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J Ped Surg Case Reports 1 (2013) 147e151

Journal of Pediatric Surgery CASE REPORTS

journal homepage: www.jpscasereports .com

Congenital pulmonary lymphangiectasis resulting in pleuraleffusions managed by thoracoamniotic shunting

Paul Singh a,*, Fatimah Ahmed b

aDepartment of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, University of Missouri Kansas City School of Medicine, 2301 Holmes Street, Kansas City,MO 64108, USAbUniversity of Missouri Kansas City School of Medicine, Kansas City, MO 64108, USA

a r t i c l e i n f o

Article history:Received 14 April 2013Received in revised form5 May 2013Accepted 7 May 2013

Key words:Congenital pulmonary lymphangiectasisPleural effusionsThoracoamniotic shunting

* Corresponding author. Tel.: þ1 817 524 5008; fax:E-mail address: paulsingh49@yahoo.com (P. Singh)

2213-5766/$ e see front matter � 2013 Elsevier Inc. Ahttp://dx.doi.org/10.1016/j.epsc.2013.05.003

a b s t r a c t

Congenital pulmonary lymphangiectasis (CPL) is a rare developmental disorder that has been associatedwith primary fetal pleural effusions. A 22 year old, Gravida-1 Caucasian woman presented at 26 gesta-tional weeks with bilateral pleural effusions and hydrops fetalis. Fetal ultrasound revealed rapidlyexpanding pleural effusions and hydrops fetalis. A throacoamniotic shunt was placed in the left pleuralspace at 27 gestational weeks. The patient eventually developed severe preeclampsia and non-reassuringfetal heart tones necessitating immediate cesarean delivery at 32 gestational weeks. Persistent bilateralpleural effusions were noted after delivery and chest tubes were immediately placed. Despite maximalventilatory support, continued bowel rest and an octreotide drip, both chest tubes continued to drain asignificant amount of chylous fluid. The neonate eventually developed multi-organ failure and expired onday of 19. Autopsy findings revealed diffuse CPL. CPL causes markedly distended pulmonary lymphaticsthat result in accumulation of fluid within the fetal pleural spaces. We report a case of CPL associatedfetal pleural effusions managed antenatally by throacoamniotic shunting.

� 2013 Elsevier Inc. All rights reserved.

Pleural effusions represent an abnormal buildup of fluid be-tween the layers of tissue that line the lungs and chest cavity.During fetal life pleural effusions occur infrequently with a reportedincidence of between 1/10,000 and 1/15,000 pregnancies [1]. Pri-mary fetal pleural effusions (FPEs) most often result from lymphaticaccumulation in the lungs brought about by anomalies in thethoracic duct, pulmonary tissue, or pleura [2e4]. Secondary FPEs,on the other hand, are most commonly associated with generalizedfluid retention seen in non-immune hydrops that can occur as aresult of a variety of etiologies such as isoimmunization, fetal ar-rhythmias, congenital infections, structural heart disease, alphathalassemia, aneuploidy, sacrococcygeal teratomas and twin totwin transfusion syndrome [5e11]. Congenital pulmonary lym-phangiectasis (CPL) is an extremely rare developmental disordercharacterized by markedly distended pulmonary lymphatics andhas been reported to result in primary FPEs [12].

Although small pleural effusions may remain stable or evenresolve spontaneously, larger ones may lead to fetal hydrops, pul-monary hypoplasia, esophageal compression with resultant poly-hydramnios, preterm birth and even stillbirth. Furthermore, FPEsmay prevent expansion of the lung parenchyma postnatally, thus,

þ1 816 404 5152..

ll rights reserved.

impeding oxygenation of the neonate following delivery. Ante-partum pleural decompression has emerged as a potential treat-ment modality for rapidly enlarging pleural effusions, pleuraleffusions resulting in a mediastinal shift or pleural effusions asso-ciated with hydrops fetalis. Indeed, fetal thoracentesis has beenshown to improve perinatal survival [13e15]. Unfortunately, sincepleural fluid often reaccumulates so rapidly, multiple pleural aspi-rations are required, thus, cumulatively increasing the risks ofprocedure associated morbidity like intrauterine infection, pretermrupture of membranes, and fetal injury [16]. Alternatively, thor-acoamniotic shunting can provide continuous pleural decompres-sion of the fetal pleural space, thus, avoiding the need for multipleinvasive procedures. We report a case of CPL that resulted inbilateral pleural effusions and hydrops fetalis managed antenatallyby throacoamniotic shunting.

1. Case presentation

A 22 year old, Gravida-1 Caucasian woman was referred to ourperinatal diagnostic center at 26 completed gestational weeks for ascreening fetal ultrasound. The fetus was found to have bilateralpleural effusions (Fig. 1), scalp edema, and polyhydramnios.The patient denied any prior medical history and had a negativeworkup for hydrops fetalis, including an otherwise normal targeted

Fig. 1. Axial ultrasound view of the fetal chest. Note the presence of bilateral pleuraleffusions.

Fig. 3. Axial ultrasound view of the fetal chest one day after placement of the thor-acoamniotic shunt. The blue arrow represents the thoracoamniotic shunt decom-pressing the left pleural space. (For interpretation of the references to color in thisfigure legend, the reader is referred to the web version of this article.)

P. Singh, F. Ahmed / J Ped Surg Case Reports 1 (2013) 147e151148

ultrasound and fetal echocardiography as well as a negativematernal antibody screen, complete blood count, KleihauereBetkestaining and maternal TORCH titers. An amniocentesis was per-formed and revealed a normal female karyotype. Follow-up so-nography at 27 completed gestational weeks demonstratedworsening pleural effusions with significantly retracted pulmonaryarchitecture noted bilaterally. Following administration of steroidsfor fetal lung maturity, a double pigtail thoracoamniotic catheter(Harrison shunt, Cook Medical, Inc., Spencer, IN, USA) was placed inthe left pleural space under ultrasound guidance. Due to fetalpositioning, the right pleural space was inaccessible and, thus, wasnot shunted. Postoperative ultrasonography performed the nextday revealed a nearly decompressed left pleural space with theshunt in proper position (Figs. 2 and 3). Serial ultrasounds per-formed weekly demonstrated a non-expanding right pleural effu-sion with no evidence of mediastinal deviation and improved signsof hydrops fetalis. Given that the stable appearance of the rightpleural effusion, right sided pleural drainage was not attempted. At32 completed weeks the patient developed severe preeclampsia

Fig. 2. Sagittal ultrasound view of the fetal chest one day after placement of thethoracoamniotic shunt demonstrating a reduction in the left pleural effusion (bluearrow). (For interpretation of the references to color in this figure legend, the reader isreferred to the web version of this article.)

and non-reassuring fetal heart tones necessitating immediate ce-sarean delivery. The 1 min, 5 min, and 10 min Apgar scores were 4,5, and 6 respectively and the birthweight was 2440 g. The arterialcord pH was 7.309 and the base deficit was 0.4. The neonateappeared dusky at birth with hypotonia and poor respiratory effort.Neonatal resuscitation was initiated with bag-masked ventilation,chest compressions and epinephrine. The infant was intubated andstarted on ventilatory support. A chest radiograph was immediatelyobtained and revealed bilateral pleural effusions. Bilateral chesttubes were placed and the thoracoamniotic shunt was removed.Molecular testing for Noonan’s syndrome was negative for thePTPN11 gene. Despite continued bowel rest, total parenteralnutrition and an octreotide drip, both chest tubes continued todrain over 200 ml/kg of chylous, straw-colored fluid. Repeat chestradiographs demonstrated hyperinflated lungs with persistentbilateral pleural effusions. The neonate eventually developedmulti-organ failure and expired on day 19. Autopsy findings revealeddiffuse CPL.

2. Discussion

First described by Virchow in 1856, congenital pulmonarylymphangiectasis (CPL) is a rare lymphatic vessel malformationcharacterized by abnormally dilated and thin-walled pulmonarysubpleural, interlobar, perivascular, and peribronchial lymphaticchannels. During fetal life lymphatic vessels within the lung nor-mally begin to diminish in size starting at approximately 20 weeksof gestation. For unknown reasons, in primary pulmonary lym-phangiectasia this regression process does not take place and thepersistence of large lymphatic vessels occurs with resultantdevelopment of severe lymphedema. In secondary pulmonarylymphangiectasia, dilated lymphatic vessels most commonlydevelop in conjunction with a variety of congenital heart defects,such as total anomalous pulmonary venous return, stenosis of thepulmonary and mitral valves, hypoplastic left heart, cor triatriatum,atresia of the pulmonary veins and atrioventricular canal defects[12]. It is hypothesized that cardiac lesions somehow interfere withthe normal regression of the lymphatic tissue elements during themid-second trimester [17]. More widespread abnormalities oflymphatic drainage have also been reported in cases of pulmonarylymphangiectasia involving dilation of lymphatic vessels in bones,viscera, and soft tissues.

P. Singh, F. Ahmed / J Ped Surg Case Reports 1 (2013) 147e151 149

The incidence of CPL is not clearly defined since only a fewisolated cases or small case series have been reported. Autopsystudies suggest, however, that approximately 0.5e1% of perinataldeaths may be attributed to CPL [17]. Most cases of CPL are sporadicand although familial occurrences have been described, no under-lying genetic etiology has yet been identified [18e20]. Two familialconditions inwhich CPLmay occur are Hennekam syndrome, whichpresents as congenital lymphedema with facial anomalies, intesti-nal lymphangiectasia, as well as varying degrees of mental retar-dation, and Njolstad syndrome, which is characterized bycongenital pulmonary lymphangiectasia along with facial andlower limb lymphedema. CPL has also been associated with 46,XY/46,XX mosaicism, ichthyosis congenita, Noonan’s syndrome, Tur-ner’s syndrome, Fryns syndrome, and Down’s syndrome [21]. Themortality rate for CPL is variable, ranging from 50% to 98%. Gener-ally, the prognosis of CPL depends on the severity of symptomsobserved in the immediate postnatal period. CPL associated withsystemic lymphangiectasia seems to have a slightly better prog-nosis than isolated CPL. The combination of CPL with hydropsfetalis, bilateral chylothorax or the immediate onset of severe res-piratory distress at birth has the worst prognosis.

Postnatally, newborns with CPL present with severe respiratorydistress, tachypnea, and cyanosis and mechanical ventilation isnearly always required. Prompt recognition of respiratory failure,surfactant administration, pleural decompression, and replacementof fluid and protein losses is paramount during the neonatal period.Nutritional support initially consists of total parenteral nutritionwith eventual introduction of a low-fat, high-protein diet, medium-chain triglycerides, and fat-soluble vitamin supplementation whenpleural drainage ceases. A low-fat intake is thought to aid inlymphatic decompression by the reduction of lymph flow fromintestinal lymphatics to pulmonary lymphatics. Frequently duringthe first month of life respiratory relapses and exacerbations occur.Infants with CPL may have significant growth failure and experi-ence recurring lower respiratory infections during early childhood.Older children can present with recurrent cough and frequentwheezing, increased respiratory effort and even congestive heartfailure.

Antenatally, CPL is most commonly associated with chylouspleural effusions; however, chylopericardium, chylous ascites,hydrops fetalis, or generalized lymphedema may also be seen. Theantepartum diagnosis of fetal pleural effusions was first describedin 1977 [1,22]. Ultrasound is the primary modality for the fetaldiagnosis of pleural effusions and appear as hypoechoic densitiessurrounding the lungs that generally conform to the normal con-tour of the chest [4]. The sonographic appearance of bilateralpleural effusions often appear as “bat wings” and may be seen bothin the axial and sagittal planes. Primary pleural effusions occuras a result of intrinsic vascular defects while secondary pleuraleffusions may be caused by a variety of etiologies that extrinsicallyalter circulatory dynamics and cause hydrops fetalis, such asbronchopulmonary sequestrations, congenital diaphragmatic her-nias, structural cardiac defects, cardiac arrhythmias, aneuploidy,congenital infections, red blood cell alloimmunization and glycogenstorage diseases. Yinon et al. stated that pleural effusions that areproportionately larger than fluid collections in other parts of thebody are more consistent with primary as opposed to secondaryeffusions [16]. Furthermore, pleural fluid with an elevatedlymphocyte count greater than 80% is more characteristic of pri-mary pleural effusions. The maternal workup for fetal pleuraleffusions includes a complete blood count, KleihauereBetkestaining, blood group and antibody screening, hemoglobin elec-trophoresis as well as toxoplasmosis, cytomegalovirus and parvo-virus serologies, while the fetal workup includes a detailedanatomical ultrasound, middle cerebral artery peak systolic velocity

measurements, fetal echocardiography, karyotype and cytomega-lovirus, toxoplasmosis, and parvovirus amniotic culture and PCR.

Although the prognosis of secondary pleural effusions is largelydependent upon treatment of the underlying disorder, spontaneousresolution of primary pleural effusions has been reported to occur.Aubard et al. described 204 cases of primary fetal hydrothorax, 22%of which spontaneously regressed [23]. Effusions that mostcommonly resolved occurred when the diagnosis wasmade early inthe second trimester, if the effusion was small and unilateral andthere was an absence of hydrops fetalis. Larger effusions, however,tend to result in worsening hydrops fetalis from cardiac tamponadeand impaired venous and lymphatic return, increased symptoms ofpreterm labor from esophageal compression with resultant poly-hydramnios and pulmonary hypoplasia due to chronic externalpressure. In cases where enlargement of the pleural effusion resultsin mediastinal deviation or significant lung retraction, fetal inter-vention to decompress the fluid collection, either via thoracentesisor thoracoamniotic shunting has been shown to improve perinatalsurvival [14,24]. Recently, Nygaard et al described seven fetuseswith primary pleural effusions who were treated by intrapleuralinjection of OK-432, which resulted in complete resolution with noperinatal mortality [25]. Further studies, however, are needed toclarify the role of this therapy.

Fetal thoracentesis, an invasive procedure to remove fluid fromthe pleural space using a 20 or 22 gage hollow needle, was firstdescribed by Peters et al., in 1982 [15]. It has been performedimmediately prior to delivery to facilitate neonatal resuscitationand to remove excess pleural fluid remote from delivery [13,14].Indeed, there have been reports of thoracentesis performed for fetalpleural effusions with complete resolution [13e15]. Unfortunately,others have reported rapid pleural fluid reaccumulation within24e48 h of fetal thoracentesis procedures, requiring multipledecompressive procedures and resulting in increased risks of in-trauterine infection, preterm rupture of membranes and fetal death[1,26e28]. Aubard et al. reported 29 cases where fetal thoracentesiswas performed between 17 and 37 weeks. Pleural fluid rapidlyreaccumulated in 76% of fetuses, 13 of which died [23]. Longakeret al. stated that thoracentesis cannot decompress the fetal chestenough to allow for pulmonary expansion and prevention of pul-monary hypoplasia [1].

Thoracoamniotic shunting for fetal pleural effusions was firstreported by Booth, Blott, and Rodeck et al. during the late 1980s[29e31]. Since then, pleural effusions have become one of themost common indications for in utero shunting. In a review of 47cases of hydropic fetuses, Picone et al. demonstrated a survival rateof 66% when thoracoamniotic shunting was performed [32]. Pet-terson et al. reported on 69 cases of thoracoamniotic shunting andfound a survival rate of 46.3% in hydropic fetuses and 100% innon-hydropic fetuses [24]. Rustico et al. recently described theirexperience of 53 fetuses who underwent thoracoamniotic shunt-ing, 43 of which were hydropic [33]. Overall survival was 58% forhydropic fetuses and 90% in non-hydropic fetuses. Finally, in alarge series of 88 patients where thoracoamniotic shunting wasperformed, Yinon et al. demonstrated a 52.5% survival in hydropicfetuses and 72.4% in non-hydropic fetuses [16]. When secondarycauses of FPEs are excluded, the survival rates for fetusesthat undergo thoracoamniotic shunting are markedly increased[27,28,34]. Although there are no randomized trials comparingthoracentesis to thoracoamniotic shunting, data analyzed retro-spectively suggests that for hydropic fetuses with pleural effusions,thoracoamniotic shunting is associated with higher survival ratescompared to serial fetal thoracentesis [23,24,33]. Complicationsof thoracoamniotic shunting include shunt obstruction and cath-eter migration into the amniotic fluid, fetal pleural space or eveninto the maternal peritoneal cavity [31]. Shunt reversal, where

P. Singh, F. Ahmed / J Ped Surg Case Reports 1 (2013) 147e151150

amniotic fluid drains into the fetal thoracic cavity as well astransient maternal ascites following thoracoamniotic shuntplacement have also been reported [31,35]. Less common fetalcomplications of thoracoamniotic shunting include fetal scarringand limb constriction [36e39]. Procedure-related fetal death israre, although may occur from hemorrhage from intercostal arterylaceration or torsion of the umbilical cord [1,11]. Maternal com-plications of thoracoamniotic shunting include chorioamnionitis,preterm premature rupture of membranes (PPROM) and pretermlabor.

Management of fetal pleural effusions depend upon the etiol-ogy, gestational age, rate of progression or regression, and presenceof hydrops. In order to exclude secondary causes of pleural effu-sions, fetal echocardiography should be performed. In cases ofsmall, unilateral effusions without hydrops or mediastinal shift, it isreasonable to proceed without any intervention since spontaneousregression may occur. It is important, however, that serial ultra-sounds be performed at least weekly since pleural effusions mayenlarge quickly. Between 24 and 32 gestational weeks, pleuraldecompression should be undertaken if mediastinal shifting,hydrops fetalis or rapid enlargement of the pleural effusion is noted[24,32,33,40,41]. Thoracentesis can be attempted initially and thefluid sent for cell count, culture, and karyotype in order to helpfurther elucidate the etiology of the pleural effusion. An additionalattempt at fetal thoracentesis may be made if the pleural effusionreaccumulates. Following two thoracentesis procedures, however,thoracoamniotic shunting should be considered. In fetuses withbilateral pleural effusions, both pleural spaces should ideally bedecompressed to avoid possible mediastinal shifting that mayoccur following unilateral decompression, preferably in a singleoperation in order to minimize uterine punctures. Yinon et al.described a technique of rotating the fetus with the blunt end of thetrocar to gain access to the contralateral side [16]. Prior to 24gestational weeks, termination of pregnancy may be performed,especially if the pleural effusion is associated with severe cardiacanomalies. After 32 gestational weeks, some authors elect to pro-ceed with delivery for worsening pleural effusions in favor ofpostnatal pleural decompression. On the other hand, given the poorsurvival of preterm neonates born with hydrops fetalis or signifi-cant pleural effusions, in utero pleural decompression has beenadvocated over premature delivery in any fetus less than 36gestational weeks [1]. Cesarean section is generally reserved forobstetrical indication. The thoracoamniotic shunts should beclamped during delivery in order to avoid development of apneumothorax. It’s imperative that intrapartum management becarried out in appropriately staffed centers capable of performingappropriate neonatal resuscitation.

3. Conclusion

Large fetal pleural effusions are a source of significant perinatalmorbidity. CPL is an extremely rare condition that can result insignificant accumulation of pleural fluidwithin the pleural space. Toour knowledge our case represents only the second reportedoccurrence of fetal pleural effusions caused by CPL managed withthoracoamniotic shunting [12]. The recognition of the differentialdiagnosis for fetal pleural effusions to include CPL and the under-standing of various modalities for prenatal surgical intervention isparamount for practitioners involved in maternal, fetal, andneonatal medicine.

Disclosure

No competing financial conflicts exist for any author-investigator.

Consent

No identifiable patient information was used in the preparationof the text or figures in this manuscript.

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