Severe Obstetric Brachial Plexus Palsies Can Be Identified at One Month of Age

Abstract

To establish whether severe obstetric brachial plexus palsy (OBPP) can be identified reliably at or before three months of age.
Severe OBPP was defined as neurotmesis or avulsion of spinal nerves C5 and C6 irrespective of additional C7-T1 lesions, assessed during surgery and confirmed by histopathological examination. We first prospectively studied a derivation group of 48 infants with OBPP with a minimal follow-up of two years. Ten dichotomous items concerning active clinical joint movement and needle electromyography of the deltoid, biceps and triceps muscles were gathered at one week, one month and three months of age. Predictors for a severe lesion were identified using a two-step forward logistic regression analysis. The results were validated in two independent cohorts of OBPP infants of 60 and 13 infants.
Prediction of severe OBPP at one month of age was better than at one week and at three months. The presence of elbow extension, elbow flexion and of motor unit potentials in the biceps muscle correctly predicted whether lesions were mild or severe in 93.6% of infants in the derivation group (sensitivity 1.0, specificity 0.88), in 88.3% in the first validation group (sensitivity 0.97, specificity 0.76) and in 84.6% in the second group (sensitivity of 1.0, specificity 0.66).
Infants with OBPP with severe lesions can be identified at one month of age by testing elbow extension, elbow flexion and recording motor unit potentials (MUPs) in the biceps muscle. The decision rule implies that children without active elbow extension at one month should be referred to a specialized center, while children with active elbow extension as well as active flexion should not. When there is active elbow extension, but no active elbow flexion an EMG is needed; absence of MUPs in the biceps muscle is an indication for referral.

Full text

Severe Obstetric Brachial Plexus Palsies Can Be Identified
at One Month of Age
Martijn J. A. Malessy
1
*, Willem Pondaag
1
, Lynda J.-S. Yang
2
, Sonja M. Hofstede-Buitenhuis
1,3
, Saskia le
Cessie
4
, J. Gert van Dijk
5
1Department of Neurosurgery, Leiden University Medical Center, Leiden, the Netherlands, 2Department of Neurosurgery, University of Michigan Hospitals, Ann Arbor,
Michigan, United States of America, 3Department of Neurosurgery Physical Therapy, Leiden University Medical Center, Leiden, the Netherlands, 4Department of
Neurosurgery Medical Statistics, Leiden University Medical Center, Leiden, the Netherlands, 5Department of Neurosurgery Neurology and Clinical Neurophysiology,
Leiden University Medical Center, Leiden, the Netherlands
Abstract
Objective:
To establish whether severe obstetric brachial plexus palsy (OBPP) can be identified reliably at or before three
months of age.
Methods:
Severe OBPP was defined as neurotmesis or avulsion of spinal nerves C5 and C6 irrespective of additional C7-
T1 lesions, assessed during surgery and confirmed by histopathological examination. We first prospectively studied a
derivation group of 48 infants with OBPP with a minimal follow-up of two years. Ten dichotomous items concerning
active clinical joint movement and needle electromyography of the deltoid, biceps and triceps muscles were gathered
at one week, one month and three months of age. Predictors for a severe lesion were identified using a two-step
forward logistic regression analysis. The results were validated in two independent cohorts of OBPP infants of 60 and 13
infants.
Results:
Prediction of severe OBPP at one month of age was better than at one week and at three months. The presence of
elbow extension, elbow flexion and of motor unit potentials in the biceps muscle correctly predicted whether lesions were
mild or severe in 93.6% of infants in the derivation group (sensitivity 1.0, specificity 0.88), in 88.3% in the first validation
group (sensitivity 0.97, specificity 0.76) and in 84.6% in the second group (sensitivity of 1.0, specificity 0.66).
Interpretation:
Infants with OBPP with severe lesions can be identified at one month of age by testing elbow extension,
elbow flexion and recording motor unit potentials (MUPs) in the biceps muscle. The decision rule implies that children
without active elbow extension at one month should be referred to a specialized center, while children with active elbow
extension as well as active flexion should not. When there is active elbow extension, but no active elbow flexion an EMG is
needed; absence of MUPs in the biceps muscle is an indication for referral.
Citation: Malessy MJA, Pondaag W, Yang LJ-S, Hofstede-Buitenhuis SM, le Cessie S, et al. (2011) Severe Obstetric Brachial Plexus Palsies Can Be Identified at One
Month of Age. PLoS ONE 6(10): e26193. doi:10.1371/journal.pone.0026193
Editor: Mel B. Feany, Brigham and Women’s Hospital, Harvard Medical School, United States of America
Received August 9, 2011; Accepted September 22, 2011; Published October 17, 2011
Copyright: ß2011 Malessy et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Martijn J. A. Malessy was supported by ZON-MW (http://www.zonmw.nl), the Netherlands Organization for Health Research and Development. The
funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: malessy@lumc.nl
Introduction
Obstetric brachial plexus palsy (OBPP) almost always involves
traction of the C5 and C6 nerve roots, resulting in weakness of
shoulder function and elbow flexion. Additional involvement of
C7, C8 and T1 roots affects elbow extension and wrist and hand
function [1], [2], [3]. The incidence of OBPP lies between 0.42–
2.9 per 1000 live births [4], [5], [6]. Life-long functional
impairment occurs in 20–30% of cases [7]. Mild lesions cannot
be distinguished reliably from severe lesions in the perinatal
period; only time reveals whether or not spontaneous recovery
will occur. Early identification of severe cases facilitates early
referral to specialized centers, where the need for reconstructive
nerve surgery can be assessed. Identifying cases that require
specialized care is challenging as no test is currently available to
identify these children in the first weeks of life. Therefore, mild
cases may be referred unnecessarily while severe cases may be
referred too late for nerve surgery that is more effective when
performed early [8]. At present, severity (based primarily on
biceps function [9]) is usually assessed at 3 months of age. Lack of
biceps function has been reported as an indication for nerve
surgery [10], [11]. However, biceps paralysis at 3 months does
not preclude a satisfactory spontaneous recovery [12], [13], [14],
and establishing biceps function reliably in infants is difficult [15].
Alternative approaches to assess severity are either complex or
performed at a later age [16], [17], [18]. Consequently,
caretakers are often presented with overly optimistic assessments
or no prediction at all, leading to parental distress [19] and
treatment delays.
We aimed to develop assessment guidelines to help primary and
secondary care physicians identify severe OBPP as early as
possible.
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Methods
This study comprised two stages. Stage 1 was the derivation
stage carried out in the Netherlands and Stage 2 was the validation
stage carried out in the Netherlands and the USA. The medical
ethics committees of the Leiden University Medical Center,
Leiden, the Netherlands and University of Michigan Hospitals,
Ann Arbor, United States of America approved the study.
Derivation
Patients were prospectively recruited between 2002 and 2004 in
the Netherlands. Infants were seen at approximately 1 week, 1
month and 3 months of age, and follow-up occurred every six
months thereafter. Infants referred at 2 months or older were
excluded. Ten dichotomous items concerning joint movement and
needle electromyography were assessed at 1 week, 1 month and 3
months (see below). Follow-up examinations comprised testing of
upper limb muscle strength, joint range of motion and function
[20].
Joint movements
Four active joint movements were examined in the supine
position.
External shoulder rotation. The upper arm was held in
internal rotation and adduction, with the elbow at 90uflexion; the
hand lay on the child’s abdomen. External rotation was present
when the forearm was lifted from the abdomen without active
elbow extension.
Elbow flexion. With the arm extended, flexion was present
when the forearm and hand were lifted while the upper arm
remained static. We did not specify a) whether flexion resulted
from action of the biceps brachii muscle or the wrist extensors, b)
the angle of abduction of the upper arm during flexion and c) the
degree of pronation or supination. Flexion was absent when
infants swung the extended arm upwards to flex the elbow.
Supination. With the elbow passively or actively held in 90u
flexion, active rotation of the distal forearm was considered
supination, regardless of flexion or extension of the wrist. When
forearm rotation was effected by wrist extension and gravity,
supination was considered absent.
Active elbow extension. With the upper arm in 90u
anteflexion, active elbow extension was present if the flexed
forearm could be extended regardless of the end point of the range
of motion.
Shoulder abduction was not considered as a potential parameter
because it remains unclear how this movement is effected in
infants [21].
Needle EMG
Needle EMG was performed on the deltoid, biceps and triceps
muscles; details will be described separately. The presence or
absence of spontaneous muscle fiber activity during rest and of
motor unit potentials (MUPs) was scored as present or absent for
each of the three muscles.
Definition of severity
A severe lesion was defined as neurotmesis or avulsion of spinal
nerves C5 and C6, irrespective of any C7-T1 lesion, assessed
during nerve surgery (described elsewhere in detail [20]). Surgery
was performed at four to five months of age when external
shoulder rotation and active elbow flexion with supination were
absent. If the presence of paralysis was indeterminate, explorative
surgery was performed before six months of age to determine the
severity of the lesion. A mild lesion was defined as the presence of
active elbow flexion and supination at six months of age
spontaneously or upon direct nerve stimulation. Patients with
mild lesions showed a subtotal range of active elbow flexion,
supination and abduction at two years of age.
Validation
Two groups were prospectively studied. One group was seen in
Leiden between 2005 and 2009, and the other at the University of
Michigan (Ann Arbor) between 2007 and 2009. Patients were
included when neurological and EMG examination could be
performed at one month.
Statistical analysis
Derivation. For each of the ten dichotomous items,
sensitivity, specificity, positive predictive value (PPV) and
negative predictive value (NPV) for the distinction between
‘mild’ and ‘severe’ cases were calculated. The optimal predictors
per visit were identified with a two-step forward selection logistic
regression analysis using likelihood-ratio tests with p,0.05 as the
inclusion criterion. The first step comprised the four items of joint
movements, and the second added the six items of the needle
EMG, mimicking the clinical decision process. This analysis
yielded a set of significant predictive items for each visit. For a
severe lesion the estimated probability was .0.5; otherwise, it was
classified as ‘mild’.
Estimated and true outcomes were used to form a 262 table,
and the sensitivity, specificity, PPV and NPV were calculated. The
proportion of correctly predicted outcomes was calculated,
consisting of the sum of correctly predicted severe and correctly
predicted mild lesions. This proportion was compared between the
three visits. The set of predictors from the logistic regression model
that resulted in the highest rate of correctly predicted results was
used to develop a clinical decision rule, applied to all visits. The
additional value of ancillary EMG testing for prediction after
clinical testing was calculated. SPSS (version 16.0, SPSS Inc,
Chicago, USA) was used.
Validation. In the two validation groups, the newly
developed assessment guideline was used to predict mild versus
severe lesions. PPV, NPV, sensitivity, specificity and the
proportion of correct prediction of outcomes were calculated in
both groups.
Results
Derivation
Over an eighteen month period, caretakers of 53 patients were
contacted and 48 gave written informed consent. (Figure 1) The
mean age at visit one was 9 days (median 9, range 12), at visit two
32 days (median 31, range 29) and at visit three 87 days (median
87, range 29). Surgical exploration was performed in twenty-three
infants. The mean age at surgery was 143 days (median 139,
standard deviation (SD) 30 days). In 20 of 23 surgically treated
infants, neurotmesis or avulsion of C5 and C6 was found (severe
lesion, 42%). Six of the 20 infants had a pure C5, C6 lesion, seven
infants had C5, C6, C7 (C8) lesions, and seven had a complete C5-
T1 lesion. The three remaining operated infants and the twenty-
five non-operated infants had an axonotmetic lesion. The mean
follow-up was 735 days (median 704 days, SD 151 days).
Prediction of response
The predictive value of all ten items is shown in Table 1. The
highest prediction rates of the four clinical items at the three visits
were as follows. Active elbow extension at visit 1 had a sensitivity
of 0.70, specificity of 0.96, PPV of 0.92, NPV of 0.81. At the
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second visit, sensitivity was 0.55, specificity 1.0, PPV 1.0, and NPV
0.75. Elbow flexion at visit 3 had a sensitivity of 0.89, specificity
0.88, PPV 0.85, NPV 0.92.
Logistic regression analysis at 1 week of age identified only 1
significant parameter for severity in the first selection step: the
presence or absence of active elbow extension. The second step
added the presence or absence of MUPs in the deltoid muscle.
This model correctly predicted the outcome in 85% (34/40) of
cases (sensitivity 0.70, specificity 0.96).
At one month of age, three items were selected: elbow
extension, elbow flexion and MUPs in the biceps (Figure 2).
These three items individually had correct prediction rates of
80.8%, 80.8% and 89.3%. The logistic model using these items
predicted the outcome correctly in 93.6% (44/47) of infants
(sensitivity 1.0, specificity 0.88, PPV 0.87, NPV 1.0). Clinical
testing of extension and flexion at one month, without performing
an EMG of the biceps muscle, resulted in a prediction rate of
80.8%. (sensitivity 1.0, specificity 0.66, PPV 0.68, NPV 1.0). EMG
increased the percentage of correct predictions by 13%.
At three months of age, the selected variables were elbow
flexion and supination. This model correctly predicted outcome in
88.8% (40/45) of infants (sensitivity 0.94, specificity 0.88).
Since the model of the second visit had the highest prediction
rate, we used this model to derive a simple assessment guideline:
the Leiden three item test (Figure 2).
Validation
325 OBPP infants were routinely referred to the LUMC; the
vast majority was referred later than one month and was excluded.
Sixty patients were included with a mean age at testing of 31 days
(median 30, range 18). Follow-up showed severe lesions in 34
infants (57%). The three item test indicated a severe lesion in 39
infants (65%), with a sensitivity of 0.97, specificity 0.76, PPV 0.84,
NPV 0.95 (Figure 3). The proportion of correctly predicted
outcomes was 88.3% (53/60). Limiting the test to extension and
flexion examination at one month resulted in a correct prediction
rate of 71.6% (sensitivity 1.0, specificity 0.34, PPV 0.66, NPV 1.0).
EMG testing increased correct prediction by 17%.
Forty-five OBPP infants were referred to the University of
Michigan, of which 13 met the inclusion criteria. Mean age at
testing was 31 days (median 33, range 18). A severe lesion was found
in 7 (54%). The three item test indicated severe lesions in 9 (69%).
The test predicted outcome correctly in 84.6% (11/13) with a
sensitivity of 1.0, specificity 0.66, PPV 0.77, NPV 1.0. The
combination of extension and flexion testing at one month resulted
in a correct prediction in 76.9% (sensitivity 1.0, specificity 0.50, PPV
0.70, NPV 1.0). EMG testing increased correct prediction by 8%.
Discussion
We aimed to identify robust parameters to assess the severity of
OBPP in a large prospective series of infants at an early age. An
assessment strategy was developed and validated in two cohorts of
infants. The best predictor of a severe lesion was achieved at one
month of age, based on three items: active elbow extension, active
elbow flexion and needle EMG of the biceps muscle. The rate of
correct predictions was excellent in the derivation group at 94%,
with a sensitivity of 1.0 and specificity of 0.88. In both validation
groups, the correct prediction rate was slightly lower at 88% and
84%. Sensitivity was similarly high, but specificity was slightly lower.
Clinical consequences
We advise that infants with OBPP, who fulfill the criteria for a
severe lesion according to the Leiden three-item test at one month
Figure 1. Flow diagram of tested patients. Over an eighteen month period 53 cases were contacted. The parents of five children chose not to
participate. For the remaining 48 cases written informed consent was obtained. Thirty-seven of the 48 infants were seen three times. Of the
remaining eleven, two were seen twice, at one week and one month, and the third visit was canceled by the parents because of good recovery. Eight
were seen relatively late, so they were only seen at one and three months. One infant was only seen at one week because of good recovery
afterwards. Not attended visits were regarded as missing data. The mean age at visit one was 9 days (median 9, range 12), at visit two 32 days
(median 31, range 29) and at visit three 87 days (median 87, range 29).
doi:10.1371/journal.pone.0026193.g001
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Table 1. The results of the ten test items at visits one (,1 week), two (,1 month) and three (,3 months).
Visit 1 Visit 2 Visit 3
Test result
Severe lesion
(n = 17)
Sensitivity
Mild lesion
(n = 23)
1-Specificity p
%
Corrrectly
predicted
(n = 40)
Severe
lesion
(n = 20)
Sensitivity
Mild lesion
(n = 27)
1-Specificity p
%
Corrrectly
predicted
(n = 47)
Severe
lesion
(n = 19)
Sensitivity
Mild
lesion
(n = 26)
1-Specificity p
%
Corrrectly
predicted
(n = 45)
Absence of
movement
External rotation 17 (100%) 20 (87.0%) 0.122 20 (50%) 20 (100%) 14 (51.9%) 0.000 23 (48.9%) 19 (100%) 13 (50.0%) 0.000 32 (71.1%)
Elbow flexion 17 (100%) 13 (56.5%) 0.002 27 (67.5%) 20 (100%) 9 (33.3%) 0.000 38 (80.8%) 17 (89.5%) 3 (11.5%) 0.000 40 (88.8%)
Supination 17 (100%) 17 (73.9%) 0.022 23 (57.5%) 20 (100%) 13 (48.1%) 0.000 34 (72.3%) 18 (94.7%) 6 (23.1%) 0.000 38 (84.4%)
Elbow extension 12 (70.6%) 1 (4.3%) 0.000 34 (85%) 11 (55.0%) 0 (0%) 0.000 38 (80.8%) 7 (36.8%) 0 (0%) 0.001 33 (73.3%)
Presence of
spontaneous
EMG activity
Deltoid 13 (76.5%) 9 (39.1%) 0.019 13 (32.5%) 17 (85.0%) 14 (51.9%) 0.018 17 (36.1%) 5 (26.3%) 1/25 (4.0%) 0.033 15/44 (34.0%)
Biceps 9 (52.9%) 8 (34.8%) 0.251 16 (40%) 18 (90.0%) 8 (29.6%) 0.000 10 (21.2%) 7 (36.8%) 3/25 (12.0%) 0.051 15/44 (34.0%)
Triceps 11 (64.7%) 4 (17.4%) 0.002 10 (25%) 15 (75.0%) 5 (18.5%) 0.000 10 (21.2%) 4 (21.1%) 2/25 (8.0%) 0.211 17/44 (38.6%)
Absence
of MUPs
Deltoid 15 (88.2%) 9 (39.1%) 0.002 29 (72.5%) 20 (100%) 9 (33.3%) 0.000 38 (80.8%) 5 (26.3%) 1/25 (4.0%) 0.033 29/44 (65.9%)
Biceps 15 (88.2%) 7 (30.4%) 0.000 31 (77.5%) 20 (100%) 5 (18.5%) 0.000 42 (89.3%) 1 (5.3%) 0/25 (0%) 0.246 26/44 (59.0%)
Triceps 10 (58.8%) 1 (4.3%) 0.000 32 (80%) 10 (50.0%) 0 (0%) 0.000 37 (78.7%) 1 (5.3%) 1/25 (4.0%) 0.842 25/44 (56.8%)
For each of the ten dichotomous items concerning joint movements and needle electromyography, the sensitivity, 1- specificity and percentage of correct prediction of a ‘mild’ or ‘severe’ lesion is indicated. Electromyography
(EMG): the presence of spontaneous muscle activity (fibrillation and/or positive sharp waves) and the absence of motor unit action potentials (MUPs). p values denote results from Pearson’s Chi-Square test.
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of age, should be referred to a specialized center (see figure 2). This
strategy has advantages: (1) minimization of delays that contribute
to the deleterious effects of prolonged denervation; (2) caretakers
can be informed promptly regarding prognosis and treatment; (3)
the first 2 items of the three item test guides primary-care
physicians when to request needle EMG of the biceps muscle.
The three item test was slightly pessimistic, as a small number of
patients with an abnormal test showed late spontaneous recovery.
We would contend that this error is more desirable than the
opposite one in which infants with severe lesions are recognized
too late. Monitoring of the progress and speed of recovery in the
2nd and 3rd months is strongly advised. When spontaneous
recovery does not occur in this time frame, the detailed
information of the three item test acquired at one month provides
adequate rationale to perform CT-myelography to detect root
avulsions [22].
Figure 2. Flow diagram of OBPP assessment at one month of age using the Leiden three item test. Prediction at one month of age was
better than at one week and three months. The decision rule implies that children without active elbow extension at one month should be referred,
while children with active elbow extension as well as flexion should not. When there is elbow extension, but no active elbow flexion an EMG is
needed; absence of MUPs in the biceps muscle is a reason for referral.
doi:10.1371/journal.pone.0026193.g002
Figure 3. Flow diagram of LUMC validation group (n = 60). Follow-up data resulted in a severe lesion in 34 infants (57%). The three item test
indicated a severe lesion in 39 infants (65%). The test predicted outcome correctly in 88% (53/60) of infants (sensitivity 0.97, specificity 0.76, PPV 0.84,
NPV 0.95. The dash style of the arrows indicates related patient flows.
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Active elbow extension emerged as a significant predictor of a
C5 and C6 lesion. Although the triceps muscle is largely
innervated through C7 and C8 roots, a possible reason for this
apparent oddity is that the C5 and C6 roots are virtually always
affected in OBPP, while the more caudal C7, C8 and T1 roots are
only affected in more extensive lesions [3]. Paralysis of elbow
extension likely acts as a proxy for severe lesions of C5 and C6
roots.
Application of the test
In routine practice, examiners generally test both active elbow
flexion and extension. When active elbow flexion and extension
are clearly present, no EMG is necessary, but reticence to perform
an EMG should not be a barrier. In our practice, the procedure of
EMG, if explained properly, is borne well by infants as well as
parents.
Unexpectedly, the predictive value of the three-item test was
better at one month than at three months of age. The slow
development of spontaneous functional recovery suggests that
recovery becomes clearer the later a child is examined. The
superiority of prediction at one month rests on the contribution of
the EMG at one month, but not at three months. An apparent
paralysis of the biceps at three months of age is almost always
accompanied by the paradoxical presence of MUPs in that muscle
[23]. In OBPP, the C5 and C6 spinal nerves are rarely completely
ruptured. Instead a ‘‘neuroma in continuity’’ is present. A small
percentage of severed axons may advance past this neuroma,
reflected by the appearance of MUPs at three months. Reasons for
the lack of a clinical counterpart have been discussed [23]. The
presence of MUPs at one month of age likely suggests that these
axons were previously dysfunctional due to neurapraxia but not
axonotmesis, thereby carrying a better prognosis.
Limitations
We actively recruited cases for the derivation study that
probably affected the proportions of mild and severe cases, but
this does not affect the validity of the Leiden three item test.
Assessment of severity was not rigidly blinded, but severity was
assessed at around 150 days of age when earlier data were not
reviewed. Combined with the applied way of assessment, we do
not feel that this factor significantly influenced the results.
Selection of severe cases involved selection of those for nerve
surgery and assessment of surgical findings. Follow-up in the
derivation group did not show any severe cases among infants who
had not undergone surgery, so the two-step procedure did not
introduce errors.
Finally, there is no widely accepted definition for the severity of
OBPP [24]. We feel that the definitions used here do justice to the
purpose of our study.
Conclusion
The severity of OBPP can be reliably predicted at one month of
age in the majority of infants with OBPP by testing active elbow
extension, active elbow flexion and recording MUPs in the biceps
muscle. The Leiden three item test can be implemented in routine
clinical practice to identify those infants with OBPP who require
prompt referral to specialized centers.
Acknowledgments
The authors thank the parents of the infants with OBPP for their
committed participation.
Author Contributions
Conceived and designed the experiments: MJAM JGD. Performed the
experiments: MJAM LJSY SMH-B JGD. Analyzed the data: MJAM SC
JGD. Contributed reagents/materials/analysis tools: SC JGD. Wrote the
paper: MJAM WP LJSY JGD.
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PLoS ONE | www.plosone.org 6 October 2011 | Volume 6 | Issue 10 | e26193