Professional Documents
Culture Documents
3:000–000, 2009
James R. Bain, M.D., M.Sc., F.R.C.S.C.,1,2 Carol DeMatteo, M.Sc., Dip. P.&O.T.,2–4
Deborah Gjertsen, B.H.Sc. O.T., 2 and Robert D. Hollenberg, M.D., F.R.C.S.C.2,5
Divisions of 1Plastic Surgery and 5Neurosurgery, Department of Surgery, 3School of Rehabilitation Science,
and 4CanChild Centre for Childhood Disability Research, McMaster University; and 2McMaster Children’s
Hospital, Hamilton, Ontario, Canada
Object. In the literature, the best recommendations are imprecise as to the timing and selection of infants with
obstetrical brachial plexus injury (OBPI) for surgical intervention. There is a gray zone (GZ) in which the decision as
to the benefits and risks of surgery versus no surgery is not clear. The authors propose to describe this category, and
they have developed a guideline to assist surgical decision-making within this GZ.
Methods. The authors first performed a critical review of the medical literature to determine the existence of a
GZ in other clinical publications. In those reports, 47–89% of infants with OBPI fell within such a GZ. Complete
recovery in those reported patients ranged from 9 to 59%. Using a prospective inception cohort design, all infants
referred to the OBPI Clinic at McMaster Children’s Hospital were systematically evaluated up to 3 years of age. The
Active Movement Scale scores were compared for surgical and nonsurgical groups of infants in the GZ to identify
any important trends that would guide surgical decision-making.
Results. In the authors’ population of infants with OBPI, 81% fell within the GZ, of whom 44% achieved com-
plete recovery. Mean scores differed significantly between surgery and no surgery groups in terms of total Active
Movement Scale score and shoulder abduction and flexion at 6 months. Elbow flexion and external rotation differed
at 3 months.
Conclusions. There is compelling evidence that there is a group of infants with OBPI in whom the assessment
of the risk/benefit ratio for surgical versus nonsurgical treatment is not evident. These infants reside within what the
authors have called the GZ. Based on their results, a guideline was derived to assist clinicians working with infants
with OBPI to navigate the GZ. (DOI: 10.3171/2008.12.PEDS0885)
T
he peripheral nerve surgeon dealing with an infant surgical or medical care given to these infants, large ret-
with an OBPI is always faced with the diagnos- rospective data sets,5,6,8,12,13 a few prospective studies,20,21
tic dilemma as to whether the injury includes sig- and systematic reviews of the literature15,19 provide very
nificant components of axonotmesis and/or neurotmesis useful guidelines. There are some clear areas of consen-
(which require timely surgical attention to maximize the sus in this body of literature. Infants in Narakas17 Group
possibility of regeneration) versus neurapraxis where IV outlined in Table 1 (total plexus injury plus Horner
one expects to see spontaneous full functional recovery. syndrome) who show no signs of recovery definitely will
Obviously the surgeon wants to avoid surgery on the require reconstructive microsurgery to repair their dam-
neurapraxic injuries and operate as soon as possible on aged plexus and improve their outcome.7,12,15,19,21 Similar-
the limb destined for hypoplasia, poor motor/sensory re- ly, consensus reigns that infants with a mild neurapraxic
covery, and eventual functional disability. injury who demonstrate full recovery by 1 month are best
Although there is no Level I evidence for any of the treated conservatively.
We have prospectively studied our patient population
Abbreviations used in this paper: AMS = Active Movement to identify clinical criteria that would enable us to devel-
Scale; GZ = gray zone; OBPI = obstetrical brachial plexus injury. op a valid guideline for these treatment decisions. This
Methods
full range 4
against gravity score
There are 2 parts to this research study: a critical re- motion ≤0.5 range 5
view of the literature and a prospective cohort of children motion >0.5 range 6
with OBPI.
full range 7
Critical Review of Literature
* Modified from Table 1 in Curtis et al., 2002, Copyright American So
A standardized search strategy and critical review ciety for Surgery of the Hand.
of the medical literature was undertaken to determine
the existence of a GZ in other clinical publications. Ar-
ticles were included in the review if the authors clearly and then at 3-month intervals or as needed by a multidis-
described the scenario for a GZ (albeit not in those words) ciplinary team including an occupational therapist and a
and provided data that allowed an actual calculation of peripheral nerve surgeon. There are ~ 4 new referrals per
the numbers of children within the GZ. Variable follow- month with 95% of infants < 2 months of age at referral.
up times and measures were accepted. Recovery was de-
Study Procedures
fined as complete or incomplete according to descriptions
provided by the authors. The prospective database of children with OBPI
treated at McMaster Children’s Hospital was analyzed to
Prospective Inception Cohort explore the discriminators between the children in the GZ
Children with OBPI treated at McMaster Children’s and the overall group. Surgical and nonsurgical interven-
Hospital between 2002 and 2005 were analyzed. Clas- tion groups of infants in the GZ were evaluated using the
sification of injury, changes in movement over time as AMS. The AMS scores of elbow flexion, shoulder flex-
measured by the AMS,7 recovery status as measured by ion, abduction, external rotation, wrist extension, and to-
the AMS, and whether surgical intervention was under- tal scores were examined at 1, 3, and 6 months to identify
taken were the variables of interest for this study. In this any important trends that would guide surgical decision-
study full recovery was defined as a perfect AMS score making. These particular movement items are the most
attained within the first 3 months. The AMS highlighted troublesome during recovery as well as the most reliably
in Table 2 is a 7-point scale with 15 items that are used measured. The AMS was administered by a trained and
to grade movement and not specific muscle action. The unblinded occupational therapist.
AMS provides a score for each of the joints in the up- The analysis of these discriminators permitted the
per limb including the hand. Scores from 1 to 4 reflect development of a guideline for surgical decision-making,
movement with gravity eliminated and scores from 5 to 7 which decreases the ambiguity of current care plans. The
are against gravity, and a score of 7 represents full range guideline was developed based on the existing evidence
against gravity. The total score with full active movement and our clinical decision-making process. It was then
against gravity is 105. The AMS provides guidelines for tested using the existing data as described below.
standardized use in infants with OBPI. Reliability of 0.89
Outcome Data
has been reported using weighted kappa on the total mea-
sure. Outcome data were examined at 1, 3, 4, 5, 6, and 12
All infants referred to the Obstetrical Brachial Plex- months and up to 3 years of age. Not all children had reached
us Clinic at McMaster Children’s Hospital are systemati- 3 years by the time of analysis. The following are the 5 out-
cally evaluated at monthly intervals until 6 months of age come categories, defined for the guideline, which describe
Full
Biceps Recovery
No. of Study Type, Recovery GZ Recovery in Total Mean
Authors & Year Patients Patients in GZ (%) Population Time Measure (%) Sample (%) FU Time
Hoeksma et al., 56 historical cohort, OBPI identified at birth >3 wks Narakas Motor 51 incomplete, 66 46 mos
2004 66 Scales 49 complete
Bisinella & Birch, 74 prospective cohort, OBPI, mean age at refer- >1 mo Mallett, Gilbert 41 incomplete, 53 32 mos
2003 89 ral 3.2 mos (range 1–9 & Raimondi 59 complete
mos)
Waters, 1999 66 prospective cohort, OBPI, evaluated w/in 1 mo Narakas, Mallet 95 incomplete, 12 36 mos
87 1–3 mos old 5 complete
Noetzel et al., 94 prospective cohort, OBPI, persistent lack of 2 mos MRC scale 28 incomplete, 66 18–24 mos
2001 71 shoulder or elbow anti- 72 complete
gravity movement at 2
wks, initial center eval-
uation before 1–2 mos
Al-Qattan, 2000 43 prospective cohort, Erb palsy, seen in clinic 2 mos AMS 70 incomplete, 60 18 mos
47 before 1 mo 30 complete
Strombeck et al., 247 prospective cohort, OBPI, sustained symp- 3 mos no standardized 91 incomplete, 27 5 yrs
2000 63 toms of deltoid & bi- tool 9 complete
ceps at 2 & 3 mos
present study 125† prospective cohort, OBPI, seen in clinic be- 1 mo AMS 56 incomplete, 49 3 yrs
81 fore 1 mos 44 complete
recovery status, treatment plan, and prognosis when an in- cations. We applied the same formula to our data: GZ =
fant exits the GZ: A, no surgery and complete recovery (number of patients with delayed recovery [> 1 month]
(These infants exit the GZ between 1 and 3 months with excluding total pan plexus Narakas Group IV)/(total num-
full AMS score and no functional deficits.); B, no surgery ber of patients). The percentage of patients in the GZ with
and delayed recovery (These infants exit the GZ between 3 complete recovery = (number of patients with complete
and 5 months and may achieve full AMS scores. At a later recovery in the GZ)/(total number of patients in the GZ).
age, these children exhibit residual functional impairment The percentage of patients in the GZ with incomplete re-
such as scapular winging, shoulder weakness, and atypical covery = (number of patients with incomplete recovery in
movement patterns. As there is a lack of strong outcome the GZ)/(total number of patients in GZ).
evidence, conservative management is the choice.); C, no Descriptive frequencies and cross-tabulations with
surgery and incomplete recovery (These children exit the Pearson chi-square calculation were carried out to exam-
GZ after 6 months with less than full AMS scores along ine associations and relationships between an outcome of
with significant functional impairment. The decision not perfect AMS score and Narakas group, and whether sur-
to proceed with surgery is due to parental choice.); D, early gery was performed and Narakas group. These analyses
surgery (These children exit the GZ before 6 months be- compare the total group of infants with the infants in the
cause of minimal progress in motor recovery, less than full GZ. The total AMS score, elbow flexion and shoulder ab-
AMS scores, and significant functional impairment.); and duction, external rotation, and flexion scores at 1, 3, and 6
E, delayed surgery (These children exit the GZ between months were compared between surgically and nonsurgi-
7 and 12 months because of lack of parental readiness for cally treated infants in the GZ.
surgery or infant health issues.). The GZ guideline was tested by examining ranges and
the mean AMS scores in surgically treated versus non-
Critical Analysis surgically treated infants. This study was approved by the
During critical analysis of the literature, the GZ was Research Ethics Board of the Faculty of Health Sciences,
calculated for all authors who provided data. Before 1 McMaster University in Hamilton, Ontario, Canada.
month of age, infants were not categorized into the GZ.
Complete recovery in the GZ is the percentage of infants Results
who did not attain complete recovery by 3 months, but
did have complete recovery at the follow-up evaluation. Table 3 summarizes the publications with data that
The following formula was used to calculate the per- allowed us to evaluate their patients with our GZ defini-
centage of infants that fell within the GZ in these publi- tion. The time to spontaneous recovery described by those
AMS Scores*
No Op Op Performed
Area Assessed & Time Points (in mos) Range Mean ± SD Range Mean ± SD p Value†
total
1 13–102 72.0 ± 21.9 32–90 59.6 ± 17.7 0.264
3 69–105 88.1 ± 18.6 37–92 69.3 ± 12.8 0.517
6 83–105 99.3 ± 6.4 66–102 82.2 ± 12.2 0.020
elbow flexion
1 0–7 3.0 ± 2.4 0–3 .9 ± 1.1 0.234
3 0–7 5.3 ± 1.7 0–6 1.8 ± 1.9 0.001
6 2–7 6.3 ± 1.3 0–7 4.0 ± 2.3 0.003
shoulder abduction
1 0–7 2.8 ± 2.2 0–5 1.3 ± 1.7 0.313
3 1–7 4.8 ± 1.9 0–5 2.9 ± 1.9 0.014
6 3–7 6.1 ± 1.0 2–6 3.7 ± 1.7 0.006
shoulder flexion
1 0–7 2.8 ± 2.0 0–5 1.6 ± 1.5 0.476
3 1–7 4.9 ± 1.7 1–6 2.9 ± 1.4 0.067
6 2–7 6.0 ± 1.2 2–6 4.1 ± 1.5 0.002
shoulder external rotation
1 0–7 2.8 ± 2.1 0–5 1.1 ± 1.7 0.815
3 0–7 4.4 ± 2.2 0–5 1.2 ± 1.8 0.002
6 1–7 5.5 ± 1.7 0–7 2.8 ± 2.4 0.007
* The total score is 105. A score of 7 for each item indicates full movement.
† Pearson chi-square test.
tainty. Many other groups have referred to this subset of The development of our GZ guideline is based on the
infants (Table 3), but they have not labeled them as such. earlier work of Gilbert,11 Michelow,16 and Curtis7 and their
Recovery times reported by these authors varied from 3 colleagues. Gilbert et al.13 concluded that assessment of
weeks to 3 months. This lack of precision supports that a biceps function best informs the need for surgery. In this
GZ exists. Clinicians require additional guidance for de- reported series of > 1000 children, the absence of biceps
cision making within this area until long-term outcomes function at 3 months of age was the primary indicator for
are well researched and clear, definitive surgical criteria surgery. Clarke et al.5,6 and Michelow et al.16 have exten-
are established. sively used the AMS7 in evaluating recovery over time in
In our population, 81% of our patients fell within infants with OBPI. Their surgical prediction model com-
this zone at 1 month of age. The large variability in their bines AMS scores of elbow flexion and extension, wrist
AMS scores at this stage makes it difficult to decide by 1 extension, thumb extension, and finger flexion and exten-
month those infants in the GZ who should undergo sur- sion. They have concluded that using elbow flexion alone
gery. However, decisions become clearer as the infant is as a predictor leads to significant false-positive findings.16
monitored through to 3 months. Using their combined prediction model, an inaccurate
A definitive decision against surgical intervention re- prediction rate is reduced to 5.2%.
quires strict criteria of full recovery. Prior series used a The GZ guideline presented in Fig. 1 is a departure
broad definition of recovery and reported 70–90% spon- from those that use only elbow flexion as a determinant
taneous recovery.16 However, a recently published system- for surgery.13 Our approach is similar to the combined
atic review of the natural history of OBPI illustrates that prediction model of Michelow et al.16 and Clarke et al.,6
this common perception is in fact inaccurate.19 There is because the AMS is an important component. The AMS
now evidence to suggest that many infants who are re- has been used as the objective measure of recovery with
ported to “recover spontaneously” do have residual defi- full recovery defined as a perfect AMS score within the
cits in function even if their nerves are intact.2,4,20 first 3 months. The AMS score alone is not enough to
Early surgery is only definitely required for chil- evaluate recovery outcomes in the toddler and child but
dren classified as Narakas Group IV, complete palsy and does work very well as early evidence of recovery in the
Horner syndrome. A very small proportion of children young infant. In keeping with Hoeksma et al.,14 Bisinella
are at this end of the spectrum. and Birch,3 and Waters,21 our GZ guideline also places
Fig. 1. Chart showing the GZ guideline for OBPI management. The asterisks indicate that the score accounts for ≥ 2 of the
following movements: elbow flexion (biceps) shoulder abduction, external rotation shoulder flexion, and wrist extension. See
Methods for the definition of the outcome categories (A–E).
strong emphasis on the assessment of shoulder function. a pattern of recovery that is often “patchy,” unusual, or
These authors have made a strong case that if recovery atypical, such as recovery in the elbow but not shoulder or
of shoulder as well as biceps function is not present by 1 vice versa. Given the analysis of our AMS scores, func-
month of age then there is a significant risk of incomplete tional outcomes, and recent evidence, we now suggest the
recovery. The residual functional problems described by inclusion of functional measures along with increased at-
Strombeck et al.20 at 5 years after support this perspective. tention to the shoulder in both surgical decision-making
We have found that infants in the GZ may demonstrate and future outcome studies.
To determine the need for surgical intervention, our Our outcomes using this guideline support the view
GZ guideline uses the criteria of AMS cutoff scores at each of Gilbert et al.11–13 that earlier surgical decision-making
month in ≥ 2 of the following movements: elbow flexion is possible and optimizes physiological recovery of dener-
(biceps), shoulder abduction, external rotation and flexion, vated muscle. Experimental and clinical data have clearly
and wrist extension. Also, we have recorded and calculated determined that time to muscle reinnervation is one of the
the mean AMS scores for our subset of children that ben- most significant factors affecting the quality and quan-
efited from surgical intervention. If a child’s total AMS tity of muscle functional recovery.10 In most experimental
score is less than the mean values in the surgical group models, delays to reinnervation beyond 3 months lead to
at the corresponding month, surgical intervention is prob- muscle fiber atrophy largely from structural protein deg-
ably warranted. If an infant has AMS scores ≤ 1 in ≥ 2 of radation, myocyte apoptosis, and secondary fibrosis and/
the previously mentioned movements at 1 month, then sur- or fatty replacement.9 Delaying microneural surgery to
gery is discussed but the child remains in the GZ. We have reconstruct the plexus with grafts, transfers, and/or neu-
seen that infants with variable AMS scores particularly at roysis condemns the muscle to incomplete recovery.10
1 month can still demonstrate recovery and improvement. We have only one opportunity in the neonatal period
Table 6 illustrates these movement scores at 1, 3, and 6 to maximize the neuronal input to the extremity to op-
months in our population. timize the physiological muscle and bone recovery. It is
If an infant with OBPI falls into the GZ they exit in important that this opportunity is given to all infants who
a number of ways within the first 6 months when surgical truly need it. All factors that can facilitate this decision
management is being decided. Figure 1 illustrates these should be considered.
outcomes. In our population of infants, no infant exited The GZ guideline presented here is a multidisci-
the zone at 1–2 months unless he or she had an AMS plinary, family-centered model that incorporates the best
score ≥ 6 in all movements on the scale. Those in Group existing evidence and the outcomes in the children fol-
A exited before 3 months by demonstrating full recovery lowed by our OBPI program.
with a complete AMS score (or > 90 points). As some
infants improve over time, more will exit the GZ without
surgery by attaining shoulder and elbow AMS scores ≥ Conclusions
5 by 5 months. The patients in Group B had good early There is compelling evidence that there is a group of
motor recovery such that surgery was not recommended infants in whom the present evidence and criteria for sur-
as it was believed the outcome would be equitable with gery do not provide a clear path for decision-making as to
no surgery. It is imperative to note that these children did the need for surgical intervention. The risks of no surgery
go on to demonstrate residual functional impairment in versus the benefit of surgery are not evident. The variation
the shoulder and scapula not captured by the AMS. The in surgical criteria and expectation for amount and timing
patients in Group D clearly required surgery, which they of recovery described in the body of literature confounds
underwent before or at 6 months. The patients in Group the issue. These infants are considered to lie within a GZ
E required surgery, but because lack of parental readi- where decisions as to surgery versus no surgery are not
ness or the child’s health, it was delayed beyond 6 months. black and white. The guideline presented in this paper
Those in Group C exited at 6 months with a decision for provides another framework for decision-making that in-
no surgery due to parental choice. These children demon- cludes other areas in addition to biceps recovery or elbow
strated significant residual impairment and primary nerve function. Although we do not have evidence from a clini-
reconstructive surgery was recommended. However, par- cal trial to support that this guideline is the best approach,
ents declined this treatment option. within the context of our prospective data collection, we
In light of recent evidence about long-term out- present this guideline to assist clinicians working with in-
comes,2,4,20,21 we are concerned about the 16 children in fants with OBPI to navigate the GZ.
Group B. These infants did not meet current evidence-
based surgical criteria based on their achievement and tim- Disclaimer
ing of AMS scores and function. This illustrates another
characteristic of children in the GZ that includes inconsis- The authors do not report any conflict of interest concerning
tency and decreased frequency of movement, despite the the materials or methods used in this study or the findings specified
in this paper.
infant attaining AMS scores of ≥ 5 in key muscle groups.
Strombeck et al.20 specifically reported that children who
had poor function at 3 months but had “recovered” by 6–9 References
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