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.
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Here’s my face.

I went to the dentists’ office recently for a regular checkup and cleaning, and when my dentist learned that I taught human anatomy, he volunteered to send me a high-res copy of my panoramic x-ray. I couldn’t think of any plausible scenario wherein someone could use it for evil, and it has lots of cool stuff in it besides teeth, so decided to post it so I could yakk about it.

First things first: my teeth are in pretty good shape. I had to have my wisdom teeth (3rd molars) pulled back in 2009, and my upper 1st molar on the left has a root canal and a porcelain crown, which stands out bright white on the radiograph. Everyone else is present and looking good. If it’s been a while since you’ve covered this, the full human dentition consists of 2 incisors, 1 canine, 2 premolars, and 3 molars on each side, top and bottom, for a total of 32 teeth. Because I’ve had all four 3rd molars removed, I’m down to 28.

I could go on and on about the cool stuff in this image. Here are 12 things that stand out:

  1. The mandibular condyle, which is the articular end of the mandible that fits into the mandibular fossa, a shallow socket on the inferior surface of the temporal bone, to form the temporomandibular joint (TMJ). There’s an articular disk made of fibrocartilage inside the joint, which separates it into two fluid-filled spaces, one against the condyle and one against the fossa. This allows us to do all kinds of wacky stuff with our lower jaws besides simply opening and closing them, such as slide the jaw fore and aft or side to side. This is a strong contrast to most carnivores, which bite down hard and therefore need a jaw joint that works as a pure hinge. See this post for pictures and discussion of the jaw joint in a bear skull.
  2. The coronoid process of the mandible, which is a muscle attachment site. A few fibers of the masseter and buccinator muscles can encroach onto the coronoid process, but mostly it is buried in the temporalis, one of the primary jaw-closing muscles. Put your fingers on the side of your head a little above and in front of your ear and bite down. That muscle you feel bulging outward is the temporalis. Back in the 1960s, Melvin Moss (1968) discovered that if he removed the temporalis muscles from newborn rats, the coronoid processes would fail to develop. Moss’s ambition was to discover the quanta of anatomy, which in his view were “functional matrices” – finite sets of soft tissues related by development and function, which might contain “skeletal units” that grew because of the morphogenetic demands of the functional matrices. His tagline was, “Functional matrices evolve, skeletal units respond”. Not all of Moss’s ideas have aged well in light of what we now know about the genetic underpinnings of skeletal development, but he wasn’t completely wrong, either, and functional matrix theory is still an interesting and frequently productive way to think about the interrelationships of bones and soft tissues. For more horrifying/enlightening Moss experiments on baby rats, see this post.
  3. The mandibular angle, which is another muscle attachment. The medial pterygoid muscle attaches to the medial surface, and the masseter attaches laterally. You can feel this, too, by putting your fingers over your mandibular angle and biting down – that’s the masseter you feel bulging outward. Note that the angle flares downward and outward on either side of my jaw. This flaring of the angle tends to be more pronounced in males than in females, and it is one of many features that forensic anthropologists (like the one I belong to) take into account when attempting to determine biological sex from human skeletal remains. Like most sexually dimorphic features of the skeleton, this is a tendency along a spectrum of variation rather than a binary yes/no thing. There are women with flared jaw angles (Courtney Thorne-Smith, probably) and men with slender mandibles, so you wouldn’t want to sex a skeleton by that feature alone.
  4. The mandibular canal, a tubular channel through the mandible that houses the inferior alveolar artery, vein, and nerve. This neurovascular bundle provides innervation and blood supply to the tooth-bearing part of the mandible and to the teeth themselves, and emerges through the mental foramen to provide sensory innervation and blood supply to the chin.
  5. The upper surface of the hard palate, formed by the palatine process of the maxilla anteriorly and by the palatine bones posteriorly. The palate is the roof of the mouth and the floor of the nasal airways.
  6. The median septum of the nasal cavity, formed by cartilage anteriorly, the perpendicular plate of the ethmoid bone superiorly, and the vomer posteriorly and inferiorly.
  7. The blue lines are the inferior margins of my maxillary sinuses – air-filled spaces created when pneumatic diverticula of the nasal cavity hollow out the maxillae. You have these, too, as well as air spaces in your frontal, ethmoid, sphenoid, and temporal bones. It looks like many of the roots of my upper molars stick up into my maxillary sinuses. This is not an illusion, as shown below.
  8. When I had the root canal on my left upper 2nd molar, the endodontist filled the pulp cavities of the tooth roots with gutta-percha, a rigid natural latex made from the sap of the tree Palaquium gutta. Gutta-percha is bioinert, so it makes a good filling material (it was also used to insulate transoceanic telegraph cables), and it’s radiopaque, which allows endodontists to confirm that the cavities have been filled completely. The other teeth show the typical structure of a dense enamel crown, less dense dentine forming the bulk of the tooth, and radiolucent pulp cavities containing blood vessels and nerves.
  9. This is the rubber bit I gripped with my incisors to keep my teeth apart and my head motionless while the CT machine rotated around me to make the scan. Not that cool in a science sense, but I figured it deserved a label.
  10. Note that the roots of the canines go farther into the jaws than those of the other teeth. This is true for all four canines, it’s just easiest to see with this one. This is a pretty standard mammalian thing, for taxa that still have canines – they tend to be big and mechanically important, so they have deep roots. Even though our canines are absolutely and proportionally much smaller than those in the other great apes, we can still see traces of their earlier importance, like these deep roots.
  11. In places you can see the trabecular internal structure of my mandible clearly. As someone who geeks out pretty much anytime I get a look inside a bone, this tickled me.
  12. The remains of an alveolus or tooth socket. I had my 3rd molars out almost a decade ago, and by now the sockets will have mostly filled in with new trabecular bone. But you can still see the ghostly outline of at least this one – a sort of morphogenetic trace fossil buried inside my mandible. I assume that in another decade or two this will have disappeared through regular bone remodeling.

Here’s a closeup of my left upper 2nd premolar and first two (and only remaining) molars. The gutta-percha filling the pulp cavities of the three roots of the 1st molar is obvious. The disparity in root length is mostly illusory – this was an oblique shot and the two ‘short’ roots are foreshortened.

Here’s the same image with the roots of the 2nd molar traced in pink, and the inferior margin of the maxillary sinus traced in blue. It’s not that uncommon for upper molar roots to stick up into the maxillary sinuses. That was true of my 3rd molars as well, and when I had them taken out, the endodontist had to put stitches into my gums to close the holes. Otherwise I would have had open connections between my oral cavity and maxillary sinuses, which would have sucked and been dangerous. Nasal mucus in the maxillary sinuses could have drained into my mouth, and food I was chewing could have been forced up into the sinuses, where it would have decomposed and caused a truly vile sinus infection.

In a developmental sense, it’s not that the roots of the teeth grow upward into the sinuses, it’s that the sinuses grow downward, eroding the bone around the roots of the teeth. This happens well after the teeth are done forming – the sinuses continue to expand as long as the skull is growing, and they retain the potential to remodel the surrounding bone for as long as we live. Even in cases like mine where the roots of the molars stick up into the sinuses, the tooth roots are still covered by soft tissue, including branches of the superior alveolar artery, vein, and nerve that enter the pulp cavities of the tooth roots through foramina at their tips.

If you ask your dentist for copies of your own dental x-rays, you’ll probably get them. If you do, have fun exploring the weird territory inside your head.

Reference

  • Moss, M. L. (1968). A theoretical analysis of the functional matrix. Acta Biotheoretica, 18(1), 195-202.

 

Internal Iliac Arteries - MJW 2011

Here’s a thing I put together to help my students understand the many branches of the internal iliac artery in humans. In the image above, we’re looking in superomedial view into the right half of the sacrum and pelvis. Bones are white, ligaments blue, the piriformis muscle sort of meat-colored, and arteries red (for a tour of the pelvis identifying all of this stuff, see my pelvic foramina slideshow). At the top is a big inverted Y-shape: the common iliac arteries branching from the abdominal aorta, which continues on, much reduced, as the median sacral artery. The right common iliac artery is shown bifurcating into the external iliac artery, which continues on out of the pelvis to become the femoral artery, and the internal iliac artery, source of much fear and doubt.

The first thing to understand is that any particular branching pattern of the internal iliac arteries, whether in an anatomical altas, a lecture, revealed in a dream, or even in your own body, will probably have no bearing whatsoever on the branching pattern in the next person you encounter, alive or dead. Furthermore, the variation between right and left in a single person can be as great as that among different people. The branches to pelvic viscera are particularly fiendish; they sometimes travel far into the pelvis as a common trunk and then “starburst” near their target organs, making identification almost impossible. Do not waste your time trying to memorize any particular branching sequence. Instead, concentrate on matching the arteries to their targets; you will discover the identities of the branches by seeing where they are going, not the order in which they branch.

There are typically 10 named branches of the internal iliac artery. Authorities quibble on the details, as we’ll see in a moment, but if you know these 10, you’ll be fine for almost any conceivable purpose. A simple scheme of my own devising for remembering them is 2-4-4:

TWO to the back body wall:

  1. iliolumbar A—may arise from external or common iliac AA; sometimes double
  2. lateral sacral A—note branches to anterior sacral foramina and anastomoses with median sacral A

FOUR leaving the pelvis entirely:

  1. obturator A—often arises from the external iliac A instead, exits pelvis through obturator canal
  2. superior gluteal A—exits pelvis through suprapiriform foramen
  3. inferior gluteal A—exits pelvis through infrapiriform foramen, with internal pudendal A
  4. internal pudendal A—exits pelvis through infrapiriform foramen, with inferior gluteal A

FOUR to pelvic viscera:

  1. superior vesical A—usually the dominant artery of the anterior trunk, this is the patent part of the obliterated umbilical artery, which survives as the medial umbilical ligament
  2. inferior vesical A (males) / vaginal A (females)—may branch off uterine A (females) or superior vesical A (both)
  3. uterine A (females)—major artery to uterus, approaches laterally within the broad ligament
    A to ductus deferens (males)—extremely small and difficult to trace
  4. middle rectal A—usually the most inferior branch of the entire internal iliac tree (at least inside the pelvis)

My way to explain those last four is to extend my index finger and say, “Everybody has to pee, so up front we have superior vesical.” Then extend my pinky and say, “And everyone has to poop, so in back we have middle rectal.” Then extend digits three and four and explain that the identity of the middle two arteries varies between the sexes (but that the inferior vesical artery of males and the vaginal artery of females are basically the same vessel).

There is a LOT of variation in the descriptions of the internal iliac artery branches among different sources — almost as much variation as there is in the arteries themselves.

  • ​The Thieme Atlas of Anatomy, 2nd Ed (Gilroy et al. 2009), Table 19.1 on p. 254, includes the inferior vesical artery for both sexes. The artery to ductus deferens is listed as a branch of the superior vesical artery, and the uterine and vaginal arteries are listed separately, bringing the total for females to 11.
  • Clinically Oriented Anatomy, 7th Ed (Moore et al. 2013), Table 3.4 and pp. 350-355, lists the 10 branches I went through above. Moore et al. explicitly say that the vaginal artery is the female homolog of the inferior vesical artery (p. 351).
  • Gray’s Anatomy, 40th Ed (Standring et al. 2008), pp. 1085-1089, splits the difference. The artery to ductus deferens is not listed; instead, the ductus deferens is said to be supplied by the inferior vesical A (in contrast to Thieme, which has it is supplied by the superior vesical A). Both the vaginal and inferior vesical arteries are listed, but the vaginal artery is said to frequently replace the inferior vesical artery.

The upshot is that pretty much all of these sources agree on how the blood is getting distributed, there are just some minor differences over what we call certain vessels. I have never personally seen a dissection detailed enough to allow an interior vesical artery to be recognized separately from the vaginal artery — the vagina lies so close behind the bladder that whatever you call the artery that runs lateral to them, it could easily be supplying both structures, and probably does. As far as I’m concerned, the inferior vesical artery in males and the vaginal artery in females are the same artery, in that they both supply the inferior portion of the bladder. I think it’s just a historical hiccup that we call them by different names, possibly perpetrated by smelly, lonely, vagina-obsessed men of centuries past.

A final note, added in revision: some sources refer to two trunks or divisions of the internal iliac artery: a posterior trunk that gives rise to the iliolumbar, lateral sacral, and superior gluteal arteries, and an anterior trunk that gives rise to everything else. If that’s what your professor tells you, smile and nod and keep your heretical thoughts to yourself. Personally, I regard the notion of trunks of the internal iliac artery alongside phlogiston, luminiferous aether, and snorkeling sauropods, as romantic nonsense at best. I have seen an obturator artery arise from a superior gluteal artery and a pudendal artery arise from a superior vesical artery. In a world where variants like those can and do turn up frequently, the stability and reason implied by regular trunks is illusory.

References

  • Gilroy, A., MacPherson, B., and Ross, L. (eds.) 2009. Atlas of Anatomy, 2nd ed. Thieme, Stuttgart.
  • Moore, K.L., Dalley, A.F., and Agur, A.M. 2013. Clincially Oriented Anatomy, 7th ed. Lippincott Williams & Wilkins, Philadelphia.
  • Standring, S. 2008. Gray’s Anatomy, 40 ed. Churchill Livingstone, London.