ttp:// The lack of analgesic use (oligoanalgesia) in small animal practice REVIEW

ttp://www.bsava.com/ REVIEW The lack of analgesic use (oligoanalgesia) in small animal practice B. T. Simon *, E. M. Scallan *, G. Carroll * and P. V. Steagall *Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, 77843-4474, USA Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Montreal, 3200 Rue Sicotte, Saint-Hyacinthe, Quebec, J2S2M2, Canada 1 Corresponding author email: BSimonDACVAA@gmail.com Oligoanalgesia is defined as failure to provide analgesia in patients with acute pain. Treatment of pain in emergencies, critical care and perioperatively may influence patient outcomes: the harmful practice of withholding analgesics occurs in teaching hospitals and private practices and results in severe physiological consequences. This article discusses the prevalence, primary causes, species and regional differences and ways to avoid oligoanalgesia in small animal practice. Oligoanalgesia may be addressed by improving education on pain management in the veterinary curriculum, providing continuing education to and implementing pain scales. Journal of Small Animal Practice (2017) 58, 543 554 DOI: 10.1111/jsap.12717 Accepted: 3 May 2017; Published online: 1 August 2017 INTRODUCTION Pain and its physiological effects A new definition of pain has been recently suggested: a distressing experience associated with actual or potential tissue damage with sensory, emotional, cognitive, and social components (Williams & Craig 2016 ). Pain may produce serious deleterious physiological consequences (Table 1 ) and further damage a patient s physical status (Wiese & Muir 2005 ). Failure to address acute perioperative pain can result in peripheral and central sensitisation and the development of neuropathic and maladaptive pain (Torebjork et al. 1992, Katz et al. 1996, Kalso et al. 2001, Nikolajsen et al. 2006, Poleshuck et al. 2006, Johansen et al. 2012, Masselin-Dubois et al. 2013 ). For example, inadequate management of postoperative pain following thoracotomy (Katz et al. 1996, Perttunen et al. 1999, Kalso et al. 2001, Pluijms et al. 2006 ), mastectomy (Poleshuck et al. 2006 ), orthopaedic (Nikolajsen et al. 2006 ), Caesarean section (de Brito Cancado et al. 2012 ), laparoscopy (Blichfeldt-Eckhardt et al. 2014 ) and inguinal herniorrhaphy (Aasvang & Kehlet 2005, Manangi et al. 2014 ) procedures produced long-term maladaptive pain in humans. Peripheral and central sensitisation lowers the pain threshold to both noxious (hyperalgesia) and innocuous (allodynia) stimuli, further exacerbating the patient s painful condition (Moore 2016 ). The objectives of this study are to discuss oligoanalgesia, the failure to recognise and provide analgesia in patients with acute pain (Wilson & Pendleton 1989 ), and suggest methods to improve the recognition and treatment of pain. ORIGINS OF OLIGOANALGESIA AND ITS PREVALENCE IN HUMAN MEDICINE Oligoanalgesia was first discussed by human physicians in the early 1970s (Marks & Sachar 1973 ) and is still a concern in human and veterinary hospitals worldwide (Wilson & Pendleton 1989, Jantos et al. 1996, Mcgrath & Frager 1996, Todd et al. 2007, Carter et al. 2016 ). A multi-centre study reported a high prevalence of pain and suboptimal pain management in 20 United States and Canadian emergency departments, reinforcing the need for further improvement in this area (Todd et al. 2007 ). The lack of analgesic administration in human emergency departments occurs: (1) in routine procedures that are not deemed to be painful ; (2) in patients reluctant or unable to vocally express their pain (Allione et al. 2011 ); (3) because of inappropriate pain assessment or documentation; (4) through allocation of inadequate time for evaluating pain due to overcrowded emergency departments; (5) in non-urgent triage codes where a patient does not require immediate attention; (6) in patients who described their pain as burning and constant; and, (7) in pain located at the extremities, back, nose or ear (Guru & Dubinsky 2000, Rupp & Delaney 2004, Allione et al. 2011 ). Factors such as extremes of age (Jones et al. 1996, Alexander & Manno 2003, Platts-Mills et al. 2012 ), gender (Chen et al. 2008 ), Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association 543

B. T. Simon et al. Table 1. Physiological consequences associated with inadequately treated acute and chronic (maladaptive) pain. (Extrapolated from Wright 2002 ) Physiological consequences associated with inadequately treated pain Acute pain Tachycardia Vasoconstriction Bronchoconstriction Tachypnea Ileus Increased myocardial workload Increased oxygen consumption Chronic (maladaptive) pain Increased release of: Cortisol Glucagon Antidiuretic hormone Aldosterone Angiotensin Growth Hormone Catecholamines Renin Interleukin-1 Cyclic adenosine monophosphate Decreased release of: Insulin ethnicity and race (Todd et al. 1993, Choi et al. 2000, Goldfrank & Knopp 2000 ) also resulted in the decreased administration of analgesic therapy. These factors in humans offer a rich area of study in veterinary medicine. PREVALENCE AND MANAGEMENT OF PAIN Within the veterinary intensive care unit and emergency department Sedation and analgesia are commonly required in the emergency critical care units. Critically ill may be defined as patients suffering from dysfunction of one or more organ systems and evidence of hypoperfusion. These patients are at a high risk of experiencing pain due to several factors, including recent surgery, acute trauma or systemic illness (pancreatitis, cancer). Since the early 1980s, provision of adequate pain relief has been recognised as both a challenge and historical problem in small animal practice (Tables 2 and 3 ) (Hansen & Hardie 1993, Joubert 2001, Wiese & Muir 2005, Hewson et al. 2006b, Joubert 2006, Lorena et al. 2014, Hunt et al. 2015 ). In 2010, The University of Georgia Veterinary Teaching Hospital evaluated the prevalence of postoperative pain in dogs in the small animal intensive care unit (Moran & Hofmeister 2013 ). Pain was evaluated by a second-year veterinary student using three different scoring systems: Glasgow composite pain scale, a visual analogue scale and a simple descriptive scale, and 22% of dogs were considered to be painful. This percentage is lower than previously reported in critically ill patients (39 to 55%) (Armitage et al. 2005, Wiese & Muir 2005 ). However, despite some training, veterinary students routinely lack the skill necessary to assess pain when compared with experienced anaesthesiologists (Barletta et al. 2016 ). Therefore, in this study, pain might have been under-diagnosed, and its prevalence in the postoperative period might be higher than reported. In the Georgia study, 6 out of the 37 dogs exhibiting pain did not receive analgesics during their intensive care unit stay (Moran & Hofmeister 2013 ). Dose and routes of administration of analgesics were not reported for those with signs of pain in the study, and therefore, it is not clear if this lack of analgesic administration was due to suboptimal dosing, frequency or inappropriate drug selection. Aggression has been reported as an indicator of pain (Hinde 1969 ), but aggressive patients were excluded, potentially lowering the overall prevalence of painful patients in this study. Multi-centre studies using highly experienced anaesthesiologists in the assessment of pain are necessary to determine the prevalence of oligoanalgesia in the intensive care unit and if data can be extrapolated to different settings. The percentage of painful small animal patients recognised in a veterinary teaching hospital emergency department has been found to be higher than that in an intensive care unit (Wiese & Muir 2005, Moran & Hofmeister 2013 ). In one study, 239 of 429 (56%) emergency department patients had signs of pain, and the percentage of pain amongst dogs and cats were similar: 179 of 317 (56%) and 60 of 112 (54%), respectively (Wiese & Muir 2005 ), 41% (73/179) of dogs in pain and 52% (31/60) of cats in pain received adequate analgesia. Although multi-modal analgesia has been advocated to provide enhanced pain relief and reduce side effects (Kehlet & Dahl 1993, Brondani et al. 2009, Steagall & Monteiro-Steagall 2013 ), it was received by only 28% of dogs and 46% of patients in pain in this emergency department. Within the veterinary outpatient service The prevalence of pain in veterinary outpatients is lower than in other settings (intensive care unit, emergency department), in a 2002 survey, only 20% of dogs (231/1153) and 14% (92/652) of cats entering a veterinary teaching hospital were considered to be in pain (Muir et al. 2004 ). In this subpopulation, older obese patients experienced more pain that was of acute duration (<7 days) and moderate in intensity. Dogs and cats more often experienced somatic deep pain and visceral pain, respectively. Lameness and behavioural changes were the most common signs of pain in dogs and cats, respectively. Central sensitisation, determined when an animal responded unfavourably to a light touch distant from the primary site of pain, was diagnosed in approximately 15 to 17% of the total outpatient population. Observers must be able to recognise, categorise and objectively assess patients for effective treatment, and although owners are familiar with their animal s normal behaviour, they lack formal training in pain assessment, implying that they may not recognise pain in their own animals. Similar to the other studies, it is unclear whether analgesic choice, dose, frequency or the inability to assess pain as an outpatient was the primary reason for its inadequate treatment. Within the perioperative period All surgical procedures involve a noxious stimulus that can be perceived as pain in an awake patient. Based on this definition, it would be appropriate to uphold that all animals undergoing a surgical procedure should receive multi-modal analgesia. Indeed, a review article (Gurney 2012 ) on the use of perioperative analgesic techniques was based on the premise that pre-emptive and 544 Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association

Oligoanalgesia in small animal practice Table 2. Studies depicting the prevalence of oligoanalgesia in University Teaching Hospitals since 1983 Veterinary services assessed, country (year[s] of assessment) Prevalence of pain: affected animals/n (%) Prevalence of pain adequately treated: adequately treated animals/animals in pain (%) Prevalence of multi-modal analgesia: animals received multi-modal analgesia/ animals received any form of analgesia (%) Study design, assessment of pain and scoring system(s) used Most common analgesics administered Comments References Dogs Cats Dogs Cats Dogs Cats North Carolina State University Teaching Hospital surgical database (1983 to 1989) The Ohio State University Veterinary Teaching Hospital outpatient database (2002) The Ohio State University Veterinary Teaching Hospital emergency department (2003) University of Georgia Veterinary Teaching Hospital ICU department (2010) 243/243 (100*) 231/1153 (20) 179/317 (56) 37/170 (27) 15/15 (100*) 92/652 (14) 60/112 (54%) 96/243 (40) 57/231 (24) 73/179 (41) NA 31/37 (84) 1/15 (7) NA NA Retrospective cross-sectional observational study, Medical records were evaluated for reports of pain ( crying, thrashing, pain, extremely uncomfortable ) written into records by students and ICU technicians. Students and technicians received no formal pain assessment training. 5/92 (5) 5/57 (9) 0/5 (0) Prospective cross-sectional observational study; all dog and cat owners were administered a from three at time of visit. Veterinarians who administered the received three training and two Q&A sessions, but pet owners did not. 31/60 (52) 33/119 (28) 19/41 (46) Prospective cross-sectional observational study; At least one of four staff completed a following an examination in all dogs and cats admitted to the ED. Staff completed three training and three3 question & answer (QA) sessions before the study and one QA session two months after the study begun. NA NA NA Prospective cross-sectional observational study; An independent second-year veterinary student observer completed a VAS, SDS and Glasgow pain scoring system twice daily for all eligible dogs in ICU. Students spent two weeks learning how to pain score under a DACVAA before the study. Opioids (Buprenorphine, morphine, butorphanol), regional nerve blocks, aspirin NSAIDs and opioids (dogs), corticosteroids and NSAIDs (cats) Carprofen, deracoxib, hydromorphone (dogs and cats), butorphanol (cats) Hydromorphone followed by buprenorphine. Other analgesics (NSAIDs) were administered but not reported Only 8/61 (13%) dogs that underwent a thoracotomy were given analgesics at extubation. Medical record terms such as PRN and as needed may discourage analgesic treatment. Most common signs of pain: Dogs: Somatic musculoskeletal; Cats: visceral. NSAIDs were only effective in resolving chronic pain in 15/24 (63%) of patients. Multi-modal analgesia was effective in all patients. Unimodal drug therapy was effective in 47% and 73% of dogs and cats, respectively. Most common pain: acute, moderate, inflammatory and somatic pain. Most common pain: Orthopaedic and neurosurgical. Hansen & Hardie 1993 Muir et al. 2004 Wiese & Muir 2005 Moran & Hofmeister 2013 N Total animals, Q&A question and answer, US United States, ED emergency department, ICU intensive care unit, DACVAA Diplomate American College Veterinary Anaesthesiology and Analgesia, VAS visual analogue scale, SDS simple descriptive scale, NSAIDs Non-steroidal anti-inflammatories, PRN pro re nata (as necessary) * Only patients considered to have had painful procedures were analysed Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association 545

B. T. Simon et al. Table 3. Studies on the use of analgesics amongst general practitioners worldwide after 1996 Country/ Geographic area and year of surveyed Study design; response rate (Surgical procedure) Veterinarians considered adequate use of analgesics /total surveyed (%) Confidence in knowledge about pain management and assessment (%) Most common analgesics administered by (% of animals received) Dogs Cats Dogs Cats Canada (~1996)* United Kingdom (1996) A paper to Canadian in mixed or companion animal practice; 275/417 (66) A paper to 2000 UK practices in 1996; 958/2000 (48) (Orthopaedic and cruciate)) 220/275 (80); (Laparotomy, not OVH)) 105/275 (38); (OVH)) 36/275 (13); (castration)) 30/275 (11) (Orthopaedic) 927/958 (97); (Laparotomy, not OVH 677/958 (71); (OVH) 511/958 (53); castration 310/958 (32) (orthopaedic and cruciate) 193/275 (70); (Laparotomy, not OVH) 121/275 (44); (OVH) 47/275 (17); (castration) 25/275 (9); (onychectomy) 132/275 (48) (Orthopaedic) 900/958 (94); (Laparotomy, not OVH) 536/958 (56); (OVH) 278/958 (26); castration 153/958 (16) 91/275 (33) Butorphanol (40), meperidine (26), oxymorphone (12) NA Buprenorphine, carprofen Butorphanol (42), meperidine (16), morphine (8) Buprenorphine, butorphanol, ketoprofen, tolfenamic acid South Africa (1999) 600 paper s were distributed to South African in 1999; 161/600 (27) (OVH and castration) 50/161 (31) (OVH and castration) 106/161 (66) NA Flunixin meglumine, (83), phenylbutazone (70), aspirin (49), pethidine (44), ibuprofen (34), xylazine (24), meloxicam (24) France (1999) A paper to French small animal practice ; 189/379 (50) (Orthopaedic) 158/189 (84); (OVH) 68/189 (36); (castration) 32/189 (17); (feline onychectomy) 109/189 (58) 77/189 (41) Gluco-corticoids (97), NSAIDs (100), ketamine (40%), α - 2 agonists (37), opioids (16) Gluco-corticoids (97), NSAIDs (100),ketamine (40), α - 2 agonists (31), opioids (8)* Concerns associated with perioperative analgesic use (species) Sedation (dog), excitement (cat), respiratory depression, bradycardia, record keeping, human abuse potential Drug adverse effects (excitement [cats], sedation [dogs]), available information, record keeping Adverse effects, lack of knowledge Difficulty in recognising pain, lack of knowledge about therapy, fear of drug adverse effects (respiratory depression, excitement [cats], sedation [dogs]), fear of suppressing protective nociception Comments Reference Women, younger and recent graduates were more likely to provide analgesics. Butorphanol was the most commonly used analgesic for pain management during orthopaedic surgery. Ketoprofen was not yet licensed during the survey. Dohoo & Dohoo 1996a, b Women were more likely than men to provide analgesics for surgery; 6.5% of felt that surgery did not usually elicit a painful enough stimulus to warrant analgesics. Recent graduates (1990s) assigned higher pain scores than older graduates. NSAIDs were the most common postoperative analgesic administered; 3% of did not administer postoperative analgesia for sterilisation procedures in dogs and cats. Continuing education was thought to improve the administration of analgesic agents. French felt their veterinary curriculum failed to teach pain management in animals 138/183 (75). Believe signs of pain do not differ between dogs and cats. Capner et al. 1999, Lascelles et al. 1999 Joubert 2001 Hugonnard et al. 2004 546 Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association

Oligoanalgesia in small animal practice Table 3 (Continued) Country/ Geographic area and year of surveyed Study design; response rate Canada (2001) A paper to Canadian in mixed or companion animal practice; 326/564 (58) New Zealand (2002) Finland (~2003) A paper to New Zealand small animal practice ; 302/1200 (28) A paper to 911 Finnish small animal practice ; 434/911 (48) Brazil (2007 2008) Questionnaires were distributed during national events to small animal and available online in Brazil from 2007 to 2008; 1298 respondents (Surgical procedure) Veterinarians considered adequate use of analgesics /total surveyed (%) Confidence in knowledge about pain management and assessment (%) Most common analgesics administered by (% of animals received) Dogs Cats Dogs Cats (Orthopaedic) 293/326 (90); (OVH) 140/326 (43); (castration) 120/326 (37) (Orthopaedic) 293/326 (90); (OVH) 130/326 (40); (castration) 98/326 (31); (Onychectomy) 254/326 (77) 157/320 (49) Butorphanol (49), meperidine (16), ketoprofen (18), meloxicam (12) Butorphanol (54, meperidine (11), ketoprofen (27), meloxicam (8) Concerns associated with perioperative analgesic use (species) No substantial risks of using NSAIDs, morphine or butorphanol were identified. Potential risk of opioidinduced respiratory depression in cats. (Orthopaedic) 285/320 (89); (soft tissue) 230/320 (72) (Orthopaedic) 245/320 (77); (soft tissue) 204/320 (64) 174/302 (58) Morphine, pethidine, buprenorphine, carprofen, meloxicam, local anaesthetics Morphine, pethidine, buprenorphine, carprofen, meloxicam Fear of drug adverse effects (sedation, respiratory depression, bradycardia), available information, record keeping, (castration) (~47); OVH (~70) (castration) (~12); OVH (~21) 236/414 (57) Opioids, NSAIDs, local anaesthetics Pain may be useful in preventing excessive movement, lack in ability of detecting pain, adverse effects (OVH) 1168/1298 (90); (orthopaedic) 1233/1298 (95); (OVH) 1012/1298 (78); (orthopaedic) 1207/1298 (93) 506/1298 (39) Tramadol (79), morphine (51), meloxicam (81), ketoprofen (70), carprofen (60), local anaesthetic nerve blocks (56), Potential adverse effects of opioids (respiratory depression, emesis, excitement) and NSAIDs (gastric toxicity, nephrotoxicity), cost, available information on opioids and NSAIDs. Comments Reference Continuing education appeared the best source of knowledge about perioperative analgesia. Only 34% of castration and 45% of OVH patients received postincisional analgesia. Over 5500 OVH and 6200 castration patients (dogs and cats) were estimated to not receive any analgesia in Canada during 2001. Regional lectures/seminars and review articles in journals were the most valuable sources for gaining knowledge on recognising and treating pain Hewson et al. 2006a, b Williams et al. 2005 Younger and those in larger practices had more choice of analgesic drugs than older in smaller practices. Women and younger treated pain more frequently than men and older. Clinical experience, national and regional meetings and courses were reported by Brazilian as the best way to enhance knowledge about pain and analgesia. Approximately 70% and 54% of dogs and cats received postoperative analgesia following orthopaedic surgery and ovariohysterectomy, respectively. Raekallio et al. 2003 Lorena et al. 2014 Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association 547

B. T. Simon et al. Table 3 (Continued) Country/ Geographic area and year of surveyed Switzerland (2010 2011) Study design; response rate A paper and electronic to 1000 Swiss ; 258/1000 (26) (Surgical procedure) Veterinarians considered adequate use of analgesics /total surveyed (%) Confidence in knowledge about pain management and assessment (%) Most common analgesics administered by (% of animals received) Dogs Cats Dogs Cats (OVH) 254/258 (98) (OVH) 239/258 (92) (castration) 238/258 (92); (Laparotomy, not OVH) 256/258 (99) 32/258 (13) Meloxicam (79), caprofen (75), butorphanol (51), local anaesthetics (44), buprenorphine (40), tolfenamic acid (38), methadone (22) United Kingdom (2013) A cross-sectional survey distributing 4100 written s to in small animal practice in the UK in 2013; 665/4100 (16) (castration, OVH, lump removal) 605/665 (91) (castration, OVH, lump removal) 545/665 (82) NA Buprenorphine, butorphanol, methadone, morphine, meloxicam, carprofen, firocoxib NA not assessed, NSAID Non-steroidal anti-inflammatory, UK United Kingdom, OVH ovariohysterectomy * Evaluated postoperative analgesia only Overall, cats were less likely to receive analgesics when compared to dogs Veterinarians always prescribing analgesics and/or local regional anaesthesia Concerns associated with perioperative analgesic use (species) Comments Reference Price, adverse effects, lack of pharmacological knowledge Recent graduates were more satisfied with their veterinary school education on pain and analgesia. Respondents stated that scientific reviews and websites dedicated to pain and analgesia would be sufficient forms of continuing education. NA Postoperative NSAIDs were administered less in cats (33%) than dogs (75%); 31% of cases received local regional analgesia. Increase in analgesic administration by when compared to 1996. Perret- Gentil et al. 2014 Hunt et al. 2015 548 Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association

Oligoanalgesia in small animal practice multi-modal analgesia were and are currently accepted practices. Hansen & Hardie ( 1993 ) published one of the first studies evaluating the use of postoperative analgesics in a veterinary teaching hospital during a six-year period (1983 to 1989). Out of 243 dogs and 15 cats that underwent various surgeries, only 96 (40%) dogs and 1 (15%) cat received analgesia following the procedure (Hansen & Hardie 1993 ). Medical records of cats indicated that these patients had moderate to severe pain, but they did not receive analgesics, similarly, almost 20% of the dogs that were supposed to receive analgesics if necessary did not receive them. Patients with documented orders written as analgesics as needed or if in extreme pain experienced resulting delays in the ordering and administration of analgesics (Hansen & Hardie 1993 ). These types of connotations permit too much subjectivity when assessing pain in veterinary patients. Lastly, patients that were transferred to the surgery ward rather than the intensive care unit were less likely to receive perioperative analgesics (Hansen & Hardie 1993 ). This discrepancy was attributed to differences in monitoring between the intensive care unit and surgery ward: intensive care units typically have more diligent monitoring and can effectively identify and manage potential analgesic-induced adverse effects if they occur. Over time, patient pain assessment decreased (45, 32 and 19% following Day 1, 2 and 3 of surgery, respectively) (Hansen & Hardie 1993 ). The lack of pain assessment has been shown to decrease analgesic administration in critical patients, which may have contributed to the inadequate pain control (Rose et al. 2013 ). Hansen & Hardie ( 1993 ) utilised students and intensive care unit technicians to monitor postoperative signs of pain. No objective assessment techniques or training were used to appropriately evaluate pain in these patients. These factors may have contributed to the lack of analgesic treatment, but pain recognition and treatment were not sophisticated at that time. Amongst the 275 Canadian small animal practitioners surveyed, less than 45 and 40% of cats and dogs (Dohoo & Dohoo 1996b ), respectively, undergoing abdominal surgeries except ovariohysterectomy received postincisional analgesia. During this period, in the UK administered analgesics to dogs undergoing an ovariohysterectomy or castration 53 and 32% of the time, respectively (Capner et al. 1999 ). Cats in the UK also received analgesia far less frequently than is now considered appropriate, at 26 and 16% for ovariohysterectomy and castrations, respectively (Lascelles et al. 1999 ). FACTORS AFFECTING ANALGESIC ADMINISTRATION Historical factors The lack of analgesia prescribed during the 1980s to 1990s may be multi-factorial. The adverse effects associated with analgesics, particularly opioids, may have persuaded to avoid their use except in cases of severe pain. Brock ( 1995 ) emphasised the importance that owners put on pain management, the need for opioids in treating pain and the rare occurrences of clinical adverse effects associated with opioid administration when pain is present (Simon & Steagall 2016 ). During this same period, our understanding of the pathophysiology of pain in veterinary medicine was developing, and validated means to assess pain in dogs and cats were non-existent. Veterinarians were unlikely to have been taught pain assessment in their veterinary curriculum. Studies describing the benefits of treating pain (improved patient outcomes, shorter time to discharge) were also lacking, which made it more difficult for to see the long-term advantages. With a better understanding of pain physiology, assessment and therapy, greater importance on pain management taught in the veterinary curriculum and expected by clients, and increased availability of licensed analgesic drugs, mean that use of perioperative analgesia in routine practice has increased worldwide (Armitage et al. 2005, Joubert 2006, Hewson et al. 2006b, Lorena et al. 2014, Hunt et al. 2015 ). In 2004, clinicians in a teaching hospital in the USA administered postoperative analgesics to 98% of its small animal population for at least 24 hours after surgery (Armitage et al. 2005 ). In a recent survey (response rate 16%), more than 90% of private practitioners in the UK administered some sort of perioperative analgesia for routine procedures (Hunt et al. 2015 ). In 2001, a survey of 652 randomly selected Canadian practitioners (response rate 57.8%) showed that more than 85% of feline and canine ovariohysterectomy and castration cases received analgesia before, after or before and after surgery (Hewson et al. 2006b ). Furthermore, the use of postincisional analgesia for ovariohysterectomy and castration procedures has increased threefold and other abdominal surgery increased twofold since the early 1990s (Hewson et al. 2006b ). Despite this improvement, of the 280 veterinarian respondents, approximately 55 and 65% of dogs and cats, respectively, still do not receive postincisional analgesia following ovariohysterectomies and castrations (Hewson et al. 2006b ). With this vast increase in the assessment and treatment of perioperative pain in the past 20 to 25 years, practitioners must be cautious with opioid overdosing and adverse effects induced by other classes of analgesics, such as nonsteroidal anti-inflammatory drugs (NSAID)s. This topic is beyond the scope of the review, but opioids have been associated with some deleterious effects (e.g. bradycardia, respiratory depression, aspiration pneumonia, dysphoria), which can be prevented or treated when appropriate (Simon & Steagall 2016 ). Regional factors The use of perioperative analgesia may also be dependent on geographical location (Farnworth et al. 2014 ). Postoperative pain has been consistently reported following neutering procedures in dogs and cats (Slingsby et al. 2006, Slingsby et al. 2011, Oliveira et al. 2014 ). Less than 11% of in New Zealand prescribed analgesics at the time of discharge for dogs and cats undergoing ovariohysterectomies and castrations (Williams et al. 2005 ). If the majority of these procedures are outpatient, analgesia was discontinued within 12 hours of the surgery. Preoperative and intraoperative analgesics were commonly administered during these surgical procedures for dogs (ovariohysterectomy 76%, castration 65%) and cats (ovariohysterectomy 64%, castration Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association 549

B. T. Simon et al. 50%) (Williams et al. 2005 ), but still less frequently than would provide optimal patient care. Orthopaedic procedures were routinely managed with analgesics (>90%) in both dogs and cats (Williams et al. 2005 ). Finnish administer analgesia to dogs and cats more often for an ovariohysterectomy (70 and 21%, respectively) when compared to castration (47 and 12%, respectively) (Raekallio et al. 2003 ). Brazilian routinely administered analgesic drugs pre-/intraoperatively during ovariohysterectomies in both dogs (90%) and cats (78%) (Lorena et al. 2014 ). Postoperative analgesics were only provided ~50% of the time in both species (Lorena et al. 2014 ). Swiss also provided significantly more analgesia before surgery (71 to 96%) compared to after surgery (2 to 23%) (Perret-Gentil et al. 2014 ). Drug availability may affect the frequency of analgesic administration, specifically that of opioids in each country. The overall use of opioid analgesics remains low in Africa, Asia, Central America, Caribbean, South America and eastern and southeastern Europe (Berterame et al. 2016 ). In Oceania, restricted financial resources, issues in sourcing from industry or imports and import and export authorisation and control measures are the main obstacles for analgesic administration (Berterame et al. 2016 ). Cultural attitudes related to opioid dependence may negatively influence the treatment of pain and the use of opioid analgesics in countries located in North America, South America and western and central Europe (Berterame et al. 2016 ). Despite these findings, the overall use of opioids in these countries has increased (Duthey & Scholten 2014 ). Species factors In one emergency department, cats (68%) were slightly more likely to receive analgesic therapy compared with dogs (66%) (Wiese & Muir 2005 ). Response to pain therapy also appeared better in cats (Wiese & Muir 2005 ). Dog outpatients [57/231 (25%)) were more likely to be treated with analgesics than cat outpatients [5/92 (5%)] (Muir et al. 2004 ). However, cats [5/5 (100%)] were more effectively managed for pain when compared with dogs (25/57 [44%]), although these low numbers preclude drawing precise conclusions (Muir et al. 2004 ). Perioperatively, cats routinely received fewer analgesics for most surgical procedures, especially opioids, when compared with dogs (Hansen & Hardie 1993, Capner et al. 1999, Lascelles et al. 1999, Raekallio et al. 2003, Hugonnard et al. 2004, Williams et al. 2005, Hewson et al. 2006a,b, Lorena et al. 2014, Perret-Gentil et al. 2014, Hunt et al. 2015 ). In contrast, a survey study performed in Brazil indicated no differences in the percentage of dogs and cats being treated with analgesics for surgical procedures (Lorena et al. 2014 ), 50% of these Brazilian respondents had participated in a continuing education, master s, PhD or residency programme, which may have biased the results. In Canada and the UK, cats were less likely to receive perioperative analgesia for orthopaedic, abdominal and castration surgeries when compared with dogs (Hewson et al. 2006b, Hunt et al. 2015 ). These disparities in the prevalence of analgesic administration may be due to the differences in the perception of pain for specific procedures between species, challenges in pain assessment including failure of recognition, level of education and fear of adverse effects produced by analgesics in general (Muir et al. 2004, Lorena et al. 2014 ). NSAID and opioid administration is used less frequently during castrations in cats when compared with dogs (Hunt et al. 2015 ). There was a lack of validated pain scoring systems in cats in past studies, which might have compromised the assessment of analgesia in this species. The assessment of pain in cats is difficult due to their stoic nature, which may contribute to the variation in analgesic administration (Hugonnard et al. 2004, Williams et al. 2005, Mathews et al. 2014 ). Recently, two composite measure pain scales, Glasgow and UNESP-Botucatu, have been validated for use in cats (Brondani et al. 2011, Brondani et al. 2013, Calvo et al. 2014 ). Discrimination using facial expressions may also provide a good indicator between cats in acutely pain and painfree cats (Holden et al. 2014 ). Additional factors affecting analgesic administration Several studies have provided reasons for oligoanalgesia in veterinary medicine (Hansen & Hardie 1993, Dohoo & Dohoo 1996b, Hugonnard et al. 2004, Muir et al. 2004, Wiese & Muir 2005, Hewson et al. 2006b, Hunt et al. 2015 ). Drug-induced adverse effects, cost of medication, drug availability, information/ evidence on a particular product for one or both species (canine and feline), potential for human drug abuse or lack of clinical experience and familiarity with the prescription and administration are still the major factors limiting the use of opioid and NSAIDs in dogs and cats (Dohoo & Dohoo 1996b, Lascelles et al. 1999, Hugonnard et al. 2004, Wiese & Muir 2005, Moran & Hofmeister 2013, Lorena et al. 2014, Hunt et al. 2015 ). Fear of diversion, theft and tampering may also preclude health care professionals from keeping controlled substances on premises, thus limiting their availability for use (Kamerman et al. 1992, Berge et al. 2012 ). In these instances, NSAIDS, alpha 2 adrenoreceptor agonists, tramadol, gabapentin, amantadine and amitriptyline alone or in combination may provide a safe analgesic alternative in small animal practice. Specific concerns for cats include fear of excitement, potential for side effects (respiratory depression and bradycardia) and challenges with pain assessment (Hansen & Hardie 1993, Dohoo & Dohoo 1996b, Lascelles et al. 1999, Lorena et al. 2014 ). Major concerns related to analgesic administration to dogs were respiratory depression, bradycardia, emesis and over-sedation (Dohoo & Dohoo 1996b, Lorena et al. 2014 ). Despite these concerns, the occurrence of adverse effects associated when administering the appropriate analgesics are rare at normal dosage regimens and are not considered to be outweighed by the disadvantages of untreated pain (Wright 2002, Gurney 2012, Mathews et al. 2014 ). When considering surgical patients with an increased likelihood for gastroesophageal reflux and aspiration pneumonia, the veterinarian may administer analgesics such as alpha 2 adrenoreceptor agonists, local anaesthetics and/or dissociatives, which are not risk factors for developing postanaesthetic aspiration pneumonia (Ovbey et al. 2014 ). Additionally, in the authors experiences, low-dose opioids or the addition of high-dose metoclopramide (bolus loading dose of 1 mg/kg, followed by 1 mg/kg/hour intravenously) are protocols that can be 550 Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association

Oligoanalgesia in small animal practice utilised in these scenarios (Wilson et al. 2006 ). Other common misconceptions by practitioners pertaining to side effects associated with analgesics include: (1) analgesics mask signs of patient deterioration, (2) NSAIDs are toxic in dogs and cats, and (3) opioids precipitate significant respiratory depression in dogs and cats (Mathews et al. 2014 ). These misconceptions are discussed by the World Small Animal Veterinary Association (WSAVA) Global Pain Council guidelines for recognition, assessment and treatment of pain. There is currently no evidence to support the withholding of analgesics due to these fears and misconceptions, particularly in healthy patients undergoing elective procedures. Inappropriate assessment and recognition of pain may be another primary cause for oligoanalgesia during the perioperative period or in the emergency critical care unit (Hugonnard et al. 2004, Moran & Hofmeister 2013 ). For instance, 39 to 77% of worldwide feel that their ability to recognise and treat pain is inadequate (Dohoo & Dohoo 1996a, Capner et al. 1999, Hugonnard et al. 2004, Williams et al. 2005, Lorena et al. 2014 ), demonstrating the importance of continuing education and veterinary curriculum content. Veterinary students have self-reported inadequate training and lack of confidence in pain-recognition skills (Hugonnard et al. 2004, Lim et al. 2014 ). Third-year veterinary students placed emphasis on the value of didactic and clinical training during their curriculum for pain assessment and the need for further training (Mich et al. 2010 ). Graduation year was shown to impact their use of analgesics in practice. Recent graduates, particularly within the last 10 years, assigned higher pain scores to patients and were more likely to prescribe analgesics when compared with older graduates (Dohoo & Dohoo 1996a, Capner et al. 1999, Hewson et al. 2006a, Lorena et al. 2014. Younger also felt more satisfied with their education on pain and analgesia (Hugonnard et al. 2004 ). This is consistent with the findings of Hunt et al. ( 2015 ), in which recent graduates were more likely to prescribe NSAID and opioids to dogs and cats following sterilisation procedures. These differences may be a result of more recent medical advances, providing current faculty with a better understanding of pain physiology and analgesia, which is then taught to the student population. Many students are unaware of the use of pain scales in veterinary medicine, which may contribute to their frustrations in assessing pain in animals (Hugonnard et al. 2004 ). Veterinarians working with two or more veterinary technicians administered analgesics more frequently than those without (Dohoo & Dohoo 1998 ). Veterinary technicians and nurses are crucial in the assessment of pain as they are commonly involved with patient monitoring and deterioration in case of pain (Coleman & Slingsby 2007 ). Intensive care unit and emergency department patients may be presented for one medical non-painful condition but have other underlying medical problems that warrant analgesic therapy. Osteoarthritis, dental pain and otitis are painful conditions where tissue injury is difficult to identify and may not have been associated with the presenting complaint. In these situations, analgesic therapy may go overlooked or may be deemed not necessary. The patient s behaviour may also impact the likelihood for adequate analgesic therapy. Aggressive dogs and cats may receive less analgesia because of the potential injury to staff and personnel. Veterinary studies evaluating oligoanalgesia in aggressive or non-compliant patients are lacking. Another cause that may lead to oligoanalgesia is the lack of compliance of the technical staff to administer analgesics (Armitage et al. 2005 ). In a veterinary teaching hospital intensive care unit, only 64% of patients received analgesics as written on their treatment orders (Armitage et al. 2005 ). The majority of changes associated with the remaining 36% was a decrease in dose by withholding medications (Armitage et al. 2005 ). Reasons for alteration of drug doses were not commonly reported in the medical records, but the potential for adverse effects of the drug itself was postulated (Armitage et al. 2005 ). Other reasons may include the terminology used on the treatment sheet that may preclude a patient from receiving analgesics (Hansen & Hardie 1993 ). In a previous study, the majority of written orders included terms such as if extremely painful, if in terrible pain, give only if needed, or as needed (Hansen & Hardie 1993 ). Rather than the use of subjective terminology, we recommend the incorporation of objective pain scales within the medical treatment orders to decrease the incidence of oligoanalgesia. STRATEGIES TO DECREASE OLIGOANALGESIA Strengthening of didactic and clinical learning is key in diminishing oligoanalgesia in veterinary medicine. Studies have shown an inadequate general knowledge of pain recognition and management in human and veterinary medicine and minimal inclusion of pain-related content in prelicensure educational programmes (Mich et al. 2010, Watt-Watson et al. 2013 ). The Texas A&M College of Veterinary Medicine and Biomedical Sciences (Table 4 ) has expanded those clinical competencies to capture specific components of pain knowledge, assessment and alleviation (Rogers et al. 2016 ). Students at the Université de Montréal are taught 12 hours of animal pain and analgesia using videobased learning, case-based discussions and hands-on wet labs as part of the third-year course on anaesthesia and pain management. They also have an optional course of 15 hours on algology. Despite these efforts, there is a general shortage of impactful instructional and assessment opportunities in the overall sum of preclinical and clinical education in veterinary education. For example, a two-week training programme was not sufficient to alter perceptions of pain in third-year veterinary students at Colorado State University (Mich et al. 2010 ). Significant factors that were thought to negatively impact pain recognition and treatments were: lack of reinforcement, clinical rotation variability, inappropriate outcome measures and assessment and failure to bridge didactic and clinical knowledge (Mich et al. 2010 ). Standardisation of teaching methodologies (pain scoring systems, case rounds, pharmacological intervention) within the clinical year may address variations between rotations and instructors. The provision of continuing education/training on pain management significantly increases analgesic treatment and compliance (Jones 1999 ). Short didactic training sessions (four hours) provided to emergency residents on problems in the man- Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association 551

B. T. Simon et al. Table 4. Clinical competencies to capture specific components of pain knowledge, assessment and alleviation in veterinary students at Texas A&M College of Veterinary Medicine & Biomedical Sciences Clinical competencies The graduate will recognise the clinical signs associated with pain in all common domestic species. Assess the type of pain, classify the level of pain, formulate a pain management plan and apply a therapy to effectively prevent and alleviate animal suffering and pain The student can: 1. Explain the physiology of pain and apply knowledge of anatomy to recognise the clinical signs associated with pain in all common domestic species 2. Explain the role of pain recognition scales in evaluating patients for pain and be able to apply those pain scales to common domestic species 3. Recognise the need for pharmacological, multi-modal and alternative therapies to address patient pain 4. List the classes of drugs that can be used to control pain, describe their mechanism of action and describe the adverse reactions that may occur as a result of these actions 5. Construct a pain management plan that matches the type and level of pain being experienced by the patient with the appropriate class, dose and route of administration of drug to effectively alleviate the pain 6. Weigh the benefits of pain management against the potential complications of pharmaceutical intervention when developing a pain management plan 7. Implement a comprehensive pain management plan and communicate long-term monitoring and treatment schemes with members of the health care team and guardians agement of acute pain, pharmacology, pharmacokinetics and pathophysiology of pain (Table 5 ) resulted in a 92% reduction in pain scores in a human emergency critical care unit (Jones 1999 ). Improvements on knowledge of pain and assessment that can help to decrease oligoanalgesia were reported in medical staff members who received pain management education (Ghandehari et al. 2013, Long 2013 ). Online information can provide valuable resources in identifying and treating pain in small animal practices. The American Animal Hospital Association and the World Small Animal Veterinary Association Global Pain Council have released open-access documents outlying pain assessment tools and ways to treat pain in dogs and cats (Mathews et al. 2014, Epstein et al. 2015 ). The wide distribution of these documents can help in decreasing oligoanalgesia in veterinary practices. National and regional continuing education meetings, along with completion of short courses, are the most helpful mechanisms in improving knowledge on pain assessment in veterinary patients (Lorena et al. 2014 ). The World Small Animal Veterinary Association now has a stream dedicated to pain management at their annual congress. The International Veterinary Academy of Pain Management is an interdisciplinary association exclusively dedicated to the education of the veterinary community to recognise and treat pain in animal species. It encourages communication of its members via a listserv and scientific investigation of the topic. In countries where have limited access to controlled analgesic agents such as opioids, an alternative approach to analgesic therapy using The World Health Organisation (WHO) analgesic three-step ladder may provide benefits (World Health Organization 2012 ). The WHO Ladder differentiates Table 5. Recommended topics in an educational programme to decrease the incidence of oligoanalgesia in veterinary hospitals [extrapolated from Jones 1999 and Guidelines from the World Small Animal Veterinary Anaesthesia Association (WSAVA), from the American Animal Hospital Association (AAHA), and the American Association of Feline Practitioners (AAFP) 2014, 2007 and 2015, respectively] Topics covered in an educational programme Incorporate pain as the fourth vital sign. The overall goal is to recognise that at a predetermined pain score, treatment is required. After analgesic treatment, evaluation of a positive response to treatment is a necessity 1. Review common causes of pain 2. Review the literature regarding the most common occurrence of oligoanalgesia (e.g. settings, medical conditions and species) 3. Pain pathophysiology, including peripheral sensitisation, central sensitisation and neuropathic pain 4. Review the principles of pain management, including when and how to treat, pain scales, multi-modal analgesia, neuroleptanalgesia 5. Understand the impact of pharmacology on dosing intervals, constant rate infusions versus intermittent bolus dosing and, review absorption and bioavailability issues across species 6. Review the World Small Animal Veterinary Anaesthesia Association and American Animal Hospital Association guidelines on pain management 7. Review pharmaceutical (opioids, non-steroidal anti-inflammatory agents (NSAIAs), N-Methyl-D-aspartate (NMDA) antagonists, -adrenoceptor agonists, local regional nerve blocks), and nonpharmaceutical options (acupuncture, physical rehabilitation, activity 2 restrictions, cold therapy) 8. Review species (feline, canine) and patient-specific considerations [e.g. age (geriatric and paediatric), pregnancy, type of surgical pain (acute abdomen, spinal cord or peripheral nerve injury, orthopaedic pain)] therapy based on the severity of the pain: mild, moderate and severe. The objective is to minimise the use of opioids for treating mild to moderate pain by the substitution of NSAIDs and, in the authors experiences, other adjuvant agents (gabapentin, amantadine, amitriptyline) (Lascelles et al. 2008, Cashmore et al. 2009, Vettorato & Corletto 2011, Lorenz et al. 2013, Madden et al. 2014, Crociolli et al. 2015 ). This technique would allow countries that cannot regularly obtain opioid analgesics to provide adequate alternative methods of pain management. A discussion on the techniques to assess pain in dogs and cats is beyond the scope of this article, but several validated pain scoring systems have been used to recognise pain, provide optimal treatment, improve compliance and create a more reliable prognosis (Mathews et al. 2014, Epstein et al. 2015 ). The World Small Animal Veterinary Association guidelines warrant the evaluation of pain as the fourth vital sign in patient care and assessment, and encourages to use validated pain scoring systems as part of the evaluation of pain. The addition of these scoring systems can significantly identify and increase the number of patients being adequately treated for pain (Murrell et al. 2008 ). In conclusion, oligoanalgesia is a critical issue in many areas of small animal practice. Evidence suggests the need for early implementation on ways to assess pain during veterinary school, continuing education on recognition and treatment of pain at all levels of veterinary practice and putting into practice the use of pain scoring systems to reduce oligoanalgesia. 552 Journal of Small Animal Practice Vol 58 October 2017 2017 British Small Animal Veterinary Association