Revascularization After H-plasty Reconstructive Surgery in the Periorbital Region Monitored With Laser Speckle Contrast Imaging

Background:

H-plasty reconstructive surgery is commonly used to close defects after tumor excision in the periorbital region. Revascularization of the bipedicle skin flaps is essential for healing. However, it has not previously been possible to study this revascularization in humans due to the lack of noninvasive perfusion monitoring techniques. The aim was to monitor perfusion in H-plasty flaps during surgery and during postoperative follow-up, using laser speckle contrast imaging.

Method:

H-plasty, i.e., bipedicle random advancement skin flaps, was used for reconstruction of the eyelids after tumor removal in 7 patients. The median length and width of the skin flaps were 13 mm (range, 8–20 mm) and 10 mm (range, 5–11 mm), respectively. Blood perfusion was measured using laser speckle contrast imaging during surgery and at follow up 1, 3, and 6 weeks postoperatively, to monitor revascularization.

Results:

Immediately postoperatively, the perfusion in the distal end of the flaps had fallen to 54% (95% CI, 38%–67%). The perfusion then quickly increased during the healing process, being 104% (86%–124%) after 1 week, 115% (94%–129%) after 3 weeks, and 112% (96%–137%) after 6 weeks. There was no clinically observable ischemia or tissue necrosis.

Conclusions:

Revascularization of the H-plasty procedure flaps occurs quickly, within a week postoperatively, presumably due to the existing vascular network of the flap pedicle, and was not dependent on significant angiogenesis. This perfusion study confirms the general opinion that H-plasty is a good reconstructive technique, especially in the periorbital region with its rich vascular supply.

Revascularization of the H-plastic procedure flaps occurs quickly, within a week postoperatively, presumably due to the existing vascular network of the flap pedicle.

H-plasty, using bipedicle advancement flaps, is often used to repair defects after tumor surgery in the head and neck region. There are several benefits of using advancement flaps compared to free skin grafts or secondary intention healing, including a good match of skin color and texture, the flaps have their own blood perfusion, and there is less contraction during healing.¹ Successful design of the advancement flaps depends on understanding the vascular supply and the process of revascularization.¹ To the best of the authors’ knowledge, no study has yet been carried out to assess the perfusion in H-plasty procedures using modern imaging techniques.

Perfusion monitoring has traditionally been performed through clinical examination, as first described by the Italian Renaissance surgeon, Gaspare Tagliacozzi, i.e., by feeling the temperature of the skin, observing the color, and measuring the capillary refill time.² Over the years, techniques such as fluorescence angiography with sodium fluorescein³ and indocyanine green angiography⁴ and thermal imaging have been tried but are invasive techniques not appropriate for repeated monitoring. Laser-based techniques are noninvasive and have recently gained ground in the monitoring of flap perfusion during reconstructive surgery. Laser speckle contrast imaging (LSCI) is a noninvasive technique that provides rapid assessment of perfusion over a wide area with high resolution. The technique relies on the scattering of coherent laser light by moving particles in the illuminated tissue, forming a speckle pattern that contains information on the concentration and speed of the moving particles, i.e., blood cells.⁵ Laser speckle contrast imaging has been used in studies of microvascular blood perfusion in plastic reconstructive procedures,^6–8 burns,⁹ and wound healing¹⁰ to gain deeper knowledge on blood perfusion and the healing process. It has also been used to detect systemic microvascular dysfunction in several vascular pathologies,¹¹ including Alzheimer’s disease, schizophrenia, hypertension, renal disease, diabetes, peripheral vascular disease, atherosclerotic coronary artery disease, heart failure, and systemic sclerosis.¹² However, although LSCI can be used to assess perfusion in flap surgery, and theoretically provide objective measures for optimizing surgery, its use is not yet widespread in the clinical setting.

The aim of this study was to investigate the possibility of using LSCI to measure the blood perfusion and revascularization of the flaps in the H-plasty procedure in the periorbital area.

METHODS

Ethics.

The experimental protocol was approved by the Ethics Committee at Lund University, Sweden. Research was carried out in accordance with the ethical principles of the Declaration of Helsinki, as amended in 2008. Fully informed consent was obtained from all the participating patients.

Subjects.

Seven patients, 1 woman and 6 men, undergoing reconstructive surgery after tumor excision in the periorbital area at Skåne University Hospital in Lund, Sweden, between March 2019 and December 2019 were included in the study. The median age was 73 years (45–91 years). Surgery was performed by 2 experienced senior surgeons. Medical factors that may affect microcirculation and healing were recorded. Three patients had cardiovascular disease, all of whom were taking anticoagulation medication and this medication was not suspended. Two patients had known hypertension and were taking antihypertensive drugs. One of them was taking β-blockers at the time of surgery. No patient had diabetes, and none was taking steroid medication. One patient smoked on a daily basis, and 2 had quit smoking more than 40 years ago. No patient had had previous radiotherapy in the periorbital area. The characteristics of patients and flaps are presented in Table.

Patient characteristics

Patient	Gender	Age (y)	Tumor type	Tumor location	Flap size: length (horizontal) × width (vertical) (mm)	Flap thickness
1	Male	86	Nodular basal cell carcinoma	Lower eyelid	Medial flap: 20 × 10 Lateral flap: 10 × 10	Skin and orbicularis muscle
2	Male	55	Squamous cell carcinoma in situ	Lower eyelid	Medial flap: 13 × 10 Lateral flap: 13 × 10	Skin and orbicularis muscle
3	Male	71	Infiltrative basal cell carcinoma	Lower eyelid	Medial flap: 10 × 5 Lateral flap: 8 × 7	Skin and orbicularis muscle
4	Male	91	Infiltrative basal cell carcinoma	Lower eyelid	Medial flap: 19 × 10 Lateral flap: 10 × 10	Skin
5	Male	73	Squamous cell carcinoma in situ	Upper eyelid	Medial flap: 13 × 11 Lateral flap: 14 × 10	Skin
6	Female	45	Nodular basal cell carcinoma	Lower eyelid	Medial flap: 15 × 6 Lateral flap: 10 × 10	Skin and orbicularis muscle
7	Male	82	Nodular basal cell carcinoma	Lower eyelid	Medial flap: 11 × 10 Lateral flap: 13 × 10	Skin and orbicularis muscle

Surgical Procedure.

Surgery was performed under local anesthesia using 20 mg/ml lidocaine (Xylocaine; AstraZeneca, Södertälje, Sweden). Adrenalin was not used to prevent interference with the perfusion measurements. An H-plasty reconstructive procedure was performed (see Fig. 1). Cutaneous bipedicle flaps were created by making 2 incisions through the skin and then subcutaneously undermining the flaps and the surrounding skin to allow flap movement and to minimize tension. In 5 patients, the flaps included the skin and the underlying orbicular muscle, while in the other 2, the flaps consisted of skin only. No Burow’s triangle excisions were made. The median horizontal length of the flaps thus created was 13 mm (range, 8–20 mm), and the median vertical width was 10 mm (range, 5–11 mm). Diathermy (25 W, bipolar, KLS Martin ME102; KLS Martin, Tuttlingen, Germany) was used with caution and avoided at the base of the flap, as the authors have found in a previous study that repeated diathermy at the base of the flap significantly affected the blood perfusion and probably caused the flap to function more like a free graft than a flap.¹³ Resorbable 5-0 Vicryl sutures were placed subcutaneous to reduce tension on the suture lines, and the skin was sutured using nonresorbable 6-0 Ethilon sutures (both from Ethicon, Somerville, NJ, U.S.A.). No dressing was applied after surgery. Blood pressure was not monitored intraoperatively or postoperatively. The skin sutures were removed after 1 week.

FIG. 1.

Representative photographs showing the H-plasty procedure and the sites at which perfusion was measured. A, The location of a basal cell carcinoma in the lower eyelid, and dotted lines indicating its excision and the extent of the bipedicle advancement flaps. B, The result 1 week postoperatively. The white circles indicate where perfusion was measured at the distal ends of the flaps. The red circle indicates the area in which the reference value of perfusion (baseline) was measured.

Laser Speckle Contrast Imaging.

Blood perfusion was monitored using an LSCI instrument (PeriCam PSI NR System; Perimed AB, Stockholm, Sweden). The skin area of interest is illuminated by an infrared 785 nm laser light. Dark and bright areas are created by interference of the light backscattered from moving particles in the illuminated area, creating a speckled pattern. This pattern is recorded in real time by a camera, with up to 100 images per second, and at a spatial resolution up to 100 μm/pixel. Perfusion is automatically calculated by the system by analyzing the variations in the speckle pattern. Perfusion was assessed at the distal ends of the flaps, as shown in Figure 1B, and is expressed in arbitrary units, perfusion units.

Perfusion was monitored immediately postoperatively (denoted 0 weeks) and on 3 follow-up occasions. Due to logistic reasons, the time of the follow-up visits varied. The data were therefore grouped into the following time intervals: follow up at 7 to 8 days (denoted 1 week), 19 to 28 days (denoted 3 weeks), and 33 to 45 days (denoted 6 weeks).

Calculations and Statistics.

The perfusion in the flap was calculated as a percentage of the perfusion at a reference point (baseline) just outside the flap, in undissected tissue (see Fig. 1B). The reference point was infiltrated with local anesthesia in the same way as the surgical area. The reference point was measured at each follow-up clinic visit. Biologic zero values were obtained by mechanically occluding the vasculature gently at the pedicle base using a Dieffenbach clamp, before suturing the flaps and the values were then subtracted. Values of perfusion, expressed as median values with 95% CIs, were obtained during surgery right after the flaps were sutured in place and on 3 follow-up occasions.

Statistical analysis was performed using the Kruskal–Wallis test with Dunn test for multiple comparisons and the Mann–Whitney test for single comparisons. Significance was defined as: p < 0.05 (*), p < 0.01 (**), p < 0.001 (***), p < 0.0001 (****), and p > 0.05 (not significant). Calculations and statistical analysis were performed using GraphPad Prism 8.3 (GraphPad software Inc., San Diego, CA, U.S.A.).

RESULTS

Surgical Outcome.

All flaps were viable at follow up. One patient had to have secondary surgery due to postoperatively developed ectropion of the lower eyelid. Another patient also developed minimal ectropion but was satisfied with the result and did not want further surgery. Both functional and esthetic results were excellent in all other cases.

Blood Perfusion Monitoring.

The perfusion at the distal end of the flaps decreased to 54% (95% CI, 38%–67%) during surgery. Revascularization was rapid, and perfusion had increased to 104% (95% CI, 86%–124%) 1 week after surgery (p < 0.0001). Perfusion remained high during the remaining follow-up period, being 115% (95% CI, 94%–129%) after 3 weeks and 112% (95% CI, 96%–137%) after 6 weeks, indicating hyperperfusion during the healing process. Figure 2 shows a representative example of perfusion monitored with LSCI, and Figure 3 shows the results for the whole group.

FIG. 2.

Representative laser speckle contrast imaging (LSCI) from 1 patient who has undergone H-plasty on the lower left eyelid using bipedicle advancement flaps. The LSCI images show the perfusion of the flaps directly after surgery (0 weeks) and the revascularization after 1, 3, and 6 weeks postoperatively. The dotted white lines indicate the extent of the flaps. The scale bar is 10 mm. PU, perfusion units.

FIG. 3.

Blood perfusion in the advancement flaps, immediately postoperatively (0 weeks), and at follow up after 1, 3, and 6 weeks. Data are expressed as the percentage (median values and 95% CIs) of the perfusion in a reference area just outside the flaps (100%, baseline) and values obtained in the occluded flap, intraoperatively (0%), were subtracted. n.s., not significant.

There was no significant difference in the perfusion in the flaps consisting of skin only (median = 102%; 95% CI, 94%–118%) compared to flaps consisting of skin and orbicularis muscle (107%; 95% CI, 72%–147%) (p > 0.3); or short (≤10 mm) (median = 97%, 95% CI, 81%–136%) compared to long flaps (>10 mm) (median = 110%; 95% CI, 72%–147%) (p > 0.3); or medial (median = 96%; 95% CI, 81%–146%) compared to lateral raised flaps (114%; 95% CI, 72%–136%) (p > 0.3), recorded immediately postoperatively.

DISCUSSION

Good blood perfusion and revascularization are vital when performing reconstructive surgery using flaps. The results of the present study show that perfusion in the flaps formed in H-plasty reconstruction is impaired immediately after surgery. The authors have previously shown that the blood perfusion in flaps during a blepharoplasty procedure decreased gradually from the base to the tip of the flap; the flap being well perfused only in the proximal 1 cm (≈40%–60%) and decreasing rapidly beyond 2 cm (≈20%).^8,13 Similar findings were made in the authors’ previous studies on porcine skin flaps.^14,15 The lengths of the flaps in the present study were 8 to 20 mm and had a median perfusion at the distal end of the flap of 54%, which is in line with the results of previous studies.

Revascularization of the flaps in this study was rapid, being 104% only 1 week after surgery. Revascularization has been studied extensively in flap models in animals, also showing that revascularization is rapid. Young¹⁶ studied the revascularization of pedicle skin flaps in a porcine model by injecting disulfine blue and observed new vascular connections between the distal viable region and the surrounding skin 3 to 4 days after surgery, and the whole flap had developed a collateral vascular supply 7 to 10 days after surgery. Cumming and Trachy¹⁷ used a porcine model to study perfusion in panniculus carnosus myocutaneous flaps using laser Doppler and a dermofluorometer and found that flap perfusion was adequate for survival without the pedicle 7 to 10 days after surgery. Tsur et al.¹⁸ studied revascularization of axial flaps in porcine and rat models and found that it was sufficient to sustain flap survival after 6 to 7 days in rats and after 4 to 5 days in pigs. They found that neovascularization started simultaneously from the wound edges and the wound bed, although adequate neovascularization from the wound bed appeared to be more important.¹⁸ These studies indicate rapid revascularization, which is supported by the authors’ findings. The reason for the rapid revascularization in bipedicle advancement flaps is probably that there is already a vascular network connected to the circulation via the flap pedicle. However, in a free skin graft, revascularization depends on angiogenesis throughout the graft, and revascularization can be expected to take longer. In a previous study, the authors examined the revascularization of free skin grafts in the Hughes procedure and found that 3 weeks were required to reach 50% revascularization and 8 weeks for complete revascularization.⁶

The H-plasty healed well in all cases, and no tissue necrosis was seen. This was expected, as the periorbital area is known to be forgiving for plastic reconstructive surgical procedures due to the rich vascular supply. Random flaps are known to be more viable in the face than elsewhere, viability decreasing with the distance from the face.¹⁹ The results of this study may be useful in other areas of reconstructive surgery where the conditions for healing are not as favorable.

The values of perfusion were found to exceed the baseline values 1 to 3 weeks postoperatively. The wound healing process consists of 4 overlapping phases: hemostasis (0 to several hours after the trauma), inflammation together with vasodilation (1–3 days), proliferation with restoration of the vascular network (4–21 days), and remodeling (21 days to 1 year).²⁰ It is, therefore, not surprising to see hyperperfusion in the postoperative healing phase. If the perfusion had been monitored the area for a longer period, the authors may have seen the perfusion return to the baseline value.

One limitation of this study is that the effect of surgical vasospasm on the reduction in perfusion immediately postoperatively could not be determined. It is well known that surgical vasospasm may occur around the flap pedicle.²¹ To determine the contribution of surgical vasospasm, it would have been necessary to make measurements during the hours following surgery. However, patients often have to travel far for this kind of surgery, and it would have been unlikely that they would have agreed to remain at the hospital for several hours after surgery. Abstinence from the use of epinephrine in the local anesthetic also deviates from the practice of many surgeons, especially given that such additives are rarely withheld due to concerns regarding vasculopathic risk factors. However, it cannot be deduced from the results of the present study whether this had any impact on the results.

Another limitation is the limited size of the study group. Analyses were carried out with regard to the location, thickness, and length of the flap, but the residual did not reach statistical significance. It could be assumed that perfusion would be greater in skin flaps including orbicularis muscle. This was investigated in one of the authors’ previous studies in pigs, showing higher perfusion in thick flaps than in thin flaps.¹⁵ A larger study must be performed in humans to investigate the effects of this. Nor was the sample size large enough to investigate whether age or impaired blood perfusion due, for example, to previous radiotherapy, cardiovascular disease, diabetes mellitus, or smoking affected the outcome of the surgery and the revascularization process. Perfusion measurements in the patient who was a smoker showed that tissue perfusion was no worse intraoperatively or postoperatively than in any of the other patients. However, there were too few patients to draw any reliable conclusions.

No hematoma was seen in the patients at clinical examination postoperatively. The presence of a postoperative hematoma would most likely reduce the LSCI signal because the system uses an invisible near-infrared laser (785 nm), which is within the range of light absorption of hemoglobin. Stationary blood cells and cell remnants (after hemolysis) would most likely have a signal blocking effect, probably proportional to the thickness of the hematoma. In the authors’ measurements, the authors did not observe any suspected artifacts in signal due to hematoma.

Laser speckle contrast imaging could easily be implemented in clinical routine in reconstructive surgery, because it is noninvasive, and the measurements are not very time-consuming. However, problems associated with motion artifacts must first be overcome. Methods of, at least partially, overcoming these, such as shorter sampling times or simultaneously recording the signal backscattered from an adjacent opaque surface, have been suggested.²² Laser speckle contrast imaging monitoring would be particularly important in flaps or grafts that risk failure, i.e., when the geometry or size of the flap indicates a risk of poor perfusion, or when the patient has poor microcirculation, as in the case of diabetics or smokers. If graft failure could be identified early, timely revision could be carried out and the healing process optimized. In procedures such as the Tagliacozzi flap and the paramedical flap procedure where the pedicle is usually cut after 3 weeks, when the revascularization of the mobilized tissue is deemed to be adequate. LSCI could be used to assess flap perfusion, allowing the pedicle to be cut earlier. This would also optimize the surgical outcome.

In conclusion, the results of the present study suggest that bipedicle advancement flaps in H-plasty procedures are adequately perfused postoperatively and that they are revascularized quickly, confirming the general surgical experience that the rich vascular supply of the periorbital region is forgiving for reconstructive surgery.

ACKNOWLEDGMENTS

This study would not have been possible without the help and encouragement of Maria Schalén and all the other surgical staff involved at Skåne University Hospital in Lund, Sweden.