Original Investigation

Long-term Histopathologic Study of the Frontalis Muscle Flap After Frontalis Suspension for Severe Ptosis Repair Chong Zou, M.D., Jia-Qi Wang, M.D., Xin Guo, M.D., Hao Yu, M.D., Xiu-Qi Li, M.D., Wu-Yan Li, M.D., and Tai-Ling Wang, M.D. Plastic Surgery Hospital, Chinese Academy of Medical Sciences, and Peking Union Medical College, Beijing, People’s Republic of China

Purpose: To investigate the long-term histopathologic changes of the frontalis muscle flap after frontalis muscle flap suspension for severe ptosis repair. Methods: Eight 3-month miniature pigs were selected as the experimental animals, and self-comparison was used. The experimental side of the upper eyelid was constructed to have severe ptosis by resection of the levator aponeurosis, while the other side served as the control. Samples of the upper eyelid composite at 6 months and 12 months after ptosis repair were obtained and studied through light microscopy and transmission electron microscopy. Results: The histopathologic study revealed that the frontalis muscle flap kept viable with normal muscular structure and direction 6 months and 12 months after the frontalis suspension procedure. Conclusions: The frontalis muscle flap appears to be a suitable material for frontalis suspension technique because of its feasibility and histopathologic stability. (Ophthal Plast Reconstr Surg 2013;29:486–491)

S

evere eyelid ptosis is defined as a ptosis >4 mm and, most importantly, levator muscle function that provides 4 mm and

down to the upper rim of the tarsus and fixed appropriately with 3 horizontal mattress sutures (Fig. 2). The skin was closed with sutures.

Histologic

RESULTS

Fig. 2.  A–C, Severe blepharoptosis was repaired by frontalis muscle suspension techniques.

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covered the midpapillary line (Fig. 3A,C). Immediately after surgery, the upper palpebral margin was elevated to about 1 mm above the upper margin of the cornea. The upper palpebral margin reduced by 1 mm 3 months after surgery. Six months after the surgical repair of blepharoptosis with the frontalis muscle suspension technique, the experimental eyes looked practically the same as the control side because the upper eyelid was located above the upper border of the cornea with a good shape and curve (Fig. 3B,D). There were no obvious recurrences and downward displacements of the eyelid 1 year after the operation. Histologic Observation Light Microscopy. Histologic examination of the eyelid on the control side with trichrome stain included the skin, glandular appendages, loose connective tissue, orbicularis muscle, tarsus, and levator aponeurosis. The frontalis muscle fibers were distributed evenly without obvious collagen fiber infiltration. The vertically oriented fibers of the frontalis muscle extended to and were interlaced with the horizontally oriented orbicularis muscle (Fig. 4). The 6-month specimen from the experimental eyes showed an approximately normal structure and direction of the frontalis muscle fibers with slight branching off of the terminal muscle fibers and infiltration of collagen fibers. There were chronic inflammation reactions at the end of the frontalis muscle flap, which were chiefly composed of lymphocytes, histiocytes, epitheloid cells, foreign body-type giant cells, and neonate small vessels (Fig. 5). The 12-month specimens from the experimental eyes showed conserved muscular structure with much proliferated nervous system tissue and some collagen fibers. The inflammatory reaction had disappeared (Fig. 6).

Transmission Electron Microscopy. The myofibrils of the control side at 6 months and 12 months showed a regular arrangement with distinct sarcomere structures and Z-lines. The specimens from the experimental side at 6 months and 12 months showed no obvious differences from the control side. The specimens showed orderly arranged myofibrils with distinct sarcomere units and Z-lines. The mitochondria were distributed normally, and there was no atrophy of the myofibrils (Fig. 7).

DISCUSSION Blepharoptosis is a common ophthalmic disease. If untreated, amblyopia may develop. Lin et al.13 reported a 21.5% incidence of amblyopia in children with congenital ptosis, with no new cases of amblyopia after surgical correction of blepharoptosis. Frontalis suspension surgery is effective for correcting congenital ptosis with poor levator function.4 Frontalis suspension techniques can be grouped into 2 categories: indirect usage and direct usage of frontalis muscle strength. The indirect frontalis sling techniques require alloplastic or autologous tissue that connects the frontalis muscle and the ptotic eyelid. These techniques depend on the structural durability and permanency in the position of the implanted materials for longevity of the results. Among these sling biomaterials, the autogenous fascia lata is believed to be the best biomaterial for blepharoptosis surgery with comparably low rates of recurrent ptosis and infections.14 However, they require a second operative site and additional surgical time. Alloplastic, such as monofilament

FIG. 3.  A and C, One month after the severe ptosis models were constructed. Two weeks (B) and 6 months (D) after repair of severe ptosis using a frontalis muscle flap suspension technique.

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FIG. 4.  A, Photomicrograph of the pig eyelid shows skin, glandular appendages, loose connective tissue and the orbicularis muscle (OM), levator aponeurosis, tarsus, and conjunctiva resembling human anatomy (Masson trichrome stain, ×2.5). B, The vertically oriented fibers of the frontalis muscle (FM) extended to and were interlaced with the horizontally oriented OM (hematoxylin-eosin, ×5).

nylon, silicone, and polytetrafluoroethylene, and banked fascia lata were also common. However, they have the risks of foreign body reactions, absorption, infection, and granuloma formation. The direct usage of frontalis muscle motion, namely the frontalis muscle flap suspension and its modified techniques, is the prevalent alternative method in Asian countries. The frontalis muscle flap suspension technique, which was first introduced by Song and Zhao15 in 1985 and reformed by many scholars, forms a frontalis muscle flap and advances into the orbit to suspend the tarsus plate directly. There were several studies that investigated the histologic changes of various suspension materials. However, there have been no studies on histologic changes of the frontalis muscle flap. Ethical issues and limits on the availability of the tissue have prevented researchers from directly studying patients. Therefore, it was necessary to develop an animal model of severe ptosis. Pfaff16 described pig eyelids as having

FIG. 5. The 6-month specimen from the experimental eyelid showed an approximately normal structure and the direction of the frontalis muscle fibers with slight branching off of the terminal muscle fibers and infiltration of collagen fibers. There were chronic inflammation reactions at the end of the frontalis muscle flap, which were chiefly composed of lymphocytes, histiocytes, epitheloid cells, foreign body-type giant cells, and neonate small vessels (hematoxylin-eosin, ×5).

a similar gross and histologic structure to human eyelids and considered pigs as a good teaching model for eyelid margin repairs. The authors found a pig’s upper eyelid region to be similar to its human counterpart and developed it as a severe ptosis model. In this study, all the experimental upper eyelids developed typical severe ptosis after the models were constructed. The second-stage frontalis muscle suspension operation resulted in a good clinical effect with the experimental sides appearing similar to the control sides. This indicated that the model highly resembled the clinical characteristics of severe blepharoptosis. Jeong et al.10 reported experimental studies on rabbits that indicated collagen fiber replacement was first noticed at 4 weeks, and complete replacement by collagen fibers with a haphazard arrangement in the implanted material was seen at 8 weeks. The prolene specimens were surrounded by fibroblast proliferation from 4 weeks after surgery without collagen tissue replacement, but the silicone band specimens were surrounded by fibroblastic proliferation from 2 to 4 weeks and then replaced by dense collagenous fibrous bands. Kook et al.9 reported that the supramid undergoes morphologic degradation by hydrolysis after implantation, and this change might be considered one of the possible factors that facilitate the recurrence of ptosis. Fogagnolo et al.17 studied the stability of silicone band frontalis suspension for the treatment of severe unilateral blepharoptosis in infant. He found that the MRD reduced by 0.6 mm within the first 3 months after surgery and 0.2 mm between 3 and 12 months after surgery. Then the MRD kept unchanged since 12 months after surgery. In the study by Lee et al.3 on frontalis sling operation using silicone rod compared with preserved fascia lata for congenital unilateral ptosis repair, the postoperative MRD reduced by 0.3 mm in silicone rod group and 0.6 mm in preserved fascia lata group between 3 months and 6 months after surgery. Between 6 months and 12 months after surgery, the MRD reduced 0.1 mm and 0.3 mm in silicone rod group and preserved fascia lata group, respectively. In this study, the upper palpebral margin reduced by about 1 mm 3 months after surgery. Between 3 months and 12 months after surgery, the height of upper eyelid appeared to be unchanged. The findings of this study were similar with those of the study by Lin et al. about silicone rod, which the height of upper eyelid kept relatively stable since 3 months after surgery.

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FIG. 6.  A and B, The 12-month specimen from the experimental eyelid showed a conserved muscular structure with much proliferated nervous system tissue and some collagen fibers. The inflammatory reaction had disappeared (A, Masson trichrome, ×2.5; B, hematoxylin-eosin, ×5).

The histopathologic study showed that the frontalis muscle flap kept viable with the normal muscle fiber structure and direction 1 year after the frontalis suspension procedure. There was no obvious degeneration and fibrosis of the frontalis muscle flap. Therefore, the frontalis muscle flap could deliver the contractile force and tension of the frontalis muscle dynamically long-term. The elasticity of the eyelid could also be preserved. The technical feasibility and histologic stability of the frontalis

muscle flap made it appropriate for severe ptosis repair, which may produce long-lasting and natural effects. There are limitations to this study. The authors aimed at investigating long-term histopathologic changes of the frontalis muscle flap. Because of the limitation of the sample size and tissue availability, they did not take short-term samples for histopathologic observation. Furthermore, due to the difficulty in making pigs cooperative, it was impossible to perform measurements and statistics of the results of surgery of the pigs. It might also be better if comparisons were made of different suspension materials directly. In conclusion, this study developed a new animal model of severe eyelid ptosis. The results may provide insight into making choices about frontalis muscle flap suspension procedures for severe ptosis repair. Additional studies with a large sample and direct comparison of different suspension materials are still needed to further comprehend the frontalis suspension techniques.

References

FIG. 7. The myofibrils of the control side at 6 months (A, ×10,000) and 12 months (C, ×17,000) showed a regular arrangement with a distinct sarcomere structure and Z-lines. The specimens from the experimental eyelid at 6 months (B, ×10,000) and 12 months (D, ×10,000) showed no obvious differences from the control side. The specimens showed orderly arranged myofibrils with a distinct sarcomere unit and Z-lines. Mitochondria were distributed normally, and there was no atrophy of the myofibrils.

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1. Callahan MA, Beard C. Beard’s Ptosis. 4th ed. Birmingham, AL: Aesculapius Publishing, 1990. 2. Ramirez OM, Peña G. Frontalis muscle advancement: a dynamic structure for the treatment of severe congenital eyelid ptosis. Plast Reconstr Surg 2004;113:1841–9; discussion 1850–1. 3. Lee MJ, Oh JY, Choung HK, et al. Frontalis sling operation using silicone rod compared with preserved fascia lata for congenital ptosis a three-year follow-up study. Ophthalmology 2009;116:123–9. 4. Yoon JS, Lee SY. Long-term functional and cosmetic outcomes after frontalis suspension using autogenous fascia lata for pediatric congenital ptosis. Ophthalmology 2009;116:1405–14. 5. Friedhofer H, Nigro MV, Sturtz G, et al. Correction of severe ptosis with a silicone implant suspensor: 22 years of experience. Plast Reconstr Surg 2012;129:453e–60e. 6. Zhang HM, Sun GC, Song RY, et al. 109 cases of blepharoptosis treated by forked frontalis muscle aponeurosis procedure with long term follow-up. Br J Plast Surg 1999;52:524–9. 7. Park DH, Lee SJ, Song CH. Recurrence of blepharoptosis after a superiorly based muscle flap: treatment by frontalis muscle advancement. Plast Reconstr Surg 2005;116:1954–9. 8. Lai CS, Chang KP, Lai CH, et al. A dynamic technique for the treatment of severe or recurrent blepharoptosis: frontalis-orbicularis oculi muscle flap shortening. Ophthalmologica 2009;223:376–82. 9. Kook KH, Lew H, Chang JH, et al. Scanning electron microscopic studies of Supramid Extra from the patients displaying recurrent ptosis after frontalis suspension. Am J Ophthalmol 2004;138:756–63. 10. Jeong S, Ma YR, Park YG. Histopathological study of frontalis suspension materials. Jpn J Ophthalmol 2000;44:171–4.

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11. Choi S, Shin JH, Cheong Y, et al. Nanostructural investigation of frontalis sling biomaterial surfaces. Scanning 2011;33:419–25. 12. Zou C, Wang JQ, Guo X, et al. Pig eyelid as a teaching model for severe ptosis repair. Ophthal Plast Reconstr Surg 2012;28:472–4. 13. Lin LK, Uzcategui N, Chang EL. Effect of surgical correction of congenital ptosis on amblyopia. Ophthal Plast Reconstr Surg 2008;24:434–6. 14. Leibovitch I, Leibovitch L, Dray JP. Long-term results of frontalis suspension using autogenous fascia lata for congenital

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ptosis in children under 3 years of age. Am J Ophthalmol 2003;136: 866–71. 15. Song YG, Zhao M. [Frontalis muscle flap for the treatment of severe ptosis]. Zhonghua Zheng Xing Shao Shang Wai Ke Za Zhi 1985;1:34–6. 16. Pfaff AJ. Pig eyelid as a teaching model for eyelid margin repair. Ophthal Plast Reconstr Surg 2004;20:383–4. 17. Fogagnolo P, Serafino M, Nucci P. Stability of silicone band frontalis suspension for the treatment of severe unilateral upper eyelid ptosis in infants. Eur J Ophthalmol 2008;18:723–7.

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Long-term histopathologic study of the frontalis muscle flap after frontalis suspension for severe ptosis repair.

To investigate the long-term histopathologic changes of the frontalis muscle flap after frontalis muscle flap suspension for severe ptosis repair...
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