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The tubed pedicle flap
THE TUBED
PEDICLE FLAP 1
By STUARTH. MILTON, B.Sc., B.M., D.Phil.
From the Department of Plastic Surgery, Churchill Hospital, Oxford, England THE most curious thing about the origin of the tubed pedicle skin flap is that the idea seems to have occurred independently to four different surgeons at the same time-Filatov (I917), Ganzer (1917), Gillies (192o) and Aymard (1917). Necessity, in time of war, was the mother of invention. But it has been overlooked that Dieffenbach (1845) preceded them by 80 years in using tubed flaps from the arm to replace noses. He described vividly the suppuration produced by the open flap method of Tagliacozzi, and devised a method of preventing it--the tubed pedicle flap. Perhaps the tubed pedicle flap was not an invention at all but merely an observation of Nature's powers of healing. The tendency of unlined plane flaps to toll into tubes by contraction of the scar on the raw surface was noted by Pickerill and White (I922), and I have confirmed this experimentally ; the same tendency is apparent in free grafts in tissue-culture (Medawar, 1948 ; Lawrence, 1961). This essay, then, is concerned with Nature's powers of healing and maintaining life in the face of injury by the surgeon's knife when raising pedicled skin flaps. It is based on observations on man, and experiments on animals. The study began by clinical observation, using indirect methods of assessing the blood flow in flaps--heatflow discs, occlusion plethysmography, and measurement of tissue oxygen tension. Observations on man are an essential beginning, as they allow an appreciation of the characteristics of a failing flap, but the scope is limited. Measurements can only be indirect, for experiments involving necrosis would be unethical, and--more important--they can only be made within the framework of current surgical practice. It is therefore necessary to devise an experimental preparation where necrosis of flaps may be produced at will, and where the sequence of changes mimics that of the failing human flap. Of all the animals examined, only the pig has a skin which resembles that of man in its texture and segmental blood supply. These animals may be operated on with the same surgical and anmsthetic instruments and techniques as used in man, and the sequence of colour changes of failing flaps closely resembles that seen in man. During the past five years 1,1o3 experimental flaps of many types have been raised--single and double pedided plane flaps, tubed flaps, island flaps and flaps with dermal pedides. The most useful preparation has been one in which several parallel single pedicled flaps are based on the row of ventral segmental vessels which emerge from the rectus sheath ; this provides a constant vascular base-line, which is reproducible from one pig to another. Each flap is made of sufficient length that the tip is bound to die, the surviving length being taken as a quantitative measure of the adequacy of the circulation. This length may be accurately predicted at the time of operation by intravenous injection of a freely diffusible non-toxic dye--Disulphine Blue. After injection of dye it is possible to treat adjacent flaps in different ways, and so to compare ~he actual survival with that predicted by dye, and thus to obtain an accurate measure of the effect of treatment without this being obscured by the different viability of the skin of different pigs and different sites on the same pig. Statistical methods were used in both the design and analysis of the experiments. Rules o f P r a c t i e e . - - I t is widely held that skilled surgeons experience little trouble with skin flaps, but this skill must have been acquired by making mistakes. Such mistakes pass unnoticed in times of war, when reconstructive surgery advances most 1 Awarded the Kay-Kilner Essay Prize, 1967. 53
54
BRITISH JOURNAL OF PLASTIC SURGERY
rapidly, but mistakes are undesirable in civilian practice. Certain rules have been developed to guide those who are unable to profit by experience, and these rules have been repeatedly quoted without thought about their origin, validity or applicability. One of these rules, that concerning the ratio of length to width, cannot be substantiated experimentally, and is based on fallacious reasoning. Experimental evidence will be advanced to show that others are in need of revision. Previous studies fall into two main groups--the prevention or treatment of failing flaps, and the assessment of blood supply. The aim of most authors has been to instruct the surgeon about the earliest time at which flaps can be safely moved, either by analogy with animal experiment, or on the basis of clinical tests. All have been based on the prevailing rules of practice, and none has been directed towards investigating these rules.
Misconceptions about B l o o d S u p p l y o f Flaps.--Almost by definition a flap is a piece of skin which carries its own blood supply, so it is natural that authors should have been preoccupied with blood supply. Some have shown, by injection techniques, that the vessels in a flap become aligned along its length, so the concept has arisen that once blood enters a flap it must flow to the other end like water in a canal. In fact, during the crucial hours after a flap is raised there is agradient of flow. I f an intravital dye is injected intravenously at the time of operation, it flows rapidly along the flap at first, then more slowly and finaUy becomes stationary. T h e reverse picture is seen as the dye is excreted. T h e rate of flow of dye decreases in inverse proportion to the distance travelled along the flap--though the exact mathematics remains to be elucidated. In man, studies of heatflow have shown that a gradient persists throughout the period of transfer of tubed pedicle flaps, but these measurements are difficult to interpret because of the analogy with a car radiator which is hottest at the inlet although there is a constant flow throughout. It should be appreciated, however, that blood does not feel morally obliged to flow to the tip of the flap, whatever the wish of the surgeon; it merely follows the principles of hcemodynamics and takes the first available route home. T h e second misconception is that blood supply is often equated with viability. In a series of papers, Stark and Dehaan showed that iontophoresis of histamine into flaps increased the blood supply as measured by injection of resin or by the size of the arterial pulse, but when survival was measured histamine was found to be detrimental. This could be explained if histamine caused a reduction in the number of capillaries and the appearance of sinusoids. Such a change in tubed pedicle flaps in man has been observed by Braithwaite (1951). It can thus be shown (by application of Poiseuille's law) that flow may remain constant, or actually increase, yet the area of the vessel wall available for exchange with the tissues may be greatly reduced. Thus experiments should be concerned not with blood supply but with viability. The crucial test of adequacy of the circulation is survival or necrosis. The surviving length is a quantitative measure of the balance between demand for oxygen and its supply; it is also what matters most to the patient. Square F l a p s . - - O n e of the basic rules is that a bipedicled tubed flap can be considered as two single pedicled flaps joined end to end. Thus it is possible to make elaborate theoretical predictions (e.g. Mustard6, 1953) without stopping to ask whether the basic premise is correct. Assuming, for the present, that the basic premise is correct, the behaviour of untubed single pedicled flaps is relevant, and such flaps are more simple to study. The Fallacy o f the Length/Width R a t i o . - - T h e viable length of a flap is said to depend on the width of its pedicle. This is probably the fundamental rule about skin flaps, yet its origin is obscure, and it appears to be without experimental foundation.
THE TUBED PEDICLE FLAP
55
Observations on the pig which first cast doubt on this principle were first made by chance during an experiment which was intended to correlate surviving length with that predicted by intravital dyes. Single pedicled flaps of I, 2, 3 and 4 cm. width survived on average to 4"o, 5"o, 5"8 and 6.2 cm. length respectively. Clearly length was not directly proportional to width. A flap was then made as wide as possible--2o cm.--and this survived to a length of only 6"4 cm. Thus there appeared to be a limit to surviving length, and the effects of width were seen only in the narrower flaps. Experiments to determine the exact relationship of length to width were complicated because differences in the viability of skin of different pigs, and different sites on the same pig, were greater than the observed effects of width. The procedure which was devised was to raise wide flaps on a constant row of vessels, to determine the viable lengths by dye, and to divide each flap into narrower ones of different widths. The surviving lengths were then adjusted by statistical means to remove the effects of differences between pigs and between sites. A clear picture emergcdmalmost all the flaps survived to about the same length. A proportion of the narrower flaps were appreciably shorter. It was predicted that the short flaps were so narrow that some had, by chance, failed to include a segmental vessel in the pedicle. A new hypothesis was advanced--that flaps made under similar conditions survive to the same length, regardless of width. The only effect of decreasing width is to reduce the probability of the pedicle containing a large vessel. Verification came from three directions--the surviving lengths of flaps of 24 or even 35 cm. width were the same as that of flaps of I to8 cm. width ; the measured distance apart of the segmental vessels was within 5 per cent. of that predicted ; and deliberate division of the segmental vessels in flaps produced the same degree of shortening as the difference between the longer and shorter flaps. The concept of a length/width ratio appears to be based on fallacious reasoning. It is argued that increasing width will allow a greater blood supply and support a greater length of flap. Although the blood supply increases with width, the consumption of oxygen is proportional to area, not length. Thus the accepted principle implies that when width is doubled, four times as much tissue can survive on only twice as much blood. This is clearly a violation of biological economy. A stable equilibrium can only result if the length of the flap is constant ; this is the situation found by experiment.
Cutaneous Pedicles o f " N o Width " - - I s l a n d F l a p s . - - I f flaps which include a vessel in the pedicle survive to the same length regardless of width (in the range of widths I to 35 cm.) what would be the surviving length of a flap with a cutaneous pedicle of no width ? The answer was most unexpected ; when all the tissues were excised, leaving only the segmental vessels, the flaps survived to the same length or longer than controls, the average lengthening being about Io per cent. This lengthening is at present unexplained, but anyone who has seen the tenuous threads of vessels would marvel that the flap could survive at all. Thus the skin of the pedicle, which has for so long been thought to play a prominent role in nutrition of the flap, can be dispensed with altogether. This is precisely what was said by J. F. S. Esser (I917)--" The principle of biological flaps or artery flaps is that the pedicles are thin, generally short and consist only in veins, arteries, lymph vessels and nerves surrounded with a small covering or protective sheet of elastic connective tissue, but have no skin or other tissue. The tissues would bring no advantage but could easily close the vessels by pressure, if the pedicles are very much turned." It is appropriate that the views of Esser should have been verified experimentally on the 5oth anniversary of his first paper on biological flaps. He was the protagonist, though not the originator. Relative Importance of Arteries and Veins.--If the arteries and veins within the pedicle are the only elements necessary for survival, it may be asked which plays the
56
B R I T I S H J O U R N A L OF P L A S T I C SURGERY
greater part. Traditionally flaps are supposed to die from venous obstruction, and the recent experiments of Fujino (1967) in the dog are Jn accord with this. However, in the pig the reverse it true--ligation of all the visible arteries reduces surviving length. Ligation of all the visible veins has no measurable effect. This is by no means a closed field of investigation for there are differences in the relative effects of obstructing the arteries and veins in different organs, such as kidney and bowel. There is, however, circumstantial evidence for thc dominant role of arteries ; the line of demarcation of flaps raised on the ventral segmental vessels takes a characteristic shape, and this curve is closely parallel to the girth of the animal. Where surviving length is longer, and girth greater, the arteries are of larger calibre--surely a beautiful example of biological economy. Secondly, if dye is injected intravenously as soon as the flap is raised, it flows only to the line of demarcation. If flaps died in venous stasis, dye would be expected to enter and remain in the distal, non-viable, part of the flap. Obviously a complete circulatory loop is necessary for normal function, but, as it has been known from the time of Harvey that the propelling force in veins is derived from that in arteries, it would seem that the arteries will be found to be the more important factor in flaps in man.
Colour.--Closely allied to the question of venous obstruction is that of colour : white flaps are supposed to be healthy and blue ones in jeopardy. When these experiments began it was noted that occasional flaps were a dusky blue and that these survived to a greater length than expected. The subsequent x85 flaps, in experiments in which the vessels were interfered with, were classified at the time of operation as blue, pink or white. Blue flaps were found to survive to a significantly greater length than white ones, with pink flaps intermediate. Island flaps were usually blue, and survived to a greater length than controls. When the arteries were cut, the flaps were usually white and they survived to a shorter length than controls. Cyanosis is not seen in anaemic patients when the haemoglobin is less than 5 g./ioo ml. Although most of the h~moglobin in flaps after operation should be in the reduced form, because of the low oxygen tension, this should not be seen as cyanosis unless there is a good arterial inflow to dilate the skin vessels. The dreaded blueness of clinical flaps may be that of actually dead skin, as seen in the pig on the day after operation. It is perhaps not sufficiently appreciated that the viable length of a flap is determined as soon as it is raised. By the use of intravital dyes it has been shown that surviving length can be accurately predicted 30 minutes after raising the flap, and there is even a good correlation between surviving length and the distance travelled by dye along the flap in the first six seconds. Does Delay double Surviving L e n g t h ?--It is a basic premise that bipedicled flaps behave as two single pedicled flaps joined end to end. This premise is reasonable when a tubed pedicle flap is first raised (delayed), but what happens when one end is detached and reimplanted ? The flap is now twice the length (or length/width ratio) ~which is regarded as safe. This is equivalent to saying that the " d e l a y i n g " procedure doubles the viable length. A number of experiments have been performed on the mechanism of delay, but none has answered this fundamental question. It is not an easy question to answer experimentally. In principle the method is to make flaps which are just short enough to survive completely, and to extend these flaps at intervals and compare the surviving length with that of a flap which had not previously been raised. The difficulty it to predict the point to which the blood would flow when the flap is raised to its full length and to base the initial flap at this point. Similar points must be chosen for (say) four flaps to be raised at weekly intervals, and the whole design must allow for growth of the pig and for differences between pigs and sites on each pig.
THE TUBED PEDICLE FLAP
57
It has been shown, by this preparation, that delay does not double surviving length ; and that there is at most a 2o per cent. increase. Delay by incising the margins of the flap, without raising, has even less effect. The technique is difficult to apply to bipedicled flaps, because necrosis would be in the centre, but unless it can be shown that the preliminary raising of a bipedicled tubedflap doubles the length which is viable on one pedicle, the value of the procedure is in question. =
Width •
I
" o
i i
t Th]cktless
=Wx T
Cross Section~t Area
O
Cro~$Sections|
Area
=Wx T
I Space Available
/I / // /Sl~ce Required / / Swelling
~E~30,
u
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./
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if
~3 No
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Width of Flap of Unit Thickness-cm.
Minimum ratio of width to thickness of tubed pedicled flaps. The meaning of this figure may be best understood by an example : a flap which is z 2 c m . wide and I c m . thick will have a cross-sectional area of T2 c m . ~ Swelling of one-third will increase the cross-sectional area to x 6 c m . 2, but the width will remain at i 2 c m . Calculation of the cross-sectional area of a tubed flap of T2 c m . circumference shows this to be T I ' 5 c m . ~ Therefore the skin must be stretched over the fat at the time of operation, and development of 0edema will increase the tension. Calculation shows that the width should be x7 times the thickness to allow for 0edema. This ratio should be regarded as approximate until it has been determined by experiment.
Specific Effect of T u b i n g the Flap.--In the previous sections it has been assumed that the behaviour of tubed flaps is similar to plane ones, but the operation of tubing adds complexity. The problem is to enclose enough fat to preserve the vessels without strangling the circulation by too much tension. Although the dangers of tension are well recognised, the only quantitative calculations (Dufourmentel and Mouly, I959) are based on the erroneous premise that the thickness of the flap which is initially raised becomes the radius of the tube ; this has the effect o f " losing" half the fat. A cross-section of a flap is a rectangle, with skin forming one edge (Fig.). When this
58
BRITISH JOURNAL OF PLASTIC SURGERY
is tubed, the fat must be completely enveloped in skin. In an idealised situation the fat can only be contained if the width of the flap is at least I2½ times its thickness. If the width is less, the skin must be stretched over the fat with consequent obstruction to blood flow. But living tissues do not behave like geometrical shapes. A normal part of the inflammatory response is an increase of fluid in tissue spaces. The magnitude of this swelling in flaps has been assessed by removing flaps at intervals and comparing the weights with controls. The viable zone was found to increase in weight by 35 per cent. in the first 24 hours. When a tube is raised, allowance must be made for this swelling, and reference to the idealiscd situation shows that width must be at least 17 times thickness. This critical ratio of width/thickness should only be taken as an approximation as it is susceptible to direct experiment, and the actual figure may well vary with regional elastic properties of the skin. B u t there seems to be a narrow path between damaging the vessels by injudicious removal of fat, and strangling them by its retention. The F u t u r e . - - T h e s e studies were undertaken in the hope that transfer of skin might be made more safe. It is now clear that advances in the future will come from increasing speed of transfer. The use of local arterial pedicle flaps would seem to be the method of first choice. More details of the cutaneous vascular anatomy in man are required, and thermography may assist in locating the vessels in the individual patient. When skin must be transferred from a distant site there may be no advantage in the initial raising of a bipedicled flap, because delay does not appear to increase viable length by an amount sufficient to justify its us~. Therefore, time would be saved if flaps were initially based on known arteries and one end immediately attached to the intermediate carrier--a method which has been practised with success (Shaw and Payne, 1946). The physiology of this intermediate attachment has not been investigated in this study, but there is evidence from several sources that arteries of appreciable size do not anastomose in nature. Some means of stimulating this anastomosis, as suggested by Muir and Stranc (I967), might be advantageous, but the use of an intermediate carrier seems to be a haphazard process--it would be unthinkable to transplant a kidney by such means. Research in the future should be directed towards transplantation of skin by direct anastomosis of the vessels of the flap with those of the recipient area. Rapid advances are being made in several centres in developing techniques of microvascular anastomosis. These workers have followed the line pioneered by Esser of transplanting skin on a vascular pedicle. The observations in this study have provided a bridge from the main stream of plastic surgery--the use of cutaneous pedicles--to an appreciation of the value of vascular pedicled flaps. It is to be hoped that in the not too distant future necrosis of pedicled skin flaps will be a matter of medical history.
REFERENCES AYMARD,J. L. (I917). Lancet, 2, 888. BRAITHWAITE,F. (I95I). Br..7. plast. Surg. 4, 28. DE HAAN,C. R. and STARK,R. B. (1958). Surg. Forum, 8, 578. (196I). Plasticrecomtr. Surg. 28, 577. DmFFn~BACH,J. F. (1845). " Die operative Chirurgie ", x, 382. Leipzig. Du~ou~vm~rrEL, C. and MOULY, R. (1959). " Chirurgie Plastique ", p. 88. Paris: Flammirion. Ess~, J. F. S. (1917). Surgery Gymc. Obstet. 34, 737. (I934). " Biological or Artery Flaps of the Face." Monaco: Institute Esser de Chirurgie Structive. FILATOV,V. P. (1917). Trans. Labunka, M., Gnudi, M. T. and Webster, J. B. (1959) in Surg. Clins. N. Am. 39, 277. FuJINO, T. (1967). Plastic reconstr. Surg. 39, 125. GA.X!ZER,H. (1917). Cited by Webster, J. P. (1959) in Surg. GEm. N. Am. 39, 274.
THE TUBED PEDICLE FLAP GILLIES, H. D. (I9zoa). New York reed. ft., p. I. - (192ob). Lancet, 2, 320. HARVEY, W. (1629). " An anatomical dissertation upon the movement of the heart and blood in animals." Facsimile reproduction and translation (1894). Canterbury: Moreton. LAWRENCE, J. C. (1961). " Wound Healing ", p. 32, ed. Slome, D. Oxford : Pergamon Press. MEDAWAR,P. B. (1948). Q.ffl micr. Sci. 89, 187. MUIR, I. F. K. and STRANC,W. E. (1967). Personal communication. MUSTARD~,,J. C. (1953). Plastic reconstr. Surg. H , 454. PICKERILL, H. P. and WHITE, J. R. (1922). Br. ft. Surg. 9, 321. SHAW, D. T. and PAYEE, R. L. (1946). Surgery Gynec. Obstet. 83, 205. STARK, R. B. (I956a). Plastic reconstr. Surg. 18, 329 . (i956b). Transpl. Bull. 3, 94. STARK, R. B. and DE HAAN, C. R. (1959). Plastic reconstr. Surg. 24, 19. TAGLIACOZZI. Cited by Gnudi, M. T. and Webster, J. P. (1951) i n " The Life and Times of Gaspare Tagliacozzi ".* New York : Reichner.
59
PEDICLE FLAP 1
By STUARTH. MILTON, B.Sc., B.M., D.Phil.
From the Department of Plastic Surgery, Churchill Hospital, Oxford, England THE most curious thing about the origin of the tubed pedicle skin flap is that the idea seems to have occurred independently to four different surgeons at the same time-Filatov (I917), Ganzer (1917), Gillies (192o) and Aymard (1917). Necessity, in time of war, was the mother of invention. But it has been overlooked that Dieffenbach (1845) preceded them by 80 years in using tubed flaps from the arm to replace noses. He described vividly the suppuration produced by the open flap method of Tagliacozzi, and devised a method of preventing it--the tubed pedicle flap. Perhaps the tubed pedicle flap was not an invention at all but merely an observation of Nature's powers of healing. The tendency of unlined plane flaps to toll into tubes by contraction of the scar on the raw surface was noted by Pickerill and White (I922), and I have confirmed this experimentally ; the same tendency is apparent in free grafts in tissue-culture (Medawar, 1948 ; Lawrence, 1961). This essay, then, is concerned with Nature's powers of healing and maintaining life in the face of injury by the surgeon's knife when raising pedicled skin flaps. It is based on observations on man, and experiments on animals. The study began by clinical observation, using indirect methods of assessing the blood flow in flaps--heatflow discs, occlusion plethysmography, and measurement of tissue oxygen tension. Observations on man are an essential beginning, as they allow an appreciation of the characteristics of a failing flap, but the scope is limited. Measurements can only be indirect, for experiments involving necrosis would be unethical, and--more important--they can only be made within the framework of current surgical practice. It is therefore necessary to devise an experimental preparation where necrosis of flaps may be produced at will, and where the sequence of changes mimics that of the failing human flap. Of all the animals examined, only the pig has a skin which resembles that of man in its texture and segmental blood supply. These animals may be operated on with the same surgical and anmsthetic instruments and techniques as used in man, and the sequence of colour changes of failing flaps closely resembles that seen in man. During the past five years 1,1o3 experimental flaps of many types have been raised--single and double pedided plane flaps, tubed flaps, island flaps and flaps with dermal pedides. The most useful preparation has been one in which several parallel single pedicled flaps are based on the row of ventral segmental vessels which emerge from the rectus sheath ; this provides a constant vascular base-line, which is reproducible from one pig to another. Each flap is made of sufficient length that the tip is bound to die, the surviving length being taken as a quantitative measure of the adequacy of the circulation. This length may be accurately predicted at the time of operation by intravenous injection of a freely diffusible non-toxic dye--Disulphine Blue. After injection of dye it is possible to treat adjacent flaps in different ways, and so to compare ~he actual survival with that predicted by dye, and thus to obtain an accurate measure of the effect of treatment without this being obscured by the different viability of the skin of different pigs and different sites on the same pig. Statistical methods were used in both the design and analysis of the experiments. Rules o f P r a c t i e e . - - I t is widely held that skilled surgeons experience little trouble with skin flaps, but this skill must have been acquired by making mistakes. Such mistakes pass unnoticed in times of war, when reconstructive surgery advances most 1 Awarded the Kay-Kilner Essay Prize, 1967. 53
54
BRITISH JOURNAL OF PLASTIC SURGERY
rapidly, but mistakes are undesirable in civilian practice. Certain rules have been developed to guide those who are unable to profit by experience, and these rules have been repeatedly quoted without thought about their origin, validity or applicability. One of these rules, that concerning the ratio of length to width, cannot be substantiated experimentally, and is based on fallacious reasoning. Experimental evidence will be advanced to show that others are in need of revision. Previous studies fall into two main groups--the prevention or treatment of failing flaps, and the assessment of blood supply. The aim of most authors has been to instruct the surgeon about the earliest time at which flaps can be safely moved, either by analogy with animal experiment, or on the basis of clinical tests. All have been based on the prevailing rules of practice, and none has been directed towards investigating these rules.
Misconceptions about B l o o d S u p p l y o f Flaps.--Almost by definition a flap is a piece of skin which carries its own blood supply, so it is natural that authors should have been preoccupied with blood supply. Some have shown, by injection techniques, that the vessels in a flap become aligned along its length, so the concept has arisen that once blood enters a flap it must flow to the other end like water in a canal. In fact, during the crucial hours after a flap is raised there is agradient of flow. I f an intravital dye is injected intravenously at the time of operation, it flows rapidly along the flap at first, then more slowly and finaUy becomes stationary. T h e reverse picture is seen as the dye is excreted. T h e rate of flow of dye decreases in inverse proportion to the distance travelled along the flap--though the exact mathematics remains to be elucidated. In man, studies of heatflow have shown that a gradient persists throughout the period of transfer of tubed pedicle flaps, but these measurements are difficult to interpret because of the analogy with a car radiator which is hottest at the inlet although there is a constant flow throughout. It should be appreciated, however, that blood does not feel morally obliged to flow to the tip of the flap, whatever the wish of the surgeon; it merely follows the principles of hcemodynamics and takes the first available route home. T h e second misconception is that blood supply is often equated with viability. In a series of papers, Stark and Dehaan showed that iontophoresis of histamine into flaps increased the blood supply as measured by injection of resin or by the size of the arterial pulse, but when survival was measured histamine was found to be detrimental. This could be explained if histamine caused a reduction in the number of capillaries and the appearance of sinusoids. Such a change in tubed pedicle flaps in man has been observed by Braithwaite (1951). It can thus be shown (by application of Poiseuille's law) that flow may remain constant, or actually increase, yet the area of the vessel wall available for exchange with the tissues may be greatly reduced. Thus experiments should be concerned not with blood supply but with viability. The crucial test of adequacy of the circulation is survival or necrosis. The surviving length is a quantitative measure of the balance between demand for oxygen and its supply; it is also what matters most to the patient. Square F l a p s . - - O n e of the basic rules is that a bipedicled tubed flap can be considered as two single pedicled flaps joined end to end. Thus it is possible to make elaborate theoretical predictions (e.g. Mustard6, 1953) without stopping to ask whether the basic premise is correct. Assuming, for the present, that the basic premise is correct, the behaviour of untubed single pedicled flaps is relevant, and such flaps are more simple to study. The Fallacy o f the Length/Width R a t i o . - - T h e viable length of a flap is said to depend on the width of its pedicle. This is probably the fundamental rule about skin flaps, yet its origin is obscure, and it appears to be without experimental foundation.
THE TUBED PEDICLE FLAP
55
Observations on the pig which first cast doubt on this principle were first made by chance during an experiment which was intended to correlate surviving length with that predicted by intravital dyes. Single pedicled flaps of I, 2, 3 and 4 cm. width survived on average to 4"o, 5"o, 5"8 and 6.2 cm. length respectively. Clearly length was not directly proportional to width. A flap was then made as wide as possible--2o cm.--and this survived to a length of only 6"4 cm. Thus there appeared to be a limit to surviving length, and the effects of width were seen only in the narrower flaps. Experiments to determine the exact relationship of length to width were complicated because differences in the viability of skin of different pigs, and different sites on the same pig, were greater than the observed effects of width. The procedure which was devised was to raise wide flaps on a constant row of vessels, to determine the viable lengths by dye, and to divide each flap into narrower ones of different widths. The surviving lengths were then adjusted by statistical means to remove the effects of differences between pigs and between sites. A clear picture emergcdmalmost all the flaps survived to about the same length. A proportion of the narrower flaps were appreciably shorter. It was predicted that the short flaps were so narrow that some had, by chance, failed to include a segmental vessel in the pedicle. A new hypothesis was advanced--that flaps made under similar conditions survive to the same length, regardless of width. The only effect of decreasing width is to reduce the probability of the pedicle containing a large vessel. Verification came from three directions--the surviving lengths of flaps of 24 or even 35 cm. width were the same as that of flaps of I to8 cm. width ; the measured distance apart of the segmental vessels was within 5 per cent. of that predicted ; and deliberate division of the segmental vessels in flaps produced the same degree of shortening as the difference between the longer and shorter flaps. The concept of a length/width ratio appears to be based on fallacious reasoning. It is argued that increasing width will allow a greater blood supply and support a greater length of flap. Although the blood supply increases with width, the consumption of oxygen is proportional to area, not length. Thus the accepted principle implies that when width is doubled, four times as much tissue can survive on only twice as much blood. This is clearly a violation of biological economy. A stable equilibrium can only result if the length of the flap is constant ; this is the situation found by experiment.
Cutaneous Pedicles o f " N o Width " - - I s l a n d F l a p s . - - I f flaps which include a vessel in the pedicle survive to the same length regardless of width (in the range of widths I to 35 cm.) what would be the surviving length of a flap with a cutaneous pedicle of no width ? The answer was most unexpected ; when all the tissues were excised, leaving only the segmental vessels, the flaps survived to the same length or longer than controls, the average lengthening being about Io per cent. This lengthening is at present unexplained, but anyone who has seen the tenuous threads of vessels would marvel that the flap could survive at all. Thus the skin of the pedicle, which has for so long been thought to play a prominent role in nutrition of the flap, can be dispensed with altogether. This is precisely what was said by J. F. S. Esser (I917)--" The principle of biological flaps or artery flaps is that the pedicles are thin, generally short and consist only in veins, arteries, lymph vessels and nerves surrounded with a small covering or protective sheet of elastic connective tissue, but have no skin or other tissue. The tissues would bring no advantage but could easily close the vessels by pressure, if the pedicles are very much turned." It is appropriate that the views of Esser should have been verified experimentally on the 5oth anniversary of his first paper on biological flaps. He was the protagonist, though not the originator. Relative Importance of Arteries and Veins.--If the arteries and veins within the pedicle are the only elements necessary for survival, it may be asked which plays the
56
B R I T I S H J O U R N A L OF P L A S T I C SURGERY
greater part. Traditionally flaps are supposed to die from venous obstruction, and the recent experiments of Fujino (1967) in the dog are Jn accord with this. However, in the pig the reverse it true--ligation of all the visible arteries reduces surviving length. Ligation of all the visible veins has no measurable effect. This is by no means a closed field of investigation for there are differences in the relative effects of obstructing the arteries and veins in different organs, such as kidney and bowel. There is, however, circumstantial evidence for thc dominant role of arteries ; the line of demarcation of flaps raised on the ventral segmental vessels takes a characteristic shape, and this curve is closely parallel to the girth of the animal. Where surviving length is longer, and girth greater, the arteries are of larger calibre--surely a beautiful example of biological economy. Secondly, if dye is injected intravenously as soon as the flap is raised, it flows only to the line of demarcation. If flaps died in venous stasis, dye would be expected to enter and remain in the distal, non-viable, part of the flap. Obviously a complete circulatory loop is necessary for normal function, but, as it has been known from the time of Harvey that the propelling force in veins is derived from that in arteries, it would seem that the arteries will be found to be the more important factor in flaps in man.
Colour.--Closely allied to the question of venous obstruction is that of colour : white flaps are supposed to be healthy and blue ones in jeopardy. When these experiments began it was noted that occasional flaps were a dusky blue and that these survived to a greater length than expected. The subsequent x85 flaps, in experiments in which the vessels were interfered with, were classified at the time of operation as blue, pink or white. Blue flaps were found to survive to a significantly greater length than white ones, with pink flaps intermediate. Island flaps were usually blue, and survived to a greater length than controls. When the arteries were cut, the flaps were usually white and they survived to a shorter length than controls. Cyanosis is not seen in anaemic patients when the haemoglobin is less than 5 g./ioo ml. Although most of the h~moglobin in flaps after operation should be in the reduced form, because of the low oxygen tension, this should not be seen as cyanosis unless there is a good arterial inflow to dilate the skin vessels. The dreaded blueness of clinical flaps may be that of actually dead skin, as seen in the pig on the day after operation. It is perhaps not sufficiently appreciated that the viable length of a flap is determined as soon as it is raised. By the use of intravital dyes it has been shown that surviving length can be accurately predicted 30 minutes after raising the flap, and there is even a good correlation between surviving length and the distance travelled by dye along the flap in the first six seconds. Does Delay double Surviving L e n g t h ?--It is a basic premise that bipedicled flaps behave as two single pedicled flaps joined end to end. This premise is reasonable when a tubed pedicle flap is first raised (delayed), but what happens when one end is detached and reimplanted ? The flap is now twice the length (or length/width ratio) ~which is regarded as safe. This is equivalent to saying that the " d e l a y i n g " procedure doubles the viable length. A number of experiments have been performed on the mechanism of delay, but none has answered this fundamental question. It is not an easy question to answer experimentally. In principle the method is to make flaps which are just short enough to survive completely, and to extend these flaps at intervals and compare the surviving length with that of a flap which had not previously been raised. The difficulty it to predict the point to which the blood would flow when the flap is raised to its full length and to base the initial flap at this point. Similar points must be chosen for (say) four flaps to be raised at weekly intervals, and the whole design must allow for growth of the pig and for differences between pigs and sites on each pig.
THE TUBED PEDICLE FLAP
57
It has been shown, by this preparation, that delay does not double surviving length ; and that there is at most a 2o per cent. increase. Delay by incising the margins of the flap, without raising, has even less effect. The technique is difficult to apply to bipedicled flaps, because necrosis would be in the centre, but unless it can be shown that the preliminary raising of a bipedicled tubedflap doubles the length which is viable on one pedicle, the value of the procedure is in question. =
Width •
I
" o
i i
t Th]cktless
=Wx T
Cross Section~t Area
O
Cro~$Sections|
Area
=Wx T
I Space Available
/I / // /Sl~ce Required / / Swelling
~E~30,
u
1
24-
/.// / A
~'/
~ 18r
./
/SpaceRequired sw..i.~
if
if
~3 No
/
//" . / f"
,./J~/,// •/
./~/
0
0
/"
///
/
/"
i/
1'2
i0
Width of Flap of Unit Thickness-cm.
Minimum ratio of width to thickness of tubed pedicled flaps. The meaning of this figure may be best understood by an example : a flap which is z 2 c m . wide and I c m . thick will have a cross-sectional area of T2 c m . ~ Swelling of one-third will increase the cross-sectional area to x 6 c m . 2, but the width will remain at i 2 c m . Calculation of the cross-sectional area of a tubed flap of T2 c m . circumference shows this to be T I ' 5 c m . ~ Therefore the skin must be stretched over the fat at the time of operation, and development of 0edema will increase the tension. Calculation shows that the width should be x7 times the thickness to allow for 0edema. This ratio should be regarded as approximate until it has been determined by experiment.
Specific Effect of T u b i n g the Flap.--In the previous sections it has been assumed that the behaviour of tubed flaps is similar to plane ones, but the operation of tubing adds complexity. The problem is to enclose enough fat to preserve the vessels without strangling the circulation by too much tension. Although the dangers of tension are well recognised, the only quantitative calculations (Dufourmentel and Mouly, I959) are based on the erroneous premise that the thickness of the flap which is initially raised becomes the radius of the tube ; this has the effect o f " losing" half the fat. A cross-section of a flap is a rectangle, with skin forming one edge (Fig.). When this
58
BRITISH JOURNAL OF PLASTIC SURGERY
is tubed, the fat must be completely enveloped in skin. In an idealised situation the fat can only be contained if the width of the flap is at least I2½ times its thickness. If the width is less, the skin must be stretched over the fat with consequent obstruction to blood flow. But living tissues do not behave like geometrical shapes. A normal part of the inflammatory response is an increase of fluid in tissue spaces. The magnitude of this swelling in flaps has been assessed by removing flaps at intervals and comparing the weights with controls. The viable zone was found to increase in weight by 35 per cent. in the first 24 hours. When a tube is raised, allowance must be made for this swelling, and reference to the idealiscd situation shows that width must be at least 17 times thickness. This critical ratio of width/thickness should only be taken as an approximation as it is susceptible to direct experiment, and the actual figure may well vary with regional elastic properties of the skin. B u t there seems to be a narrow path between damaging the vessels by injudicious removal of fat, and strangling them by its retention. The F u t u r e . - - T h e s e studies were undertaken in the hope that transfer of skin might be made more safe. It is now clear that advances in the future will come from increasing speed of transfer. The use of local arterial pedicle flaps would seem to be the method of first choice. More details of the cutaneous vascular anatomy in man are required, and thermography may assist in locating the vessels in the individual patient. When skin must be transferred from a distant site there may be no advantage in the initial raising of a bipedicled flap, because delay does not appear to increase viable length by an amount sufficient to justify its us~. Therefore, time would be saved if flaps were initially based on known arteries and one end immediately attached to the intermediate carrier--a method which has been practised with success (Shaw and Payne, 1946). The physiology of this intermediate attachment has not been investigated in this study, but there is evidence from several sources that arteries of appreciable size do not anastomose in nature. Some means of stimulating this anastomosis, as suggested by Muir and Stranc (I967), might be advantageous, but the use of an intermediate carrier seems to be a haphazard process--it would be unthinkable to transplant a kidney by such means. Research in the future should be directed towards transplantation of skin by direct anastomosis of the vessels of the flap with those of the recipient area. Rapid advances are being made in several centres in developing techniques of microvascular anastomosis. These workers have followed the line pioneered by Esser of transplanting skin on a vascular pedicle. The observations in this study have provided a bridge from the main stream of plastic surgery--the use of cutaneous pedicles--to an appreciation of the value of vascular pedicled flaps. It is to be hoped that in the not too distant future necrosis of pedicled skin flaps will be a matter of medical history.
REFERENCES AYMARD,J. L. (I917). Lancet, 2, 888. BRAITHWAITE,F. (I95I). Br..7. plast. Surg. 4, 28. DE HAAN,C. R. and STARK,R. B. (1958). Surg. Forum, 8, 578. (196I). Plasticrecomtr. Surg. 28, 577. DmFFn~BACH,J. F. (1845). " Die operative Chirurgie ", x, 382. Leipzig. Du~ou~vm~rrEL, C. and MOULY, R. (1959). " Chirurgie Plastique ", p. 88. Paris: Flammirion. Ess~, J. F. S. (1917). Surgery Gymc. Obstet. 34, 737. (I934). " Biological or Artery Flaps of the Face." Monaco: Institute Esser de Chirurgie Structive. FILATOV,V. P. (1917). Trans. Labunka, M., Gnudi, M. T. and Webster, J. B. (1959) in Surg. Clins. N. Am. 39, 277. FuJINO, T. (1967). Plastic reconstr. Surg. 39, 125. GA.X!ZER,H. (1917). Cited by Webster, J. P. (1959) in Surg. GEm. N. Am. 39, 274.
THE TUBED PEDICLE FLAP GILLIES, H. D. (I9zoa). New York reed. ft., p. I. - (192ob). Lancet, 2, 320. HARVEY, W. (1629). " An anatomical dissertation upon the movement of the heart and blood in animals." Facsimile reproduction and translation (1894). Canterbury: Moreton. LAWRENCE, J. C. (1961). " Wound Healing ", p. 32, ed. Slome, D. Oxford : Pergamon Press. MEDAWAR,P. B. (1948). Q.ffl micr. Sci. 89, 187. MUIR, I. F. K. and STRANC,W. E. (1967). Personal communication. MUSTARD~,,J. C. (1953). Plastic reconstr. Surg. H , 454. PICKERILL, H. P. and WHITE, J. R. (1922). Br. ft. Surg. 9, 321. SHAW, D. T. and PAYEE, R. L. (1946). Surgery Gynec. Obstet. 83, 205. STARK, R. B. (I956a). Plastic reconstr. Surg. 18, 329 . (i956b). Transpl. Bull. 3, 94. STARK, R. B. and DE HAAN, C. R. (1959). Plastic reconstr. Surg. 24, 19. TAGLIACOZZI. Cited by Gnudi, M. T. and Webster, J. P. (1951) i n " The Life and Times of Gaspare Tagliacozzi ".* New York : Reichner.
59