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Journal of Pediatric Surgery (2011) 46, 507–513

Congenital vascular anomalies in amniotic band syndromeof the limbs☆,☆☆

Mahendra Daya⁎, Manti Makakole

Department of Plastic and Reconstructive Surgery, Nelson R Mandela school of Medicine, University of Kwazulu-Natal,Durban, South Africa

Received 27 July 2009; revised 8 September 2010; accepted 9 September 2010

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Key words:Amniotic band syndrome;Vascular anomalies

AbstractIntroduction: Bone abnormalities and nerve compression are sparsely reported features of amniotic bandsyndrome. No studies of the vascular architecture of limbs affected by this syndrome have been published.Material and Methods: Patients with amniotic band syndrome affecting the limbs were evaluated in theperiod between 1997 and 2007. The arterial blood supply was studied using magnetic resonanceangiography or computed tomographic angiography. The subjects comprised 8 patients with bilateral and2 with unilateral limb involvement. The patients' ages ranged from 2 months to 8 years. The male-to-female ratio was 4:6. A total of 20 limbs was investigated, comprising 18 lower limbs and 2 upper limbs.The amniotic bands were divided into superficial or deep.Results: The patients were divided into 4 groups: group 1, thigh bands; group 2, below-knee amputations;group 3, leg bands; and group 4, upper limb bands. A single patient in group 1 with a deep band had apersistent sciatic artery. In group 2, three limbs demonstrated attenuated segments in the superficialfemoral artery and/or abnormalities arising at the popliteal artery division. In group 3 (14 legs), 7 with deepbands showed some anomaly either in the popliteal artery division or its branches or both. In the other 7,and in group 4, all with superficial bands, no vascular abnormalities were seen except in one.Conclusion: Our findings show that amniotic band syndrome is definitely associated with vascularabnormalities and the depth of the band is an important contributory factor.© 2011 Published by Elsevier Inc.

The amniotic band syndrome (ABS) is a rare collection of

☆ Meeting at which this paper was presented: the Association of Plasticnd Reconstructive Surgeons of South Africa congress, Cape Town, Southfrica, October 2007.

☆☆ No specific or external funding was received for this study. Theatients were treated in a public hospital and the cost of the treatment wasaid for by the state. The authors have derived no financial benefits from theonduction of this study.⁎ Corresponding author. Department of Plastic and Reconstructive

urgery, Inkosi Albert Luthuli Central Hospital, Mayville, 4058, Southfrica. Tel.: +27 0 31 240 2134; fax: +27 0 31 240 2133.E-mail address: dayam@iafrica.com (M. Daya).

022-3468/$ – see front matter © 2011 Published by Elsevier Inc.oi:10.1016/j.jpedsurg.2010.09.006

fetal abnormalities. External clinical manifestations in thelimbs are those of a triad of constriction rings, acrosyndac-tyly, and limb reduction defects. In addition to the limbdefects, the syndrome can be associated with visceralabnormalities. The manifestation or effects on internalstructures of affected limbs have not adequately been studied.There are a few reports of bone and nerve involvement [1,2].Other than ischemic threatened limbs or in utero limbamputation, nothing has been recorded about the vascularconsequences. Multiple synonyms have been used for thesyndrome reflecting the varied theories of its pathogenesis.

508 M. Daya, M. Makakole

In a prospective study, we undertook to investigate thevasculature of the affected limbs in this syndrome. The aimof the study was to determine in the limbs of childrenaffected by ABS the vascular architecture, the presence ofany abnormalities in the major vessels, and a possible causalrelationship if abnormalities were found.

Table 1 Tabulated summary of the clinical series of the subjects inv

Group no. Patient groups Case Level Depth

1 Upper thigh andleg bands

1 L thigh, leg Thighleg—s

2 Below-kneeamputation

2 R upper and middlethird interface

3 R upper and middlethird interface

4 R upper and middlethird interface

3 Leg bands 5 R lower third leg Deep

4 L lower third of leg Deep

3 L lower third of leg Upperlower—

6 R lower third of leg Deep

7 R lower third of leg Deep

7 L lower third of leg Deep

8 R lower third of leg Deep

9 R lower third of leg Superf9 L lower and middle

third of legsuperf

5 L lower third of leg Superf10 R lower third of leg Superf10 L lower third of leg Superf8 L lower third of leg Superf6 L lower third of leg Superf

4 Upper limbbands

7 L upper arm Superf9 L distal forearm Superf

a indicates artery; L, left; R, right; PFA, profunda femoris artery.

1. Materials and methods

All patients presenting with ABS affecting the long bonesection of the limbs were evaluated in the period between1997 and 2007. The arterial vasculature was studied usingmagnetic resonance angiography (MRA) or computed

estigated for vascular anomalies

Vascular abnormality Figure no.

—deep,uperficial

L persistent sciatic a, absent SFAand bifurcation of popliteal a

1, 2

Very attenuated vessels pasttrifurcation of popliteal arterywith attenuated proximal segmentof the SFA

3, 4

No PA with ATA and PTA cutoffat the stumpVery attenuated branches ofbifurcation of popliteal artery.Attenuation of the proximal anddistal part of SFATrifurcation of the popliteal a. PAcontinues into the foot. The ATAand PTA peters out in the calf

5, 6, 7

Bifurcation of popliteal a. AbsentPA. ATA continues into foot andPTA peters out above band andcollateral flow is seen into thefoot

—deep,superficial

Trifurcation of the popliteal a.ATA cutoff above band with anormal PA and PTATrifurcation of the popliteal a.ATA peters out in midcalf. Aslightly attenuated PTA continuesinto the foot. An HypertrophiedPA continues into foot as ATA

8, 9

Bifurcation of the popliteal a.with an absent PTA. Poorlyvisualized PFABifurcation of the popliteal a.with an absent ATA. Poorlyvisualized PFATrifurcation of the popliteal a.With runoff into the distal legwith a dominant ATA

icial Normalicial ATA cutoff at the band, PTA and

PA enlargedicial Normal 5, 6, 7icial Normalicial Normalicial Normalicial Normal 8, 9icial Normalicial Normal

ig. 2 On the medial view the PSA (A) is noted in the posteriorigh and the superficial femoral artery (B) is of smaller caliber andinterrupted in the middle of the thigh.

509Amniotic band syndrome of the limbs

tomographic angiography. The study comprised 10 patients,of whom 8 patients had bilateral and 2 unilateral involvement(Table 1). The patients' ages ranged from 2 months to8 years. The male-to-female ratio was 4:6. There was a totalof 20 limbs involved with 18 lower and 2 upper limbs. In thelower limb–affected patients, 1 had thigh and leg involve-ment, whereas 17 had leg involvement only. Of these, 3 wereassociated with clubfoot deformities.

In retrospect, the bands, based on the magneticresonance imaging and photographs, were subjectivelydivided into superficial or deep. Superficial bands demon-strated relatively shallow indentation on imaging withsubcutaneous tissue interposed between the band andunderlying musculoskeletal structures, whereas deepbands had relatively deep indentations with no or verylittle subcutaneous fat. Seven lower limbs had superficialbands only and 6 had deep bands only. Two limbs had botha superficial and a deep band. Three of the lower limbs hadamputations at the junction of the upper and middle third ofthe leg. Both of the affected upper limbs had superficialbands only.

2. Results

The single-patient group 1 presented with a deep thighband and a superficial leg band (Fig. 1). This patient also hadmany other congenital abnormalities. The reader is referredto our published case report [14]. The MRA demonstrated apersistent sciatic artery and the superficial femoral artery(SFA) terminated after the profunda femoris branchcommencement. The popliteal continuation of the SFAended in a bifurcation (Fig. 2).

The second group included 3 patients, each demonstratinga below-knee amputation at the junction between the upperand middle thirds of the tibia. All 3 limbs demonstrated a

Fig. 1 Three-month-old child with constrictions on the left thighand leg (the side with the PSA) and duplication of the right kneeand tibia.

Fthis

coned stump (Fig. 3). Two of these limbs demonstrated anattenuated segment in the SFA (Fig. 4) Two of them alsodemonstrated a bifurcation of the popliteal artery and one a

Fig. 3 A child demonstrating a below-knee amputation on theright side and a left clubbed foot with digital reduction, with anabsence of bands on the leg.

Fig. 4 On the right, a very attenuated segment of the SFA with nodiscernable branches of the popliteal artery on this MRAreconstruction is shown. On the left, normal vasculature is shown.

Fig. 5 A patient showing a band on the distal third of the eachleg. The right was classified as deep and the left as superficial.

ig. 6 Magnetic resonance imaging scan shows the right band isevoid of any deep fat and the left has some fat noted. The bands areerefore respectively classified as deep and superficial.

510 M. Daya, M. Makakole

trifurcation. In 2 of them, the branches of the popliteal arterywere very attenuated after the commencement and failed toreach the end of the stump (Fig. 4). Only in one stump wasit evident that the attenuated 2 vessels extended to thestump end.

The third group included 8 patients with 14 affected legs,of which 7 had deep bands and 7 had superficial bands. Allthe legs with a deep band demonstrated an anomaly orvariation in the vasculature of the leg. Four legs demon-strated a trifurcation, and 3 legs showed a bifurcation of thepopliteal artery (Figs. 5-7).

Two of the legs with trifurcations had one of the branchesend above the band and the other 2 vessels continued distal tothe band. In the one leg (case 3), the former was the anteriortibial artery (ATA) and the latter were the peroneal artery(PA) and the posterior tibial artery (PTA). In the other leg,too, the discontinued branch was the ATA, but in the foot,the PTA was slightly attenuated and the PA was hypertro-phied. In the foot, the PA appeared to have taken over theterritory of the ATA (Figs. 8 and 9). In the other 2 legs withtrifurcation, the one leg showed 2 branches (ATA and PTA)expend themselves above the band, and the other PAcontinued beyond into the foot supplying the territory of theATA and PTA (Fig. 7). In the other leg, a normal runoff withdominant ATA was seen.

In the 3 legs with the bifurcation of the popliteal artery,each leg in turn showed the absence of each one of thebranches of the popliteal artery. In one leg (case 4), the

Fdth

Fig. 7 Magnetic resonance angiography scan on the right showsa trifurcation, with both the ATA and the PTA petering out in thecalf and the PA continuing into the foot, supplying the territory ofboth the ATA and PTA.

Fig. 8 A patient showing bilateral bands with the right beingdeep and the left being superficial.

Fig. 9 Magnetic resonance angiography scan shows on the rightan ATA ending in the midcalf. The PA continues into the footsupplying the ATA territory there. The continuation of the PTA intothe foot is slightly attenuated. On the left, the popliteal artery andbranches are noted to be normal.

511Amniotic band syndrome of the limbs

absent vessel was the PA, and the ATA was the only vesselthat continued into the foot; the PTA petered out above theband with filling of its territory in the foot occurring bycollateral flow. The other 2 legs belonged to a single patient(case 7). In both these legs, the profunda femoris vessel waspoorly visualized.

In the 7 lower limbs with single superficial bands, only 1leg demonstrated an anomaly. The popliteal artery showed anormal trifurcation with the ATA ending at the band, and thePTA and PA continued distally beyond the band butappeared to be enlarged. Two other lower limbs withvascular anomalies, case 1 (Fig. 2) and case 3, also had

Table 2 Vascular abnormality relative to depth of amnioticband or amputation

Amniotic bandof limb

Vascular anatomy Total

Normal Abnormal

Depth BKA 0 3 (100%) 3Deep 0 8 (100%) 8superficial 8 (89%) 1 (11%) 9

Total 8 (40%) 12 (60%) 20

BKA indicates below-knee amputation.

512 M. Daya, M. Makakole

superficial bands, but these limbs also had a more proximaldeep band.

In the fourth group, the 2 upper limbs with superficialbands demonstrated normal MRA.

2.1. Assessment of the association between depthand abnormality

The risk of vascular abnormality in deep bands was100%, but was 11.1% in superficial bands. Depth of bandwas significantly associated with arterial abnormality with aP b .001 (Table 2).

3. Discussion

The incidence of congenital absence of a major artery ofthe leg does not in the normal population exceed 2% [3]. Ourseries of patients with amniotic bands of the limbsdemonstrated a congenital anomaly incidence of the vascularsupply of 60%. Clearly, the depth of bands was an importantfactor with regard the likelihood of a vascular anomalybecause deep bands had a 100% incidence as compared to11.1% for the superficial bands. Group 2, the amputationgroup, which probably represents the ultimate injury in termsof depth, also demonstrated a 100% incidence of vascularanomalies in the affected limbs.

A feature of this series was that in most cases of abnormalvascular anatomy, the anomalies occurred a fair distanceproximal to the region of the band. These included absentmajor vessels (Fig. 2), atretic segments in the major limbarteries (eg, Fig. 4), and absent branches (eg, Fig. 7). Somebranches of the trifurcation petered out above the band (eg,Figs. 7 and 9) with one leg demonstrating hypertrophiedvessels with unusual territorial takeover of the foot arterialsupply (Fig. 9).

The etiology of ABS is controversial with multipletheories having been proposed by various researchers overthe decades. The 2 main theories are the intrinsic andextrinsic theories.

In 1930, Streeter, the main proponent of the intrinsictheory, implicated imperfect histiogenesis as the develop-mental error responsible for the focal limb deficiency [4].He concluded that a primitive defect of the germinal platewas responsible for anomalies of formation of theamniotic membrane.. Some authors supported this hy-pothesis and even expanded it [5-7]. A teratogenic insultor vascular disruption has been suggested as sources of themalformations. Van Allen et al supported this theory in1992 when they presented 2 cases showing evidence ofvascular disruption in the absence of any demonstrableamniotic bands. Serial intrapartum diagnostic screeningshowed hepatic infarction in one case and a vanishingtwin in the other, signifying indirect evidence of avascular disruption [5].

The extrinsic theory appears to be the most accepted. In1965, Torpin strongly supported amniotic bands as the causeof ABS [8]. He proposed as the mechanism separation of theamnion from the chorion. This in turn leads to tears in theamniotic membrane through which fetal parts couldprotrude. Initially, the amniotic fluid gets absorbed by thechorion, resulting in a transient period of oligohydramnios. Itis this oligohydramnios that is thought to result in clubbedfeet, a condition that accompanies ABS in 33% of cases [9].With time, the chorion matures resulting in decreasedabsorption of liquor, and normal liquor volume is restored.Fibrous strands form on the chorionic side and the extrudedfetal parts get caught by these, resulting in the typical bandsfound in this condition. Higginbottom and associatescomplemented Torpin's theory in a review of 79 cases,suggesting that the defects seen in ABS are subject to thegestational age at which the sac ruptures [10]. Roswell wasable to reproduce the limb defects using ligatures arounddeveloping limbs of a fetal rat model [11]. Moerman andcolleagues studied the fetopathology of several patients withABS. They found that the constrictive bands involved clearlyconsisted of tissue that was amniogenic in nature [12].Finally, in 1995, Laberge and associates demonstratedconclusively a case of antepartum diagnosis of an amnioticband attached to and restricting the movement of a fetal limbin utero, using real-time video sonography. The baby waslater confirmed to have an amniotic band at the same site atbirth [13].

The case in group 1 probably reflects the earliest insultto the vascular embryologic development in the lower limb[14]. The sciatic artery is the axial artery of the leg at 6weeks (6 mm) and some of its territories are taken over bythe femoral artery reaching the adult pattern of vasculatureof the lower limb by the eighth week (22 mm). Therefore,it would be logical to surmise that for these reportedanomalies to occur, they would have to occur before theeighth week. At that stage it is unlikely that the extrinsicetiology is the contributing factor. Furthermore, intrinsictheories may explain our case with persistent sciatic artery.The patient demonstrated other seemingly unrelatedabnormalities in the opposite limb, which can only beexplained by a common intrinsic insult between the 6- and22-mm stages of embryogenesis. However, work done byKennedy demonstrated a constellation of defects in ratfetuses by amniotic puncture at 14 to 16 days of gestation,which is the time equivalent of 4 to 6 weeks of gestationin humans [15].

Most of the vascular anomalies that were detected onthe magnetic resonance imaging appeared to be fairlyproximal to the band or amputations. The deep amnioticbands had a 100% incidence of vascular anomalies. Thelatter finding maybe indicative of in utero extrinsiccompression from the deep band interfering with anormally developing limb artery. In response, secondaryvascular changes may include attrition of the arteryproximal to the band, persistent patency of a more

513Amniotic band syndrome of the limbs

primitive limb artery, and alternate collateral flowdevelopment. If a proximal primary intrinsic insult and avascular disruption were the more likely cause of the limbreduction defects of ABS, should we not have seen a muchhigher vascular anomaly rate than 11.1% with superficialbands? Werler investigated maternal vasoactive agentexposure during pregnancy in births with amniotic bandsvs the terminal transverse limb deficiencies, both of whichhave been attributed to vascular disruption. He concludedthat vascular disruption may not play a major role in thepathogenesis in either type of limb deficiency [16].On theother hand, in our series, the finding of attenuatedsegments of the major vessels or the total absence ofthem may not be secondary to the band formation in theaffected limb. Our findings of vascular anomalies as anindicator of causal relationship or a common pathogenesisremain unclear.

4. Conclusion

This series is the first study that has investigated thevascular architecture in ABSs of the limbs. Our findingsshow that ABS is definitely associated with vascularabnormalities. It is generally accepted that the depth of theband is an indicator of the severity of the in utero insult andin all likelihood, as shown in this series, a marker ofunderlying vascular anomalies. The vascular anomaly iseasily explained as an effect of ABS, but a causal associationcannot be excluded. Nevertheless, the etiology of ABSremains unclear and abnormalities cannot be explained by asingle theory. However, it is hoped that the finding ofvascular anomalies in ABS will help direct future research.

Acknowledgment

My sincere gratitude is extended to Dr Warwick Morrisfor reviewing the manuscript.

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