Dogan Kaner Han Zhao Hendrik Terheyden Anton Friedmann
Authors’ affiliations: Dogan Kaner, Han Zhao, Anton Friedmann, Department of Periodontology, University of Witten/Herdecke, Witten, Germany Hendrik Terheyden, Department of Maxillofacial Surgery, Rotes Kreuz Krankenhaus Kassel, Kassel, Germany
Improvement of microcirculation and wound healing in vertical ridge augmentation after pre-treatment with self-inflating soft tissue expanders – a randomized study in dogs
Key words: bone augmentation, Laser Doppler flowmetry, microcirculation, soft tissue
expansion Abstract Objectives: We investigated the effect of soft tissue expansion (STE) on vertical ridge augmentation with regard to the incidence of wound dehiscences and the impairment of
Corresponding author: Dr Dogan Kaner Department of Periodontology Dental School, Faculty of Health University of Witten/Herdecke Alfred-Herrhausen-Str. 45, 58448 Witten Germany Tel.: +49 2302 926 656 Fax: +49 2302 926 661 e-mail: [email protected]
microcirculation in dogs, and the applicability of laser Doppler flowmetry (LDF) to explore the relation between microcirculation and wound healing. Material and methods: Bone defects were created on both mandibular sides in ten beagle dogs by extraction of premolars and removal of bone. Six weeks later, self-filling tissue expanders were implanted in randomly assigned test sites. After 5 weeks of expansion, vertical augmentation was carried out in test and control sites using calvarial onlay grafts side by side with granular biphasic calcium phosphate covered with a resorbable polyethylene glycol membrane. Microcirculation was evaluated with laser Doppler flowmetry (LDF). The incidence of wound dehiscences was evaluated after 2 weeks. The validity of LDF to predict dehiscences was evaluated by construction of receiver operating characteristic (ROC) curves. Results: After augmentation, test sites showed significantly better perfusion than control sites without preceding STE (P = 0.012). Three days after surgery, perfusion was still significantly decreased in control sites (P = 0.005), while microcirculation in test sites had returned to presurgical levels. After 2 weeks, healing in test sites was good, whereas eight dehiscences were found in control sites (P = 0.002). ROC curves showed that microcirculation levels immediately after augmentation surgery significantly predicted subsequent wound dehiscences (AUC = 0.799, CI 0.642–0.955, P = 0.006). Conclusions: Laser Doppler flowmetry is suitable for evaluation of soft tissue microcirculation after ridge augmentation. STE reduced the impairment of microcirculation caused by vertical ridge augmentation and decreased the incidence of wound dehiscences in the investigated animal model.
Date: Accepted 22 February 2014 To cite this article: Kaner D, Zhao H, Terheyden H, Friedmann A. Improvement of microcirculation and wound healing in vertical ridge augmentation after pre-treatment with self-inflating soft tissue expanders – a randomized study in dogs. Clin. Oral Impl. Res. 26, 2015, 720–724 doi: 10.1111/clr.12377
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Wound dehiscences and subsequent exposures of bone grafts are a common complication of complex augmentation procedures and occur in approximately 20% of cases (Jensen & Terheyden 2009; Kaner & Friedmann 2011). Dehiscences are attributed to difficulties in achieving tension-free primary wound closure and remaining high tension forces on the flap (Lundgren et al. 2008; Burkhardt & Lang 2010). When compared to straightforward surgical procedures, primary closure after complex augmentation necessitates extensive advancement of the flap by placement of releasing incisions into the
periosteum and submucosa. Generally, the elevation of a flap disturbs perfusion and causes ischaemia (McLean et al. 1995), while preservation of sufficient blood flow is important for tissue survival (Nakayama et al. 1982). Conversely, massive reduction of blood supply and subsequent ischaemia-reperfusion injury may affect the operated tissue and may cause complications such as necrosis of the flap (Carroll & Esclamado 2000). These negative effects from surgical trauma may impair wound healing after implantation of biomaterials or grafts and may further cause complications of bone grafting
© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
Kaner et al Soft tissue expanders and vertical augmentation
procedures, that is, post-surgical wound dehiscence and subsequent exposure of bone grafts despite proper execution of surgery and satisfactory initial primary closure (Kaner & Friedmann 2011). Generation of additional soft tissue before reconstructive surgery using subcutaneous tissue expanders to increase tissue quantity and quality for ease of primary closure and reduction of tissue traumatization is an established method in plastic surgery. Soft tissue expansion (STE) using self-filling osmotic hydrogel expanders prior to complex ridge augmentation surgery using autogenous bone grafts has been applied in two case series and one randomized study in humans, and resulted in high gain of regenerated bone, only minimal resorption of newly gained bone and a comparatively very low incidence of wound dehiscences (Kaner & Friedmann 2011; Abrahamsson et al. 2012; Mertens et al. 2013). However, the effects of STE on disturbance of microcirculation after augmentation surgery and the relation of microcirculation to soft tissue healing have not been investigated. Laser Doppler flowmetry has been used for evaluation of microcirculation after periodontal surgery and after implantation of tissue expanders (Donos et al. 2005; Kaner et al. 2013). However, LDF has not been applied for assessment of microcirculation after bone augmentation. The aims of our study were to explore the applicability of LDF for evaluation of microcirculation after augmentation surgery and to assess the effect of STE on microcirculation and soft tissue healing after vertical ridge augmentation in dogs.
Material and methods The study protocol was approved by the Food Safety and Animal Health Protection Board of the Regional Council of Pest, Hungary. The study was conducted at the Research Institute for Animal Breeding and Nutrition, Herceghalom, Hungary. Ten male beagle dogs (mean age 8.1 0.9 months, mean weight 12.2 1.3 kg) were used for the study. All surgeries and measurements were performed in general anaesthesia using intravenous injections of ketamin hydrochloride (2.5 ml/10 kg, Ketavet 10%; Pfizer, Berlin, Germany) and xylazine hydrochloride (1 ml/10 kg, Xylavet 2%; Sanofi-Aventis, Budapest, Hungary) every 15 min. Metamizole (1 ml/10 kg, Algopyrin; SanofiAventis) was injected intramuscularly after
surgeries and continued for 3 days for pain control. A single intramuscular injection of amoxicillin hydrochloride solution (150 mg, 1 ml/10 kg; Pfizer) was administered after surgeries for prevention of infections. Surgery Bone defects and implantation of tissue expanders
The creation of bone defects and implantation of tissue expanders have been described previously in detail (Kaner et al. 2013). After extraction of all mandibular premolars, the residual bone at the lingual side was reduced by 5 mm, while the buccal bone was additionally reduced to the bottom of the sockets of the extracted teeth in order to mimic a chronic severe vertical and horizontal bone defect. Six weeks after creation of bone defects, self-filling osmotic tissue expanders (cylinder type, final volume 0.7 ml; Osmed, Ilmenau, Germany) were implanted in randomly assigned sides of the mandible (test sites) into a submucosal pouch prepared without elevation of the periosteum. Augmentation surgery
After 5 weeks of expansion, ridge augmentation was carried out at test sites and at contralateral control sites after standardized doses of local anaesthesia (2 9 0.5 ml each buccally and lingually; articaine 4% with epinephrine 1 : 100,000; UDS forte, SanofiAventis, Frankfurt, Germany). At test sites with preceding STE, a midcrestal incision was placed above the tissue expander and extended into the sulci of the canine and the first molar for ease of reflection, but without vertical releasing incisions. The tissue expander was removed, the periosteum was cut in mesio-distal direction to expose the underlying bone, and buccal and lingual flaps were elevated. At control sites without preceding STE, a midcrestal incision was placed and extended
(a)
into the sulci of the adjacent teeth. Vertical releasing incisions were placed buccally at the mesial line angle of the canine and the distal line angle of the first molar and extended into the mucosa. The recipient bone was perforated with a small bur, and the ridge was augmented with a screw-fixated cortical bone graft harvested from the calvaria with a diamond saw and with granular biphasic calcium phosphate (BCP, Bone Ceramic; Institut Straumann AG, Basel, Switzerland) covered with a resorbable polyethylene glycol membrane (PEG; MembraGel, Institut Straumann AG). The grafts were placed side by side, but separated by at least 3 mm (Fig. 1a,b), after the positions (mesial/distal) of the grafts had been randomly assigned by flip of a coin. At test sites, primary closure was achieved without additional advancement of the flaps. At control sites, the flaps were advanced by placement of vertical releasing incisions and incisions into periosteum and submucosa until the flaps passively covered the augmented area, as generally recommended (Greenstein et al. 2009). Then, the flaps were approximated with vertical mattress sutures (Vicryl 3.0; Ethicon, Norderstedt, Germany), and the incision was closed with a continuous suture using fine resorbable monofilament sutures (Monocryl 6.0; Ethicon). Evaluation of soft tissue healing and microcirculation
The primary outcome, soft tissue dehiscences over the grafted areas, was assessed dichotomously (yes/no) 2 weeks after augmentation surgery. A laser Doppler flowmeter (Periflux 5010; Perimed AB, Jarfalla, Sweden) equipped with a PF 416 probe (outside diameter 1.0 mm, fibre separation 0.25 mm; wavelength 780 nm) was used for assessment of microcirculation. The flowmeter recordings were measured in perfusion units (PU) and moni-
(b)
Fig. 1. (a,b) Resorbed ridge augmented with BCP and PEG membrane (left) and calvarial onlay graft (right).
© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd
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Kaner et al Soft tissue expanders and vertical augmentation
tored using the Perisoft software (Perisoft 2.10; Perimed). Microcirculation was assessed at augmentation surgery before local anaesthesia (baseline), 2 min after local anaesthesia (T1), directly after termination of augmentation surgery (T2) and after 3 days (T3). A customized acrylic stent was fixed with silicone impression material at the adjacent teeth to facilitate standardized reproducible measurements, as reported previously (Kaner et al. 2013). The LDF probe was aligned at the stent, and 1-min measurements were always performed at the same two positions per flap, perpendicular to the tissue and at a distance of 0.5 mm to the flap. All measurements were carried out by the same calibrated investigator (H.Z.). Statistical analysis
Averages of the 1-min LDF measurements were calculated with the Perisoft software. Changes of blood flow in relation to the baseline values were calculated, and statistical analysis was carried out per protocol using a statistics software (SPSS 19.0; SPSS Inc., Chicago, IL, USA). Nonparametric tests were used for comparisons between test and control sites (Mann–Whitney U-test and Fisher’ exact test) and the various time points (Wilcoxon’s signed-rank test). The validity of LDF measurements to predict the occurrence of wound dehiscences was evaluated by construction of receiver operating characteristic (ROC) curves. P < 0.05 was considered significant.
Results Ten tissue expanders were implanted at test sites. Surgery and initial healing were uneventful and free of complications. Until augmentation surgery (baseline, 5 weeks after implantation of tissue expanders), three expanders were lost. The statistical analysis was carried out per protocol; hence, these sites were excluded. Soft tissue healing
Two weeks after grafting, no wound dehiscence was found in test sites, whereas eight wound dehiscences were noted in the control group (Fig. 2a,b; Table 1, significant difference favouring the test group, P = 0.002, Fisher’s exact test).
(a)
(b)
Fig. 2. (a) Control site with dehiscence 2 weeks after augmentation surgery: exposure of bone block graft (left) and loss of BCP + PEG membrane (right). (b) STE test site 2 weeks after surgery: closed flap and good soft tissue healing.
Table 1. Contingency table for wound dehiscences noted 2 weeks after augmentation surgery. Significant difference favouring the test group (Fisher’s exact test, P = 0.002) Exposition No exposition
Test group
Control group
0 7
8 2
(T1), blood flow changed significantly in test sites by 6.1 PU (median, Q1 11.9, Q3 3.5, P = 0.001) and, similarly (no significant difference between groups), in control sites by 5.1 PU (Q1 10.7, Q3 1.4, P = 0.001). From T1 to conclusion of augmentation surgery (T2), perfusion decreased significantly further in control sites to 11.4 PU (Q1 15.8, Q3 7.0, P < 0.001), whereas perfusion in test sites remained unchanged ( 5.8 PU, Q1 13.0, Q3 0.9, P > 0.05) with the result of significantly better microcirculation in the test group at T2 (P = 0.012). From T2 to T3 (3 days after augmentation surgery), no significant change was noted in test sites, while perfusion increased significantly in control sites ( 4.3 PU, Q1 11.8, Q3 0.5, P = 0.001). However – in contrast to test sites – microcirculation measurements at control sites were still significantly lower at T3, when compared to baseline (P = 0.005). Prediction of soft tissue dehiscence
Receiver operating characteristic curves for microcirculation measurements taken at
baseline, T1 (after local anaesthesia), T2 (after augmentation surgery) and T3 (3 days after augmentation surgery) as predictors of subsequent wound dehiscences are shown in Fig. 3a,b. Perfusion values at baseline, T1 and T3, respectively, did not predict a subsequent wound dehiscence (Fig. 3a). However, perfusion measurements taken directly after augmentation surgery (T2) were able to significantly predict a subsequent wound dehiscence (Fig. 3b. AUC = 0.799, P = 0.003, 95% confidence interval (CI) 0.642–0.955).
Discussion The aim of our randomized split-mouth study in dogs was to investigate the effects of soft tissue expansion (STE) on healing and microcirculation after vertical ridge augmentation. In contrast to the low rate of expander losses (9%) in our preceding case series in humans (Kaner & Friedmann 2011), 3 of 10 expanders (30%) were lost during the 5-week expansion phase. Mechanical irritation of the expansion area can lead to loss of tissue expanders (Mertens et al. 2013). Although the teeth opposite to the surgical sites had been removed prior to the implantation of tissue expanders, the comparatively high rate of expander losses may be attributed to continued uncontrolled mastication on the surgical sites.
Table 2. Time course of microcirculation changes expressed as difference in perfusion units (PU) from baseline (medians and interquartiles) Baseline (before local anaesthesia) Test Control
0 0
T1 (after local anaesthesia) 6.1 ( 11.9; 5.1 ( 10.7;
T2 (after bone augmentation) 3.5)a 1.4)a
5.8 ( 13.0; 11.4 ( 15.8;
T3 (3 days after surgery) 0.9)b,g 7.0)c,e,g
5.9 ( 12.3; 4.3) 4.3 ( 11.8; 0.5)d,f
Significantly different from baseline (Wilcoxon signed-rank test, P = 0.001). Significantly different from baseline (Wilcoxon signed-rank test, P = 0.006). Significantly different from baseline (Wilcoxon signed-rank test, P < 0.001). d Significantly different from baseline (Wilcoxon signed-rank test, P = 0.005). e Significantly different from T1 (Wilcoxon signed-rank test, P = 0.005). f Significantly different from T2 (Wilcoxon signed-rank test, P = 0.001). g Significant difference between test and control group (Mann–Whitney U-test, P = 0.012). a
b c
Microcirculation
Test and control sites showed similar microcirculation measurements at baseline (Table 2). After application of local anaesthesia
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© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd
Kaner et al Soft tissue expanders and vertical augmentation
(a)
(b)
Fig. 3. (a) ROC curves for the ability of LDF measurements at baseline (BL), T1 and T3 to predict a subsequent wound dehiscence and graft exposure. BL: AUC = 0.601, CI 0.405–0.796; P = 0.317. T1: AUC = 0.420, CI 0.218– 0.622; P = 0.427. T3: AUC = 0.550, CI 0.351–0.750; P = 0.617. (b) ROC curve for the ability of LDF measurements at T2 to predict a subsequent wound dehiscence and graft exposure. AUC = 0.799, CI 0.642–0.955; P = 0.003.
Two weeks after bone augmentation, no dehiscences were found in test sites with preceding STE, whereas eight dehiscences with exposure of bone grafts were noted in control sites. Generally, the occurrence of wound dehiscences is attributed to difficulties in achieving tension-free primary closure of the flap (Lundgren et al. 2008). Concordantly, a clinical study demonstrated that wound closure was maintained during healing, when minimal or no force was needed for suturing of the flap after augmentation. In contrast, patients with higher flap tension forces showed dehiscences in 40–100% of the treated sites (Burkhardt & Lang 2010). In our study, STE created a surplus of soft tissue that allowed passive primary closure after bone augmentation in test sites without flap advancement, incisions into the periosteum or remaining tension. No wound dehiscences were noted in these sites during healing; hence, the outcome of test sites confirms the relation between ease of primary closure and healing of the flap. Further, it corroborates the finding of good soft tissue healing after bone grafting subsequent to STE observed previously in clinical and other animal studies (Abrahamsson et al. 2011, 2012; Kaner & Friedmann 2011; Mertens et al. 2013). The incidence of dehiscences in control sites (8/10) appears high and questions the design and handling of the flaps elevated for augmentation surgery. Commonly, gentle manipulation and a favourable length-towidth ratio are considered as prerequisites for flap survival. Flaps not exceeding a length-towidth ratio of 2 or 2.5 to 1 are generally considered as safe and viable, irrespective of flap size and the need of advancement (M€ ormann
& Ciancio 1977; Greenstein et al. 2009). The placement of vertical releasing incisions and incisions into periosteum and submucosa in our study was in agreement with common recommendations for flap advancement for primary closure after major grafting procedures (Greenstein et al. 2009). As the flaps in control sites clearly had a favourable design, that is, a length-to-width ratio of approximately 2 : 3, the high frequency of dehiscences despite proper execution of surgery is intriguing. In plastic surgery, the straightforward concept of a relation of flap survival to a linear correlation between flap length and width has been discarded as being too simplistic (Milton 1970). In this fundamental study, the survival of skin flaps was correlated with the number of vessels in the flap pedicle, but not to the sole width of the flap base. This was attributed to the fact that oxygen demand is a function of total flap area, rather than of flap length. Hence, flaps may lack blood supply although their design appears favourable according to the concept of length-to-width ratio. Accordingly, the different outcomes of test and control groups in our study may be related to the effects of the different treatment procedures on the blood supply of the operated tissues. Incision and elevation of a mucoperiosteal flap disturb perfusion and induce ischaemia (McLean et al. 1995). The mucoperiosteal flap represents an ischaemia-reperfusion flap model in which the outcome of surgery relates to the extent and duration of microvascular damage (Carroll & Esclamado 2000; Retzepi et al. 2007b) that can be quantified using laser Doppler flowmetry (LDF; Donos et al. 2005). The injection of a local anaesthetic with vasoconstrictor prior to bone augmentation
© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd
caused a significant decrease in LDF measurements of microcirculation, being in line with own earlier results and other studies (Donos et al. 2005; Retzepi et al. 2007a,b; Kaner et al. 2013), and regardless of whether a tissue expander was in place or not. Subsequent augmentation surgery resulted in an additional significant impairment of microcirculation in control sites without preceding STE, but did not cause further decrease in blood flow in test sites. Here, the effect of surgery did not fall beyond the effect of local anaesthesia. Accordingly, significantly greater microcirculation values were found at the end of augmentation surgery in STE sites. In addition to the lower blood flow noticed in control sites immediately after grafting, significantly reduced LDF measurements of microcirculation were still found in these sites after 3 days of healing. LDF has previously been used to investigate the effects of periodontal surgical procedures with different extents of invasiveness. In this study, a minimally invasive flap design resulted in faster recovery of microcirculation, when compared to a conventional procedure (Retzepi et al. 2007a). Further, the mandibular gingival vasculature in dogs and humans shows arterial vessels that traverse obliquely from posterior to anterior (Jeffcoat et al. 1982; Kleinheinz et al. 2005), and the placement of long vertical releasing incisions basically affects revascularization of flaps (M€ ormann & Ciancio 1977). This is concordant with our investigation, which attributes the profound impact of augmentation surgery upon microcirculation in control sites to the standard technique of flap advancement by placing vertical releasing incisions and multiple incisions into periosteum and submucosa, whereas the minimally invasive procedure being carried out in test sites after STE did not significantly affect perfusion of the operated tissue. Perioperative assessment of microcirculation is widely used for surveillance of complications of reconstructive surgery (Phillips et al. 2012), and LDF monitoring of perfusion is able to predict necrosis of skin flaps (Heden et al. 1986). In our study, LDF measurements of vascularization can be considered as metric diagnostic data that preceded a related event, the dehiscence of flaps after 2 weeks. To further explore the relationship between the extent of disturbance of microcirculation and the occurrence of wound dehiscences, we calculated receiver operating characteristic (ROC) curves, an effective method for evaluation of performance of diagnostic tests (Hanley & McNeil 1982; Akobeng 2007). LDF measurements taken at baseline, after local anaesthesia and 3 days
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after augmentation surgery were not able to predict a subsequent wound dehiscence (Fig. 3a). However, LDF values of perfusion recorded directly after conclusion of augmentation surgery were a significant and strong predictor of subsequent wound dehiscences (AUC = 0.799, CI 0.642–0.955; P = 0.006, Fig. 3b). Given that reperfusion is essential for flap survival (Morris et al. 1993), our finding illustrates not only the applicability of LDF for monitoring of perioperative microcirculation, but also the impact of post-opera-
tive microcirculation on the outcome of augmentation surgery. In conclusion, our study showed the validity of LDF in assessing microcirculatory changes caused by different surgical procedures. STE resulted in less impairment of microcirculation caused by subsequent augmentation surgery. The positive effect of STE on blood flow after surgery decreased the incidence of wound dehiscences in the investigated animal model.
Acknowledgements: This study was supported by the ITI Foundation for the Promotion of Oral Implantology, Switzerland (Grant No. 687-2010). Institut Straumann AG, Basel, Switzerland, and Osmed GmbH, Ilmenau, Germany, donated clinical materials. We thank Dr. Endre Felszhegy, Semmelweis University, Budapest, Hungary, and Dr. Aart Molenberg, Institut Straumann AG, Basel, Switzerland, for their kind and competent support.
Jeffcoat, M.K., Kaplan, M.L., Rumbaugh, C.L. & Goldhaber, P. (1982) Magnification angiography in beagles with periodontal disease. Journal of Periodontal Research 17: 294–299. Jensen, S.S. & Terheyden, H. (2009) Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone-substitute materials. International Journal of Oral & Maxillofacial Implants 24(Suppl.): 218–236. Kaner, D. & Friedmann, A. (2011) Soft tissue expansion with self-filling osmotic tissue expanders before vertical ridge augmentation: a proof of principle study. Journal of Clinical Periodontology 38: 95–101. Kaner, D., Zhao, H., Terheyden, H. & Friedmann, A. (2013) Submucosal implantation of soft tissue expanders does not affect microcirculation. Clinical Oral Implants Research 18: 12158. Kleinheinz, J., B€ uchter, A., Kruse-L€ osler, B., Weingart, D. & Joos, U. (2005) Incision design in implant dentistry based on vascularization of the mucosa. Clinical Oral Implants Research 16: 518–523. Lundgren, S., Sjostrom, M., Nystrom, E. & Sennerby, L. (2008) Strategies in reconstruction of the atrophic maxilla with autogenous bone grafts and endosseous implants. Periodontology 2000 47: 143–161. McLean, T.N., Smith, B.A., Morrison, E.C., Nasjleti, C.E. & Caffesse, R.G. (1995) Vascular changes following mucoperiosteal flap surgery: a fluorescein angiography study in dogs. Journal of Periodontology 66: 205–210. Mertens, C., Thiele, O., Engel, M., Seeberger, R., Hoffmann, J. & Freier, K. (2013) The use of selfinflating soft tissue expanders prior to bone
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References Abrahamsson, P., Isaksson, S. & Andersson, G. (2011) Guided bone generation in a rabbit mandible model after periosteal expansion with an osmotic tissue expander. Clinical Oral Implants Research 22: 1282–1288. Abrahamsson, P., Walivaara, D.A., Isaksson, S. & Andersson, G. (2012) Periosteal expansion before local bone reconstruction using a new technique for measuring soft tissue profile stability: a clinical study. Journal of Oral and Maxillofacial Surgery 70: e521–e530. Akobeng, A.K. (2007) Understanding diagnostic tests 3: receiver operating characteristic curves. Acta Paediatrica 96: 644–647. Burkhardt, R. & Lang, N.P. (2010) Role of flap tension in primary wound closure of mucoperiosteal flaps: a prospective cohort study. Clinical Oral Implants Research 21: 50–54. Carroll, W.R. & Esclamado, R.M. (2000) Ischemia/ reperfusion injury in microvascular surgery. Head and Neck 22: 700–713. Donos, N., D’Aiuto, F., Retzepi, M. & Tonetti, M. (2005) Evaluation of gingival blood flow by the use of laser doppler flowmetry following periodontal surgery. A pilot study. Journal of Periodontal Research 40: 129–137. Greenstein, G., Greenstein, B., Cavallaro, J., Elian, N. & Tarnow, D. (2009) Flap advancement: practical techniques to attain tension-free primary closure. Journal of Periodontology 80: 4–15. Hanley, J.A. & McNeil, B.J. (1982) The meaning and use of the area under a receiver operating characteristic (roc) curve. Radiology 143: 29–36. Heden, P., Jurell, G. & Arnander, C. (1986) Prediction of skin flap necrosis: a comparative study between laser doppler flowmetry and fluorescein test in a rat model. Annals of plastic surgery 17: 485–488.
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Authors’ affiliations: Dogan Kaner, Han Zhao, Anton Friedmann, Department of Periodontology, University of Witten/Herdecke, Witten, Germany Hendrik Terheyden, Department of Maxillofacial Surgery, Rotes Kreuz Krankenhaus Kassel, Kassel, Germany
Improvement of microcirculation and wound healing in vertical ridge augmentation after pre-treatment with self-inflating soft tissue expanders – a randomized study in dogs
Key words: bone augmentation, Laser Doppler flowmetry, microcirculation, soft tissue
expansion Abstract Objectives: We investigated the effect of soft tissue expansion (STE) on vertical ridge augmentation with regard to the incidence of wound dehiscences and the impairment of
Corresponding author: Dr Dogan Kaner Department of Periodontology Dental School, Faculty of Health University of Witten/Herdecke Alfred-Herrhausen-Str. 45, 58448 Witten Germany Tel.: +49 2302 926 656 Fax: +49 2302 926 661 e-mail: [email protected]
microcirculation in dogs, and the applicability of laser Doppler flowmetry (LDF) to explore the relation between microcirculation and wound healing. Material and methods: Bone defects were created on both mandibular sides in ten beagle dogs by extraction of premolars and removal of bone. Six weeks later, self-filling tissue expanders were implanted in randomly assigned test sites. After 5 weeks of expansion, vertical augmentation was carried out in test and control sites using calvarial onlay grafts side by side with granular biphasic calcium phosphate covered with a resorbable polyethylene glycol membrane. Microcirculation was evaluated with laser Doppler flowmetry (LDF). The incidence of wound dehiscences was evaluated after 2 weeks. The validity of LDF to predict dehiscences was evaluated by construction of receiver operating characteristic (ROC) curves. Results: After augmentation, test sites showed significantly better perfusion than control sites without preceding STE (P = 0.012). Three days after surgery, perfusion was still significantly decreased in control sites (P = 0.005), while microcirculation in test sites had returned to presurgical levels. After 2 weeks, healing in test sites was good, whereas eight dehiscences were found in control sites (P = 0.002). ROC curves showed that microcirculation levels immediately after augmentation surgery significantly predicted subsequent wound dehiscences (AUC = 0.799, CI 0.642–0.955, P = 0.006). Conclusions: Laser Doppler flowmetry is suitable for evaluation of soft tissue microcirculation after ridge augmentation. STE reduced the impairment of microcirculation caused by vertical ridge augmentation and decreased the incidence of wound dehiscences in the investigated animal model.
Date: Accepted 22 February 2014 To cite this article: Kaner D, Zhao H, Terheyden H, Friedmann A. Improvement of microcirculation and wound healing in vertical ridge augmentation after pre-treatment with self-inflating soft tissue expanders – a randomized study in dogs. Clin. Oral Impl. Res. 26, 2015, 720–724 doi: 10.1111/clr.12377
720
Wound dehiscences and subsequent exposures of bone grafts are a common complication of complex augmentation procedures and occur in approximately 20% of cases (Jensen & Terheyden 2009; Kaner & Friedmann 2011). Dehiscences are attributed to difficulties in achieving tension-free primary wound closure and remaining high tension forces on the flap (Lundgren et al. 2008; Burkhardt & Lang 2010). When compared to straightforward surgical procedures, primary closure after complex augmentation necessitates extensive advancement of the flap by placement of releasing incisions into the
periosteum and submucosa. Generally, the elevation of a flap disturbs perfusion and causes ischaemia (McLean et al. 1995), while preservation of sufficient blood flow is important for tissue survival (Nakayama et al. 1982). Conversely, massive reduction of blood supply and subsequent ischaemia-reperfusion injury may affect the operated tissue and may cause complications such as necrosis of the flap (Carroll & Esclamado 2000). These negative effects from surgical trauma may impair wound healing after implantation of biomaterials or grafts and may further cause complications of bone grafting
© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
Kaner et al Soft tissue expanders and vertical augmentation
procedures, that is, post-surgical wound dehiscence and subsequent exposure of bone grafts despite proper execution of surgery and satisfactory initial primary closure (Kaner & Friedmann 2011). Generation of additional soft tissue before reconstructive surgery using subcutaneous tissue expanders to increase tissue quantity and quality for ease of primary closure and reduction of tissue traumatization is an established method in plastic surgery. Soft tissue expansion (STE) using self-filling osmotic hydrogel expanders prior to complex ridge augmentation surgery using autogenous bone grafts has been applied in two case series and one randomized study in humans, and resulted in high gain of regenerated bone, only minimal resorption of newly gained bone and a comparatively very low incidence of wound dehiscences (Kaner & Friedmann 2011; Abrahamsson et al. 2012; Mertens et al. 2013). However, the effects of STE on disturbance of microcirculation after augmentation surgery and the relation of microcirculation to soft tissue healing have not been investigated. Laser Doppler flowmetry has been used for evaluation of microcirculation after periodontal surgery and after implantation of tissue expanders (Donos et al. 2005; Kaner et al. 2013). However, LDF has not been applied for assessment of microcirculation after bone augmentation. The aims of our study were to explore the applicability of LDF for evaluation of microcirculation after augmentation surgery and to assess the effect of STE on microcirculation and soft tissue healing after vertical ridge augmentation in dogs.
Material and methods The study protocol was approved by the Food Safety and Animal Health Protection Board of the Regional Council of Pest, Hungary. The study was conducted at the Research Institute for Animal Breeding and Nutrition, Herceghalom, Hungary. Ten male beagle dogs (mean age 8.1 0.9 months, mean weight 12.2 1.3 kg) were used for the study. All surgeries and measurements were performed in general anaesthesia using intravenous injections of ketamin hydrochloride (2.5 ml/10 kg, Ketavet 10%; Pfizer, Berlin, Germany) and xylazine hydrochloride (1 ml/10 kg, Xylavet 2%; Sanofi-Aventis, Budapest, Hungary) every 15 min. Metamizole (1 ml/10 kg, Algopyrin; SanofiAventis) was injected intramuscularly after
surgeries and continued for 3 days for pain control. A single intramuscular injection of amoxicillin hydrochloride solution (150 mg, 1 ml/10 kg; Pfizer) was administered after surgeries for prevention of infections. Surgery Bone defects and implantation of tissue expanders
The creation of bone defects and implantation of tissue expanders have been described previously in detail (Kaner et al. 2013). After extraction of all mandibular premolars, the residual bone at the lingual side was reduced by 5 mm, while the buccal bone was additionally reduced to the bottom of the sockets of the extracted teeth in order to mimic a chronic severe vertical and horizontal bone defect. Six weeks after creation of bone defects, self-filling osmotic tissue expanders (cylinder type, final volume 0.7 ml; Osmed, Ilmenau, Germany) were implanted in randomly assigned sides of the mandible (test sites) into a submucosal pouch prepared without elevation of the periosteum. Augmentation surgery
After 5 weeks of expansion, ridge augmentation was carried out at test sites and at contralateral control sites after standardized doses of local anaesthesia (2 9 0.5 ml each buccally and lingually; articaine 4% with epinephrine 1 : 100,000; UDS forte, SanofiAventis, Frankfurt, Germany). At test sites with preceding STE, a midcrestal incision was placed above the tissue expander and extended into the sulci of the canine and the first molar for ease of reflection, but without vertical releasing incisions. The tissue expander was removed, the periosteum was cut in mesio-distal direction to expose the underlying bone, and buccal and lingual flaps were elevated. At control sites without preceding STE, a midcrestal incision was placed and extended
(a)
into the sulci of the adjacent teeth. Vertical releasing incisions were placed buccally at the mesial line angle of the canine and the distal line angle of the first molar and extended into the mucosa. The recipient bone was perforated with a small bur, and the ridge was augmented with a screw-fixated cortical bone graft harvested from the calvaria with a diamond saw and with granular biphasic calcium phosphate (BCP, Bone Ceramic; Institut Straumann AG, Basel, Switzerland) covered with a resorbable polyethylene glycol membrane (PEG; MembraGel, Institut Straumann AG). The grafts were placed side by side, but separated by at least 3 mm (Fig. 1a,b), after the positions (mesial/distal) of the grafts had been randomly assigned by flip of a coin. At test sites, primary closure was achieved without additional advancement of the flaps. At control sites, the flaps were advanced by placement of vertical releasing incisions and incisions into periosteum and submucosa until the flaps passively covered the augmented area, as generally recommended (Greenstein et al. 2009). Then, the flaps were approximated with vertical mattress sutures (Vicryl 3.0; Ethicon, Norderstedt, Germany), and the incision was closed with a continuous suture using fine resorbable monofilament sutures (Monocryl 6.0; Ethicon). Evaluation of soft tissue healing and microcirculation
The primary outcome, soft tissue dehiscences over the grafted areas, was assessed dichotomously (yes/no) 2 weeks after augmentation surgery. A laser Doppler flowmeter (Periflux 5010; Perimed AB, Jarfalla, Sweden) equipped with a PF 416 probe (outside diameter 1.0 mm, fibre separation 0.25 mm; wavelength 780 nm) was used for assessment of microcirculation. The flowmeter recordings were measured in perfusion units (PU) and moni-
(b)
Fig. 1. (a,b) Resorbed ridge augmented with BCP and PEG membrane (left) and calvarial onlay graft (right).
© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd
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Kaner et al Soft tissue expanders and vertical augmentation
tored using the Perisoft software (Perisoft 2.10; Perimed). Microcirculation was assessed at augmentation surgery before local anaesthesia (baseline), 2 min after local anaesthesia (T1), directly after termination of augmentation surgery (T2) and after 3 days (T3). A customized acrylic stent was fixed with silicone impression material at the adjacent teeth to facilitate standardized reproducible measurements, as reported previously (Kaner et al. 2013). The LDF probe was aligned at the stent, and 1-min measurements were always performed at the same two positions per flap, perpendicular to the tissue and at a distance of 0.5 mm to the flap. All measurements were carried out by the same calibrated investigator (H.Z.). Statistical analysis
Averages of the 1-min LDF measurements were calculated with the Perisoft software. Changes of blood flow in relation to the baseline values were calculated, and statistical analysis was carried out per protocol using a statistics software (SPSS 19.0; SPSS Inc., Chicago, IL, USA). Nonparametric tests were used for comparisons between test and control sites (Mann–Whitney U-test and Fisher’ exact test) and the various time points (Wilcoxon’s signed-rank test). The validity of LDF measurements to predict the occurrence of wound dehiscences was evaluated by construction of receiver operating characteristic (ROC) curves. P < 0.05 was considered significant.
Results Ten tissue expanders were implanted at test sites. Surgery and initial healing were uneventful and free of complications. Until augmentation surgery (baseline, 5 weeks after implantation of tissue expanders), three expanders were lost. The statistical analysis was carried out per protocol; hence, these sites were excluded. Soft tissue healing
Two weeks after grafting, no wound dehiscence was found in test sites, whereas eight wound dehiscences were noted in the control group (Fig. 2a,b; Table 1, significant difference favouring the test group, P = 0.002, Fisher’s exact test).
(a)
(b)
Fig. 2. (a) Control site with dehiscence 2 weeks after augmentation surgery: exposure of bone block graft (left) and loss of BCP + PEG membrane (right). (b) STE test site 2 weeks after surgery: closed flap and good soft tissue healing.
Table 1. Contingency table for wound dehiscences noted 2 weeks after augmentation surgery. Significant difference favouring the test group (Fisher’s exact test, P = 0.002) Exposition No exposition
Test group
Control group
0 7
8 2
(T1), blood flow changed significantly in test sites by 6.1 PU (median, Q1 11.9, Q3 3.5, P = 0.001) and, similarly (no significant difference between groups), in control sites by 5.1 PU (Q1 10.7, Q3 1.4, P = 0.001). From T1 to conclusion of augmentation surgery (T2), perfusion decreased significantly further in control sites to 11.4 PU (Q1 15.8, Q3 7.0, P < 0.001), whereas perfusion in test sites remained unchanged ( 5.8 PU, Q1 13.0, Q3 0.9, P > 0.05) with the result of significantly better microcirculation in the test group at T2 (P = 0.012). From T2 to T3 (3 days after augmentation surgery), no significant change was noted in test sites, while perfusion increased significantly in control sites ( 4.3 PU, Q1 11.8, Q3 0.5, P = 0.001). However – in contrast to test sites – microcirculation measurements at control sites were still significantly lower at T3, when compared to baseline (P = 0.005). Prediction of soft tissue dehiscence
Receiver operating characteristic curves for microcirculation measurements taken at
baseline, T1 (after local anaesthesia), T2 (after augmentation surgery) and T3 (3 days after augmentation surgery) as predictors of subsequent wound dehiscences are shown in Fig. 3a,b. Perfusion values at baseline, T1 and T3, respectively, did not predict a subsequent wound dehiscence (Fig. 3a). However, perfusion measurements taken directly after augmentation surgery (T2) were able to significantly predict a subsequent wound dehiscence (Fig. 3b. AUC = 0.799, P = 0.003, 95% confidence interval (CI) 0.642–0.955).
Discussion The aim of our randomized split-mouth study in dogs was to investigate the effects of soft tissue expansion (STE) on healing and microcirculation after vertical ridge augmentation. In contrast to the low rate of expander losses (9%) in our preceding case series in humans (Kaner & Friedmann 2011), 3 of 10 expanders (30%) were lost during the 5-week expansion phase. Mechanical irritation of the expansion area can lead to loss of tissue expanders (Mertens et al. 2013). Although the teeth opposite to the surgical sites had been removed prior to the implantation of tissue expanders, the comparatively high rate of expander losses may be attributed to continued uncontrolled mastication on the surgical sites.
Table 2. Time course of microcirculation changes expressed as difference in perfusion units (PU) from baseline (medians and interquartiles) Baseline (before local anaesthesia) Test Control
0 0
T1 (after local anaesthesia) 6.1 ( 11.9; 5.1 ( 10.7;
T2 (after bone augmentation) 3.5)a 1.4)a
5.8 ( 13.0; 11.4 ( 15.8;
T3 (3 days after surgery) 0.9)b,g 7.0)c,e,g
5.9 ( 12.3; 4.3) 4.3 ( 11.8; 0.5)d,f
Significantly different from baseline (Wilcoxon signed-rank test, P = 0.001). Significantly different from baseline (Wilcoxon signed-rank test, P = 0.006). Significantly different from baseline (Wilcoxon signed-rank test, P < 0.001). d Significantly different from baseline (Wilcoxon signed-rank test, P = 0.005). e Significantly different from T1 (Wilcoxon signed-rank test, P = 0.005). f Significantly different from T2 (Wilcoxon signed-rank test, P = 0.001). g Significant difference between test and control group (Mann–Whitney U-test, P = 0.012). a
b c
Microcirculation
Test and control sites showed similar microcirculation measurements at baseline (Table 2). After application of local anaesthesia
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© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd
Kaner et al Soft tissue expanders and vertical augmentation
(a)
(b)
Fig. 3. (a) ROC curves for the ability of LDF measurements at baseline (BL), T1 and T3 to predict a subsequent wound dehiscence and graft exposure. BL: AUC = 0.601, CI 0.405–0.796; P = 0.317. T1: AUC = 0.420, CI 0.218– 0.622; P = 0.427. T3: AUC = 0.550, CI 0.351–0.750; P = 0.617. (b) ROC curve for the ability of LDF measurements at T2 to predict a subsequent wound dehiscence and graft exposure. AUC = 0.799, CI 0.642–0.955; P = 0.003.
Two weeks after bone augmentation, no dehiscences were found in test sites with preceding STE, whereas eight dehiscences with exposure of bone grafts were noted in control sites. Generally, the occurrence of wound dehiscences is attributed to difficulties in achieving tension-free primary closure of the flap (Lundgren et al. 2008). Concordantly, a clinical study demonstrated that wound closure was maintained during healing, when minimal or no force was needed for suturing of the flap after augmentation. In contrast, patients with higher flap tension forces showed dehiscences in 40–100% of the treated sites (Burkhardt & Lang 2010). In our study, STE created a surplus of soft tissue that allowed passive primary closure after bone augmentation in test sites without flap advancement, incisions into the periosteum or remaining tension. No wound dehiscences were noted in these sites during healing; hence, the outcome of test sites confirms the relation between ease of primary closure and healing of the flap. Further, it corroborates the finding of good soft tissue healing after bone grafting subsequent to STE observed previously in clinical and other animal studies (Abrahamsson et al. 2011, 2012; Kaner & Friedmann 2011; Mertens et al. 2013). The incidence of dehiscences in control sites (8/10) appears high and questions the design and handling of the flaps elevated for augmentation surgery. Commonly, gentle manipulation and a favourable length-towidth ratio are considered as prerequisites for flap survival. Flaps not exceeding a length-towidth ratio of 2 or 2.5 to 1 are generally considered as safe and viable, irrespective of flap size and the need of advancement (M€ ormann
& Ciancio 1977; Greenstein et al. 2009). The placement of vertical releasing incisions and incisions into periosteum and submucosa in our study was in agreement with common recommendations for flap advancement for primary closure after major grafting procedures (Greenstein et al. 2009). As the flaps in control sites clearly had a favourable design, that is, a length-to-width ratio of approximately 2 : 3, the high frequency of dehiscences despite proper execution of surgery is intriguing. In plastic surgery, the straightforward concept of a relation of flap survival to a linear correlation between flap length and width has been discarded as being too simplistic (Milton 1970). In this fundamental study, the survival of skin flaps was correlated with the number of vessels in the flap pedicle, but not to the sole width of the flap base. This was attributed to the fact that oxygen demand is a function of total flap area, rather than of flap length. Hence, flaps may lack blood supply although their design appears favourable according to the concept of length-to-width ratio. Accordingly, the different outcomes of test and control groups in our study may be related to the effects of the different treatment procedures on the blood supply of the operated tissues. Incision and elevation of a mucoperiosteal flap disturb perfusion and induce ischaemia (McLean et al. 1995). The mucoperiosteal flap represents an ischaemia-reperfusion flap model in which the outcome of surgery relates to the extent and duration of microvascular damage (Carroll & Esclamado 2000; Retzepi et al. 2007b) that can be quantified using laser Doppler flowmetry (LDF; Donos et al. 2005). The injection of a local anaesthetic with vasoconstrictor prior to bone augmentation
© 2014 The Authors. Clinical Oral Implants Research Published by John Wiley & Sons Ltd
caused a significant decrease in LDF measurements of microcirculation, being in line with own earlier results and other studies (Donos et al. 2005; Retzepi et al. 2007a,b; Kaner et al. 2013), and regardless of whether a tissue expander was in place or not. Subsequent augmentation surgery resulted in an additional significant impairment of microcirculation in control sites without preceding STE, but did not cause further decrease in blood flow in test sites. Here, the effect of surgery did not fall beyond the effect of local anaesthesia. Accordingly, significantly greater microcirculation values were found at the end of augmentation surgery in STE sites. In addition to the lower blood flow noticed in control sites immediately after grafting, significantly reduced LDF measurements of microcirculation were still found in these sites after 3 days of healing. LDF has previously been used to investigate the effects of periodontal surgical procedures with different extents of invasiveness. In this study, a minimally invasive flap design resulted in faster recovery of microcirculation, when compared to a conventional procedure (Retzepi et al. 2007a). Further, the mandibular gingival vasculature in dogs and humans shows arterial vessels that traverse obliquely from posterior to anterior (Jeffcoat et al. 1982; Kleinheinz et al. 2005), and the placement of long vertical releasing incisions basically affects revascularization of flaps (M€ ormann & Ciancio 1977). This is concordant with our investigation, which attributes the profound impact of augmentation surgery upon microcirculation in control sites to the standard technique of flap advancement by placing vertical releasing incisions and multiple incisions into periosteum and submucosa, whereas the minimally invasive procedure being carried out in test sites after STE did not significantly affect perfusion of the operated tissue. Perioperative assessment of microcirculation is widely used for surveillance of complications of reconstructive surgery (Phillips et al. 2012), and LDF monitoring of perfusion is able to predict necrosis of skin flaps (Heden et al. 1986). In our study, LDF measurements of vascularization can be considered as metric diagnostic data that preceded a related event, the dehiscence of flaps after 2 weeks. To further explore the relationship between the extent of disturbance of microcirculation and the occurrence of wound dehiscences, we calculated receiver operating characteristic (ROC) curves, an effective method for evaluation of performance of diagnostic tests (Hanley & McNeil 1982; Akobeng 2007). LDF measurements taken at baseline, after local anaesthesia and 3 days
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after augmentation surgery were not able to predict a subsequent wound dehiscence (Fig. 3a). However, LDF values of perfusion recorded directly after conclusion of augmentation surgery were a significant and strong predictor of subsequent wound dehiscences (AUC = 0.799, CI 0.642–0.955; P = 0.006, Fig. 3b). Given that reperfusion is essential for flap survival (Morris et al. 1993), our finding illustrates not only the applicability of LDF for monitoring of perioperative microcirculation, but also the impact of post-opera-
tive microcirculation on the outcome of augmentation surgery. In conclusion, our study showed the validity of LDF in assessing microcirculatory changes caused by different surgical procedures. STE resulted in less impairment of microcirculation caused by subsequent augmentation surgery. The positive effect of STE on blood flow after surgery decreased the incidence of wound dehiscences in the investigated animal model.
Acknowledgements: This study was supported by the ITI Foundation for the Promotion of Oral Implantology, Switzerland (Grant No. 687-2010). Institut Straumann AG, Basel, Switzerland, and Osmed GmbH, Ilmenau, Germany, donated clinical materials. We thank Dr. Endre Felszhegy, Semmelweis University, Budapest, Hungary, and Dr. Aart Molenberg, Institut Straumann AG, Basel, Switzerland, for their kind and competent support.
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