TYPE Original Research PUBLISHED 12 January 2023 DOI 10.3389/fvets.2022.1070206 Development of flank lesions in OPEN ACCESS growing pigs after weaning: A case study EDITED BY Alexandra Harlander, University of Guelph, Canada REVIEWED BY Maggie Henry, Marianna Norring1*, Heng-Lun Ko1,2 and Anna Valros1 University of Guelph, Canada Giuliana Miguel-Pacheco, 1 Research Centre for Animal Welfare, Department of Production Animal Medicine, University of University of Saskatchewan, Canada Helsinki, Helsinki, Finland, 2 Department of Animal and Food Science, School of Veterinary Science, *CORRESPONDENCE Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain Marianna Norring marianna.norring@helsinki.fi SPECIALTY SECTION Flank lesions in pigs are a common yet poorly understood consequence of This article was submitted to damaging social behavior. One group of pigs on a commercial farm with group Animal Behavior and Welfare, a section of the journal lactation and late weaning, and with the history of flank lesions was studied. Frontiers in Veterinary Science Skin lesions on the flanks, including linear and circular lesions, and tail lesions RECEIVED 14 October 2022 on 69 pigs were recorded six times during 5 weeks after weaning at the age of ACCEPTED 19 December 2022 9 weeks. Nosing behavior was scanned during six sessions with multiple scans. PUBLISHED 12 January 2023 The associations of age, trunk whiteness, weight gain, sow parity, litter size, CITATION sex, and tail lesions with the number of circular and linear lesions were analyzed Norring M, Ko H-L and Valros A (2023) Development of flank lesions in using linear mixed models. The number of linear lesions increased as pigs aged, growing pigs after weaning: A case and pigs with a higher weight gain had more linear lesions. Moreover, pigs with study. Front. Vet. Sci. 9:1070206. doi: 10.3389/fvets.2022.1070206 a whiter trunk color were scored with more lesions of both types. According to descriptive behavior data, nosing and biting behaviors were most frequent COPYRIGHT © 2023 Norring, Ko and Valros. This is during weeks 2–4 after weaning at the age of 11–13 weeks. On average, an open-access article distributed seven circular flank lesions were found per pig during the experiment, at the under the terms of the Creative Commons Attribution License (CC BY). age of 10–14 weeks. After the peak on day 17, their occurrence decreased. The use, distribution or reproduction Skin lesion occurrence was related to a lighter skin color on the trunks of in other forums is permitted, provided pigs. We recommend reporting skin color in connection with lesion scoring the original author(s) and the copyright owner(s) are credited and that the results. Nosing behavior and flank lesions both peaked from 2 to 4 weeks after original publication in this journal is weaning, suggesting that nosing behavior contributed to lesion development cited, in accordance with accepted academic practice. No use, distribution during this time. or reproduction is permitted which does not comply with these terms. KEYWORDS damaging behavior, flank lesion, injurious behavior, skin lesion, Sus scrofa 1. Introduction A survey conducted in the UK reported that farmers ranked the tail, ear and flank biting as the most important welfare issue to be tackled in the grower and finisher stage (1). According to a Danish investigation, ear necrosis and tail and flank bites, accounted for 43% of the clinical signs reported on finisher pigs (2). While damaging behaviors are considered as a serious welfare issue per se (3), the lesions caused by these behaviors may also be an economic loss for farmers (4). While extensive information is available on some damaging behaviors, especially on tail and ear biting, less is known about the development of flank lesions. Frontiers in Veterinary Science 01 frontiersin.org Norring et al. 10.3389/fvets.2022.1070206 Flank biting behavior in pigs, however, appears to be weaning). The study commenced after weaning and continued common, and flank-directed behavior was noted in almost all for 6 weeks (Figure 1). of the 31 finishing pig farms in an Irish study (5). However, The pigs were fed three times a day (at 08:00, 16:00, the onset and the peak of flank-nosing or flank-biting behavior and 21:00) a diet following Finnish recommendations. Water seem to vary: Straw and Bartlett (6) observed a peak of nosing was provided ad libitum. In the growing pen, there were behaviors, including flank and belly nosing about 1-week post- three designated areas, all with solid concrete flooring: a weaning in piglets weaned at 3–4 weeks of age. van Staaveren feeding area (17.4∗ 2.5 m), corridor (17.4∗ 2.6 m), and resting et al. (7) observed that flank lesions were more prevalent at area (17.4∗ 2.5 m) (Figure 2). There were nine feed troughs in older ages (8–13 weeks and in finishers) than in 4–8 week- the feeding area, as well as three additional feed troughs and old pigs. Chou et al. (8) observed a peak in the frequency six nipple drinkers in the corridor. The roof-covered resting of damaging behaviors at 20 weeks of age in finisher pigs. area was straw-bedded, and several wooden logs hung from the The histology of flank biting lesions was described by Mirt wall by chains. Straw bedding was renewed weekly. The room (9), who suggested that they might be caused by a similar temperature was maintained at ∼19 ± 2◦ C. pathogenesis to ear lesions, whereby a slight trauma of the skin, for example, due to manipulation by another pig, allows infection with staphylococci. However, the etiology or causes 2.2. Procedures and skin lesion are not well described or understood. van Staaveren et al. (5) assessment found that mild and severe flank lesions existed together. In the same study, flank-directed behaviors were not correlated with For another experiment, piglets had been ear-tagged after flank lesion prevalence, while tail and ear directed behaviors and birth using different colors for each litter. All the pigs were corresponding lesions were. weighed on the day of weaning (9 weeks of age), as well as In general, damaging behaviors such as ear biting and tail 7 days (10 weeks of age), 17 days (13 weeks of age), and 29 biting often appear simultaneously in the same individuals (10, days (14 weeks of age) post-weaning. While the pigs were on 11). Furthermore, skin lesions in general have been correlated the scale, lesions were closely observed with a hand-held light with flank lesion prevalence on farms (7). Similar risk factors source. Two trained observers were used to score the lesions. might influence these different damaging behaviors: pigs on Linear lesions were scored on the day of weaning and 3 and farms using chains as enrichment objects displayed more 7 days post-weaning. As the current study focused on circular damaging behaviors overall, as well as flank biting, compared to lesions, circular lesions and tail lesions were assessed on the day pigs on farms using wooden or plastic devices (5). of weaning and 3, 7, 17, 29, and 39 days after weaning. Circular This case study aimed at describing the development of and linear lesions were observed on sides and back, excluding pig skin lesions in a group of growing pigs as an attempt to head, neck and belly areas. understand the etiology of flank biting. In addition, we observed The number and severity of circular lesions were scored nosing behaviors during the same period to assess whether these according to a scoring system modified from Diana et al. were temporally linked to lesion occurrence. (12) (Table 1). The weighted number of circular lesions was calculated by multiplying the number of severe lesions (Table 1) by two and summing it with number of minor circular lesions 2. Materials and methods to better describe the overall severity and affected skin area and because only few severe lesions were found. 2.1. Animals and housing In addition, as some pigs were completely white or black and some had black spots, the trunk color was recorded as The study was performed from February to March 2018 on the estimated percentage of the total trunk (sides and back, a commercial farm located in Southern Finland with a history excluding head, neck, and belly areas) that was white (i.e., trunk of flank lesions. According to the farmer, the occurrence of whiteness) during the first lesion observations. flank lesions was similar to other groups of weaned pigs on the farm. Sixty-nine weaners from six litters (mean litter size: 12 ± 4) were born in a group-farrowing system. The sows were 2.3. Behavioral observations Landrace and Landrace × Yorkshire mixed breeds. Two groups of three sows and their offspring were kept separately for the Two previously trained observers scan sampled the pig first 6 weeks. During the 5th week after farrowing, the sows group at 5-min intervals. As the whole group was not visible at were removed daily for about 8 h to promote estrus. On the 6th once, the growing pen was divided into six observation sectors week after farrowing, these two groups were mixed together into (two feeding sectors, two corridor sectors, two resting sectors, a group pen where this study was performed. The sows were Figure 2). One observer scanned three sectors and the other finally removed when the piglets reached the age of 9 weeks (i.e., observer simultaneously scanned the other three sectors (see Frontiers in Veterinary Science 02 frontiersin.org Norring et al. 10.3389/fvets.2022.1070206 FIGURE 1 Timeline of the on-farm management (from Week 0 to 9) and the experimental design (from Week 9 to 15). The black dots indicate the week of the age of the piglets. The gray dots indicate the days post-weaning (P-W.) in which we carried out the experimental work, including piglet weighing or the assessment of linear/circular/tail lesions on piglets. The white dots indicate the days for behavioral observation (days 1, 3, 8, 10, 22, and 38 post-weaning). FIGURE 2 Schematic diagram illustrating the three areas in the growing pen, including the feeding area (17.4*2.5 m), corridor (17.4*2.6 m), and resting area (17.4*2.5 m). The blue shaded trapezoid in the resting area indicates the roof cover. Several wooden logs were hung from the wall by metal chains as drawn in the resting area. The narrow black rectangle indicates the gates where pigs could not pass between the resting area and corridor. The white rectangles in the corridor and feeding area indicate the feed troughs. The water droplets indicate the location of nipple drinkers. The red dashed lines indicate the division of the pen into separate observation sectors for live behavioral observation (feeding 1, corridor 1, and resting 1 to the right; feeding 2, corridor 2, and resting 2 to the left). TABLE 1 Scoring system for the circular, linear, and tail lesions in pigs [adapted from (12)]. Lesion type Description Minor circular lesion A minor (superficial, diameter: ≥1 cm) circular lesion. Severe circular lesion A larger (diameter: ≥2 cm), or deep circular lesion and/or blood and/or infection on the flank. Linear lesion Red and/or swollen fresh linear scratches. Mild tail lesion Redness of the skin or minor scratches. Severe tail lesion An open wound, and/or a clear bite mark, and/or part of the tail missing and/or swollen lesion. Frontiers in Veterinary Science 03 frontiersin.org Norring et al. 10.3389/fvets.2022.1070206 the division in Figure 2). Behavior was observed for 4 h per were not significantly (P > 0.05) related to lesion numbers and day (between 9:00 and 15:00), resulting in 48 scans per day. were thus removed from the final model. Observations took place for 6 days (twice during weeks 1 and The chi-squared test was used to analyze the development of 2 and once during weeks 4 and 6 after weaning). tail lesions after weaning. Only descriptive data were available A biting event was defined as the focal pig biting the for the development of behavior. Statistical analyses were receiver’s trunk, belly, or other body parts (including the neck, performed with SPSS 24. face, tail, and legs) once. Nosing was defined as the focal pig’s snout continuously making physical contact with the receiver’s trunk, belly, or other body parts. A minimum of three 3. Results consecutive contacts with a certain body part (trunk/belly/other) were needed to be considered as the beginning of one nosing 3.1. Circular and linear lesions event. All pigs visible were scanned and if physical contact was observed this pig was followed to see if the contact continued. The number of circular lesions on the flanks peaked on day Nosing event was considered discontinued when 3 s elapsed 17 post-weaning (P = 0.001, Figure 3). The number of linear lesions on the flanks increased as pigs aged (P = 0.001). The without physical contact. Biting events very seldomly occurred and they were thus scored as combined with the more numerous number of linear lesions were: 9 ± 1.0a on the day of weaning, nosing events. 15 ± 1.4b on day 3, and 18 ± 1.8b on day 7 (ab different letter The number of events was recorded per observation sector. indicates difference). Pigs with a higher weight gain had more Nosing and biting events per day were summed for data analysis, linear lesions (slope 26.3, P = 0.017). and weekly averages were calculated for the weeks with two Pigs with a whiter trunk color were scored with more observation days (weeks 1 and 2). As the pigs could not be circular lesions (slope 0.31, P = 0.023) and a higher weighted identified from a distance, only descriptive data on behavior number of circular lesions (slope 0.30, P = 0.040). Moreover, are reported. pigs with a whiter trunk color were scored with more linear lesions (slope 9.9, P = 0.001). 2.4. Ethical statement 3.2. Tail lesions Pigs were managed according to normal farm practices The majority of the pig tails were intact and no severe under commercial conditions (13). No additional harm was tail lesions were recorded. The occurrence of mild tail lesions expected to occur by handling and spectating, as the animals differed significantly between days (P = 0.007). The number of were moved with their usual group, and individual observation mild tail lesions (total number of tails assessed) were: 18 (69) on of skin lesions only took a few minutes. The study was licensed the day of weaning, 6 (69) on day 3, 23(69) on day 7, 15 (64) on by the National Animal Experiment Board and complied with day 17, 12 (65) on day 29, and 9 (65) on day 39. However, no the national rules derived from European Directive 2010/63 on clear temporal pattern could be distinguished. the protection of animals used for scientific purposes. 3.3. Biting and nosing behavior after 2.5. Statistical analysis weaning The associations of age, trunk whiteness, weight gain, sow The development of the total frequency of nosing and biting parity, litter size, pig sex, and tail lesions with the number of behavior after weaning is illustrated in Figure 4. The descriptive circular lesions and weighted number of circular lesions were data are based on the averages of 6 days (4 h of observations analyzed with linear mixed models. Age (6 levels) was used as per day) of observations. The nosing and biting frequency are repeated effect and pig was considered as the statistical unit. divided by the number of animals visible (as hourly averages) at Weight gain, sow parity, litter size, pig sex, and tail lesions were any sampling time (5-min intervals). Figure 4 displays data from not significantly (P > 0.05) related to numbers of circular lesions three resting areas only (resting 1, 2, and corridor 2, which had and were thus removed from the final model. bedding), as very few nosing or biting behaviors were observed The associations of age, trunk whiteness, weight gain, sow in the feeding and the unbedded corridor areas. parity, litter size, pig sex, and tail lesions with the number of On average, nosing or biting of the belly area was observed linear lesions were analyzed with linear mixed models. Age (3 the least, followed by the flank area, while other areas (including levels) was used as a repeated effect and pig was considered as the neck, face, tail, and legs) attracted the highest frequency of the statistical unit. Sow parity, litter size, pig sex, and tail lesions nosing or biting events (belly 0.0004, flank 0.0017, other areas Frontiers in Veterinary Science 04 frontiersin.org Norring et al. 10.3389/fvets.2022.1070206 FIGURE 3 Development of the number of circular lesions (mean ± SE) per pig on the flanks of 69 pigs after weaning at 9 weeks of age. Means with different capital letters indicate a significant difference between days in the weighted number of circular lesions, and different lower-case letters indicate a significant difference between days in the number of circular lesions (P < 0.05). The weighted number of circular lesions was calculated by multiplying the number of severe lesions by two and summing it with the number of small lesions to reflect the size and severity of lesions. 0.0054 nosing events per 5-min scan sample divided by the study of van Staaveren et al. (7). Thus, it is difficult to evaluate number of pigs visible). the effect of piglet age and that of weaning age in the light of the current scientific literature. A possible reason for this finding might be that even though weaning might cause a temporary 4. Discussion increase in flank biting behavior, piglets are normally still very small at this age, and do not easily cause damage to the skin by Circular flank lesions increased after weaning, which manipulating each other. However, as the pigs in the current occurred at the age of 9 weeks in the studied pigs. Circular study were older, and thus probably stronger at the time of flank lesions were most prominent on observation day 17 after weaning, after which their occurrence decreased. Thus, our weaning, the increase in flank manipulation after weaning more study suggested that the problem appeared to be temporary. easily resulted in skin damage, and thus the lesions. In the current study, we observed an average of seven While the etiology of flank lesions is not clear, our results flank lesions per pig, which is more than that reported by van suggest that biting, nosing, or snout manipulation could be Staaveren et al. (5) in finisher pigs namely <1 mild and 2 a contributing factor. In the current study, the manipulative severe flank lesions per pig. In addition, van Staaveren et al. behavior appeared to increase at the same time when the (7) observed that 0.4% of weaners at ages of 8–13 weeks had flank lesion numbers were the highest, during weeks 2–4 after lesions. The difference might owe to the fact that the current weaning. Actual biting events were only seldomly observed study observed lesions from close distance instead of scanning in our study (results not shown), while nosing was the the group of pigs outside of their pen. predominant form of manipulative behavior. This supports the A further explanation for the higher level of flank lesions in hypothesis proposed by Mirt (9) that flank lesions are due to the present study as compared to that of van Staaveren et al. (5, 7) a combination of a slight trauma caused by other pigs and a might be that the pigs in the current study were older at weaning bacterial infection, instead of being due to mechanical damage (4 vs. 9 weeks). Weaning at 9 weeks is considerably older than in from biting only. common commercial pig production. In the current study, flank Biting and other injurious social behaviors occur biting behavior appeared to peak at 2–4 weeks after weaning, sporadically, creating difficulties in the observation of these while lesions were more frequently observed in older pigs in the situations. van Staaveren et al. (5) recorded 0.24 flank-directed Frontiers in Veterinary Science 05 frontiersin.org Norring et al. 10.3389/fvets.2022.1070206 FIGURE 4 Frequency of nosing or biting behavior (directed to the trunk, belly, or other body parts) after weaning (weaning at 9 weeks of age) in one group of 69 pigs. Descriptive data based on weekly averages of 4 h instantaneous sampling (5-min interval), with observations during the daytime. Behaviors were observed twice during weeks 9 and 10 and once during weeks 12 and 14. Observed nosing events were divided by the number of animals visible in one of the three areas the pigs used for resting. damaging behaviors per finisher pig per hour. Diana et al. it is unclear whether belly nosing and flank biting are different (12) observed 1–60 flank biting behaviors per hour per pen in behaviors linked with each other or perhaps behaviors with the weaner pigs. Due to the large number of animals in the pen, scan same motivational backgrounds. sampling was chosen as a feasible method. The current study The number of linear lesions increased during the first week included all nosing and biting events during scan sampling of a after weaning, paralleling the increase in circular lesions. These large pen and a group of pigs. linear lesions are assumed to be caused by fighting between pigs While very little is known about flank manipulation, more for resources such as feeder space after weaning from the sow. information is available on belly nosing, which appears to be The number of linear lesions indeed indicated that better gaining somewhat similar behavior. Both behaviors are directed to the weaners engaged in more fighting than pigs gaining weight more middle part of the trunk and involve nose contact. Belly nosing slowly, as fighting activity is correlated with more lesions (20). behavior is considered to be linked with general nosing activity Tail lesions were very rare and mild, and their occurrence (14, 15), peaking 2–3 weeks after weaning in piglets weaned displayed no marked temporal patterns, in contrast to the other at 12 or 21 days of age (16). Piglets weaned at the age of 4 lesion types, which suggests that the risk factors for tail lesions weeks exhibited a peak in belly nosing frequency 2 weeks after are not the same as for circular flank lesions. However, the weaning (17, 18). The increase in disturbing behaviors after housing system on the present farm includes several features that weaning perhaps indicates negative effects on welfare caused by are known to reduce the risk of tail biting, including straw (21), abrupt weaning. Belly nosing behavior increased in a stressful wooden logs (22), and a low animal density (23). environment (with unfamiliar conspecifics, no straw, and less In the current study, lesion occurrence was related to the space allowance) after weaning (19). Belly nosing piglets tended whiter trunk coloration of the pigs. It is possible, that this was to grow slower than others after weaning and are suggested merely due to the white trunk coloration making lesions more to be affected by nutritional needs, which motivate massage- visible, not to trunk coloration being an actual risk factor for like behavior (15). On the other hand, belly nosing behavior lesions. However, color of the skin could potentially also be intermingled in sequences with social interaction, suggesting linked to personality traits (24). However, as trunk coloration that the motivational background is related to social needs (14). has not been reported in earlier studies, the significance of it is Some piglets perform more belly nosing and some less, but it difficult to assess. We thus recommend reporting skin color in is generally performed by the majority of piglets (14). However, connection with lesion scoring results. Frontiers in Veterinary Science 06 frontiersin.org Norring et al. 10.3389/fvets.2022.1070206 5. Conclusion wrote the first draft of the manuscript. All authors contributed to manuscript revision, read, and approved the submitted version. Flank lesions increased after weaning at the age of 9 weeks and peaked during the 3rd week after weaning in this group. The emergence of flank lesions is possibly connected to weaning- Acknowledgments related factors. The authors wish to thank the farmer for providing access to the pigs and the GroupHouseNet (COST Action CA15134), an Data availability statement EU funded project, which made H-LK’s trip to Helsinki possible. The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation. Conflict of interest The authors declare that the research was conducted in the Ethics statement absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The animal study was reviewed and approved by National Animal Experiment Board, Complied European Directive 2010/63. Written informed consent was obtained from the Publisher’s note owners for the participation of their animals in this study. All claims expressed in this article are solely those of the authors and do not necessarily represent those Author contributions of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be MN, H-LK, and AV contributed to conception and design evaluated in this article, or claim that may be made by of the study. H-LK organized the database and wrote sections its manufacturer, is not guaranteed or endorsed by the of the manuscript. MN performed the statistical analysis and publisher. References 1. Camerlink I, Turner SP. Farmers’ perception of aggression between growing 11. Brunberg E, Wallenbeck A, Keeling LJ. Tail biting in fattening pigs: pigs. Appl Anim Behav Sci. (2017) 192:42–7. doi: 10.1016/j.applanim.2016. associations between frequency of tail biting and other abnormal behaviours. Appl 11.009 Anim Behav Sci. (2011) 133:18–25. doi: 10.1016/j.applanim.2011.04.019 2. 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