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J Clinic Periodontology - 2019 - Moreno Rodríguez - Supra Alveolar Attachment Gain in The Treatment of Combined
J Clinic Periodontology - 2019 - Moreno Rodríguez - Supra Alveolar Attachment Gain in The Treatment of Combined
DOI: 10.1111/jcpe.13158
CLINICAL PERIODONTOLOGY
1
Private Practice, Murcia, Spain
2 Abstract
Department of Stomatology, Faculty of
Medicine, University of Murcia, Murcia, Aim: To assess the effectiveness of non‐incised papillae surgical approach (NIPSA) in
Spain
periodontal reconstructive surgery of combined intra‐suprabony defects.
3
Postgraduate Periodontics, Complutense
University of Madrid, Madrid, Spain
Materials and Methods: Patients with deep periodontal defects treated with
NIPSA (n = 20) were analysed. Defects were treated with enamel matrix derivative
Correspondence
Jose A. Moreno Rodríguez, C/Ctra de
plus xenograft. Clinical outcomes were assessed before surgery and at 12 months.
Granada no. 46, Caravaca de la Cruz, 30400 Wound closure was assessed one week post‐surgery. Supra‐alveolar attachment gain
Murcia, Spain.
Email: joseantonio171087@gmail.com
(SUPRA‐AG) was recorded at 12 months post‐surgery.
Results: Non‐incised papillae surgical approach showed significant improvements in
clinical attachment gain (5.9 ± 2.38 mm; p < 0.001), recession reduction (0.25 ± 0.44;
p < 0.05) and tip of the papillae coronal displacement (0.4 ± 0.5; p < 0.05). It also
showed complete wound closure of the apical mucosal incision in the 85% of the
cases, with no interproximal tissue necrosis. SUPRA‐AG (1.9 ± 1.74) showed a posi‐
tive tendency, associated with complete intrabony defect resolution.
Conclusions: Non‐incised papillae surgical approach promoted primary intention
healing, wound stability and space provision for optimal periodontal reconstruction,
preserving supra‐alveolar soft tissue integrity.
KEYWORDS
periodontitis, reconstructive surgery, regeneration, surgical flaps
J Clin Periodontol. 2019;46:927–936. wileyonlinelibrary.com/journal/jcpe © 2019 John Wiley & Sons A/S. | 927
Published by John Wiley & Sons Ltd
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928 | MORENO RODRÍGUEZ et al.
F I G U R E 1 Supra‐alveolar attachment gain (SUPRA‐AG) concept. Non‐incised papillae surgical approach (NIPSA) outcome (a–f) and
schematic illustrations (g–i). Black and white line border‐lining the cementum–enamel junction (CEJ); Black and white arrow: CEJ; yellow
arrow: pre‐surgery BC; yellow line indicating bone crest contour; blue arrow indicating location of probe tip (in figure e: blue arrow
indicating location of probe tip from figure d). (a) Pre‐surgical periapical X‐ray. Orange arrow indicating BD. (b) Pre‐surgical CAL = 8 mm. (c)
Intra‐surgical probing. CEJ‐BD = 12 mm. INTRA = 5 mm. CEJ‐BC = 7 mm. (d) 12 months after surgery CAL = 3 mm. (e) Re‐entry 18 months
after surgery, probe indicating differences from bone crest on the buccal (light arrow) and interproximal area (green arrow); SUPRA‐AG (light
blue line: distance between yellow and blue arrows), calculated as (intra‐surgical CEJ‐BC)‐post‐op CAL = 4 mm. (Photograph taken at the
time of treating an adjacent tooth treatment not included in the present study). (f) 18 months after surgery periapical X‐ray. g. Periodontal
lesions with combined intrabony and supra‐alveolar defect. (h) A positive SUPRA‐AG value indicates an attachment gain above pre‐surgery
BC (i). A negative SUPRA‐AG value indicate an incomplete resolution of the intrabony defect
(g) (h)
(i) (j)
far removed from the inter‐dental papillae and marginal keratinized and the inner surface of the coronal flap were cut with micro‐scis‐
tissues as possible. Mesiodistally, the incision extended sufficiently sors (Mamadent®; Tuttlingen, Germany) and removed. Root planing
to allow correct granulation tissue debridement and intrabony defect was performed considering the fibres attached to cementum and
manipulation. The tissue coronal to the incision was reflected apico‐ the coronal limits of the flap reflected. Soft tissues not attached to
coronally maintaining marginal tissue integrity. The papillae structure the root surface were removed with micro‐curettes and micro‐ul‐
was pulled coronally with a micro‐papillae elevator (Mamadent®; trasonic instruments (After Five® Piezo Scaling tip; Hu‐Friedy).
Tuttlingen, Germany) to increase space provision in the supra‐alveo‐ After defect debridement and root surface instrumentation, 24%
lar component for debridement, biomaterial application and clot sta‐ ethylenediaminetetraacetic acid gel (Prefgel®; Straumann) was ap‐
bilization. Before defect debridement, the flap was protected with a plied on the root for 2 min. The area was carefully rinsed with saline.
periosteal elevator (Mamadent®; Tuttlingen, Germany) and frequent EMD (Emdogain®; Straumann) was applied on the root followed by a
saline irrigation. Granulation tissue was detached from the bony walls composite graft of deproteinized bovine bone xenograft (Bio‐Oss®;
with micro‐curettes (Micro Mini Five® Gracey; Hu‐Friedy). Pocket ep‐ Geistlich Pharma) and EMD (Emdogain®; Straumann). The mucosal
ithelium and granulation tissue attached to the base of the papilla incision line was closed with a double layer of suturing (PGA 6.0;
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MORENO RODRÍGUEZ et al. | 931
(g) (h)
(i) (j)
Hu‐Friedy): first, with horizontal mattress sutures, placed 2 mm away significant and a common standard deviation (SD) of 2.0. A drop‐
from the borders, promoting connective tissue contact, and then, sin‐ out rate of 0% was anticipated. (“Sample size and power calculator,”
gle interrupted sutures placed as a second line of closure. https://www.imim.cat/ofertadeser veis/software-public/granmo/).
Descriptive statistics were made of patient characteristics and
the specific site, defect morphology, pre‐surgical and post‐surgical
2.3.3 | Post‐surgical procedures
clinical measurements.
Patients were instructed to rinse with a 0.2% chlorhexidine digluco‐ Quantitative variables were expressed as means and SD.
nate solution twice a day for 4 weeks. Sutures were removed after Outcome variables were assessed using Student's t test for paired
7 days. At 4 weeks, patients were instructed to start brushing with a data. P‐values < 0.05 were considered statistically significant.
soft toothbrush and a roll technique. Patients were recalled for con‐ Cases were also categorized according to WC (=2 or < 2). Cases
trol and prophylaxis at weeks 1, 2, 3 and 4 and at 3, 6 and 12 months. with WC = 2 and cases with WC < 2 were compared to determine
The follow‐up was 12 months. which variables were associated with wound failure. P‐values < 0.05
were considered statistically significant.
Subject and defect characteristics of the sample population are in structural and vascular support (Bosshardt, 2018). Pre‐surgical
presented in Table 1. minimally invasive conditioning of the periodontal pocket (Moreno
Rodríguez & Caffesse, 2018; Moreno Rodríguez et al., 2018) may
improve the quality of the connective tissue, optimizing the tone of
3.1 | Clinical outcomes at 12 months
the marginal soft tissue at the time of surgery.
Clinical outcomes are shown in Tables 2 and 3. At 12 months, the The interproximal tissues are nourished by a profuse vascu‐
results showed statistically significant gains from baseline in PPD lar network (McLean, Smith, Morrison, Nasjleti, & Caffesse, 1995;
and CAL (p < 0.001), significant reduction in recession (p < 0.02) and Mörmann, Meier, & Firestone, 1979; Nobuto et al., 2005). However,
a significant increase in TP (p = 0.002). No difference was obtained the dimensions and morphology of the inter‐dental tissues affect the
in KT. Furthermore, after 12 months, the mean SUPRA‐AG value was re‐establishment of blood perfusion (Kohl et al, 1961). A thin papilla
found to be positive. with a narrow base has a delicate terminal blood supply, which is
significantly affected by making an incision at its base and raising a
marginal mucoperiosteal flap (Nobuto et al., 2005; Retzepi, Tonetti,
3.2 | Wound healing and post‐operative pain & Donos, 2007). The apical incision performed and the lack of mar‐
CWC was present in 17 sites (85%) and IWC in three sites, with no ginal tissue reflected with NIPSA may permit better maintenance of
NT. One week after surgery, the mean WC value was 1.85 ± 0.34, the terminal blood supply to the papillae.
and no differences were found in clinical outcomes between WC = 2 Histological studies have shown different patterns of healing
and WC < 2 (Table 4). The mean dose of ibuprofen taken was after periodontal surgery, either by regeneration or repair (Caton,
1,470 ± 714 mg. Nyman, & Zander, 1980; Listgarten & Rosenberg, 1979). Under opti‐
mal circumstances, periodontal regeneration is achievable (Polimeni,
Susin, & Wikesjö, 2009; Wikesjö, Lim, Thomson, & Hardwick,
A residual active pocket results in inflammation and focal destruction in periodontal regeneration (Susin et al., 2015). Studies evaluating
that modifies the condition of the connective tissue, with changes healing have suggested that interfering with the adsorption, adhe‐
sion and maturation of a root surface‐adhering fibrin clot resulted
TA B L E 1 Patient and defect characteristics in the formation of a junctional epithelium (Hiatt, Stallard, Butler, &
Badgett, 1968; Linghorne & O’Connell, 1950; Polson & Proye, 1983).
NIPSA (n = 20)
Accessing the periodontal defect by raising the flap using a pap‐
Study population illary incision and intrasulcular detachment significantly improved
Sex (male/female) 12/8 PPD reduction, as already reported (Cortellini, Prato, & Tonetti, 1999;
Age (years) (mean ± SD) 47.3 ± 9.54 Cortellini & Tonetti, 2007; Moreno Rodríguez et al., 2018; Trombelli,
Non‐smoker/smokers/former smoker 8/5/7 Simonelli, Schincaglia, Cucchi, & Farina, 2012; Di Tullio et al., 2013);
Dental arch (upper/lower) 10/10 however, CAG and PPD were associated with an increase in REC and
CEJ‐BD (mean ± SD) 10.75 ± 2.59 the defect with limited connective tissue support may compromise the
nutrition to the overlaying soft tissue, increasing the risk of wound de‐
CEJ‐BC (mean ± SD) 5.25 ± 1.2
hiscence or interproximal soft tissue necrosis during the early healing
INTRA 5.3 ± 2.39
period (Farina et al., 2013; Moreno Rodríguez et al., 2018; Mörmann et
3‐wall 2.75 ± 1.62
al., 1979; Retzepi et al., 2007; Wikesjö, Lim, et al., 2003). The marginal
SUPRA‐ST 7.25 ± 2.34
soft tissue morphology, the inter‐dental space, the avascular nature of
Intrabony defect configuration
the root surface, the confined papillary dimension and the mechanical
1/3‐wall 14 forces acting on the wound margins may compromise the outcome,
2/3‐wall 1 increasing supra‐alveolar soft tissue contraction (Farina et al., 2013;
1/2‐wall 1 Sanz et al., 2004; Sigurdsson et al., 1994; Trombelli, Kim, Zimmerman,
3‐wall 1 & Wikesjö, 1997). Thus, marginal approaches may provide limited ca‐
2‐wall 0 pacity for space provision in non‐contained and supra‐alveolar defects
1‐wall 3 (Jentsch & Purschwitz, 2008).
The apical approach was evaluated (NIPSA; Moreno Rodríguez &
Abbreviations: CEJ, cemento‐enamel junction; INTRA, intrabony defect;
NIPSA, non‐incised papillae surgical approach; SUPRA‐ST, interproximal Caffesse, 2018; Moreno Rodríguez et al., 2018), to assess the clini‐
supra‐alveolar soft tissue. cal results in combined intra‐suprabony periodontal defects. NIPSA
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MORENO RODRÍGUEZ et al. | 933
TA B L E 2 Clinical measurements
Baseline 12 months Change Significance, pf
(mm ± SD)
PPD 8.15 ± 2.48 2.55 ± 0.6 5.6 ± 2.48a <0.001
CAL 9.25 ± 2.71 3.35 ± 0.99 5.9 ± 2,38b <0.001
c
REC 1.1 ± 0.85 0.85 ± 0.93 0.25 ± 0.44 0.021
TP 2.00 ± 1.38 2.4 ± 1.35 −0.4 ± 0.5d 0.002
KT 3.5 ± 1.7 3.5 ± 1.7 – NS
SUPRA‐AG 1.9 ± 1.74e
Abbreviations: CAL, clinical attachment level; KT, keratinized tissue; mm, millimetres; NS, not
significant, p > 0.05; PPD, probing pocket depth; REC, recession; SUPRA‐AG, supra‐alveolar attach‐
ment gain; TP, tip of the papillae.
a
PPD change = PPDr.
b
CAL change = CAG.
c
Positive value in REC indicates decreased recession.
d
Negative value in TP indicates papillae coronal displacement.
e
Negative value in SUPRA‐AG indicates incomplete resolution of the intrabony defect.
*Paired t test.
TA B L E 3 Frequency distributions of CAL and PPD changes at and clinical advantages: space provision is created by pulling the in‐
1 year terproximal supra‐alveolar soft tissue coronally and by preserving the
architecture of the interproximal and marginal tissues. The unaltered
CAG PPDr
integrity of the supra‐alveolar soft tissue, acting as a dome protecting
n % n % the clot, enhances wound stability and supports mechanical traumas
0–1 mm 0 — 0 — during early healing. The fact that the incision is located apically, far
2–3 mm 2 10 3 15 from the marginal tissue on cortical bone and mucosa, facilitates pri‐
4–5 mm 9 45 8 40 mary closure during early healing: 85% of surgeries showed CWC com‐
6–7 mm 5 25 5 25 pared to 15% with IWC, with minimal flap dehiscence sealed by a fibrin
clot, far from the defects and the regenerative materials. Furthermore,
≥8 mm 4 20 4 20
inter‐dental soft tissue necrosis, which may increase contamination in
Abbreviations: CAG, clinical attachment gain; PPDr, probing pocket
the regenerating area (De Sanctis et al., 1996), and soft tissue contrac‐
depth reduction.
tion with unaesthetic results are avoided.
In this study, only intrabony defects associated with horizon‐
resulted in significant PPD reduction, CAG, REC reduction and TP tal bone loss were included, and the changes in the supra‐alveolar
coronal displacement, indicating its capacity to better preserve soft component were evaluated. SUPRA‐AG was introduced to assess
tissue level. NIPSA is being proposed as an approach to promote the the resolution of the intrabony defect. NIPSA showed a positive
conditions for optimal periodontal regeneration, even in supra‐alveo‐ tendency in SUPRA‐AG that means a complete resolution of the in‐
lar defects. As already described, its apical access has several technical trabony component. The apical approach may be also indicated in
Abbreviations: CAG, clinical attachment gain; Ch, change; KT, keratinized tissue; mm, millimetres;
NS, not significant, p > 0.05.; PPDr, probing pocket depth reduction; REC, recession; SUPRA‐AG,
supra‐alveolar attachment gain; TP, tip of the papillae; WC, wound closure.
a
Positive value in REC indicates decreased recession.
b
Negative value in TP indicates papillae coronal displacement.
c
Negative value in SUPRA‐AG indicates incomplete resolution of the intrabony defect.
*t test
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934 | MORENO RODRÍGUEZ et al.
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pacity to trigger regeneration have been widely reported (Arweiler,
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Auschill, Donos, & Sculean, 2002; Groeger, Windhorst, & Meyle, Periodontics and Restorative Dentistry, 19, 589–599.
2016; Melloning, 1999; Miron, Dard, & Weinreb, 2015; Yukna & Cortellini, P., & Tonetti, M. S. (2007). A minimally invasive surgical tech‐
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a graft material enhanced the clinical outcome of EMD (Matarasso
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et al., 2015; Tu, Woolston, & Faggion, 2010), improving its space‐ Cortellini, P., & Tonetti, M. S. (2009). Improved wound stability
making potential, by preventing collapse of the overlying soft tissues with a modified minimally invasive surgical technique in the re‐
into the area to be regenerated (De Leonardis & Paolantonio, 2013). generative treatment of isolated interdental intrabony de‐
fects. Journal of Clinical Periodontology, 36, 157–163. https ://doi.
Although RCTs are required, NIPSA seems to create optimal
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conditions for space provision, wound stabilization and primary
Cortellini, P., Tonetti, M. S., Lang, N. P., Suvan, J. E., Zucchelli, G.,
intention healing, avoiding collapse and soft tissue contraction by Vangsted, T., … Adriaens, P. (2001). The simplified papilla pres‐
maintaining the integrity of the marginal tissues and preserving the ervation flap in the regenerative treatment of deep intrabony
papillary architecture intact. defects: Clinical outcomes and postoperative morbidity. Journal
of Periodontology, 72, 1702–1712. https ://doi.org/10.1902/
jop.2001.72.12.1702
AC K N OW L E D G E M E N T S De Leonardis, D., & Paolantonio, M. (2013). Enamel matrix derivative,
alone or associated with a synthetic bone substitute, in the treat‐
We thank Dr Manuel Canteras, Professor of Biostatistics, Department ment of 1‐ to 2‐wall intrabony defects. Journal of Periodontology, 84,
of Social and Public Health Science, Faculty of Medicine, University 444–455.
De Sanctis, M., Zucchelli, G., & Clauser, C. (1996). Bacterial coloniza‐
of Murcia, for carrying out the statistical tests.
tion of bioabsorbable barrier material and periodontal regeneration.
Journal of Periodontology, 67, 1193–1200. https://doi.org/10.1902/
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C O N FL I C T O F I N T E R E S T
Di Tullio, M., Femminella, B., Pilloni, A., Romano, L., D'Arcangelo, C.,
The authors report no conflicts of interest. De Ninis, P., & Paolantonio, M. J. (2013). Treatment of supra‐alve‐
olar‐type defects by a simplified papilla preservation technique for
access flap surgery with or without enamel matrix proteins. Journal
ORCID of Periodontology, 84(8), 1100–1110. https ://doi.org/10.1902/
jop.2012.120075
Jose A. Moreno Rodríguez https://orcid.org/0000-0002-0284-3496 Farina, R., Simonelli, A., Rizzi, A., Pramstraller, M., Cucchi, A., &
Trombelli, L. (2013). Early postoperative healing follow‐ ing buccal
single flap approach to access intraosseous periodontal defects.
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Wikesjö, U. M., Lim, W. H., Thomson, R. C., & Hardwick, W. R. (2003).
Caffesse RG. Supra‐alveolar attachment gain in the
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