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Traumatic neuroma development in tail docked piglets is not associated with long-term changes in spinal nociceptive processing

Traumatic neuroma development in tail docked piglets is not associated with long-term changes in spinal nociceptive processing. By Sandercock, D., S. Smith, J. Coe, P. Di Giminiani, S. Edwards, 2016. Royal Dublin Society: Abstracts book of the 24th International Pig Veterinary Society (IPVS) Congress, Dublin, Republic of Ireland 7-10th June 2016. p. 611.

Abstract

Introduction: Concerns exist over the long term consequences for tail stump pain experienced by piglets after docking, especially in relation to traumatic neuroma development in caudal nerves after docking injury. Neuroma formation may cause detrimental sensory changes in the tail due to altered axonal excitability leading to abnormal sensation or pain.

Aims: To characterize pig tail histopathology at time intervals up to 16 weeks after tail docking and to measure expression of key neuropeptides in caudal dorsal root ganglia and spinal cord neurons associated with (i) peripheral nerve regeneration; activating transcription factor-3 (ATF3), (ii) inflammatory pain; Calcitonin gene-related peptide (CGRP) and (iii) the maintenance of chronic pain; N-methyl D-aspartate (NMDA) ionotropic glutamate receptor subtype 2B (GRIN2B) at the same time points after tail docking injury.

Materials and Methods: Thirty-two female piglets (Landrace/Large White x synthetic sireline) were used (16 docked/16 sham-docked). Piglets were tail docked (amputation of approx. 2/3 of the tail) on post-natal day 3 using a gas hot docking iron. Equivalent sham-docked piglets served as intact controls. Pigs were euthanized by barbiturate overdose 1, 4, 8 and 16 weeks after sham/tail docking. Tail stumps (2 cm) were collected post-mortem for histopathological assessment. Caudal dorsal root ganglia (Ca1-Ca4+) and associated spinal cord were collected for gene expression analysis by real-time quantitative PCR of mRNA.

Results: Non-specific epidermal and dermal changes associated with healing were observed after tail docking. Mild inflammation, ulceration and oedema were present at 1 week. Traumatic neuroma development was a consistent feature from 4 weeks after tail docking. Neuroma axonal dispersion in the tail stump was on-going 16 weeks after tail docking. ATF-3 mRNA was significantly upregulated in caudal DRGs up to 8 weeks after tail docking, but did not differ at 16 weeks compared with sham controls. Both CGRP and GRIN2B mRNA expression was significantly upregulated 1 week after tail docking in caudal spinal cord neurons but were not significantly different from sham-docked pigs thereafter.

Conclusion: Histopathological lesions that occur shortly after tail docking (beyond 1 week) are not likely to induce or maintain pain. The effects of tail docking on peripheral nerve axonal proliferation and dispersion are relatively short-lived and, although still present, are attenuated by 16 weeks after tail docking injury. Changes in peripheral and spinal nociceptive processing associated with possible inflammatory and chronic pain appear to resolve by 4 weeks after tail docking injury.

Poster Sandercock IPVS

Temporal changes in mechanical nociceptive thresholds in juvenile pigs subjected to surgical tail amputation: a model of injury induced by tail biting

Temporal changes in mechanical nociceptive thresholds in juvenile pigs subjected to surgical tail amputation: a model of injury induced by tail biting. By Di Giminiani, P., E. Malcolm, M. Leach, M. Herskin, D. Sandercock, S. Edwards, 2016. Royal Dublin Society: Abstracts book of the 24th International Pig Veterinary Society (IPVS) Congress, Dublin, Republic of Ireland 7-10th June 2016. p. 649.

Abstract

Introduction: Tail biting is a global welfare problem in the pig industry leading to significant tail injury and potential carcass rejection. The temporal effects of such injuries and subsequent healing are presently unknown, although limb amputation in humans can lead to abnormal neural activity and decreased nociceptive thresholds. In order to evaluate potential sensitisation following tail damage, we created a model by surgical amputation of tails, and assessed mechanical nociceptive thresholds.

Materials and Methods: Surgical tail resection was performed to assess the influence of age, extent of tail amputated and time since amputation on thresholds of mechanical nociception. To evaluate the effect of age at the time of injury, female pigs underwent surgery at 9 weeks (±3 days ‘weaner’) (n=19) or 17 weeks (±3 days ‘finisher’) (n=43). The effect of time after amputation was evaluated on 24 pigs at 8 weeks, and 38 pigs at 16 weeks after surgery. The effect of the extent of tail amputated was assessed by assigning the pigs to 3 treatments (‘Intact’: sham-amputation; ‘short tail’: 2/3 of tail removed; ‘long tail’: 1/3 of tail removed). A Pressure Application Measurement device was used to record mechanical nociceptive thresholds (tail flick or tail clamp withdrawal responses). Within a single session, three stimuli were applied to a skin area proximal to the site of amputation, 3 days pre-surgery, 1 week and either 8 or 16 weeks post-amputation.

Results: Across the two amputation ages, results indicated that tail amputation induced a significant reduction (P<0.05) in mechanical nociceptive thresholds in short and long tails one week after surgery. The same treatment effect was observed at 16 weeks after amputation performed at 9 weeks of age (P<0.05). For surgeries performed at 17 weeks of age, thresholds tended to be lower in short compared to intact tails (P=0.081) and significantly lower (P<0.05) in long tail pigs 8 weeks after amputation. No significant difference was observed at 16 weeks following surgeries performed at 17 weeks of age.

Conclusion: These results show that surgical amputation of pig tails leads to decreased cutaneous mechanical nociceptive thresholds in the skin area proximal to the site of injury. Results indicated that severe tail injury occurring in the weaner period may be associated with sensitisation up to 16 weeks following the injury. In contrast, injuries occurring in the finishing period appeared to be associated with shorter lasting mechanical sensitisation, resolving within 16 weeks.

Poster Di Giminiani IPVS

 

Application of a handheld Pressure Application Measurement device for the characterisation of mechanical nociceptive thresholds in intact pig tails

Application of a handheld Pressure Application Measurement device for the characterisation of mechanical nociceptive thresholds in intact pig tails. By Pierpaolo Di Giminiani, Dale A. Sandercock, Emma M. Malcolm, Matthew C. Leach, Mette S. Herskin and Sandra A. Edwards. 2016. Physiology & Behavior 165: 119–126.

Highlights

• Mechanical nociceptive thresholds were quantified for the first time in pig tails.
• The PAM device allowed determining anatomical and age-specific thresholds in pigs.
• A platform for the assessment of painful conditions in pigs is proposed.

Abstract

The assessment of nociceptive thresholds is employed in animals and humans to evaluate changes in sensitivity potentially arising from tissue damage. Its application on the intact pig tail might represent a suitable method to assess changes in nociceptive thresholds arising from tail injury, such as tail docking or tail biting. The Pressure Application Measurement (PAM) device is used here for the first time on the tail of pigs to determine the reliability of the methods and to provide novel data on mechanical nociceptive thresholds (MNT) associated with four different age groups (9, 17, 24 and 32 weeks) and with proximity of the target region to the body of the animal. We recorded an overall acceptable level of intra-individual reliability, with mean values of CV ranging between 30.1 and 32.6%. Across all age groups, the first single measurement of MNT recorded at region 1 (proximal) was significantly higher (P b 0.05) than the following two. This was not observed at tail regions 2 and 3 (more distal). Age had a significant effect (P b 0.05) on the mean thresholds of nociception with increasing age corresponding to higher thresholds. Furthermore, a significant effect of proximity of tail region to the body was observed (P b 0.05), with MNT being higher in the proximal tail region in pigs of 9, 17 and 24 weeks of age.
There was also a significant positive correlation (P b 0.05) between mechanical nociceptive thresholds and age/body size of the animals.
To the best of our knowledge, no other investigation of tail nociceptive thresholds has been performed with the PAM device or alternative methods to obtain mechanical nociceptive thresholds in intact tails of pigs of different age/body size. The reliability of the data obtained with the PAM device support its use in the measurement of mechanical nociceptive threshold in pig tails. This methodological approach is possibly suitable for assessing changes in tail stump MNTs after tail injury caused by tail docking and biting.

Histopathological Characterization of Tail Injury and Traumatic Neuroma Development after Tail Docking in Piglets

Histopathological Characterization of Tail Injury and Traumatic Neuroma Development after Tail Docking in Piglets. By: D.A. Sandercock, S.H. Smith, P. Di Giminiani, S.A. Edwards, 2016. Journal of Comparative Pathology 155: 40-49.

Abstract

Tail docking of neonatal pigs is widely used as a measure to reduce the incidence of tail biting, a complex management problem in the pig industry. Concerns exist over the long-term consequences of tail docking for possible tail stump pain sensitivity due to the development of traumatic neuromas in injured peripheral nerves. Tail stumps were obtained post mortem from four female pigs at each of 1, 4, 8 and 16 weeks following tail amputation (approximately two-thirds removed) by a gas-heated docking iron on post natal day 3. Tissues were processed routinely for histopathological examination. Non-neural inflammatory and reparative epidermal and dermal changes associated with tissue thickening and healing were observed 1 to 4 months after docking. Mild neutrophilic inflammation was present in some cases, although this and other degenerative and non-neural reparative changes are not likely to have caused pain. Traumatic neuroma and neuromatous tissue development was not observed 1 week after tail docking, but was evident 1 month after tail docking. Over time there was marked nerve sheath and axonal proliferation leading to the formation of neuromata, which were either localized and circumscribed or comprised of multiple axons dispersed within granulation tissue. Four months after tail resection, neuroma formation was still incomplete, with possible implications for sensitivity of the tail stump.

Corrigendum to “Histopathological Characterization of Tail Injury and Traumatic Neuroma Development after Tail Docking in Piglets” J Comp Pathol 155 (1) (2016) 40-49.

The authors wish to clarify terminology used in their paper entitled ‘Histopathological characterization of tail injury and traumatic neuroma development after tail docking in piglets’ and thank the Editor for the opportunity to do so. In the absence of a specific immunohistochemical label for detection of axons, the words ‘axon/axonal’ were inaccurately used and should be replaced by ‘Schwann cell’. Without more specific proof, it
certainly does not confirm, or necessarily infer, conduction. Secondly, ‘S100 neurofilament’ was inadvertently used instead of simply ‘S100’. The authors apologise for this error, which was wholly editorial on their part. Finally, in our opinion, the literature definitions of traumatic neuromas are such that there is likely to be some disagreement as to their required component features, particularly at different stages of lesion development, in different species and in different age groups of animals. In our paper, descriptions of traumatic neuroma presence and development were also based on haematoxylin and eosin staining and not solely confined to S100 immunolabelling. To this end, features such as variably-sized microfascicles, disorderly (often circumferential) neural proliferation and nerve fibres turning back on themselves are consistent with previous reports on traumatic neuromas in a number of species, including pigs.
While the aforementioned errors are regretted, this work was intended as a descriptive morphological characterization of a wide range of histopathological changes over known time points post docking. We have had some criticism that, due to our use of the word axonal, we have implied or claimed innervation, and thus pain sensation,
during the weeks after docking. This was not our intention – rather, our opinion is neutral in terms of whether or not traumatic neuromas are painful. The last sentence of the paper acknowledged that this work could not determine that. This study was considered descriptive and foundational, to serve as a platform for further investigation.
Its take-home message, irrespective of the error in terminology, is that neural proliferation consistent with traumatic neuroma development appears to be still ongoing at 16 weeks after tail docking.

Investigating the effect of rooting substrate provision on the group lying behaviour of pigs using machine vision

Investigating the effect of rooting substrate provision on the group lying behaviour of pigs using machine vision. By: Abozar Nasirahmadi, Sandra A Edwards, Barbara Sturm,
Conference Paper · June 2016. Conference: CIGR-AgEng Conference, Aarhus, Denmark

Abstract

To deliver good animal welfare, pigs should have a hygienic and undisturbed lying area within the pen. However, the provision of a rooting material is desirable to meet behavioural needs and this can only be given onto solid floor away from the dunging area, which might disrupt the group lying pattern. To determine whether daily provision of a rooting material (maize silage) onto a solid plate in the lying area of a fully slatted pen resulted in changed lying location, the lying patterns of pigs in 6 enriched pens were compared with those of 6 control pens which had only a suspended enrichment toy. Since visual monitoring of pig behaviours over long periods is very time consuming, an image
processing technique was applied to identify any changes pig lying positions and behaviour. Pigs were monitored by top view CCTV cameras and animals were extracted from their background using image processing algorithms. The x–y coordinates of each binary image were used for ellipse fitting algorithms to localize each pig. In order to find the lying positions, ellipse parameters were calculated for all fitted ellipses. Each pen was virtually subdivided into four zones in images and the centroid of each fitted ellipse was used for finding the position of each lying pig at 10 minute intervals during their lying period, after use of an algorithm to remove images in motion preceding the scan. By means of the ellipse properties it was possible to automatically find and compare the
changes in lying position of pigs in the pens. Results showed that once daily provision of rooting material did significantly change lying behaviour.

Histological and neurophysiological pain assessment in young pigs

Original title: Approche histologique et neurophysiologie de la douleur liée à la coupe de queue chez les porcelets

Presentation of Dr. Dale Sandercock (SRUC) at a seminar on histological and neurophysiological approaches to pain assessment in young pigs. INRA-PEGASE, St-Gilles, France, December 14th 2015

Abstract

Concerns exist over the long term consequences of tail docking on possible tail stump pain sensitivity due to the development of traumatic neuromas in injured peripheral nerves. Traumatic neuroma formation may cause detrimental sensory changes in the tail due to altered peripheral and spinal neuronal excitability leading to abnormal sensation or pain. We have investigated tail injury and traumatic neuroma development by histopathological assessment after tail docking and measured the expression of key neuropeptides associated with peripheral nerve regeneration, inflammation and chronic pain. In complimentary studies on tail docking and tail biting, we have developed behavioural assessment approaches to measure mechanical nociceptive thresholds (MNT) in the pig tail in purpose built test set-up using a Pressure Application Measurement (PAM) device. Using these approaches we have determined baseline MNT in intact tails along different regions of the tail and also measured changes in MNT over time in pig with resected tails (simulation of the effect of tail biting). An overview of other Scotland’s Rural College (SRUC) pig health and welfare research projects is also presented.

Presentation Pic INRA seminar on pain (D Sandercock, 2015))

Strategies to reduce the risk of tail biting in pigs managed on slatted floors

By Jen-Yun (author)

A 4-year project of “Strategies to reduce the risk of tail biting in pigs managed on slatted floors” has started. It is a collaboration between Teagasc, SRUC and the University of Edinburgh.
Below is a poster on the project presented in the Teagasc Pig Farmers’ Conference 2015.
The project will aim to explore ways to reduce tail-biting on slatted floor systems where straw is not available by environmental enrichment and nutritional strategies.
The enrichments used at the moment are compressed straw and different wood types.
Later the project will also investigate the effects of various lengths of tails, measures to predict tail-biting outbreaks and methods to interfere effectively.
The project will be supervised by Dr Keelin O’Driscoll (Teagasc), Dr Rick D’Eath (SRUC), Dr Dale Sandercock (SRUC), and Prof Natalie Waran (University of Edinburgh).
Dr Amy Haigh is the postdoctoral researcher working together on this project in Teagasc, and Dr Laura Boyle and Dr Edgar Garcia Manzanilla are also the collaborating researchers in Teagasc. I (Jen-Yun) am the PhD student on this project.
fwd uk jy291015 entail poster - JC 28102015c

Preliminary study on tail nerves in piglets after tail docking

Carr, R.W., J.E. Coe, E. Forsch, M. Schmelz, D.A. Sandercock, 2015. Structural and functional characterisation of peripheral axons in the caudal nerve of the neonatal pigs: Preliminary data. Proceedings of the 9th EFIC Congress, Vienna, Sept 2-5.

Summary

The pig tail is innervated by the caudal tail nerves and it is evident at the site of injury after tail docking (i.e. 8/9th caudal vertebrae) that a relatively high proportion of both C and A-fibres can be affected following peripheral nerve transection, with implications for axonal excitability and nociceptive processing in the tail stump.
As a proof of principle, it is possible to assess A- and C-fibre axonal function using electrical axonal excitability techniques for pig caudal tail nerve. In neonatal caudal nerves, A and C-fibre axons show significant changes in conduction speed which are related primarily to neonatal age.
Future studies will examine axonal functional properties in pig tails later in life where traumatic neuroma formation in the caudal nerves is present.

Annotated TEM micrograph of tail nerves (Dale Sandercock)

Abstract

Structural and functional characterisation of peripheral axons in the caudal nerve of the neonatal pigs: Preliminary data
R.W. Carr1, J.E. Coe2, E. Forsch1, M. Schmelz1, D.A. Sandercock2
1Department of Anaesthesiology, University of Heidelberg, Mannheim, Germany
2Animal and Veterinary Science Research Group, Scotland’s Rural College (SRUC), Easter Bush, United Kingdom

Background and aims: Early postnatal tail docking (amputation of 2/3rds of the tail) in piglets is performed as a preventative measure to minimize potential trauma associated with tail biting in older animals. The aim of this study was to investigate caudal nerve axonal composition and the effects of tail docking on axonal function in neonatal pigs.
Methods: Axonal composition was examined using Transmission Electron Microscopy (TEM). Functional assessment of A and C-fibre axons was performed in vitro using compound action potential (CAP) recordings from isolated nerve fascicles.
Results: TEM revealed both myelinated and unmyelinated axons in dorsal and ventral caudal nerves. Myelinated axons ranged in size from small diameter thinly myelinated Aδ-axons to larger diameter Aβ-axons (mean 2.30; range 0.7-6.3 μm). Unmyelinated C-fibre axons clustered together in multiple Remak bundles (mean 0.7; range 0.3-1.9 μm). Caudal nerves were harvested for functional assessment at 5 days of age from undocked tails and at 12.3 days (i.e. 9.3 days after docking) from docked pigs. The average A-fibre CAP amplitude from undocked tails was larger (1599.6±552.9μV) and conducted more rapidly (9.79±2.04m/s) than the A-fibres from docked tails (amplitude 1065.1±507.6μV and c.v.=7.78±2.57m/s). For C-fibres, the average axonal conduction velocity in docked tails was slower (1.74±0.2m/s) than in undocked tails (2.26±0.41m/s). Axonal conduction in caudal nerve C-fibres from both intact and docked animals was completely blocked by 500 nM tetrodotoxin (TTX) suggesting conduction was mediated primarily by TTX-sensitive NaV-isoforms.
Conclusions: As a proof of principle study, it is possible to functionally assess A- and C-fibre axons in pig caudal nerve using electrical axonal excitability techniques.
Acknowledgments: ANIWHA.

Poster Carr et al. 2015

Tail docking in pigs alters gene expression in the brain associated with increased anxiety-like behaviour

Oberst et al. (2015) presented a poster on the effect of tail docking in neonatal pigs on the expression of genes involved in modulating anxiety-like behaviour at the annual meeting of the Scandinavian Association for the Study of Pain (SASP) at the Karolinska Institute, Stockholm, Sweden (13-14th April 2015).

The abstract is presented below; the poster can be found here

Abstract

Background: Adverse experiences in early life, such as exposure to stress, can have long term detrimental effects on the future physiology and behaviour of the animal. Typically animals exposed to such experiences are more anxious and more reactive to stress in later life. Tail biting is a major problem in modern pig production, both in terms of animal welfare and productivity. Tail docking in early postnatal life is common practice to reduce risk of this problem, but causes pain and may alter pain sensitivity.

Aims: To investigate whether a significant painful experience in early life (tail docking) alters the expression of genes in the amygdala that are linked to an anxiety-prone phenotype.

Methods: Eight female piglets (Landrace/Large White x synthetic sireline) were used. Four piglets were tail docked (amputation of approx. 2/3 of the tail) on post-natal day 3 using hot-iron cautery and four sham-docked piglets served as intact controls. On post-natal day 10, pigs were sedated and then euthanized by barbiturate overdose. Brains were removed, the amygdala grossly dissected and frozen on dry ice. 20μm sections were cut and subsequently processed using in situ hybridisation with radiolabelled probes complementary to corticotropin-releasing hormone receptor-1 (Crhr1) and CRH receptor-2 (Crhr2) mRNA.

Results: Crhr1 mRNA expression was significantly greater (p<0.05) in the amygdala of tail-docked piglets compared with the sham-docked animals. There was no significant difference detected in Crhr2 expression in the amygdala between the groups.

Conclusion: Increased expression of Crhr1 in the amygdala is associated with an anxiety-prone phenotype in rats and pigs, thus it is likely that tail docking in early life leads to enhanced anxiety which may have a negative impact on pig welfare. Ongoing experiments will determine whether these central changes in gene expression are long-lasting.

[Support: BBSRC, DEFRA-part of ANIWHA ERA-NET initiative].

Source:
Oberst, P., D.A Sandercock, P.Di Giminiani, S.A. Edwards, P.J. Brunton, 2015. The effect of tail docking in neonatal pigs on the central expression of genes involved in modulating anxiety-like behaviour. Abstract for the poster presentation at the Scandinavian Association for the Study of Pain (SASP) Annual Meeting, Karolinska Institute, Stockholm, Sweden. 13-14th April 2015.

Poster