THE PIG AS AN EXPERIMENTAL MODEL FOR SKIN FLAP BEHAVIOUR: A REAPPRAISAL OF PREVIOUS STUDIES By P. M. STELL, F.R.C.S. Department of Oto-Rhino-Laryngology, Ear, Nose and Throat Infirmary, Myrtle Street, Liverpool L7 7DF
MILTON’S classical studies of flaps raised on the flanks of pigs, which culminated in his uncompromising statement “flaps made under the same conditions of blood supply survive to the same length regardless of width” (Milton, 1970X were made when plastic surgeons were just becoming aware of the 2 quite separate varieties of flaps in man which have since been called “axial pattern” and “random pattern” flaps. Since many of Milton’s flaps contained the segmental vessels of the pig’s abdominal wall, his results were acceptable as applying to axial pattern flaps. However Daniel and Williams (1973) studied 3 kinds of flaps in pigs: “arterial” containing the segmental vessels, “cutaneous” in which the segmental vessels were divided at the base and which might be presumed to be random patterned and “island”. Although at narrow widths the surviving length of their cutaneous flaps did increase with width, they interpreted their results as showing that “an increase in width did not result in an increased length of survival”. These results are now illustrated and apparently accepted in at least one textbook of plastic surgery as being applicable in man (Grabb and Smith, 1973). This concept is not acceptable to many surgeons with wide experience of local or bridge pedicle flaps of random pattern on the human trunk and limbs. Within the range of size and sites of such clinical flaps any attempt to raise one larger than it is broad carries a high risk of distal necrosis; in other words, the longer the flap required the wider the base must be. To try to resolve this discrepancy 3 studies have been carried out: The blood supply of the pig’s skin has been examined so that random pattern flaps could reliably be raised. A series of 164 random pattern flaps with varying base width have been raised and their surviving length measured. Since it became apparent that at smaller base widths the surviving length is indeed related to the width, the surface area of the pig has been measured and compared to that of man to see if the size of clinical random flaps in man was comparable to the size of those in the pig whose surviving length was dependent on the base width. THE BLOODSUPPLY OF THE ABDOMINALSKIN OF THE PIG The abdominal walls of 3 pigs were dissected. A large artery, the superficial cranial epigastric artery, leaves the thoracic cavity immediately behind the rib margin about 4 cm lateral to the midline and runs caudally to anastomose with the superficial caudal epigastric artery running cranially from the groin. These vessels appear to correspond to the superior and inferior epigastric arteries in the human. The superficial cranial epigastric artery runs about 3 cm lateral to the nipple line deep to the panniculus carnosus and gives off branches about every 2 cm which run laterally below the panniculus carnosus parallel to the skin surface (Fig. I). If the dissection is carried out in the plane between the skin and the panniculus carnosus no 30/I-A
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FIG. I. FIG. 2.
Abdominal
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skin raised including the panniculus
skin raised superficial to the panniculus vessels.
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carnosus to show segmental vessels. carnosus to show the absence of segmental
large arteries are found, and only small end arteries piercing the deep fascia perpendicular to the skin are seen (Fig. 2). The cranial superficial epigastric artery in another pig was injected with Micropaque and water in equal amounts. The skin of the entire abdomen on that side was removed including the panniculus carnosus. A radiograph shows the longitudinal artery running parallel to the nipple line giving off lateral branches (Fig. 3). The panniculus carnosus was then dissected off and further radiographs taken; it can be seen (Fig. 4) that the vessels are no longer visible. It would seem therefore that if skin flaps are dissected superficial to the panniculus carnosus they will be random pattern; if deep to the panniculus carnosus and with the segmental vessels preserved, axial pattern. The panniculus carnosus of the pig differs from that of other laboratory animals in that it is not firmly attached to the skin but is
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FIG. 3. Radiograph
FIG. 4. Radiograph
MODEL FOR SKIN FLAP BEHAVIOUR
of abdominal skin including the panniculus
of abdominal
carnosus.
skin after removal of the panniculus
carnosus.
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separated from it by a layer of fat. recognisable on the abdominal wall.
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Although almost vestigial, the structure
Are jlaps raised superficial to the panniculus
is easily
carnosus reliably random pattern?
Further evidence that this was so was obtained by 2 series of experiments: Firstly, 55 flaps were raised superficial to the panmculus carnosus. They were all 50 mm wide and long enough for the distal part to become necrotic. Thirty-four were raised parallel to the coronal axis and 21 parallel to the sagittal axis. The latter might be regarded as random pattern even if the panniculus carnosus is included since the main blood vessels run coronally and would be divided. The results are shown in Table I. Although there was a statistically significant
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Minimal surviving lengths of random flaps Mean S.E.M.
Coronal flaps (34) 49.1 mm
Sagittal flaps
(21)
59’3 3’42
I.81
t = 2.83; d.f. = 53; P
difference between the minimal surviving lengths of the 2 groups, the surviving lengths of the 2 groups were fairly similar, coronal flaps having the shorter surviving length of the 2. The coronal flaps could thus not be axial flaps. Their surviving length was also remarkably constant. Secondly, the surviving lengths of “random” (i.e. raised superficial to the panniculus carnosus) and axial flaps of the same width were compared. Five pairs of flaps were designed, each pair consisting of a random coronal flap based on the nipple line and an axial coronal flap based on the perforating vessels 3 cm lateral to the nipple line; the flaps were all rectangular in shape and 35 mm wide. The side on which each flap was
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Minimal surviving lengths of random flaps compared to axial flaps Mean S.E.M.
Axial flaps 83.8 -
Random flaps
7’0
6.1
49.8 -
t = 3.83; d.f. = 8; Pco.005 (one tail). Analysed by a Students’ t-test for paired data.
placed was randomised by drawing cards from a bag. The results are shown in Table II. The surviving length of axial flaps was approximately 60 per cent greater than that of random flaps, and the difference was statistically significant. Conclusion.
carnosus
Flaps raised on the pig’s abdomen superficial to the pamriculus are reliably random patterned. Axial pattern flaps should include the
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carnosus and stop 3 cm from the nipple line where the segmental vessels
THE RELATIONSHIPBETWEENSURVIVINGLENGTH ANDBASEWIDTH OF RANDOMPATTERNFLAPS IN PIGS Young pigs of both sexes weighing between 30 and 35 kg were used on which were raised 84 random pattern flaps whose base width ranged from 5 to IOO mm giving replicas at IO points. Previously (Stell and Green, 1975) 40 rectangular flaps were compared with 40 triangular flaps; all had been elevated superficial to the panniculus carnosus so that a total of 164 random pattern flaps were available for analysis. The mean results are listed in Table III. When plotted as a graph they produced
TABLE III Mean and variance of minimal surviving lengths of complete range of flaps (pooling results for rectangular and triangular flaps) Size of base (mm)
Minimal surviving length T-_--A____, Mean (mm) S.E.M. 15.3 28.9 33.8 38.8 41.6 49.8 52.6 50’0 52’0 55.8
1.51 3.06 7’19 i.55 2.81 6.14 2.72 1.72 7’0 2,83
an asymptotic curve, which appeared as if it would fit a hyperbola of the type L = c - -!?
fun
where L is the surviving length, f(W) is some function of the width of the base, and b The most suitable function of width proved to be JW and by and c are constants. regression analysis the relationship of the surviving length to the width of the base was found to be given by the formula L = 67.3 - 12I’4. The means of the minimal surviving \: w lengths with a curve fitted by the least squares method using this formula and with intervals corresponding to the standard error of the mean are shown in Figure 5. Conclusion. This work confirms the traditional clinical concept that the surviving length of a flap is dictated by its width, with the important proviso that there is an upper limit of surviving length which cannot be increased by increasing the width of the base. It is interesting that Daniel and Williams publish a curve of the same shape as that shown in Figure I for their cutaneous flaps but ignore the curved part in their interpretation. Their flaps may not have been wholly random as dividing the segmental vessel(s) is not quite the same as elevating the flap superficial to the pticulus carnosus. The graphs which Milton (1970) published also show a similar curved initial portion. Most of Milton’s flaps contained I or more segmental vessels but the narrower
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minimal surviving length (mm) 60-
50-
30-
20-
10-
I 10
I 20
I 30
I 40
I 50
I 60
I 70
I 80 width
I 90
I 100
of base (mm)
FIG. 5- Minimal surviving lengths of random flaps.
the base the less likely this would be and some at least of the narrower flaps would be random patterned.
THE SURFACEAREA OF THE PIG Since it was now apparent that for smaller random pattern flaps in pigs the surviving length was dependent on the base width the surface area of the pig has been measured and compared with that of man. “It is not possible to compare one species with another nor to apply the results deduced from any given species to any other species until some quantitative correlation between the measurements in different species has been established” (Dreyer et al., 1912). This fundamental principle presumably applies to skin flaps on experimental animals which are smaller than those on a human. Dreyer et al. have also shown that the surface area of small mammals is directly proportional to the cross-sectional area of their aorta, so that it appears reasonable to suppose that the surviving length of a skin flap will bear some relation to the surface area of the animal because the survival of a skin flap is dictated by its blood supply. The surface area was measured using a technique similar to that used by DuBois and DuBois (1915) in their classic studies of the surface area of man. Three squares of thick paper, one IOO cm2, one 25 cm2, and one 5 cm2insize, were used to mark out squares covering the entire surface of pigs of different sizes (the smaller squares were needed to mark
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small irregular areas). The squares were then counted. Eight pigs of a mixed Large White/La&ace cross were used varying in size from 9.6 to 39.0 kg. The results are reported in Table IV. A plot on log-log graph paper gave a straight
TABLE
wt (kg)
Total
IV surface
area
(cm?) 39’0 33’5 27.0 35’0 35’5 14’5 9.6 17.7 The
surface
9,230 9,650 7,820 8,955 8,960 4,970 4,135 51570
area of 8 pigs of varying
weight.
line. The logarithmic values were used therefore for regression analysis which showed that the surface area conforms to the formula Area = 102oWO.~~, and that the correlation coefficient was statistically highly significant (r = 0.9962, t = 28.01, d.f. = 6, P
DISCUSSION The surface area of pigs in the range 30-35 kg, which is a convenient size for experiments, is about 0.8 m2, compared with a surface area of 1.8 ma for the average man. Whilst there is no direct proof that the size of flaps on a pig can be multiplied by a factor of 2.25 (i.e. 1.8/o-8) to arrive at their human equivalents, such a manipulation does in fact allow 2 close parallels to be drawn. Milton’s results showed that increasing the size of the base of his flaps led to a slight increase in the surviving length up to 8 cm, beyond which the surviving length did not increase irrespective of the size of the base. Milton’s flaps can be considered as the porcine equivalent of the human deltopectoral flap. It is therefore interesting to note that 8 cm (the surviving length of his pig flaps) scaled up by a factor of 2.25 is 18 cm, which happens to be the average length of the deltopectoral flap used in clinical practice. The second parallel relates to random flaps. As has been shown above the maximum length of a random pattern flap which will survive on a pig’s abdomen is about 6 cm. Multiplying this length by a factor of 2.25 gives approximately 12-5 cm (5 inches). Clinical evidence indicates that a random human flap probably has a maximum surviving length of this order, beyond which it cannot be increased irrespective of the size of the base, unless it is first delayed. The relative surface area of the animal should be borne in mind when designing and interpreting flap experiments to ensure that the flaps studied are of a size which is relevant to clinical practice. If Milton had taken this factor into account he would probably not have come to the conclusion that all flaps survive to the same length regardless of width, In fact he investigated very wide flaps, a conclusion not accepted in many quarters.
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some of them consisting of the entire skin of the ventral surface of the trunk, and did not apparently realise that flaps of this size were of no practical significance. SUMMARY Skin flaps in the pig raised superficial to the panniculus carnosus are random pattern flaps. The surviving length of such flaps increases with their width until a certain length is reached after which widening the base has no further effect. The statement by Milton reinforced by that of Daniel and Williams that the surviving length is not related to its width is only true of the larger flaps. When the surface area of the pig is compared with that of man, flaps in the pig comparable in size with those in use clinically, are within the range where the surviving length is dependent on the base width.
The author wishes to acknowledge his gratitude to the Research Committee, Liverpool Area Health Authority (T) f or Ji nancial support, and to Professor R. Shields,Department of Surgery, University of Liverpool, for his encouragement and for making laboratoryfacilities available. REFERENCES
DANIEL, R. K. and WILLIAMS, H. B. (1973). The free transfer of skin flaps by microvascular anastomoses. An experimental study and a reappraisal. Plastic and Reconstructive, Surgery 52, 16. DREYER, G., RAY, W. and AINLEY WALKER, E. W. (tgr2-IS). The size of the aorta in warm blooded animals and its relationship to the body weight and to the surface area expressed in a formula. Proceedings of the Royal Society, London, Series B, 86, 39. DUBOIS, D. and DUBOIS, E. F. (1915). The measurement of the surface area of man. Archives of Internal Medicine, 15, 868. GRABB,W. G. and SMITH, J. W. (1978). “Plastic Surgery”, p. 52. Boston: Little Brown &Co. MILTON, S. H. (1970). Pedicled skin flaps. The fallacy of the length: width ratio. British Journal of Surgery, 57, 502. STELL, P. M. and GREEN, J. R. (1975). The viability of triangular skin flaps. British Journal
of Plastic Surgery,
28, 247.