 0.06 |
| (0.57) | (1.15) | (0.96) | (0.68) | (0.75) | |
| 0.75g | 1.37 | -0.37 | 1.57 | 1.27 | 0.15 |
| (0.97) | (1.95) | (1.63) | (1.15) | (1.27) | |
| Without collagen membrane as reference | |||||
| With biomembrane | 0.21 | 0.07 | -0.10 | 0.46 | -1.24 |
| (0.52) | (1.06) | (0.89) | (0.62) | (0.69) | |
| Without membrane perforation as reference | |||||
| With membrane perforation | 0.67 | 0.82 | 0.84 | 0.70 | 0.32 |
| (0.62) | (1.25) | (1.04) | (0.74) | (0.81) | |
| LIPSC | -0.24 | 0.15 | -0.66 | -0.04 | -0.26 |
| (0.32) | (0.64) | (0.54) | (0.38) | (0.42) | |
| Constant | -2.50 | -7.13 | 2.43 | -3.90 | 2.83 |
| (4.51) | (9.09) | (7.62) | (5.37) | (5.94) | |
| R-squared | 0.92 | 0.85 | 0.85 | 0.94 | 0.85 |
| RBH, residual bone height; LIPSC, length of the implant protruding into the sinus cavity; β-TCP, β-tricalcium phosphate; LIPSC, length of the implant protruding into the sinus cavity. * p < 0.1; Standard errors are in the parentheses. | |||||
The primary objective of this study was to describe a novel minimally invasive technique featuring a small bone window access and one-stage surgery for lSFE with regard to implant survival rate, long-term stability of the grafted area, and potential influential factors. The clinical trial demonstrated that the minimally invasive technique was a reliable clinical procedure with a 100% implant survival rate during the entire follow-up period. The 3D stability of the bone graft in maxillary sinus was detected, the height of bone graft decreased rapidly during the first 6 months. Smoking and the type of bone graft were significant explanatory variable for RBH changes. There was no statistically significant correlation between RBH changes and preoperative RBH.
The lSFE technique was first introduced by Boyne and James using a large round burr to open a window at the lateral bone32. The size of the bone window remains a controversial issue. A wide flap and a large bone window were proposed to allow maximum accessibility and sufficient visualization of the surgical area, a wide flap and a large bone window were proposed33. The surface area of a large window is generally larger than 80 mm2 (10mm in length and 8mm in height), fabricated by piezoelectric devices or round burrs34–36. However, as a significant source of blood supply contributing to bone formation, the lateral bone is destroyed by a large bone window to a great extent. A number of studies have demonstrated that a large lateral window negatively influenced vascularization and bone formation in a grafted area30,37,38. A recent study by Zhu et al. also reached a similar conclusion that patients with a small bone window exhibited increased osteogenic potential, including higher mineral apposition rate, higher bone formation rate and larger new bone area39. The possible concerns of the small bone window were restricted visibility and limited access to lift the Schneiderian membrane and fill the bone graft. A study by Baldini and colleagues dispelled concerns14. Compared with large window group, preparing a small bone window and performing sinus filling took a shorter time. Membrane elevation in the small window group could be performed as quickly as in the large-window group. This indicates that a small bone window can provide surgeons with adequate accessibility and visualization. According to studies providing data on the dimensions of a small bone window, a length of approximately 6–8 mm and a height of 4–6 mm have been reported14,16,30,39−41. Generally, the surface area of a small lateral bone window is less than 40 mm2. The area of the small bone window prepared in this study was approximately 27 mm2, which is consistent with the results of previous studies.
Perforation of the Schneiderian membrane is the most frequent intraoperative complication of an lSFE. The reported incidence rate ranges from 10–60%42. Of 30 patients, three suffered from membrane perforation, in accordance with the literatures. Al-Dajani and colleagues systematically reviewed the incidence of membrane perforations in patients with lSFE. In this review, 12 studies and 388 membrane perforations were included43. The incidence of membrane perforation ranges from 3.6–41.8%, leading to a weighted prevalence of 23.5%. Whether membrane perforation influences implant survival remains under discussion. Hernandez-Alfaro and colleagues verified that membrane perforation size has a negative effect on implant survival rate44. When the perforation size was larger than 5mm, bioabsorbable membranes were utilized to repair the perforation, probably resulting in decreased bone formation and implant failure45. However, with the development of surgical equipment and techniques, large membrane perforations do not usually occur. A up to 20-year retrospective study showed that membrane perforation was unlikely to influence implant survival when patients with membrane perforation were treated properly and carefully46.
Initial RBH was considered a predictive indicator for the clinical option of one- and two-stage surgeries for maxillary sinus elevation. When the RBH is 5 mm or less, the lSFE is usually preferred. In particular, two-stage surgery is recommended in cases with RBH < 4 mm47,48. With innovations in surgical equipment and technology, the indications for lSFE with one-stage surgery have expanded. lSFE with one-stage surgery was treated as a feasible and reliable clinical option, even with RBH < 4 mm. A previous animal study was conducted to provide evidence that implant sites with 2 mm RBH showed similar stability as implants with 8 mmm RBH at the time of implant placement49. Stacchi et al., in a histomorphometric study, pointed out that a sufficient degree of newly formed bone tissue could be recognized regardless of RBH50. According to the observation at the 6-month follow-up, the study also verified that implant survival was not significantly influenced by RBH. A comparative evaluation was conducted to demonstrate that simultaneous implant placement could be accomplished at the site with RBH < 5 mm. During the 5-year observation period, the survival rate did not show significant differences between the two RBH groups (< 5 and > 5 mm)51. Peleg et al., suggested that under the premise of meticulous surgical planning and skills, implants could be simultaneously placed in sites with at least 1 mm of RBH, resulting in an extraordinarily high survival rate within an observation period of 9 years52. A long-term retrospective research by Han and the colleagues investigated the 10 and 20-year cumulative survival rates of implants placed simultaneously with lSFE, and they did not observe significant differences in the survival rates of implants placed in different RBHs during the 10-year period, but the survival rate was markedly lower for implants placed in < 3 mm RBH than for those placed in ≥ 3 mm RBH at 20 years46. Yet it is worth noting that the 20-year survival rate for implants placed in < 3 mm RBH was 78.8%, which was considered acceptable by the researchers.
The strong correlation between smoking status and BH changes in lSFE performed using a minimally invasive technique was demonstrated in the present study. Currently, several studies are available to confirm this finding. Schwartz-Arad et al., suggested that peri-implant BH showed greater resorption in smokers53. Guan and the colleagues in a clinical retrospective study, showed that smokers had bone loss of 0.7 mm compared with non-smokers54. This study adopted a linear mixed model to describe smoking status as a potential influencing factor associated with bone graft resorption in the sinus cavity. More air pressure was placed in the maxillary sinus of smokers, leading to great resorption of the bone graft and a decrease in its height. The peri-implant microbiome, related to osseointegration, can also be affected by nicotine55. These were possible reasons why smoking status was the key factor in bone graft resorption. However, based on the retrospective radiographic research carried out by Geurs et al., although a greater change in graft height was found in the smoking group at the 3-year follow-up, there was no statistical significance between the smoking and nonsmoking groups56. Trombelli and the colleagues also confirmed that smoking had a limited impact on radiographic outcomes 6 months after maxillary sinus elevation57. These two studies performed ANOVA and U-test and found no significant differences in mean graft change between smokers and nonsmokers56,57. However, the above results ignored the other possible factors that may influence the mean graft changes, such as sex, age, and especially the type of bone graft, which might produce estimation errors to a large extent. In this study, we considered the factors that may affect the mean graft changes as much as possible and used mixed linear regression to explore the possible risk factors for graft height changes.
In order to exactly understand the results of the present study, the limitations are as follows. First, it is a retrospective study with a small sample size, which probably caused inherent bias in the results. There was no control group to compare patients with lSFE with a large bone window or tSFE. Thus, a prospective study or randomized controlled study with a larger sample size is preferred. Second, although a 3D analysis device (CBCT) was employed to determine the stability of the grafted area, the volume of bone gain was not directly analyzed. Instead of volumetric analysis, the BH of the peri-implant was measured circumferentially; notwithstanding, previous studies have suggested that this is a reliable option of measuring bone gain in the sinus cavity30,54,58. Third, the 2-year observation period was relatively short, despite this being the longest follow-up period in the study of lSFE with small bone window. Further clinical trials with longer follow-up periods are warranted.
Thirty patients, who underwent lSFE with minimally invasive technique from May 2015 to November 2019 at West China Hospital of Stomatology, Sichuan University were included in the study. The study was followed strengthening the reporting of the observational studies in epidemiology (STROBE) guidelines. The clinical trial was performed to fully conform to the World Medical Association Declaration of Helsinki59. Ethics Committee of West China Hospital of Stomatology, Sichuan University approved the research procedures (WCHSIRB-CT-2022-452). All patients were informed of the clinical study procedure and signed the informed consent.
1. Patients older than 18 years old.
2. Patients who signed informed consent.
3. Patients who underwent lSFE with minimally invasive technique (small lateral window and simultaneous placement of single implant).
4. Patients in good health without contraindications to implant surgery.
1. Pregnant and lactating patients.
2. Patients with active maxillary acute sinusitis or diseases affecting wound healing and osteogenesis.
3. Patients taking immunosuppressive drugs.
4. Patients with a history of neck or head radiotherapy.
5. Patients with bruxism.
The features of patients were collected including (a) sex, (b) age, (c) smoking status, (d) history of periodontitis, (e) sinus membrane thickness, (f) implant sites, (g) pre-surgery residual bone height (RBH), (h) implant system, (i) implant diameter, (j) implant length, (k) initial stability of implants, (l) type of bone graft materials, (m) quantity of bone graft, (n) presence of collagen membrane, (o) length of the implant protruding into the sinus cavity (LIPSC), (p) presence of membrane perforation and (q) the number of lost implants.
All surgical procedures were conducted by the same experienced surgeon (X.C., Figure 6). At the beginning of surgery, local anesthesia (primacaine) was administered to the maxillary posterior area. Following crestal and vertical incisions, the mucoperiosteal flap was fully raised to explore the lateral bone of the maxillary sinus. A small rectangular lateral bone window was opened, and the Schneiderian membrane was carefully detached from the sinus floor using a DASK kit (Dentium, Seoul, South Korea). The height and length of the bone window were measured using a periodontal probe. Simultaneously, the implants were placed. The initial stability of the implants was guaranteed in all cases. After implantation, the space between the Schneiderian membrane and the sinus floor was filled with a mixture of autogenous bone and DBBM (Bio-Oss; Geistlich Pharma, Wolhusen, Switzerland) or β-tricalcium phosphate (β-TCP; RTR, Haibo Han, China). A resorbable collagen membrane (Bio-Gide, Geistlich Pharma, Switzerland) was utilized to cover the bone window and implant sites. Mucosal flaps were sutured with 5-0 non-absorbable polypropylene sutures (Prolene; Johnson & Johnson, USA).
Postoperatively, amoxicillin and metronidazole were prescribed three times daily for 7 days. All patients were asked to use a chlorhexidine mouthwash three times a day for 2 weeks. All sutures were removed within 10 to 14 days after surgery.
Six months after surgery, second-stage surgery was performed to replace the closure caps with healing abutments. The final prostheses of the single-ceramic crowns were fabricated. Patients underwent follow-up assessment every 6 months.
All patients in the study were examined with radiation analysis of CBCT (of slice thickness, 0.25 mm) before implant surgery, immediately after implant surgery (T0), 6 months after implant surgery (before second-stage surgery, T1) and at the last follow-up visit (T2). RBH was measured using CBCT images before implant surgery. The distance between the implant platform and the uppermost level of bone graft was defined as BH. BH was measured at five aspects of each implant at T0, T1 and T2: central (BHC), mesial (BHM), and distal (BHD), buccal (BHB), and palatal (BHP) aspects. BHC measurements were made along the central axis of the implant, and BHM, BHD, BHB and BHP analyses were performed along the axis and tangential to each side of the implant, respectively26,30. Radiographic bone gain was calculated by the subtracting BHCT0 and RBH. To analyze the stability of grafted area in the sinus cavity, BH changes from T0 to T1 (ΔBHT0-T1) and from T0 to T2 (ΔBH T0-T2) were used.
All data analyses were performed using Stata software (StataCorp, College Station, TX, USA). All measurement variables were showed as mean ± standard deviation (SD). Significant differences in BH at T0 and T1 and BH at T1 and T2 were assessed by one-way repeated-measures analysis of variance (ANOVA). Pearson correlation analysis was included in the present study to determine any relationships among ΔCBH T0-T1, ΔMBH T0-T1, ΔDBH T0-T1, ΔBBH T0-T1 and ΔPBH T0-T1. The comparison of mean BH changes based on patient characteristics were analyzed using a paired t-test. Multivariate linear regression analysis was used to determine the possible relationship between RBH and ΔBH1. A linear mixed model was adopted to determine the risk factors for ΔBH1. p-values <0.1 were considered statistically significant.
lSFE with a small lateral bone window and one-stage surgery has a 100% implant survival rate, limited bone graft resorption, and few influential factors during the 4-year observation period. The present study revealed a strong negative correlation between changes in BH and smoking status, and no influence of RBH was detected. Autogenous bone mixed with DBBM was again demonstrated one of the most promising candidates for bone graft filling of the sinus cavity.
Data availability statement: Data available within the article or its supplementary materials.
Acknowledgements: This study was supported by National Natural Science Foundation of China (81970986, 81771125).
Conflict of interests: There are no conflicts of interest to declare.
Contributions: X. Cai and S. Gao conceived this project. X. Cai performed all surgery procedures. S. Gao, Y. Jiang, and Y. Yao designed the project and collected the data. S. Gao and Y. Jiang analyzed the data and wrote the manuscript. S. Li provided help during data collection. X. Cai and Y. Jiang provided writing assistance and helped during proof-reading of the article.
Ethics approval statement: The respective study was performed in accordance with the World Medical Association Declaration of Helsinki.
Patient consent statement: All patients were informed of the clinical trial procedure and provided written informed consent.