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 273

Evaluation of a Resorbable Collagen

Matrix Infused with rhPDGF-BB in
Peri-implant Soft Tissue Augmentation:
A Preliminary Report with 3.5 Years of
Observation

Massimo Simion, MD, DDS*/Isabella Rocchietta, DDS** The peri-implant soft tissues are
Filippo Fontana, DDS***/Claudia Dellavia, DDS**** critical when dealing with the ante-
rior maxilla because of the high es-
thetic demands and the challenge
Soft tissue augmentation around dental implants in the esthetic region remains a challenging of manipulating such tissues. Efforts
and unpredictable procedure. The ideal surgical technique would include of an off-the-shelf are constantly made to preserve the
product to minimize morbidity after autogenous grafting procedures. The aim of this study volume of these tissues around den-
was to use a resorbable collagen matrix (Mucograft) to serve as a scaffold to recombinant tal implants in the anterior maxilla.
human platelet-derived growth factor BB (rhPDGF-BB) to increase peri-implant soft tissue
The connective tissue graft1
volume in anterior maxillary sites. A total of six patients who had previously undergone
represents a viable and well-
a bone regeneration procedure were included in this study. The collagen matrix was
applied during stage-two surgery (expanded polytetrafluoroethylene membrane removal documented technique to supple-
and implant placement). Measurements were performed through customized stents by ment the thickness of the soft tissues
means of endodontic files, and at abutment connection, a soft tissue biopsy specimen was and can be applied for both single-
harvested for histologic examination. The healing period was uneventful in all six patients. stage and two-stage implants.2,3
Measurements were taken apically, centrally, and occlusally for each site. The mean gains
Moreover, the use of connective
in volume from baseline to the 4-month measurement at the apical, central, and occlusal
tissue improves the local metabolic
aspects were 0.87 ± 2.13 mm, 2.14 ± 3.27 mm, and 0.35 ± 3.20 mm, respectively.
The results showed a moderate increase in the soft tissue volume in esthetic peri-implant environment of the superficial soft
sites when applying a collagen matrix infused with rhPDGF-BB. However, the measuring tissues and preserves the keratin-
techniques available need to be further improved to record exact changes in the soft tissue ized tissue, obtaining satisfactory
volume. (Int J Periodontics Restorative Dent 2012;32:273–282.) peri-implant marginal sealing.4
Thus, optimal tissue conditioning
and a natural appearance of the
*Chairman, Department of Periodontology, Università degli studi di Milano, Fondazione prosthetic crown can be achieved.5
Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca’ Grande, Milano, Italy. However, this surgical tech-
**Researcher, Department of Periodontology, Università degli studi di Milano, Fondazione nique requires a donor site, with a
IRCCS Ca’ Grande, Milano, Italy.
***Researcher, Department of Implant Dentistry, Università degli studi di Milano,
consequent second surgical site. In
Fondazione IRCCS Ca’ Grande, Milano, Italy. addition to postoperative discom-
****Assistant Professor, Department of Human Morphology and Biomedical Science, fort for the patient, the volume of
Università degli Studi di Milano, Milano, Italy.
available connective tissue is clearly
Correspondence to: Dr Massimo Simion, Viale Tunisia 48, 20124 Milan, Italy; dependent on the host’s anatomical
email: msimion@studiosimion.it. limitations.

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274

In the past decade, attempts pletely replaced by healthy con- an optimal choice when treating
have been made to avoid autog- nective tissue in a 30-day period challenging soft tissue sites.14 The
enous soft tissue harvesting. Ma- when used under a soft tissue flap. aim of this study was to use a re-
terials primarily of allogenic origin The same porcine collagen matrix sorbable collagen matrix (Muco-
have been developed and used in (Mucograft) was recently investigat- graft) to serve as a scaffold to the
mucogingival surgery, beginning ed in patients with fixed prosthetic rhPDGF-BB to increase the peri-
in the late 1970s with freeze-dried restorations.12 The aim of that study implant soft tissue volume in the
skin allografts and later moving to- was to test this new collagen ma- anterior maxilla.
ward allogenic dermal substitutes trix in increasing the height of ke-
such as the acellular dermal matrix ratinized tissue compared to a free
graft (AlloDerm, Life Cell), origi- connective tissue graft. The results, Method and materials
nally developed for covering full- based on a total of 20 patients,
thickness burn wounds.6,7 reported the collagen matrix pro- A total of six patients were enrolled
The advent of tissue engineer- totype to be as effective as the tra- in this study. All patients had pre-
ing has recently introduced prod- ditional free connective tissue graft viously undergone bone regen-
ucts based on isolated cells or cell in gaining a band of keratinized eration in the maxilla by means of
substitutes, tissue-inducing sub- tissue adjacent to prosthetic recon- a titanium-reinforced expanded
stances (biologic mediators), and structions. An approximate 60% to polytetrafluoroethylene (e-PTFE)
scaffolds of natural or synthetic 70% degree of contraction was also membrane. Two patients had un-
origin.8 Materials such as human reported for both cohorts. dergone simultaneous implant
fibroblast–derived dermal sub- The current literature reports placement, and in four patients,
stitute have been investigated in various attempts to augment the the implants were placed at e-PTFE
clinical trials by applying them to oral soft tissues using numerous membrane removal. Collagen ma-
different clinical indications.9 materials; however, no ideal ma- trix (Mucograft) was applied during
A recent study by Wehrhan terial is currently available and, stage-two surgery, ie, when the e-
et al10 investigated the epitheli- most of all, predictable.13 In addi- PTFE membrane was removed.
alization, vascularization, scarring/ tion, most of these papers focus
fibrosis, and tissue integration of on mucogingival therapy around
a porcine collagen matrix (Muco- teeth, and very scarce data are Impressions and creation of a
graft prototype, Geistlich) in a der- provided on peri-implant soft tis- surgical stent
mal pig model. The authors reveal sue volume augmentation. Hence,
this type I/III collagen matrix to an alternative material that would Two weeks prior to baseline, an
be a plausible alternative to full- provide the adequate volume alginate impression of the maxilla
thickness dermal replacement sub- necessary for soft tissue aug- and mandible was taken to create a
stitute resulting from an identical mentation and avoid postsurgi- surgical stent. The acrylic resin was
epithelialization, vascularization, cal morbidity would be ideal for constructed with three metal tubes
and degradation as autogenous the purpose of improving peri- placed in predetermined positions
dermal grafts. implant esthetics in the maxillary for each dental implant site. The
Concordant results were re- region. tubes were positioned perpendicu-
ported in a preclinical study The well-known positive prop- lar to a line tangent to the two most
conducted in the porcine oral erties of recombinant human apical portions of the cemento-
cavity using an analogous ma- platelet-derived growth factor BB enamel junction (CEJ) of the mesial
trix.11 Results showed the matrix (rhPDGF-BB) in the wound-healing and distal teeth. The perpendicular
was safe, compatible, and com- cascade make this growth factor line corresponded to the center of

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 275

MGJ

Fig 1 Measurement points related to the adjacent teeth and muco- Fig 2 An edentulous anterior maxilla. Bone augmentation was
gingival junction (MGJ). needed to place dental implants.

each implant site. The first tube The stent was then removed care-
corresponded to the occlusal sur- fully with the file in place, and the
face, the second to the tangent line measurement from the apex of the
passing through the most apical file to the stop was marked. This
point of the adjacent CEJ, and the corresponded to the thickness of
third was in the buccal portion api- the soft tissue from the buccal epi-
cal to the mucogingival line (Fig 1). thelium to the bone crest.
A midcrestal incision was per-
formed extending intrasulcularly
Test procedure to the distal aspect of the two ad-
jacent teeth. A full-thickness buc-
Prior to the initiation of local anes- cal flap was elevated to expose the
thesia, the surgical stent was ap- bone crest covered by the titanium-
plied. The soft tissue thickness was reinforced e-PTFE membrane,
measured through an endodontic which was removed. Collagen ma-
25-µm-diameter file with a stop. trix was cut and adapted to the site.
The file was inserted in each of Prior to this, the matrix was infused
the three metal tubes of the stent, with rhPDGF-BB and placed buc-
and the stop corresponded to the cally and occlusally over the bone
epithelial portion of the soft tissue. crest (Figs 2 to 6).

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276

Fig 3 The bone crest appears atrophic with vertical and horizontal Fig 4 A titanium-reinforced e-PTFE membrane was securely
defects. Three tenting screws were inserted to sustain the particu- adapted and fashioned to the deficient bone crest by means of
late graft and the overlying membrane. palatal and vestibular fixation screws. A particulate graft comprising
autogenous graft and deproteinized bovine bone in a 1:1 ratio was
compacted underneath the barrier membrane.

Fig 5 Six months after augmentation surgery, the site was re- Fig 6 rhPDGF-BB–infused collagen matrix adapted to the site and
opened. Note the sufficient volume of alveolar bone. The e-PTFE placed over the bone crest and implants.
membrane was removed, and three dental implants were placed in
the newly regenerated bone.

The flaps were closed using in- prosthesis, the apical measure- to 100%) and xylol for 12 hours, and
ternal horizontal mattress sutures ments were the only data that embedded in paraffin (Paraplast
prior to interrupted sutures to ensure could be reported. Plus, Bioptica). Those samples har-
primary passive closure of the tissue. vested from sites with underlying
Sutures were removed at 14 days, bone regeneration contained some
and measurements were recorded Histologic processing remnants of the bone substitute
at baseline, 14 days, and 1 and 4 and needed a decalcification proce-
months. At the 4-month follow-up, All specimens were immediately dure before immersion. Therefore,
a soft tissue biopsy was performed fixed in 4% formalin/0.1 mol/L the partially mineralized specimens
(Figs 7 to 11). phosphate-buffered saline (pH, 7.4) were decalcified for 30 days with a
Long-term data were recorded for 24 hours at room temperature, solution containing sodium citrate
3.5 years from baseline. Because routinely dehydrated in increasing (250 g in 125 mL distilled/purified
of the presence of the definitive concentrations of ethanol (from 70% water) and formic acid (625 mL in

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 277

Fig 7 Anterior maxilla 4 months after implant and collagen matrix Fig 8 After 4 months, healing abutments were connected and a
placement. The tissues appear voluminous, healthy, and esthetically punch biopsy performed. Note the thickness of the healed soft tis-
satisfying. No scar tissue is present. sue and the length of the transmucosal portion.

625 mL distilled/purified water) healing of connective tissue graft

prior to dehydration. After radio- procedures. By 2 weeks, the wound
graphic assessment of the decal- exhibited minimal color alteration
cification, specimens were rinsed with reduced edema and erythe-
with running water for 48 hours ma. These characteristics progres-
and processed as soft tissue biop- sively disappeared during the first
sy specimens. Serial sections were month. At 4 months, the gingival
obtained at 4 to 5 µm and stained color, texture, and contour of the
with freshly made hematoxylin- treated areas appeared essentially
eosin to evaluate the tissue mor- identical to the adjacent soft tis-
phology. The sections were viewed sues, and minimal scarring was only
and photographed using a Nikon sometimes noticeable in the alveo-
light microscope (Eclipse E600) lar mucosa (Figs 7 and 8).
equipped with a calibrated digital Results of the measurements
camera (DXM1200, Nikon). performed throughout the heal-
ing period are reported in Table 1.
Because of the limited number of
Results samples, only a descriptive statis-
tical analysis was performed. One
Clinical outcomes patient withdrew before the 3.5-
year follow-up because she moved
The healing period was uneventful to another country.
in all six patients. No evidence of At the apical site, the mean
serious adverse local or systemic soft tissue depth was 3.41 ± 1.93
side effects was observed in any mm at baseline. The mean value in-
patient where the resorbable col- creased at 14 days (6.13 ± 2.81 mm)
lagen matrix was used in associa- and 1 month (6.47 ± 2.40 mm),
tion with rhPDGF-BB. Healing of but then decreased at 4 months
each site progressed as normal for (4.86 ± 2.05 mm). After 3.5 years,

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278

Table 1 Mean soft tissue thickness at the apical, central, and occlusal sites (mm)

Baseline 14 d 1 mo 4 mo 3.5 y
Apical 3.41 6.13 6.47 4.86 4.30
Central 3.91 5.94 6.34 6.07 –
Occlusal 5.04 7.53 6.56 5.57 –

Fig 9 Soft tissue biopsy specimen harvested at healing abutment Fig 10 Surgical stent in place. An endodontic file with a stop was
connection for histologic analysis. Note the thickness of the core. used to measure the thickness of the buccal soft tissues.

7.00
6.00
Soft tissue (mm)

5.00
4.00
3.00
2.00
1.00
0.00
Baseline 14 d 1 mo 4 mo 3.5 y

Fig 11 Definitive prosthetic rehabilitation. Fig 12 Mean soft tissue depth at the apical site at baseline,
14 days, 1 and 4 months, and 3.5 years.

the mean soft tissue depth was at 1 month. The mean gain at
4.30 ± 2.13 mm, resulting in a the last follow-up (4 months) was
mean gain of 0.87 ± 2.13 mm from 2.14 ± 3.27 mm. At the occlusal
baseline (Fig 12). At the central site, the mean value changed from
site, the mean soft tissue depth 5.04 ± 2.25 mm at baseline to
varied from 3.91 mm at baseline to 5.57 ± 2.23 mm at 4 months, for a
5.94 mm at 14 days and 6.34 mm mean gain of 0.35 ± 3.20 mm.

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 279

Fig 13 (left) Histologic section stained with hematoxylin-eosin 4

months from baseline. The global architecture of the soft tissues
resembles healthy normal mucosa (magnification ×25).

Fig 14 (below) Microphotograph of the oral epithelium and

underlying connective tissue in the same specimen as that in Fig 13
showing a normal keratinocyte stratification and a well-organized
three-dimensional distribution of collagen fiber bundles (magnifica-
tion ×100).

Histologic outcomes found alternate to connective papil-

lae of different dimensions (Fig 14).
After 4 months of healing, all sam- The lamina propria consisted of
ples showed complete resorption dense connective tissue rich in
of the collagen matrix. No areas blood vessels and collagen fiber
of necrosis, tissue degeneration, bundles running in all directions.
or inflammatory infiltrate were In the samples obtained from
present. The architecture of the bone-regenerated sites, several
regenerated soft tissue appeared xenograft particles were found in
similar to the healthy gingival mucosa the deeper portion of the biopsy
(Fig 13). specimens. The xenograft particles
A stratified squamous parake- that were present in the biopsy
ratinized epithelium with differen- specimens resulted from the previ-
tiating keratinocytes was observed. ous regeneration procedure. Those
In the epithelial layers, no signs of remnants were encapsulated in ei-
acanthosis were detectable. At the ther fibrous connective tissue or
epithelium–connective tissue inter- newly formed woven bone without
face, normal epithelial crests were grafted vs host reactions.

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280

Discussion Collagen matrix has been

shown to reabsorb quite rapidly,
An ideal implant-supported pros- with a 30-day timeframe in ani-
thetic rehabilitation in the anterior mal studies11 and 4 months in this
maxilla should mimic the natural study. It must be noted, though,
dentition as much as possible. This that the 4-month timeframe was se-
implies an adequate volume of lected to perform a biopsy; hence,
healthy soft tissue contour. Howev- the authors are unaware of whether
er, in the most challenging clinical the collagen matrix might have re-
conditions, significant bone loss is absorbed at an earlier time point.
most frequently accompanied by a This implies that collagen matrix
major loss of the soft tissue, which alone may increase the soft tissue
creates a difficult starting point for volume over a short period of time
an excellent esthetic result. until it reabsorbs completely.
Given the need of augment- The combination of rhPDGF-
ing the soft tissues around dental BB with resorbable collagen ma-
implants, especially if placed in the trix may dramatically increase the
anterior maxilla, an “off-the-shelf” number of fibroblasts in situ, with a
product would be ideal to avoid au- consequent soft tissue augmenta-
togenous tissue grafts. The aim of tion that remains stable over a long
this study was to combine two key period of time.
elements to follow this rationale: a The authors do not have any
chemically crossed-linked resorb- clinical evidence of whether the
able collagen matrix that would collagen matrix alone could help a
serve as a scaffold (Mucograft) and soft tissue augmentation to remain
a potent growth factor (rhPDGF- stable over time around dental im-
BB). The latter has the capability plants. Further studies are needed
of attracting a significant number to determine this.
of fibroblasts as a result of its high The results of this study were
chemiotactic, angiogenetic, and reported over short- and long-term
mitogenic characteristics.15 follow-ups. The apical measure-
A recent study conducted on ment was the only one that could
an animal model11 showed no ad- be taken after 3.5 years because of
verse reactions when the collagen the presence of the definitive pros-
matrix (Mucograft) was applied to thetic restoration, which impeded
the oral soft tissues in a submerged the measurements of the central
technique and an open wound en- and occlusal portions. The apical
vironment. This was confirmed in site showed a mean increase in soft
the present study in that optimal tissue volume of 0.87 ± 2.13 mm
integration of the collagen matrix after 3.5 years. The mean gains at
into the surrounding soft tissue was the short-term follow-up (4 months)
observed since no soft tissue com- for the central and occlusal por-
plications occurred throughout the tions were 2.14 ± 3.27 mm and
entire study period. 0.35 ± 3.20 mm, respectively. These

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 281

results were difficult to compare to measurements was applied. These register the volume changes using
the mean gain in thickness of an aspects influence and limit clinical a three-dimensional camera and
autogenous subepithelial connec- applicability. composed into one digital image
tive tissue graft (SCTG) because The measurements performed by computer-aided design/comput-
of a lack of data and information in this study were also subject to a er-assisted manufacture software.
on assessment methodology. It degree of error. Even though each A defined region of interest was
must be noted that no reliable patient had a customized measure- measured in all sites, and the vol-
human data on soft tissue thick- ment stent and the measurements ume differences between the time
ness gain using the treatment of were performed by the same clini- points were calculated.
choice (SCTG) are reported in the cian, the readings were performed This technique was derived
literature; hence, the authors do using endodontic files adjacent to from earlier studies that developed
not have any landmark values. a periodontal probe. Therefore, optical three-dimensional systems
To obtain this information, both a values were recorded to the near- to capture information about tooth
positive and negative control could est 0.5 mm. A more sophisticated preparations and the surrounding
have been included in this study. method of measurement would be soft tissues.19–21 The same method
In a recent systematic review, ideal, possibly using ultrasounds. has been used to measure dimen-
the dental literature was searched Also, a significant degree of error sional changes of the ridge con-
for techniques and materials to may be applied when inserting the tour in a preclinical study22 and to
augment soft tissue around dental file in the soft tissues resulting from document volumetric soft tissue
implants and teeth.13 With respect potential flexibility of the file itself. changes of the interdental papilla23
to soft tissue volume augmenta- Another study reported soft tissue and the buccal mucosal contour
tion, only a limited number of stud- shrinkage/augmentation measured at dental implants.24 Nevertheless,
ies have been identified, rendering using a periodontal probe. How- this technique measures the entire
a weak level of evidence. One study ever, those measurements may not volume, including the hard and soft
was designed solely as a compara- reflect changes of the entire aug- tissues. It does not distinguish be-
tive cohort study.16 The greatest mented volume.17 tween the bone and overlying soft
amount of soft tissue volume was Recently, a new method has tissues; hence, a potential increase
observed for the SCTG, with sig- been described to measure soft in hard tissue volume resulting from
nificant differences when com- tissue volume.18 An animal study the young age of the animals test-
pared to the control groups (free tested whether soft tissue augmen- ed or a hard tissue shrinkage result-
gingival grafts, untreated sites). tation with a newly developed col- ing from the surgery itself may alter
However, these sites were subject lagen matrix led to volume gain the overall results slightly.
to a significant loss of volume. No in alveolar ridge defects similar to Thoma et al18 reported no sta-
comparative studies were found those obtained by an autogenous tistically significant differences in
using allogenic devices instead of SCTG. The canine mandibular soft mean volume between the collagen
autogenous tissue for volumetric tissues were incremented by posi- matrix and SCTG at 28 and 48 days
augmentation. tioning a double-folded collagen (P > .10). These results showed that
The major reason for the lack matrix (Mucograft) in a submerged the SCTG may be potentially sub-
of data available is the absence of technique, an autogenous SCTG, or stituted by the Mucograft matrix
standardized reliable techniques a sham-operated site as a control. when soft tissue augmentation is
for the measurement of soft tis- Changes in soft tissue volume were needed. This was confirmed by the
sue volume. In the aforementioned assessed by creating master casts similar results in this study, where
study,16 a time-consuming and ex- at baseline and 28 and 48 days. the combination of collagen matrix
pensive procedure based on cast The latter were optically scanned to and rhPDGF-BB could possibly be

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282

used as a replacement for an SCTG 4. Grunder U, Spielman HP, Gaberthuel T. 15. Nevins M, Lynch SE, Cappetta EG.
Implant-supported single tooth replace- Treatment of advanced periodontal
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191–199. 6 months of treatment. J Periodontol
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lograft dermal matrix (AlloDerm) in the 18. Thoma DS, Jung RE, Schneider D, et
showed that the combination of
management of full-thickness burns. al. Soft tissue volume augmentation by
a resorbable collagen matrix and Burns 1995;21:243–248. the use of collagen-based matrices: A
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