Sauropod Vertebra Picture of the Week

The image I put together explaining the new discovery. Modified from Staples et al. (2019: fig. 6).

Today sees the publication of a new paper, “Cutaneous branch of the obturator nerve extending to the medial ankle and foot: a report of two cadaveric cases,” by Brittany Staples, Edward Ennedy, Tae Kim, Steven Nguyen, Andrew Shore, Thomas Vu, Jonathan Labovitz, and yours truly. I’m excited for two reasons: first, the paper reports some genuinely new human gross anatomy, which happens surprisingly often but still isn’t an everyday occurrence, and second, the first six authors are my former students. This isn’t my discovery, it’s theirs. But I’m still going to yap about it.

When the obturator nerve won’t stay in its lane

Your skin is innervated by cutaneous nerves, which relay sensations of touch, pressure, vibration, temperature, and pain to your central nervous system, and carry autonomic (involuntary) fibers to your sweat and sebaceous glands and the arrector pili muscles that raise and lower your hairs (as when we get goosebumps). Every inch of your skin lies in the domain of one cutaneous nerve or another. Known boundaries between cutaneous branches of different nerves are approximate, both because they vary from person to person, and because the territories of the nerves themselves interdigitate and overlap at very fine scales. That said, aside from complex areas where the domains of multiple nerves intersect (like the groin), most body regions get their cutaneous innervation from just one nerve.

The obturator nerve arises from the spinal levels of the 2nd-4th lumbar vertebrae (L2-L4), exits the pelvis through the obturator canal behind the superior ramus of the pubis, and innervates the adductor muscles of the medial compartment of the thigh. The cutaneous branch of the obturator nerve typically innervates a variable but limited patch of skin on the inner thigh. Here’s a diagram from Gray’s Anatomy, 40th edition, showing the common cutaneous distribution of the obturator nerve (Standring et al. 2008 fig. 79.17, modified):

In rare cases, however, the obturator nerve doesn’t stay in the thigh. I was teaching in the gross anatomy lab in the fall of 2013 when one of our podiatry students, Brittany Staples, called me over to her table. We were skinning the thigh and leg that day, and in her assigned cadaver, Brittany had found a nerve from the medial thigh running all the way down to the inner side of the ankle and foot.

I didn’t immediately freak out, because everyone has a nerve from the thigh running down to the inner side of the ankle and foot: the saphenous branch of the femoral nerve, which comes out of the anterior thigh (also highlighted in the above image). But when we traced back Brittany’s nerve, it wasn’t coming from the femoral nerve. Instead, it was coming from the anterior division of the obturator nerve, right behind the adductor longus muscle (when people do the splits, this is the muscle that makes a visible ridge from the inner thigh to the groin). We carefully cleaned and photographed the nerve, and then we hit the books. Our first question: was this a known variation, or had Brittany discovered something new in the annals of human anatomy?

Standing on the shoulders of giants

Virtually all introductory anatomy textbooks show the obturator nerve only going to the thigh. But a little digging turned up Bouaziz et al. (2002), which in turn reproduced a figure from Rouvière and Delmas (1973), a French textbook, which showed the obturator nerve passing the knee and innervating part of the calf. That was at least an advance on what we knew starting out. We found a similar written description in Sunderland (1968).

Bouaziz et al. (2002: fig. 1)

Then we discovered Bardeen (1906), a magnificent and magisterial work 130 pages in length. Titled, “Development and variation of the nerves and the musculature of the inferior extremity and of the neighboring regions of the trunk in man”, the paper delivers on its impressive title. Bardeen (1906: 285 and 317) reported than in 22 out of 80 cadavers, the cutaneous branch of the obturator nerve (CBO) reached the knee; in 10 of those cases it could be traced at least to the middle third of the calf; and in one case it reached “nearly to ankle”. Bardeen also commented on the difficulty of tracing out the limits of this tiny nerve (p. 285):

“How constant the cutaneous branch of the obturator may be I have been unable satisfactorily to determine. Students dissecting frequently fail to find it. Owing to the fact that this may often be due to its small size the negative records cannot safely be used in making up statistics.”

All of us on the paper can back up Bardeen’s comments here: by the time they reach the skin, cutaneous nerves might be as big around as a pencil lead, or a strand of dental floss, or a human hair, but they won’t be much bigger. Sometimes they run just under the skin, sometimes down in the subcutaneous fat and fascia (with vanishingly small extensions spidering out to the underside of the skin), always variable in their courses and often devilishly hard to find, preserve, and trace.

If there is a prior report in the literature of a CBO passing the ankle, we haven’t found it, and neither have the numerous podiatric physicians who commented on the manuscript before we submitted, nor the reviewers and editors of the Journal of Foot & Ankle Surgery. I feel pretty safe saying that this is truly new (and if you know otherwise, please let me know in the comments!).

The second case, and the long silence

Every year since 2013, I’ve warned our medical and podiatric students to be on the lookout for anomalously long branches of the obturator nerve. The very next year, a group of summer anatomy students found a second example (they’re authors 2-6 on the paper). Since then, nada, in over 200 more bodies as of this summer. Either we got crazy lucky to find two examples in back to back years, or long CBOs are more common than we think, just really hard to find and identify. More on that in a minute.

A quick aside: we didn’t deliberately hold up the paper while we were looking for more examples, we’ve all just been busy. Brittany and the other student authors were occupied with passing med school and their board exams, surviving clinical rotations, and applying to residency programs. I’m happy to say “were occupied” with all those things because they’re all graduated now, and in residency training. Anyway, that’s why the paper had a 5-year gestation: med school doesn’t leave a lot of time for research and writing. Kudos to Brittany for giving all of us regular kicks to keep things moving along. In every sense, the paper would not exist without her skill and dedication.

So what’s going on here?

There are two sides to this: what happened to produce the variants we found in 2013 and 2014, and why variants like that escaped detection for so long, and I’ll tackle them in that order.

We found both of the long CBOs in the territory normally occupied by the saphenous branch of the femoral nerve. The saphenous nerve is so named because it runs along the great saphenous vein, the major superficial vein of the medial leg and thigh. Sometimes the saphenous nerve has only a single main trunk, but more commonly it splits into two parallel branches, one on either side of the saphenous vein, as illustrated here by Wilmot and Evans (2013: fig. 3):

In both of our cases, the saphenous branch of the femoral nerve was present, but it only had one branch, in front of the big vein, and the long CBO ran behind the vein, in the place usually occupied by the posterior branch of the saphenous nerve. In effect, the posterior part of the saphenous branch of the femoral nerve had been replaced by a sort of saphenous branch of the obturator nerve. This has interesting implications.

Suppose you were a surgeon, harvesting the distal portion of the saphenous vein for a coronary artery bypass graft, and you saw two nerves accompanying the vein, one in front and one behind. You would probably assume that both branches arose from the femoral nerve, because that is what happens most commonly. But if the posterior branch actually came from the obturator nerve, you’d have no way of knowing that, without tracing the nerve back to its origin in the inner thigh. The watchwords in surgery these days are “minimally invasive” and “patient outcomes” — smaller openings in the body mean less pain, fewer complications, faster recoveries, and happier patients. So surgeons aren’t going to flay patients open from ankle to groin just to chase down a nerve that might be coming from the normal place after all.

If you only get to look inside the box, these two things look the same.

We suspect that long CBOs may be fairly common, just hard to recognize, because who is going to find them? Medical students dissecting human cadavers have the opportunity to trace long cutaneous nerves back to their origins, but since it’s the students’ first time cutting, they usually haven’t yet developed the experience to recognize weird versions of tiny nerves, nor the skill to preserve them. Surgeons have the experience and the skill, but not the opportunity, because they can’t go around filleting their patients to see where all the nerves come from. So long CBOs probably fall into a perceptual blind spot, in which almost no-one who cuts on human bodies has both the opportunity to find them, and the skill to preserve them — my former students excepted (he said with no small helping of pride).

That’s pretty darned interesting, and it makes me wonder what other perceptual blind spots are out there, in both anatomy and paleontology. I know of at least one: the true nature and extent of the fluid-filled interstitial tissues that pervade our bodies (and those of all other vertebrates at least) were not fully appreciated until just last year, because the first step in the production of most histological slides is to dehydrate the tissues, which collapses the fluid-filled spaces and makes the interstitium look like regular connective tissue (Benias et al. 2018). That is a spooky kind of observer effect, and it makes me wonder what else we’re missing because of the ways we choose — or are constrained — to look.

What next?

What’s the fallout from this study? For me, two things. First — obviously — we’re going to keep looking for more examples of long CBOs, and for other similar cases in which one nerve may have been replaced by its neighbor. This is more than trivia. Knowing which nerves to expect and where to find them is important, not only for surgeons but also for anaesthetists and pain management physicians doing nerve blocks. The decks may be stacked against med students for some of these discoveries, but clearly “difficult” does not mean “impossible” or I’d have nothing to write about. Lightning has already struck twice, so I’ll keep flying this particular kite.

Second, this case, a few other odd things we’ve found in the lab over the years, and other recently-reported discoveries in human anatomy have caused me to wonder: could we formulate predictive maxims to help guide future discoveries in human anatomy, or in anatomy full stop? I think so, and provided my abstract is accepted, I’ll be presenting on that topic at SVPCA in a couple of months. More on that in due time.

Finally — and this cannot be overstated — without the keen eyes, skilled hands, sharp minds, and hard work of the student authors, there would be no discovery and no paper. So congratulations to Brittany, Edward, Tae, Steven, Andrew, and Thomas. Or as I’m happy to address them now, Drs. Staples, Ennedy, Kim, Nguyen, Shore, and Vu. Y’all done good. Keep it up.

References

• Bardeen, C.R. 1906. Development and variation of the nerves and the musculature of the inferior extremity and of the neighboring regions of the trunk in man. Developmental Dynamics 6(1):259-390.
• Benias, P.C., Wells, R.G., Sackey-Aboagye, B., Klavan, H., Reidy, J., Buonocore, D., Miranda, M., Kornacki, S., Wayne, M., Carr-Locke, D.L. and Theise, N.D. 2018. Structure and distribution of an unrecognized interstitium in human tissues. Scientific Reports, 8:4947.
• Bouaziz, H., Vial, F., Jochum, D., Macalou, D., Heck, M., Meuret, P., Braun, M., and Laxenaire, M.C. 2002. An evaluation of the cutaneous distribution after obturator nerve block. Anesthesia & Analgesia 94(2):445-449.
• Rouvière, H., and Delmas, A. 1973. Anatomie humaine, descriptive, topographique et fonctionnelle: tome 3—membres-système nerveux central, ed 11, Masson, Paris.
• Standring, S. (ed.) 2008. Gray’s Anatomy: The Anatomical Basis of Clinical Practice, 41st ed, Elsevier Health Sciences, London.
• Staples, B., Ennedy, E., Kim, T., Nguyen, S., Shore, A., Vu, T., Labovitz, J., and Wedel, M. 2019. Cutaneous branch of the obturator nerve extending to the medial ankle and foot: a report of two cadaveric cases. Journal of Foot & Ankle Surgery, advance online publication.
• Sunderland, S. 1968. Nerves and Nerve Injuries. Churchill Livingstone, Edinburgh.
• Wilmot, V.V., and Evans, D.J.R. 2013. Categorizing the distribution of the saphenous nerve in relation to the great saphenous vein. Clinical Anatomy 26(4):531-536.