19433670, 2021, 2, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.19-0656, Wiley Online Library on [24/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Received: 17 November 2019 Revised: 9 April 2020 Accepted: 26 April 2020
DOI: 10.1002/JPER.19-0656
ORIGINAL ARTICLE
The vertical course of bone regeneration in maxillary sinus
floor augmentations: A histomorphometric analysis of
human biopsies
Florian Beck1,* Karoline Maria Reich2,3,* Stefan Lettner2,3 Patrick Heimel2,3
Stefan Tangl2,3 Heinz Redl3,4 Christian Ulm1
1 Division of Oral Surgery, University
Clinic of Dentistry, Medical University of Abstract
Vienna, Vienna, Austria Background: Maxillary sinus floor augmentation (MSFA) is a well-established
2 Karl Donath Laboratory for Hard Tissue
and predictable augmentation method in severely resorbed maxillae. However,
and Biomaterial Research, Division of
Oral Surgery, University Clinic of
data on the vertical course of bone graft consolidation within the maxillary sinus
Dentistry, Medical University of Vienna, are rare. The aim of the present study was to quantify the vertical distribution of
Vienna, Austria new bone formation (nBF) in MSFA and to characterize the vertical gradient of
3Austrian Cluster for Tissue
bone graft consolidation.
Regeneration, Vienna, Austria
4 Methods: Eighty-five human sinus biopsies were harvested 6 ± 1 months after
Ludwig Boltzmann Institute for
Experimental and Clinical Traumatology, MSFA. Histological thin-ground sections were prepared and histomorphometri-
AUVA Research Centre, Vienna, Austria cally analyzed. The volume of newly formed bone (nBV/TV) was measured in
Correspondence
serial zones of 100 μm proceeding from the bottom of the sinus floor (SF) up to
Dr. Florian Beck, Division of Oral Surgery, the apical top of the biopsy. The gradient of nBV/TV within the augmentation
University Clinic of Dentistry, Medical area was determined by the vertical distribution of nBV/TV along these zones.
University of Vienna, Sensengasse 2a, 1090
Vienna, Austria. Results: In the premolar region, nBV/TV slightly declined from 20.4% in the
Email: zone adjacent to the SF to 17.7% at a distance of 8 mm. The gradient was steeper
* Florian Beck and Karoline Maria Reich
in the molar region: nBV/TV decreased from 18.7% to 12.8%. This decline was
contributed equally to the authorship of even more distinct when the volume fraction and the height of the residual bone
this work and are considered joint first of the SF were low.
authors.
Conclusions: nBF follows a gradient from native bone of the SF towards the
apical part of the augmentation area. The distance to primordial bone thus plays
a critical role for bone regeneration in MSFA, particularly in the molar region.
KEYWORDS
bone regeneration, bone substitutes, histological analysis, maxillary sinus floor elevation
1 INTRODUCTION in the edentulous maxillary region.1,2 Besides a success-
ful surgical procedure, the decisive factor for augmenta-
The maxillary sinus floor augmentation (MSFA) is an tion success is the consolidation of the grafted material into
effective and predictable therapy to increase bone supply bone.
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.
© 2020 American Academy of Periodontology
J Periodontol. 2021;92:263–272. wileyonlinelibrary.com/journal/jper 263
, 19433670, 2021, 2, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.19-0656, Wiley Online Library on [24/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
264 BECK et al.
T A B L E 1 Number of biopsies with deproteinized bovine bone augmented area follows a gradient from the native bone
mineral and adjuncts of the SF towards the apical part of the augmented area
Bone graft materials n % and the elevated SM. Unlike previous studies10,11,17,18 that
DBBM 7 8.2 investigated nBF in a few pre-defined discrete zones, we
DBBM + aB 44 51.8 herewith introduced a new method that allows describ-
DBBM + aBcells 15 17.7 ing the vertical distribution and extension of new bone
DBBM + aB + PC 14 16.4
continuously over the whole length of the biopsy.
DBBM + MSC 5 5.9
Total 85 100
2 MATERIALS AND METHODS
aB, autologous bone; aBcells, autologous bone cells; DBBM, deproteinized
bovine bone mineral; MSC, mesenchymal stem cells; PC, platelet concentrates.
Seven Medical Universities (Departments of Oral Surgery,
Department of Prosthodontics and Departments of Oral
Controversy exists in the literature regarding the tissue and Maxillofacial Surgery) from Austria (n = 2) and Ger-
from which bone regeneration originates in MSFA. Both, many (n = 5) provided biopsies of MSFA for a multicen-
the residual bone of the sinus floor (SF) and the Schneide- ter study of Reich et al.19 The present study investigates
rian membrane (SM) are discussed in this context:3‒6 the histologic material under a new scientific perspec-
Palma et al.7 performed MSFA in capuchin primates and tive which has not been studied to date. This study was
found de novo bone formation in contact with SM, indi- approved by the human subjects ethics board of Austria
cating an osteogenic potential of SM. This observation is and Germany [Austria: 102/2004, 22/2007, 18-053 ex 06/07;
in accordance with Srouji et al.8 and Rong et al.9 who Germany: 837.274.04 (4432)] and was conducted in accor-
studied the role of the SM in an ectopic tissue transplant dance with the Helsinki Declaration of 1975, as revised in
model in nude mice and in a sinus lifting model in canines. 2013.
Both reported that the SM appears to have osteogenic and
osteoinductive properties and thus might contribute to
bone formation in MSFA. 2.1 Eligibility criteria for recruitment
Jungner et al.4 by contrast could not detect any bone for-
mation originating from the SM in capuchin primates. In Patients destined for a two-stage approach of MSFA with
fact, the authors found new bone formation (nBF) sprout- a residual alveolar bone height (oldB.Ht) of the poste-
ing from the bottom of the SF, extending into the elevated rior maxilla of <5 mm, requiring at least one dental
area surrounding the implant. This is in line with Busen- implant (premolar or molar region) and aged >18 years
lechner et al.10 and Fuerst et al.11 who reported that in were enrolled. Exclusion criteria were recent tooth extrac-
mini-pigs, graft consolidation after MSFA largely depends tion at the site of implant installation (within the last
on the osteoinductive potential of the surrounding bone. A 3 to 18 months), periodontal disease, pathological con-
graft consolidation gradient was identified showing more ditions of the maxillary sinus, metabolic or degenera-
new bone in zones adjacent to the SF and less new bone in tive diseases of the bone (e.g., osteoporosis, diabetes mel-
the more distant zones. litus, hyperparathyroidism), long-term medication with
At present, clinical recommendations for MSFA mainly corticosteroids or NSAIDs, smoking (>5 cigarettes/day),
address the choice of surgical approach, single- versus two- and alcoholism. All patients provided written informed
stage procedure based on minimum requirements for the consent.
width and the height of the residual alveolar ridge.12,13
However, recommendations on the lifting height of the SM
and subsequently the augmentation height itself are rare 2.2 MSFA and sample processing
and usually only consider the possible installation of an
implant length of 12 to 13 mm.13‒16 The question whether MSFA procedures were performed following a lateral
a larger augmentation height actually results in a larger approach20,21 under local or general anaesthesia. After
graft consolidation height or whether excessive bone graft- window preparation and careful elevation of SM, the
ing might even be detrimental to successful graft consoli- grafting material was placed into the created void space.
dation remains open. Patients with obvious signs of inflammation, large SM per-
Based on this background, the aim of the present study forations or other complications were excluded from this
was to quantify the vertical distribution of nBF in human study.
sinus biopsies 6 months after MSFA by means of modern After a healing period of 6 ± 1 months, sinus biop-
histomorphometry. We hypothesized that nBF in the sies from the premolar and/or the molar region were
Received: 17 November 2019 Revised: 9 April 2020 Accepted: 26 April 2020
DOI: 10.1002/JPER.19-0656
ORIGINAL ARTICLE
The vertical course of bone regeneration in maxillary sinus
floor augmentations: A histomorphometric analysis of
human biopsies
Florian Beck1,* Karoline Maria Reich2,3,* Stefan Lettner2,3 Patrick Heimel2,3
Stefan Tangl2,3 Heinz Redl3,4 Christian Ulm1
1 Division of Oral Surgery, University
Clinic of Dentistry, Medical University of Abstract
Vienna, Vienna, Austria Background: Maxillary sinus floor augmentation (MSFA) is a well-established
2 Karl Donath Laboratory for Hard Tissue
and predictable augmentation method in severely resorbed maxillae. However,
and Biomaterial Research, Division of
Oral Surgery, University Clinic of
data on the vertical course of bone graft consolidation within the maxillary sinus
Dentistry, Medical University of Vienna, are rare. The aim of the present study was to quantify the vertical distribution of
Vienna, Austria new bone formation (nBF) in MSFA and to characterize the vertical gradient of
3Austrian Cluster for Tissue
bone graft consolidation.
Regeneration, Vienna, Austria
4 Methods: Eighty-five human sinus biopsies were harvested 6 ± 1 months after
Ludwig Boltzmann Institute for
Experimental and Clinical Traumatology, MSFA. Histological thin-ground sections were prepared and histomorphometri-
AUVA Research Centre, Vienna, Austria cally analyzed. The volume of newly formed bone (nBV/TV) was measured in
Correspondence
serial zones of 100 μm proceeding from the bottom of the sinus floor (SF) up to
Dr. Florian Beck, Division of Oral Surgery, the apical top of the biopsy. The gradient of nBV/TV within the augmentation
University Clinic of Dentistry, Medical area was determined by the vertical distribution of nBV/TV along these zones.
University of Vienna, Sensengasse 2a, 1090
Vienna, Austria. Results: In the premolar region, nBV/TV slightly declined from 20.4% in the
Email: zone adjacent to the SF to 17.7% at a distance of 8 mm. The gradient was steeper
* Florian Beck and Karoline Maria Reich
in the molar region: nBV/TV decreased from 18.7% to 12.8%. This decline was
contributed equally to the authorship of even more distinct when the volume fraction and the height of the residual bone
this work and are considered joint first of the SF were low.
authors.
Conclusions: nBF follows a gradient from native bone of the SF towards the
apical part of the augmentation area. The distance to primordial bone thus plays
a critical role for bone regeneration in MSFA, particularly in the molar region.
KEYWORDS
bone regeneration, bone substitutes, histological analysis, maxillary sinus floor elevation
1 INTRODUCTION in the edentulous maxillary region.1,2 Besides a success-
ful surgical procedure, the decisive factor for augmenta-
The maxillary sinus floor augmentation (MSFA) is an tion success is the consolidation of the grafted material into
effective and predictable therapy to increase bone supply bone.
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.
© 2020 American Academy of Periodontology
J Periodontol. 2021;92:263–272. wileyonlinelibrary.com/journal/jper 263
, 19433670, 2021, 2, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.19-0656, Wiley Online Library on [24/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
264 BECK et al.
T A B L E 1 Number of biopsies with deproteinized bovine bone augmented area follows a gradient from the native bone
mineral and adjuncts of the SF towards the apical part of the augmented area
Bone graft materials n % and the elevated SM. Unlike previous studies10,11,17,18 that
DBBM 7 8.2 investigated nBF in a few pre-defined discrete zones, we
DBBM + aB 44 51.8 herewith introduced a new method that allows describ-
DBBM + aBcells 15 17.7 ing the vertical distribution and extension of new bone
DBBM + aB + PC 14 16.4
continuously over the whole length of the biopsy.
DBBM + MSC 5 5.9
Total 85 100
2 MATERIALS AND METHODS
aB, autologous bone; aBcells, autologous bone cells; DBBM, deproteinized
bovine bone mineral; MSC, mesenchymal stem cells; PC, platelet concentrates.
Seven Medical Universities (Departments of Oral Surgery,
Department of Prosthodontics and Departments of Oral
Controversy exists in the literature regarding the tissue and Maxillofacial Surgery) from Austria (n = 2) and Ger-
from which bone regeneration originates in MSFA. Both, many (n = 5) provided biopsies of MSFA for a multicen-
the residual bone of the sinus floor (SF) and the Schneide- ter study of Reich et al.19 The present study investigates
rian membrane (SM) are discussed in this context:3‒6 the histologic material under a new scientific perspec-
Palma et al.7 performed MSFA in capuchin primates and tive which has not been studied to date. This study was
found de novo bone formation in contact with SM, indi- approved by the human subjects ethics board of Austria
cating an osteogenic potential of SM. This observation is and Germany [Austria: 102/2004, 22/2007, 18-053 ex 06/07;
in accordance with Srouji et al.8 and Rong et al.9 who Germany: 837.274.04 (4432)] and was conducted in accor-
studied the role of the SM in an ectopic tissue transplant dance with the Helsinki Declaration of 1975, as revised in
model in nude mice and in a sinus lifting model in canines. 2013.
Both reported that the SM appears to have osteogenic and
osteoinductive properties and thus might contribute to
bone formation in MSFA. 2.1 Eligibility criteria for recruitment
Jungner et al.4 by contrast could not detect any bone for-
mation originating from the SM in capuchin primates. In Patients destined for a two-stage approach of MSFA with
fact, the authors found new bone formation (nBF) sprout- a residual alveolar bone height (oldB.Ht) of the poste-
ing from the bottom of the SF, extending into the elevated rior maxilla of <5 mm, requiring at least one dental
area surrounding the implant. This is in line with Busen- implant (premolar or molar region) and aged >18 years
lechner et al.10 and Fuerst et al.11 who reported that in were enrolled. Exclusion criteria were recent tooth extrac-
mini-pigs, graft consolidation after MSFA largely depends tion at the site of implant installation (within the last
on the osteoinductive potential of the surrounding bone. A 3 to 18 months), periodontal disease, pathological con-
graft consolidation gradient was identified showing more ditions of the maxillary sinus, metabolic or degenera-
new bone in zones adjacent to the SF and less new bone in tive diseases of the bone (e.g., osteoporosis, diabetes mel-
the more distant zones. litus, hyperparathyroidism), long-term medication with
At present, clinical recommendations for MSFA mainly corticosteroids or NSAIDs, smoking (>5 cigarettes/day),
address the choice of surgical approach, single- versus two- and alcoholism. All patients provided written informed
stage procedure based on minimum requirements for the consent.
width and the height of the residual alveolar ridge.12,13
However, recommendations on the lifting height of the SM
and subsequently the augmentation height itself are rare 2.2 MSFA and sample processing
and usually only consider the possible installation of an
implant length of 12 to 13 mm.13‒16 The question whether MSFA procedures were performed following a lateral
a larger augmentation height actually results in a larger approach20,21 under local or general anaesthesia. After
graft consolidation height or whether excessive bone graft- window preparation and careful elevation of SM, the
ing might even be detrimental to successful graft consoli- grafting material was placed into the created void space.
dation remains open. Patients with obvious signs of inflammation, large SM per-
Based on this background, the aim of the present study forations or other complications were excluded from this
was to quantify the vertical distribution of nBF in human study.
sinus biopsies 6 months after MSFA by means of modern After a healing period of 6 ± 1 months, sinus biop-
histomorphometry. We hypothesized that nBF in the sies from the premolar and/or the molar region were
