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Journal of Equine Veterinary Science 84 (2020) 102847

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Journal of Equine Veterinary Science

journal homepage: www.j -evs.com

Case Report

Rare Finding of a Full Nuchal Ligament Lamellae With AttachmentPoints From C2eC7 in One Australian Stock Horse

Sharon May-Davis a, *, Zefanja Vermeulen b, Robert Hunter a, Wendy Brown a

a Canine and Equine Research Group, University of New England, Armidale, New South Wales, Australiab Equine Studies, Dussen, the Netherlands

a r t i c l e i n f o

Article history:Received 4 September 2019Received in revised form21 October 2019Accepted 8 November 2019Available online 14 November 2019

Keywords:Australian stock horseWalerNuchal ligament lamellaeCervical vertebraeDutch konikIsolated breeds

Animal welfare/Ethical statement: No horses were euthis case report. The horses were chiefly sourced frposely by the owner or euthanized on a property befConflict of interest statement: The authors declare the

in the preparation or presentation of this original cas* Corresponding author at: Canine and Equine Resea

England, Armidale, New South Wales, Australia.E-mail address: maydavis@bigpond.com (S. May-D

https://doi.org/10.1016/j.jevs.2019.1028470737-0806/© 2019 Elsevier Inc. All rights reserved.

a b s t r a c t

For over 200 years, equine anatomic literature has chiefly portrayed the attachment points of the nuchalligament lamellae (NLL) from the second to the seventh cervical vertebrae (C2eC7). However, recentstudies have shown that the modern domestic horse, Equus caballus, primarily exhibits the attachmentspoints from C2eC5. Here we present the rare finding of a complete NLL attached from C2eC7 in oneAustralian Stock Horse (ASH) and discuss the potential implications of these findings. Previously, thistrait has only been confirmed among close descendants of Equus ferus ferus; namely the primitive DutchKonik and Bosnian Mountain Horse. The examination of the NLL attachment points in 55 unrelatedhorses of mixed breeds revealed that 52 horses had attachments from C2eC5; 1 horse (Welsh Cob) hadattachments from C2eC6; and only 2 horses (ASH and Dutch Konik) presented with a complete NLLattached from C2eC7. In light of earlier findings that suggest this loss of NLL attachment at C6 and C7occurred after domestication, a possible explanation for this finding in 1 ASH is that it is a remnant traitfrom the founder population of Waler horses that contributed to the early development of the ASH breed.The reported rare occurrence of a complete NLL (C2eC7) in a modern domesticated equine (ASH) sug-gests that there may be other individuals expressing this unique trait, providing opportunity for itspreservation.

© 2019 Elsevier Inc. All rights reserved.

1. Introduction

According to the available anatomic literature dating back to1777, the equine nuchal ligament comprises the nuchal ligamentfunicular cord (NLFC) and the nuchal ligament lamellae (NLL)[1e10]. The NLL consists of 2 sheets of elastic fibers originating fromthe second to third thoracic vertebrae and the NLFC; thereafter, thefibers traverse cranioventrally before inserting on the dorsal spinesof C2eC7 or on occasion C2eC6 [1e10]. Yet, two recent morpho-logical studies contradicted the existing literature after examining23 breeds of Equus caballus (n¼ 128) and finding a complete NLL inonly 3 individuals: 2 Dutch Koniks (DK; a primitive breed) and 1

thanized for the purpose ofom abattoirs sent there pur-ore burial for health reasons.y have no conflict of intereste report.rch Group, University of New

avis).

Bosnian Mountain Horse (BMH) [11,12]. The NLL attachment pointsranged from C2eC5 (n ¼ 123), C2eC6 (n ¼ 2), and C2eC7 (n ¼ 3)(Fig. 1) [12].

Although cadaveric details were lacking, pre-1900s anatomicliterature consistently depicted the NLL attachment points fromC2eC7 [1e10]. By comparison, the two recent morphologicalstudies contradict pre-1900s literature, and furthermore, theyprovide details of the specimens including their geographical di-versity [11,12]. It is not feasible to demonstrate the NLL attachmentspoints in all 540 breeds of E. caballus; however, it is conceivable thata domestic breed or individual in domestic E. caballus could stillretain the NLL from C2eC7, given the frequency of representation inpre-1900s anatomic literature [1e10].

Notably, the two cited studies reported the DK and BMH werethe only breeds in the study with a complete NLL from C2eC7closely descended from Equus ferus ferus that exhibited a completeNLL from C2eC7 in the last 200 years, before it became extinct inthe early 1900s [11e14]. The remaining breeds covered a longerancestral history of over 4000 years, most of which were undervarious forms of domestication [15,16].

Fig. 1. Examples of the attachment points of the NLL in domestic horse. (A) Shetland pony C2eC5. (B) Welsh Cob C2eC6. (C) Bosnian Mountain Horse C2eC7. C2eC5, the second tothe fifth cervical vertebrae; C2eC6, the second to the sixth cervical vertebrae; C2eC7, the second to the seventh cervical vertebrae; NLL, nuchal ligament lamellae.

S. May-Davis et al. / Journal of Equine Veterinary Science 84 (2020) 1028472

Therefore, this case report discusses the findings of a domesti-cally bred E. caballus (Australian Stock Horse [ASH]) presentingwith a fully functional NLL from C2eC7. Furthermore, the findingsfrom the examination of the NLL attachment points in 55 unrelatedhorses of mixed breeds provides further evidence in relation to therarity of this trait.

2. Materials and Methods

2.1. Ethical Statement

No horses were euthanized for the purpose of this study and allobservations were obtained postmortem.

2.2. Geographic Location

Horses were accessed from 6 countries: Australia (n ¼ 22), theNetherlands (n¼ 19), New Zealand (n¼ 6), United Kingdom (n¼ 5),Sweden (n ¼ 2), and Japan (n ¼ 1).

2.3. Dissections

The dissections revealing the NLL for examination were per-formed by 2 of the authors, Sharon May-Davis and Zefanja Ver-meulen as per previously documented protocols [12].

Table 1Observations of the attachment points of the NLL to the cervical vertebrae in 55 horses

Breed (age) n GenderMale/Female

1. Thoroughbred (8e22) 12 8 M/4 F2. Warmblood (9e18) 19 8 M/11 F3. Crossbred (7e15) 7 3 M/4 F4. Standardbred (13e22) 2 2 M5. Aust. Stock Horse (4.5e22) 3 2 M/1 F6. Fjord (4.5e20) 3 3 F7. Paint (13) 1 1 M8. Quarter Horse (10) 1 1 M9. Irish Sport Horse (5) 1 1 F10. Appaloosa 1 1 F11. Welsh Cob (18) 1 1 F12. Friesian 1 1 M13. Hunter (13) 1 1 M14. Shetland (5) 1 1 F15. Dutch Konik (2 d) 1 1 FTotal 55 27 M/28 F

Abbreviations: C2eC5, the second to the fifth cervical vertebrae; C2eC6, the second to thnuchal ligament lamellae.

Animal details including breed, age, and gender were recorded;and the presence or absence of the NLL attachments to the cervicalvertebrae from C2eC7 were documented (Table 1).

3. Results

The examination of the NLL in 55 horses revealed 52 with NLLattachments from C2eC5 and 1 with NLL attachments from C2eC6.Only two animals revealed the NLL attachments from C2eC7, theprimitive DKwith close E. ferus ferus heritage and the domestic ASH(Fig. 2). The NLL fibers on C6 and C7 in the ASH were comparativelyless robust and fewer than those for each digitation from C2eC5.

The presentation of the NLL in the ASH revealed similar struc-tural morphology to the DK and BMH including the spinalis dorsimuscle attaching to the digitations of the NLL from C6eC7 [12].

4. Discussion

Our findings of 52/54 modern domestically bred horses pre-senting with NLL attachments from C2eC5 supports that of recentstudies, where a further 133/135 displayed the same traits [11,12].Suggesting this morphological presentation of the NLL from C2eC5is normal for the species E. caballus. This is contrary to the previ-ously acknowledged literature referring to the attachment points asC2eC7, or on occasion C2eC6 [1e10]. Furthermore, the primitive

revealed by postmortem examination.

C2eC5 C2eC6 C2eC7

1219722 131111

1111

152 1 2

e sixth cervical vertebrae; C2eC7, the second to the seventh cervical vertebrae; NLL,

Fig. 2. Dissection revealed NLL attachments points from C2eC7 in the ASH. ASH, Australian Stock Horse; NLL, nuchal ligament lamellae; C2eC7, the second to the seventh cervicalvertebrae.

S. May-Davis et al. / Journal of Equine Veterinary Science 84 (2020) 102847 3

DK in this case report remained consistent with recent studies,implying the C2eC7 trait was present in its ancestry, notably E. ferusferus [11e13]. However, this does not explain why one ASHexpressed this trait; the first report of a complete NLL attached fromC2eC7 in a modern domestic breed in recent times.

The ASH traces its ancestry to a type of horse known as the“Waler”, a crossbred derived from over 10 breeds of small, light, andheavy horses [15,16]. The Waler has demonstrated a high incidenceof rare allelic diversity, acquired from the variety of breeds thatcontributed to its origins [17]. This may provide one explanation forthe rare finding of C2eC7 attachments as observed in the ASHexamined in this study. Today, the true Waler is a rare sight andalthough an established breed by the 1830s, mechanization soonreplaced its usefulness 130 years later. By 1971, Australian breederswishing to create a versatile cattle horse used existing Walerbloodlines to establish the ASH. Before the end of the 1900s, theintroduction of Thoroughbred and Quarter Horse bloodlinesheavily diluted the breed [15,16].

Previous reports of a single anatomic variation remainingconsistent within a population because of isolation and closedbreeding programs already exist [18,19]. Even though there is adisparity between equine NLL anatomic literature and recentstudies, the etiology to its disappearance on C6 and C7 in thedomesticate is unclear. However, the appearance of a complete NLLin numerous pre-1900s anatomic literature suggests it was presentand accordingly, its disappearance on C6 and C7 in the domesticatepotentially occurred within the last 200 years. This indicates iso-lated populations may still retain a complete NLL, where this reportis an example.

The relevance of the disappearing NLL on C6 and C7 may beassociated with the increase in caudal cervical osteoarthritis (OA)and especially, the now-recognized limitations it places on per-formance in domestic horses [20e23]. Two previous studiespostulated this very connection between the decrease in functionalNLL and the increase in caudal cervical OA; although to date anexamination of this hypothesis has not been forthcoming [11,12].Furthermore, examination of the NLL from C2eC7 in the live horsehas not been determined but will assist in identifying this trait insmall populations without removing allelic diversity. Therefore,isolated populations before 1900s may still retain the NLL attach-ment points from C2eC7, and as such we suggest this uniquenessrequires preservation.

5. Conclusion

With two recent studies describing the attachments points ofthe NLL in modern domestic horse as predominantly C2eC5, this

finding of NLL attachments from C2eC7 in an ASH is rare. Therefore,we suggest that isolated populations may still preserve this traitand recommend further investigation.

Acknowledgments

Sharon May-Davis is currently undertaking a PhD at the Uni-versity of New England. This research was funded by the AustralianGovernment Research Training Program.

The authors wish to thank Paardenslachterij van de Veen,Havenstraat 3, 3861VS Nijkerk gld Holland, the Netherlands, for theuse of their facility and cadaver preparation; Equine Studies, theNetherlands, for logistical assistance and resources; Tanja De Boodefrom Freenature for organizing a Dutch Konik horse; the AustralianCollege of Equine Podiotherapy for the use of its facilities; and tothose authors/editors/publishers of those articles, journals, andbooks cited in this article.

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