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Clinical and Histological Evaluation of Socket Grafting Using Different Types

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DOI: 10.1097/ID.0000000000000106 · Source: PubMed

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 IMPLANT DENTISTRY / VOLUME 23, NUMBER 4 2014 489

Clinical and Histological Evaluation of

Socket Grafting Using Different Types of
Bone Substitute in Adult Patients
James Rudolph Collins, DDS,* Ely Jiménez, DDS,† Carol Martínez, DDS,† Rubén Tobias Polanco, DDS,‡
Ronaldo Hirata, DDS, MS, PhD,§ Ramy Mousa, MS,k Paulo G. Coelho, DDS, MS, BS, MSMtE, PhD,¶
Estevam A. Bonfante, DDS, MS, PhD,# and Nick Tovar, PhD**

fter the extraction of a tooth, Purpose: This clinical and his- immunogenic response, were observed.

A a significant amount of bone

loss occurs in the horizontal
and vertical dimensions, with the most
tological study evaluated the healing
of extraction sockets after implanta-
tion of a biphasic calcium sulfate
Histological findings showed a mean
new bone (NB) of 33% for sockets
filled with biphasic CS and 31% for
severe loss found in the horizontal (CS) alone or in combination with sockets filled with biphasic CS in
aspect of the alveolar bone.1–4 Such
a gamma-radiated human mineral- combination with allograft material.
bone loss hinders the placement of
dental implants and may render imme- ized allograft. There was no statistically significant
diate placement of dental implants Materials and Methods: Ten difference in the percentage of NB and
unpredictable. In attempt to assure pre- healthy adult patients participated the presence of soft tissue between
dictability, clinicians have been devel- in the study. A minimum of 2 teeth, graft materials.
oping protocols to ensure the success per patient, extracted for different Conclusion: Biphasic CS used
of an immediately placed implant after reasons were evaluated. Each alone or in combination with an
tooth extraction. socket was randomly filled to the allograft resulted in the same
Recent developments in immediate crest with either (a) a biphasic CS amount of NB formation in alveolar
implant placement protocols include or (b) large particulate gamma-radi- ridge preservation procedures.
*Professor and Director of Graduate Periodontics, Department
ated human mineralized allograft in (Implant Dent 2014;23:489–495)
of Periodontics, School of Dentistry, Pontificia Universidad
Católica Madre y Maestra (PUCMM), Santo Domingo,
combination with a biphasic CS. Key Words: graft, bone regen-
Dominican Republic.
†Resident, Department of Periodontology, Graduate School,
Results: No complications during eration, socket preservation,
Catholic University of Santo Domingo, Santo Domingo,
Dominican Republic.
reentry of the socket site during bone clinical
‡Professor and Director, Department of Prosthodontics,
Graduate School, Catholic University of Santo Domingo, Santo core retrieval, such as inflammation/
Domingo, Dominican Republic.
§Assistant Professor, Department of Biomaterials and Biomimetics,
New York University College of Dentistry, New York, NY.
kUndergraduate Student, New York University College of Dentistry,
New York, NY.
¶Associate Professor, Department of Biomaterials and
Biomimetics, New York University College of Dentistry, New York,
restoration in conjunction with subepi- after tooth extraction can prevent bone
NY; Director, Research Department of Periodontology and
Implant Dentistry, New York University College of Dentistry, New
thelial connective tissue grafting and resorption.5–9 Also, a study by Bersani
York, NY; Affiliated Faculty, Division of Engineering, New York
University Abu Dhabi, Abu Dhabi, United Arab Emirates.
bone grafting in the esthetic zone.5 In et al10 suggests that immediate place-
#Assistant Professor, Department of Prosthodontics, Bauru
College of Dentistry, University of São Paulo, Bauru, SP, Brazil.
a case series using this protocol, the ment may be an alternative for hopeless
**Adjunct Professor, Director, Material Analysis and Testing periimplant tissue response was evalu- molars. However, there are a vast num-
Laboratory, Department of Biomaterials and Biomimetics,
New York University College of Dentistry, New York, NY. ated, and results suggest that the facial ber of clinical situations when immedi-
Reprint requests and correspondence to: Estevam A. gingival level around single immedi- ate implant placement into extraction
Bonfante, DDS, MS, PhD, Department of ately placed implants can be maintained sockets is not recommended.11 They
Prosthodontics, Bauru School of Dentistry, University of
São Paulo, Alameda Octávio Pinheiro Brisola 9-75, after connective tissue grafting, proper include teeth with acute periapical
Bauru, São Paulo 17012-901, Brazil, Phone: 55(14) 3-dimensional implant positioning, and infection, preexisting periodontal dis-
3235-8904, Fax: 55 (14) 3234-2566, E-mail:
estevamab@gmail.com placement of bone graft into the ease, insufficient primary stability, and
implant-socket gap.4,5 Although a con- large dehiscence, especially in the
ISSN 1056-6163/14/02304-489
Implant Dentistry troversial topic, some clinical and esthetic zone where soft tissue profile
Volume 23  Number 4
Copyright © 2014 by Lippincott Williams & Wilkins in vivo studies have shown that imme- becomes critical.12 When immediate
DOI: 10.1097/ID.0000000000000106 diate implant placement procedures implant placement is not possible,
490 CLINICAL AND HISTOLOGICAL EVALUATION OF SOCKET GRAFTING  COLLINS ET AL

clinicians should consider the augmen- consistent properties, leading to pre- bone.37 In a clinical study using CS,
tation of the socket extraction.13,14 dictable outcomes, and can be manufac- histological analysis revealed the com-
Studies have shown that bone aug- tured in abundant quantities. One of the plete degradation of CS after 3 months,
mentation procedures with the use of first alloplasts used in dentistry was cal- which was replaced by newly formed
bone graft materials may prevent pro- cium sulfate (CS), which has shown bone.3,38
gressive bone resorption.15–18 Auto- osteoconductive properties.31 In vivo To date, it is still unclear which
genous bone graft is considered the studies using CS demonstrate alveolar alveolar ridge preservation technique is
gold standard in regenerative proce- ridge preservation techniques resulting the most predictable. The aim of this
dures because it fulfills the 3 basic in less contour reduction from the buc- clinical histological study was to eval-
requirements for bone regeneration: cal aspect when compared with unas- uate the effect of the combination of
osteogenesis, osteoinduction, and osteo- sisted socket healing.32–35 graft materials on NB formation during
conduction. Osteogenesis is the mecha- Allograft materials can be used in healing of extraction sockets after
nism of bone growth from osteoblasts. combination with CS to prevent allo- a period of 7 to 12 months. A biphasic
Osteoinduction involves inducing graft migration into the oral cavity. CS alloplast, alone or in combination
mesenchymal cells to differentiate into Toloue et al36 found that CS is as effec- with a gamma-radiated human mineral-
osteoblasts. Osteoconduction is the pro- tive as FDBA in preserving postextrac- ized allograft, was used.
cess that allows bone apposition from tion ridge dimensions in nonmolar
existing bone.19,20 Despite these 3 essen- extraction sites. The study showed an
tial properties, limitations involving increase in CS material degradation MATERIALS AND METHODS
autogenous bone grafting, such as the and new bone (NB) formation after Ten healthy adult patients (3 men
need for the second surgery, significant 3 months compared with FDBA alone and 7 women, ranging from 18 to
donor site morbidity, limitations in in these sites. In an in vivo rabbit tibia 61 years of age) were included in the
quantity, and the potential for complica- study, the microvessel density (MVD) study. Informed consent was obtained
tions,21,22 have led to the study of alter- was evaluated to determine angiogenic from all patients. Voluntary study
native materials. potential using CS versus autogenous candidates reported to the clinical
Alternative bone grafting materials bone and concluded that there is a highly facility at the Graduate School of the
include xenografts, allografts, and allo- significant increase in MVD in defects Catholic University of Santo Domingo.
plasts. These biocompatible and readily treated with CS after 4 weeks compared Potential subjects, who have completed
available materials have been success- with defects treated with autogenous the informed consent process, including
fully used with membrane barriers for
the augmentation of bone after tooth
extraction.23–27 Xenografts are taken
from another species and can cause an
immune response. Previous studies
have used a bovine xenograft to pre-
serve ridge dimensions with varied suc-
cess.28,29 Allografts are taken from the
same species but can potentially trans-
mit disease. They can be processed in
various methods as freeze-dried allog-
rafts (FDBA), demineralized allograft
(DFDBA) putties, and irradiated can-
cellous bone. Results may vary depend-
ing on allograft type as shown by
Piattelli et al,30 in which the differences
between FDBA and DFDBA were
studied. FDBA resorption process is
scarce, and cells with acid phosphatase
were not found, whereas with DFDBA,
the resorption process is present, and
cells were positive for acid phospha-
tase. In FDBA, the particles furthest
from the host bone were lined with Fig. 1. A, Occlusal aspect before extraction, showing extensive decay of incisors. B, After
newly developed bone, whereas the mucoperiosteal flap elevation, the buccal wall can be seen. Note the interproximal caries on
#7, 8, 9, and 10. C, Extracted roots of teeth #7, 8, 9, and 10. D, A periosteal relieving incision
DFDBA particles were located far from is made to the base of the buccal flap with a no. 15c blade. E, The buccal flap is displaced
the host bone and composed of scarce coronally without tension to evaluate flap margin approximation. F, BB graft was injected into
extracellular matrix. Alloplasts are syn- the socket of #9 to the level of the crest and on #8, a combination of BB + allograft was used.
thetic materials manufactured to have
 IMPLANT DENTISTRY / VOLUME 23, NUMBER 4 2014 491

the medical history, were screened filled up to the crest of the alveolus with a Reentry Procedure
by the dental examiner to identify synthetic biphasic CS (BondBone [BB]; After a minimum of 7 months and
those who were eligible for the study. MIS Implants Technologies, Shlomi, maximum of 12 months, patients were
The initial screening procedure Israel) and (b) One socket was filled administered local anesthesia (2% of
consists of a soft tissue assessment with a gamma-radiated human mineral- lidocaine, DFL, with epinephrine).
before proceeding with study eligi- ized allograft of large particles (Puros; Crestal and intrasulcular incisions were
bility evaluations. Zimmer Dental, Tutogen Medical US made to expose bone, and a special
Inc., Centerpulse, Carlsbad, CA) in trephine (2 3 7 mm) was used to take
Initial Examination
combination with BB (1:1). Decortical- a core of bone from 9 patients (Fig. 2, A
Eligible patients were registered for
ization of the bone was made for an and B). One patient did not return for
an initial visit. The first 10 patients who
increase in blood supply, and soft tissue treatment and could not be contacted.
completed all the inclusion criteria were
management was performed to obtain After the samples were retrieved,
invited to participate in the study. Sub-
closure of the alveolus. To minimize loss each patient received 2 endosseous
jects had to be in good general health,
of the FDBA particles, a thin layer of dental implants of various diameter
without periodontal disease, a minimum
CS was used at the most coronal aspect and lengths (Seven Internal Hex; MIS
of 2 teeth that were anterior to the
of the extraction site. Primary closure Implants Technologies) (Fig. 2, C
third molars, and had to be extracted for
was obtained with simple sutures. No and D). The same type of implant
different reasons, such as extensive
absorbable collagen wound dressing or surgical procedure was performed for
caries and root fracture (Fig. 1, A). A
barrier membrane was placed (Fig. 1, E all surgeries under local anesthesia.
radiographic and written refer report
and F), and photographs were taken with Full-thickness flaps were elevated,
indicating the reason for the extraction
the patient’s approval. Radiographic and osteotomies made, and implants placed.
had to be provided. Qualified subjects
clinical follow-up were made at the time Sutures were removed after 7 days.
were provided with an initial prophy-
of socket preservation at 1-, 3-, 6-, and After the bone core was obtained,
laxis in the Department of Periodon-
12-month time points. they were fixed in a 10% of buffered
tology. All patients were nonsmokers
formaldehyde solution and were then
and had no known allergies to the bio-
Postoperative Care referred for histological processing.
materials used in this study. Before
All patients received the same The bone core samples were then
extraction, only scenarios presenting
written postoperative treatment and placed in a series of alcohol solution
a minimum of 3 socket walls and #3 mm
indication care: local spray of 0.12% ranging from 70% to 100% for the
buccal bone loss were considered.
of chlorhexidine 3 times daily for purpose of dehydration. The samples
Surgical Procedure 14 days, amoxicillin and clavulanic were infiltrated and finally embedded
Ten patients with 2 alveolus each acid (875 and 125 mg, respectively) using a methacrylate-based resin (Tech-
(20 in total) requiring teeth extraction every 12 hours for 7 days. Also, 25 mg novit 9100; Heraeus Kulzer GmbH,
followed by socket grafting for ridge of dexketoprofen 3 times daily for Wehrheim, Germany). The polymerized
preservation received the treatment. 3 days was administered as an analge- blocks were then cut into slices (approx-
The extraction was carefully performed sic. Patients returned after 7 days for imately 150 mm thickness) with a preci-
with local anesthesia in an atraumatic a postoperative examination and suture sion diamond saw (Isomet 2000;
procedure, and when necessary, a resec- removal and were seen every 2 weeks Buehler Ltd., Lake Bluff, IL), glued to
tive radicular surgery was indicated in until soft tissue was closed. acrylic plates with an acrylate-based
multiradicular teeth to preserve bone
(Fig. 1, B–D). Also, depending on the
patient needs, a mucoperiosteal flap
was elevated. After tooth extraction,
the integrity of the 4 walls of the socket
and buccal plate measuring #3 mm
from the gingival margin were verified
clinically by a North Carolina probe.
The extracted teeth included 3 maxil-
lary incisors, 1 mandibular incisor,
2 mandibular canines, 3 maxillary can-
ines, 5 maxillary molars, and 4 man-
dibular molars. Tissue debris was
eliminated from the alveolus, and the
bone graft was hydrated after the man-
ufacturer’s instructions.
Fig. 2. A, Eleven months after surgery. B, Trephine biopsy removal. C, Implant osteotomies
Each of the 20 sockets, 2 per sub- and their parallelism on #7 and 10. C and D, A fixture (13 3 3.75 mm) is placed on #7 and 10
ject, were assigned randomly to one of with their respective healing abutments and sutured flap.
the 2 treatments: (a) One socket was
492 CLINICAL AND HISTOLOGICAL EVALUATION OF SOCKET GRAFTING  COLLINS ET AL

cement (Technovit 7210 VLC; Heraeus encapsulation found surrounding bulk Puros sites (Fig. 4, B). There were also
Kulzer GmbH), and after a 24-hour amounts of CS. The percent of bone, no significant differences found when
setting time, ground and polished to remaining grafting material, and soft comparing the percentage amount of
a final thickness of approximately 100 tissue quantified by histomorphometry soft tissue (P ¼ 0.38) and percentage
mm by means of a series of SiC abrasive are presented in Figure 4, A. Histolog- of graft material (P ¼ 0.06) (Fig. 4, C
papers (280, 400, 800, and 1200 grit) ical findings showed no significant dif- and D). Although not significant, an
(Buehler Ltd.) using a grinding/polishing ferences (P ¼ 0.7) in the mean NB: increased amount of combination of
machine (Metaserv 3000; Buehler Ltd.) 33 6 9% in the BB socket sites and a BB and Puros grafting components is
under water irrigation.39–41 A 1-mm poli- mean of NB of 31 6 19% in the BB + found relative to BB alone.
shing compound was used to remove
residual scratches. A Stevenel blue and
Van Gieson picro fuchsin differential tis-
sue stain (SVG) was used for staining the
sections. SVG stains soft tissue green-
blue and mineralized tissue red-orange,
whereas graft material will stain a
brown-black. The stained sections
were scanned to digital format using
a histology slide scanning system
(Aperio Technologies, Vista, CA).
Bone, soft tissue, and graft material
are then coded using specific colors
through Photoshop software (Adobe,
San Jose, CA). QWin software (Leica
Microsystems Inc., Buffalo Grove,
IL) is then used to quantify percent-
age values based on specified colors
with precise results with mega pixel
accuracy.

RESULTS
All surgical procedures were
uneventful, and there were no compli-
cations during the healing period for all
patients. Observations showed no signs
of infection in either connective tissue or
bone in proximity of the surgical sites for
all time points. One patient was excluded
from the study because he failed to
return to the follow-up appointments
for unknown reasons. The remaining
9 patients were compliant and during
the initial follow-up no complications or
infection were observed during reentry
surgery for histological sample retrieval.
The histological results for the dif-
ferent groups are presented in Figure 3.
From a healing morphology standpoint,
a similar healing pattern was observed for
both groups, with new vital bone found
directly interfacing with the graft materi-
als. Woven bone was observed through- Fig. 3. A, Bone core with new vital bone and BB (*) observed in a bluish-greyish color.
out the bone core, interfacing directly B, Bone core with new vital bone and BB (*) and Puros (+), the latter appearing in a reddish
color. Note the similar healing pattern depicted in both micrographs, with new vital bone
with the allograft material. Blood vessels interfacing the graft materials, and woven bone present throughout the bone core, interfacing
were observed forming within the allo- directly with the allograft material. Blood vessels can be observed within the allograft material
graft material and throughout the bone and throughout the bone core. Thin sections were stained with SVG.
core. There was slight immunogenic
 IMPLANT DENTISTRY / VOLUME 23, NUMBER 4 2014 493

tooth extraction. Histological analysis

of the bone core revealed nonvital spi-
cules of mature calcified bone with
a highly organized matrix surrounded
by viable noncalcified immature bone
matrix or osteoid. Our study showed
a similar viable bone matrix in the pres-
ence of the allograft.
It has been demonstrated that rem-
nants of CS are completely reabsorbed
and replaced by newly formed bone
from 3 to 6 months of socket preserva-
tion procedure, which is important if
implant placement is planned.38,43–45 In
this study, the BB-treated socket sites
showed a small amount of residual
material remaining, 7%, whereas the
BB + FDBA–treated socket showed
a 21% of residual material at postex-
traction evaluation. This difference in
Fig. 4. A, Percentage of vital bone, residual graft material (BB or BB + Puros mix), and soft degradation is an important quality to
tissue. B, Percentage of new vital bone. C, Percentage of soft tissue. D, Percentage of
residual graft particles.
consider when planning the time in
which an implant is to be placed. It
may be possible to tune the resorption
time of graft materials by combining
DISCUSSION material alone. An increased amount of
them in varying quantities based
degradation is also observed for the BB
This clinical study evaluated the on the implant placement treatment
alone versus the combination BB and
effect of using an alloplast CS bone plan.
Puros, namely 7% versus 21%, respec- Finally, postsurgical complica-
substitute, BB, alone or in combination
with a cortical gamma-radiated human tively. The combination of graft materi- tions associated with exposed mem-
bone mineralized allograft (Puros). The als, with their decreased degradation, is branes have been reported after socket
quality and amount of vital NB forma- evidently maintaining the space within preservation attempts.46,47 This study
tion, presence of soft tissue, and residual the defect site, preventing the penetra- used no membranes and used BB as
graft material remaining after socket tion of soft tissue (48%) compared with an initial barrier to prevent soft tissue
preservation between 7 and 12 months the BB alone (56%). ingrowth at early healing stages, and
in paired samples within the same The results of our study contradict no complications were noted.
patient were analyzed. Histological find- the study by Guarnieri et al3 who
ings showed no significant differences in studied the influence of CS hemihy-
the mean NB between BB socket sites drate on the histopathology pattern of CONCLUSION
and the combination BB + Puros. In intrasocket regenerated bone and eval- In this human histological study,
a previous study, 31 extraction sites uated histologically the effect CS has on biphasic CS used alone or in combina-
were selected to determine whether CS the extraction socket sites in 10 patients. tion with an allograft resulted in the
is as effective as FDBA in preserving Their study found a 58% of newly same amount of NB formation in alve-
postextraction ridge dimensions and formed bone and no residual graft after olar ridge preservation procedures. CS
to evaluate the amount of NB forma- 3 months of histological evaluation of alone had an increased resorption,
tion and remaining graft material after socket preservation with CS, whereas which may be an appropriate character-
3 months.36 Histological analysis re- our study found slightly more than istic if implants are to be placed shortly
vealed an average of 32% NB formation 30% of newly formed bone and up to after the grafting procedure. However,
in the CS group, which is similar to our 7% residual graft at greater time points. an increased amount of graft material in
findings, 33 6 9% in the BB socket. In another study, Froum et al26 re- combination with an allograft, and CS
When comparing their 16.7% of NB for- ported the percentage of vital bone may be needed if implant placement is
mation for the FDBA alone, we formation using bioactive glass and planned to occur after longer periods
observed that the BB + Puros mixture DFDBA of 59.5% and 32.4%, respec- after grafting procedure.
within our study gave us a similar NB tively, whereas in the control nongrafted
compared with the BB alone. It is possi- sockets, the amount was 34.7%.
ble that by combining these types of A recent 5-month clinical study by DISCLOSURE
grafts materials, there is an increased Minichetti et al42 used gamma-radiated The authors claim to have no
amount of NB than just an allograft human mineralized allograft alone after financial interest, either directly or
494 CLINICAL AND HISTOLOGICAL EVALUATION OF SOCKET GRAFTING  COLLINS ET AL

indirectly, in the products or informa- 10. Bersani E, Coppede AR, de Paula in implantology: A systematic review.
tion listed in the article. Pinto Prata HH. Immediate loading of im- Implant Dent. 2013;22:304–308.
plants placed in fresh extraction sockets in 24. Zitzmann NU, Schärer P, Marinello
the molar area with flapless and graftless CP, et al. Alveolar ridge augmentation with
ACKNOWLEDGMENTS procedures: A case series. Int J Periodon- Bio-Oss: A histologic study in humans. Int
tics Restorative Dent. 2010;30:291–299. J Periodontics Restorative Dent. 2001;21:
This study was partially supported 11. Koh RU, Rudek I, Wang HL. Imme- 288–295.
by MIS Implants Technologies, Shlomi diate implant placement: Positives and 25. Becker W, Clokie C, Sennerby L,
Israel. negatives. Implant Dent. 2010;19:98–108. et al. Histologic findings after implantation
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P, et al. Critical review of immediate als and titanium micro screws into extrac-
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