Plastic and Reconstructive Surgery

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Plastic & Reconstructive Surgery:
doi: 10.1097/01.prs.0000435843.87927.90
CME

Pressure Ulcers and Perineal Reconstruction

Larson, Jeffrey D. M.D.; Altman, Andrew M. M.D.; Bentz, Michael L. M.D.; Larson, David L. M.D.

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Author Information

Madison and Milwaukee, Wis.

From the Department of Plastic Surgery, University of Wisconsin Medical School; and Department of Plastic Surgery, The Medical College of Wisconsin.

Received for publication June 12, 2012; accepted July 30, 2012.

Disclosure: The authors have no associations or financial disclosures to report.

Related Video content is available for this article. The videos can be found under the “Related Videos” section of the full-text article, or, for Ovid users, using the URL citations published in the article.

Jeffrey D. Larson, M.D., Department of Plastic Surgery, Medical College of Wisconsin, 8700 Watertown Plank Road, Milwaukee, Wis. 3226–3595, dlarson@mcw.edu

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Abstract

Learning Objectives: After reading this article, the participant should be able to: 1. Discuss the approach and rationale of pressure sore management, including specific techniques of bone biopsy and postoperative care resulting in a significant reduction in recurrence rates. 2. Develop a surgical plan for reconstructing defects of the perineum, taking into account the local tissue factors and the soft-tissue requirements for reconstruction.

Summary: As close as the buttocks and the perineum are anatomically, the clinical settings and the solutions to wound problems in these areas are quite different. The ubiquitous “pressure ulcer” presents more commonly as a clinical management problem than a reconstruction issue. On the other hand, the perineal defect is almost always a reconstruction challenge following tumor ablation. For these reasons, the authors have chosen to separate this Continuing Medical Education offering into two parts. The first part addresses the pressure ulcer, while the latter discusses the perineum.

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PRESSURE ULCER MANAGEMENT

Despite improved measures in prevention and advances in surgical and nonsurgical management, pressure sores remain a formidable problem for medical practitioners in many disciplines and for plastic surgeons in particular. With the recent addition of pressure ulcers to the Center for Medicare and Medicaid’s list of “never events,” efficient and cost-effective treatment becomes even more important in managing these difficult clinical problems.

Management of the pressure ulcer can be challenging for inexperienced and experienced surgeons alike. One source of this conundrum is a paucity of evidence-based literature on the subject. Questions and wide-ranging opinions abound regarding almost all aspects of management of the late stage (stages 3 and 4) pressure ulcer. Within the last few years, there has been literature that provides some sensible rationales in response to these queries that may provide aid in the definitive management of this age-old problem. We offer this material for the mature plastic surgeon, with recent literature regarding pressure ulcers complemented with illustrations and narrated videos.

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Diagnosing Pressure Ulcers

Diagnosis of pressure ulcers is primarily a clinical diagnosis. Imaging studies are typically of little utility.

There is no shortage of controversy on diagnosing pressure ulcers, specifically with regard to the use of radiologic studies. In general, imaging is of little use in diagnosing pressure ulcers. The most significant area of controversy in the literature lies in the diagnosis of osteomyelitis. While magnetic resonance imaging has been used to describe soft-tissue and bony changes in these lesions,1 studies that have attempted to use it to diagnose osteomyelitis in pressure ulcer patients have been limited by poor study design and selection bias.2,3 Recent studies suggest that plain film radiography may be as good as, if not better than, more expensive and invasive imaging modalities such as computed tomography, but they did not include magnetic resonance imaging in their comparisons (Level of Evidence: Diagnostic, IV).4

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Diagnosing Osteomyelitis in Pressure Ulcers

The accepted standard for diagnosing osteomyelitis is an open bone biopsy, which can only be accomplished with a surgical procedure. (See Video, Supplemental Digital Content 1, which displays a bone biopsy, available in the “Related Videos” section of the full-text article on PRSJournal.com or, for Ovid users, at http://links.lww.com/PRS/A929.) Though some studies suggest that Jamshidi core needle biopsy may be useful for diagnosis,5,6 it is technically challenging as either a bedside or interventional radiologic procedure because the bone in question may be too dense for needle penetration but may still be actively infected. Osteomyelitis typically found in the base of the pressure ulcer is superficial and limited to the exposed bony surface at the base of the chronic, open wound. The medullary portion of the bone is not involved (Level of Evidence: Therapeutic, IV).7 Therefore, removal of the cortex and bone using a sterile rongeur to obtain the culture and sensitivity of the offending bone will provide the information needed for the diagnosis of osteomyelitis.

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Regardless of the status of the bone, in most cases, osteomyelitis is not a contraindication to definitive surgery and can be treated definitively with decortication of the bone and appropriate soft-tissue coverage.

Though many have advocated complete débridement of the infected bone in conjunction with medical treatment of osteomyelitis with a protracted (6- to 8-week) course of preoperative intravenous antibiotics, there is little evidence to support such a position. The rationale for this statement is twofold. As noted above, short of an open biopsy, there is no definitive method of reliably identifying the offending organism or even making a radiologic diagnosis of osteomyelitis; therefore, it is impossible to know which antibiotic to use in a given case. Furthermore, it is equally difficult to know when the presumed “infection” has been eradicated. Even if one has the specific culture and sensitivity of bone, leaving it exposed and not covered with good soft tissue during a 6-week course of intravenous antibiotics simply means it can become colonized with other organisms in its open state. The most efficient and effective management of the pressure ulcer suspected of harboring osteomyelitis, therefore, is removal of the associated bursa, mechanical débridement of the bony base of the wound (e.g., sterile rongeur) (see Video, Supplemental Digital Content 1, available in the “Related Videos” section of the full-text article on PRSJournal.com or, for Ovid users, at http://links.lww.com/PRS/A929), ostectomy of the cortex of the bone, definitive culture, and immediate coverage of the bone with muscle or other healthy, viable tissue. Studies have shown that this method of treatment is not associated with any higher recurrence rate (Level of Evidence: Therapeutic, IV).14

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Nutritional Status of the Patient

The nutritional status of the patient is not as important as once thought and may be improved with definitive wound closure. In an ideal world, the patient’s preoperative albumin level should be 3.5 g/dl and the prealbumin level should be at least 20 g/dl, with normal levels of zinc and vitamins and a good caloric intake. Interestingly, there is no clear evidence that this has any effect on the healing of existing, or prevention of future, pressure ulcers.8 However, in the debilitated and chronically ill patient, in whom most pressure ulcers occur, it is extremely difficult to attain normal levels of any of the accepted nutritional standards, primarily for two reasons. First, the patient is probably not in an ideal clinical setting (hence the development of the ulcer in the first place); second, and intuitively, the open wound serves as a “sink hole” for orally ingested protein, which is lost to the wound before it can be incorporated into the patient’s organ systems. Therefore, the only way to get many of these patients in a true-positive nitrogen balance is through enteral hyperalimentation, something that is prohibitively invasive and not tolerated well by the patient. There is evidence that abnormal nutritional markers (e.g., anemia, serum protein, inflammatory markers) do become normal after surgery.9,14 As suggested in a recent article, these indicators, rather than being risk factors, may be the consequence of pressure ulceration.10

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Bed Rest

Total bed rest following surgery is of vital importance and should probably be done as an inpatient. It is recognized that all phases of wound healing are impaired in the denervated patient.11 In light of this fact, it is recommended that some period of mandatory rest be given to patients in the immediate postoperative period. The length of that bed rest ranges between a few days and 8 weeks.12 There is good evidence that, after surgery, 3 weeks of flat bed rest followed by a graduated sitting schedule results in improved outcomes (Level of Evidence: Therapeutic, IV).13 (See Appendix, Supplemental Digital Content 2, which shows the Pressure Ulcer Reconstruction PostOp Orders document, http://links.lww.com/PRS/A931.) Whether bed rest takes place in an inpatient environment or a subacute, long-term care facility is open to debate. A recent report of 107 consecutive patients over a 5-year period (22-month recurrence rate of 16 percent) using 3 weeks of acute care hospitalization suggests that this timeframe should be considered.14 Another option includes transfer to an intermediate facility, a nursing home, or even to the patient’s own residence. Each of these settings places the patient out of the direct care of the medical team (surgeon, primary care physician, physical medicine/rehabilitation, specialized nurses, social service, physical therapist, psychologist, and so on). If there were some assurance that a protocol of flat bed rest could be maintained in these venues, all would be well. Such is rarely the case, and the patient returns to the clinic shortly after surgery to find that there is ulcer recurrence, starting the entire process over. Our experience14 has been disappointing in anything short of inpatient acute care management.

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Indicators for Surgery

The presence of a stage 3 or 4 pressure ulcer is not always an indication for surgery. Though patients may die with pressure ulcers, few actually die of pressure ulcers. At surgery, almost all of these are “clean contaminated” wounds, and despite their size and appearance, they are not sources of systemic infection. The source of fevers in pressure ulcer patients is most frequently urinary or pulmonary in nature.15,16 In addition to the presence of an ulcer, other factors that must be considered include the home support system, patient motivation, comorbidities, and the availability and quality of outpatient medical care.

Appropriate closure of a pressure ulcer is not always a regional flap. Many times, advancement of local tissue is sufficient. (See Video, Supplemental Digital Content 3, which demonstrates pressure ulcer surgery, available in the “Related Videos” section of the full-text article on PRSJournal.com or, for Ovid users, at http://links.lww.com/PRS/A930.)

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Contrary to the recommendation that closure with local tissue is prone to a very high recurrence rate,17 others14 have found that complete excision of the walls of the ulcer bursa back to healthy, nonscarred tissue results in sufficient healthy tissue that can easily be advanced to provide a secure layered closure. This use of local tissue has not resulted in any higher recurrence rate than that in patients for whom a regional flap was used.14

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RECONSTRUCTION OF PELVIC AND PERINEAL DEFECTS

A successful reconstructive surgical approach to the complex composite defect of the pelvis and perineum requires an analytical eye and flexibility in achieving a durable surgical outcome. Although the etiology of defects may be congenital or traumatic, most defects are secondary to extirpative surgical procedures for malignancy of the reproductive and lower gastrointestinal tracts. Varied tissue elements must be replaced depending on the ultimate functional and structural reconstructive goals of the surgeon. Optimum reconstruction requires sound planning involving the patient, the ablative surgeon, and the reconstructive surgical team.

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Local Tissue Environment

Understanding the quality of the local tissue environment is of critical importance in planning. Consideration of the perioperative anatomic extent of radiotherapy is an important variable. External beam radiation has a profound impact on the local wound environment, causing local histopathology that includes small vessel thrombosis, fibroblast dysfunction, and an altered cytokine milieu contributing to neutrophil dysfunction. Collectively, these features lead to impaired wound healing of the affected tissues within the treatment zone and mandate the introduction of healthy, nonirradiated, well-vascularized tissues to optimize healing of the reconstructed defect. Other key considerations in surgical planning include the zone of injury in cases of trauma and the anatomic extent of previous surgical scars.

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Abdominally Based Reconstruction

Rectus abdominis flaps and perforator variants are the foundation of abdominally based reconstruction. Abdominal flaps are a mainstay of reconstructive surgical management of pelvic and perineal defects following ablative surgical procedure via laparotomy. The transpelvic vertical rectus abdominis myocutaneous (VRAM) flap is the primary workhorse flap used in this setting. It provides vigorous vascularized composite soft tissue to reconstruct a variety of defects using healthy tissue taken from a region typically outside the zone of the radiotherapy field in cases of malignancy. The rectus abdominis flap is a Mathes/Nahai type III flap, with in situ blood supply from the superior epigastric artery cephalad and the dominant inferior epigastric artery caudally. In pelvic reconstruction, a skin paddle is designed paramedian to the midline laparotomy incision. The rectus is divided at its cephalic extent and dissected inferiorly to the inferior epigastric vascular pedicle; at this point, the flap is mobilized and rotated into the pelvis, with the skin paddle inset into the perineal or pelvic component of the defect (Figs. 1 and 2). The flap provides excellent soft-tissue fill of pelvic and perineal deadspace, while simultaneously allowing significant and versatile resurfacing of the skin or mucosal defect. The skin paddle can be folded upon inset for vaginal reconstruction, providing a durable and functional epithelial lining. Traditional experience has dictated this flap be avoided in cases where both urinary and fecal diversion are anticipated, as the cumulative insult to the abdominal wall was thought to be excessive when combined with use of the rectus abdominis. This has been shown to be incorrect. Recent reports have described use of the VRAM flap for perineal reconstruction via an extra-abdominal approach, insetting the flap into the perineum via a generous subcutaneous tunnel.18 Such approaches may well broaden its applicability. Advantages include the ability to provide reliable bulk and resurfacing potential to the perineum without a laparotomy being necessary. This strategy may prove especially useful in cases in which previous surgical procedures or external beam radiation therapy has rendered the abdominal wall or pelvis difficult to navigate safely. Disadvantages include the need for the flap to traverse the anterior rectus sheath and the associated risk of hernia. Furthermore, our experience has shown this to provide somewhat of a bulky perineal inset in terms of resurfacing needs. In some cases, this extra bulk may be advantageous, depending on the topography of the wound requiring reconstruction.

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Fig. 2
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Paramount abdominal donor-site perforator flaps that have been used in perineal reconstruction include the deep inferior epigastric artery perforator (DIEP) flap and the muscle-sparing VRAM flap. Popularized in breast reconstruction, the DIEP’s application in reconstruction of the perineum was described by Wang et al., who detailed a successful outcome in a series of five patients.19 The technical elements were refined somewhat by Ang et al.20 (Reference 20, Level of Evidence: Therapeutic, V) to include sub–Scarpa’s fascia thinning and were reported in 2009.18 Further modifications included an elliptical design of the flap measuring 5 to 7 cm × 16 to 24 cm on the long axis, and a Z-plasty–type inset. Proponents of the DIEP flap point to minimized donor-site morbidity; detractors cite the arduous and lengthy dissection required. To address this issue, Weiwei et al. recently reported on the use of the muscle-sparing VRAM in a clinical series of five patients.21 The authors describe the design of a 6 × 20-cm flap that was successful in all reconstructions at 2- to 9-month follow-up. They cite the relative speed and ease of flap elevation.

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Groin Flaps

The Singapore flap and perforator flap derivatives provide reliable functional reconstruction and perineal resurfacing. Groin flaps are used primarily to reconstruct surface defects of the perineum and groin, and vary in design (Fig. 3). Most common among groin-based regional flaps is the pudendal flap, widely known as the Singapore flap. The Singapore flap is a type I flap, based on the pudendal artery. Bilateral flaps can be used in tandem for functional vaginal reconstruction and perineal resurfacing.

Fig. 3
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Perforator flap reconstruction using groin donor sites has a history that can be traced back to the description of the pudendal thigh flap by Wee and Joseph in 1989 (Level of Evidence: Therapeutic, V).22 The authors reported an initial case series of three patients and used a 15 × 6-cm flap based on a network of perforating vessels from the internal pudendal artery and neighboring angiosomic systems. The flap and its variants gained widespread popularity, and a large clinical experience has been reported. Attributes include reliability of vascular supply and relative ease of flap elevation, while detractors have pointed out the poor skin quality for functional vaginal reconstruction. Sawada et al. described a variant, referred to as the lotus flap, based on perforators of the superficial perineal artery, a branch of the internal pudendal artery.23 Their case series of five patients described only minor complications and touted the versatility and stout nature of the flap. In 2001, Hashimoto et al. reported a further variant, known as the gluteal fold flap, based on internal pudendal artery perforators, utilizing the flap successfully in 10 patients.24 They described an inconspicuous donor site, the ability to debulk the flap safely, and only transient donor-site discomfort. Further freedom-of-inset has been more recently described by Sinna et al., who used propeller flaps based on similar perforating vessels.25 This variation expands the versatility of these proven workhorse flaps.

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Thigh Flaps

Perforator variations have extended the utility and dependability of gracilis and other thigh flaps. Thigh flaps are the alternative to the VRAM flap when considering reconstruction of large composite defects of the perineum and pelvis. They are generally favored in cases where a laparotomy approach has not been utilized by the ablative team. The gracilis flap (unilateral or bilateral) stands as the primary flap selected in these cases (Reference 27, Level of Evidence: Therapeutic, IV).26,27 It can be designed either as a muscle flap or as a myocutaneous flap (Fig. 4). This type II flap has a primary blood supply from the ascending branch of the medial circumflex femoral artery, arising from the profunda femoris system. The secondary segmental blood supply is from branches of the superficial femoral artery distally. The skin paddle design of the gracilis flap is traditionally oriented in a vertical manner in line with the long axis of the muscle, allowing for a less conspicuous donor-site scar position and for ease of closure (Figs. 4 through 5). The distal extent of the skin paddle when designed in this manner is well known to be predisposed toward epidermolysis or necrosis, given the variable and suboptimal perfusion of this distal cutaneous zone. More extensive soft-tissue defects in female patients often require bilateral flaps for sufficient bulk, as do many reconstructions in male patients given the inherently longer dimensions of the male pelvis. Skin paddles may be inset side to side and positioned to allow for functional vaginal reconstruction by providing durable epithelium. In addition, these skin paddles may also be designed with a sensory component. Other thigh donor-site flaps can be considered should the gracilis be unavailable or otherwise less desirable. The posterior thigh flap, based on the descending branch of the inferior gluteal artery, has been described for reconstruction of challenging pelvic and perineal defects.28 Similar to the gracilis, this flap is used primarily in cases in which a laparotomy has not been used for the extirpative portion of the procedure, in cases in which both urinary and lower intestinal diversion has been performed, or when resurfacing is required.

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Fig. 5
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Medial thigh perforator flap evolution has spurred the development of gracilis flap refinements. In 1989, Soper and colleagues described a gracilis flap variant based on the terminal branch of the obturator artery, with a 91 percent success rate and a less bulky, more pliable flap.29 More recent derivations include propeller flap modifications using dual donor sites, as described by Sinna et al.30 The posterior thigh flap, based on perforating vessels from the inferior gluteal artery, was initially described by Hurwitz and colleagues in 1981.31 A more nuanced appreciation of the angiosome has brought these flaps into the modern perforator flap era in the form of the superior gluteal artery perforator, inferior gluteal artery perforator, and related variant flaps, well described and proven in the reconstruction of various perineal defects (Figs. 5 and 6).32–36 Wagstaff and colleagues advocate the standard use of preoperative computed tomographic angiography to delineate the optimum choice of superior versus inferior gluteal artery perforator in posterior vaginal reconstruction.34 Of final importance in discussion of thigh donor perforator flaps is the application of the pedicled anterolateral thigh flap, based on perforators from the descending branch of the lateral circumflex femoral artery. This fasciocutaneous flap continues to gain popularity in perineal reconstruction and has broad utility in providing both bulk and resurfacing potential.37,38 Wang and colleagues have reported on a series of 18 patients in whom the anterolateral thigh flap was utilized in a pedicled fashion for reconstruction of posttumor ablative defects and chronic wounds, describing successful reconstruction in all cases.39 The authors emphasize the benefits in this setting of a long vascular pedicle, tension-free transfer to the perineum, ability to design the anterolateral thigh flap as a sensate flap, large skin paddle potential, and reliability, noting the minor downsides of color and hair density mismatch. As experience continues to deepen with this workhorse flap, it will certainly be an increasingly prominent and useful tool in the contemporary approach to perineal resurfacing.

Fig. 6
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Outcomes

Outcomes are good in general with modern techniques. Abdominal flaps may provide more reliable results with fewer complications. Outcomes are generally favorable after complex pelvic and perineal reconstruction, with flap failure being relatively uncommon. That said, the complex nature of the defects encountered, often in the setting of radiotherapy and medical comorbidities, make minor wound complications common. A recent study by Crosby et al. reviewed a series of 72 female patients undergoing immediate pedicled flap partial vaginal reconstruction, noting an 8 percent rate of readmission or reoperation and complications correlating with radiotherapy history and dose.40 Overall, outcomes were favorable, with 68 percent of patients reporting a functional reconstruction at a mean follow-up interval of 32 months.

In general, flap necrosis issues are more common with the gracilis and other thigh flaps than with the VRAM flaps. Given this, recent studies have compared outcomes in VRAM versus thigh flaps in the reconstruction of postoncologic ablative defects, finding superior outcomes with fewer complications in the VRAM group (Level of Evidence: Therapeutic, III).41 Given both options, the authors preferentially use the VRAM in cases in which both abdominal and thigh donor-site options are available.

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SUMMARY

The ongoing evolution of perforator variants of established abdominal, thigh, and groin flaps, in combination with their extended application, will have a positive impact on the future of perineal reconstruction. Considering the appropriate use of abdominal versus thigh/groin donor site, the current body of literature favors a more liberal application of the VRAM flap. As demonstrated by Nelson and Butler, in the presence of an abdominal component to the ablative approach, the VRAM flap should be the preferred source of a large volume of nonirradiated, healthy, well-vascularized tissue with a vigorous and reliable skin paddle.41 This will require a slight paradigm shift toward this reliable workhorse flap in preference to thigh flaps, despite the potential abdominal wall morbidity, given the more reliable coverage. Furthermore, in some cases, close coordination with the surgical oncologist and urologic surgeon may allow strategic siting of urinary and intestinal diversion for minimal impact on the contralateral abdominal wall, providing for the safe use of either the ipsilateral or contralateral rectus.

Of further note in discussion of the emerging, expanded range of the VRAM flap is a report of its use in an extraperitoneal fashion, perhaps foreshadowing a further broadened application in patients previously thought not to be candidates for VRAM reconstruction given a strictly nonabdominal approach to the extirpative operative portion. The recent description of this technique by Nigriny et al. portends this trend, again, based on this flap’s proven robustness and broad utility (Level of Evidence: Therapeutic, IV).18 These tunneled rectus flaps, in combination with Singapore, other groin, thigh, or emerging perforator flaps, may well prove to be a significant benefit in the ongoing management of complex reconstructive challenges in the pelvis and perineum. In the future, ongoing experience with perforator flap techniques and extended applications of the VRAM flap will continue to shape ever-improving solutions, and thus optimize outcomes.

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REFERENCES

1. Hencey JY, Vermess M, van Geertruyden HH, Binard JE, Manchepalli S. Magnetic resonance imaging examinations of gluteal decubitus ulcers in spinal cord injury patients. J Spinal Cord Med. 1996;19:5–8

2. Ruan CM, Escobedo E, Harrison S, Goldstein B. Magnetic resonance imaging of nonhealing pressure ulcers and myocutaneous flaps. Arch Phys Med Rehabil. 1998;79:1080–1088

3. Huang AB, Schweitzer ME, Hume E, Batte WG. Osteomyelitis of the pelvis/hips in paralyzed patients: Accuracy and clinical utility of MRI. J Comput Assist Tomogr. 1998;22:437–443

4. Larson DL, Gilstrap J, Simonelic K, Carrera GF. Is there a simple, definitive, and cost-effective way to diagnose osteomyelitis in the pressure ulcer patient? Plast Reconstr Surg. 2011;127:670–676

5. Han H, Lewis VL Jr, Wiedrich TA, Patel PK. The value of Jamshidi core needle bone biopsy in predicting postoperative osteomyelitis in grade IV pressure ulcer patients. Plast Reconstr Surg. 2002;110:118–122

6. Lewis VL Jr, Bailey MH, Pulawski G, Kind G, Bashioum RW, Hendrix RW. The diagnosis of osteomyelitis in patients with pressure sores. Plast Reconstr Surg. 1988;81:229–232

7. Cierny G 3rd. Surgical treatment of osteomyelitis. Plast Reconstr Surg. 2011;127(Suppl 1):190S–204S

8. Langer G, Schloemer G, Knerr A, Kuss O, Behrens J. Nutritional interventions for preventing and treating pressure ulcers. Cochrane Database Syst Rev. 2003(4):CD003216

9. Scivoletto G, Fuoco U, Morganti B, Cosentino E, Molinari M. Pressure sores and blood and serum dysmetabolism in spinal cord injury patients. Spinal Cord. 2004;42:473–476

10. Tchanque-Fossuo CN, Kuzon WM Jr. An evidence-based approach to pressure sores. Plast Reconstr Surg. 2011;127:932–939

11. Barker AR, Rosson GD, Dellon AL. Wound healing in denervated tissue. Ann Plast Surg. 2006;57:339–342

12. Keys KA, Daniali LN, Warner KJ, Mathes DW. Multivariate predictors of failure after flap coverage of pressure ulcers. Plast Reconstr Surg. 2010;125:1725–1734

13. Dzwierzynski WW, Spitz K, Hartz A, Guse C, Larson DL. Improvement in resource utilization after development of a clinical pathway for patients with pressure ulcers. Plast Reconstr Surg. 1998;102:2006–2011

14. Larson DL, Hudak KA, Waring WP, Orr MR, Simonelic K. Protocol management of late-stage pressure ulcers: A 5-year retrospective study of 101 consecutive patients with 179 ulcers. Plast Reconstr Surg. 2012;129:897–904

15. Siroky MB. Pathogenesis of bacteriuria and infection in the spinal cord injured patient. Am J Med. 2002;113(Suppl 1A):67S–79S

16. Waites KB, Canupp KC, Chen Y, et al. Bacteremia after spinal cord injury in initial versus subsequent hospitalizations. J Spinal Cord Med. 2001;24:96

17. Marriott R, Rubayi S. Successful truncated osteomyelitis treatment for chronic osteomyelitis secondary to pressure ulcers in spinal cord injury patients. Ann Plast Surg. 2008;61:425–429

18. Nigriny JF, Wu P, Butler CE. Perineal reconstruction with an extrapelvic vertical rectus abdominis myocutaneous flap. Int J Gynecol Cancer. 2010;20:1609–1612

19. Wang X, Qiao Q, Burd A, et al. A new technique of vaginal reconstruction with the deep inferior epigastric perforator flap: A preliminary report. Plast Reconstr Surg. 2007;119:1785–1790 discussion 1791

20. Ang Z, Qun Q, Peirong Y, et al. Refined DIEP flap technique for vaginal reconstruction. Urology. 2009;74:197–201

21. Weiwei L, Zhifei L, Ang Z, Lin Z, Dan L, Qun Q. Vaginal reconstruction with the muscle-sparing vertical rectus abdominis myocutaneous flap. J Plast Reconstr Aesthet Surg. 2009;62:335–340

22. Wee JT, Joseph VT. A new technique of vaginal reconstruction using neurovascular pudendal-thigh flaps: A preliminary report. Plast Reconstr Surg. 1989;83:701–709

23. Sawada M, Kimata Y, Kasamatsu T, et al. Versatile lotus petal flap for vulvoperineal reconstruction after gynecological ablative surgery. Gynecol Oncol. 2004;95:330–335

24. Hashimoto I, Nakanishi H, Nagae H, Harada H, Sedo H. The gluteal-fold flap for vulvar and buttock reconstruction: Anatomic study and adjustment of flap volume. Plast Reconstr Surg. 2001;108:1998–2005

25. Sinna R, Qassemyar Q, Benhaim T, et al. Perforator flaps: A new option in perineal reconstruction. J Plast Reconstr Aesthet Surg. 2010;63:e766–e774

26. Vyas RM, Pomahac B. Use of a bilobed gracilis myocutaneous flap in perineal and genital reconstruction. Ann Plast Surg. 2010;65:225–227

27. Ducic I, Dayan JH, Attinger CE, Curry P. Complex perineal and groin wound reconstruction using the extended dissection technique of the gracilis flap. Plast Reconstr Surg. 2008;122:472–478

28. Friedman JD, Reece GR, Eldor L. The utility of the posterior thigh flap for complex pelvic and perineal reconstruction. Plast Reconstr Surg. 2010;126:146–155

29. Soper JT, Larson D, Hunter VJ, Berchuck A, Clarke-Pearson DL. Short gracilis myocutaneous flaps for vulvovaginal reconstruction after radical pelvic surgery. Obstet Gynecol. 1989;74:823–827

30. Sinna R, Benhaim T, Qassemyar Q, Bréhant O, Mauvais F. Double L-shaped free-style perforator flap for perineal and vaginal reconstruction after cylindrical abdominoperineal resection. J Plast Reconstr Aesthet Surg. 2010;63:1740–1743

31. Hurwitz DJ, Swartz WM, Mathes SJ. The gluteal thigh flap: A reliable, sensate flap for the closure of buttock and perineal wounds. Plast Reconstr Surg. 1981;68:521–532

32. Leow M, Lim J, Lim TC. The superior gluteal artery perforator flap for the closure of sacral sores. Singapore Med J. 2004;45:37–39

33. Ahmadzadeh R, Bergeron L, Tang M, Morris SF. The superior and inferior gluteal artery perforator flaps. Int J Surg. 2005;3:53–60

34. Wagstaff MJ, Rozen WM, Whitaker IS, Enajat M, Audolfsson T, Acosta R. Perineal and posterior vaginal wall reconstruction with superior and inferior gluteal artery perforator flaps. Microsurgery. 2009;29:626–629

35. Benito P, García J, De Juan A, Alcazar JA, Elena E, Cano M. Reconstruction of a perianal defect by means of a bilateral V-Y advancement flap based on the perforating arteries of the gluteus maximus shaped over a cicatricial area. J Plast Reconstr Aesthet Surg. 2009;62:412–414

36. Boccola MA, Rozen WM, Ek EW, Teh BM, Croxford M, Grinsell D. Inferior gluteal artery myocutaneous island transposition flap reconstruction of irradiated perineal defects. J Plast Reconstr Aesthet Surg. 2010;63:1169–1175

37. Yu P, Sanger JR, Matloub HS, Gosain A, Larson D. Anterolateral thigh fasciocutaneous island flaps in perineoscrotal reconstruction. Plast Reconstr Surg. 2002;109:610–616 discussion 617

38. Ali RS, Bluebond-Langner R, Rodriguez ED, Cheng MH. The versatility of the anterolateral thigh flap. Plast Reconstr Surg. 2009;124(6 Suppl):e395–e407

39. Wang X, Qiao Q, Burd A, et al. Perineum reconstruction with pedicled anterolateral thigh fasciocutaneous flap. Ann Plast Surg. 2006;56:151–155

40. Crosby MA, Hanasono MM, Feng L, Butler CE. Outcomes of partial vaginal reconstruction with pedicled flaps following oncologic resection. Plast Reconstr Surg. 2011;127:663–669

41. Nelson RA, Butler CE. Surgical outcomes of VRAM versus thigh flaps for immediate reconstruction of pelvic and perineal cancer resection defects. Plast Reconstr Surg. 2009;123:175–183

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