European Review for Medical and Pharmacological Sciences 2017; 21: 454-459 Quantitative difference of acute intraoperative expansion in various body regions

E. RAPOSIO, N. BERTOZZI

Department of Surgical Sciences, Plastic Division, University of Parma, Parma, Italy; Cutaneous, Mini-invasive, Regenerative and Unit, Parma University Hospital, Parma, Italy

Abstract. – OBJECTIVE: To investigate the ef- pansion could stretch the beyond its natural ficacy of intraoperative sustained limited expan- limit, reducing the closure tension of surgical sion (ISLE) by examining the ex vivo biomechan- and allowing immediate reconstruction. ical properties of acutely expanded skin flaps. MATERIALS AND METHODS: The technique can be performed under either lo- Fourteen fresh cal or general anesthesia. First, an adequate-sized male cadavers were tested. On both sides of each cadaver, a 4 × 10 cm, the laterally based flap was pocket is created, and a tissue expander is im- raised at the external auditory canal of the scalp planted. This is then positioned and held in place and a 15 × 8 cm, the proximately based flap was by a temporary suture with its tube exiting from raised at the lateral arm, anterior thorax, and later- one end. Finally, a cycle consisting of a 3-minute al thigh. For each body region, a flap on one side expansion followed by a 3-minute rest is repeated was subject to acute intermittent expansion, while three times. Each time, the expander is filled as the corresponding contralateral flap served as the control. Both control and acutely expanded flaps much as possible according to the tissue tolerance underwent stepwise loading to assess their bio- as revealed by capillary refilling and the firmness mechanical properties. of the implanted expander. After each load cycle, RESULTS: No dimensional changes were ob- the fill volume is increased, demonstrating the served in the acutely expanded flaps when com- occurrence of tissue recruitment. pared to the controls. Mean stiffness and strain Although a number of decades have passed values were not significantly different from control since Sasaki’s initial report, a consensus on values for flaps raised on the scalp, but statistically significant changes were found for those on the lat- the true efficacy of ISLE is yet to be reached. 2 eral arm, anterior thorax and lateral thigh (p < 0.05). For example, Abramo et al reported success- CONCLUSIONS: ISLE produced statistically ful cleft-palate repair for large defects using significant biomechanical improvements when a 5-mm Foley catheter, and Mackay et al3 applied to the flaps raised on the arm, thorax performed ISLE in a pig model, reporting that and thigh, leading to a significant gain in com- undermining the edges resulted in de- pliance. We suggest that the ineffectiveness of ISLE, when applied to scalp flaps, was due creased closure tension and that this goal could to the inelasticity of the galea aponeurotica. not be achieved via ISLE. However, Bartell and 4 Our findings confirm the general effectiveness Mustoe showed that the biomechanical proper- of acute skin expansion as means of reduc- ties of pig skin are significantly different from ing wound-closure tension after large skin ex- those of human skin, thereby diminishing the cisions; at least in regions other than the scalp. relevance of Mackay et al3 and other work5,6 Key Words: since it was performed using animal models. , Biomechanical phenomena, Hochman et al6 demonstrated that ISLE could Wound closure technique, Reconstructive surgery. effectively reduce wound closure tension, but when the degree of undermining achieved by the implant was matched surgically, no differ- Introduction ence between the techniques was observed. It is reported that ILSE is capable of inducing Background viscoelastic behavior in the affected skin, even The method of intraoperative sustained limited though the reduction in wound-closure tension expansion (ISLE) was first introduced by Sasaki mainly derives from the undermining neces- in 19871. He reported that acute intermittent ex- sary for insertion of the implant7.

454 Corresponding Author: Raposio Edoardo, MD; e-mail: [email protected] Quantitative difference of acute intraoperative expansion in various body regions

With this paper, we set out to assess the effi- the method of Sasaki1. The acute expansion was cacy of ISLE by examining the ex vivo biome- carried out while the researcher’s hand pressed on chanical properties of acutely expanded skin flaps the base of each flap, thus preventing excessive on the scalp the lateral arm, anterior thorax and undermining of the tissue, which could alter the lateral thigh8,9. results of the study. After acute expansion, the flaps were immediately measured to quantify any change in their size. Control and expanded flaps Materials and Methods were then raised from the underlying fascia and a rigid metal ruler was positioned at the base of For this study, 14 fresh male cadavers (mean each flap and fixed to the muscular fascial plane age at death, 64 years; ranging from 38 to 81 with a 4/0 nylon suture. Then a 1/0 Maxon suture years) were tested. The bodies were not subject to was passed full-thickness through each flap, 0.5 embalming or other preservation processes. cm lateral to the tip and 2.5 cm from the midpoint of the tip on both sides. Design of Scalp Flaps For all cadavers, a 4 × 10 cm, the laterally based Assessment of Acutely Expanded Flaps flap was raised from the external auditory canal and Data Collection on each side of the scalp. This was followed by 4 × Stepwise loading was performed by means 10 cm subgaleal undermining of both flaps to cre- of a dynamometer (FD111; Borletti, Florence, ate pockets for the tissue expander. The expander Italy) and a force transducer (D2000; Maywood (elliptical implant, 10 × 6 cm, 75 cc; Mentor, Santa Instruments Ltd., Hampshire, UK) connected to Barbara, CA, USA) was randomly inserted into the Maxon suture10-15. A 5-N increase in loading one of the bilateral pockets and the other pocket stress was applied for each step (range: 0 to 50 served as the control. Temporary wound closure N). The force was applied as fast as possible to was achieved using a continuous 1/0 silk suture. reduce the bias that can result from the viscous The stress cycle was performed as previously components of the flaps16. Flaps were not under described by Sasaki1. The flap started from the tension between the loading steps. For the flaps superior border of the ear lobe to reduce the risk of the scalp, each measurement took approxi- of further undermining due to implant expansion. mately 2 seconds. For flaps at the other body At the end of the acute expansion, the flaps were regions, the measurement took approximately 4 immediately measured to quantify any change in seconds. Raposio and Nordström10,11, Raposio et their size. Control and expanded flaps were then al12-14, Raposio15 previously demonstrated that this raised with the underlying galea aponeurotica. time interval was capable of eliciting viscoelastic A rigid metal ruler was positioned at the base of behavior of the skin; while the loading stress ap- each flap and fixed to the pericranium with a 4/0 plied did not result in a permanent change in the nylon suture. Then a 1/0 Maxon (Davis & Geck, flap length. Gosport, UK) suture was passed full-thickness During each loading step, the force applied and through each flap, 0.5 cm lateral to the tip and 1 the elongation obtained were recorded to create cm anterior and posterior to the midpoint of the tip. a load-elongation curve from which the stress/ strain relationship and the mean stiffness could Design of Flaps on the Lateral Arm, the be obtained. The biomechanical properties of Anterior Thorax and the Lateral Thigh the cutaneous tissue can be described in terms A 15 × 8 cm, the proximately based flap was of stress (force per unit of original cross section) raised on the lateral arm, anterior thorax and lat- and strain (change in length divided by the origi- eral thigh on both sides of each cadaver. Under nal length)17, with the stress/strain curve showing each flap, a subcutaneous pocket was created the relationship between the force (stress) and the starting from the 8-cm tip incisions. As above, resulting elongation (strain) for a given cross-sec- the expander (rectangular implant, 15 × 8 cm × tional area15. The slope of the stress-strain curve 6.5 cm, 680 cc; CUI Corporation, Santa Barbara, represents the stiffness of the cutaneous tissue CA, USA) was randomly inserted into the pocket and is given by the ratio of the applied force to the of one side only, while the contralateral pocket displacement of the flap8,9. Thus, the compliance served as the control. A continuous 1/0 silk suture of the flap is indirectly described by the mean was used to achieve temporary wound closure and stiffness: the greater the mean stiffness, the lower the stress cycle was again performed according to the compliance.

455 E. Raposio, N. Bertozzi

Statistical Analysis (load range: 0 to 5 N) but it gradually reduced The mean, standard deviation and standard er- (load range: 5 to 15 N) until the stress-strain ror were calculated for all outcomes. A two-tailed relationship became exponential due to the rap- paired t-test was used to compare control and idly increasing stiffness (load range: 15 to 50 N). treatment values. Differences were considered Mean stiffness values for all flaps are given in statistically significant if p was less than 0.05. Figure 1. Our previous work10 demonstrated that 15 N is the optimal closing-tension load at a suture when Results advancing a cutaneous flap; therefore, we graphed and compared the mean strain values of the flaps Data were successfully obtained from all flaps. when a 15-N stress was applied (Figure 2). No statistically significant dimensional changes were found in the acutely expanded flaps. Acutely Expanded Scalp Flaps The load-elongation curves were obtained for The difference between the stiffness values both control and acutely expanded flaps. The of acutely expanded (mean, 153.74 gr/mm; SD = tissue’s stress response to displacement (expan- ±15.4) and control (mean, 154.05 gr/mm; SD = sion) was visualized in both acutely expanded ±15.7) flaps was not statistically significant (p < and control flaps as a three-phase characteristic. 0.05). The mean strain of the acutely expanded Cutaneous tissue compliance was initially linear (mean, 10.893 mm; SD = ±2.478) and control

Figure 1. Mean stiffness of acutely expanded and control flaps under progressively increasing stress. The difference between expanded and control flaps was not statistically significant for those raised on the scalp (p > 0.05). In contrast, a statistically significant decrease was found for flaps raised on the lateral arm, anterior thorax and lateral thigh (p < 0.05).

456 Quantitative difference of acute intraoperative expansion in various body regions

Figure 2. Mean strains of acutely expanded and control flaps calculated when a 15-N load was applied. The difference between expanded and control flaps was not statistically significant for flaps raised on the scalp (p > 0.05). A statistically significant difference was found for flaps raised at the lateral arm, anterior thorax and lateral thigh (p < 0.05).

(mean, 10.869 mm; SD = ±2.431) scalp flaps un- performed using a force that was applied ho- der a 15-N stress also did not show any statistical- mogenously to the skin flap and parallel to the ly significant difference (p < 0.05). surrounding skin surface in order to minimize the influence of anisotropy. Conversely, the vis- Acutely Expanded Flaps on the Lateral coelasticity of skin is essential to the efficacy Arm, Anterior Thorax and Lateral Thigh of ISLE in reconstructive surgery. Cutaneous The difference between the stiffness values of tissue shows both viscous and elastic properties. acutely expanded and control flaps raised at the When low stress is applied, skin acts as an elas- same body region (contralaterally) was statistical- tic material; it demonstrates immediate strain ly significant (p < 0.05). The same was true of the but it returns to its original state as soon as the mean strain values for flaps in these regions (p < force is removed. However, under higher stress, 0.05; applied stress, 15 N). it behaves like a viscous material and strain be- comes a function of both stress and time. This leads to the time-dependent phenomena of creep Discussion and stress relaxation that are routinely exploited in the acute intermittent expansion. Mechanical Unlike many engineering materials, cutane- creep refers to the increase in the length of the ous tissue is a living heterogeneous substance, skin when it is placed under a constant stress. composed of different biological materials and When the stress applied is sufficiently high, capable of responding to physical stimuli. In- slight creep can occur shortly afterward as a deed, non-linearity, anisotropy and viscoelastic- consequence of collagen-fiber straightening and ity are all characteristic of the skin’s mechanical displacement of interstitial fluid. Stress relax- behavior17. Therefore, the stress cycles were ation is the reduction of the force required when

457 E. Raposio, N. Bertozzi the skin is kept under constant tension by a giv- wound-closure tension after a large skin excision. en strain. Serial excision of large lesions relies The technique produced significant gains in skin- on this stress-relaxation response of the skin. flap compliance (8.5-15.5%) in all tested body In our work, the biomechanical properties of regions, with the notable exception of the scalp. acutely expanded (ISLE) and control flaps were We suggest that the absence of an effect at the determined using an ex vivo model. No sta- scalp was due to the inelasticity of the galea apo- tistically significant dimensional changes were neurotica, but further researches will be required observed in the acutely expanded flaps, but sig- to test this hypothesis. nificant changes in their tensiometric properties were found. Under a 15-N stress, the mean stiff- ness of acutely expanded flaps on the lateral arm, lateral thigh and anterior thorax was significantly Authors’ declaration of personal interests: decreased versus that of corresponding contra- Edoardo Raposio has not served as a speaker, con- lateral control flaps, which were subcutaneously sultant or advisory-board member for any organiza- undermined but not subjected to expansion. This tion. He is not an employee of any organization and corresponded to respective compliance gains of does not own stocks or shares in any organization. 15.48%, 8.48% and 14.44% for flaps on the lateral Nicolò Bertozzi has not served as a speaker, consul- tant or advisory-board member for any organization. arm, anterior thorax and lateral thigh. According He is not an employee of any organization and does to our results, acute skin expansion appears to be not own stocks or shares in any organization. The au- an effective means of reducing wound-closure thors, Nicolò Bertozzi and Edoardo Raposio, declare tension. The gains obtained were similar to those that they have no conflicts of interest. reported by Chretien-Marquet18 (10.5%) but con- siderably smaller than those reported by Auletta et al19 (36%). In contrast, acute expansion of scalp flaps did Declaration of funding interests: not induce any compliance gain over the sim- This study, including the preparation of this manu- ple subgaleal undermining of the controls; mean script, did not receive any funding. Initial data analy- stiffness, tissue compliance and flap lengths were sis was performed by the authors. not statistically different between the two groups. Our data was acquired from cadaveric rather than living tissue; therefore, one could argue that ISLE References relies on biological properties of the skin that are lost postmortem. However, acute expansion of 1) Sasaki GH. Intraoperative sustained limited ex- flaps in regions of the body other than the scalp pansion (ISLE) as an immediate reconstructive did produce significant biomechanical improve- technique. Clin Plast Surg 1987; 14: 563-573. ments; hence we regard our model as effective 2) Abramo AC, Viola JC, Angelo AJ. Intraoperative and this has been demonstrated by other clinical rapid expansion in cleft palate repair. Plast Re- studies18,19. A more consistent explanation for our constr Surg 1993; 91: 441-444. scalp results might be that flaps raised here differ 3) Mackday DR, Saggers GC, Kotwal N, Manders EK. from those elsewhere in the body, owing to the Stretching skin: undermining is more important presence of the galea aponeurotica. The galea than intraoperative expansion. Plast Reconstr Surg 1990; 86: 722-730. aponeurotica is an inelastic membrane between 4) Bartell TH, Mustoe TA. Animal models of human the subcutaneous connective tissue and the loose tissue expansion. Plast Reconstr Surg 1989; 83: connective tissue of the pericranium. Its inelastic- 681-686. ity might prevent the acute intermittent expansion 5) Aboelatta YA, Elshahm A, Saleh MA, Kamel IH, Aly from inducing mechanical creep in the overlying HM. Intraoperative and delayed wound approx- skin. To the best of our knowledge, no study has imation in closure of skin defects in different yet been carried out to examine this hypothesis. areas. J Wound Care 2015; 24: 600-605. 6) Hochman M, Branham G, Thomas JR. Relative ef- fects of intraoperative tissue expansion on wound closing tension. Arch Otolaryngol Head Neck Conclusions Surg 1992; 118: 1185-1187. 7) Fan J, Raposio E, Nordström REA. Filling Policy. In: Our findings confirm the effectiveness of Tissue Expansion, Edited by R.E.A. Nordström, acute intermittent skin expansion for reducing Butterworth Heinemann, 1996; pp. 40-47.

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