Distally Based Dorsal Forearm Fasciosubcutaneous Flap

Distally Based Dorsal Forearm Fasciosubcutaneous Flap Kwang Seog Kim, M.D., Ph.D. Gwangju, Korea Use of a local flap is often required for the reconstruction of a skin defect on the dorsum of the hand. For this purpose, a distally based dorsal forearm fasciosubcutaneous flap based on the perforators of the posterior interosseous artery was developed. From 1997 until 2002, this flap was used to reconstruct skin defects on the dorsum of the hand in nine patients at Chonnam National University Medical School. The sizes of these flaps ranged from 10 to 14 cm in length and from 5 to 7 cm in width. The flaps survived in all patients. Marginal loss over the distal edge of the flap was noted in one patient. Three flaps that developed minimal skin-graft loss were treated successfully with a subsequent split-thickness skin graft. The long-term follow-up showed good flap durability and elasticity. The distally based dorsal forearm fasciosubcutaneous flap is a convenient and reliable alternative for reconstructing skin defects of the dorsum of the hand involving vital structure exposure. It obviates the need for more complicated and time-consuming procedures. (Plast. Reconstr. Surg. 114: 389, 2004.) Although skin defects with exposure of bones or tendons on the dorsum of hands can be a difficult problem, several surgical techniques using local flaps have been developed to resurface the defect. A local adipofascial turnover flap from the dorsal forearm is a reliable and simple technique for resurfacing the dorsum of the hand if the surrounding soft tissue is available, but this flap is limited in terms of size because it is a random pattern flap. And although the posterior interosseous artery flap is suitable for the coverage of dorsal skin defects of the hand and avoids interference with the two main arteries of the forearm, the dissection of the vascular pedicle is frequently quite complex and tedious. In an attempt to resolve these problems, I developed a distally based dorsal forearm fasciosubcutaneous flap based on the perforators of the posterior interosseous artery. I present this technique and my results along with a brief review of the literature. ANATOMY The forearm fasciosubcutaneous tissue consists of two layers, the subcutaneous tissue and the fascia, enveloped between the dermis and the muscle bellies. The subcutaneous tissue is the superficial layer of loose connective tissue and fat immediately beneath the skin containing cutaneous veins and nerves and possesses the richest network of arterial perfusion. The perforating vessels of the posterior interosseous artery penetrate the fascia to run longitudinally with numerous transverse anastomoses in the subcutaneous tissue. The fascia is the deep layer of dense connective tissue that not only envelops the muscle bellies but also thickens to form a septum between them. The posterior interosseous artery arises from the common interosseous artery, enters the posterior compartment of the forearm at the junction of the proximal and middle thirds on a line drawn between the lateral epicondyle of the humerus and the distal radioulnar joint or the ulnar head, and then runs distally in the intermuscular septum between the extensor carpi ulnaris and the extensor digiti minimi proprius, giving off perforators all along its length (Figs. 1 and 2). The septocutaneous perforators anastomose in the superficial layer of the deep fascia and form rich vascular arcades with longitudinal anastomoses. Near the wrist joint, three types of anastomosis have been identified. The first one, which is usually From the Department of Plastic and Reconstructive Surgery, Chonnam National University Medical School. Received for publication March 21, 2003; revised August 21, 2003. DOI: 10.1097/01.PRS.0000131985.32954.C0 389

390 PLASTIC AND RECONSTRUCTIVE SURGERY, August 2004 FIG. 1. Schematic cross-section through the middle third of the forearm shows the positions of the principal vessels and the courses of their septocutaneous perforators. U, ulna; R, radius; PL, palmaris longus; FCR, flexor carpi radialis; FDS, flexor digitorum superficialis; FCU, flexor carpi ulnaris; B, brachioradialis; PT, pronator teres; ECRB, extensor carpi radialis brevis; ECRL, extensor carpi radialis longus; FDP, flexor digitorum profundus; FPL, flexor pollicis longus; EPL, extensor pollicis longus; EPB, extensor pollicis brevis; APL, abductor pollicis longus; ECU, extensor carpi ulnaris; EDMP, extensor digiti minimi proprius; ED, extensor digitorum. FIG. 2. Branches (arrows) arising from the posterior interosseous artery in the intermuscular septum between the extensor carpi ulnaris and the extensor digiti minimi proprius. The septocutaneous perforators anastomose in the superficial layer of the deep fascia and form rich vascular arcades with longitudinal anastomoses. located at the just proximal area of the distal radioulnar joint, is with the anterior interosseous artery, the second system is established with the dorsal carpal arch, and the third includes several branches that surround the ulnar head on both sides and linked with the ulnar artery. 1 The distally based dorsal forearm fasciosubcutaneous flap is based on the distal perforators of the posterior interosseous artery and its branches as a perforator-based flap and is supported by anastomotic branches located around the wrist joint. Therefore, although a branch of these main anastomotic branches may be injured, this flap can still be safely elevated using the other anastomotic branches. The flap is pedicled on the distal fascia and subcutaneous tissue and the fasciosubcutaneous vascular network. There is no single axial artery in the pedicle; however, the incorporation of sizable perforating vessels and a welldeveloped longitudinal vascular network within the subcutaneous tissue provide significant vascularity to the dorsal forearm fasciosubcutaneous flap. Venous drainage is from both the superficial and the deep systems, as there are multiple anastomoses between these venous channels. One or two venae comitantes ordinarily follow each of the perforators with communicating branches between the venae comitantes allowing reverse flow via both crossover and bypass patterns. Sufficient reverse flow venous drainage through the venae comitantes and the superficial veins contained in the pedicle occurs to ensure flap survival. PATIENTS AND METHODS Patients Between the years 1997 and 2002, nine patients (eight male, one female) underwent distally based dorsal forearm fasciosubcutaneous flap procedures to reconstruct skin defects on

Vol. 114, No. 2 / DORSAL FOREARM FASCIOSUBCUTANEOUS FLAP 391 TABLE I Summary of Distally Based Dorsal Forearm Fasciosubcutaneous Flaps for Complicated Dorsal Skin Defects of the Hand Patient Sex Age (yrs) Cause Side the dorsal aspect of hands. Ages ranged from 18 to 62 years (mean, 40.2 years), and follow-up ranged from 7 to 20 months (mean, 11 months). All patients had acute and subacute wounds resulting from trauma. The sizes of the flaps ranged from 10 to 14 cm in length and from 5 to 7 cm in width (Table I). Size (cm 2 ) Defect Flap Flap Base Complication 1 M 38 Crush Right 7.0 9.0 7.0 14.0 7.0 3.0 2 F 62 Burn Right 6.0 9.0 7.0 13.0 7.0 2.0 GL 3 M 46 Avulsion Right 5.0 8.0 6.0 12.0 6.0 2.0 D 4 M 27 Crush Right 5.0 7.0 5.0 10.0 5.0 2.0 5 M 18 Crush Right 5.0 7.0 6.0 12.0 6.0 3.0 6 M 52 Avulsion Right 6.0 7.0 6.0 12.0 6.0 2.0 7 M 34 Crush Left 6.0 7.0 6.0 12.0 6.0 2.0 GL 8 M 42 Crush Left 5.0 6.0 5.0 12.0 5.0 3.0 9 M 43 Crush Right 6.0 6.0 6.0 13.0 6.0 4.0 FL, GL Cases 1 and 2 were presented in the article. M, male; F, female; GL, minimal skin-graft loss; D, desquamation of flap-donor site; FL, marginal loss over the distal edge of the flap. Operative Technique After devitalized tissue is débrided and the wound massively irrigated, the elbow is positioned in full pronation and 90 degrees of flexion. The distally based dorsal forearm fasciosubcutaneous flap is drawn as a rectangle along an axis extending from the lateral epicondyle of the humerus to the distal radioulnar joint, which represents the course of the posterior interosseous artery in the dorsal forearm. Although more proximal extension of the flap may be possible, the proximal limit of the flap can be safely placed at the junction of the proximal and middle thirds on the axis. The pivot point of the flap is given by the origin of the sizable septocutaneous perforator of the posterior interosseous artery at the just proximal level of the distal radioulnar joint. The flap can be designed as large as the complete width of the dorsal forearm. It is prudent to avoid the radial edge of the forearm whenever possible to minimize injury to the radial cutaneous nerve branches. The flap is designed slightly larger than the measured defect and the flap base (Fig. 3, above). The operative procedure is performed under pneumatic tourniquet without exsanguinating the limb for better identification of the cutaneous vessels. The skin is incised in a curvilinear or zigzag fashion along the central axis of the proposed flap. The skin flaps are carefully elevated to leave some subcutaneous tis- FIG. 3. Flap design. (Above) The flap is drawn as a rectangle along an axis extending from the lateral epicondyle of the humerus to the distal radioulnar joint, which represents the course of the posterior interosseous artery in the dorsal forearm. (Below) Line drawing of the anatomic basis of the distally based dorsal forearm fasciosubcutaneous flap. This flap contains the tissue indicated by the dashed line. The posterior interosseous artery and septocutaneous perforators are noted. The skin, superficial layer of subcutaneous fat, and posterior interosseous artery are not contained in the flap.

392 PLASTIC AND RECONSTRUCTIVE SURGERY, August 2004 sue on the underlying fascia investing the musculotendinous layer of the forearm. The fascia is then exposed and sharply incised along the flap outline on the dorsal forearm skin. After a sizable septocutaneous perforator of the posterior interosseous artery has been identified and preserved at the proximal level of the distal radioulnar joint, the dissection is carried out in the plane above the deep fascia from the proximal to the distal side. Many perforators from the posterior interosseous artery to the fascia are coagulated. Elevation is completed at the flap base (Fig. 3, below). After release of the tourniquet, excellent blood flow to the fasciosubcutaneous flap should be observed. The flap is turned over distally 180 degrees to cover the defect. Its margin is sutured to the edge of the defect, and the entire raw surface of the hand, including the raw flap, is resurfaced with a splitthickness skin graft. After a suction drain is placed beneath the donor skin flaps, the donor area is closed primarily. The hand is elevated to minimize postoperative venous congestion, but anticoagulants are not used. The hand is immobilized by a short arm splint for 1 week to ensure graft success, after which time both passive and active mobilization can carefully begin. RESULTS The flaps survived in all patients. Although marginal loss over the distal edge of the flap was noted in one patient, no other flap was needed for defect repair. The skin graft over the fasciosubcutaneous flap did not take completely in three patients. Three flaps that developed minimal skin-graft loss were treated successfully with a subsequent split-thickness skin graft. Desquamation of the replacing flap donor-site skin occurred in one patient. No scar or sequela caused by desquamation was noted (Table I). In all patients, the normal gliding motion of the involved tendons and joints was gained, and the cosmetic result in the donor site was quite acceptable. The longterm follow-up (mean, 11 months) showed good flap durability and elasticity. Figures 4 and 5 show two illustrative cases. DISCUSSION Soft-tissue reconstruction of the hand remains a challenge for plastic and reconstructive surgeons. Dorsal skin defects on the hand may be covered by local, distant, or free flaps, depending on the patient s general condition and the conditions of the local wound and donor site. Free flaps offer flexibility in size, shape, and positioning and do not add donorsite morbidity to the injured hand. Free flap coverage is a time-consuming procedure, however, that requires a more difficult technique and complicated postoperative care. Distant flaps provide enough tissue for reconstruction but require multiple-stage operations involving prolonged immobilization. Although local flaps must be widely based and are usually limited in size and mobility by the size and location of the defect, they offer relatively simple and safe wound coverage, spare the distant donor site for further reconstruction, and do not interfere with the patient s activities and physical therapy. Several surgical techniques use local flaps to resurface dorsal skin defects of the hand. One group of local flaps is distally based; these are raised from the volar aspect of the forearm. The axial-pattern reverse radial forearm flap 2 provides a good amount of tissue for coverage, and is one of the primary flaps used for the reconstruction of soft-tissue defects of the hand. The advantages of this pedicled flap are that it is a safe, simple, and effective one-stage procedure providing thin, pliable, relatively hairless, good quality skin with a robust blood supply. The main disadvantages of this flap are sacrifice of a major artery, which may jeopardize hand viability, and morbidity of the donor site. The axial-pattern reverse fascial forearm flap procedure 3 6 includes the fascial forearm flap and split-thickness skin graft for coverage of the hand. The major advantage of this flap is reduced donor-site morbidity as a result of harvesting the fascia alone; however, this flap also involves sacrificing a major artery. The distally based radial forearm fasciosubcutaneous flap with preservation of the radial artery 7 is based on the septocutaneous perforators of the distal radial artery. This method substantially avoids the two main drawbacks of the axial-pattern reverse radial forearm flap. The other group of local flaps involves distally based flaps raised from the dorsal aspect of the forearm. The deepithelialized turnover flap 8,9 represents a reliable method, but the flap donor-site skin is killed and a large amount of skin graft is needed to resurface the wound. Epithelial cysts and discharging sinuses may be a bothersome problem, and the characteristic adherence of the buried dermis may also impede the gliding

Vol. 114, No. 2 / DORSAL FOREARM FASCIOSUBCUTANEOUS FLAP 393 FIG. 4. Case 1. A 38-year old man with a crush injury on the dorsum of his right hand. (Above, left) Preoperative view. Exposed extensor tendons, denuded of paratenon, were cleaned and the devitalized tissue was débrided. (Above, right) Flap elevation. The resulting skin defect was covered with a distally based dorsal forearm fasciosubcutaneous flap measuring 7.0 14.0 cm with a 7.0 3.0-cm base. (Below, left) Immediate postoperative view. The donor area was closed primarily, and the recipient site was covered with a split-thickness skin graft. (Below, right) One-year postoperative view. The postoperative course was uneventful and long-term follow-up showed normal function of the hand with excellent flap pliability. motion of the involved tendon. The local adipofascial turnover flap 10,11 represents a reliable and simple technique for resurfacing the dorsum of the hand if the surrounding soft tissue is available, but this is not always possible because of the limitation of the degree to which the flap can be raised. The posterior interosseous artery flap 12 15 is suitable for the coverage of dorsal skin defects of the hand and avoids interference with the two main arteries of the

394 PLASTIC AND RECONSTRUCTIVE SURGERY, August 2004 FIG. 5. Case 2. A 62-year-old woman with a full-thickness flame burn on the dorsum of her right hand. (Above, left) Preoperative view. Devitalized extensor tendons of the index finger were excised. (Above, right) Flap elevation. After the extensor tendons were reconstructed with palmaris longus tendon grafts, a distally based dorsal forearm fasciosubcutaneous flap, measuring 7.0 13.0 cm with a 7.0 2.0-cm base, was raised to cover the defect. A sizable septocutaneous perforator of the posterior interosseous artery was identified and preserved at the proximal level of the distal radioulnar joint (arrow). (Below, left) Immediate postoperative view. The donor area was closed primarily, and the recipient site was covered with a split-thickness skin graft. Postoperatively, there was complete flap survival with minimal skin-graft loss, which was treated successfully with a subsequent split-thickness skin graft. (Below, right) Ten-month postoperative view. Functional outcome was good. forearm. The dissection of the vascular pedicle, however, is frequently quite complex and tedious. The distally based dorsal forearm fasciosubcutaneous flap is very similar to the distally based radial forearm fasciosubcutaneous flap

Vol. 114, No. 2 / DORSAL FOREARM FASCIOSUBCUTANEOUS FLAP 395 with preservation of the radial artery. These flaps avoid sacrificing a major artery and reduce morbidity of the donor site because they are perforator-based fasciosubcutaneous flaps. Because most of the lymphatic and venous drainage of the hand courses through the volar surface of the forearm, large flaps raised in this region, such the distally based radial forearm fasciosubcutaneous flap with preservation of the radial artery, block these lymphatic and venous channels, producing temporary hand edema that is inconvenient in previously traumatized hands. 15,16 The distally based dorsal forearm fasciosubcutaneous flap, however, provides a large amount of tissue for hand reconstruction with minimal interference of lymphatic and venous drainage. The distally based dorsal forearm fasciosubcutaneous flap offers the advantages of both the posterior interosseous artery flap and the local adipofascial turnover flap from the dorsal forearm. It provides enough tissue for reconstruction, like the axial-pattern flap, is a relatively simple procedure, and can be transposed easily. As with all surgical procedures, there are certain disadvantages. It is necessary to have local healthy tissue around the wrist joint. If the distal perforators of the posterior interosseous artery and its branches are injured, the distally based dorsal forearm fasciosubcutaneous flap should be abandoned. A skin graft over the fasciosubcutaneous flap cannot be as aesthetically pleasing as a skin flap. It has been reported that distally based fasciosubcutaneous flaps often suffer minor skin-graft loss. This phenomenon following the immediate skin grafting of fasciosubcutaneous flaps has been thought to be attributable to flap edema and an apparent decrease in flap vascularity during the immediate postoperative period. 7 In three cases of my series, minimal skin-graft loss also developed and a subsequent split-thickness skin graft was required. If the flap is immediately covered with a skin graft after the flap transfer, prudent postoperative care (e.g., preservation of hand elevation, removal of seroma, and application of splint) is a requirement for reducing skin-graft loss. Some authors prefer to delay skin grafting until the flap edema subsides to avoid this problem. 7 Random pattern fasciosubcutaneous flaps are based on the attached pedicle. As described in some reports, 9 11,17 the length-tobase ratio below 1.5:1, length-to-width ratio below 2.0:1, and flap-to-base area ratio below 4.0:1 are essential for flap survival. The width of the attached pedicle is usually kept at approximately 1 cm but may be made as narrow as 0.5 cm in fingers and as wide as 2.5 cm in extremities other than the hand. These principles of designing the random pattern fasciosubcutaneous flap are not applied to the distally based dorsal forearm fasciosubcutaneous flap because the flap is a perforator-based flap. The anatomy of the posterior interosseous artery system and its variations, in connection to the distally based dorsal forearm fasciosubcutaneous flap, are well described in the literature. 1,12 15,18,19 Cadaveric studies have shown that the artery narrows at the middle of the forearm. 12,14 Angrigiani et al. 15 reported that in clinical cases, the artery was larger at the level of the distal anastomosis (range, 0.9 to 1.1 mm) than at the middle of the forearm (range, 0.3 to 0.6 mm). The continuity of the posterior interosseous artery was absent at the middle of the forearm in 1.4 to 5.7 percent of clinical cases and cadaveric dissections. 14,15,18 These findings suggest that the area might be considered as a choke anastomosis between the proximal and the distal parts of the posterior interosseous artery. 15 These anatomic variations, however, do not prevent the use of the distally based dorsal forearm fasciosubcutaneous flap because the flap is perfused from the distal communicating arteries through the cutaneous branches. Cadaveric injection studies of the posterior interosseous artery by Costa and Soutar 12 and Costa et al. 13 showed staining the dorsal skin of the forearm extending from 2 to 4 cm below the interepicondylar line to the wrist. In contrast, Angrigiani et al. 15 reported that ink injections through a catheter placed in the distal part of the anterior interosseous artery stained the distal two-thirds of the dorsal forearm. According to Penteado et al., 18 the skin overlying the upper fourth of the dorsal forearm is supplied by the ascending branch of the posterior interosseous artery (i.e., the recurrent interosseous artery). These findings suggest that the distally based dorsal forearm fasciosubcutaneous flap may suffer tissue loss when raised in the proximal third of the dorsal forearm. Therefore, although more proximal extension of the flap might be possible, it is desirable that the proximal limit of the flap be placed at the junction of the proximal and middle thirds of the dorsal forearm. Three anastomosis types of the posterior interosseous artery (i.e., the anastomoses between the pos-

396 PLASTIC AND RECONSTRUCTIVE SURGERY, August 2004 terior interosseous artery and the anterior interosseous artery, the dorsal carpal arch, and the ulnar artery) have been identified near the wrist joint. 1 Penteado et al. 18 found there was absence of any communication at the level of the wrist joint in 1 of 70 specimens (1.4 percent) and Bayon and Pho 19 reported the absence of the distal anastomosis between the anterior and posterior interosseous arteries in one of 35 specimens (2.9 percent). The great majority of authors 12 15 have reported that the anastomoses between the posterior interosseous artery and the anterior interosseous artery, the dorsal carpal arch, and the ulnar artery were always present. Although the anatomy of the posterior interosseous artery system may vary, it is well known. Because the distally based dorsal forearm fasciosubcutaneous flap contains only fasciosubcutaneous tissues, anatomical variations of the artery that prohibit the use of the posterior interosseous artery flap (e.g., the distribution patterns of the septocutaneous perforators, 12 the relation types of the posterior intraosseous artery and the posterior interosseous nerve 14 ) are not significant problems in dissecting the distally based dorsal forearm fasciosubcutaneous flap. Moreover, the distal anastomoses of the posterior interosseous artery are constant at the wrist joint level, which are the most important structures for harvesting the flap. Therefore, the distally based dorsal forearm fasciosubcutaneous flap is a safe procedure. CONCLUSIONS The distally based dorsal forearm fasciosubcutaneous flap is a convenient and reliable alternative for reconstructing skin defects of the dorsum of the hand involving vital structure exposure. It obviates the need for more complicated and time-consuming procedures. Early use of this flap allows preservation of vital structures, decreases morbidity, and allows for early rehabilitation. Kwang Seog Kim, M.D., Ph.D. Department of Plastic and Reconstructive Surgery Chonnam National University Medical School 8 Hak-dong, Dong-gu Gwangju 501-757, Korea pskim@chonnam.ac.kr REFERENCES 1. Landi, A., Luchetti, R., Soragni, O., De Santis, G., and Sacchetti, G. L. The distally based posterior interosseous island flap for the coverage of skin loss of the hand. Ann. Plast. Surg. 27: 527, 1991. 2. Reid, C. D., and Moss, L. H. One-stage repair with vascularised tendon grafts in a dorsal hand injury using the Chinese forearm flap. Br. J. Plast. Surg. 36: 473, 1983. 3. Soutar, D. S., and Tanner, N. S. B. The radial forearm flap in the management of soft tissue injuries of the hand. Br. J. Plast. Surg. 37: 18, 1984. 4. Jin, Y., Guan, W., Shi, T., Quian, Y., Xu, L., and Chang, T. Reverse island forearm fascial flap in hand surgery. Ann. Plast. Surg. 15: 340, 1985. 5. Reyes, F. A., and Burkhalter, W. E. The fascial radial arm flap. J. Hand Surg. (Am.) 13: 432, 1988. 6. Cherup, L. L., Zachary, L. S., Gottlieb, L. J., and Petti, C. A. The radial forearm skin graft-fascial flap. Plast. Reconstr. Surg. 85: 898, 1990. 7. Weinzweig, N., Chen, L., and Chen, Z. The distally based radial forearm fasciosubcutaneous flap with preservation of the radial artery: An anatomic and clinical approach. Plast. Reconstr. Surg. 94: 675, 1994. 8. Thatte, R. L., Gopalakrishina, A., and Prasad, S. The use of de-epithelized turn-over flaps in the hand. Br. J. Plast. Surg. 35: 293, 1982. 9. Yang, J. Y., Tsai, Y. C., and Noordhoff, M. S. The application of turn-over flaps to burn wounds. Burns 12: 115, 1985. 10. Lai, C., Lin, S., Yang, C., and Chou, C. The adipofascial turn-over flap for complicated dorsal skin defects of the hand and finger. Br. J. Plast. Surg. 44: 165, 1991. 11. Lai, C., Lin, S., Chou, C., and Tsai, C. Clinical application of adipofascial turn-over flaps for burn wounds. Burns 19: 73, 1993. 12. Costa, H., and Soutar, D. S. The distally based posterior interosseous flap. Br. J. Plast. Surg. 41: 221, 1988. 13. Costa, H., Comba, A., Martins, A., Rodrigues, J., Reis, J., and Amarante, J. Further experience with the posterior interosseous flap. Br. J. Plast. Surg. 44: 449, 1991. 14. Büchler, U., and Frey, H. Retrograde posterior interosseous flap. J. Hand Surg. (Am.) 16: 283, 1991. 15. Angrigiani, C., Grilli, D., Dominikow, D., and Zancolli, E. A. Posterior interosseous reverse forearm flap: Experience with 80 consecutive cases. Plast. Reconstr. Surg. 92: 285, 1993. 16. Timmons, M. J., Missotten, F. E., Poole, M. D., and Davies, D. M. Complications of radial forearm flap donor sites. Br. J. Plast. Surg. 39: 176, 1986. 17. Yang, J., and Noordhoff, M. S. Early adipofascial flap coverage of deep electrical burn wounds of upper extremities. Plast. Reconstr. Surg. 91: 819, 1993. 18. Penteado, C. V., Masquelet, A. C., and Chevrel, J. P. The anatomic basis of the fasciocutaneous flap of the posterior interosseous artery. Surg. Radiol. Anat. 8: 209, 1986. 19. Bayon, P., and Pho, R. W. Anatomical basis of dorsal forearm flap based on posterior interosseous vessels. J. Hand Surg. (Br.) 13: 435, 1988.