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Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital
G Model IJPP-59; No. of Pages 6
ARTICLE IN PRESS International Journal of Paleopathology xxx (2012) xxx–xxx
Contents lists available at SciVerse ScienceDirect
International Journal of Paleopathology journal homepage: www.elsevier.com/locate/ijpp
Case Study
Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital Brooklynne “Tyr” Fothergill a,∗ , Richard Thomas a , James Morris b a b
School of Archaeology and Ancient History, University of Leicester, Leicester LE1 7RH, UK Museum of London Archaeology, Mortimer Wheeler House, London N1 7ED, UK
a r t i c l e
i n f o
Article history: Received 30 May 2012 Received in revised form 9 October 2012 Accepted 10 October 2012 Keywords: Turkey Meleagris gallopavo Tibial dyschondroplasia Tibiotarsus Improvement
a b s t r a c t In this paper we call attention to the first recorded archaeological examples of avian tibial dyschondroplasia. This condition is identified in three turkey (Meleagris gallopavo L. 1758) tibiotarsi from the Royal London Hospital site in London, UK. The lesions are described, radiographed and differentially diagnosed. Recognition of this condition testifies to the pace of breed development in the 19th-century and the unintended health consequences of ‘improvement’. © 2012 Elsevier Inc. All rights reserved.
1. Introduction Tibial dyschondroplasia is one of the most frequently observed skeletal diseases in domestic birds. It commonly affects rapidly growing ducks, turkeys and chickens and is precipitated by a variety of factors that include: genetic predisposition; growth rate; diet; teratogens; mycotoxin infection; and environmental conditions (Leach and Lilburn, 1992; Leach and Monsonego-Ornan, 2007; Lynch et al., 1992; Orth and Cook, 1994; Poulos et al., 1978; Walser et al., 1982; Whitehead, 1997). The condition shares similarities with physeal osteochondrosis in mammals. It is characterised by the presence and persistence of an avascular mass of cartilage (composed of transitional (prehypertrophic) chondrocytes) of variable shape and size located beneath the growth plate and extending into the metaphysis (Thorp, 1994: 209). Clinical radiographic studies show that this lesion becomes visible from two weeks of age (Lynch et al., 1992). The proximal tibiotarsus is most frequently affected because it is the fastest growing growth plate; however, other long bones can also be involved (Farquharson and Jeffries, 2000: 995). Skeletal lesions linked to tibial dyschondroplasia include: bilateral angulation of the proximal articulation and curvature of the shaft (an effect of biomechanical forces acting upon the less rigid cartilage mass); traumatic damage to both the tibiotarsus and fibula; and a predilection for secondary
∗ Corresponding author. Tel.: +44 116 2708055; fax: +44 116 2525005. E-mail addresses: [email protected] (B. Fothergill), [email protected] (R. Thomas), [email protected] (J. Morris).
osteomyelitis (Bartels et al., 1989; Julian, 1998; Lynch et al., 1992; Thorp, 1994). As a direct or indirect consequence of these deformities birds can become lame; the severity of lameness (and bowing) is correlated to the size of the underlying lesion and possibly also body weight (Thorp, 1994: 211; Walser et al., 1982: 269). Although the cartilaginous abnormalities resolve over time, the associated bone deformity is permanent (Siller, 1970: 40). Avian tibial dyschondroplasia has not previously been described in archaeologically recovered animal bones. This probably reflects a combination of factors, including the fact that the selection of fastgrowing meat breeds, a major contributing cause of the disease, is a relatively recent phenomenon and that later post-mediaeval faunal remains in the UK are infrequently subjected to detailed analysis (Thomas, 2009). Here, we describe three turkey tibiotarsi from 19th-century London that exhibit lesions consistent with a diagnosis of avian tibial dyschondroplasia.
2. Materials and methods The remains were recovered during a series of excavations by Museum of London Archaeology in 2006 and 2007 in advance of building redevelopment at the Royal London Hospital, Whitechapel, East London (Fig. 1). The controlled excavation in an area formerly known as Bedstead Square revealed archaeological features relating to the use and development of the hospital in the early 19th century. In addition to a substantial collection of human remains, the excavations produced a collection of 1974 animal bones that included food remains from hospital kitchens and
1879-9817/$ – see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ijpp.2012.10.003
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
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ARTICLE IN PRESS B. Fothergill et al. / International Journal of Paleopathology xxx (2012) xxx–xxx
Fig. 1. Location map of the Royal London Hospital site, drawing by James Morris and Tracy Wellman. Copyright MOLA.
animal bones used by the anatomy school connected to the hospital (Morris, in press). Three turkey bones were collected from context [660], a disturbed deposit above a group of human inhumations in a cemetery used between 1841 and 1854 (Fowler and Powers, 2012). The context is disturbed and contains redeposited pottery from the hospital dating to the first half of the 19th century as well as disarticulated human remains (at least 58 individuals), which appear to derive from the hospital’s anatomy school. The remains thus date from the 19th century but the disturbed and redeposited nature of the context limits our ability to refine this date. Amongst this material were a number of dog and cat remains, as well as individual monkey elements that also appear to have derived from the anatomy school (Morris et al., 2011). However, the majority
of the faunal remains consist of highly butchered sheep/goat vertebrae and pelves, originating from the hospital’s kitchens. Written accounts refer to turkeys being carved by hospital residents on Christmas Day in the late 1800s (Clark-Kennedy, 1962: 102), but the presence of only three turkey elements, all of which exhibit clear pathological changes, could suggest they came from the anatomy school. Gross lesions were recorded using a modified version of the methods described by Vann and Thomas (2006) and Vann (2008) and the three bones were also subjected to digital radiographic examination using a Xograph DRagon mobile x-ray unit (52 KvP; 1.6 mAs; 0.025 s). To assess the degree of ‘bowing’ in the ventrodorsal plane, the angle of the tibial plateau was measured on radiographs of the lateral view of the tibiotarsi. Following the
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
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Fig. 3. Ankylosed fibula of the paired left tibiotarsus exhibiting a small periosteal callus.
Fig. 2. Lateral view of the three tibiotarsi illustrating antero-posterior bowing (the pair are on the left). The arrow indicates the location of small carnivore gnawing marks.
recommendations of Lynch et al. (1992), any resulting angle in excess of 25◦ is typical of avian tibial dyschondroplasia (Lynch et al., 1992: 282). As the presence of radiolucent cavities surrounded by more opaque, sclerotic tissue is another characteristic of the disease (Bartels et al., 1989: 255), the radiographs were also examined for their presence.
paired left tibiotarsus, an area of new bone formation consistent in appearance with a fracture callus is visible (Fig. 3). The distal articulation of all three specimens is generally free of pathology. The only lesions present in this region are two small enthesophytes on the lateral surfaces of the distal condyles and a further enthesophyte on the anterior surface, immediately proximal to the lateral condyle (Fig. 4). These lesions are present in all three tibiotarsi and correspond to the formation of new bone at the insertion points for the tendon of the peroneus longus muscle and the oblique ligament which crosses the extensor canal, respectively. The most obvious lesions occur in the proximal metaphysis of all three specimens. Both the unpaired and paired left specimens exhibit a cavity within the region distal to the tibial crest (Figs. 5 and 6); the maximum length and width measurements of these cavities were 16.5 mm × 7.2 mm and 15.2 mm × 13.4 mm, respectively. Taphonomic damage to the unpaired specimen has prevented a depth measurement from being taken; however, the lesion present in the paired left tibiotarsus is 7.8 mm deep. The edge of these cavities is smooth, the internal walls are complete and have the appearance of very dense trabecular bone and there is no associated periosteal reaction (Fig. 5). Abrasion and rodent gnawing of the cranial and lateral cnemial crests prevented the identification of any pathology on the proximal articular surface.
3. Results Three complete turkey tibiotarsi (two left and one right) were recovered from the Royal London Hospital, representing the only identified remains from this species (Morris et al., 2011). The three bones are very well preserved and residual connective tissue is preserved at some attachment sites. However, the proximal articular surfaces exhibit three forms of taphonomic damage: rodent gnawing, a series of punctures inflicted by a small carnivore on one specimen; and mechanical damage to the cranial cnemial crest of two specimens. Metrical analysis of the distal articulation (breadth and depth) confirmed a visual assessment that two of the specimens were probably paired; the isolated left tibiotarsus was slightly broader and deeper. Pathology and taphonomic damage meant it was not possible to measure the greatest length accurately. All three tibiotarsi exhibited bowing of the shafts in an anteroposterior direction (Fig. 2); although this deviation is more marked in the paired specimens. The fibula of the two left specimens was ankylosed to the shaft through the ossification of the inter-osseous ligament. In the proximal third of the fibula that accompanies the
Fig. 4. Lateral aspect of the paired left tibiotarsus with arrows indicating the location of three small enthesophytes.
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
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Fig. 5. Cavity in the proximal metaphysis of the paired left specimen.
Radiographic analysis of the bones reveals that the cortical bone on the concave (posterior) aspect of the bowed tibiotarsi is significantly thicker than the cortical bone on the convex (anterior) aspect (Fig. 7), along with distal extension of trabecular structures into the medullary cavity (Fig. 8a). The radiographs also reveal that the cavities in the proximal ends of both left specimens have a sclerotic margin (Fig. 8b). Calculation of the angle of the tibial plateau from the radiograph was only possible in the right paired specimen, because of the damage to the cnemial crest in the other two bones; this produced a value of 30◦ . Angular deviation and endosteal thickening in the region of the fracture callus in the left tibiotarsi are also visible in the radiographs (Fig. 8c). As Schmidt et al. (2003: 154) note, avian bone remodelling includes the formation of an endosteal callus provided that the two fractured ends of
Fig. 6. Cavity in the proximal metaphysis of the unpaired left specimen.
Fig. 7. Radiograph of all three tibiotarsi exhibiting thickening of the posterior cortical wall in the paired specimens (lateral view; the pair are on the left).
Fig. 8. Radiograph of all three tibiotarsi (posterior view; the pair are on the left) exhibiting: (a) distal extension of trabecular bone into the diaphysis; (b) angular deviation and callus formation in the fibula; and (c) sclerotic margin around the cavity.
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
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the bone are stabilised (as is the case here) due to the presence of an anatomical splint.
4. Discussion As with all pathology, it is essential to exclude the possible causes of each lesion before one or more diagnoses can be suggested. The unilateral thickening of the posterior cortical wall evident in the radiographs testifies to secondary appositional bone growth to compensate for the additional compressive forces resulting from the abnormal curvature. Enthesophyte formation at the distal articulation may have also occurred in response to higher tension at ligament/tendon attachment sites as a consequence of the changed loading and biomechanical forces caused by the bowing, although similar lesions do also occur in birds of advanced age. In relation to the cavities, it is possible to exclude infection (specifically osteomyelitis), because there is no adjacent periosteal reaction and the cavity does not extend into the metaphysis to form a draining sinus (cloaca). The sclerotic margin of these lesions, the compact nature of the wall and the smooth margins are instead indicative of the presence of an underlying soft tissue mass. Several disease processes result in the deformation of long bone shape in poultry: • fracture; • rickets; • torsional (rotational) and valgus (lateral)/varus (medial) angular deformities; • chondrodystrophy; • avian tibial dyschondroplasia. Fractures of the shaft can be excluded due to the absence of foreshortening, deviation, a periosteal or endosteal callus and radiographic evidence of a fracture line. The consistency in appearance of the bowing instead suggests that it was caused by a developmental disorder affecting bone or cartilage formation. Rickets is caused by a deficiency or imbalance in vitamin D3, calcium, or phosphorus in young birds resulting in thickening and inadequate mineralisation of all growth plates (Thorp, 1994: 213). Skeletal lesions observed in rachitic birds include: bowing; reduced bone length; valgus and varus (angular) deformities of the leg bones; metaphyseal flaring; and pathological fracture (e.g. Itakura et al., 1978; Long et al., 1984a, 1984b, 1984c). However, not all of these lesions necessarily occur in the same individual depending on the age of the bird and the length and degree of nutritional deficiency. Nevertheless, the fact that the distal metaphysis is unaffected by bone changes in the Royal London Hospital specimens suggests that if rickets was the cause, then it was only a mild case affecting the fastest growing growth plate. Rotational and angular deformities, which can result from a lack of physical activity, metabolic disease (e.g. rickets) and infection, are frequently described in the distal tibiotarsus and proximal tarsometatarsus of domestic fowl (e.g. Duff and Thorp, 1985; Thorp, 1994: 206–207). However, these conditions can be excluded because the Royal London Hospital specimens display no morphological changes to the distal articulation, one of the primary foci of these disorders. Chondrodystrophy is a generalised disruption of long bone growth plates caused by a nutritional deficiency or mycoplasma infection (in turkeys), although inheritance affects susceptibility (Thorp, 1994: 215). The disorder results in impaired longitudinal growth but normal width growth; consequently, affected long bones are shortened, thickened, misshapen and can exhibit enlargement of the hock and secondary valgus/varus deformity
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(Thorp, 1994: 214). The complete absence of these characteristics in the Royal London Hospital tibiotarsi excludes this cause. The only remaining possibility is avian tibial dyschondroplasia. In clinical cases, the separation of rickets and tibial dyschondroplasia is best achieved through histological analysis of the growth plate cartilage (Thorp, 1994: 209, 213). In the absence of soft tissue preservation, however, zooarchaeologists are forced to rely upon the nature and distribution of gross lesions in dry bone. Despite the challenges, avian tibial dyschondroplasia is considered to be the most likely diagnosis for a number of reasons. Firstly, the lesions only affect the proximal metaphysis and the curvature of the element, traumatic damage to the fibula, and tibial plateau angles in excess of 25◦ are all consistent with this interpretation. Secondly, the cavities within the proximal metaphysis of the left specimens are consistent with the “bulbous enlargement of the posterior medial aspect of the proximal tibiotarsus” described by Walser et al. (1982: 269) in five lines of turkey displaying the disease. The medial side of the bone is a predilection site for dyschondroplastic lesions in the tibiotarsus due to the mechanical loading acting on this side (Praul et al., 2000: 1011). It is probable that these lesions represent loci of the distally extended growth plate cartilage that is pathognomonic of this disease. Indeed, Siller (1970: 42) notes that these masses are surrounded by a thin ‘shell’ of bone; taphonomic processes in the Royal London Hospital specimens have presumably damaged this ‘shell’, exposing the underlying cavity. Finally, it is speculated that the persistence of trabeculae within the proximal metaphysis and mid-shaft testifies to the failure of normal remodelling, perhaps as a consequence of the need to strengthen a bone weakened by the presence of an avascular cartilage mass. 5. Conclusions While it is impossible to pinpoint the precise aetiology of avian tibial dyschondroplasia from archaeological remains, the identification of this condition in 19th-century turkeys is notable because it is during this period that increasing efforts were made to improve poultry productivity. Albarella et al. (1997) noted a younger age at slaughter and increased size in the 18th-century chickens and geese from Castle Mall in Norwich and while it is possible that some advances were made as early as the 17th century, it is only in the late 19th century that historical records indicate the existence of industrial-scale poultry production (Thirsk, 1997: 189–195). In particular, the selection of fast-growing breeds reared in unnatural environments had a number of profound health consequences; issues that remain a major economic and animal welfare issue in contemporary poultry farms (Pines et al., 2005: 285). Identification of conditions like tibial dyschondroplasia in the archaeological record potentially provides a valuable, but currently underexplored source of information concerning the history and nature of ‘livestock’ improvement in the past. Acknowledgements We would like to thank Louise Fowler, Natasha Powers, Nicky Powel and Tracy Wellman of Museum of London Archaeology. The archaeological work at Royal London Hospital was funded by Skanska and Barts and the Royal London NHS Trust. We are also grateful to the anonymous reviewer whose comments strengthened this paper. References Albarella, U., Beech, M., Mulville, J., 1997. The Saxon, Medieval and Post-Medieval mammal and bird bones excavated 1989–91 from Castle Mall, Norwich, Norfolk. In: Ancient Monuments Laboratory Report 72/97. English Heritage, London.
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
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Bartels, J.E., McDaniel, G.R., Hoerr, F.J., 1989. Radiographic diagnosis of tibial dyschondroplasia in broilers: a field selection technique. Avian Diseases 33 (2), 254–257. Clark-Kennedy, A.E., 1962. The London: A Study in the Voluntary Hospital System, vol. 1. Pitman Medical Publishing, London, pp. 1740–1840. Duff, S.R.I., Thorp, B.H., 1985. Abnormal angulation/torsion of the pelvic appendicular skeleton in broiler fowl: morphological and radiological findings. Research in Veterinary Science 39, 313–319. Farquharson, C., Jeffries, D., 2000. Chondrocytes and longitudinal bone growth: the development of tibial dyschondroplasia. Poultry Science 79, 994–1004. Fowler, L., Powers, N. (Eds.), 2012. Doctors, Dissection and Resurrection Men: Excavations in the 19th Century Burial Ground of the London Hospital, 2006. London: Museum of London Archaeology Monograph Series 62. Itakura, C., Yamasaki, K., Goto, M., Takahashi, M., 1978. Pathology of experimental vitamin D deficiency rickets in growing chickens. I. Bone. Avian Pathology 7, 491–513. Julian, R.J., 1998. Rapid growth problems: ascites and skeletal deformities in broilers. Poultry Science 77, 1773–1780. Leach, R.M., Lilburn, M.S., 1992. Current knowledge on the aetiology of tibial dyschondroplasia in the avian species. Poultry Science Review 4, 57–65. Leach, R.M., Monsonego-Ornan, E., 2007. Tibial dyschondroplasia 40 years later. Poultry Science 86, 2053–2058. Long, P.H., Lee, S.R., Rowland, G.N., Britton, W.M., 1984a. Experimental rickets in broilers: gross microscopic, and radiographic lesions. I. Phosphorus deficiency and calcium excess. Avian Diseases 28 (2.), 460–474. Long, P.H., Lee, S.R., Rowland, G.N., Britton, W.M., 1984b. Experimental rickets in broilers: gross microscopic, and radiographic lesions. II. Calcium deficiency. Avian Diseases 28 (4.), 921–932. Long, P.H., Lee, S.R., Rowland, G.N., Britton, W.M., 1984c. Experimental rickets in broilers: gross, microscopic, and radiographic lesions. III. Vitamin D deficiency. Avian Diseases 28 (4), 933–943. Lynch, M., Thorp, B.H., Whitehead, C.C., 1992. Avian tibial dyschondroplasia as a cause of bone deformity. Avian Pathology 21, 275–285. Morris, J., Fowler, L., Powers, N., 2011. A hospital with connections; 19th century exotic animal remains at the Royal London Hospital. Post-Medieval Archaeology 45 (2), 367–373.
Morris, J. Explorations in anatomy: the remains from Royal London Hospital. In: Thomas, R., Fothergill, B. (Eds.), Animals and their Bones in the Modern World. Museum National d’Histoire Naturelle, Paris, in press. Orth, M.W., Cook, M.E., 1994. Avian tibial dyschondroplasia: a morphological and biochemical review of the growth plate lesion and its causes. Veterinary Pathology 31, 403–404. Pines, M., Hasdaia, A., Monsonego-Ornan, E., 2005. Tibial dyschondroplasia – tools, new insights and future prospects. Worlds Poultry Science Journal 61, 285–297. Poulos, P.W., Reiland, S., Elwinger, K., Olsson, S.E., 1978. Skeletal lesions in the broiler, with special reference to dyschondroplasia (osteochondrosis). Pathology, frequency and clinical significance in two strains of birds on high and low energy feed. Acta Radiologica. Supplementum 358, 229–275. Praul, C.A., Ford, B.C., Gay, C.V., Pines, M., Leach, R.M., 2000. Gene expression and tibial dyschondroplasia. Poultry Science 79, 1009–1013. Schmidt, R.E., Deauvill, D.R., Phalen, D.N., 2003. Pathology of Pet and Aviary Birds. Wiley-Blackwell, Chichester. Siller, W.G., 1970. Tibial dyschondroplasia in the fowl. Journal of Pathology 101 (1), 39–46. Thirsk, J., 1997. Alternative Agriculture: A History. Oxford University Press, Oxford. Thomas, R., 2009. Bones of contention: why later post-medieval assemblages of animal bones matter. In: Horning, A., Palmer, M. (Eds.), Crossing Paths or Sharing Tracks: Future Directions in the Archaeological Study of Post-1550 Britain and Ireland. Boydell and Brewer Ltd., Woodbridge, pp. 133–148. Thorp, B.H., 1994. Skeletal disorders in the fowl: a review. Avian Pathology 23, 203–236. Vann, S., 2008. Recording the facts: a generic recording system for animal palaeopathology. Unpublished PhD Thesis, University of Leicester, Leicester. Vann, S., Thomas, R., 2006. Humans, other animals and disease: a comparative approach towards the development of a standardised recording protocol for animal palaeopathology. Internet Archaeology 20 http://intarch.ac.uk/ journal/issue20/vannthomas index.html Walser, M.M., Cherms, F., Dziuk, H., 1982. Osseous development and tibial dyschondroplasia in five lines of turkeys. Avian Diseases 26 (2), 265–271. Whitehead, C.C., 1997. Dyschondroplasia in poultry. Proceedings of the Nutrition Society 56, 957–966.
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
ARTICLE IN PRESS International Journal of Paleopathology xxx (2012) xxx–xxx
Contents lists available at SciVerse ScienceDirect
International Journal of Paleopathology journal homepage: www.elsevier.com/locate/ijpp
Case Study
Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital Brooklynne “Tyr” Fothergill a,∗ , Richard Thomas a , James Morris b a b
School of Archaeology and Ancient History, University of Leicester, Leicester LE1 7RH, UK Museum of London Archaeology, Mortimer Wheeler House, London N1 7ED, UK
a r t i c l e
i n f o
Article history: Received 30 May 2012 Received in revised form 9 October 2012 Accepted 10 October 2012 Keywords: Turkey Meleagris gallopavo Tibial dyschondroplasia Tibiotarsus Improvement
a b s t r a c t In this paper we call attention to the first recorded archaeological examples of avian tibial dyschondroplasia. This condition is identified in three turkey (Meleagris gallopavo L. 1758) tibiotarsi from the Royal London Hospital site in London, UK. The lesions are described, radiographed and differentially diagnosed. Recognition of this condition testifies to the pace of breed development in the 19th-century and the unintended health consequences of ‘improvement’. © 2012 Elsevier Inc. All rights reserved.
1. Introduction Tibial dyschondroplasia is one of the most frequently observed skeletal diseases in domestic birds. It commonly affects rapidly growing ducks, turkeys and chickens and is precipitated by a variety of factors that include: genetic predisposition; growth rate; diet; teratogens; mycotoxin infection; and environmental conditions (Leach and Lilburn, 1992; Leach and Monsonego-Ornan, 2007; Lynch et al., 1992; Orth and Cook, 1994; Poulos et al., 1978; Walser et al., 1982; Whitehead, 1997). The condition shares similarities with physeal osteochondrosis in mammals. It is characterised by the presence and persistence of an avascular mass of cartilage (composed of transitional (prehypertrophic) chondrocytes) of variable shape and size located beneath the growth plate and extending into the metaphysis (Thorp, 1994: 209). Clinical radiographic studies show that this lesion becomes visible from two weeks of age (Lynch et al., 1992). The proximal tibiotarsus is most frequently affected because it is the fastest growing growth plate; however, other long bones can also be involved (Farquharson and Jeffries, 2000: 995). Skeletal lesions linked to tibial dyschondroplasia include: bilateral angulation of the proximal articulation and curvature of the shaft (an effect of biomechanical forces acting upon the less rigid cartilage mass); traumatic damage to both the tibiotarsus and fibula; and a predilection for secondary
∗ Corresponding author. Tel.: +44 116 2708055; fax: +44 116 2525005. E-mail addresses: [email protected] (B. Fothergill), [email protected] (R. Thomas), [email protected] (J. Morris).
osteomyelitis (Bartels et al., 1989; Julian, 1998; Lynch et al., 1992; Thorp, 1994). As a direct or indirect consequence of these deformities birds can become lame; the severity of lameness (and bowing) is correlated to the size of the underlying lesion and possibly also body weight (Thorp, 1994: 211; Walser et al., 1982: 269). Although the cartilaginous abnormalities resolve over time, the associated bone deformity is permanent (Siller, 1970: 40). Avian tibial dyschondroplasia has not previously been described in archaeologically recovered animal bones. This probably reflects a combination of factors, including the fact that the selection of fastgrowing meat breeds, a major contributing cause of the disease, is a relatively recent phenomenon and that later post-mediaeval faunal remains in the UK are infrequently subjected to detailed analysis (Thomas, 2009). Here, we describe three turkey tibiotarsi from 19th-century London that exhibit lesions consistent with a diagnosis of avian tibial dyschondroplasia.
2. Materials and methods The remains were recovered during a series of excavations by Museum of London Archaeology in 2006 and 2007 in advance of building redevelopment at the Royal London Hospital, Whitechapel, East London (Fig. 1). The controlled excavation in an area formerly known as Bedstead Square revealed archaeological features relating to the use and development of the hospital in the early 19th century. In addition to a substantial collection of human remains, the excavations produced a collection of 1974 animal bones that included food remains from hospital kitchens and
1879-9817/$ – see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ijpp.2012.10.003
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
G Model IJPP-59; No. of Pages 6 2
ARTICLE IN PRESS B. Fothergill et al. / International Journal of Paleopathology xxx (2012) xxx–xxx
Fig. 1. Location map of the Royal London Hospital site, drawing by James Morris and Tracy Wellman. Copyright MOLA.
animal bones used by the anatomy school connected to the hospital (Morris, in press). Three turkey bones were collected from context [660], a disturbed deposit above a group of human inhumations in a cemetery used between 1841 and 1854 (Fowler and Powers, 2012). The context is disturbed and contains redeposited pottery from the hospital dating to the first half of the 19th century as well as disarticulated human remains (at least 58 individuals), which appear to derive from the hospital’s anatomy school. The remains thus date from the 19th century but the disturbed and redeposited nature of the context limits our ability to refine this date. Amongst this material were a number of dog and cat remains, as well as individual monkey elements that also appear to have derived from the anatomy school (Morris et al., 2011). However, the majority
of the faunal remains consist of highly butchered sheep/goat vertebrae and pelves, originating from the hospital’s kitchens. Written accounts refer to turkeys being carved by hospital residents on Christmas Day in the late 1800s (Clark-Kennedy, 1962: 102), but the presence of only three turkey elements, all of which exhibit clear pathological changes, could suggest they came from the anatomy school. Gross lesions were recorded using a modified version of the methods described by Vann and Thomas (2006) and Vann (2008) and the three bones were also subjected to digital radiographic examination using a Xograph DRagon mobile x-ray unit (52 KvP; 1.6 mAs; 0.025 s). To assess the degree of ‘bowing’ in the ventrodorsal plane, the angle of the tibial plateau was measured on radiographs of the lateral view of the tibiotarsi. Following the
Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003
G Model IJPP-59; No. of Pages 6
ARTICLE IN PRESS B. Fothergill et al. / International Journal of Paleopathology xxx (2012) xxx–xxx
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Fig. 3. Ankylosed fibula of the paired left tibiotarsus exhibiting a small periosteal callus.
Fig. 2. Lateral view of the three tibiotarsi illustrating antero-posterior bowing (the pair are on the left). The arrow indicates the location of small carnivore gnawing marks.
recommendations of Lynch et al. (1992), any resulting angle in excess of 25◦ is typical of avian tibial dyschondroplasia (Lynch et al., 1992: 282). As the presence of radiolucent cavities surrounded by more opaque, sclerotic tissue is another characteristic of the disease (Bartels et al., 1989: 255), the radiographs were also examined for their presence.
paired left tibiotarsus, an area of new bone formation consistent in appearance with a fracture callus is visible (Fig. 3). The distal articulation of all three specimens is generally free of pathology. The only lesions present in this region are two small enthesophytes on the lateral surfaces of the distal condyles and a further enthesophyte on the anterior surface, immediately proximal to the lateral condyle (Fig. 4). These lesions are present in all three tibiotarsi and correspond to the formation of new bone at the insertion points for the tendon of the peroneus longus muscle and the oblique ligament which crosses the extensor canal, respectively. The most obvious lesions occur in the proximal metaphysis of all three specimens. Both the unpaired and paired left specimens exhibit a cavity within the region distal to the tibial crest (Figs. 5 and 6); the maximum length and width measurements of these cavities were 16.5 mm × 7.2 mm and 15.2 mm × 13.4 mm, respectively. Taphonomic damage to the unpaired specimen has prevented a depth measurement from being taken; however, the lesion present in the paired left tibiotarsus is 7.8 mm deep. The edge of these cavities is smooth, the internal walls are complete and have the appearance of very dense trabecular bone and there is no associated periosteal reaction (Fig. 5). Abrasion and rodent gnawing of the cranial and lateral cnemial crests prevented the identification of any pathology on the proximal articular surface.
3. Results Three complete turkey tibiotarsi (two left and one right) were recovered from the Royal London Hospital, representing the only identified remains from this species (Morris et al., 2011). The three bones are very well preserved and residual connective tissue is preserved at some attachment sites. However, the proximal articular surfaces exhibit three forms of taphonomic damage: rodent gnawing, a series of punctures inflicted by a small carnivore on one specimen; and mechanical damage to the cranial cnemial crest of two specimens. Metrical analysis of the distal articulation (breadth and depth) confirmed a visual assessment that two of the specimens were probably paired; the isolated left tibiotarsus was slightly broader and deeper. Pathology and taphonomic damage meant it was not possible to measure the greatest length accurately. All three tibiotarsi exhibited bowing of the shafts in an anteroposterior direction (Fig. 2); although this deviation is more marked in the paired specimens. The fibula of the two left specimens was ankylosed to the shaft through the ossification of the inter-osseous ligament. In the proximal third of the fibula that accompanies the
Fig. 4. Lateral aspect of the paired left tibiotarsus with arrows indicating the location of three small enthesophytes.
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Fig. 5. Cavity in the proximal metaphysis of the paired left specimen.
Radiographic analysis of the bones reveals that the cortical bone on the concave (posterior) aspect of the bowed tibiotarsi is significantly thicker than the cortical bone on the convex (anterior) aspect (Fig. 7), along with distal extension of trabecular structures into the medullary cavity (Fig. 8a). The radiographs also reveal that the cavities in the proximal ends of both left specimens have a sclerotic margin (Fig. 8b). Calculation of the angle of the tibial plateau from the radiograph was only possible in the right paired specimen, because of the damage to the cnemial crest in the other two bones; this produced a value of 30◦ . Angular deviation and endosteal thickening in the region of the fracture callus in the left tibiotarsi are also visible in the radiographs (Fig. 8c). As Schmidt et al. (2003: 154) note, avian bone remodelling includes the formation of an endosteal callus provided that the two fractured ends of
Fig. 6. Cavity in the proximal metaphysis of the unpaired left specimen.
Fig. 7. Radiograph of all three tibiotarsi exhibiting thickening of the posterior cortical wall in the paired specimens (lateral view; the pair are on the left).
Fig. 8. Radiograph of all three tibiotarsi (posterior view; the pair are on the left) exhibiting: (a) distal extension of trabecular bone into the diaphysis; (b) angular deviation and callus formation in the fibula; and (c) sclerotic margin around the cavity.
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the bone are stabilised (as is the case here) due to the presence of an anatomical splint.
4. Discussion As with all pathology, it is essential to exclude the possible causes of each lesion before one or more diagnoses can be suggested. The unilateral thickening of the posterior cortical wall evident in the radiographs testifies to secondary appositional bone growth to compensate for the additional compressive forces resulting from the abnormal curvature. Enthesophyte formation at the distal articulation may have also occurred in response to higher tension at ligament/tendon attachment sites as a consequence of the changed loading and biomechanical forces caused by the bowing, although similar lesions do also occur in birds of advanced age. In relation to the cavities, it is possible to exclude infection (specifically osteomyelitis), because there is no adjacent periosteal reaction and the cavity does not extend into the metaphysis to form a draining sinus (cloaca). The sclerotic margin of these lesions, the compact nature of the wall and the smooth margins are instead indicative of the presence of an underlying soft tissue mass. Several disease processes result in the deformation of long bone shape in poultry: • fracture; • rickets; • torsional (rotational) and valgus (lateral)/varus (medial) angular deformities; • chondrodystrophy; • avian tibial dyschondroplasia. Fractures of the shaft can be excluded due to the absence of foreshortening, deviation, a periosteal or endosteal callus and radiographic evidence of a fracture line. The consistency in appearance of the bowing instead suggests that it was caused by a developmental disorder affecting bone or cartilage formation. Rickets is caused by a deficiency or imbalance in vitamin D3, calcium, or phosphorus in young birds resulting in thickening and inadequate mineralisation of all growth plates (Thorp, 1994: 213). Skeletal lesions observed in rachitic birds include: bowing; reduced bone length; valgus and varus (angular) deformities of the leg bones; metaphyseal flaring; and pathological fracture (e.g. Itakura et al., 1978; Long et al., 1984a, 1984b, 1984c). However, not all of these lesions necessarily occur in the same individual depending on the age of the bird and the length and degree of nutritional deficiency. Nevertheless, the fact that the distal metaphysis is unaffected by bone changes in the Royal London Hospital specimens suggests that if rickets was the cause, then it was only a mild case affecting the fastest growing growth plate. Rotational and angular deformities, which can result from a lack of physical activity, metabolic disease (e.g. rickets) and infection, are frequently described in the distal tibiotarsus and proximal tarsometatarsus of domestic fowl (e.g. Duff and Thorp, 1985; Thorp, 1994: 206–207). However, these conditions can be excluded because the Royal London Hospital specimens display no morphological changes to the distal articulation, one of the primary foci of these disorders. Chondrodystrophy is a generalised disruption of long bone growth plates caused by a nutritional deficiency or mycoplasma infection (in turkeys), although inheritance affects susceptibility (Thorp, 1994: 215). The disorder results in impaired longitudinal growth but normal width growth; consequently, affected long bones are shortened, thickened, misshapen and can exhibit enlargement of the hock and secondary valgus/varus deformity
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(Thorp, 1994: 214). The complete absence of these characteristics in the Royal London Hospital tibiotarsi excludes this cause. The only remaining possibility is avian tibial dyschondroplasia. In clinical cases, the separation of rickets and tibial dyschondroplasia is best achieved through histological analysis of the growth plate cartilage (Thorp, 1994: 209, 213). In the absence of soft tissue preservation, however, zooarchaeologists are forced to rely upon the nature and distribution of gross lesions in dry bone. Despite the challenges, avian tibial dyschondroplasia is considered to be the most likely diagnosis for a number of reasons. Firstly, the lesions only affect the proximal metaphysis and the curvature of the element, traumatic damage to the fibula, and tibial plateau angles in excess of 25◦ are all consistent with this interpretation. Secondly, the cavities within the proximal metaphysis of the left specimens are consistent with the “bulbous enlargement of the posterior medial aspect of the proximal tibiotarsus” described by Walser et al. (1982: 269) in five lines of turkey displaying the disease. The medial side of the bone is a predilection site for dyschondroplastic lesions in the tibiotarsus due to the mechanical loading acting on this side (Praul et al., 2000: 1011). It is probable that these lesions represent loci of the distally extended growth plate cartilage that is pathognomonic of this disease. Indeed, Siller (1970: 42) notes that these masses are surrounded by a thin ‘shell’ of bone; taphonomic processes in the Royal London Hospital specimens have presumably damaged this ‘shell’, exposing the underlying cavity. Finally, it is speculated that the persistence of trabeculae within the proximal metaphysis and mid-shaft testifies to the failure of normal remodelling, perhaps as a consequence of the need to strengthen a bone weakened by the presence of an avascular cartilage mass. 5. Conclusions While it is impossible to pinpoint the precise aetiology of avian tibial dyschondroplasia from archaeological remains, the identification of this condition in 19th-century turkeys is notable because it is during this period that increasing efforts were made to improve poultry productivity. Albarella et al. (1997) noted a younger age at slaughter and increased size in the 18th-century chickens and geese from Castle Mall in Norwich and while it is possible that some advances were made as early as the 17th century, it is only in the late 19th century that historical records indicate the existence of industrial-scale poultry production (Thirsk, 1997: 189–195). In particular, the selection of fast-growing breeds reared in unnatural environments had a number of profound health consequences; issues that remain a major economic and animal welfare issue in contemporary poultry farms (Pines et al., 2005: 285). Identification of conditions like tibial dyschondroplasia in the archaeological record potentially provides a valuable, but currently underexplored source of information concerning the history and nature of ‘livestock’ improvement in the past. Acknowledgements We would like to thank Louise Fowler, Natasha Powers, Nicky Powel and Tracy Wellman of Museum of London Archaeology. The archaeological work at Royal London Hospital was funded by Skanska and Barts and the Royal London NHS Trust. We are also grateful to the anonymous reviewer whose comments strengthened this paper. References Albarella, U., Beech, M., Mulville, J., 1997. The Saxon, Medieval and Post-Medieval mammal and bird bones excavated 1989–91 from Castle Mall, Norwich, Norfolk. In: Ancient Monuments Laboratory Report 72/97. English Heritage, London.
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Please cite this article in press as: Fothergill, B., et al., Avian tibial dyschondroplasia in 19th-century turkey (Meleagris gallopavo L. 1758) remains from the Royal London Hospital. Int. J. Paleopathol. (2012), http://dx.doi.org/10.1016/j.ijpp.2012.10.003