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ORTHOPAEDIC REVIEW
A Review Paper
Painful Lumbosacral Sensory Distribution Patterns: Embryogenesis to Adulthood
James W. Simmons, MD, Robert Ricketson. MD, John N. McMillin, MD
Orthop Rev. 1993 Oct;22(10):1110-8. PMID:8265218
ABSTRACT
When the dorsal root ganglion is irritated by any of a variety of mechanisms, pain is referred to the
various structures innervated by that root. In many circumstances, this pain is specific and may be
used as a diagnostic aid. Unfortunately, emphasis is placed on defining a dermatomal distribution; the
existence of a myotomal or sclerotomal origin of referred pain is often overlooked. This review pre-
sents the embryologic, anatomic, and neurophysiologic etiology of referred pain from the lumbar
spine.
Low back pain is one of the most common presentations to the orthopedic surgeon, affecting nearly
85% of the population during their lifetime. It is frequently accompanied by radiation and/or
dysesthesias down the length of one or both of the lower extremities in either a dermatomal,1, 2 or
somatotopic (sclerotomal3,7 or myotomal8) sensory pattern. Additionally, moderate to acutely tender
distal motor points have been described in disk pathology.8, 9
“Referred pain” is defined as pain that is felt in a region other than its source of origin.10 For example,
pain from myocardial ischemia is commonly referred to the left arm, that from splenic abnormalities
to the left shoulder, and that from an' acutely inflamed appendix to the umbilicus11. As with visceral
structures, when a spinal nerve root ganglion is irritated pain, is referred to the various structures
innervated by that root. In many circumstances, this pain is specific and may be used as a diagnostic
tool. Unfortunately, emphasis is placed on defining a dermatomal distribution, and little emphasis is
attributed to the existence of the myotome or sclerotome.
The purpose of this review is to recapitulate the embryologic basis for referred pain patterns, with
specific regard to their dermatomal, myotomal, and sclerotomal origin. In addition, we present the
current understanding of the neurophysiologic and anatomic basis of referred pain of lumbosacral
origin.
EMBRYOLOGIC DEVELOPMENT
Very early in embryologic development, there is an intimate segmental relationship established
between each nerve and its corresponding dermatomal, myotomal, and sclerotomal components. A
brief review of this process provides clinically important clues to why affliction of one structure can
manifest itself in other segmentally related structures.
The musculoskeletal system is derived from the embryonic mesoderm, which subsequently
differentiates into three parts: the paraxial, intermediate, and lateral mesoderm. The paraxial
mesoderm is the major thrust of this review.
MESODERM INDUCTION
Mesoderm induction is initiated before the zygotic genome is transcriptionally active and the extra-
embryonic proteins needed to initiate induction are most likely oocytic in origin 10,11. In the vertebrate,
the formation of both the mesoderm and endoderm appears to require requires signaling by nodal
protein-related ligands from the TGFβ superfamily 1,2,3. The exact signaling mechanism in humans is
not known. However, Ogawa et al (2007) reported TGFβ regulates multiple effectors of embryonic
stem cell pluripotency and differentiation5. Lee et al., (2011) demonstrated high-level Nodal signaling
with Activin, also a member of the TGFβ superfamily9, and induced differentiation toward
mesoendoderm formation6.
The effect of tobacco smoke on mesoderm development was recently studied by Liszewski, et al 4.
ORTHOPAEDIC REVIEW
Their work with human expressed stem cells (hesc) demonstrated that Brachyury, an early mesoderm
marker expressed by the Tal1 and Nkx2-5 genes (human mesoderm development), was increased 10-
fold and persisted longer than expected when exposed to tobacco smoke and resulted in an adverse
impact on mesoderm specification7. The persistence of nodal may also be the result of tobacco-induced
increased expression of hsa-mir 302a8. MicroRNAs (miRNAs) are small RNAs thought to control the
post-transcriptional expression of over 30% of human coding genes. The hsa-mir 302 cluster has been
shown to promote pluripotency and hsa-mir 302a inhibits the post-transcriptional translation of Lefty1,
a nodal inhibitor7, 8. The effect of increased nodal signaling, therefore, very likely causes the delay in
differentiation seen by tobacco exposure.
Illustration (Mesoderm induction)
After induction (day 32-beginning of gastrulation), the paraxial mesoderm condenses to form 42
somites that run the entire length of the embryo in a cephalocaudal sequence, located adjacent to the
neural tube. The somite then differentiates to produce a ventromedial portion (sclerotome) and a
dorsolateral portion (dermomyotome). Subsequent division of the dermomyotome forms the
dermatome and the myotome.
Figure 1. The emerging nerve is seen prior to division into anterior and posterior primary rami.
The paraxial mesoderm has differentiated to the dermomyotome and sclerotome. (Image
reconstructed from the original, 3/15/2018, by author, See Original Illustrations).
Sclerotome development
The vertebral bodies originate from the sclerotomes, each of which differentiates into a cephalic and
a caudal portion. The cephalic portion fuses with the caudal portion of the adjacent sclerotome to form
a vertebral segment, and an intervertebral disk develops between each vertebral body. The
sinovertebral nerve is seen to branch from the postganglionic anterior primary ramus to innervate a
portion of the segmental sclerotome, sending fibers to the intervertebral disk, posterior longitudinal
ligament, anterior dura, and periosteum (Figure 2). There are also afferent autonomic sympathetic
branches from the paraspinal sympathetic ganglion (above L2) and from the sympathetic chain (below
I.2) that develop connections to the sinuvertebral nerve.21.22
The limb bud arises from the lateral mesoderm, a condensation of mesenchyme separate from somitic
mesoderm. The lateral mesoderm divides to form the splanchnic and somatic mesoderm. IS Within
the somatic mesoderm will arise a separate condensation of mesenchyme, ultimately giving rise to the
lower limb myotome and sclerotome (Figure 2). The splanchnic mesoderm does not appear to
contribute to myotomal or sclerotomal structures.
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Figure 2. The posterior primary ramus has entered the paraspinous muscles that arose from the
dermomyotome. The anterior primary ramus descends toward the separate mesenchymal condensation
that ultimately forms the limb bud. The sinuvertebral nerve arises from the anterior primary ramus and
is seen to innervate the sclerotomal structures. (Image reconstructed from the original, 3/15/2018, by
author, See Original Illustrations).
The sclerotome ultimately becomes mature bone from the cartilaginous anlage through endochondral
ossification, a process that has been well described in basic textbooks of histology. Nerve endings
have been identified within the periosteum of the developing embryo as well as within the ligaments and
synovial membrane of human
joints."
These are separate from the cutaneous nerve endings supplying the
dermatomes. The peripheral nerve of origin of these sensory afferents is not well defined, however, but they
probably arise from the nerve passing in closest approximation.
How, then, is pain experienced (perceived) when these structures receive noxious stimuli in an
adult? These fibers can be directly stimulated, as when a penetrating object comes in contact with
periosteum. Such stimulation results in a sensation that
is
dull and aching in quality and may be
associated with such constitutional manifestations as nausea, vomiting, sweating, and
vasoconstriction, resulting "in a
"sickening feeling
4
.
Myotome Development
The myotome that arises within the somite (somitic mesoderm) further differentiates to form the
epimere. The dorsal primary ramus, containing both motor and sensory afferent fibers, enters the
epimere and supplies the innervation required for that segment24. The dermatome overlying the
dorsal myotome is also supplied by the sensory fibers in a cutaneous distribution.
The myotomes developing out of the somatic mesoderm form condensations of myomeres, from
which arise myoblasts. It is from these myotomes that the muscle groups of the lower extremities
ultimately form. The developing anterior primary ramus enters the myotome, supplying the
innervation to that segment (Figure 3).
As
with development of somitic mesoderm, this innervation
is critical to the development of functional muscle tissue. It has also been postulated that innervation
of the lower-limb myotomes occurs progressively in a time-ordered fashion. Once a structure has
received appropriate innervation, the environment is modified so that no
other entering
neuroblast is
able to innervate that segment. The succeeding neuroblast is then deflected away from the newly
innervated segment and grows further into the mesoderm. Once these connections are made, dendritic
sprouts arise from the neuroblasts to
form the neural end plate of the myoneural junction. Afferent nerve endings have also been identified
within fascia and tendons of the developing embryo where they form the sensorimotor feedback loop.
What differentiates pain experienced from the sclerotomal structures from that derived from the
myotomal structures is probably a combination of perception and elicitation. Both result in a deep,
dull, aching sensation. Myotomal pain, in contrast, can be well localized, as in the acutely tender
ORTHOPAEDIC REVIEW
motor point, and can be elicited by direct pressure. This tender area is not uncommonly associated
with a palpable muscle spasm.
Figure 3. The nerve roots enter the limb bud in a spatiotemporal sequence to innervate the
musculature of the lower limb. (Image reconstructed from the original, 3/15/2018, by author, See
Original Illustrations).
Dermatome Development
As the lower limb develops, medial rotation around its central axis occurs (Figure 4). Thus, the great
toe is located on the medial aspect of the foot, as can be observed on the various dermatomal charts.
The mesoderm overlying the myotomes also receives sensory innervation from various peripheral
nerves, giving rise to the dermatomes. These dermatomes lie directly beneath the skin and are formed
by the sensory afferents located within the subcutaneous tissue and the dermis of the skin.
It has been demonstrated that if a nerve root is compressed, what is experienced is numbness and
paresthesias. However, when the root is inflamed,
ORTHOPAEDIC REVIEW
Figure 4. Medial rotation of the limb occurs, placing L-4 medial to the L-5 sensory distribution.
(Image reconstructed from the original, 3/15/2018, by author, See Original Illustrations).
pain is referred to the portion of the limb innervated by that
segment.
We are becoming increasingly
aware of the many pain mediators within the spine and their role in pain provocation (Table 1) 12,13,17. We
have all seen cases in which the patient presents with severe leg pain in a "dermatome" pattern, negative
tension signs, and little radiographic evidence of nerve compression. When one considers the local
environment of the nerve root in the presence of these chemical irritants, the dorsal root ganglion, as well
as the free nerve endings within the various structures previously discussed, are stimulated, resulting in
referred pain (dysesthesias) without tension signs or neurologic deficit. This phenomenon can be
explained by convergence, which will be discussed later. There does appear to be significant overlap with
regard to the sensation associated with the cutaneous distribution of each cutaneous sensory nerve.
Therefore, the various dermatomal charts are most useful as a general reference rather than a sine qua non
and should not be counted on to guide one to a specific diagnosis by their use alone.
Table I. Pain Mediators in the Spine
Substance P
Vasoactive intestinal polypeptide (VIP)
Cholecystokinin
Neurotensin
Calcitonin gene-related peptide
Somatostatin
Enkephalin
Angiotensin
Bombesin gastric-related peptide
Nerves emerging from the lumbar region innervate the various segmental structures. These structures
include: the annulus fibrosis of an intervertebral disk, spinal ligaments, fascia, and tendons of the
paraspinous and lower limb muscles; periosteum and synovial membrane within
the
joints of long bones;
ORTHOPAEDIC REVIEW
and the dermis and subcutaneous tissue with sclerotomal, dermatomal, and myotomal extensions
corresponding to that nerve. In the next section we describe the neurophysiologic and anatomic
characteristics of the adult sensorimotor segment and present information from the. literature
regarding the nature of referred pain from a spinal segment.
Table Il. Innervation of the Lower Extremity Musculature
Lumbosacral nerve
Lower extremity musculature
L-2, L-3
Iliopsoas, Gracilis, Sartorius, Pectineus, Adductor longus,
Adductor brevis
L-3
Quadratus lumborum, Iliopsoas, Gracilis, Sartorius,
Pectineus, Adductor longus, Adductor brevis
L4
Adductor brevis, Quadriceps femoris, Adductor magnus,
Obturator externus, Quadratus lumborum, Gluteus
medius, Gluteus minimus, Tensor fascia lata, Tibialis
anterior, Gemelli
L5; S1
Tibialis anterior, Gluteus maximus, Gluteus medius,
Gluteus minimus, Tensor fascia lata, Extensor digitorurn
brevis, Flexor digitorum longus, Adductor hallucis,
Adductor digiti quinti, Flexor digiti quinti brevis,
Interossei, Popliteus, Plantaris, Soleus, Gastrocnemius,
Extensor digitorurn brevis, Flexor digitorum longus,
Adductor hallucis, Adductor digiti quinti, Flexor digiti
quinti brevis, Interossei
NEUROANATOMY AND PHYSIOLOGY
It is beyond the scope of this review article to take each nerve and describe its particular
characteristics. For the purpose of clarity, we will use the L4 segment (L4-5 intervertebral disk and
L-4 nerve) as an example. We refer the reader to Table II for a review of the musculature of the lower
extremities and their innervation.
The sinuvertebral nerve is a sensory afferent nerve relaying pain stimulus from nociceptive free
nerve endings. Bogduk describes three branches: the ascending, descending, and transverse branches.
The ascending branch relays information from the posterior longitudinal ligament (PLL), disk, and
anterior dura of the segment above. The descending and transverse branches supply the entry-level
disk, PLL, and anterior dura and may also bring interaction from as many as two to three segments
below.21, 22 Therefore, there is significant overlap between as many as three separate segments. This
sclerotomal information then passes into the ventral
primary
ramus and dorsal root ganglion. Its
corresponding pseudo-unipolar cell then transmits its information to the spinal cord via the dorsal
root through the dorsal-root entry zone (DREZ).
These fibers then enter the Zone of Lissauer at the lateral corner of the dorsal columns, where they
then divide into ascending and descending
branches.
Within the zone of Lissauer, they descend or
ascend one to two segments before terminating on their cell body in the posterior marginal nucleus
as well as in the nucleus proprius of the dorsal gray matter. The posterior marginal nucleus functions
as the relay station for pain and temperature, whereas the nucleus proprius serves to interpret
information with descending column.
ORTHOPAEDIC REVIEW
ORTHOPAEDIC REVIEW
Figure 5. (A) Convergence-facilitation pattern of referred pain. Subthreshold sensory input from the lower
cutaneous receptors synapse upon the same spinothalamic cell body as the sensory Input from the
sinuvertebral nerve. When suprathreshold painful stimulus occurs, pain is referred to the leg. (8)
Convergence projection pattern of referred pain. Painful stimulus from the annulus synapse converge upon
the same cell body within the spinothalamic tract as the cutaneous receptors. The information is projected to
the sensory cortex and interpreted as arising from the leg. (C) Pain reflex pathway. Referred pain via the
torn annulus results in referred pain pattern as well as myotomal pain from reflex muscle spasm the theory
of convergence-facilitation (Figure 5A), as described by Ruch and Patton, continuous afferent impulses are
normally coming in from cutaneous receptors but are insufficient to excite the spinothalamic tract (STT)
cell bodies. Another nociceptive impulse from another afferent fiber-for example, an annular tear
stimulating the sinuvertebral nerve-synapses upon the same cell, which then facilitates excitation that
results in the referral of pain to that region of cutaneous sensation. Therefore, impulses from exteroceptive
nociceptor fibers in the skin that are giving a continuous stimulus due to their exposure to environmental
stimuli can be amplified by the addition of a stimulus from the nociceptive fibers within an acutely torn
annulus. (Image reconstructed from the original, 3/15/2018, by author, See Original Illustrations).
According to the convergence-projection theory of referred pain (Figure 5B), afferent axons from two
different regions synapse upon the same cells that receive their primary input from other structures. For
example, a primary SIT cell receives dermatomal information from cutaneous receptors, but also receives
sensory input from the sclerotomal (as from the annulus) and myotomal component. Once stimulated, the
SIT
cell projects the
in
formation to the thalamus and sensory cortex through the anterolateral tract, and
this pain stimulus is perceived as arising from one structure. There is experimental evidence that many
SIT
cells in the spinal cord receive muscle input in addition to cutaneous input." There is, then, at least
indirect experimental evidence for the existence of a plausible explanation for referred pain.
CLINICAL CORRELATION
Many investigators have demonstrated specific patterns of referred pain upon the stimulation of a
variety of anatomic regions within particular spinal segments.2-7, l4. Their conclusions are presented in
Figures
6A, 6B,
and 6C. When this information is added to our current knowledge of the embryologic,
anatomic, and neurophysiologic basis of referred pain.
pain patterns, it is possible to improve our understanding and diagnosis of the various manifestations of this
pain as seen
in
our patients.
ORTHOPAEDIC REVIEW
Figure 6. (A) Dermatome, myotome, and sclerotome patterns of; (A) dermatome, (B) myotome, (C)
sclerotome patterns. D. Innervation of dermatomes, myotomes, and sclerotomes
CASE 1
A 40-year-old woman presented with a gradual onset of low back pain and radiation to the left posterior
calf associated with occasional paresthesias and numbness along the plantar aspect of her left foot. On
physical examination, she had a positive straight-leg raise in the affected leg. Tenderness
was
elicited
upon palpation of the paraspinous musculature of her lower lumbar spine. Neurologic examination
demonstrated an absent left Achilles tendon reflex, diminished sensation over the 5-1 dermatome of her
left foot, and 5/5 strength of all motor groups in the left leg.
Subsequent evaluation by magnetic resonance imaging (MRI) demonstrated a large left paracentral
disk herniation at L-S-5-l. Electromyography (EMG) showed an S-1 radiculopathy consistent with the
above clinical and radiographic assessment. The patient subsequently underwent discectomy and had
improvement of her symptoms.
Discussion
ORTHOPAEDIC REVIEW
This case adequately illustrates sclerotomal,
myotomal,
and dermatomal manifestations of lumbar disk
disease with "radiculopathy." The pain the patient experienced in her back and leg represented the local
and referred sclerotomal pattern of a tom annulus. There was no referral of pain to her feet, as might
have been expected if there was a dermatomal pain pattern from convergence. Instead, the dermatomal
response of paresthesias and numbness in the L5-S1 region was consistent with the usual presentation
of compression neuropathies in the extremities. Again, upon straight leg raising, there was sclerotomal
referral due to annular injury (discogenic). Myotomal pain was elicited upon palpation of the
paraspinous musculature. This localized pain was set up by spasm that was induced by segmental
intraspinal reflexes mediated by the posterior primary ramus through the stimulation of afferents within
the torn annulus.
CASE 2
A 39-year-old man presented with chronic low back pain radiating to both buttocks, to the right
lateral thigh, and into the right posterior calf. The pain began after he lifted a heavy object at work.
Since that occasion, he had continued to have moderately dull, aching back pain with intermittent
acute exacerbations. He denied weakness, paresthesias, or numbness in the lower extremities.
Physical examination demonstrated tenderness to palpation over the lumbosacral junction without
spasm. Both forward bending and extension increased the low back pain. He exhibited no increase in
pain with straight-leg raising. After failed conservative care, EMG, MRI, and awake diskography
were performed; all results were normal. Diagnostic facet blocks were performed with 0.5%
bupivacaine and a corticosteroid at L4-5 and L5-S1, which resulted in excellent short-term relief.
Subsequently, the patient underwent chemical rhizolysis with phenol. which resulted in more
prolonged pain relief.
Discussion
This patient exhibited a sclerotomal pain pattern mediated through the L-5 segment that is similar
to that of the patient in Case 1. However, because the painful impulse
was
generated via the posterior
primary ramus, there were noticeable differences. As there was no neural compression, paresthesias
were not present This accounts for the normal radiographic evaluations.
CONCLUSION
There are always difficulties in the evaluation of the patient with spinal problems. The spine is uniquely
complicated. appearing to contain a vast sensory apparatus equipped with afferent and efferent neural modulators
that we are only recently beginning to understand. Several conclusions are supported by our review of embryology,
neuroanatomy, and physiology as they pertain to pain patterns of the lumbar segment First, pain patterns seem to
depend upon the structure involved, its innervation; and its embryologic development Second, referred pain may
not always be caused by direct nerve-root
in
volvement, as with disk lesions, but can arise from other structures that
lie in proximity to the neural canal (e.g., facets and ligaments). The locus of perception by the sensory cortex
depends in part on the phenomenon of convergence, as sensory input from a variety of receptors relay through the
spinothalamic tract. The extent and intensity of the pain depends on the degree of involvement of the segmental
parts.
An evaluation of low back pain that considers the dermatomal, myotomal, and sclerotomal patterns plays an
important role in pain
as
sessment and the choice of diagnostic testing, especially when few significant physical
signs are present. Although these pain patterns are still somewhat ambiguous due to their significant overlap, it is
possible to develop a diagnostic strategy that will enable more precise identification of the painful segment, as well
as of the region from which the injury arises. It is through careful evaluation of the patient via a thorough history
and physical examination coupled with various supportive diagnostic tests that we may eventually sort through
the maze of complex spinal symptoms to arrive
at
an appropriate therapeutic strategy.
ORTHOPAEDIC REVIEW
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ORIGINAL ILLUSTRATIONS:
Figure 1.
Figure 2.
Figure 3.
Figure 4.
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Figure 5.
Figure 6.