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4 Effective Pain Management T his chapter presents an overview of the basic clinical strategies, both pharmacologic and nonpharmacologic, for managing pain in labora- tory animals. Topics include preventive analgesia, consequences of unrelieved pain, and ethical considerations relating to pain as a subject of study. Available information on pain management of nonmammalian spe- cies is also presented. INTRODUCTION The regulatory review process (see Appendix B) requires that investiga- tors adequately control pain in research animals, unless procedures that may cause more than momentary or slight pain are justified for scientific reasons and approved by the IACUC. In order to treat or prevent pain, it is necessary to evaluate its source and intensity (for additional discussion see Chapter 3). As a rule, pain is likely to occur in proportional terms as a result of tissue injury—more extensive tissue damage results in greater pain and thus a need for a stronger analgesic regimen. While certain conditions reliably cause severe pain (e.g., acute nerve compression, burns, spastic contraction of smooth muscle) and inflammation often contributes to the worsening of pain, scientists do not fully understand how much pain to expect in various animal species. Information about the cause and effect of surgery or disease and pain in clinical veterinary medicine is largely based on observation and anecdote and tends to focus on commonly treated spe- cies, such as dogs, cats, and horses. Table 1-1 of Chapter 1 lists examples 1

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2 RECOGNITION AND ALLEVIATION OF PAIN IN LABORATORY ANIMALS of typically painful conditions that occur either spontaneously or as a result of experimental procedure. CLINICAL VETERINARY PAIN MANAGEMENT The principles of clinical veterinary pain management and prevention, summarized in Boxes 4-1 and 4-2, are comparatively easy to apply in clini- cally familiar species such as dogs and cats, for which ranges of doses and drug combinations are relatively well known. However, the application of the principles discussed below to other laboratory animal species is a matter of trial and error until adequate scientific information is available to establish evidence-based guidelines, including information on the feasibil- ity of various routes of administration (e.g., oral bioavailability, palatability, transdermal preparations). Readers are encouraged to seek publications (including the American College of Veterinary Anesthesiologists’ Position Paper on the Treatment of Pain [ACVA 1998]), reports, books, and the vet- erinary literature for specific information on available drugs, doses, routes of administration, side effects, contraindications, and the like that may be useful for dogs, cats, rabbits, and other species used as research animals. BOX 4-1 Current Guidelines for Clinical Veterinary Pain Management • Sedation does not provide pain relief and may mask the animal’s response to pain. • Use of analgesic and adjunct drugs should be at effective plasma/tissue con- centrations especially when the nociceptive barrage and pain are greatest (i.e., after surgery or injury). • Use of more than one type of management strategy (e.g., multimodal anal- gesia [targeting multiple pain mechanisms with the use of local anesthetics and opioids] or anxiolytics when postsurgical pain is likely to be moderate to severe) is recommended. • Avoidance of peaks and valleys in analgesic dosing (best accomplished by the administration of continuous or overlapping regimes) when postsurgical pain is expected to be severe maintains animal well-being. • Monitoring, at appropriate intervals, of the effectiveness of analgesics admin- istered is crucial. • If there is doubt about the source of an animal’s clinical signs, administration of an additional dose of analgesic—dependent on the drug, species, and often the individual animal—can help determine whether pain was the cause (while this is not commonly done in laboratory animal medicine, this method of pain control/alleviation in nonrodent species is common in clinical veterinary prac- tice in a patient-specific manner).

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3 EFFECTIVE PAIN MANAGEMENT BOX 4-2 Additional Considerations for the Prevention and Management of Pain in Laboratory Animals • Pain in animals is often unrecognized and undertreated. • If a procedure is considered painful in humans, it should be assumed to be painful in laboratory animals, regardless of their age or species. • Adequate treatment of pain may be associated with decreased complications, lower mortality, reduced variability in experimental data, and improved scien- tific outcomes. • The appropriate use of environmental, nonpharmacologic, or pharmacological interventions, as well as the selection of humane endpoints in animal experi- mentation, can prevent or reduce animal pain in most experimental designs without compromising the scientific validity of the research, except where pain is the subject of research. • Researchers, veterinarians, and animal care professionals should be respon- sible for learning about the assessment, prevention, and management of pain in laboratory animals. • Veterinarians and animal care professionals should develop IACUC-approved educational guidelines and protocols for the management of pain in laboratory animals at their institution. Some ranges for effective doses of analgesics in rats and mice (i.e., doses that reduce experimental measures of pain and/or reach tissue con- centrations believed to be effective in other species) are available through literature search. However, strain differences in animals’ responses to anal- gesics and anesthetics are an important factor to consider (Mogil et al. 2005; Terner et al. 2003; Wilson et al. 2003a,b). STRATEGIES FOR MANAGING PAIN IN LABORATORY ANIMALS Effective management of pain in laboratory animals often begins with general (surgical) anesthesia, but also includes local anesthetics, analgesics, anxiolytics, and sedatives as well as nonpharmacological methods (includ- ing minimization of tissue trauma). Pain management goals range from total elimination (as, for example, during general anesthesia for a surgical procedure) to pain that is tolerated without compromising the animal’s well-being. General Anesthesia When animals are anesthetized for procedures that would otherwise cause pain, it is important to maintain an appropriate depth of anesthesia.

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4 RECOGNITION AND ALLEVIATION OF PAIN IN LABORATORY ANIMALS A wide range of indices have been developed to assess depth of anesthe- sia in animals and humans (Appadu and Vaidya 2008; Bruhn et al. 2006; Franks 2008; John and Prichep 2005; Lu et al. 2003; Murrell and Johnson 2006; Otto 2008; Whelan and Flecknell 1992); these include autonomic responses such as changes in heart rate and blood pressure, alterations in the EEG or other measures of CNS function, or changes in somatic reflex responses to noxious stimuli. During anesthesia not accompanied by neu- romuscular blocking agents, depression of somatic reflex responses is the most widely used method for ensuring an appropriate depth of anesthesia. In all animal species, absence of the pedal withdrawal reflex indicates a surgical plane of anesthesia (i.e., anesthesia that is deep enough to elimi- nate the experience of pain and thus allow surgery to take place). Although this is an easily assessed index, it is important to use a stimulus that is suf- ficiently noxious but not so strong as to produce tissue damage. In some species, other reflexes, such as the response to applying a clamp to the nasal septum (pigs) or pinching the ears (rabbit, guinea pig), are also useful but reliance on these responses has been criticized (Antognini et al. 2005) because animals may lose consciousness at much lighter anesthesia planes, in which case the persistence of reflexes would not indicate pain perception (see also Box 1-3 in Chapter 1). Doses of anesthetic agents sufficient to sup- press spinal reflexes may therefore be greater than those required to carry out surgery humanely; if these reflexes are not suppressed, surgery will be hampered by the animals’ repeated reflex movements. Although the use of neuromuscular blocking agents (which prevent neurotransmitters from act- ing on their receptors in skeletal muscles) could prevent such movements, it would also require intubation and mechanical ventilation of the animal. For practical reasons, suppression of withdrawal responses remains the most useful means of ensuring loss of both awareness and responses to surgical stimuli. The ideal general anesthetic should rapidly and/or smoothly induce muscle relaxation and a surgical plane of anesthesia, and should be readily controllable and reversible. There are two categories of general anesthetics used in laboratory animal medicine: volatile inhalants (e.g., isoflurane) and injectable drugs (e.g., barbiturates, other sedative-hypnotic agents such as propofol, or combinations of drugs such as propofol-fentanyl). The latter category also includes total intravenous anesthesia (TIVA). TIVA techniques may be useful in laboratory animal settings where the equipment required for inhalant anesthesia is not practical or possible (e.g., near MRI units). Other injectable general anesthetic drugs still in use due to their unique application in specialized studies include α-chloralose, tribromoethanol, and urethane. These drugs have certain specific applications but may not be appropriate for situations in which animals will recover (Gaertner et al. 2008; Karas and Silverman 2006; Koblin 2002; Meyer and Fish 2005) as,

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 EFFECTIVE PAIN MANAGEMENT after surgery, with anesthetic withdrawal and recovery, the animals will experience pain unless they receive analgesics. Sedation/Anxiolysis Sedatives and anxiolytics are adjuncts to general anesthetics and are also used in pain management strategies. These two distinct classes of drugs are often used in combination to modulate, block, or relieve pain. Terminol- ogy varies but a general distinction between the sedative-hypnotic agents and anxiolytics is often useful. Sedative-hypnotic drugs (e.g., barbiturates and drugs with significant sedating properties such as α2-adrenoreceptor agonists) produce dose-dependent states of CNS depression that vary from somnolence to general anesthesia and even death. Anxiolytics are drugs that reduce anxiety or fear (e.g., benzodiazepines) and can induce sleep. Some anxiolytic drugs, previously termed “tranquilizers” (e.g., phenothiazines like acepromazine and butyrophenones like haloperidol and droperidol), produce a state of relaxation and indifference to external stimuli and, in elevated doses, can induce an undesirable cataleptic state rather than gen- eral anesthesia. Of the above drugs and classes, only the α2-adrenoreceptor agonists have analgesic efficacy. Neither barbiturates nor anxiolytics are analgesic; barbiturates may in fact contribute to a hyperalgesic state, while phenothiazines and butyrophenones are generally considered devoid of analgesic efficacy. Readers are referred to the section “Modulatory Influ- ences on Pain: Anxiety, Fear, and Stress” in Chapter 2 for a discussion of the relationship of anxiety and pain. Neuroleptanalgesia is an intense analgesic and amnesic state produced by the combination of an opioid analgesic and a neuroleptic drug (this description is adapted from the American Heritage Medical Dictionary 2007). The neuroleptic drug component is a phenothiazine or butyrophe- none (or possibly an anxiolytic) and the analgesic is a potent and efficacious opioid that also acts as a major tranquilizer (i.e., anxiolytic). Butorphanol- acepromazine, fentanyl-fluanisone (Hypnorm®1), and oxymorphone- midazolam are examples of commonly used veterinary neuroleptanalgesic combinations. Neuroleptanalgesic combinations by themselves are not suffi- cient for most surgical interventions. However, the use of drugs with sedative or tranquilizing properties (neurolepts as well as α2-adrenoreceptor agonists) combined with opioids, ketamine, or tiletamine-zolazepam (Telazol®) can cause states ranging from modified consciousness (e.g., reduction of anxiety or “conscious sedation”) to complete unconsciousness (general anesthesia). Table 4-1 summarizes the analgesic properties of selected drugs, includ- 1 Hypnorm is not available in the United States (as of August 2009).

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6 RECOGNITION AND ALLEVIATION OF PAIN IN LABORATORY ANIMALS TABLE 4-1 Analgesic Properties of Selected Anesthetic Drugs and Adjuncts Analgesic Drug Class Efficacy α2-Adrenoreceptor agonists Analgesic/sedative-hypnotic Yes Barbiturates Sedative-hypnotic No Benzodiazepines Anxiolytic No Butyrophenones Neuroleptic/anxiolytic No Chloralose, chloral hydrate Sedative-hypnotic No Halogenated inhalant anesthetics General anesthetic No Ketamine Dissociative, NMDA antagonist Yes Nitrous oxide General anesthetic (human); general Yes anesthetic adjunct only in animals Opioids Analgesic Yes Phenothiazines Neuroleptic/anxiolytic No Propofol Sedative-hypnotic No (Telazol®) Tiletamine-zolazepam Combination of a dissociative/ Yes NMDA receptor antagonist and a benzodiazepine anxiolytic Tribromoethanol Sedative-hypnotic No Urethane (e.g., ethyl carbamate) Not classified No NOTE: Drugs with inherent analgesic effects may contribute to postoperative pain control but are not sufficient to exert such control in and of themselves. ing tranquilizers, sedatives, and anesthetics, commonly used in laboratory animals. Analgesia Conventional analgesic drug classes include opioids, NSAIDs, and local anesthetics. Although analgesia is defined as “lack of pain,” complete elimi- nation of pain in awake animals is commonly neither achievable nor desir- able. Pain has a protective role as it usually serves to limit further injury; for example, humans with no skin sensation are prone to undetectable injury or infection. But in some instances animals with untreated severe pain may struggle or self-mutilate and exacerbate or cause additional injury to them- selves. With most analgesic techniques, however, residual pain naturally limits activity, although it is not a restraint mechanism and should not be used to restrain animals.

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 EFFECTIVE PAIN MANAGEMENT The goal of analgesic drug intervention is to achieve a balanced state during which an animal is neither substantially hindered by pain nor adversely affected by the side effects of analgesics. Often the use of a single analgesic is sufficient. An emerging practice for the prevention or treatment of established pain in both human and veterinary patients, however, is the combined use of two or more types of analgesics, or “multimodal analgesia” (Buvanendran and Kroin 2007; Corletto 2007; Hellyer et al. 2007; Kehlet et al. 2006; Lemke 2004; White 2005; White et al. 2007). Multimodal post- surgical analgesia may be regarded as overly complicated, but cited benefits include more effective and efficient analgesia and possible dose reduction of one or more individual drugs. In theory, treatment of patients with nonopioid analgesics to reduce the overall requirement for opioids would result in fewer opioid-induced side effects. The concept, known as “opioid sparing,” is a desirable goal because extended or high-dose opioid therapy is often accompanied by unwanted side effects (e.g., sedation, constipation, urinary retention, or analgesic tol- erance) that prolong or complicate convalescence (Kehlet 2004; White et al. 2007). Synergy (i.e., greater analgesia than predicted from a simple additive effect of the combination of two drugs acting with different mechanisms) has been demonstrated in numerous experimental animal models (e.g., Price et al. 1996; Kolesnikov et al. 2000; Matthews and Dickenson 2002; Qiu et al. 2007) as well as with combinations of opioids, NSAIDs, local anesthetics, α2-agonists, ketamine, tramadol, and gabapentin (Guillou et al. 2003; Koppert et al. 2004; Reuben and Buvanendran 2007; White et al. 2007). Multimodal analgesia using “adjuvant analgesics” (i.e., antidepres- sants, antiepileptic drugs, NMDA antagonists, or transdermal lidocaine) may also be an effective alternative for the treatment of refractory chronic pain unresponsive to the administration of a single agent (Knotkova and Pap- pagallo 2007). Table 4-2 summarizes pharmacologic methods for treating pain of various intensities. Advanced Analgesic Techniques The ability to provide analgesia to laboratory animals is limited by the lack of information about species-specific drug effects and doses. It is perhaps useful to understand the state-of-the-art techniques currently used in clinical (i.e., nonlaboratory) veterinary medicine as a potential objective for laboratory animal pain medicine; identification of the most useful tech- niques may lead to important innovations to help overcome barriers to the provision of analgesia. Needless to say, size, species, and technical aspects will continue to be limiting factors for many techniques. Box 4-3 provides a summary of analgesic techniques and their limitations.

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8 RECOGNITION AND ALLEVIATION OF PAIN IN LABORATORY ANIMALS TABLE 4-2 Pharmacologic Approach to Pain Management Based on Predicted Intensity Pain Intensity Analgesic Approach Low Single-agent therapy acceptable NSAIDs, local anesthetic infiltration, or opioid agonist-antagonists (butorphanol, buprenorphine) Moderate Multimodal analgesia to be considered NSAIDs in combination with adjuncts such as local anesthetics, opioid agonist-antagonists (buprenorphine), tramadol, α2-agonists, NMDA antagonists High Multimodal analgesia recommended mu-opioid agonists (morphine, hydromorphone, fentanyl, methadone) + one or more of the following: NSAIDs, local anesthetics, α2-agonists, antiepileptic drugs, NMDA antagonists Advanced analgesic techniques: epidural administration of local anesthetics with or without opioids and constant rate infusions Nonpharmacologic Methods Nonpharmacologic approaches to pain management are appropriate when the use of pharmacological methods is contraindicated, when effec- tive analgesic drugs are not available, or to complement drug therapy. Non- pharmacologic methods include preventive strategies that help minimize causative factors for pain, through, for example, appropriate animal han- dling and minimization of tissue trauma during surgery. Such techniques are important because both long-duration surgery and extensive tissue manipu- lation (e.g., rib retraction, prolonged tourniquet-induced limb ischemia, disproportionately long incision relative to animal size) result in increased postoperative pain. Training in proper surgical techniques coupled with knowledge of comparative anatomy is necessary to appreciate the distinct needs of each animal species before, during, and after surgery and to uphold the 3Rs principle of refinement. Moreover, nonphysiologic restraint or surgical positioning of animals may exert undue pressure on joints, nerves, or soft tissues and cause significant postprocedural pain. These sources of pain are avoidable if investigators and animal care personnel are trained to understand that any form of tissue pressure, damage, or ischemia is a potential cause of pain (Martini et al. 2000; LASA 1990). Minimally invasive surgery techniques (e.g., fiberoptic technologies) reduce tissue injury and are associated with reduced postsurgical pain, stress response, and convalescence time compared to open or scalpel surgery (reviewed by Karas et al. 2008).

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 EFFECTIVE PAIN MANAGEMENT BOX 4-3 Advanced Analgesic Techniques • Low-dose epidural administration of opioids or opioid-local anesthetic com- binations can result in analgesia whose quality is similar to if not better than that achieved with systemic administration. This method depends on technical expertise and may be challenging to implement in very small animals. Epidural administration of drugs has not been studied in nonmammalian vertebrates. • Local anesthetics can be injected into joints, wounds, and body cavities (ab- dominal or pleural) by continuous or intermittent injection through intra-wound catheters, greatly reducing the need for systemic administration of other anal- gesics (Liu et al. 2006). The relatively short duration of the action of local an- esthetics may limit their utility in situations where redosing is difficult. Lidocaine is used intravenously to provide analgesia after tissue injury (Omote 2007). • Oral administration of some analgesics is feasible (e.g., NSAIDs, opioids, gabapentin), but for some drugs (opioids) first-pass (species-dependent) me- tabolism limits bioavailability, necessitating dose adjustment, use of a different route of administration, or selection of another drug. Compounding of drugs into palatable forms that animals are willing to consume is possible, but without data to support a particular method, one must be concerned about absorption, shelf life, and efficacy. • Dilution of injectable analgesics to make them easier to use or to improve provision in very small animals must be done with the understanding that formulations may not work as well and that shelf life is not predictable. • Continuous infusion of certain types of analgesics (e.g., opioids, ketamine, α2-adrenoreceptor agonists) avoids “peaks and valleys” in drug concentration and may provide better coverage for moderate to severe pain. Transdermal preparations are available in formulations suitable for larger animals and may be useful in producing uninterrupted analgesia. Sustained-release formula- tions make it possible to avoid periods of inadequate drug administration. For further consultation please see Carroll 2008; Flecknell 2009; Gaynor and Muir 2002; Hellyer et al. 2007; Krugner-Higby et al. 2008; Lamont and Mathews 2007; Robertson 2005; Tranquilli et al. 2007; Valverde and Gunkel 2005. METHODS FOR THE PREVENTION OR MANAGEMENT OF PAIN While classic pharmacologic treatment requires drugs with specific analgesic properties, unconventional drugs, such as antiepileptics, can also be effective. And when anxiety contributes to pain, drugs with anxiolytic properties can be added. Analgesics A thorough review of the effects and doses of analgesic drugs is beyond the scope of this work (for comprehensive reviews see Carroll 2008; Fleck-

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80 RECOGNITION AND ALLEVIATION OF PAIN IN LABORATORY ANIMALS nell and Waterman-Pearson 2000; Gaynor and Muir 2002; Hawk et al. 2005; Lamont and Mathews 2007; Robertson 2005; Valverde and Gunkel 2005). Instead, this section provides an overview of analgesic drugs that are currently used or may become useful in laboratory animal medicine. Opioids Opioid analgesics are important drugs for surgical analgesia and/or therapeutic management of moderate to severe pain in humans and certain animal species. There are two general categories of such analgesics (Ross et al. 2006; Stefano et al. 2005; Waldhoer et al. 2004): opioid receptor ago- nists (e.g., morphine, hydromorphone, fentanyl) and mixed opioid recep- tor agonist/antagonists (e.g., buprenorphine, butorphanol); the latter group possesses (in a single molecule) agonist efficacy at one of the three types of opioid receptor and antagonist efficacy at a different opioid receptor. A third group of endogenous opioid peptides (e.g., endorphins, enkeph- alins, and dynorphins) are produced by the body and also act on opioid receptors. It is a misconception, however, to assume that the only role of endogenous opioid peptides is to produce analgesia; they have multiple, nonanalgesic functions depending on where in the body they are produced and released. Given the existence of three distinct opioid receptors, all located in variable densities in various tissues, differences in the selectivity and affinity of opioid drugs and endogenous opioid peptides are believed to account for many of the variations in the effect profile of opioids (Fields 2004; Waldhoer et al. 2004). And because opioid receptors are subject to regulation (e.g., by phosphorylation or endocytosis), the effects of both endogenous and exogenous opioids can be influenced by the “state” of the receptor. Changes such as these presumably account for the phenomenon of analgesic tolerance, a reduction in the analgesic effectiveness of a given dose of drug after repeated administration. Opioids are the most efficacious analgesics available, but their use is accompanied by undesirable effects that include an increase in smooth muscle tone and reduction in propulsive motility of the gastrointestinal tract (leading to constipation), cough suppression, respiratory depression, behavioral changes (euphoria and dysphoria, excitement, or increased loco- motion), and physiological dependence. In addition to their presence on neurons both in the nociceptive pathway (see Chapter 2) and elsewhere in the body (e.g., the gastrointestinal tract), opioid receptors are found on cells of the immune system and opioid effects on immune function vary from stimulation to inhibition (Stefano et al. 2005; Page et al. 2001). In rats and other rodents, pica (the ingestion of nonedible substances, such as bedding) and the consumption of large volumes of food have been noted with the use of the partial opioid receptor agonist/weak antagonist buprenorphine (Aung

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81 EFFECTIVE PAIN MANAGEMENT et al. 2004; Bosgraaf et al. 2004; Clark et al. 1997; Yamamoto et al. 2004). Concern about the undesirable side effects of opioids is frequently cited as a reason for not using them, but for limited or short-term therapy the side effects are often either manageable or not a problem. Dose regimens of opioid analgesics for dogs, cats, horses, rats, mice, a few species of birds, and sheep have been reported. When such regimens are based on experimental evidence, it frequently derives from an analge- siometric testing method (such as thermal threshold; Johnson et al. 2007; Robertson et al. 2005a,b; Waterman et al. 1991; Wilson et al. 2003a,b). Doses for other mammals currently listed in formularies are based on extrapolation. Relatively little is known about the efficacy, drug choices, or side effects of opioids in amphibians, reptiles, invertebrates, and most birds. In addition to classical intravenous, intramuscular, and intraperitoneal routes of administration, many opioids are also substantially bioavailable by nasal, sublingual, or rectal routes (Lindhardt et al. 2000; Robertson et al. 2005a). Oral administration of opioids in mammals often diminishes their bioavailability, making this method of delivery less effective. Addi- tionally, long-duration formulations of opioids have been investigated in animal models and, although not yet commercially available, may repre- sent a future method to provide sustained analgesia in laboratory animals (Krugner-Higby et al. 2008; Smith et al. 2004). Because of the relative safety of opioids, information about effective dose ranges and novel methods of administration would be useful. Research is needed to determine ranges and methods for most laboratory animal species. Tramadol Tramadol2 is a centrally acting synthetic analgesic used to treat post- operative and chronic pain in humans. It has a multimodal action: it is an opioid receptor agonist and it inhibits norepinephrine and serotonin reuptake from neurons where those amines are released, including in the spinal cord where both norepinephrine and serotonin can contribute to the modulation of nociception (Grond and Sablotzki 2004). An active (M1) metabolite of tramadol binds with high affinity to mu-opioid receptors; indeed it has more affinity for the opioid receptor than the parent drug. The use of tramadol has recently increased significantly in veterinary medicine. However, in humans and dogs (and possibly other species) with an inherited 2 Draft FDA guidance on tramadol is available at www.fda.gov/downloads/Drugs/Guidance- ComplianceRegulatoryInformation/Guidance/ucm090703.pdf (accessed July 28, 2009).

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