1977 - Mormann - Blood Supply of Human Gingiva Following Periodontal Surgery A Fluorescein Angiographic Study

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Blood Supply of Human 
Gingiva Following 
Periodontal Surgery 
A Fluorescein Angiographic Study 
by 
WERNER MORMANN, D.M.D.* 
SEBASTIAN G . CIANCIO, D.D .s.† 
T H E VASCULAR supply of gingival tissues during and 
subsequent to periodontal surgery is critical to the 
healing of the tissue. Most studies of the blood supply 
of gingiva have been done in animals or on human 
cadavers, and have shown that the blood supply to the 
free and attached gingiva is derived mainly from the 
supraperiosteal vessels 1 2 while the periodontal liga­
ment is supplied by vessels perforating the alveolar 
bone proper. 3 K i n d l o v a 4 , 5 described anastomoses be­
tween vessels of the gingiva and periodontal ligament, 
though the capillaries were arranged differently in each 
of these two networks. In the normal periodontium of 
different laboratory animals, connections between gin­
gival and periodontal ligament vessels were seldom 
observed. 6 
The independence of the gingival and periodontal 
ligament blood supplies also has been demonstrated 
functionally. Occlusion of vessels in the periodontal 
ligament does not effect the blood supply of the 
gingiva 7 and occlusion of arterioles supplying the gin­
giva does not appear to alter the blood supply of the 
periodontal ligament. 8 However, in the latter study, 
the initial revascularization of the gingiva was derived 
from vessels of the periodontal ligament, thus demon­
strating a potential for extensive collateral circulation 
to the gingiva from the periodontal ligament. Garfun-
kel and Sciaky 9 have made a similar observation in 
describing the vasculature of the gingiva and periodon­
tal ligament. Kennedy 1 0 also showed that when specific 
needs arise a compensatory blood supply can be pro­
vided easily. 
The distribution pattern of the vessels in human 
jaws was studied by Hayashi 1 1 using carmine gelatin. 
He found a richer blood supply in the upper jaw, with 
more vascularization on the lingual periosteal aspects 
of both upper and lower jaws than the buccal, though 
the anterior teeth were an exception to this rule. 
Cohen 1 2 injected the same dye into the common carotid 
artery to study the vascular architecture of the cat 
mandible and demonstrated that the blood supply to 
the periodontal ligament emanates from three different 
sources; namely, alveolar bone, gingiva and apical 
arteries. 
Techniques to study gingival capillary architecture 
and function have been reviewed by Clemmesen 1 3 and 
Gehrke et a l . 1 4 Recently, a fluorescence vital micros­
copy method was used for repeated in vivo examination 
of vascular patterns in the buccal gingiva of cats and 
dogs . 1 5 , 1 6 
The use of fluorescein angiography to observe the 
blood circulation in healthy and inflamed gingiva in 
man was described by Mormann and Lu tz . 1 7 The 
method allowed successful evaluation of functional 
conditions in the gingival capillary bed. Sodium fluo­
rescein was selected to study the circulation in view of 
its widespread use in medicine. 1 8 The 5th edition of 
Goodman and Gilman's text 1 9 states that its diagnostic 
usefulness lies in its fluorescent properties and that 
untoward effects are minimal. When they do occur, 
they are limited to nausea and vomiting. Our experi­
ence with this agent resulted in only one patient 
experiencing mild nausea. 
The purpose of the present study was to use fluores­
cein angiography in humans in order to observe altera­
tions in gingival circulation following various modifica­
tions of mucogingival flap design. 
The rationale for this approach was to confirm, in 
humans, previous animal findings concerning pathways 
of gingival circulation as well as to provide additional 
information relative to current concepts of periodontal 
flap design. 
MATERIALS AND METHODS 
Injection Technique 
A l l patients received an intravenous injection of 2 
ml of 20% sodium fluorescein at 24 hours after the 
surgical procedure. Employing a rapid injection ante-
cubital venipuncture technique an adequate fluorescein 
concentration occurred during the first passage of the 
dye through the gingival vasculature. After 15 to 20 
seconds, the Na-fluorescein entered the gingival capil­
lary system. A n initial photographic sequence of 15 
exposures showed that the intracapillary phase of the 
fluorescein labeling occurred 15 seconds after the 
beginning of the injection. The fluorescein was then 
allowed to permeate through the vessel walls and to 
diffuse evenly into the gingival tissue. Additional pho­
tographs were taken 1, 3, 5 and 10 minutes after 
injection, to document postangiographic plasma fluid 
diffusion. 
Photographic Technique 
The principles of fluorescein angiography of the 
gingiva have been described p rev ious ly . 1 7 , 2 0 - 2 3 In this 
study a new photographic system was used (Fig. 1). 
* Department of Cariology and Periodontology, Dental Institute, 
University of Zurich, Zurich, Switzerland. 
† Department of Periodontology, School of Dentistry, State Uni­
versity of New York at Buffalo, 3435 Main St., Buffalo, N Y . 
681 
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682 Mormann, Ciancio 
J. Periodontol. 
November, 1977 
The system consisted of a Zeiss operating microscope 
with a newly constructed integral coaxial electron 
strobe light (720 W sec), an integral halogen pilot 
light (100 W) and a monitoring Zeiss power and 
electronic timer unit. Optimal harmonizing of the Zeiss 
emulsion (485 nm) and absorption (520 nm) filters 
provided fluorescein angiographs of high contrast. K o ­
dak Ektachrome High Speed film was used and proc­
essed at 800 A S A . 
Eight subjects with an age range of 20 to 50 (4 male 
and 4 female) were included in this study. A l l surgical 
procedures described were performed under local infil-
FIGURE 1. Z = Zeiss operating microscope, and 0 2 
separate optical systems, and M 2 motor driven cameras, F 
= focusing knob, H = height dial, HP = head positioner, 
WB = removable individual wax bite, LR = lip retractor, CS 
= chin support, ST = standardizing device. 
FIGURE 2. Schematic drawing of gingival blood supply and 
experimental dissection by a horizontal incision running in the 
facial attached gingiva extending to bone in Subject A and 
dissection of the gingivo-periodontal anastomosis incision in 
Subject B. 
FIGURE 3. Subject A. Angiograph 24 hours after full thickness horizontal incision running in attached gingiva of the lower 
anterior region indicated by thick vertical black arrows. Long white arrows show central anemia, short arrows show zones of 
partial blood supply by collateral circulation, clear zones: normal blood supply. 
683 Blood Supply of Human Gingiva 
Volume 48 
Number 11 
tration anesthesia (Xylocaine with 1:80,000 epineph­
rine). Silk sutures (5.0) were placed wherever a flap 
was raised. A l l flaps were covered with a periodontal 
dressing which was removed at the time of photogra­
phy. 
In subject A a horizontal incision extending to bone 
was made at the mucogingival junction in the area of 
the mandibular incisors. The purpose of this procedure 
was to determine the effect of dissecting the supraper-
iosteal gingival vessels at the mucogingival junction on 
gingival blood circulation coronal to the incision as 
shown in the schematic drawing (Fig. 2). 
In subject B an internal bevel incision extending to 
bone was made as shown in F ig . 2. This surgical 
procedure was carried out at two sites: The facial 
aspect of the mandibular right central incisor and the 
facial papilla between the mandibular left central and 
lateral incisors (Fig. 5). The purpose of this procedure 
was to determine the effect of dissecting the anasto­
mosis between the gingival and the periodontal vessels 
at the gingival margin. 
In subject C the incisions for a full thickness flap 
were made extending to bone in the mandibular right 
anterior region but the flap was not raised. Between 
the mandibular left incisors the same incisions were 
made and a labial full thickness replacedflap was 
raised (Fig. 7). The purpose of this experimental 
procedure was to evaluate the effect on circulation of 
raising a flap. 
In subject D two labial full thickness replaced flaps 
FIGURE 4. Subject A. Clinical aspect 48 hours after horizontal incision. Three areas of superficial necrosis coronal to horizontal 
incision (arrows). 
FIGURE 5. Subject B. Clinical view immediately after internally beveled incisions (IBI), BL = blood. 
684 Mörmann, Ciancio 
J. Periodontal. 
November, 1977 
were raised. Between the mandibular right incisors the 
vertical incisions extended to the mucogingival junc­
tion. Between the mandibular left incisors the vertical 
incisions were twice as long, extending beyond the 
mucogingival junction (Fig. 10). The purpose of this 
design was to determine the effect of the length of the 
incision and the ratio of length to width on gingival 
flap blood supply in replaced full thickness flaps. 
In subject E two labial laterally positioned flap 
procedures were performed to cover areas of recession 
over the mandibular right and left lateral incisors. 
Both flaps were prepared with an experimental flap 
design so that they were partial thickness in their 
coronal half and full thickness in their apical position 
(Fig. 13). Both flaps had approximately the same 
length but the base of the right flap (NF) was narrower 
than that of the left (BF) in terms of the relationship 
of flap base to length. This design allowed an evalua­
tion of the role of the width of the base/flap length. 
In subject F a laterally positioned flap was placed 
over an area of recession on the labial aspect of the 
maxillary left cuspid (Fig. 16). The coronal half of the 
flap was partial thickness and the apical half was full 
thickness. The flap was designed so that its base was 
less than ½ of its length. Flap mobilization was easy 
because of its length. The purpose of this design was 
to determine the effect on blood supply of overextend-
ing the length of a flap. 
FIGURE 6. Subject B. Angiograph 24 hours after internally bevelled incisions (IBI). 
FIGURE 7. Subject C. Clinical view 24 hours after surgery; vertical incisions as for a full thickness flap (I) and actual raised full 
thickness flap ( F F ) . 
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685 Blood Supply of Human Gingiva Volume 48 
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FIGURE 8. Subject C. Angiograph 24 hours after surgery showing disturbance of capillary blood supply (arrows) at incision sites 
(I) and in the area of the raised full thickness flap ( F F ) . 
FIGURE 9. Subject C, angiograph 96 hours after surgery showing still more areas of repair at raised and retracted full thickness 
flap ( F F , arrows). 
In subject G the same flap as that described for 
subjects E and F was positioned over an area of 
recession on the buccal of the maxillary right first 
premolar (Fig. 19). This flap differed from that for 
subject E in that its base lay in a zone of attached 
gingiva which had been widened by a free graft of 
palatal mucosa 3 months ago. Therefore this flap had 
less mobility than the others described. Consequently, 
in being laterally positioned the flap was bent with 
traction force needed to fix it to the recipient site. 
Tension was exerted by the sutures as they held the 
flap in place. With this design the combined effect of 
tension and flexion on the flap's blood circulation 
could be evaluated. 
RESULTS 
Subject A 
The horizontal incision in subject A was evaluated 
24 hours after it was made (Fig. 3). A t this time a 
disturbance in gingival blood supply was present coro­
nal to the incision. This suggests that the blood flow to 
the gingiva was mainly in an apical to coronal direction. 
When the blood vessels were dissected horizontally, a 
collateral circulation was not initially established in the 
gingival areas coronal to the horizontal incision as 
shown in the 24-hour angiograph (Fig. 3). Clinically 
the horizontal incision resulted in local superficial 
gingival necrosis in the same region of angiographic 
686 Mörmann, Ciancio 
J. Periodontal. 
November, 1977 
circulation disturbance 48 hours after it was made 
(Fig-4) . 
Subject B 
The internal bevel incisions in subject B are angio-
graphically shown 24 hours later (Fig. 6). A t 24 hours 
no changes were seen in gingival circulation. This 
suggests that the blood supply to the gingival tissues 
was adequate even when the blood vessels from the 
papillary and periosteal area were severed. 
Subject C 
The incisions and flap in subject C are shown angio-
graphically (Fig. 8) at 24 hours after surgery. Both 
areas showed a disturbance in circulation (Fig. 8); 
however, examination of the angiographs shows that 
circulation was reduced by about 50% at the site 
where the full thickness flap was both raised and 
retracted. A t 96 hours both wounds appeared clinically 
similar. However, the vascular pattern of the area 
along the incision lines of the raised flap was still 
poorer than that of the "nonelevated flap" (Fig. 9). 
Subject D 
In subject D the flap with the longer vertical incisions 
showed a poorer revascularization at 24, 48 and 96 
hours (Figs. 10, 11, 12). The poorer revascularization 
of the longer flap (LF) resulted in a triangular, cleft­
like tissue loss at its marginal edges of approximately 2 
mm as indicated by the vertical dotted lines in Figs. 
10, 11 and 12. A s can be seen from the photographs, 
the short flap (SF) showed less circulation disturbance 
FIGURE 10. Subject D, angiograph 24 hours after surgery . Short full thickness replaced flap (SF). Long full thickness replaced 
flap ( L F ) . Distances A , B, C , D from cemento-enamel junction to respective flap margins. Arrows indicate clinical flap outline 
and area of subsequent necrosis. 
FIGURE 11. Subject D, angiograph 96 hours after surgery. Increased tissue loss at long flap (LF) as indicated by C and D ' . 
687 Blood Supply of Human Gingiva 
Volume 48 
Number 11 
FIGURE 12. Subject D, angiograph 96 hours after surgery. Increased tissue loss at long flap ( L F ) as indicated by C " and D " . 
FIGURE 13. Subject E, clinical aspect immediately following surgery, narrow based partial split thickness flap ( N F ) and broad 
based partial split thickness flap ( B F ) . 
and a better healing of the gingival margin than the 
long flap ( L F ) . 
Subject E 
In subject E at 24 hours (Figs. 13, 14) the flap on 
the right with the narrow base (NF) showed a reduced 
circulation of approximately 50%. The flap with the 
wide base (BF) showed less disturbance. A t 7 days 
(Fig. 15), the vascular pattern in both flaps was the 
same. After 7 days (Fig. 15) a cleft-like tissue loss 
(TL) was discernible at the gingival margin of the 
narrow based flap. Healing of the gingival margin at 
the wide based flap showed an acceptable gingival 
margin with minimal clef ting. 
Subject F 
In subject F minimal tension and flexion was neces­
sary to position and fix the overlong flap laterally. 
Nevertheless, a small ischemic mark (N) was produced 
by the suture (Fig. 17). A l so , the vascular pattern in 
the flap was good at 24 hours (Fig. 17) and 7 days 
(Fig. 18), new circulation in the donor site (DS). 
Subject G 
In subject G the flap was bent into position and 
tension was exerted by the suture to hold the flap in 
place. A t 24 hours no vascularization was present in 
the flap (Fig. 19). A t 5 days the flap had sloughed 
away from the root surface (Fig. 20). 
688 Mörmann, Ciancio 
J. Periodontal. 
November, 1977 
FIGURE 14. Subject E, angiograph 24 hours after surgery. Fifty percent circulation only in narrow based flap ( N F ) , clinical 
outline of flap indicated by arrows. Eighty percent circulation in broad based flap ( F B ) . 
FIGURE 15. Subject E, angiograph 7 days after surgery. More tissue loss ( T L ) at the narrow flap ( N F ) than at the broad flap 
( B F ) . New vascularization in the donor site (DS) . 
DISCUSSION 
The effect of various types of surgical procedures on 
the gingival capillaryblood circulation was evaluated 
by means of fluorescein angiography. The circulation 
changes observed suggested that flaps receive their 
major blood supply from their apical aspects. The full 
thickness incision in clinically healthy gingiva revealed 
that, functionally, the blood supply was mainly directed 
caudocranially from the vestibule to the gingival mar­
gin. This is consistent with the morphological findings 
in animals by K i n d l o v a 4 , 5 and the histologic findings in 
mongrel dogs of Novaes et a l . 2 4 
In a fluorescein angiographic study on the gingival 
blood circulation with experimental full thickness inci­
sions in humans, vascular disturbances were observed. 
They resulted in superficial necrosis in those areas 
coronal to the incisions. 2 3 These findings indicate that 
main gingival vessels may have been severed in these 
regions. Ryan , 2 5 in another human study, reported 
that the blood supply of skin is not homogenous. Our 
angiographic observations suggest that the same is true 
for human gingiva. 
In this study, the internal bevelled incision (subject 
B) severed the anastomosis between gingival and peri­
odontal vasculature and between gingival and interden­
tal vasculature. Angiographically, the separations from 
689 Blood Supply of Human Gingiva 
Volume 48 
Number 11 
either vasculatures showed no effect on circulation of 
the free and alveolar gingiva. This finding verifies the 
results of circulation measurements in man, which 
have shown that gingival and periodontal vessels are 
independent of each other. 2 6 - 2 8 
The flaps raised in patient D suggest that the greater 
the ratio of flap length to base, the greater is the 
amount of vascular disturbance. These findings corrob­
orate previous animal studies of pedicle flaps on the 
backs of rabbits, 2 9 which indicated that the intrinsic 
circulation of the flap is maintained up to the point 
where the ratio of the length to width of the simple 
parallel pedicle flap is 2:1. Regarding the design of the 
flap, these findings suggest that the broader the flap 
base, the better is its circulation pattern. This was also 
stated by Patterson 3 0 who described a series of experi­
ments in the flank of the pig in which pedicle flaps 
were raised. He found that randomly placed pedicle 
grafts had a constant 34% reduction in survival length 
when compared with control flaps designed to include 
a major artery. Kon et a l . , 3 1 using a carbon black 
perfusion technique in dogs, found histologically that 
the main vessels had been maintained within broad 
full thickness flaps during raising and retracting the 
flap. In subject C , raising and retracting a full thickness 
flap affected an approximate 50% disturbance of the 
superficial capillary circulation. 
In subjects E to G these principles were tested in 
FIGURE 16. Subject F, clinical aspect immediately following surgery. Overextension in length of experimental flap design. Easy 
mobilization of flap and minimal tension placed on flap by suturing. 
FIGURE 17. Subject F, angiograph 24 hours after surgery. Good flap circulation. Small necrosis area (N) caused by sutures. 
Tissue loss at flap end ( T L ) . Donor site ( D S ) . 
690 Mörmann, Ciancio J. Periodontol. 
November, 1977 
FIGURE 18. Subject F, angiograph 7 days after surgery. Some tissue loss at flap end ( T L ) . Good circulation in maintained part of 
flap end. Slightly advanced re- and neo vascularization of donor site (DS) . 
FIGURE 19. Subject G, angiograph 24 hours after surgery. No circulation in flap area. 
lateral sliding flap procedures. These operations were 
similar to those described by a number of other inves­
tigators 3 2 - 3 9 and were modified slightly to test the 
effects of various modalities on their circulation. The 
results in these subjects suggest that sliding flaps should 
be sufficiently extended into the alveolar mucosa to 
provide adequate mobilization. Myer et a l . 4 0 found, in 
the dog, that pedicle grafts under tension which dem­
onstrated complete vascular filling retained their vital­
ity for 3 or 4 days after surgery. However, Gl ickman 4 1 
stated that excess tension and bending impair the 
circulation when the flap is moved. Regarding the 
failure of the flap in subject G , tension was certainly 
involved, and persisting changes in the vasculature 
caused by the previous operation may have played a 
role also in that mobility was decreased. R y a n 2 5 re­
ported that skin graft sites can develop areas of dimin­
ished resistance to further surgery. 
A full thickness or partial thickness preparation may 
be used in lateral sliding f l aps . 3 5 , 3 6 In the donor site a 
loss of bone (0.5 mm) and recession (1.5 mm) is 
reported with full thickness f l aps . 3 3 , 4 1 Therefore, at 
the donor site a partial thickness flap is preferable 
because it offers the advantage of more rapid healing 
and reduces the risk of postsurgical recession, particu­
larly if the bone is thin or a dehiscence or fenestration 
is suspected. However, if the gingiva is thin, partial 
thickness may not be sufficient for flap survival . 3 3 , 3 8 A 
691 Blood Supply of Human Gingiva Volume 48 
Number 11 
FIGURE 20. Subject G, angiograph 5 days after surgery. The flap sloughed away from the root surface. 
study on pig skin showed that thick pedicle flaps 
separated from their wound beds had a 55.7% survival 
rate whereas thin flaps separated from their wound 
bed had a 26.5% survival rate. 4 2 This study also 
showed that the survival of thin flaps is dependent on 
the vascular quality of the recipient site. These findings 
are in agreement with histologic impressions reported 
by Staffileno et a l . 4 3 and may explain the excellent 
healing they reported for split thickness flaps reposi­
tioned to their original position. Compared to these 
sites, a thin flap cannot provide nutrition for the 
grafted tissue if its own blood supply is inadequate. 
Therefore, partial thickness flaps or parts of flaps 
which are designed to cover an avascular area should 
not be prepared too thin. The success of the very long 
partial thickness flap in this study in subject F can be 
explained by its full thickness preparation in its apical 
part which may have preserved a major gingival vessel 
inside the flap and by the relative thickness of the 
partial thickness dissection. 
CONCLUSIONS 
This study demonstrates changes in the gingival 
vascular supply of humans following various periodon­
tal surgical procedures. A special system was used to 
photograph circulatory changes following an i.v. injec­
tion of sodium fluorescein to visualize blood supply. 
The results of this study suggest that the following 
concepts are important in the design of periodontal 
flaps. 
1. Flaps should be broad enough at their base to 
include major gingival vessels. 
2. A flap's length to width ratio should not exceed 2:1. 
3. Minimal tension should be produced by suturing 
techniques and the tissue should be managed gently 
during the surgical procedure. 
4. Partial thickness flap preparations to cover avas­
cular areas should not be too thin so that more blood 
vessels are included in them. 
5. The apical portion of periodontal flaps should be 
full thickness when possible. 
ACKNOWLEDGMENTS 
The authors wish to acknowledge the support of the Zeiss 
Company, Zurich, Switzerland, the technical advice of Dr. 
Walter H . Lang, Director, Medical Optical Department, 
Zeiss Company, Oberkochen, West Germany, and the clini­
cal assistance of Dr. Andre Bachmann. 
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Announcement 
T H E SIR WILFRED FISH R E S E A R C H PRIZE 
The 'Sir Wilfred Fish Research Prize' was instituted in 1970 by The 
British Society of Periodontology with the object of promoting 
periodontal research by young workers. The prize of £100 will be 
awarded annually where appropriate. 
The research work should have an application to periodontology 
and must be unpublished. Individuals may compete either on their 
own behalf or on behalf of a research group. Eligibility is limited to 
those under the age of 40. 
A short list will be drawn up from the manuscripts submitted to the 
Panel of Judges. Entrants who reach the short list will be expected to 
present their work, at their own expense, in the form of a paper of 
fifteen minutes duration, followed by a 10-minute discussion period, 
during the Society's International Meeting to be held at the Europa 
Hotel, London, England on 3rd and 4th of April, 1978. The final 
selection will be made on the content and presentation of the work. 
The closing date for receipt of manuscripts (three copies) which 
must be submitted to the Honorary Secretary, is 31st January 1978. 
Honorary Secretary: 
H . D. G L E N W R I G H T 
The Dental School, 
St. Chad's Queensway, 
Birmingham, B4 6NN, 
England.