Lymphocintilographic evaluation of lymphatic circulation in victims of circuferential degloving injuries of the lower limbs

ABSTRACT Introduction: secondary forms of lymphedema may occur as consequence of tumors, surgeries, radiotherapy, trauma and infections. Degloving injuries are severe and infrequent forms of trauma, with avulsion at the level of muscular fascia, and consequent injury of the lymphatic system. Objective: to evaluate the alterations in lymphatic circulation in patients being victims of circumferential degloving injuries in the lower limbs, using lymphoscintigraphic. Patients and Methods: retrospective analysis of the cases treated in the period from 2010 to 2016. Segmental, circumferential and unilateral injuries with involvement of the lower limbs were included. Lymphoscintigraphy was performed after a minimum interval of 12 months after the end of treatment. The non-injured lower limb was used as control. The Kleinhans Semiquantitative Index (KSI) was used for the semiquantitative evaluation of the lymphoscintigraphic findings. Results: eighteen patients were evaluated, six of whom were female and 12 were male. The mean age was 28.11 years. The average vertical extension of the circumferential traumatized segment was 29.33cm. The injured area presented variations of 5 to 15% of the body surface, with an average of 8.95%. Lymphoscintigraphy was performed after an average interval of 22.55 months. Alterations were observed on the traumatized limb (TL) in 13 patients. All control limbs (CL) were normal. The mean KSI observed in TL was 8.32, while in CL, the average value was 0.58 (p<0.001). Conclusion: patients with circumferential degloving injuries in the lower limbs present compromised lymphatic circulation and high probability to develop lymphedema.


INTRODUCTION
T he lymphatic system is a complex network, made up of capillaries and lymphatic vessels, lymph nodes, and lymphatic organs, which are vitally important for the maintenance of liquid homeostasis and for immunological aspects 1 .
Lymphedema can be understood as a manifestation of the insufficiency of the lymphatic system due to an alteration in circulation, that is, a reduction in transport of primary or secondary origin.It should not be understood only as a simple local edema process, but as a complex and systemic disease 2,3 .
Secondary forms of lymphedema, also called obstructive, are the most frequent, in more than 95% of cases 4,5 .There are clinical signs, which are usually more accentuated the greater the degree of stasis and the longer the duration of the process.
The etiologies normally associated with this type of injury are 6,7 : • Malignant neoplasms, as well as related or procedures, and genetic predispositions associated with environmental factors may play a role 3,8,9 .
There is scarce literature related to cases of post-traumatic lymphedema, and occurrences related to extensive injuries and deep burns can be found, with or without skin grafts, including prolonged latent periods [10][11][12][13][14][15][16] .Some authors have described that posttraumatic lymphedema can occur months or even years after trauma to the lower limbs.They also highlighted that there are still significant limitations in analyzing the evolution of the lymphatic system in the healing process.
They considered that there may be recanalization or even regeneration in scarring areas, including partial thickness skin grafts 15,17,18 .
Degloving injuries are uncommon skin and soft tissue traumas, characterized by avulsions of the skin and subcutaneous tissue from the plane of the muscle fascia, involving injury to the fasciocutaneous and musculocutaneous perforating vessels.They result from the application of sudden and high intensity forces with tangential vectors, promoting compression, stretching, torsion, and friction of the structures.Most injuries present as a continuity solution of variable size, with exposure of the fascia and muscles, being called open, typical, or anatomical degloving 19,20 .
In our service, we observed that, in cases with circumferential involvement, especially when there is greater vertical extension, postoperative edema of the distal segment was more significant and prolonged.This study aims to evaluate the sequelae and alterations of the lymphatic drainage in victims of circumferential degloving injuries of the lower limbs, based on lymphoscintigraphic analysis.

METHODS
We conducted a retrospective analysis of medical and photographic records of degloving injuries cases affecting the lower limbs, treated in the period from 2010 to 2016.
We included cases with exclusive trauma to the lower limbs, with segmental, circumferential, and unilateral involvement, who underwent debridement of traumatized tissues, subsequent wound preparation, and partial skin grafting.
The exclusion criteria were: • Bilateral lower limb trauma; • Associated vascular trauma; • Amputation of lower limb segment; • Previous edema of systemic etiologyheart, renal, thyroid, or liver failure; • Personal history of vascular surgeries in the lower limbs; • Personal history of thromboembolic events or diagnosis of post-thrombotic syndrome; and • Morbid obesity.
We analyzed sex, age, date of trauma, interval until the lymphoscintigraphy examination, affected body surface (ABS) by degloving injury (in %, using the Lund and Browder table), and vertical extension of the traumatized circumferential segment (in cm).
Regarding the type of skin graft used, all cases underwent a conventional hin split-thickness skin graft, removed with a Blair knife, with small random perforations for drainage.Expansion of the grafts by means of a reticular apparatus (mesh graft) was not performed.
Lymphoscintigraphy (LFCG) was performed after a minimum interval of 12 months after the initial surgical treatment (skin grafts in the raw areas).We used the non-traumatized lower limb as a control.
To assess the lymphoscintigraphic findings, we used the Kleinhans Semiquantitative Index -KSI.
We assessed the patterns of distribution, flow and path All patients signed an informed consent form.

RESULTS
In the period from 2010 to 2016, 75 victims of degloving injuries with involvement of the lower limbs were treated, and of these, 18 met the inclusion criteria.
In this group, 12 (66.7%)were males and six (33.3%) females.All patients had been run over by motor vehicles.
As for the affected side, the left corresponded to 55.6% of the cases (10), and the right, to the other eight patients.The time elapsed between treatment and lymphoscintigraphy was on average 22.55 months (13-31).
Regarding the occurrence of clinical manifestations in the traumatized limb (TL), these were In CL the mean value was 0.58 (0.15-0.75) (Table 1 and Figures 7 and 8).We observed five normal exams in the traumatized limbs, of which three did not present clinical manifestations.The other two had edema.In the group of patients who had altered lymphoscintigraphic exams (13), only one had no clinical manifestation.Table 2 shows the comparison of patients with normal and altered KSI exams.

Normal LFCG Altered LFCG
Fracture -Present 4 7 Fracture -Absent 1 6 Table 3 shows the comparative data of the KSI observed in TLs.

DISCUSSION
There has been an increase in the incidence of lymphedema, but unfortunately there is limited attention by the public and supplementary health systems, even in developed countries [21][22][23] .
Lymphedema is an inhibiting factor for healing.After trauma, there is the formation and opening of collateral lymphatic vessels, as well as the opening of connections between the superficial and deep systems 10.15,24,25 .
Trauma rarely presents itself as an etiology for lymphedema, and there are few related publications.
Lesser lesions, even if repetitive, present effective healing and vascular and lymphatic repair.For more extensive lesions, observations in the literature are inconsistent 26,27 .As for the occurrence of TL fractures, there were 11 cases.Table 4 brings the data referring to the findings of the LFCG exam.There were no cases of fractures in the CL.As mentioned, the occurrence of post-traumatic lymphedema is a rare and even unpredictable occurrence.
The existing observations come from case reports, mostly or at most from small series.One must also consider the limitations for analyzes based on these publications, given the different etiologies involved.Cases have been reported after a few months to a few years.One could question whether there was an evaluation only from more evident edema cases, with a possible existence of undiagnosed cases in earlier periods.
LFCG is the most used test to assess the lymphatic system, as well as for suspected lymphedema, still considered the standard test.It is a non-invasive procedure and is associated with minimal discomfort.Its disadvantages are the use of ionizing radiation and limited anatomical resolution [28][29][30] .
As for the LFCG findings, the presence of a popliteal lymph node is a sign of failure of lymphatic drainage through normal pathways.Dermal reflux is a sign of contrast extravasation due to hypertension in the proximal collectors, and contrast retention is a sign of overload and increased local hydrostatic pressure.
Collateral circulation is also a pathological marker 31 .
The Kleinhans's index has a sensitivity of 97.4% and a specificity of 90.3%.It is considered reliable and is well associated with clinical conditions 32,33 .
As for the time to perform the LFCG, we did not find any reference to similar cases in the literature for comparison.We chose to establish a period of 12 months after the partial skin graft, believing that the edema related to the usual postoperative period would have already regressed.
We observed five normal LFCG exams in the TL, and three of these patients also did not present symptoms.In the other two cases, there was edema.We did not find infectious conditions or thromboembolic events.The possibility of the occurrence of clinical or LFCG alterations in a longer follow-up period is disputed.
We did not expect normal results in LFCG exams in TL.There are no similar cases in the literature that allow for comparisons.From an anatomical point of view, we can assume that there was a complete loss of conventional superficial lymphatic circulation pathways in the lower limbs secondary to circumferential and extensive degloving injury.
Although there are no specific studies in the literature, we believe that the fenestration of the skin layers used may mean extra damage to the residual dermis and greater difficulties for recanalization or maintenance of flow through the residual lymphatic vessels.
split-thickness skin grafting is an unfavorable factor for the neoformation of lymphatic vessels, although this is an impression of case reports or small series.The available results show the absence of vessels in the segment directly below the grafted skin layers, which is a significant problem in cases such as the ones in this series, as they are grafts of greater length.
As for the existence of TL fractures, there was no association with severity or alterations in LFCG.In the 11 cases with fractures, four had normal exams.LFCG displayed alterations in six of the seven cases without fractures.
In our cases, all treatments for fractures were successful, without the occurrence of instability, lack of consolidation, or pseudarthrosis.All patients had open fractures with the possibility of bone coverage despite the soft tissue injury (Gustillo IIIa).More complex reconstructions with flaps (Gustillo IIIb) were not necessary, nor were associated vascular lesions requiring repair (Gustillo IIIc).Sapienza et al. 33 highlighted the identification of prominent lymphatic vessels or those with collaterals, as well as DR, in cases of edema after trauma or operations.The observation by Van Zanten et al. 18 is that there can be recanalization or even regeneration in scar areas or after trauma.These authors evaluated 17 cases of patients with Gustillo IIIb open fractures.Factors such as inflammation and hypoxia can also be limiting for the neoformation of lymphatic vessels 34,35 .
Lymphedema must be understood as a chronic, incurable, and slowly progressive disease, requiring lifelong treatment.The need for continuous care does not mean it cannot be effective or satisfactory 2,3,36 .In cases of treatment failures or difficulties, progressive skin changes, recurrent infections, progressive physical limitations, and psychosocial problems are observed 2 .
Considering the mechanism involved for the occurrence of degloving injuries, with transfer of significant amounts of energy after the contusion, in addition to the frequent association with fractures, we

R E S U M O R E S U M O
far, there are no factors that allow predicting the occurrence of lymphedema after trauma, operations, 1 -Irmandade da Santa Casa de Misericórdia de São Paulo, Serviço de Cirurgia Plástica -São Paulo -SP -Brasil 2 -Irmandade da Santa Casa de Misericórdia de São Paulo, Serviço de Emergência -São Paulo -SP -Brasil Mello Lymphocintilographic evaluation of lymphatic circulation in victims of circuferential degloving injuries of the lower limbs of lymphatic vessels, time to identify inguinal lymph nodes, and appearance, as well as the presence of collateralization, dermal reflux (DR), and the existence of a popliteal lymph node.The Kleinhans Semiquantitative Index ranges from 0 to 45, values less than 10 being considered normal.The maximum time for lymph nodes to appear is 200 min, with a score of 8.The absence of uptake will receive a score of 9.For statistical analysis of these results, we used the Wilcoxon and Mann-Whitney tests.This study was approved by the Ethics in Research Committee of the Irmandade da Santa Casa de Misericórdia of São Paulo, being registered under number (CAAE) 54209416.4.0000.5479and opinion 1.569,384.
present in 14 cases (77.7%),only edema being evidenced, observed from 12 to 18 months (according to reports and subjective assessment of patients).No local infection or thromboembolic events were observed, either in the TL or in the control limb (CL).As for the classification of the International Society of Lymphology, we observed four Grade 0 cases, six Grade 1, and eight Grade 2 cases.There were no Grade 3 cases.All patients underwent the LFCG exam within the established protocol and without complications.Changes in the TL examination were present in 13 cases (72.22%) and absent in five.The LFCG exam was normal in all CLs.The mean KSI observed in the TL was 8.32 (0.3-20.75), and we observed indexes >10 in nine patients.

Table 2 .
Comparison between normal and altered lymphoscintigraphic exams.

Table 4 .
Relationship between LFCG results and fractures in the traumatized limb (TL).

Table 1 .
Comparison between TL and CL lymphoscintigraphic exams.