Autologous Fat Grafting in Plastic and Reconstructive Surgery: An Historical Perspective

Autologous fat grafting (AFG or lipofilling) is a common technique used in plastic and reconstructive surgery that involves the transfer of autologous fat tissue from one region of the body to another. The indications and techniques of AFG have changed dramatically over the years. We recount the historic milestones to the current state.

Introduction

Fat grafting, also known as lipofilling, is a surgical technique that involves the transfer of autologous fat tissue from one region of the body to another. The history of fat grafting spans 3 centuries and has been divided into 3 distinct periods:

the open-air period before the discovery of liposuction (1889-1977)—adipose tissue was obtained by surgical excision;
the second period (1977-1994) marked by the advent of liposuction, called non-purified or traumatic;
the purified or atraumatic period following Coleman’s work (1994 to this day).¹

Discussion

The Open-Air Period

The open-air period corresponds to the first attempts of fat tissue grafting. It was a time of experiments and errors.

The introduction of fat as a bulking agent in surgery dates to 1889 when Meulen treated a diaphragmatic hernia with the epiploon,² whereas the first grafting of fat was performed in 1893 by Neuber, who transplanted adipose tissue from the arm to the orbit to correct adherent, depressed scars sequelae of osteomyelitis.³

Soon after in 1895 Czerny used a large lipoma taken from the dorsal region to fill a breast lumpectomy defect.⁴ This is reported as the first case of breast reconstruction using autologous fat.⁵ Yet at the end of the 19th century, correction of depressions and contour were mainly done by paraffin injection. One of the most common indications was the correction of saddle nose secondary to congenital syphilis, with the material apparently being inert and the technique quick. However, it resulted in disastrous results and frequent complications, including recurrent infections, chronic inflammation, drainage, granuloma formation (paraffinoma), and even necrosis.⁶

To contrast the paraffin adverse effects, the injection of a more natural filler (ie, fat) was proposed in the early years of the 20th century.

In 1910 Lexer was the first to use autologous adipose tissue in cosmetic surgery for the augmentation of malar regions as the filling for facial wrinkles and lines to fight off the effects of aging as well as for facial contouring of a patient with Romberg syndrome.⁷ Moreover, he proposed the grafting of fat to restore the gliding tissue around the tendons for the treatment of Dupuytren disease.⁸ In 1911 Brunning published a rhinoplasty technique that involved the injection of small fragments of adipose tissue in the nasal dermis.⁹ In the same years as Lexer and Brunning, Holländer also began to use fat instead of paraffin but soon noticed its high rate of reabsorption. To minimize this problem, he mixed the patients’ adipose tissue with a harder kind of fat harvested from rams. Despite the few complications reported and the satisfactory outcomes, Holländer’s idea had limited impact and clinical application.¹⁰

In 1941 Billings and May presented a case of bilateral breast reconstruction with autologous fat grafting (AFG) on one side and adipose tissue and fascia grafting on the other with the idea that the fascia allowed for a better preservation of fat.¹¹

Surgeons enthusiastically supported the technique of AFG, alone or in combination with skin or fascia flaps, because it often represented a unique tool to easily solve major healing problems. However, with growing experience they realized that the very encouraging early results obtained with fat grafting worsened in the long term because of unpredictable reabsorption rate and cysts and fibrosis formation. For this reason, adipose tissue transplantation was considered questionable.

In the 1950s Peer accurately investigated the fate of autogenous adipose tissue transfer for 1 year and demonstrated that approximately 50% of fat cells ruptured and died after transplantation and that the graft structure was replaced by fibrous tissue. Cells that did not rupture survived, constituting the adipose tissue that remained.^12,13

Because of these considerations, adipose tissue grafting fell from favor gradually, becoming an almost-obsolete procedure. Still, we have reports of conditions treated by means of this technique during the 1950s: in the context of breast hypoplasia, Schrocher¹⁴reported 8 cases of breast augmentation by fat grafting; in maxillofacial surgery, Grandin filled the enucleation cavity due to a mandibular cyst;¹⁵ whereas Egyedi used the Bichat's fat pad to seal oral-sinusal communications.¹⁶

The Non-Purified or Traumatic Period

Fat grafting was reconsidered after the introduction of liposuction in 1974 by Arpad and Fischer,¹⁷ which would allow for the extraction of adipose tissue without surgical excision. Illouz modified Fischer's technique by introducing blunt cannulas of smaller diameters to reduce the section of nerves, lymphatics, and blood vessels.¹⁸ On occasion, a marked aspiration of adipose tissue resulted in unpleasant contour irregularities with depressions and holes. Reintroduction of the lipoaspirate using a syringe was regarded as the solution of choice even though complete or almost complete reabsorption of the reinjected material within a few weeks was reported.^19-21

Still his technique of extracting adipose tissue by aspiration opened up new horizons and awakened new interest in the field of AFG because a greater number of adipocytes would remain intact, thus allowing for their reimplantation.

In 1987 Bircoll presented several cases of breast symmetrization with the injection of the lipoaspirate,^22-23 whereas in 1995 Hang-Fu used liposuction fat-fillant implants (ie, prostheses comprising autologous adipose tissue contained within an impermeable or semi-permeable membrane capable of implantation)²⁴ for breast augmentation and reconstruction to avoid all the inconveniences associated with the direct injection of fat.

In the battle against reabsorption, Chajchir emphasized the following crucial steps for favorable and long-lasting results after autologous fat injection: cautious manipulation of the adipocyte to minimize rupture of its fragile cell, rinsing of the lipoaspirate in saline to eliminate dead cells and debris, and finally, grafting of fat in a well-vascularized bed.²⁵

The Atraumatic Period and Regenerative Medicine

The standardization for the harvesting, processing, and reinjection of fat is credited to Coleman, who published his technique in 1992 and set up a protocol that he later named Lipostructure® and whose fundamental principle was the atraumatic nature of the manipulation of adipose tissue.

His method involved the harvesting of fat from various donor sites by means of a 3-mm blunt cannula connected to a 10-mL syringe at low negative pressure to decrease adipocyte trauma; the subsequent centrifugation of the lipoaspirate, which allows for the separation of the unwanted components (oil, blood, local anesthetic, and other noncellular material) from the pure fat; and, finally, fat injection in small tunnels created by needles or blunt cannulas. Placement of the fat in small aliquots is the key to the Coleman technique because it ensures the proximity of the injected fat to a blood supply and allows the fat to anchor to the recipient tissue. These aliquots should be placed as the cannula is withdrawn, and no more than 0.1 mL of fat should be placed with each pass. In fact, if fat is injected in a bolus, fat cells will be clumped together and only those cells on the periphery of the injected area will have contact with the recipient tissue and will be more likely to survive.²⁶

Coleman’s technique increased fat graft survival, making its adoption more reliable and predictable. Initially used as a filler to correct volume deficiencies and for aesthetic purposes,²⁷ AFG found a progressively greater field of application and entered regenerative medicine as clinicians came to understand that adipose tissue was a connective tissue containing a reservoir of mesenchymal stem cells that can divide indefinitely, producing various cellular lines.^28-30

The experience of Rigotti and coworkers³¹ in treating radiodystrophic outcomes obtaining local improvement of tegument trophic characteristics after AFG was pioneering.

Inspired by these results, Klinger and colleagues applied the same technique to burn scars with excellent clinical results. Histologic examination of the treated skin showed patterns of new collagen deposition, local hypervascularity, and dermal hyperplasia with tissue regeneration.³² Building on these results, they began to treat other kinds of pathologic scars with an overall improvement in tissue quality. In their experience, AFG has proved to be an efficient and safe procedure to treat scars of various origin, demonstrating the capability of lipostructure to achieve architectural remodeling and loose connective regeneration.^33-40

In various clinical settings, Klinger and colleagues observed how lipostructure managed to relieve neuropathic pain thanks not only to regenerative effects but also as a result of molecular changes induced in the microenvironment and secretion of substances able to give prolonged analgesia.^41-53

Finally, they positively adopted its regenerative properties in the setting of post-traumatic "hard-to-heal" wounds, obtaining an improvement of healed skin quality and elasticity that appears very similar to normal skin.^54-58

In aesthetic and reconstructive surgery, AFG has also been recently used as an option for primary breast reconstruction especially after lumpectomies (lipofilling)⁵⁹; as an adjunct to autologous and implant-based breast reconstruction owing to its main role in the correction of breast contour deformities^59-64; and as a treatment of postmastectomy pain due to its regenerative properties.^5,42,53,65

In patients with congenital dentofacial malformations submitted to orthognathic surgery and/or additional procedures (genioplasty, alloplastic implants), noticeable facial asymmetry may persist despite achieving skeletal symmetry. AFG allows for the correction of these defects with satisfactory results.⁶⁶The case reported by Klinger et al. in a 2015 article "Autologous fat grafting in the treatment of painful postsurgical scar of the oral mucosa"⁴⁹ expanded the field of application of AFG to the treatment of retractile scars of the buccal vestibule. Recently an integrated approach involving percutaneous needleotomy, AFG, and local flaps has been described for the revision of sequelae of cleft lip correction surgery—and thus of secondary deformities of the nasolabial region of the midface.⁶⁷

Conclusions

AFG is increasingly used in plastic and reconstructive surgery. The evolution of this technique has spanned several decades. Despite the various fields of applications, AFG remains an important area of research. Clinicians should seek to provide ongoing data and push science to continue to improve the outcomes.

Acknowledgments

Affiliations: ¹HUNIMED: Humanitas University, Pieve Emanuele, Milan, Italy; ²Università degli Studi di Roma "Tor Vergata", Roma, Italy; ³Università degli Studi di Pavia, Pavia, Italy

Correspondence: Domenico Costanzo; domenico.costanzo@mail.com

Disclosures: The authors have no non-financial or commercial, proprietary, or financial interest in the products or companies described in the manuscript. The author(s) did not receive grants or a consultant honorarium to conduct the study, write the manuscript, or otherwise assist in the development of the above-mentioned manuscript.

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