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Ann Thorac Surg 2003;76:1417-1420
© 2003 The Society of Thoracic Surgeons

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Original article: cardiovascular

Video-assisted ductal ligation in premature infants

^a Department of Cardiothoracic Surgery, Brenner Children’s Hospital, Wake Forest University/Baptist Medical Center, Winston-Salem, North Carolina, USA
^b Department of Pediatric Cardiology, Brenner Children’s Hospital, Wake Forest University/Baptist Medical Center, Winston-Salem, North Carolina, USA
^c Department of Pediatric Cardiac Anesthesia, Brenner Children’s Hospital, Wake Forest University/Baptist Medical Center, Winston-Salem, North Carolina, USA

^* Address reprint requests to Dr Hines, Department of CT Surgery, Wake Forest University School of Medicine, Medical Center Blvd, Winston-Salem, NC 27157, USA.
e-mail: mhines{at}wfubmc.edu

Presented at the Forty-ninth Annual Meeting of the Southern Thoracic Surgical Association, Miami Beach, FL, Nov 7–9, 2002.

	Abstract

Top Abstract Introduction Material and methods Results Comment Discussion References

 
BACKGROUND: Video-assisted thoracic surgery has been shown to be a safe and effective method of closing the patent ductus arteriosus in infants and children. We have applied this technique in low birth weight premature infants and now report our experience.

METHODS: Since 1996, we have used video-assisted thoracic surgery ligation as the treatment of choice for all patent ductus arteriosus, including 100 performed on premature infants (23 to 31 weeks’ gestation, mean 25.6 weeks; 0.420 to 1.5 kg, mean 0.859 kg). A modification of our previously described technique was used with a three-port approach. All patients had some degree of symptoms of congestive failure with failure to wean from ventilatory support or oxygen dependency. Five infants had associated patent foramen, and 1 had a small ventricular septal defect.

RESULTS: All 100 procedures were performed in the operating room. One infant was found to have a coarctation, and the procedure was aborted. The remaining 99 were successfully ligated, although three were converted to an open procedure (3%) because of coagulopathy, poor pulmonary compliance, or hemodynamic instability. There were no procedure-related deaths; however, 15 infants subsequently died of complications of prematurity, including enterocolitis, sepsis, and late respiratory failure. Six infants had chest tubes left in place for coagulopathy, effusions, suspected air leak, and existing empyema. There were six residual pneumothoraces, four requiring treatment.

CONCLUSIONS: Video-assisted thoracic surgery is a safe and effective technique for patent ductus arteriosus ligation in premature infants, including those with very low and extremely low birth weight.

	Introduction

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Video-assisted approach to patent ductus ligation has been used by several centers since its first description in 1995, including a previous report from our institution with our initial experience of 59 patients [1–5]. To date we have performed 250 such procedures with excellent results and minimal morbidity. As our experience progressed we extended the use of the technique to include not only term infants but also premature infants weighing less than 1 kg, as has been previously reported in a smaller series by another group [6]. Although the benefits of a minimally invasive approach over an open thoracotomy are easily demonstrated in older children, the safety of this technique and its potential benefits in premature infants remains controversial. We have now performed the procedure in 100 premature infants of very low birth weight (< 1500 g) and extremely low birth weight (ELBW, < 1000 g) and report our experience.

	Material and methods

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We retrospectively reviewed our experience with 100 premature infants treated over a 6-year period from June 1996 until May 2002. After gaining some early experience with the technique of video-assisted thoracoscopic surgery (VATS) to close the patent ductus arteriosus (PDA), we extended use of the technique to smaller infants, performing our first procedure on a child less than 1 kg at 1 year into our total VATS experience (June 1996). After that, all patients were deemed candidates for the minimally invasive procedure unless they were considered too unstable for transport either hemodynamically or from a ventilation standpoint, in which case the ductus was ligated through a minithoracotomy in the neonatal intensive care unit (NICU). Patients maintained on the high frequency oscillatory ventilation were converted to conventional support before transport to the operating room. Inability to tolerate this change constituted instability necessitating open ligation in the neonatal intensive care unit (usually about 2 to 4 patients per year). The 100 patients included 51 males and 49 females weighing from 420 to 1500 g (mean, 859 g). Mean age at operation was 16 days (3 to 51 days). Gestational age ranged from 23 to 31 weeks with a mean of 25.6 weeks, and all but 6 of the 100 were less than 28 weeks. Five infants had an associated patent foramen, and 1 child had a small ventricular septal defect. All VATS patients had some degree of congestive heart failure symptoms or failure to wean from ventilatory support as their indication for operation. The presence of the patent ductus was confirmed in all cases by preoperative transthoracic echocardiography, usually after at least one course of indomethacin failed to close the ductus. Although 6 infants received no indomethacin therapy before closure, the majority were treated with one to four courses, with an average of two courses. The ductal size was evaluated by echocardiography and categorized on a five-point scale with the average of 3.2. (1 = small, 2 = small to moderate, 3 = moderate, 4 = moderate to large, 5 = large).

All procedures were performed in the operating room, with the patient under general endotracheal anesthesia and in the left thoracotomy position. We used a slight modification of the technique previously reported for older children [5]. Only three ports were used in the majority of this population; we omitted the axillary port used for instrumentation. Cotton-tip applicators were used as lung retractors through the anterior port, and the camera port remained in the midaxillary line. A 2.7-mm, 30-degree angled scope was used. Clip application was performed through the posterior port. Intraoperative transesophageal echocardiography was not available because of the size of the patients, and postoperative echocardiograms were not obtained routinely because of the excellent visualization of the ductal closure with the scope in these small patients. Chest tubes were left in place only in selected high-risk cases, and patients were returned to the neonatal intensive care unit on positive pressure ventilation after the procedure. Retrospective review examined morbidity, including conversion to thoracotomy, chest tubes, wound complications, recurrent nerve injury, and survival. Analysis of the mortality and survival was compared to expected survival using standardized survival indices based on gestational age and the percentage of the studied population, and then summed to obtain a predicted survival for the group [7].

	Results

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Of the 100 patients taken to the operating room, four procedures (4%) were converted to minithoracotomy (muscle sparing by expansion of the auscultatory triangle). One procedure was abandoned and converted to open thoracotomy when it was discovered that the infant had an undiagnosed coarctation. The other three were converted for open PDA ligation (3%) for coagulopathy obscuring visualization with the scope, severe noncompliance of the lung impeding exposure, and cardiorespiratory instability requiring resuscitation and replacement of the endotracheal tube. The remaining 96 patients underwent successful closure of the PDA. Procedure times ranged from 13 to 63 minutes (mean, 32.8 minutes). There was no intraoperative bleeding requiring transfusion, although several infants did receive a transfusion during the procedure after it being started preoperatively in the neonatal intensive care unit for routine indications.

Five recurrent nerve injuries (5%) were identified by bronchoscopy in the postoperative period. We did not routinely evaluate all infants; however, any infant with suspected aspiration, difficulty with swallowing, or any observed hoarseness of cry after extubation underwent evaluation. We included both paresis and frank cord paralysis on the left side as a nerve injury. Four of the five injuries were followed up and found to be temporary, and the fifth had not resolved at the 18-month follow-up (1%). No evaluation was available for infants who did not survive because they never were successfully weaned from the ventilator and therefore never qualified for an examination.

Although chest tubes were removed routinely in the operating room under positive pressure ventilation and gentle aspiration, 6 patients had drains left in place. Three of these patients were coagulopathic and had a recent history of thrombocytopenia with significant oozing during the procedure. A fourth patient had some abraded areas along the left upper lobe, and a tube was placed because of concerns of a possible air leak. All four of these tubes were removed on postoperative day one. Two other patients were found to have white cloudy effusions in the left pleural space, one with significant pleural inflammation. Cultures and chemistry studies were obtained, which demonstrated positive triglycerides and negative cultures. Both infants had been receiving central hyperalimentation and intralipid infusions. Both underwent successful ligation of their ductus and then had tubes left in for drainage of the effusion. These were removed on postoperative day 2 and 4. No wound infections were noted in the series.

Postoperative chest x-rays obtained on the evening of the operation revealed a pneumothorax in 6 patients. Two were insignificant and resolved without treatment. One noted soon after the operation was aspirated successfully. The remaining 3 patients had chest tubes placed through the anterior port site that evening for significant pneumothoraces. None of these infants had air leaks after reexpansion of the lung, and the tubes were removed the following day. Three other infants developed new pneumothoraces within 48 hours of the procedure, after initially having normal postoperative chest x-rays. One of the three was on the right side, and all three were thought to be related to difficulty with ventilation and were temporally related to increases in ventilator support. One child was incidentally noted to have free air under the right hemidiaphragm and underwent abdominal exploration where a remote ileal perforation was identified and treated.

There were no intraoperative deaths. Fifteen of the 100 premature infants did not survive to discharge, expiring from postoperative day 2 up to day 148 (Table 1). Eleven of the 15 died secondary to sepsis, including 5 with associated necrotizing enterocolitis. Of the remaining 4, 3 died late of extensive chronic respiratory disease at least 2 months after the procedure, and the fourth succumbed to eventual multisystem failure after 3 months. None of the deaths were believed to have any relationship to the procedure or its complications.

	Comment

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The absence of any need for transfusion or urgent thoracotomy demonstrates that the previously reported VATS technique in children and adults can be applied safely to very low birth weight and extremely low birth weight infants as well. The 15% mortality rate in the series appears to be unrelated to the surgical procedure, but rather due to the underlying diseases and complications of prematurity. Predicted survival for this group of infants based on standardized indices for gestational age, and calculated based on the 86 patients between 23 and 27 weeks’ gestation was 65%, and the actual survival rate was 86%. Therefore an observed survival of 85% in the entire group is not unexpected and in fact better than predicted, and can be explained by complications of prematurity independent of the operation.

While we have demonstrated that video-assisted ductal ligation is feasible in even the smallest of premature infants, it is much more difficult to establish its advantages over an open technique than it is with young children who have less pain, less scar, no narcotics, and not only avoid a night in the intensive care unit, but are discharged the evening of the operation. First, the sum total of the three port incisions is almost as long as a minithoracotomy incision. Second, these infants return to the neonatal intensive care unit on the ventilator, and it has never been shown that even open PDA ligation has a significant effect on their hospital stay. What we are left with is a potential benefit of scoliosis reduction and a perceived benefit in metabolic stress.

It has been clearly demonstrated that there is an increased risk of scoliosis after thoracotomy, although the exact forces which lead to the deformity are not known [9, 10]. Division of the latissimus and serratus, intercostal muscle division and closure, and pleural scarring have all been implicated. Theoretically, the smaller the patient at the time of the thoracotomy, the longer the forces have to affect spinal column growth, and potentially, the worse the scoliosis. This would imply that minimally invasive techniques may provide the most benefit with the smallest patients. In the face of this uncertainty, we propose that minimizing the incisions and trauma to the chest wall may in fact minimize the impact on the spine. Although we can now ligate a ductus through a fairly small skin incision in an open technique while sparing the latissimus and serratus, it still requires division of the intercostal muscles and spreading of the ribs to some degree, an effect that is avoided with the VATS approach. Obviously this question will remain unanswered until we have sufficient patients entering into their early adolescent years to undergo spinal evaluations and be compared to both historical controls (open PDA ligation) and temporal thoracotomy controls (open PDA ligation, coarctation, tracheoesophageal fistula, etc). We are currently planning this investigation as our earliest patients are now reaching school age.

Although it is extremely difficult to evaluate the effect of a surgical procedure on the metabolic or stress response of a premature infant, our neonatology colleagues have expressed a sense that the procedure seems to be less injurious in general than an open procedure. Although this is still not measurable, this perception has led to several interesting patterns of behavior that may have indirectly decreased the potential morbidity of repeated and persistent medical therapy with indomethacin. While the numbers are too small to apply statistical analysis, Table 2 shows a trend over the past 6 years toward earlier consultation for surgery with fewer rounds of medical attempts to close the PDA, including several patients referred for closure without any treatment with indomethacin because of one or more relative contraindications to its use, including renal insufficiency, recent intracranial hemorrhage, thrombocytopenia, and suspected or proven necrotizing enterocolitis. Although it may be an unproven perception of decreased morbidity with a less invasive approach, if the perception changes behavior, and if the resultant surgical intervention is at least as safe as the open technique, its earlier application may lead to fewer attempts at closure with medical treatment and the concomitant risks.

	Discussion

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DR KRISTINE GULESERIAN (St. Louis, MO): I really enjoyed your presentation. I have just one question for you. Since many premature infants require high-frequency oscillatory ventilation, how many, if any, patients in your series were on an oscillator at the time of the PDA ligation using the thoracoscopic approach?

DR HINES: In the first couple of years many of the kids were on the oscillator, and we used the oscillator as a contraindication; we would operate on those kids upstairs in the unit. But as the neonatologists got enamored with this procedure, they would convert them from the oscillator to the conventional vent. If they are stable for 2, 3, or 4 hours, we would take them to the operating room, would do it through the thoracoscope, take them back up and they will put them back on it.

Those are usually kids that have pulmonary interstitial emphysema and other indications for the oscillator, and in fact now only the kids who are just really crashing and hemodynamically sick get done open in the unit, and that is about two to four kids per year, and the oscillator has not been a contraindication at all.

DR ERLE H. AUSTIN III (Louisville, KY): Dr Hines that was a lovely presentation and you are clearly skilled in this technique. My question to you relates to using this technique with a residency program in thoracic surgery. I do think there is some skill and some risk to it, and unfortunately, because the interventionalists have taken away a lot of the procedures that we typically use as the first thing we help a resident through, I am concerned that this technique is too risky to help a resident perform. My question is: do you help the residents perform this technique in premature infants?

DR HINES: That is an excellent question. Currently, no, we are not teaching the residents how to do this, because our training program has been training residents who are interested in adult cardiac or adult thoracic surgery. I am committed, if we get a resident interested in doing congenital heart disease, to teach him how to do it. The problem is that they are not interested in doing this, and in fact, if we then open the sick kids in the unit, I make sure the resident is available to get that experience.

We have had very few complications from this, and of the ones in the unit, one resident accidentally tore the ductus and one resident clipped the ductus and part of the aorta. So I am getting less likely to want to do it open.

However, it is an important part of the training program, but because congenital heart surgery is getting so specialized, and with these premature infants, very few adult surgeons are really dabbling in this.

Now, again, if we get a resident who is very interested in congenital heart surgery and wants to spend the time, I am certainly willing to teach him. I think if you start teaching with the older kids, work your way down, you can certainly do it.

	References

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1. Burke R.P., van der Velde M., Hansen D., Jonas R.A. Patent ductus arteriosus: interruption by video-assisted thoracoscopic surgery (VATS) in 100 consecutive patients. Circulation 1995;92(Suppl 1):121.
2. Laborde F., Noirhomme P., Karam J., et al. A new video-assisted thoracoscopic technique for interruption of patent ductus arteriosus in infants and children. J Thorac Cardiovasc Surg 1993;105:278-280.[Abstract]
3. Laborde F., Folliguet T., Batisse A., et al. Video-assisted thoracoscopic surgical interruption. The technique of choice for patent ductus arteriosus. Routine experience in 230 pediatric cases. J Thorac Cardiovasc Surg 1995;110:1681-1685.[Abstract/Free Full Text]
4. Chu J.J., Chang C.H., Lin P., et al. Video-assisted thoracoscopic operation for interruption of patent ductus arteriosus in adults. Ann Thorac Surg 1977;63:175-179.
5. Hines M.H., Bensky A.S., Hammon J.W., Pennington D.G. Video-Assisted Thoracoscopic Ligation of Patent Ductus Arteriosus. Safe and Outpatient. Ann Thorac Surg 1998;66:853-859.
6. Burke R.P., Jacobs J.P., Cheng W., et al. Video-Assisted Thoracoscopic Surgery for Patent Ductus Arteriosus in Low Birth Weight Neonates and Infants. Pediatrics 1999;104(2):227-230.[Abstract/Free Full Text]
7. Rothman, KJ. "Standardization of Rates" in Modern Epidemiology. Chapter 5. pp 40–47. Little, Brown and Company 1986
8. Bensky A.S., Raines K.H., Hines M.H. Late follow-up after thoracoscopic ductal ligation. Am J Cardiol 2000;86(3):360-361.[Medline]
9. Van Biezen F.C., Bakx P.A.G.M., De Villeneuve V.H., Hop W.C.J. Scoliosis in children after thoracotomy for aortic coarctation. J Bone Joint Surg 1993;75-A(4):514-518.[Abstract/Free Full Text]
10. Westfelt J.N., Nordwall A. Thoracotomy and scoliosis. Spine 1991;16:1124-1125.[Medline]

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