Open Access

A retrospective study of forensic cases of skin ulcerations in Danish pigs from 2000 to 2014

Acta Veterinaria Scandinavica201658:48

https://doi.org/10.1186/s13028-016-0229-0

Received: 19 February 2016

Accepted: 7 July 2016

Published: 15 July 2016

Abstract

Background

Ulcerations in pigs, as in other farm animals, are considered to be painful and therefore hampering the welfare. Farmers are obliged to provide an intervention to protect animals against unnecessary suffering and failure to do so is considered negligence. Moreover, animals with severe open wounds are considered unfit for transportation and so are pigs with ulcerations located on hernias. This paper presents a retrospective study of forensic case files concerning ulcerations in Danish pigs from 2000 to 2014. The aim of the study was to clarify the number of cases, the number of pigs, the anatomical localization and size of ulcerations, evaluate changes during years and the age of the lesions.

Results

A total of 209 case files concerning 283 pigs with 459 ulcerations were included. In 2004, 2005, 2007–2009 and 2011, sows with shoulder ulcerations were the most frequently submitted, while in 2014 pigs with ulcerations on umbilical outpouchings dominated. The change in pattern on body location most likely reflects specific national regulations enforced from 2003 to 2009. The ulcerations were estimated to be from 4 h to several months old and the median diameter of ulcerations was 4 cm.

Conclusions

Since 2004, the number of cases per year has declined. However, the number of affected pigs has remained almost constant from 2004 to 2014 (23.8 ± 8.5 pigs per year). The change in pattern on body parts with ulcerations likely reflected specific national regulations.

Keywords

Forensic pathology Pig Ulcerations Welfare

Background

Ulcerations in pigs, as in other farm animals, are considered to be painful and therefore hampering the welfare. If neglected, an ulceration can result in a forensic case, i.e. being reported to the police [1, 2]. Most ulcerations are due to external trauma while others are due to fistulation to the skin surface from an underlying condition [37]. However, farmers are obliged to provide an intervention to protect animals against unnecessary suffering no matter the cause of the ulceration. Failure to do so is considered negligence and a violation of the European Union Council Directive concerning the protection of animals kept for farming purposes [8]. In addition, animals with severe open wounds are considered unfit for transportation [9]. It has been specified by the Danish Veterinary and Food Administration that animals with ulcerations larger than 3 cm in diameter are unsuitable for transportation from transit locations or for transport across borders [10]. Moreover, the Danish Animal Welfare Council has stated that transport of slaughter pigs with ulcerations located on hernias is prohibited [11, 12].

Since 2003, special attention has been drawn to shoulder ulcerations on sows in Denmark and other countries (e.g. England and Canada) [1, 2, 4, 1315]. Consequently, the Danish Animal Welfare Council stated that all shoulder ulcerations involving the subcutaneous tissue or deeper structures are considered a violation of the Danish Animal Protection Act [1619].

The aim of a veterinary forensic examination requested by the police is to perform a thorough and precise documentation of the lesions with respect to diagnosis, dimensions, anatomical localization, and an assessment of the age of the lesions [20, 21]. Depending on the case, the estimated age of ulcerations is used to interpret the degree of negligence; i.e., ulcerations left untreated for a longer period are legally considered more serious than acute lesions [18].

In Denmark, all veterinary forensic investigations are requested by the police and carried out at the University of Copenhagen. This paper presents a retrospective study of forensic case files concerning ulcerations in Danish pigs from 2000 to 2014 submitted to Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen. The aim of the study was to clarify the number of cases, the number of pigs, the anatomical localization and size of ulcerations, evaluate changes during years and the age of lesions.

Methods

Case files concerning ulcerations in pigs sent for forensic investigation to the University of Copenhagen from 2000 to 2014 were examined retrospectively. A case file was defined as a single police record and included information regarding the number of pigs, the number and anatomical localizations of the ulcerations, the sex and age of the animal, the gross and histological descriptions of the ulcerations and usually photo documentation of lesions.

An ulceration was defined as a breach of the epidermis including the basal membrane [3]. Ulcerations included were due to an external force while case files concerning fistulation to the skin surface from underlying lesions were not included. All ulcerations were originally reported to the police by veterinary enforcement officers, i.e. by The Veterinary Task Force for livestock inspection, at transit locations, or at meat inspection at slaughterhouses.

The gross and histological evaluations of the ulcerations had been carried out by five experienced veterinary pathologist (i.e. professors with more than 10 years of experience with diagnostic pathology). Age estimations stated in the case files were made by the pathologists basing their estimations on the presence and amount of granulation tissue. In a few cases, in which granulation tissue was not grossly visible, the histological inflammatory reaction was used to state the age of the ulcerations. As reference to the estimation of age, studies of wound healing in pigs and humans were used [2227]. Based on the gross (presence of granulation tissue) and histological descriptions, ulcerations were divided into four age intervals: (1) 0–3 days; (2) 4–7 days; (3) 8–28 days; and (4) >28 days. If granulation tissue was absent the ulceration was estimated to be less than 3 days old. In ulcerations with granulation tissue, the mean thickness was [mean ± standard deviation (SD)]: 4–7 days = 0.5 ± 0.3 cm; 8–28 days = 1.5 ± 1.2 cm; >28 days = 2.7 ± 2.5 cm. In ulcerations in which granulation tissue was not grossly visible, histology was applied to state the age of the ulceration. From these ulcerations new sections were cut and evaluated.

From the information given in the case files, the sex and age of the pigs were registered and pigs were grouped according to the anatomical localization of the ulceration: (1) shoulder, (2) umbilical outpouching (hernias, enterocystoma and preputial diverticula), (3) body (head, neck and back), (4) limb and (5) tail region. A pig with multiple ulcerations at different anatomical localizations was allocated to each of the specified anatomical localizations. For each of the anatomical localizations, measurements of the ulcerations were evaluated for normality and data were found to be nonparametric (SAS Institute 9.4). A Wilcoxon Rank Sum Test was used to compare the medians of the five groups (SAS Institute 9.4), and a P value below 0.05 was interpreted as a significant difference between groups.

Results

The inclusion criteria were fulfilled for 209 case files (Fig. 1). Each case file included 1–10 pigs with an average (\(\bar{x}\)) ± SD of 1.4 ± 1.2 pigs. Each pig had between 1 and 60 ulcerations (1.7 ± 3.7, \(\bar{x}\) ± SD) with a median of 1. In total, tissue from 283 pigs had been submitted in which 459 ulcerations were described. In 40 of the 283 pigs, the exact number of ulcerations was not stated. The pigs were registered as females (53 %), males (5 %) and of unknown sex (42 %). Approximately half of the pigs were sows (51.2 %), while 34.3, 6.7, 0.4 and 7.4 % were slaughter pigs (5–6 months), younger pigs (<5 months), adult boars and pigs of unknown age, respectively.
Fig. 1

The annual number of forensic case files of skin ulcerations in pigs examined from 2000 to 2014

During 2000–2003, 13 cases were sent for forensic investigation (Fig. 1). In 2004, the number of case files peaked (35 case files) being more than 11 times higher than in 2003 (3 case files). After 2004, the number of case files declined, however, the number of pigs with ulcerations each year showed an almost constant level of 23.5 ± 8.5 (\(\bar{x}\) ± SD) pigs per year (Fig. 2). The proportion (%) of pigs submitted in relation to the number of produced pigs in Denmark showed roughly the same tendency as seen in Fig. 3. The pattern of distribution of ulcerations in the five groups of anatomical localization is presented in Fig. 4. In total, 131 out of 283 (46.3 %) of the pigs submitted from 2000 to 2014 were sows with shoulder ulcerations. In slaughter pigs and younger pigs, some ulcerations were located on abdominal outpouchings. In total, 52 out of 283 (18.4 %) of all pigs had an ulcerated outpouching in the abdominal region. Ulcerations on the body and limbs were present in pigs of all ages and were present in 49 out of 283 (17.3 %) and in 61 out of 283 (21.5 %) of pigs, respectively. Ulcerations in the tail region were present in 23 out of 283 pigs (8.1 %). The total sum of the percentages exceeds 100 % as 22 pigs had ulcerations located at more than one location.
Fig. 2

The annual number of pigs with skin ulcerations examined from 2000 to 2014

Fig. 3

Proportion of pigs with skin ulcerations submitted for forensic examination in relation to the total number of pigs produced in Denmark annually from 2000 to 2014

Fig. 4

The annual number of pigs with skin ulcerations localized on the shoulder, umbilical outpouching, body, limbs or tail

In 90.8 % of the ulcerations (417 out of 459), measurements of dimensions were registered. The median diameter of all ulcerations was 4 cm. The median, minimum and maximum values for the diameter of ulcerations in each of the anatomical localizations and totally are presented in Table 1. Differences in the diameter of the ulcerations were highly dependent on the anatomical localization (P < 0.0001).
Table 1

The diameter of 417 skin ulcerations in forensic case files (2000–2014)

Anatomical localization

Number of ulcerations

Median diameter (cm)

Minimum diameter (cm)

Maximum diameter (cm)

Shoulder

159

5

1

11

Umbilical outpouching

56

5.8

0.7

21

Body

37

1

0.3

10

Limb

142

1.5

0.2

14

Tail

23

3

1

18

Total

417

4

0.2

21

The age had been determined for 65.4 % of the ulcerations (300 out of 459). The ulcerations were evaluated to be: (1) 0–3 days, n = 27; (2) 4–7 days, n = 3; (3) 8–28 days, n = 237; and (4) >28 days, n = 33.

New histological sections were cut in 29 out of 459 (6.3 %) ulcerations because granulation tissue had not been observed at gross evaluation. In a single ulceration, inflammation or granulation tissue was absent at the histological evaluation, and the age was stated as unknown. In another ulceration, in which the amount of granulation tissue could not be determined no estimate of an age was given. Three ulcerations were characterized by the infiltration of neutrophils and stated to be at least 4 h old. In nine ulcerations, both neutrophils and macrophages were present and the ulcerations were estimated to be between 6 and 24 h of age. In 15 ulcerations proliferation of fibroblasts was present and in some of the ulcerations newly formed capillaries were also observed. These ulcerations were stated to be 2–3 days old (n = 11) and between 16 and 32 h old (n = 4).

Discussion

Despite the number of case files per year had declined since 2004, the number of pigs affected remained almost constant during the last 10 years suggesting fewer but more serious offenders (Figs. 1, 2). Since 2003, shoulder ulcerations have received increased attention as a reflection of the publication of several papers [1, 2, 4, 14] and statements from the Danish Animal Welfare Council on the subject [1719]. The development in the number of sows with shoulder ulcerations submitted for forensic investigation reflects the increased attention on the subject (Fig. 4). The first paper addressing the problem with shoulder ulcerations in sows was published in 2003 [14] and already the year after more than 25 cases were received for forensic investigation (Fig. 4). It is also likely that the increase in pigs with ulcerations on umbilical outpouchings from 2011 to 2014 is a consequence of two specific regulations on transportation of animals with ulcerations on umbilical outpouchings enforced by the Danish Animal Welfare Council in 2008 and 2009 [11, 12]. In these regulations, it was deducted that pigs with umbilical outpouching with a diameter of more than 15 cm or with ulcerations were unfit for transportation. Before that time, statements on umbilical outpouching were vaguer; i.e. animals were unfit for transportation if they were hampered by the outpouching.

The median diameter (4 cm) of all ulcerations exceeded the threshold of 3 cm set by the Danish Veterinary and Food Administration regarding ulcerations being too large to allow transportation of the animal. The median diameter of ulcerations on shoulders and umbilical outpouchings both exceeded 3 cm, while the median diameter of ulcerations on the tail, body and limbs did not exceed 3 cm (Table 1).

Estimating the age of ulcerations is central to a forensic investigation, as this in a judicial setting will be used to interpret the degree of negligence or in apportioning blame. In the majority of ulcerations, the age was estimated based on the presence of granulation tissue at gross examination. In order to document the level of violence of animal protection legislations, it is crucial that all cases are examined and filed in a well-documented professional manner. Therefore, in Denmark all requests for forensic examination of porcine ulcerations are taken care of at the University of Copenhagen. Moreover, the filing of cases is also highly important when sending out information material to pig producers, arrangement of courses and communicating with the authorities, e.g. the police and The Danish Welfare Council.

Conclusions

Since 2004, the number of cases per year has declined while the number of affected pigs has remained almost constant. The changes in anatomical localization of the ulcerations during 2000–2014 likely reflected specific national regulations.

Declarations

Authors’ contributions

All authors contributed to the design of the study, the collection of data and interpretation of data. In addition, KB performed the statistical analyses and drafted the manuscript. All authors read and approved the final manuscript.

Acknowledgements

The following Associated Professors are acknowledged for contribution of case files: Jørgen S. Agerholm, Tine Iburg, Pall S. Leifsson and Ole L. Nielsen.

Competing interests

The authors declare that they have no competing interests.

Ethics approval

This study did not require official or institutional ethical approval.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen

References

  1. Herskin MS, Bonde MK, Jørgensen E, Jensen KH. Decubital shoulder ulcers in sows: a review of classification, pain and welfare consequences. Animal. 2011;5:757–66.View ArticlePubMedGoogle Scholar
  2. Larsen T, Kaiser M, Herskin MS. Does the presence of shoulder ulcers affect the behaviour of sows? Res Vet Sci. 2015;98:19–24.View ArticlePubMedGoogle Scholar
  3. Hargis AM, Ginn PE. The integument. In: Zachary JF, McGavin MD, editors. Pathologic basis of veterinary disease. 5th ed. Missouri: Elsevier; 2012. p. 972–1084.Google Scholar
  4. Jensen HE. Investigation into the pathology of shoulder ulcerations in sows. Vet Rec. 2009;165:171–4.View ArticlePubMedGoogle Scholar
  5. Mirt D. Lesions of so-called flank biting and necrotic ear syndrome in pigs. Vet Rec. 1999;144:92–6.View ArticlePubMedGoogle Scholar
  6. Petersen HH, Nielsen EO, Hassing AG, Ersbøll AK, Nielsen JP. Prevalence of clinical signs of disease in Danish finisher pigs. Vet Rec. 2008;162:377–82.View ArticlePubMedGoogle Scholar
  7. Schrøder-Petersen DL, Simonsen H. Tail biting in pigs. Vet J. 2001;162:196–210.View ArticlePubMedGoogle Scholar
  8. Commission European. Council Directive (98/58/EC) of 20 July 1998 concerning the protection of animals kept for farming purposes. Off J Eur Commun. 1998;L221:23–7.Google Scholar
  9. Commission European. Council Regulation (EC) (No 1/2005) of 22 December 2004 on the protection of animals during transport and related operations and amending Directives 64/432/EEC and 93/119/EC and Regulation (EC) No 1255/97. Off J Eur Commun. 2005;L3:1–44.Google Scholar
  10. Anon. Announcement regarding transportation of animals [in Danish]. The Veterinary Food Administration 21.05.2005.Google Scholar
  11. Anon. The Danish Animal Welfare Council statement regarding transportation of diseased or injured production animals including horses [in Danish]. The Danish Animal Welfare Council 17.02. 2009.Google Scholar
  12. Anon. Statement of the 2 of December 2008 regarding pigs with umbillical or inguinal hernia [in Danish]. The Danish Animal Welfare Council 02.12.2008.Google Scholar
  13. KilBride AL, Gilman CE, Green LE. A cross sectional study of the prevalence, risk factors and population attributable fractions for limb and body lesions in lactating sows on commercial farms in England. BMC Vet Res. 2009;5:30.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Lund M, Aalbaek B, Jensen HE. Shoulder ulcerations in sows—animal ethics [in Danish]. Dansk Veterinær Tidskrift. 2003;86:8–11.Google Scholar
  15. Zurbrigg K. Sow shoulder lesions: risk factors and treatment effects on an Ontario farm. J Anim Sci. 2006;84:2509–14.View ArticlePubMedGoogle Scholar
  16. Anon. The Danish animal protection law LBK nr. 473 af 15.05.2014. [in Danish].Google Scholar
  17. Anon. Supplemental statement regarding shoulder ulcerations in sows [in Danish]. The Danish Animal Welfare Council 23.05.2008.Google Scholar
  18. Anon. Statement regarding shoulder ulcerations in sows, specific questions [in Danish]. The Danish Animal Welfare Council 18.10.2007.Google Scholar
  19. Anon. The Danish Animal Welfare Council statement regarding shoulder ulcerations in sows [in Danish]. The Danish Animal Welfare Council 19.11.2003.Google Scholar
  20. Munro R, Munro HMC. Some challenges in forensic veterinary pathology: a review. J Comp Pathol. 2013;149:57–73.View ArticlePubMedGoogle Scholar
  21. Salvagni FA, Siqueira AD, Maria ACBE, Santos CRDS, Ramos AT, Maiorka PC. Forensic veterinary pathology: old dog learns a trick. Braz J Vet Pathol. 2011;5:37–8.Google Scholar
  22. Betz P. Histological and enzyme histochemical parameters for the age estimation of human skin wounds. Int J Legal Med. 1994;170:60–8.View ArticleGoogle Scholar
  23. Heffernan D, Dudley B, McNeil PL, Howdieshell TR. Local Arginine Supplementation results in sustained wound nitric oxide production and reductions in vascular endothelial growth factor expression and granulation tissue formation. J Surg Res. 2006;133:46–54.View ArticlePubMedGoogle Scholar
  24. Kondo T, Ishida Y. Molecular pathology of wound healing. Forensic Sci Int. 2010;203:93–8.View ArticlePubMedGoogle Scholar
  25. Singer AJ, Clark RAF. Cutaneous wound healing. N Engl J Med. 1999;341:738–46.View ArticlePubMedGoogle Scholar
  26. Takamiya M, Fujita S, Saigusa K, Aoki Y. Simultaneous detection of eight cytokines in human dermal wounds with a multiplex bead-based immunoassay for wound age estimation. Int J Legal Med. 2008;122:143–8.View ArticlePubMedGoogle Scholar
  27. van der Laan N, de Leij LF, ten Duis HJ. Immunohistopathological appearance of three different types of injury in human skin. Inflamm Res. 2001;50:350–6.View ArticleGoogle Scholar

Copyright

© Barington et al 2016

Advertisement