Pain assessment in animal models: do we need further studies?

Figures & data

Table 1 Articles analyzing pain evaluation in cattle

First author	Publication year	Animal model	Pain evaluation in cattle
Newby et al^Citation23	2013	Cows	Behavioral assessment with an ethogram
Bruijnis et al^Citation19	2012	Cattle	Locomotion score
O’Driscoll et al^Citation20	2009	Cows	Locomotion score
Saeed et al^Citation24	2008	Calves	RR, HR, ability to change posture
Coetzee et al^Citation25	2008	Calves	Vocalization and change in attitude or temperament
Rajkondawar et al^Citation21	2006	Cows	Reaction after claw compression and gait score
Thoefner et al^Citation22	2004	Heifers	Evaluation of lameness, signs of claw inflammation, cardiovascular function, gastrointestinal function

Abbreviations: HR, heart rate; RR, respiratory rate.

Table 2 Articles analyzing pain evaluation in ponies

First author	Publication year	Animal model	Pain evaluation in ponies
Freitas et al^Citation30	2011	Ponies	Lameness, HR, SAP, RR, T, intestinal motility
Boatwright et al^Citation27	1996	Ponies	CPS – kicking, pawing, head movement
Roelvink et al^Citation28	1991	Ponies	Head-shaking, flehmen, yawning, stretching, restlessness, leaning against the stocks, looking at the abdomen, kicking the abdomen and pawing the ground
Fikes et al^Citation29	1989	Ponies	Movement, attempts to kick, turning the head towards the site of a pin prick
Pippi et al^Citation26	1978	Ponies	Superficial, deep, and visceral pain tests

Abbreviations: CPS, composite pain scale; HR, heart rate; RR, respiration rate; SAP, systolic arterial pressure; T, body temperature.

Table 3 Articles analyzing pain evaluation in sheep

First author	Publication year	Animal model	Pain evaluation in sheep
Yong et al^Citation39	2014	Sheep	Gait abnormalities, teeth-gnawing, social isolation
Wilkes et al^Citation32	2012	Sheep	Hind limb withdrawal thresholds
Hee et al^Citation40	2011	Sheep	Animal alertness, movement, flock behavior, feeding behavior, and respiratory rate
Dolan et al^Citation31	2011	Sheep	Withdrawal response to mechanical stimulation; time spent not bearing weight or flinching
Stubsjøen et al^Citation33	2010	Sheep	Lifting the limb after tourniquet inflation
Wegener et al^Citation37	2009	Sheep	Limping and other signs of pain
Stubsjøen et al^Citation41	2009	Sheep	Eye temperature, heart rate, heart rate variability, blood pressure, vocalization, lip-licking, ear posture
Houfflin Debarge et al^Citation38	2005	Sheep	Nociceptive flexion reflex, neurovegetative response (mean aortic pressure and fetal heart rate), EMG
Johansen et al^Citation36	2004	Sheep	Appetite, posture, ambulation, herding activity, reaction to the environment, and rectal body temperature Behavior and motor function recorded on a four-grade scale
Jongman et al^Citation43	2000	Sheep	EEG changes
Mather et al^Citation35	2000	Sheep	Foreleg lift escape response
Ong et al^Citation34	1997	Sheep	Escape-avoidance responses to the electrical stimuli
Welsh et al^Citation42	1993	Sheep	VAS and NRS score

Abbreviations: EEG, electroencephalography; EMG, electromyography; NRS, numerical rating scale; VAS, visual analog scale.

Table 4 Articles analyzing pain evaluation in horses

First author	Publication year	Animal model	Pain evaluation in horses
van Loon et al^Citation55	2012	Horses	CPS with physiological response to treatment and behavioral data
Foreman et al^Citation50	2012	Horses	Lameness scale and HR
Cayzer et al^Citation53	2012	Horses	Flexion test, response to pain in palpation of joints, swelling flexion test, swelling
Scantlebury et al^Citation56	2011	Horses	Signs of colic and clinical signs
Foreman et al^Citation48	2011	Horses	Lameness score and HR
Fureix et al^Citation60	2010	Horses	Increased aggressiveness towards humans
Foreman et al^Citation49	2008	Horses	Lameness score and HR
Bussières et al^Citation54	2008	Horses	CPS with physiological response to treatment and behavioral data
Haussler et al^Citation59	2007	Horses	Avoidance reactions
Frisbie et al^Citation46	2006	Horses	Lameness
Seino et al^Citation51	2003	Horses	Lameness score and HR
Buchner et al^Citation45	2001	Horses	Lameness
Cornelissen et al^Citation52	1998	Horses	Lameness scale and local signs
Hamm et al^Citation57	1997	Horses	Subjective signs of carpal pain and clinical signs
Buchner et al^Citation44	1996	Horses	Lameness score
Miller et al^Citation58	1995	Horses	EEG, EMG HR, BP
Collier et al^Citation47	1985	Horses	Lameness score and clinical signs (heat and swelling)

Abbreviations: BP, blood pressure; CPS, composite pain scale; ECG, EMG, electromyography; EEG, electroencephalography; HR, heart rate.

Table 5 Articles evaluating pain in pigs

First author	Publication year	Animal model	Pain evaluation
Royal et al^Citation87	2013	Pigs	HR, RR, subjective pain assessment with a modified VAS
Di Giminiani et al^Citation85	2014	Pigs	Body movement, rubbing, muscle twitches Leg movements, lifting the leg, kicking
Navarro et al^Citation75	2012	Minipigs	Withdrawal response to a mechanical stimulus, vocalization, muscle hypertonia and hyperreflexia, anal sensation, and presence of allodynia
Mustonen et al^Citation78	2012	Pigs	General behavior, RR, locomotion, rectal temperature
Janczak et al^Citation86	2012	Piglets	Withdrawal response
Kluivers-Poodt et al^Citation68	2012	Piglets	Vocalization
Sutherland et al^Citation76	2012	Pigs	Scooting, sitting, huddling, vocalization
Rault et al^Citation81	2011	Piglets	Tail-wagging, huddling up, trembling, stiffness, lying prostrate, spasms, scratching, sleep spasms
Van Beirendonck et al^Citation82	2011	Piglets	Huddling up, trembling, spasms, scratching, tail-wagging
Mustonen et al^Citation79	2011	Sows	Lameness
Lupu et al^Citation74	2010	Pig	Vocalization and/or withdrawal of the forelimb
Murison et al^Citation77	2009	Pigs	Wound palpation, behavior, and locomotion scoring
Rukwied et al^Citation89	2008	Pigs	Reflex erythema
Carroll et al^Citation84	2006	Pigs	Active, lying, sitting, standing, and nursing
Haga et al^Citation88	2005	Piglets	EEG, MAP, pulse rate
Walker et al^Citation70	2004	Piglets	Vocalization and movement
Friton et al^Citation80	2003	Pigs	Lameness, food intake, behavior
Reyes et al^Citation71	2002	Piglets	Lameness, isolation, posture, vocalization, aggression, restlessness, agitation, and playfulness
Harvey-Clark et al^Citation83	2000	Pigs	Inactivity, recumbency, aggression, depression, head-pressing, coprophagy, stereotypical chewing, changes in activity
Cornefjord et al^Citation90	1995	Pigs	Increase in substance P

Abbreviations: EEG, electroencephalography; HR, heart rate; MAP, mean arterial blood pressure; RR, respiratory rate; VAS, visual analog scale.

Table 6 Biological similarities between humans and large animals

1. Phylogenetic proximity:

– Greater sequence homology

– Better prediction of human metabolism

– Less species-specific variations in sequence patterns

– Different evolutionary pressure

2. Median body size

3. Humans and pigs are both omnivorous

4. Similar digestive apparatus with porcine species

5. Similarity with porcine skin:

– Number, size, distribution, and communications of dermal vessels

– Tissue turnover time

– Keratinous proteins in the epidermis

– Epidermal–dermal junctions

6. Immunoreactivity in the peptide nerve fibers

7. Similarities in nociceptive and non-nociceptive fiber classes

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