Esophagography Predicts Favorable Outcomes
after Laparoscopic Nissen Fundoplication for
Patients with Esophageal Dysmotility
Matthew J D’Alessio, MD, Steven Rakita, MD, Mark Bloomston, MD, Christopher M Chambers, MD,
Emmanuel E Zervos, MD, FACS, Steven B Goldin, MD, FACS, Jerry Poklepovic, MD, H Worth Boyce, MD,
Alexander S Rosemurgy, MD, FACS
We undertook this study to determine if clearance of a food bolus at preoperative esophagography predicts acceptable outcomes after laparoscopic Nissen fundoplication for patients with
manometrically abnormal esophageal motility.
STUDY DESIGN: Patients with gastroesophageal reflux disease (GERD) or symptomatic hiatal hernia with evidence of esophageal dysmotility by stationary manometry underwent videoesophagography to
document the ability of their esophagus to clear food boluses of varying consistencies. Sixty-six
patients were identified who had manometric dysmotility yet were able to clear a food bolus at
esophagography, and subsequently underwent laparoscopic Nissen fundoplication. These patients were compared with 100 randomly selected patients with normal motility who underwent laparoscopic Nissen fundoplication. Symptom reduction and satisfaction were assessed
through followup. Patients with normal motility were compared with those with manometrically moderate and severe dysmotility.
RESULTS:
Preoperative patient demographic data, symptoms, and symptom scores were similar among
patients with normal motility and moderate or severe dysmotility. After fundoplication, symptom reduction was notable for all patients regardless of preoperative motility (p ⬍ 0.01, paired
Student’s t-test). There was no notable difference in postoperative symptom scores (p ⫽ NS,
Kruskal-Wallis ANOVA) or in patient satisfaction (p ⫽ NS, chi-square analysis) among patients
stratified by esophageal motility.
CONCLUSIONS: Patients with esophageal dysmotility documented by manometry who are able to clear a food
bolus at contrast esophagography, have functional results after laparoscopic Nissen fundoplication similar to patients with normal motility. Preoperative esophagography predicts successful
outcomes after laparoscopic Nissen fundoplication for patients with manometric esophageal
dysmotility. (J Am Coll Surg 2005;201:335–342. © 2005 by the American College of
Surgeons)
BACKGROUND:
Esophageal dysmotility commonly occurs with gastroesophageal reflux disease (GERD). In a study of more
than 1,000 patients with GERD, 44% had an esophageal motility disorder.1 Degree of esophageal dysmotility
can correlate with the severity of GERD.2,3 Although the
association between GERD and esophageal dysmotility
is clear, a cause-and-effect relationship is not obvious. And
although pronounced dysmotility is a recognized cause
of GERD, mechanisms by which GERD can promote
esophageal dysmotility are unestablished.4 Whether dysmotility is a result of acid in the esophageal lumen, the
corresponding mucosal injury, or other causes, remains a
point of speculation. Adding to the debate, medical control of reflux symptoms has not been successful in restoring esophageal motility.5,6 In contrast, several studies
have shown that operative correction of GERD results
in partial or even complete resolution of esophageal
dysmotility.3,7-10 This probably reflects the superior efficacy of reflux control through operative reconstruction
Competing Interests Declared: None.
Received April 16, 2004; Revised April 27, 2005; Accepted April 29, 2005.
From the Departments of Surgery (D’Alessio, Rakita, Bloomston, Chambers,
Zervos, Goldin, Boyce, Rosemurgy) and Radiology (Poklepovic), University
of South Florida College of Medicine, Tampa, FL.
Correspondence address: Alexander S Rosemurgy, MD, FACS, Department
of Surgery, University of South Florida, Tampa General Hospital, PO Box
1289, Rm F-145, Tampa, FL 33601.
© 2005 by the American College of Surgeons
Published by Elsevier Inc.
335
ISSN 1072-7515/05/$30.00
doi:10.1016/j.jamcollsurg.2005.04.036
336
D’Alessio et al
Esophagography and Esophageal Dysmotility
of the lower esophageal sphincter mechanism compared
with medical antisecretory therapy. Notably, other investigators have shown that there is little or no resolution
of esophageal dysmotility after operative correction of
GERD.11
Management of patients with medically refractory
GERD and esophageal dysmotility is controversial.
Conventional wisdom purports a limited role for operative intervention in the presence of esophageal dysmotility, citing a propensity for substantial dysphagia after
fundoplication. Consistent with this, successful outcomes after Nissen fundoplication for patients with
esophageal dysmotility are difficult to predict.12 Although some surgeons maintain that complete (Nissen
360°) fundoplication is well tolerated by patients with
esophageal dysmotility, other surgeons argue that partial
fundoplication is less likely to cause dysphagia.12-14 The
difficulty in predicting outcomes after fundoplication in
patients with GERD and manometric esophageal dysmotility has led some surgeons to undertake partial fundoplication, with its limited efficacy, to avoid postoperative dysphagia or to defer surgical intervention altogether.15-17
The ability to identify clinically adequate esophageal
emptying would be helpful in predicting successful outcomes for patients with abnormal motility by esophageal
manometry. It has been our practice to evaluate patients
with abnormal manometric motility using videoesophagography with barium-laden food boluses with patients
in a 15° Trendelenberg position. Patients with adequate
esophageal clearance by videoesophagography underwent laparoscopic Nissen fundoplication.
This study was undertaken to report our results with
laparoscopic Nissen fundoplication for patients with
esophageal dysmotility by stationary esophageal manometry and adequate esophageal clearance by videoesophagography with barium-laden food boluses with
the patient in a 15° Trendelenberg position. Our hypothesis in undertaking this study was that patients with
manometric esophageal dysmotility who are able to clear
a barium-laden food bolus at preoperative esophagography in a 15° Trendelenberg position would achieve functional outcomes after laparoscopic Nissen fundoplication similar to those seen with patients having normal
manometric esophageal motility.
METHODS
More than 800 patients with GERD or symptomatic
hiatal hernia, or both, who underwent fundoplication
J Am Coll Surg
from 1991 to 2002 were prospectively followed through
a registry system. Before laparoscopic Nissen fundoplication, patients underwent stationary water perfusion
esophageal manometry and 24-hour pH monitoring using commercially available instrumentation. Patient
data collection and study design were conducted in concordance with a protocol approved by the Institutional
Review Board of the University of South Florida College
of Medicine.
Esophageal motility
Esophageal motility was graded by contraction amplitude (mmHg) and propagation of peristalsis (%) measured by stationary esophageal manometry. Normal
esophageal motility was defined as mean distal esophageal contractions of ⬎ 60 mmHg and ⬎ 80% of esophageal contractions propagated as peristaltic waves. Patients with abnormal motility were stratified by the
degree of esophageal dysmotility. Moderate dysmotility
was defined as mean contractions of 31 to 60 mmHg or
51% to 80% propagation of peristalsis, and severe dysmotility was defined as mean contractions of ⬍ 30
mmHg or ⬍ 50% propagation of peristalsis.
Videoesophagography
Patients with dysmotility identified by esophageal manometry underwent videoesophagography with fluoroscopic imaging. Esophageal peristalsis and emptying
were examined in prone horizontal and prone 15° Trendelenburg position. Patients were asked to swallow a
single large bolus of barium (Barosperse, Lafayette Pharmaceutical Co) thinned with water to a 20% suspension.
Peristalsis was first observed during a single large bolus
swallow of barium. A normal examination consisted of
uninterrupted progression of the contraction wave and
complete emptying of the esophagus with two or fewer
stripping waves. Incomplete emptying of the upper third
of the esophagus was not considered abnormal. Patients
were then challenged with a food bolus using a mechanical soft (marshmallow) and then a solid (bagel) food
bolus. Patients were given what they considered their
usual-sized portion (ie, bite) of the marshmallow or bagel. Once the food left their mouth, they swallowed a
small amount of the thinned liquid barium. Adequate
clearance was again judged as passage of the food bolus
with two or fewer stripping motions. Failure was defined
as incomplete progression of peristaltic contractions or
the need for repeated (more than two) stripping motions
Vol. 201, No. 3, September 2005
D’Alessio et al
for clearance of the esophagus. Patients with manometric dysmotility who failed to adequately clear the food
bolus did not undergo laparoscopic Nissen fundoplication because of concern that they would experience severe dysphagia postoperatively. Patients with GERD or
symptomatic hiatal hernia, or both, with normal motility and those with dysmotility who were able to adequately clear a food bolus during the preoperative
esophagography as described underwent laparoscopic
Nissen fundoplication.
Esophagography and Esophageal Dysmotility
337
terior fundus behind the esophagus to the right crus to
remove tension, which might otherwise result in twisting of the lower esophagus or promote “unwrapping” of
the fundoplication. All trocar sites were closed with
monofilament absorbable suture under laparoscopic visualization using the Endo Close device (US Surgical
Corporation). Patients routinely began a liquid diet
when awake, and were generally discharged home
within 24 hours of their operation.
Statistical analysis
Clinical assessment
Patients with dysmotility who had adequate food clearance on esophagography and then underwent laparoscopic Nissen fundoplication were identified from the
registry. They were compared with 100 randomly selected patients with normal esophageal motility who underwent laparoscopic Nissen fundoplication.
Preoperative and postoperative symptom scores were
graded by patients using a Likert scale (range 0 to 10)
during their clinic visits or, for some late followup, by
mail or telephone.
Statistical analysis was undertaken using True EPISTAT
(Epistat Services). Median scores (mean ⫾ standard deviation) for each symptom were calculated before and
after fundoplication. Paired Student’s t-test was used to
compare symptom scores before and after fundoplication for patients categorized by degree of dysmotility.
The Kruskal-Wallis ANOVA was used to compare preoperative and postoperative symptom scores among
patients with normal motility and moderate or severe
dysmotility. Patient satisfaction was compared using
chi-square analysis. Two-tailed probabilities were used to
assign statistical significance with 95% confidence.
Technique of fundoplication
Laparoscopic Nissen fundoplication was undertaken
with the patients supine using a five-port technique. The
gastrohepatic omentum was opened widely in a stellate
manner. Dissection was carried along the edge of the
right crus, working to reduce any hiatal hernia and free
an adequate (approaching 8 cm) length of intraabdominal esophagus. The stomach was then rolled to the patients’ right and the short gastric vessels were divided.
Dissection was carried along the edge of the left crus and
into the mediastinum, such that any hiatal hernia was
completely reduced. A generous window dorsal to the
esophagus was established. A posterior cruroplasty was
sutured with 0-gauge braided polyester sutures (Surgidac, US Surgical Corporation) to close the esophageal
hiatal defect. The gastroesophageal fat pad was routinely
removed. The posterior fundus was brought behind the
esophagus with a 52F to 60F bougie placed po into the
stomach and the fundoplication was constructed. The
anterior fundus was secured to the esophagus and to the
posterior fundus well above the gastroesophageal junction with two sutures. A third suture brought the anterior fundus and the posterior fundus together at the
gastroesophageal junction. A posterior gastropexy was
constructed, suturing the dorsal most portion of the pos-
RESULTS
Sixty-six patients with GERD or symptomatic hiatal
hernia, or both, who were shown to have dysmotility by
esophageal manometry, yet were able to adequately clear
a barium-laden food bolus during videoesophagography, underwent laparoscopic Nissen fundoplication. Of
these patients, 33 had severe dysmotility by esophageal
manometry, although 33 had moderate dysmotility. For
comparison, 100 patients with GERD or symptomatic
hiatal hernia, or both, and normal esophageal motility
by manometry who underwent laparoscopic Nissen fundoplication were randomly selected from our prospectively collected database. Preoperative characteristics of
these patients are presented in Table 1. There were no
notable differences in age, gender distribution, preoperative DeMeester scores, or preoperative symptom scores
among patients stratified by esophageal motility. Heartburn, dysphagia, gas and bloat, and postprandial nausea
were the four most commonly reported preoperative
symptoms.
A small number of patients had normal DeMeester
scores. These patients had symptomatic large sliding hiatal or paraesophageal hernias, or both, with dysphagia
as a predominant symptom, and were distributed evenly
338
D’Alessio et al
Esophagography and Esophageal Dysmotility
J Am Coll Surg
Table 1. Preoperative Characteristics of Patients Undergoing Laparoscopic Nissen Fundoplication Stratified by Degree of
Esophageal Dysmotility
Preoperative characteristics
N
Mean age ⫾ SD (y)
Gender (% male)
Median DeMeester score, range
Mean contraction amplitude ⫾ SD (mmHg)
Mean percentage of propagated swallows ⫾ SD
Mean heartburn score ⫾ SD
Mean nausea score ⫾ SD
Mean dysphagia score ⫾ SD
Mean gas/bloat score ⫾ SD
Mean length of followup (mo), range
Normal motility
Moderate dysmotility
Severe dysmotility
p Value
100
52 ⫾ 14.6
40
34, 1⫺234
102 ⫾ 33
99 ⫾ 2.2
8.1 ⫾ 2.7
4.5 ⫾ 4.2
5.0 ⫾ 4.2
6.3 ⫾ 3.9
22, 1⫺78
33
53 ⫾ 15.4
48
39, 1⫺361
55 ⫾ 10
94 ⫾ 10.5
8.7 ⫾ 2.8
5.2 ⫾ 4.2
6.2 ⫾ 3.7
5.8 ⫾ 4.0
23, 1⫺72
33
49 ⫾ 13.3
57
32, 5⫺221
39 ⫾ 26
48 ⫾ 35.7
7.0 ⫾ 3.7
3.2 ⫾ 3.7
5.6 ⫾ 3.6
4.0 ⫾ 3.4
15, 1⫺63
—
NS*
NS†
NS*
—
—
NS*
NS*
NS*
NS*
NS*
*Kruskal-Wallis ANOVA.
†
Chi-square analysis.
NS, differences are not statistically significant (p ⬎ 0.05).
among patients with normal motility and moderate or
severe dysmotility (14 patients, 1 patient, and 5 patients:
respectively; p ⫽ NS, chi-square).
Overall, mean length of follow up was 21.4 (⫾20.5)
months. The mean symptom scores for heartburn, dys-
phagia (sensation of food stuck in the chest), and nausea
were notably reduced by laparoscopic Nissen fundoplication for patients of all categories of motility (p ⬍ 0.05,
paired t-test) (Fig. 1). Postoperative symptom scores for
heartburn, dysphagia, nausea, and gas and bloat did not
Figure 1. Mean symptom scores before and after laparoscopic Nissen fundoplication for patients with normal preoperative
esophageal motility and moderate or severe dysmotility. Reductions in severity of symptoms after fundoplication were
statistically significant (p ⬍ 0.05, paired t-test) except for gas/bloat, as noted. No significant differences (*p ⫽ NS,
Kruskal-Wallis ANOVA) in postoperative symptom scores were found among patients with normal esophageal motility and
those with moderate or severe dysmotility.
Vol. 201, No. 3, September 2005
D’Alessio et al
differ notably among patients stratified by esophageal
motility (p ⫽ NS, Kruskal-Wallis ANOVA). Of note,
symptoms of gas and bloat, frequently reported before
operation, were not worsened by fundoplication. Although mean scores for dysphagia decreased with laparoscopic Nissen fundoplication, an increase in the dysphagia score occurred in 14% of patients with normal
preoperative motility, 9% of patients with moderate dysmotility, and in 9% of patients with severe dysmotility
(p ⫽ NS, chi-square). None of the patients who reported an increase in dysphagia required additional endoscopic or surgical intervention. Preoperative dysphagia scores had no impact on postoperative dysphagia
scores by regression analysis for all patients
(p ⫽ NS, r2 ⫽ 0.007), and for patients with severe
dysphagia (p ⫽ NS, r2 ⫽ 0.06), moderate dysphagia
(p ⫽ NS, r2 ⫽ 0.10), and normal motility (p ⫽ NS,
r2 ⫽ 0.0008).
Eight patients (4.8%) required reoperative procedures. Mean age was 46 ⫾ 18.3 years. Mean body mass
index was 28 ⫾ 4.6. Five patients had normal motility
and three had moderate dysmotility. Seven hiatal failures
occurred and three wrap failures, one that had been
somewhat obstructive. There was one slipped fundoplication and an unrelated gastric outlet obstruction developed in one patient. Two patients had documented severe blunt trauma as a possible cause of their hiatal
disruption. Of the six patients who reported subjective
outcomes after reoperation, three described good outcomes and four would undergo an operation again, despite having required revision.
Complications associated with laparoscopic Nissen
fundoplication were uncommon. Overall complication
rate was 8%. Complications were minor, the most common was urinary retention and CO2 pneumothorax.
There were no gastrotomies, esophagotomies, leaks,
myocardial infarctions, pulmonary emboli, strokes, major exacerbations of preoperative medical comorbidities,
or deaths.
Patient satisfaction is depicted in Figure 2. Overall,
85% of patients who underwent laparoscopic Nissen
fundoplication were satisfied with outcomes of the operation at the time of followup. There was no notable
difference in satisfaction rates among patients with normal esophageal motility, and those with moderate or
severe manometric dysmotility with normal esophageal
clearance by videoesophagography (p ⫽ NS, chisquare). Satisfaction was not uniform. Dissatisfaction
Esophagography and Esophageal Dysmotility
339
Figure 2. Percentage of patients reporting overall satisfaction after
laparoscopic Nissen fundoplication stratified by degree of manometric dysmotility. Differences between groups were not statistically
significant (p ⫽ NS, chi-square).
was often a result because issues involving cost of care,
hospital amenities, pain and discomfort, and in a small
number, exacerbation of dysphagia, or need for operative revision.
DISCUSSION
Manometric esophageal dysmotility is commonly encountered during the preoperative evaluation of patients
with medically refractory GERD or symptomatic hiatal
hernia.10 Although the role for Nissen fundoplication for
patients with GERD and normal esophageal motility is
well established, the role for operative intervention for
patients with esophageal manometric dysmotility and
intractable GERD remains controversial despite extensive study.7-14,18-21 Although there are several reports of
excellent outcomes after Nissen fundoplication for patients with manometric dysmotility, these results are not
universal.6,7,12,18,19 New dysphagia, or exacerbations of
existing dysphagia, develop in a substantial number (approaching 20%) of patients with GERD and esophageal
dysmotility after Nissen fundoplication.19,21 In summation, outcomes after Nissen fundoplication for patients
with esophageal dysmotility is too often poor and impossible to predict by the nature and degree of manometric dysmotility.12 This study defines a group of patients with esophageal manometric dysmotility that can
undergo laparoscopic Nissen fundoplication with outcomes indistinguishable from patients with normal
esophageal manometric motility.
Although it is tempting to apply complete (Nissen
360°) fundoplication because of its low rate of recurrent
reflux, some surgeons in an effort to avoid dysphagia,
promote partial fundoplication or other (eg, Hill) anti-
340
D’Alessio et al
Esophagography and Esophageal Dysmotility
reflux procedures.10,13-15 Although these latter procedures might seem attractive because of prospects of
decreased postoperative dysphagia, similar efficacy
compared with Nissen fundoplication has not been consistently demonstrated.19 Unfortunately, poor durability
of partial fundoplications, with relatively high rates of
recurrent reflux, renders these procedures less than optimal.16,17 This is the first study to establish a preoperative screening method that is able to determine which
patients with manometric esophageal dysmotility have
adequate esophageal peristaltic function to undergo
laparoscopic Nissen fundoplication with outcomes indistinguishable from patients with normal manometric
esophageal motility.
This study is a single institutional outcomes analysis
that involves predominantly middle-aged patients with
GERD stratified by degree of manometric esophageal
dysmotility. Our criteria for defining moderate and severe dysmotility are consistent with the criteria used in
other current studies of esophageal dysmotility.9,10,15 All
patients underwent laparoscopic Nissen fundoplication
for treatment of GERD or symptomatic hiatal hernia.
Patients unable to clear food boluses at esophagography
were not offered operative therapy.
Preoperative DeMeester scores were similarly elevated
for those with normal and impaired esophageal motility.
Preoperative symptom scores were similarly elevated for
patients with all categories of manometric motility.
Followup ranged from 1 to 72 months and was similar among the patients categorized by esophageal motility. Laparoscopic Nissen fundoplication brought about
substantial reduction in symptom scores for heartburn,
dysphagia, and postprandial nausea for patients with
normal motility and for those with moderate and severe
manometric dysmotility. Severity of preoperative dysphagia had no association with severity of postoperative
dysphagia. This is not unexpected, given that patients
with severe preoperative dysphagia generally have symptoms caused by a large hiatal hernia that was reduced and
repaired in the course of the operation. Symptom scores
for gas and bloat were not increased after fundoplication. This finding is consistent with previously published data, and contradicts the commonly held belief
that discomfort from gas and bloating are solely a consequence of Nissen fundoplication.22
Postoperative satisfaction in this study was high,
though not uniform, often being impacted by a host of
factors unrelated to gastroesophageal reflux, symptom
J Am Coll Surg
control, or the fundoplication. There were no notable
differences in postoperative satisfaction rates among patients with normal preoperative motility and those with
preoperative manometric dysmotility and adequate
esophageal clearance by esophagography. Specifically,
patients with manometric dysmotility and normal
esophageal clearance by esophagography had similar
rates and severities of postoperative dysphagia and relief
of heartburn compared with patients with normal
manometry.
Failures requiring reoperation occurred uniformly
early in our experience. One issue likely involved is
that early in our experience a cruroplasty was not
routinely undertaken if there appeared to be no hiatal
defect. We have also seen an association of failure with
temporally related blunt trauma, such as motor vehicle accidents.
Inability to clear a food bolus at esophagography is
often seen in patients with manometric esophageal dysmotility, especially severe dysmotility. Patients with dysmotility who were unable to clear a food bolus during
esophagography did not undergo laparoscopic Nissen
fundoplication and were not included in this report.
Their reflux continues to be medically treated, and they
are not followed in the registry. In deferring surgical
intervention, it was felt that the risk of causing severe
dysphagia after fundoplication made these patients unacceptable operative candidates. Only very infrequently
do we offer partial fundoplication to select patients with
dysmotility and inadequate esophageal clearance. Our
experience, as such, with antireflux operation for patients unable to clear food boluses at esophagography is
limited. Although the combination of esophageal reflux
and dysmotility can represent an ideal indication for
partial fundoplication, published data suggest less than
optimal results, with considerable rates of recurrent reflux and dysphagia.16,17 It is not certain whether partial
fundoplication is superior to medical management
alone. This study does not delineate the role of antireflux
operation in treatment of patients with dysmotility and
inadequate esophageal clearance at esophagography. A
prospective randomized trial would be warranted to address this issue.
In general, our patients have done well after laparoscopic Nissen fundoplication, even when they have
been undertaken as reoperative procedures.22,23 Possibly this reflects our intent to construct a “floppy”
Nissen fundoplication, which involves division of all
Vol. 201, No. 3, September 2005
D’Alessio et al
short gastric vessels and construction of a short wrap
over a large bougie. Prevalence of new or increased
dysphagia in this study was less than that in other
recent studies, and none of our patients with postoperative dysphagia required surgical or endoscopic intervention, as in other studies.12,21 Notably, in this
study, patients with normal and abnormal esophageal
motility commonly reported preoperative dysphagia.
Laparoscopic Nissen fundoplication brought about
pronounced reductions in dysphagia scores regardless of
the degree of preoperative esophageal dysmotility. New
or more severe dysphagia after fundoplication developed
in ⬍ 10% of patients with dysmotility, whether moderate or severe.
Real-time videoesophagography with bariumladen food boluses of varying consistencies represents
an ideal tool for preoperative evaluation of patients
with manometric dysmotility. It is inexpensive and
readily available. It is not a new study, and thereby,
extension to determining esophageal motility is a
small step.24-27 It does require a working relationship
with an interested radiologist. It must be interpreted
“real-time” with esophageal clearance in mind. The
examination provides a direct visualization of esophageal function, allowing the operator to evaluate the
quality of esophageal peristalsis, and the overall ability of the patient’s esophagus to clear food boluses of
consistencies typically encountered in a usual diet.
Failure to pass any of the various food consistencies
with two or fewer peristaltic waves would constitute a
failure of the test.
This study documents that patients with manometric
esophageal dysmotility who are able to adequately clear a
food bolus at preoperative esophagography have satisfactory outcomes after laparoscopic Nissen fundoplication;
they are not at increased risk for new or exacerbating
existing dysphagia developing after laparoscopic Nissen
fundoplication. Their outcomes are similar to those experienced by patients with normal esophageal motility.
Preoperative videoesophagography with mechanical soft
and solid food boluses can predict successful outcomes
after laparoscopic Nissen fundoplication for patients
with GERD or symptomatic hiatal hernia, or both, and
manometric esophageal dysmotility. This offers hope for
patients with manometric esophageal dysmotility and
increases the number of patients who can undergo laparoscopic Nissen fundoplication with the expectation of
satisfactory outcomes.
Esophagography and Esophageal Dysmotility
341
Author Contributions
Study conception and design: Zervos, Goldin, Poklepovic, Boyce, Rosemurgy
Acquisition of data: Bloomston, Chambers, Poklepovic,
Boyce
Analysis and interpretation of data: D’Alessio, Rakita,
Zervos, Goldin
Drafting of manuscript: D’Alessio
Critical revision: D’Alessio, Rakita, Rosemurgy
Supervision: Rosemurgy
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