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7/28/2019 j.1553-2712.2010.00703.x
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A Descriptive Comparison of Ultrasound-guided Central Venous Cannulation of theInternal Jugular Vein to Landmark-based
Subclavian Vein CannulationDaniel Theodoro, MD, Brian Bausano, MD, Lawrence Lewis, MD, Bradley Evanoff, MD, MPH, andMarin Kollef, MD
Abstract
Objectives: The safest site for central venous cannulation (CVC) remains debated. Many emergency phy-
sicians (EPs) advocate the ultrasound-guided internal jugular (USIJ) approach because of data support-
ing its efficiency. However, a number of physicians prefer, and are most comfortable with, the
subclavian (SC) vein approach. The purpose of this study was to describe adverse event rates among
operators using the USIJ approach, and the landmark SC vein approach without US.
Methods: This was a prospective observational trial of patients undergoing CVC of the SC or internaljugular veins in the emergency department (ED). Physicians performing the procedures did not undergo
standardized training in either technique. The primary outcome was a composite of adverse events
defined as hematoma, arterial cannulation, pneumothorax, and failure to cannulate. Physicians recorded
the anatomical site of cannulation, US assistance, indications, and acute complications. Variables of
interest were collected from the pharmacy and ED record. Physician experience was based on a self-
reported survey. The authors followed outcomes of central line insertion until device removal or patient
discharge.
Results: Physicians attempted 236 USIJ and 132 SC cannulations on 333 patients. The overall adverse
event rate was 22% with failure to cannulate being the most common. Adverse events occurred in 19%
of USIJ attempts, compared to 29% of nonUS-guided SC attempts. Among highly experienced opera-
tors, CVCs placed at the SC site resulted in more adverse events than those performed using USIJ (rela-
tive risk [RR] = 1.89, 95% confidence interval [CI] = 1.05 to 3.39).
Conclusions: While limited by observational design, our results suggest that the USIJ technique may
result in fewer adverse events compared to the landmark SC approach.
ACADEMIC EMERGENCY MEDICINE 2010; 17:416422 2010 by the Society for Academic Emergency
Medicine
Keywords: catheterization, central venous; ultrasonography, interventional; emergency medicine
Physicians in the United States insert over 5 million
central venous catheters (CVC) annually.1,2 In
studies that examine acute mechanical complica-
tions, no anatomical site proves more advantageous than
the other.3,4 Two emergency department (ED) random-
ized clinical trials demonstrate that ultrasound (US) guid-
ance decreases the mean number of needle sticks
required to successfully cannulate the internal jugular
vein and modestly reduces adverse events.5,6 However,
these studies involved groups of physicians with an
interest or special expertise in US-guided procedures.
Moreover, hospital surveys indicate that physicians may
favor the subclavian (SC) approach over other sites.7,8
Therefore, in this study, we sought to compare adverse
events among patients who underwent US-guided
ISSN 1069-6563 2010 by the Society for Academic Emergency Medicine
416 PII ISSN 1069-6563583 doi: 10.1111/j.1553-2712.2010.00703.x
From the Division of Emergency Medicine (DT, BB, LL), the
Division of General Medical Sciences (BE), and the Medical
Intensive Care Unit (MK), Washington University School of
Medicine, St. Louis, MO.
Received August 20, 2009; revision received October 15, 2009;
accepted October 19, 2009.
Presented at the Society for Academic Emergency Medicine
Annual Meeting in Washington, DC, May 2008.
This study was supported by the Washington University School
of Medicine CTSA Grant (UL1 RR024992) and the Washington
University School of Medicines Clinical Research Training Cen-
ter (KL2 RR024994).
Address for correspondence and reprints: Daniel Theodoro,
MD; e-mail: [email protected].
7/28/2019 j.1553-2712.2010.00703.x
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cannulation of the internal jugular vein (USIJ) to that in
patients undergoing the nonUS-guided SC approach in
a setting where physicians without focused training in
either technique performed the procedure.
METHODS
Study Design
We assembled a prospective cohort of adult patients
who underwent CVC in the ED. The institutional human
research protection office approved the study and
waived informed consent.
Study Setting and Population
We conducted the study in an academic, urban, 63-bed
ED with a volume of 79,000 visits per year. The emer-
gency medicine training program includes 48 residents
total (12 per year). During the year the study took place,
42 full-time emergency physicians (EPs) staffed the ED.
We collected a convenience sample of consecutive
CVC attempts in our ED. The study was conducted
from March 20, 2007, to March 17, 2008. We includedany patient who underwent cannulation of either the
internal jugular or SC vein, as determined by the treat-
ing EP caring for the patient. We excluded patients
with a concurrent indwelling CVC, suspected traumatic
injury of the vessels in the neck or thorax, or overlying
dermatologic process that precluded insertion at either
site and those who underwent CVC at another anatomi-
cal site.
Study Protocol
To capture consecutive central line attempts, we cre-
ated a standardized electronic procedure note for the
EDs electronic medical record system. Physiciansworking in the ED noted the indication for the proce-
dure, the anatomical site of the procedure, if US guid-
ance was employed, and any adverse event that may
have occurred during the procedure. Any patient who
required central venous access due to lack of peripheral
access was defined as poor access. Any patient who
required central venous access for resuscitation or he-
modynamic monitoring (as in cases of presumed sepsis)
was defined as septichypovolemic or hypotensive. If
the central line was inserted while the patient was in
cardiopulmonary arrest (from either traumatic or medi-
cal reasons) the indication for cannulation was consid-
ered as code line. USIJ was defined as the real-time
use of an US probe to direct the locator needle toward
the internal jugular vein. We excluded central lines
placed via the static approach (using the US probe to
site the vein but not actively cannulate it). SC vein cann-
ulation was defined as any infraclavicular attempt to
cannulate the SC vein, without US guidance to locate
the vessel or direct the needle. We specifically defined
an attempt as a single operators performance of the
procedure from beginning to completion at one ana-
tomic site. If a second operator attempted the proce-
dure at the same site, this was considered a new
attempt. Because the purpose of our study was to
examine adverse events and not efficiency outcomes,
we did not include the number of needle sticks ortime required for either procedure in this analysis. To
improve the precision of our data collection instrument,
we made two semiannual presentations regarding our
definitions of each variable. We did not modify the data
collection instrument during the study.
Demographic characteristics and vital signs were col-
lected from the patients ED charts. Body mass index
(BMI) was calculated according the patients self-
reported height and weight at the time of admission tothe hospital and categorized according to World Health
Organization BMI classifications. If no weight was
recorded, the weight in the ED chart recorded by the
ED nurse caring for the patient was noted. The height
at the nearest prior admission or from the patients
identification card copied into the chart was recorded if
no other record existed. The International Normalized
Ratio (INR) was obtained from the ED chart. Any
patient with systolic blood pressure (sBP) of
90 mm Hg at any time during the ED stay was consid-
ered hypotensive. Patients who required pressors
were identified by review of pharmacy records to deter-
mine whether the patient received vasopressors (epi-
nephrine, norepinephrine, or dopamine) or inotropes(dobutamine) at any time during the ED stay. We
defined mortality as those patients who did not sur-
vive the ED to hospital admission and those who
expired during their hospitalization.
All of the operators participating in the study were
physicians. The operators underwent training for each
technique under the apprenticeship model, meaning
they gained central line experience while simulta-
neously clinically caring for patients. There were two
additional lectures provided for US-guided techniques,
but there were no separate simulation or hands-on
sessions offered. All EPs were asked to fill out a survey
indicating their overall experience with CVC. The sur-vey asked the physicians how many central lines, irre-
spective of site or technique, they had placed in
increments of 10 to a maximum of 50 or above. We
identified no prior validated definition of experienced
operator, and all operators indicated they had placed
more than 20 central lines throughout their career, a
threshold used in prior studies.5 We defined experi-
enced operator as one who had performed more than
50 cannulations (not site specific) throughout their
career since our survey results indicated that a majority
of the operators had attained this level of experience.
Level of experience was missing for 16 attempts (5%).
All were from physicians with four or more years oftraining.
Measurements
Our primary outcome of interest was a composite of
acute adverse events. Borrowing from prior definitions,
we considered an adverse event to occur when a cann-
ulation attempt resulted in an accepted complication of,
or failure in, its technical performance.912 We there-
fore defined an acute adverse event as a composite of
the following outcomes: arterial puncture, pneumotho-
rax, hematoma, extravascular or misplacement, and
failed attempt at cannulation. An arterial puncture was
judged to have occurred when physicians aspirated pul-
satile arterial (bright red) blood into an 18-gauge loca-tor syringe. The presence of a pneumothorax was
ACAD EMERG MED April 2010, Vol. 17, No. 4 www.aemj.org 417
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determined using plain films of the chest (either stan-
dard posteroanterior or portable anteroposterior) as
read by a radiologist blinded to the technique used for
central line cannulation. Any ipsilateral pneumothorax
identified within 24 hours of line placement was consid-
ered a complication of the procedure unless the patient
underwent another procedure that could also cause a
pneumothorax on the side in question. Physicians ornurses documented a hematoma if an area of bruising
or swelling greater than 3 cm was noted around the
insertion site. Placement of the central line outside of
the vascular lumen was defined by failure to aspirate
blood through any of the ports or a visible extravasa-
tion of intravenous fluid in the soft tissues (a blown
line appearance). A failed attempt at cannulation was
specifically defined as the inability to complete the
intended procedure by the primary operator for lack of
successfully cannulating the intended vessel. Any pur-
ported puncture of the vein that resulted in the inability
to pass a guide wire, and therefore complete the proce-
dure, was considered a failed attempt. We did not
attempt to determine the number of needle passes forthis analysis.
In the event that more than one adverse outcome
occurred, we recorded the complication that required a
therapeutic intervention as the primary adverse out-
come. We considered pneumothorax, failed cannula-
tion, and misplacement as primary adverse events if
they occurred simultaneously with arterial puncture
and hematoma. However, any occurrence of any com-
plication was considered an adverse event.
We followed subjects until there was radiologic or
medical record evidence that the ED central line was
removed or replaced, or to hospital discharge, to exam-
ine whether seemingly insignificant acute complicationsresulted in any therapeutic intervention or delayed
complications. A chart reviewer (SP and MP), blinded
to the site and technique of insertion, reviewed daily
nursing notes for the mention of hematoma or
transfusion. Patient discharge summaries were exam-
ined for evidence of a central line related adverse event.
Any mention of central line complication or cannu-
lation device complication triggered an audit of inpa-
tient nursing and operative records. Operative records
were reviewed for any mention of a vascular procedure
related to central line complications. In addition we
reviewed the annual records of our quality improve-
ment process for any cases referred to the committeethat involved an ED central line. For the purposes of
this study, catheter-related infections or thrombotic
events were not recorded.
Data Analysis
Results were inserted into an SAS (Version 9.2, SAS
Institute, Cary, NC) database. We performed bivariate
analysis for variables of interest using chi-square tests
and report the 95% confidence intervals (CI). Power cal-
culations were performed using an assumption of a
15% acute complication rate using the external land-
mark technique and a 5% acute complication rate using
the US-guided technique. Using these figures and
accounting for dropouts, we determined that it wouldrequire 128 patients in each group to have a power of
0.80 to detect this difference at the 0.05 level of signifi-
cance.
RESULTS
Physicians reported a total of 729 CVC attempts during
a 1-year period from March 20, 2007, to March 17, 2008
(Figure 1). Almost one-third (32.8%) were inserted into
the femoral vein. We excluded those central lines
inserted into the internal jugular vein without the use
of US, and those inserted into the SC vein under US
guidance, as well as all central lines inserted by physi-
cians who did not meet our minimum requirement of
20 central lines during their career (16.2%). Our final
sample consisted of 333 patients who underwent cann-
ulation by 63 physicians. Physicians indicated that 254
(69%) central lines were inserted for shock, 97 (26%)
were inserted for lack of peripheral access, and 17 (5%)
were inserted for cardiopulmonary resuscitation
(Advanced Cardiac Life Support or Advanced Trauma
Life Support protocols). A total of 32 physicians (51%)
contributed one attempt to each group, and 17 physi-cians (27%) contributed two or more attempts to each
group. Physicians indicating that they had placed more
than 50 central lines throughout their career made 275
attempts (76%). Physicians in their first, second, and
third years of training contributed 35 attempts (10%),
61 attempts (17%), and 104 attempts (28%), respectively.
Attending physicians and those in their fourth year of
training contributed 168 attempts (46%).
Overall there were 82 adverse events (22%, 95%
CI = 18.2% to 30.0%). Of the 236 central lines inserted
using the USIJ technique, 44 (19%) resulted in an
Central Line Attemptsn = 729
Chest or Neck Attemptsn = 490
Non Ultrasound GuidedInternal Jugular Attempts
n = 20
Ultrasound GuidedSubclavation Attempts
n = 1
Ultrasound Guided Internal JugularAttemptsn = 236
Performed byInexperienced Operator
n = 98
n = 470
n = 456
Femoral Siten = 239
Landmark Based Subclavation Attemptsn = 132
Figure 1. Study flow.
418 Theodoro et al. US-GUIDED CVC
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adverse event. Of the 132 attempts made at the SC, 38
(29%) resulted in an adverse event (Table 1). There was
no statistically significant difference between USIJ and
SC attempts among any clinical or demographic char-
acteristics, except age and mortality. Physicians who
met our definition of experienced operator used the
SC more often than the USIJ technique.
The most common adverse event across both sites
was failed attempt at cannulation. In total, 53 attempts
at initial cannulation failed. In the SC group, 30 (23%)
cannulation failures and two (2%) pneumothoraces
occurred. Both pneumothoraces required thoracosto-my. SC attempts resulted in two (2%) hematomas and
three (2%) arterial punctures, and one (1%) catheter
was misplaced in the soft tissues. The misplaced cathe-
ter resulted in no therapeutic intervention after
removal. The USIJ technique failed to result in cannula-
tion in 23 (10%) attempts and zero pneumothoraces
occurred. There were 17 (7%) hematomas noted, four
(2%) inadvertent arterial punctures, and zero misplace-
ments.
We found no instance where a delayed complication
occurred or where a seemingly insignificant complica-
tion in the ED required direct therapeutic intervention
upon follow-up in either group. One USIJ resulted in a
delayed hematoma 48 hours after the time of admis-
sion. The patient was on heparin therapy and did not
undergo any further therapeutic intervention, nor was
heparin therapy discontinued. The quality improvement
team reported no additional adverse events.
In general, more adverse events were noted amongthose patients undergoing attempted cannulation of the
SC compared to those undergoing USIJ cannulation,
regardless of operator experience. The adverse event
rate decreased with operator experience regardless of
approach used (Figure 2). Cannulations performed by
experienced operators were more likely to result in an
adverse event at the SC site than those performed
Table 1Baseline Characteristics of 368 Central Line Attempts
US-guided InternalJugular Approach
(n = 236), n (%)
Landmark SCApproach
(n = 132), n (%) % D 95% CI
Age 65 years 109 (46.1) 47 (35.6) 10.6 0.6 to 20.5Male sex 107 (45.3) 73 (55.3) 10.0 20.0 to 0.6African American 139 (58.9) 81 (61.3) 2.4 8.4 to 13.0COPDasthma 35 (14.8) 20 (15.1) 7.9 17.1 to 0.6Hypotensive in the ED 155 (65.6) 97 (73.4) 7.8 17.4 to 2.5Requiring pressor* 87 (36.8) 57 (43.1) 6.3 17.1 to 4.4BMI > 30 76 (32.2) 32 (24.2) 7.9 2.2 to 17.3INR > 2.0 41 (17.4) 15 (11.4) 6.0 2.3 to 13.3ACLSATLS 8 (3.4) 9 (6.8) 3.4 9.8 to 1.4Mortality 40 (16.9) 37 (28.0) 11.0 20.8 to 1.9Inserted by operator
with >50 CVCs in career162 (72.0) 113 (89.0) 17.0 25.8 to 7.9
Adverse event 44 (18.6) 38 (28.8) 10.2 19.5 to 1.2
ACLS = advanced cardiac life support; ATLS = advanced trauma life support; BMI = body mass index; COPD = chronic obstruc-tive pulmonary disease; CVC = central venous cannulation; INR = international normalized ratio;*Vasopressorinotrope administered.
Figure 2. The effect of experience as defined by 50 or more
cannulations (the absolute numbers of adverse events and
attempts are provided in the columns). USIJ = ultrasound-
guided internal jugular approach; SC = subclavian approach.
Figure 3. The effect of experience as defined by postgraduate
year level (the absolute numbers of adverse events and
attempts are provided in the columns). USIJ = ultrasound-
guided internal jugular approach; SC = subclavian approach.
ACAD EMERG MED April 2010, Vol. 17, No. 4 www.aemj.org 419
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using USIJ (relative risk [RR] = 1.89, 95% CI = 1.05 to
3.39), but there was no difference among novice opera-
tors in adverse events when using the SC technique
(RR = 2.2, 95% CI = 0.66 to 7.3). There was no signifi-
cant difference in adverse events by postgraduate year
(v2 = 1.53, p = 0.68; Figure 3).
DISCUSSION
Although our study was observational by design and
therefore limited, our findings suggest that physicians
who adopt US guidance when cannulating the internal
jugular in an apprenticeship model are less likely to
encounter an adverse event compared to the landmark
SC technique. Past studies that compared vascular
access sites to one another did not account for the
impact of US guidance. In these studies, adverse events
occurred with nearly equal proportion in both groups,
and no anatomic location was conclusively superior in
regard to acute mechanical complications.2,4,1320 While
a randomized clinical trial would be required to recom-
mend a change in practice, our observational studysuggests a benefit to using US-guided cannulation.
Our study also found that adverse events occurred
less frequently with the USIJ technique compared to
the SC technique among experienced operators. Past
studies suggest that US guidance conveys its greatest
benefit on operators with less experience, while more
experienced operators may realize less improvement in
their cannulation outcomes.21 Our findings suggest that
the US-guided technique confers benefit to experienced
operators in the absence of rigorous standardized train-
ing in either technique. Measuring expert operator per-
formance by strict counts may have limitations.
However, accreditation boards and prior research inthe area have focused on the number of procedures
performed to assess technical competence.5,2224 Our
study also relied on the number of performed proce-
dures, but it was self-reported and not site-specific.
Among our most experienced operators (those who
performed >50 CVC in their careers), USIJ resulted in
fewer adverse events, specifically fewer cannulation
failures. Although we caution the interpretation of an
individual component of our composite, our study sug-
gests that even operators with significant experience
can gain benefit from US-guided procedures. Overall
experience with cannulation may facilitate the acquisi-
tion of skills that pertain to US-assisted procedures.
With the exception of two pneumothoraces that
required chest tubes, none of our 333 patients sustained
an adverse event that required clinical interventions.
These findings echo past studies suggesting that the
majority of acute adverse events resulting from
attempted CVC in the ED are typically no harm
events. While this observation ignores the impact that
failed access may have on resource consumption and
timeliness of therapeutic interventions, it underscores
the modest extent to which CVC leads to adverse
events requiring intervention.
In prior studies comparing US-guided attempts to
non-US-guided attempts at a single site, the decrease in
adverse events that required a direct intervention wasmodest as well. In the study by Milling et al.,6 no
attempts resulted in a pneumothorax, and in the study
by Leung et al.,5 1 of 65 attempts resulted in a pneumo-
thorax in the non-US group. Both studies demonstrated
fewer hematomas and arterial punctures, but did not
report any therapeutic consequences.5,6
Hematomas were more common in our USIJ group
than in previous studies. This may be due to the fact
that our physicians were not selected for demonstratedexpertise in USIJ and may better reflect the true inci-
dence of this complication in a real-world experience.
Hematomas were reported significantly less often in the
SC group than in the USIJ group. This could be attrib-
uted to the difficulty in identifying hematomas in the
subclavicular location. The effect of this would be to
bias the study toward the SC approach. However, no
hematoma in either group resulted in a clinical inter-
vention in our cohort. Whether resource utilization,
timeliness of therapy, and a decrease in thoracostomies
becomes sufficiently significant across larger popula-
tions to justify solely using US-assisted techniques
remains a question for further investigation in larger
trials.Our cohort sustained a high failure rate utilizing US
compared to prior studies in similar settings.5,6,21,25 We
attributed this to a lack of hands-on training or simula-
tor-based learning opportunities. In prior ED studies,
US-guided cannulations (intervention arms) were per-
formed by small groups of physicians with targeted
training suggesting possible operator bias frequently
noted in US research. The study by Milling et al.6
involved nine physicians, and the study by Leung et al.5
involved 13 physicians, compared to the 63 physicians
involved in our cohort. The 63 physicians in our cohort
did not undergo intense targeted training in the use of
US assistance, but adopted the procedure in the classicapprenticeship model. Despite the lack of focused train-
ing, the intervention of US assistance resulted in some
benefit. Whether the impressive decrease in US-guided
central line complications noted in other studies is a
factor of directed educational sessions or a trend only
among physicians with highly specialized training in US
remains unexplored.
The adoption of the US-guided technique came at the
expense of performing fewer nonUS-guided central
lines. This may be partly explained by the suggestion
from prior studies that physicians in training may bene-
fit the most from US guidance.21,26 This may represent
a concerning practice shift, since failed US-guidedattempts may require rescue by nonUS-guided tech-
niques. Given that a majority of community EDs have
limited access to US technology, training programs
should be wary of overemphasizing US-guided tech-
niques so as to not impede the development of non
US-guided techniques among their graduates.27
Our SC adverse event rate was higher than in studies
conducted by experienced operators, yet lower than in
some studies of inexperienced operators, a fact likely
explained by the nature of emergent central lines and
the acutely ill ED patient population.16,26,28,29 The
mortality rate of patients undergoing the SC technique
was higher than those undergoing USIJ. Our data sug-
gested that this was due to physician preference forlandmark-based approaches during code situations.
420 Theodoro et al. US-GUIDED CVC
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The poor prognosis of these patients likely explains the
baseline difference in mortality rates between the two
central line approaches. Whether US guidance can
assist placement of SC vein catheters in the ED requires
further investigation.
LIMITATIONS
Due to the observational design, central line attempts
were not randomly assigned, increasing the likelihood
that selection bias was introduced. We hypothesized
that physicians would preferentially use the technique
with which they were most comfortable, possibly bias-
ing our results toward the null. Despite this, we still
found a difference in adverse events, even among those
considered experienced with CVC. Although we
accounted for patient factors that might make venous
cannulation difficult (e.g., BMI), it is possible that sev-
eral unrecorded patient variables could result in a
selection bias toward one technique or the other.
We relied on the apprenticeship model to teach
both techniques. It is possible that an institutional trenddeveloped whereby USIJ became the preferred method.
This may have biased the results in favor of USIJ in that
less time was devoted to acquiring skills of non-US
techniques. However, a survey during the study indi-
cated that 80% of all physicians were initially taught
solely nonUS-guided techniques, and 68% did not use
US in almost half their central line attempts.30 However,
as the study proceeded, more physicians opted for US
guidance than the landmark technique.
As in prior studies, our measure of physician experi-
ence was based on survey data. The results of our sur-
vey are subject to recall bias. Furthermore, we asked
physicians to indicate their general experience withCVC, not their experience with each procedure and not
their experience with US. This may bias operator expe-
rience results because physicians may have reported
experience solely with one technique and at one site,
not both. In this case, adverse events may be explained
more by experience than technique. Although we
restricted our analysis to exclude beginner-level
physicians, we were not able to confirm the level of
experience of operators for each technique. However,
current studies and accreditation standards currently
do not define experience other than by the total
number of cannulations performed during training or
career.
It is likely that physician and nurse self-report led to
measurement bias. Other than pneumothorax, unsuc-
cessful cannulation, and misplacement, the outcomes
studied do not have gold standards and rely on report-
ing by the physician or the nurse. In addition, some
adverse events may be more obvious in certain ana-
tomic areas. Furthermore, our results would be greatly
biased if physicians reported their successes less com-
monly with their preferred technique while they
reported their failures more commonly with their least
preferred technique or vice versa. However, the rates
of our adverse events were similar to those found in
other studies, and our quality assurance committee
found no instance of an unreported adverse event thattook place in the ED during this study.
CONCLUSIONS
Our observational trial suggests that physicians without
rigorous standardized training can adopt the ultra-
sound-guided internal jugular technique and decrease
the number of acute adverse events, compared to using
the landmark subclavian approach. However, our study
was limited by its design, and a randomized control
trial would be necessary to recommend a change inpractice. Very few adverse events from central venous
cannulation attempts require direct clinical intervention.
Whether the benefit of ultrasound guidance translates
to other outcomes, such as timeliness of therapy,
resource utilization, or thrombotic or infectious compli-
cations, remains unstudied and will likely require large
coordinated efforts to gain statistical power. Physicians
who solely perform the landmark subclavian approach
may expose their patients to a modestly increased risk
of an acute adverse event, mainly the risk of failing to
complete the intended procedure.
The authors acknowledge Sarah Boslaugh, PhD, and Missy Krauss,MPH, for their statistical advice for this work. We also acknowl-
edge Max Palatnik, Connor Deal, and Shruti Patil for their contri-
butions to this project.
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