79

Regional Accelerated Phenomenon in

the Mandible Following Mucoperiosteal
Flap Surgery
Avinoam Yaffe, *
Nachum Fine,f and Itzhak Binderman*

Striking remodeling activity occurs adjacent to the site of injury in orthopedic

surgery. This reaction has been described as regional accelerated phenomenon (RAP),
as it speeds up the healing stage. The phenomenon is a transient burst of localized
remodeling process following surgical wounding of cortical bone. We explored whether
RAP occurs following mucoperiosteal flap surgery in the jaw bone. Mucoperiosteal flaps
were performed on 60 Wistar rats, either only on the buccal aspect or both on buccal
and lingual aspects of the mandible. The surgical procedure lasted an average of 30
seconds and the flap was readapted without sutures. The rats were sacrificed at 3, 7, 10,
14, 21, and 120 days. High resolution x-ray microradiography of 1 to 1.5 mm thick
ground sections between premolar and molar regions of the mandible were analyzed and
revealed large areas of radiolucency which correlated to massive résorption of the alveolar
bone, as well as areas in the bone proper. The RAP was observed as early as 10 days
in the treated side group. Striking résorption of the cortical bone, both on the surface
and the bone proper, occurred on the periodontal aspect of the crestal bone leading to
widening of the periodontal ligament space, where a mucoperiosteal flap was performed
on the buccal aspect. The résorption was more prominent when a mucoperiosteal flap
was performed both on the lingual and buccal aspect. The alveolar bone recovered almost
to control levels 120 days after surgery. Both the histology sections and the microradi-
ographs in the mesio-distal direction demonstrated a typical RAP mechanism to potentiate
tissue healing, a phenomenon observed by orthopedists in long bone. It is this phenom-
enon that might be responsible for the increasing mobility immediately following peri-
odontal surgery. Also, bone dehiscences following periodontal surgery and open flap
curettage may occur when the bone in the area is thin. J Periodontol 1994; 65:79-83.
Key Words: Bone remodeling; surgical flaps; bone résorption.

Mucoperiosteal flaps in periodontal surgery are used for
debridement and pocket elimination in the management of
moderate and deep periodontal defects. This procedure gives
access to bone and root surfaces. During the dissective
process, the periosteum is usually separated from the bone
proper, particularly in the area of attached gingiva. Usually
a layer of lining cells remains, essentially on the bone sur-
face, and the rest of the fibrous connective tissue layer is
retained as part of the reflected flap.
The possibility that periodontal surgical procedures may
result in loss of alveolar bone has been of concern.18 Many
*Prosthodontic Department, Hebrew University Hadassah School of Den-
tal Medicine, Jerusalem, Israel.
fHard Tissue Laboratory, Tel Aviv-Elias Sourasky Medical Center, Tel
Aviv, Israel.
Hard Tissue Laboratory, Tel Aviv-Elias Sourasky Medical Center and
Oral Biology, The Maurice and Gabriela Goldschleger School of Dental
Medicine, Tel Aviv University, Tel Aviv, Israel.
reports show that periodontal surgery stimulates osteoclastic
activity with varying amounts of alveolar crest loss; this
has resulted in modifications of surgical technique to pro-
vide more protection for the alveolar bone as in partial
thickness flaps.4 Pfeifer6 investigated the reaction of alveo-
lar bone to flap procedures, mucoperiosteal flap, and split
flap technique (periosteal retention). In both flap procedures
osteoclastic activity was observed. While in the mucoper-
iosteal flap, a considerable amount of osteoclastic activity
was evident along the whole length of alveolar bone, in the
split flap technique there was little evidence for osteoclastic
activity.6 Also, in both flap procedures osteoclastic activity
was observed along the periodontal ligament surface. Bone
loss has been assessed by a computer-assisted densitometer
image analysis.9'10 Resorptive activity as assessed by den-
sitometry was greater following periodontal surgery than
following scaling and root planing.9'10 The phenomenon of
bone loss due to surgical exposure is well documented.1"10
 J Periodontol
80 LOCALIZED REMODELING OF THE MANDIBLE FOLLOWING SURGERY January 1994

In orthopedic surgery, striking remodeling activity occurs

adjacent to the site of injury. Frost11,12 described this re-
action as regional accelerated phenomenon (RAP), which
speeds up the healing stage. The phenomenon is a transient
burst of localized remodeling process following surgical
wounding of cortical bone.13 It was suggested that osteo-
clasts which resorb bone and osteoblasts that form new bone
at each stage normally do not exist in sufficient numbers
to heal the bone following surgery.1113 The RAP effect
mainly occurred in long bones that recruits these cells.1113
The purpose of this study was to explore whether this
RAP phenomenon occurs following mucoperiosteal flap
procedures on mandible bone, and whether this phenome-
non can cause alveolar bone aberrations.

MATERIALS AND METHODS

The 60 Wistar rats used in this experiment were divided
into the following groups: group A, control, untreated (15);
Figure 1. High resolution microradiography of mandible cross sections
10 days after surgery. Mesio-distal x-ray direction. C control
E experimental. Thin arrow shows mandibular canal; small arrows point
=
—

group B, mucoperiosteal flap performed on the buccal as- to alveolar bone résorption on the periodontal aspect of the alveolar bone,

pect only (15); and group C, mucoperiosteal flap performed
on both the buccal and lingual aspects (15). The rats were
anesthetized prior to surgery using a mixture of 25 mg/kg
body weight of Ketalar§ and 42 mg/kg body weight of Xy-
lazine11 intraperitoneally (IP). The flap was elevated using
a special small periosteal elevator, and readapted immedi-
ately in place without sutures; the procedure lasted 20 to
40 seconds. The rats were fed a liquid diet for 24 hours
after surgery to avoid flap displacement. On examination
48 hours after surgery, the surgical site resembled the con-
tralateral side. The flap surgery was performed in the region
of premolars and molars of the right side of the mandible,
one quadrant per rat. The rats were sacrificed 7, 10, 14,
17, 21, and 120 days following the flap procedure.
In each group of rats the following parameters were ex-
amined and a separate group of rats was used for each type
of analysis. Group A: (34 rats) high resolution x-ray mi-
croradiography analysis of 1 to 1.5 mm thick ground sec-
tions between premolar and molar regions of the mandible
in a buccal-lingual direction (4 to 5 sections in each side
of the mandible) was performed 10, 21, and 120 days after
surgery. The x-ray analysis was performed in a mesio-distal
direction using a safety film in a Faxitron cabinet x-ray
system for 5 seconds and 20KVP. Group B: histology sec-
tions (6 rats) of the mandible in buccal lingual direction
were done 10 and 21 days following surgery. The sections
were prepared in the following manner: the mandible was
separated, fixed in 10% buffered formalin for 72 hours,
demineralized, stained for H&E and prepared for analysis.
Group C: 45Ca retention (20 rats) in the corresponding bone
plate of the rats injected IP, lmCi 2 weeks prior to surgery-
was performed 7, 10, 14, 17, and 21 days after surgery.
Accurate dissection of the regional bone proper at the
site of surgery and the corresponding controls was done.
§Malgene 1000 Rhone Merieux, Lyon, France.
'Rampun Bayer, Leverkusen, Germany.
leading to thinning of the buccal plate.
The bone was weighed and put in 5 ml of 0.5N HCl to
release the mineral. The 45Ca retention was counted using
a beta counter.
The 45Ca retention is expressed as counts per minute
(CPM) per mg of weight. The statistical test was done using
paired student / test, since each experimental site was com-
pared to the control site of the same animal.
RESULTS
The high resolution microradiography revealed large areas
of radiolucency which correlate to massive résorption of
the alveolar bone, as well as areas in the bone proper. This
phenomenon can be seen very clearly in a cross section x-
ray specimen made in the mesio-distal direction (Fig. 1).
The microradiographs used here make it possible to observe
detailed changes in the mineralized matrices, while the bucco-
lingual exposure shows practically no change (Fig. 2). The
RAP phenomenon was observed as early as 10 days in the
treated side of group (Fig. 1). RAP phenomenon after 3
weeks in group C is shown in Figure 3, where striking
résorption of the cortical bone, both on the surfaces as well
as in the bone proper, occurred on the periodontal aspect
of the crestal bone, leading to widening of the periodontal
ligament space. When the mucoperiosteal flap surgery was
performed both on the lingual and buccal aspect, the ré-
sorption was more prominent (group C, Fig. 3) than when
surgery was performed only on the buccal aspect (group
B). The résorption of the lingual alveolar plate was greater
than the buccal plate. This could be because of the greater
width of the buccal plate. When analyzing the sections at
different time intervals, the maximum résorption is seen 3
weeks following surgery. The alveolar bone recovered al-
most to control levels 120 days after surgery (Fig. 4).
 Volume 65
Number 1 YAFFE, FINE, BINDERMAN 81

Figure 2. High resolution microradiographs of whole mandibles. Bucco-

lingual conventional x-ray direction (C control; E experimental).
= =

The 45Ca retention assay (Table 1) in the corresponding

bone plates exhibited interesting findings. The 45Ca reten-
tion counts were less after 7 days in the experimental side
than in the untreated control side; similar retention rates
Figure 4. High resolution microradiographs of mandible cross sections.
Mesio-distal x-ray direction. A (top): experimental, 3 months following
surgery; and (bottom): control.

were obtained at 10 and 14 days. However the 45Ca in the

experimental site recovered to control values as early as 17
days after surgery (Table 1). The decrease in 45Ca retention
during the first 2 weeks after surgery possibly expresses the
fast release of mineral before the organic matrix is resorbed.
Interestingly, no difference in 45Ca retention is seen after
3 weeks, although severe bone loss is seen on the micro-
radiographs. It appears that the organic matrix is also de-
graded at this time period.
Table 1. 45Ca Retention* in the Alveolar Bone Following Surgery
Days Control Experimental E/C
7 132.5 ±5.4 103.6 ±5.9 0.78*
10 73.0 ±3.7 59.7±3.8 0.81*
14 31.0±2.9 25.2±3.3 0.81*
17 28.9 ±2.7 28.0 ±3.5 0.97
21 23.3 ±2.8 24.0 ±3.2 1.03
Figure 3. High resolution microradiographs of mandible cross sections. *45Ca cpm 103.
Mesio-distal direction (C control; E experimental). Three weeks fol-
= =
< 0.05, Student t test.
lowing surgery. Each number is mean ± S.E. of 6 rats.

82 LOCALIZED REMODELING OF THE MANDIBLE FOLLOWING SURGERY
Thehistological sections in Figure 5 show a very active
phase of alveolar bone résorption 10 days after surgery.
Increased Haversiian canals both on the periosteal and en-
dosteal aspects of cortical bone are seen (Fig. 5A). In the
higher magnification shown in Figure 5B, resorptive la-
cunae are prominent both on the periodontal ligament and
periosteal aspects of alveolar bone. (Fig. 5B). This picture
is a typical example of RAP in early stages after surgery.
DISCUSSION
In this study we evaluated the effect of full thickness flap
elevation on mandibular bone. Tissue healing after peri-
odontal flap procedures in humans has been monitored using
clinical probing and periapical radiographs.15'16 In the last
few years computer-assisted densitometric image analysis
has been used to identify quantitative changes in alveolar
bone density following periodontal surgery.9,10 Experimen-
tal studies in animals and humans have shown that résorp-
tion may be observed following alveolar bone exposure by
flap elevation.3'4 Researchers report that the amount of al-
veolar bone loss following periodontal surgery and flap pro-
cedures is clinically significant after full thickness flaps7'17
and insignificant with partial thickness flaps.6-18 It is im-
portant to note that the main parameter used clinically to
assess bone loss and the progression of periodontal disease
is regular x-ray radiography that is a summation of buccal
and lingual plates of bone. Bender and Seltzer14 found, that
in order to observe the periapical lesion, décalcification of
40% of the surrounding bone should occur and the cortical
plates must be affected. In our study the radiographs were
Figure 5. Histological section of the alveolar bone 10 days after surgery A (left): note the numerous résorption
lacunae (white arrows) (original magnification x210); B. (right): increased Haversian canals (black arrows);
(original magnification 420).
J Periodontol
January 1994
taken in a mesio-distal direction (Fig. 3) that revealed sig-
nificant damage, which could not be observed on regular
radiographs taken in the conventional buccal lingual direc-
tion (Fig. 2). We found that most of the resorptive activity
occurs during the first week (decrease of 22% in 45Ca re-
tention) (Table 1). It is tempting to speculate that the real
damage following periodontal surgery that involves flap
procedures is much greater and more extensive than is seen
on periapical radiographs. The time frame of 14 and 21
days used with the rats in our study is equivalent to 6 weeks
and 3 and 6 months in humans, respectively; the 120-day
period is comparable to a period of 2 plus years.
Both the histology sections and the microradiographs in
the mesio-distal direction demonstrated a typical RAP
mechanism to potentiate tissue healing, the phenomenon
observed by orthopedists in long bones.11'12 Normally, RAP
in humans begins within a few days of surgery, typically
peaks at 1 to 2 months, and may take 6 to more than 24
months to subside. During RAP, extensive regional intra-
cortical bone remodeling occurs, recruiting cellular activity
necessary for activation of the subsequent healing process.
The RAP occurs in more than 97% of bone injuries and is
essential for adequate healing. Of interest, inadequate RAP
seldom occurs in children or in healthy laboratory ani-
mals.12 Our study demonstrated that a similar RAP occurs
in cortical bone adjacent to teeth of rat mandible, following
elevation of a full thickness flap. It is important to note that
activation of RAP starts with accelerated resorptive activity
which will lead to further bone regeneration. However, lo-
cal factors such as infection,19"22 occlusal trauma,23"25 and
 Volume 65
Number 1
bone geometry may quantitatively affect the bone regen-
eration stage. It is this phenomenon that might be respon-
sible for the increasing mobility immediately following
periodontal surgery.23'24 Also bone dehiscences may occur
following periodontal surgery, and open flap curettage, when
the bone in the area is very thin. Roberts and colleagues
pointed out that RAP of jaw bone occurs after implant sur-
gery.26-27 It should be emphasized that this phenomenon
creates cortical bone porosity which recovers to normal after
one or more years. This loss of bone mass may cause mi-
crodamage of the bone plate under implant loading. In con-
clusion, this paper describes the occurrence of RAP after a
typical flap procedure. Using cross-section microradi-
ographs it emphasizes the extent of résorption activity in
the early phase which returns to normal if the template has
not been destroyed during surgery.
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Send reprint requests to: Dr. A Yaffe, Department of Prosthodontics,
Hebrew University Hadassah School of Dental Medicine, PO Box 1172
Jerusalem, Israel.
Accepted for publication July 27, 1993.