Correlation between histopathological nerve assessment and clinical recovery in brachial plexus birth injuries

Abstract

In the management of brachial plexus birth palsies, the quality of the roots eligible for reconstruction is thought to be a key issue. The aim of the present study was to evaluate the correlations between pathological root examination and motor recovery after brachial plexus reconstructions. Quantitative histopathological analysis of intraneural fibrosis was conducted on 72 nerve transections (40 roots, 18 trunks and 14 suprascapular nerves) in 20 patients. Clinical recovery of targeted muscles after surgery was assessed by standardized functional scores. After a mean follow-up of 32 months, patients with a lower fibrosis rate for the suprascapular nerve had greater global Mallet scores (r = −0.57; p = 0.042) as well as a greater active shoulder flexion (r = −0.66; p = 0.015). Correlations were also found between C6 root and upper trunk fibrosis rate and some of the subsections of the Mallet score, active movement scale for the biceps and active elbow flexion. These results seem to confirm the relevance of intraoperative pathological evaluation of the roots and nerves after neuroma resection to optimally define the reconstruction strategy.

Level of evidence: IV

Keywords

Brachial plexus birth injuries histopathological analysis pathological root analysis root avulsion nerve graft

Introduction

Defined as a traumatic stretching injury of the brachial plexus occurring during childbirth, most often related to difficult deliveries, brachial plexus birth injuries (BPBI) have been reported to have an incidence in the range of 0.9–1.5 per 1000 live births (Foad et al., 2008; Kay, 1998), with incomplete recovery in 10%–30% of cases (Terzis and Kokkalis, 2009; Vakhshori et al., 2020). However, its incidence has fallen in some countries with changes in obstetric practice (Hems and Todd-Hems, 2023). Two types of nerve damage can be observed, including radicular avulsions, in which pre-ganglionic roots are torn from the spinal cord, and post-ganglionic root and/or trunk stretch injuries, which can lead to axonal degeneration and neuroma formation depending on their severity (Comtet et al., 1993; Seddon, 1943).

Primary reconstruction of the brachial plexus consists of resecting the post-traumatic neuroma and grafting between proximal roots and distal stumps (i.e. trunks, divisions, cords, nerves), with or without additional nerve transfers (Kozin, 2020). According to numerous authors (Al-Qattan, 2000; Gilbert and Tassin, 1984; Waters, 1999), patients with incomplete recovery may benefit from such surgery before 6 months of life. However, there remains a lack of strong evidence that nerve repair improves outcomes (Pondaag and Malessy, 2021). As reported in the current literature, surgical strategy depends directly on the intraoperative assessment of the quality of the roots (Bellity et al., 2021). Avulsed roots are inherently unusable for reconstruction, and severely fibrotic roots are commonly considered unsuitable as well. In fact, since the aim is to perform nerve grafts and/or transfers on non-fibrotic tissues, the quality of both stumps, proximal (i.e. roots) and distal (i.e. trunks), must be carefully assessed. During surgery, quality assessment is most commonly qualitative, based on intraoperative estimates by the surgeon under magnifying loupes or operative microscope (Lombard et al., 2020; Malessy and Pondaag, 2012). Conversely, semi-quantitative histological data, such as the percentage of intraneural fibrosis or frozen section histology stained with toluidine blue (Murji et al., 2008), do not seem to be routinely used to guide the reconstructive strategy (Comtet et al., 1993; Gschmeissner et al., 1991; Malessy and Pondaag, 2012). Based on these observations, Bellity et al. (2021) conducted a preliminary study showing that histological analyses commonly revealed higher rates of intraneural fibrosis than those estimated surgically. These results outlined the potential usefulness of extemporaneous histopathological examination to adapt the reconstruction strategy intraoperatively, but no functional outcomes were reported.

The aim of the present study was to assess the correlation between intraoperative histopathological data and functional recovery after brachial plexus reconstruction. Our hypothesis was that histologic fibrosis rates of roots, trunks and nerves are correlated with clinical outcomes.

Methods

A retrospective single-centre study, in Trousseau Hospital, Paris, France, was performed in 20 children who underwent nerve reconstruction for brachial plexus birth injury between January 2019 and May 2021. The local institutional review board approved the study.

Surgical indications

Indications for brachial plexus reconstruction were based on the initial extent of the BPBI and the clinical course of recovery. The extent of the injury was assessed according to the Narakas classification at the age of 1 month (Al-Qattan et al., 2009). In cases of complete palsy (i.e. Narakas groups III and IV), surgery was performed at the age of 3 months if active elbow flexion against gravity had not recovered (Gilbert and Tassin, 1984). In cases of upper plexus palsy (i.e. Narakas groups I and II), surgical reconstruction was performed at the age of 4–6 months in patients without active elbow flexion against gravity (Chuang et al., 2005; Gilbert and Pivato, 2004; Smith et al., 2004; Waters, 1999).

If patients recovered active elbow flexion against gravity, conservative treatment was continued, with follow-up consultations every 6 months until the age of 18 months. In cases of persistent motor deficit, patients underwent elective nerve transfers at 9–18 months of age (Sénès et al., 2015).

Intraoperative assessment

Brachial plexus reconstructions were performed under optical magnification by two senior surgeons (MB and FF) with level 4 expertise (Tang and Giddins, 2016). A standard V-shaped cervical approach was used to expose the supraclavicular brachial plexus, allowing the identification, dissection and electrical stimulation of the roots upstream of the neuroma, and of the trunks, trunk divisions, cords and nerves downstream. The neuroma was then resected, allowing surgical assessment of nerve stumps, including the roots proximally, and the trunks, divisions, cords and nerves distally.

Nerve sections were taken from the non-avulsed root stumps that were considered satisfactory by the surgeon (i.e. no fibrosis visualized under operating optical magnification) and were sent to the pathologist for histological analysis. In cases of an unsatisfactory stump after neuroma resection, the surgeon performed further proximal transections of the root until the stump quality was deemed satisfactory (i.e. root quality was not grossly pathologic), or until no more transections could be made proximally (i.e. root exit from the intervertebral foramen); only the last section was sent for analysis. In cases of avulsed roots, the proximal end of the root was transected and also sent for histological analysis. Unaffected roots were left in continuity, without pathological analysis.

Trunks, divisions and terminal branches were transected distally at their respective exits from the neuroma. If the stump quality was deemed satisfactory by the surgeon, a neural section was sent to the pathologist for analysis. Otherwise, iterative transections were performed until the stump quality was considered satisfactory, and only the last section was sent for pathology. Brachial plexus reconstruction was then performed with sural grafts (Figure 1).

Pathological examination

All histological sections were analysed by a board-certified pathologist, blinded to the study hypothesis and surgical findings, using a light microscope (Leica DM2000, Leica Microsystems, Wetzlar, Germany). Surgical biopsies were fixed in formalin and paraffin-embedded, deparaffinized in xylene and stained with conventional Haematoxylin-Eosin-Saffron (HES) coloration. Immunohistochemical studies using S-100 antibodies (Leica polyclonal RDI, Leica Biosystems™, Wetzlar, Germany) were additionally performed (Miko and Varga, 2015). The first examination of the entire section was conducted at a low magnification (×20) by the pathologist, to identify an area of intraneural tissue that was representative of the whole section while focusing on architectural disorganization and fibrosis. This section area was then examined at a higher magnification (×50), allowing the determination of the percentage of the area that was occupied by fibrotic tissues using a semi-quantitative system. This percentage was then generalized to the whole sample, giving an estimate of the proportion of intraneural fibrosis for the entire section.

A global proportion of intraneural fibrosis was calculated for each child as the mean of the values from the specimens analysed.

Clinical examination

At last follow-up, all patients underwent comprehensive assessments of muscular strength, conducted by specialized physiotherapists with an exclusive paediatric practice. Since most children were too young to understand the examiner’s requests, strength was rated from 0 to 3. In addition, the deltoid, biceps and triceps muscles were specifically assessed using the active movement scale (AMS) (Curtis et al., 2002). The AMS has been shown to be effective in BPBI follow-up, with scores <5 considered to be poor results, scores equal to 5 fair results and scores >5 good results (Lombard et al., 2020). Finally, each patient’s functional status was assessed using the Mallet score for shoulder function and the Raimondi–Gilbert score for hand function (Al-Qattan et al., 2009; Haerle and Gilbert, 2004; Russo et al., 2014).

Statistical analysis

All data were collected by an independent observer: preoperative characteristics; intraoperative assessments; histological findings; and functional outcomes. We used the Spearman correlation test to explore the correlation between intraneural fibrosis and clinical outcomes after confirming the normality of the data. A p-value <0.05 was considered to be statistically significant.

Results

Preoperative characteristics of the 20 patients are shown in Table 1. Mean age at operation was 6.5 months (range 3–14), including 15 patients who underwent primary brachial plexus repair (i.e. before 6 months) and five who underwent secondary nerve transfers of the spinal accessory nerve (SAN) to the suprascapular nerve (SSN) to restore active shoulder external rotation (Table 2).

Table 1.

Cohort characteristics.

Characteristics	Value
No. of patients	20
Age at surgery (months)	6.5 (1.9)
Sex (F/M)	13/7
Birth weight (g)	3977 (820)
Affected side (R/L)^a	11/10
Type of BPBI^b
I	3
II	4
III	1
IV	12
Type of surgery
Early surgical management	15
Secondary nerve transfers	5
Type of neural stumps
Roots	41
Trunks/divisions	16
Suprascapular nerves	13

Data are expressed as number or mean (SD), unless otherwise stated.

One patient had a bilateral palsy.

According to the Narakas classification.

BPBI: brachial plexus birth injuries.

Table 2.

Brachial plexus repair procedures.

Patients	Age at surgery (months)	Narakas classification	Procedure
Patients	Age at surgery (months)	Narakas classification	C5	C6	C7	C8	SAN to SSN
1	5	IV	Gr UT, SSN	Gr UT, MT and C8	Direct suture C8
2	3	IV	Gr UT				Y
3	4	IV	Gr UT	Gr LT	Direct suture C8		Y
4	6	IV	Gr UT, SSN	Gr UT, MT	Gr MT
5	7	IV	Gr UT	Gr UT	Gr LT	Gr LT
6	6	IV	Gr UT, SSN	Gr UT, LT
7	7	IV	Gr LT				Y
8	6	IV	Gr UT	Gr MT	Direct suture C8		Y
9	11	II					Y
10	5	IV	Gr UT	Gr MT, LT			Y
11	4	II	Gr UT	Gr MT			Y
12	4	IV	Gr UT	Gr UT	Gr MT, LT	Gr LT	Y
13	8	I					Y
14	7	II					Y
15	6	IV	Gr UT	Gr UT, MT	Direct suture C8		Y
16	4	III	Gr UT	Gr MT			Y
17	5	IV	Gr UT		Gr UT		Y
18	14	I					Y
19	10	I					Y
20	5	II	Gr UT	Gr UT			Y

Gr: Graft to; LT: lower trunk; MT: middle trunk, SAN: spinal accessory nerve; SSN: suprascapular nerve; UT: upper trunk; Y: yes.

The proportion of intraneural fibrosis was determined histologically in 80 nerve transection samples, harvested from 52 proximal stumps (i.e. roots) and 28 distal stumps.

After excluding the avulsed roots that were not used during the reconstruction and the patient lost to follow-up, 72 nerve transections samples were available for statistical analysis (Table 3).

Table 3.

Semi-quantitative histological analysis.

	Proportion of fibrosis after histological analysis
Patients	C5	C6	C7	C8	T1	Trunks	SSN	Global
1	0.20	0.40	0.40	Avulsed			0.50	0.37
2	0.30	0.80	Avulsed	Avulsed	Avulsed			0.55
3	0.60	0.40	0.80	Avulsed				0.6
4	0.50	0.30	0.10			UT 0.40MT 0.40		0.34
5	0.05	0.05	0.05	0.20	Avulsed		0.00	0.07
6	0.00	0.25		Avulsed	Avulsed			0.12
7	0.10	Avulsed	Avulsed	Avulsed	Avulsed	LT 0	0.60	0.23
8	0.40	0.40	0.20	Avulsed	Avulsed	UT 0.30MT 0.15LT 0.10	0.10	0.24
9							0.00	0.00
10	0.10	0.40	0.90	Avulsed	Avulsed	UT 0.45MT 0.05LT 0.30	0.10	0.33
11	0.60	0.50	Avulsed			UT 0.33MT 0.40LT 0	0.40	0.37
12	0.30	0.30	0.25	0.40	Avulsed	UT 0.40MT 0.50LT 0.30	0.10	0.32
13							0.00	0.00
14							0.00	0.00
15	0.50	0.10	0.40	0.50		UT 0.4MT 0.7		0.43
16	0.05	0.05	Avulsed					0.05
17	0.00	0.90	0.80	Avulsed		UT 0.5	0.80	0.6
18							0.50	0.50
19							0.20	0.20
20	0.25						0.02	0.13

LT: lower trunk; MT: middle trunk; SSN: suprascapular nerve; UT: upper trunk.

Correlation between intraneural fibrosis and clinical outcomes

Clinical outcomes after a mean follow-up of 32 months (range 19–45) show considerable variation in shoulder and elbow function (Table 4). Four children did not regain 90° of elbow flexion. Patients with lower fibrosis rates in the SSN had greater global Mallet scores (r = −0.57; p = 0.042) as well as a greater ‘hand to neck’ task and a greater active shoulder and elbow flexion (r = −0.7, −0.66 and –0.73; p = 0.007, 0.015 and 0.005, respectively) (Tables 4 and 5).

Table 4.

Clinical results.

Patients	FU (months)	Mallet score					Total Mallet score	Raimondi	AMS deltoid	AMS biceps	AMS triceps	Active elbow flexion (°)	Active shoulder flexion (°)	Active elbow extension (°)
Patients	FU (months)	Active abduction	External rotation	Hand neck	Hand backs	Hand mouth	Total Mallet score	Raimondi	AMS deltoid	AMS biceps	AMS triceps	Active elbow flexion (°)	Active shoulder flexion (°)	Active elbow extension (°)
1	45	2	1	2	1	3	9	2	5	6	2	110	30	N/A
2	38	3	1	1	1	1	7	2	5	0	0	0	90	N/A
3	35	3	1	2	2	4	12	2	5	5	0	120	80	N/A
4	40	4	4	4	3	4	19	3	6	6	7	140	130	180
5	34	3	2	2	2	2	11	2	5	5	2	110	90	180
6	32	3	2	2	2	2	11	2	5	1	6	0	80	180
7	36	3	1	1	3	1	9	2	5	0	5	0	30	180
8	37	4	2	2	3	3	14	2	6	7	3	130	100
9	38	5	5	4	4	4	22	4	7	7	7	140	180	180
10	31	3	2	2	3	2	12	1	5	6	7	90	75	180
11	31	3	4	2	2	3	14	4	5	7	6	120	45	170
12	30	3	1	2	2	3	11	2	5	5	5	90	60	N/A
13	26	4	3	4	4	5	20	4	6	7	7	140	160	170
14	Lost to FU	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A
15	27	3	2	2	3	3	13	3	5	6	6	110	80	170
16	27	3	1	2	2	3	11	4	5	5	6	90	80	170
17	31	3	2	1	1	2	9	2	5	5	6	65	60	170
18	26	4	2	2	3	2	13	4	6	5	7	90	120	180
19	22	3	3	3	3	2	14	4	5	6	6	90	90	N/A
20	19	3	2	2	3	2	12	3	5	6	7	120	90	180

AMS: active movement scale; FU: follow-up; N/A: not applicable.

Table 5.

Significant correlations matrix between roots/nerves fibrosis rate and clinical tests.

Clinical test	Correlation coefficient	p-value
Correlation matrix for SSN
Global Mallet score	−0.57	0.042
Hand to neck	−0.703	0.007
Active shoulder flexion	−0.658	0.015
Active elbow flexion	−0.727	0.005
Correlation matrix of C6
Hand to neck	−0.562	0.045
Correlation matrix for global fibrosis
Hand to neck	−0.506	0.027
Hand to back	−0.491	0.033
Correlation matrix for upper trunk
AMS biceps	−0.784	0.037
Active elbow flexion	−0.665	0.007

AMS: active movement scale; SSN: suprascapular nerve.

Correlations were also found between roots and trunk fibrosis and subsections of the Mallet’s score; ‘hand to neck’ task was correlated with C6, and global fibrosis rate (r = −0.56 and −0.51; p = 0.045 and 0.027, respectively) (Figure 2). ‘Hand to back’ task was correlated with global fibrosis rate (r = −0.49; p = 0.033). Correlations were also found between upper trunk fibrosis and AMS of the biceps and active elbow flexion (r = −0.78 and −0.66; p = 0.037 and 0.007, respectively) (Table 5).

No significant correlations were found between root pathology and the clinical recovery concerning the deltoid and triceps AMS, Raimondi score and active elbow extension.

Discussion

In this study, we found that clinical scores were statistically correlated with roots, trunks and SSN fibrosis rate with less favourable outcomes associated with higher proportions of fibrosis. Several authors have been working on quantitative criteria for evaluating the quality of nerve stumps. From this perspective, Bellity et al. (2021) have shown the inaccuracy of the surgeon’s assessment of root quality, with higher percentages of fibrosis in some roots than estimated during surgery. Malessy et al. (1999) found a significant correlation between the amount of fibrotic tissue in the cross-section of the proximal stump and biceps strength at last follow-up in adult brachial plexus lesions. With a follow-up of 35 months in 25 patients and 50 roots studied, their study concluded that the cut-off for myelin percentage was 50% to adapt the surgical strategy: at more than 50%, the root was suitable for grafting, otherwise the surgeon should use nerve transfer. Gschmeissner et al. (1991) reported on ways to assess the root fibrosis percentage intraoperatively by using methylene blue, or by creating a method of rapid frozen section assessment taking only 2 minutes, suitable for the operating room. Their primary observation was that histological study of resected stumps from plexus surgery shows a discrepancy between the macroscopic appearance and the histological findings. These studies raise the two points on which our study focuses: the need for an objective criterion of root evaluation and the correlation between root quality and clinical outcomes.

In our study, a lower percentage of global fibrosis was correlated with a better clinical recovery according to some of the Mallet score tasks. No significant correlations were observed regarding the Raimondi score, probably because avulsed distal roots were not included in pathologic analysis since they were not repaired. The Raimondi (scale) evaluates hand function (Haerle and Gilbert, 2004) and hand recovery after a brachial plexus reconstruction is slow. Improvement continues for at least 3 years after repair and hand function will progress for longer, up to a maximum of 8 years after surgery (Birch et al., 2005). Therefore, although our follow-up was too short to evaluate the final recovery of hand function, we found correlations with the Mallet score for shoulder function, AMS score for biceps, and active shoulder and elbow flexion.

Based on our findings, we recommend performing intraoperative an pathological examination to improve surgical strategy and increase the chances of functional recovery. We have started to put this policy into practice and the pathological assessment has allowed us to adapt our surgical strategy. We send every root and nerve trimming to pathology when their quality is deemed good macroscopically and get the results before finishing sural nerve harvesting. If the fibrosis rate is too high (we have arbitrarily chosen a rate of over 50%), we recut the roots and nerves distal to the neuroma, if possible, in order to decrease the fibrosis rate as much as possible, although more neuroma resection demands the use of longer grafts. We direct the majority of sural grafts from the less fibrosed roots. However, the amount of fibrosis that contraindicates nerve grafting has yet to be determined.

Possibilities, which could be explored, include innovative techniques for interpreting anatomopathological sections. For example, full-field optical coherence tomography has been used since 2011 in the analyses of tissues and is currently being studied in the analysis of biopsies in several cancers (Jain et al., 2011). This small device, which is the size of a microscope, could be easily implemented in the operating theatre. All that is needed is to put the samples into the device and, with trained surgeons, the proportion of fibrosis could be assessed in real time.

The present study has some limitations. First, we used only one histological parameter: intraneural fibrosis. We could have assessed other parameters, such as the amount of myelin, number of thick fibres or aberrant fibres as described by Malessy et al. (1999). However, the measurement of intraneural fibrosis alone is a fast procedure and we have now demonstrated that the assessment of the amount of roots fibrosis correlates with clinical recovery. Measurement of intraneural fibrosis costs the least and requires the least preparation. It is also a repeatable technique that can be used by other centres. Second, our study included a small number of patients with a mixture of nerve graft and nerve transfer cases. A larger cohort of at least 50 participants would have been preferable for multivariate regression. However, we were able to evaluate a large number of nerve samples. Unfortunately, this small number of patients does not allow us to conclude on the fibrosis rate, which is minimal to allow good clinical results. Third, the clinical examination of children aged under 3 years is difficult, so we have set up repeated clinical examinations to pool the results and overcome this difficulty. Fourth, the r-values are somewhat moderate but not strong correlations, which would be >0.7. Some confounding factors, such as age and Narakas grades, were not accounted for.

In conclusion, we showed that the percentage of intraneural fibrosis was statistically correlated with functional recovery according to Mallet’s score, AMS for the biceps, and active shoulder and elbow flexion. These results confirm the relevance of intraoperative histopathological evaluation of the roots, trunks and nerves after resection of the neuroma to define the surgical reconstruction strategy and improve clinical results. Further work is needed to show whether outcomes are improved using this approach.

Footnotes

Declaration of conflicting interests

The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

Ethical approval for this study was obtained from the Institutional Review Board (approval number 2023/RV_FF/1).

Informed consent

Written informed consent was obtained from legally authorized representatives before the study.

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