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The social context of neonatal pain Patrick J. McGrath, PhDa,*, Anita M. Unruh, PhD, RSW, OT(C)RegNSb a

Department of Psychology, Life Sciences Centre, Dalhousie University Halifax, NS B3H 4J1, Canada b School of Occupational Therapy, 5869 University Avenue, Forrest Building, Dalhousie University, Halifax, NS B3H 3J5, Canada

Pain is more than a physiologic event. It is a communication that is dependent on a social context that is receptive to the communication. This social context consists of health professionals, parents, and the larger public and professional community. Sick neonates are among the most vulnerable members of our society. They have no ability to protect themselves, to protest about their pain experiences, or to object to the failure to ameliorate pain. Despite their vulnerability, neonates are frequently subjected to painful procedures. The roles of doctors, nurses, and patients are socially prescribed. Although the physical trauma due to a medical procedure or the pharmacokinetics of drugs may not be directly influenced by social factors, the recognition that there is a problem in need of investigation and management, the use of comforting interventions, the use of invasive medical procedures that cause pain, and the prescription of drugs to ameliorate pain are, in part, the product of the social context. There have been dramatic changes in our practice of managing neonatal pain in the last 20 years. These changes are due to a confluence of forces in which scientific research has played an important role. It is an oversimplification, however, to believe that scientific research is the only factor that has changed our understanding of neonatal pain or that scientific research occurs in a vacuum. Health practices and experiences are always embedded in the social context in which they arise [1]. The context in which pain occurs helps to determine the reactivity of the infant. The pain reactivity of infants may also be influenced by learning.

The first author’s research is supported by grants from the Social Sciences and Humanities Research Council and the Canadian Institutes of Health Research. The first author is also supported by a Distinguished Scientist Award of the Canadian Institutes of Health Research. An earlier version of these arguments appeared as a chapter in Anand KJS, Stevens B, McGrath PJ, editors. Pain in neonates. 2nd edition. Amsterdam: Elsevier; 2000. * Corresponding author. 0095-5108/02/$ – see front matter D 2002, Elsevier Science (USA). All rights reserved. PII: S 0 0 9 5 - 5 1 0 8 ( 0 2 ) 0 0 0 2 1 - 0

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Only a short while ago, pain in the infant was not considered a reasonable topic for health professionals and researchers. Health care professionals who were concerned with neonatal pain were considered unscientific and had difficulty in obtaining funding. Although these problems may persist, neonatal pain has gradually been changed into a topic deserving both clinical attention and research. Attitudes about scientific merit have changed not only because of outstanding advances in our science but also because of social influences. The climate for research in neonatal pain has improved dramatically, even though the field is still in its earliest stages of development. In this article, the authors sketch social influences on (1) the prevalence of pain in neonates, (2) pain as communication, (3) the changing practice of neonatal pain, (4) the impetus for change, (5) the resistance to change, and (6) the neonate’s learning about pain. The article concludes by examining standards for practice and neonatal pain research. Unfortunately, there has been little systematic work on the social context of pediatric pain and, as a result, most of this article is anecdotal.

Prevalence of pain in neonates It is a contradiction that most of us do not notice—we routinely impose pain on sick and vulnerable infants. Of course, pain is the side effect of procedures intended to save the life and/or improve the health of the sick neonate. Although this is true, recognition that health professionals inflict most of the pain suffered by neonates through medical investigations and therapeutic procedures should alert us to our responsibility to protect infants from unnecessary pain and from the untoward consequences of pain. Such procedural pain, unlike naturally occurring pain, serves no protective purpose for the neonate. It has no positive effect. The extent to which neonates are subjected to many painful procedures has been documented in a recent study of neonatal intensive care units (NICUs) across Canada. Johnston and colleagues [2] had nurses record procedures for neonates who were hospitalized for more than simple prematurity. Their sample of 239 patients had a total of 2134 invasive procedures over the 1-week study period. Although procedural pain has no value in terms of teaching the infant to avoid harmful events or alerting the caregiver of the infant’s pain, medication to protect the infant from pain was given for only 0.8% of the procedures. Doubtless, each procedure is ordered with the intent of contributing to the best medical care for the infant. Parents give permission in the belief that these procedures are necessary and that every effort will be made to prevent or limit pain. It is only in this social context that we permit the infliction of pain on infants. There is, however, little evidence that all painful diagnostic procedures benefit infants. Blood draws may be done routinely without influencing care. Some procedures could be reduced by better organization. For example, two blood draws may not be needed if one is used for two assays or if health professionals had better communication. Few NICUs have policies and proce-

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dures to prevent unnecessary painful procedures. There is little doubt that more could be done to reduce the pain from procedures. In sharp contrast to this readily sanctioned permission to cause pain in infants in the medical context is the universal right to protection from physical interference, including the infliction of pain. This standard is particularly important for those who are unable to protect themselves. This expectation or value becomes obvious in our laws on assault and laws about child abuse and neglect. One cannot physically interfere with someone else without that person’s permission. In almost all jurisdictions, laws exist that make the harming of children or, in certain circumstances, the failure to prevent harm to children a criminal matter. We all believe that infants should be protected from harm, including pain. Parents see protection of their children from unnecessary pain as their responsibility. In the medical context, parents delegate this responsibility to health care professionals in the trust that professionals will do everything they can to prevent their children from suffering pain. Pain from surgery and pain from procedures do no good in themselves. The trust that parents have given to health care providers to prevent pain is violated when doctors and nurses do not use the best scientific evidence available to provide safe and effective pain relief and pain prevention and when institutions do not provide policies and procedures to insure that pain to those who are vulnerable is minimized.

Pain as communication Health care professionals usually see pain as a complex physiologic event, but a full understanding of pain requires that it be seen in a broader context. Craig [3,4] and colleagues developed a model of pain as communication. Information about pain is transmitted by means of behavior to caregivers who may or may not receive the information and act on it. In the case of neonates, especially sick neonates, their ability to communicate pain may be reduced by their weakened state, by being in an incubator and, in many cases, by being intubated. Communication may be inhibited or facilitated by training of caregivers, changing beliefs and behavior of caregivers, and policies or procedures of the unit. For example, an NICU that has developed a neonatal pain initiative consisting of educational programs about neonatal pain, policies requiring the use of neonatal pain measures, and training programs for nurses in the use of an appropriate scale may have a better chance of detecting pain in neonates than a unit that has not developed a neonatal pain initiative. Social factors also influence a neonate’s capacity to communicate about pain in another way. Social factors about neonates themselves and about work in an NICU may limit the extent to which professionals regard their neonatal patients as social beings. Neonates who are surrounded by complex medical equipment that is essential to maintain life do not have the same warm appeal that one anticipates on seeing a newborn. Very premature babies have very thin limbs,

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underdeveloped facial features, little visible body hair, and high-pitched irritating cries. In addition, the neonate may have been born with an apparent disability and/or congenital anomalies. The problem of appearing, in some sense, less appealingly human is compounded by the neurologic and physiologic immaturity of vulnerable neonates compared with healthy neonates or older infants. Reduced social reciprocity between health professional and the neonate may lead to less social attentiveness between health care giver and the neonate. Healthy neonates enjoy eye contact, vocalizing, and physical cuddling with their parents and their nurses. The responsiveness of the neonate encourages increased social attention and nurturance on the part of parents and health care professionals and increases the probability of attending to the neonate’s communication about pain. An ill neonate may have very little capability to engage in social exchanges, thereby reducing the probability that a health professional will initiate social attention. In addition, reduction in handling of sick neonates because handling causes distress may limit the opportunities for social interaction. The demands of caring for ill neonates will limit the time that is available for social contact. Social reciprocity between neonate and health care giver is hindered by the very real life and death struggle that exists for many neonates, especially the very premature baby. Professionals may reserve their social time and their attachment to a neonate whose state can alter rapidly between life and death. There may be considerable anxiety over the expected quality of life that would result if the baby lives. Limited social reciprocity and detachment between neonate and health caregiver leads to a greater ability to distance oneself from the neonate, to be less observant of behaviors that communicate pain, and to consciously or subconsciously discount the effects of pain on the neonate.

The changing practice of neonatal pain Over the last 2 decades, there have been significant changes in the management of pain in neonates. There have been some advances in technology, but most changes have not been due to technologic improvements. There have been a few new drugs and drug delivery routes developed or expanded to use in neonates, and we know much more about behavioral, environmental, and nutraceutic interventions, but the basic armamentarium of pain management, even in the neonate, has not dramatically changed in this time. A clear shift in beliefs and attitudes about neonatal pain has occurred, and this seems to have prompted changes in what medical personnel do. These changes in beliefs and attitudes and the influence on reported behavior are demonstrated by a 1988 survey of pediatric anesthetists in the United Kingdom and the Republic of Ireland [5] that was repeated again in 1995 [6]. In 1988, some pediatric anesthetists still thought newborns (13%) and neonates (7%) did not feel pain; 23% of the anesthetists were undecided. By 1995, there was almost universal agreement that newborns and neonates perceived pain. These changes in attitudes and beliefs were accompanied by reported changes in behavior. Fig. 1 shows the

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Fig. 1: Percentage of pediatric anesthetists reporting that they always or usually used systemic opioids in babies of different ages following major surgery. (Data from de Lima J, Lloyd-Thomas AR, Howard RF, et al. Infant and neonatal pain: anaesthetists’ perceptions and prescribing patterns. BMJ 1996;313:707; and Purcell-Jones G, Dormon F, Sumner E. Pediatric anaesthetists perceptions of neonatal and infant pain. Pain 1988;33:181 – 7.)

shift in prescribing of systemic opioids for babies of different ages. As the figure shows, at all ages, the use of systemic opioids increased over the 7-year span, but the increase was most significant in the newborns. Similarly, the use of regional analgesia showed very sharp increases over time (Fig. 2). The increase was most evident in the youngest age groups but was very significant at all ages. The use of local anesthetic and acetaminophen for minor surgery had also increased by 1995. These findings are what anesthetists say they do and may err in terms of a bias toward what is regarded as socially acceptable or the correct thing to do. This survey of pediatric anesthesiologists may not reflect the practice of physicians in other specialties, but there is no reason to believe that similar studies using pediatric anesthesiologist samples outside of the United Kingdom and Ireland would have different results.

Figure 2: Percentage of pediatric anesthetists reporting that they always or usually used regional analgesia in babies of different ages following major surgery (Data from de Lima J, Lloyd-Thomas AR, Howard RF, et al. Infant and neonatal pain: anaesthetists’ perceptions and prescribing patterns. BMJ 1996;313:707; and Purcell-Jones G, Dormon F, Sumner E. Pediatric anaesthetists perceptions of neonatal and infant pain. Pain 1988;33:181 – 7.)

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Porter et al [7] surveyed 374 nurses and physicians in 11 level 2 and 4 level 3 nurseries in a large metropolitan area in the United States. Most physicians (59%) and most nurses (64%) believed that infants can feel the same amount of pain as adults. About 27% believed that infants feel more pain than adults; only 10% believed that infants feel less pain than adults. They rated nine procedures as ‘‘at least moderately painful’’: endotracheal intubation, insertion of chest tube, circumcision, arterial or venous cutdown, lumbar puncture, intramuscular injection, insertion of peripheral intravenous line, heel stick, and insertion of radial or tibial arterial catheter. Three procedures—insertion of gavage tube, tracheal suctioning, and insertion of umbilical catheter—were rated as ‘‘somewhat painful.’’ Circumcision and insertion of chest tubes were seen as causing the most pain. Drugs were reported to be used infrequently even for the most painful procedures. Physicians, more often than nurses, reported that drugs were used. Comfort measures were not used frequently, but they were used more often than drugs. Both nurses and physicians felt that pharmacologic and comfort measures should be used more frequently. It is not possible to determine causal relationships between attitudes and behavior from survey studies. Changes in attitude can lead to changes in practice, but changes in practice may also lead to changes in attitudes. Controversy over what is appropriate management of neonatal pain has (and will continue to have) an impact on health care professionals who are caught between current practices in their own units and the freedom of their patients from unnecessary pain. The debate in the scientific and professional literature has changed. Clinicians and researchers no longer insist that neonates do not feel pain. Analgesia/anesthesia for surgery is now standard practice [2]. Many nurses and physicians agree that more aggressive pain management should be undertaken for painful procedures using both pharmacology and comfort measures. Pain management for invasive procedures, however, lags behind because of the lack of unequivocal scientific information about effective management of procedure pain and because practice has not kept up with science. For example, there are safe and effective pharmacologic methods to control pain from the most painful procedures such as circumcision and chest tube insertion but they are not widely used. Comfort measures such as the use of pacifiers and bundling are not universally used. The success of pain management for neonates has generated another potential problem, that is, the use of pain-management regimens that have not been sufficiently evaluated. For example, if infants are often in pain, should we not prevent pain by having them on constant opioid infusions? Unfortunately, we do not know the long-term effects of such approaches (although research is ongoing). Should we risk pain or should we risk the side effects of the drug? Pain research on the most vulnerable and at-risk infants (infants at high risk for cognitive impairment) is minimal. Although there is an emerging interest in pain in children with cognitive impairment [8– 12], there has been little research on neonates. They may be at particular risk for pain because of their medical condition, the uncertainty about how to assess their pain, and because of the feelings of hopelessness they may engender in their caregivers.

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The impetus for change Change in neonatal pain management has been rapid but has not always been easy. Scientists often believe that change will occur when they have discovered the best strategy to manage a problem. For example, a scientist who finds a better way to manage pain from a procedure likely believes that when clinicians are aware of the discovery (eg, through hearing about it at a scientific meeting or reading about it in a research journal), they will adopt this new procedure. This belief is clearly wrong. Dozens of examples in all areas of health care have shown that change does not occur simply with new scientific discoveries. Change is a social process that requires social influence as well as scientific and technical knowledge. Largely, social pressures along with scientific research prompted the changes that have occurred in pain management in the last 20 years. Research has established a foundation of evidence that infants and children experience pain and do benefit psychologically, physiologically, and clinically from proper pain relief. Lobbying, especially by parents, however, produces powerful social and public pressure that can (and has) resulted in rapid changes in health care. We will trace the somewhat curious interacting of these two factors—lobbying and scientific research in neonatal pain—by examining the social context of the Jeffrey Lawson story and the scientific research of K.J.S. Anand.

The social context of the Jeffrey Lawson story Jeffrey had holes cut on both sides of his neck, another cut in his right chest, an incision from his breastbone around to his backbone, his ribs pried apart, and an extra artery near his heart tied off. This was topped off with another hole cut in his left side for a chest tube. This operation lasted hours. Jeffrey was awake through it all. The anesthesiologist paralyzed him with Pavulon, a curare drug that left him unable to move, but totally conscious. When I questioned the anesthesiologist later about her use of Pavulon, she said Jeffrey was too sick to tolerate powerful anesthetics. Anyway, she said, it had never been demonstrated to her that premature babies feel pain. [13]

In 1985, 1 pound, 11 ounce neonate Jeffrey Lawson was operated on to correct a patent ductus arteriosus. His mother had inquired about anesthesia, and she was reassured by the child’s neonatologist that her son would be anesthetized [14]. The infant died a month after surgery. His mother, Jill Lawson, later reviewed her child’s medical chart and found that at no point during the surgery had her son had anesthesia. She began an unrelenting struggle to change the practice of lack of anesthesia in neonatal surgery. The medical establishment opposed her struggle. She was patronized and discouraged from pursuing legal action, but she also had her supporters [15]. Her son’s neonatologist described neonatal surgery with only muscle relaxant and minimal anesthesia as based on ‘‘ignorance, hubris and barbarism’’ [16]. It was not until August 1986, when The Washington Post published the story of Jeffrey Lawson’s surgery, that the resistance to examining neonatal pain

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practice in the NICUs of the United States began to dissolve [14]. Jill Lawson’s personal struggle had generated collective pressure through the public press. Other parents supported her efforts [17 – 19]. Lobbying by parents changed neonatal pain practices in a variety of settings, beginning with the Children’s Hospital National Medical Center in Washington, the setting of Jeffrey Lawson’s surgery [20]. Jill Lawson’s efforts began with reasoned appeals to change anesthetic practice, but when she met with resistance, she made her son’s situation the focus of an impassioned and, at times, bitter crusade. She used language that was not scientific discourse and the attacks were personal, pointed and, perhaps at times, from the point of view of those who were the target, unfair. But a mother reacting to the suffering of her child should be passionate. The passion and the vehemence of her efforts were the major reasons they were taken up in the popular press. The media respond to passion. Her work made a major contribution to the re-examination of neonatal pain. We doubt that a calm, reasoned, dispassionate discourse would have been as effective. The American Pain Society established the Jeffrey Lawson Award to recognize advocacy in pediatric pain. Jill Lawson was the first recipient of this award. Many changes in neonatal practice occurred in response to Jill Lawson’s public demands. Change may also occur in response to specific demands by parents of an individual child. Harrison [14] and Butler [21] suggested that parents consider the following options to ensure adequate pain management of their newborn.   







Infant pain and NICU procedures can be discussed prior to birth with the obstetrician and pediatrician when a premature delivery is a possibility. Parents can choose not to have optional surgery such as circumcision for their baby. When babies are hospitalized, parents can discuss with the physician and nurses how pain in neonates is assessed and managed and what medication will be given in their infant’s unit. Anesthesia can be discussed with both the surgeon and the anesthesiologist prior to surgery. Risks of anesthesia and analgesics, risks of their alternatives, and additional methods of providing comfort may be discussed with the physician. Parents may also choose to sign a limited consent form specifying consent only for anesthetized surgery. Many physicians, however, may not accept a limited consent because it impinges on their professional responsibility to do what they think is most appropriate. Parents can seek an independent second opinion when conflict arises.

Physicians, nurses and other allied health professionals are also in a position to develop changes in protocols and procedures for neonatal pain practice within their own units. Resources such as the Pediatric Pain Sourcebook (http://is.dal.ca/ ~painsrc/), which provides examples of policies and protocols that have been

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adopted by other institutions, and published detailed guidelines such as those recently published by expert consensus groups [22] or professional organizations [23] can be of assistance. The social context of the scientific work of K.J.S. Anand Scattered scientific reports and reviews have appeared for years suggesting that full-term and premature neonates feel pain and should be treated for pain [24,25]. Even the ancient Greeks believed that infants were capable of pain sensation. In fact, Plato (about 400 BC) thought that for infants, all feeling was essentially painful [26]. Felix Wurtz, a physician of the seventeenth century questioned, If a new skin in old people be tender, what is it you think in a new born Babe? Doth a small thing pain you so much on a finger, how painful is it then to a Child, which is tormented all the body over, which hath but tender grown flesh? If such a perfect Child is tormented so soon, what shall we think of a Child, which stayed not in the wombe its full time? Surely it is twice worse with him. ([27] p. 204 – 5)

Despite the long history of clinical and philosophic opinion and a few scattered scientific reports, it was the randomized trials of Dr. Kanwaljeet Singh Anand and his colleagues that were the key scientific studies to raise the issue of pain in the neonate. Although the studies themselves were very important, it was the social context—more specifically, the public controversy surrounding the studies—that brought neonatal pain to the public press and the national consciousness in the United Kingdom. Following medical and pediatric training in India, Dr. Anand began his doctoral research in medical sciences on a Rhodes scholarship in Oxford, England. His research was under the direction of Professor A. Aynsley-Green and was focused on the measurement of physiologic stress from anesthesia in the newborn. Anand [28] first reviewed the prevalence of minimal anesthesia for surgical correction of patent ductus arteriosus as reported in published studies. He found that 77% of the 1157 neonates in these studies were given a muscle relaxant without anesthetic or a muscle relaxant with nitrous oxide (minimal anesthetic). This was commonly known as the Liverpool technique and it was standard practice at the John Radcliffe Hospital where Anand was conducting his research. Following this review, a pilot study was developed to examine the stress response in neonates undergoing repair for a patent ductus. This study demonstrated that a massive stress response occurred in all babies. Finally, the research team devised a set of randomized trials to conclusively determine whether or not deep anesthesia could blunt the stress response. Throughout, the research group consulted with methodological experts to insure that the studies were scientifically sound. An independent ethics committee subjected all studies to careful ethical review. The results showed that deep anesthesia substantially blunted the stress response and may have contributed to better clinical outcome.

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A mention of the work by Anand and colleagues was made in an editorial in the British Medical Journal [29], with a suggestion that this research indicated that changes in intensive care units should be considered. A paper by Anand based on this work was presented during April 1986 at the annual meeting of the British Paediatric Association and won the Michael Blacow prize for the best paper. The first article was published in January 1987 in Lancet [30], followed shortly by an article in the British Medical Journal [31]. These studies were noticed by academics and medical professionals and reported in the general press but did not receive a great deal of public notice. In June 1987, however, the Daily Mail, a London tabloid that specialized in scandal and screaming headlines, featured Anand’s research in an article titled, ‘‘Pain-killer shock in babies’ operations,’’ and accused the researchers of unethical behavior. After Professor Aynsley-Green contacted the newspaper to correct these errors, he was once again attacked in the Daily Mail under the headline, ‘‘This test is a crying shame.’’ There was some notice in the other press, but the controversy died down until 14 members of Parliament who belonged to the All-Party Parliamentary Pro-Life Group issued a press release under the heading, ‘‘Inhumane baby operations slammed.’’ At the same time, Anand was being acclaimed by his fellow scientists for his presentations of the elegant data from this series of studies to the World Congress of the International Association for the Study of Pain in late August 1987. The press release accused the investigators of barbarous experimentation and demanded an investigation by the General Medical Council Disciplinary Committee for misconduct and negligence. The uproar was immediate and widespread. Initially, press reports focused on the accusations of the members of Parliament; however, quickly there was a rush of distinguished researchers and clinicians who pointed out that the studies were entirely ethical and would lead to better care of babies. The control group had received standard care, which was clearly inferior to the more aggressive approach in the treatment group. Over the next few months, several editorials in leading medical journals reviewed this controversy and supported the ethics of the studies. The attacks by the Daily Mail and the All-party Parliamentary Pro-life Group gained an incredible amount of publicity for the Anand studies. This public controversy appeared to be effective in bringing about change to what had been standard care in neonatal anesthesia. Again, the social context was instrumental. Public pressure is a very crude method to trigger change. Public pressure does not distinguish between well-validated scientific findings and quack medicine or speculation. If public pressure is effective in changing practice without adequate research, harmful analgesic practices could become standard practice. Eugene Braunwald (cited in [32]) emphasized that the premature dissemination of a new medical technique, before evaluation by carefully designed clinical trials, is like the proverbial genie escaped from the bottle. The confusion resulting from unrestrained therapeutic exuberance cannot be reversed. On the other hand, if change does not occur rapidly, the short attention span of the media may cause a topic to enter and leave public awareness very quickly. Nevertheless, without public pressure, change is not easily implemented.

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Resistance to change ‘‘It took me a few days to stop thinking of them as people, as human beings, and to revert to seeing them primarily as receivers of treatment.’’ This comment was made by a neonatal fellow on returning to service on a neonatal unit after several months’ absence. There are two factors that may prevent change in neonatal pain management: denial and desensitization. Denial involves not acknowledging pain; desensitization involves the failure to attach the normal emotional response to neonatal pain. To function effectively in the NICU and to deal emotionally with performing invasive procedures on neonates without analgesia or with limited pain relief, physicians and nurses may rely on these processes. In the past, professional conferences, textbooks, and journals concerned with pediatric care tended to give little attention to neonatal or pediatric pain management. This attention has dramatically changed. For example, pediatric pain research presented at the Pediatric Academic Societies annual meetings (the principal American venue for pediatric research) has quadrupled from fewer than 10 abstracts in 1988 to more than 40 in 1993 [33]. In 1987, when Rana [34] reviewed the leading English language textbooks of pediatrics, virtually no information on pain (less than 1 page out of 12,000 pages) was found. Currently, every major pediatric text has complete chapters on pain and pain management, and pain is discussed throughout the texts. Furthermore, a textbook on neonatal pain has now gone into its second edition [35]. Similarly, the publication of articles in pediatric pain has increased significantly [33,36], and several books are devoted to pain in children [37 – 39]. Although we have no documentation as to the change in neonatal pain literature, this literature seems to have paralleled the pediatric literature. Although awareness of neonatal pain has increased and education has improved, denial, desensitization, and rationalization may still play a role and may occur for a variety of emotional and cognitive reasons. Pain responses may still be explained as reflexive or random movements. A difficulty in neonatal medicine is the understandable preoccupation with survival—in some cases, to the exclusion of all else [20]. Pain treatment may be considered of secondary importance, especially if methods of pain relief are believed to be harmful to the patient. These views are harder to maintain as the evidence for safety of analgesia improves. Even 2 decades ago, many health care professionals were concerned with neonatal pain. Fletcher [20] noted that neonatal pain perception was not denied by all: Certainly, not by those of us at the bedside of critically ill infants, who see them flinch from procedures, startle in response to loud noises, and turn from bright lights and various other forms of stimulation. Not by those who have heard infants’ anguished cries and seen their vigorous withdrawals from painful stimuli. Not by those who have observed their increasing heart and respiratory rates and profuse sweating in response to heel sticks or circumcision.

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A professional who has come to know a neonate intimately has more chance to learn how to differentiate between neonatal pain behavior and behavior related to other needs. Attending to the neonate as a social being is more complicated than caring for a full-term infant for many of the reasons that were previously discussed; a neonate does not have many of the physical features that draw out social attention. It takes more time and more effort to recognize and understand the communication of a neonate. It can be tempting to attribute behavioral distress of the neonate to the absence of a parent or disruptions in routine rather than to pain as the result of a procedure. Desensitization, denial, and rationalization have negative consequences for the neonate, the parents, the parent-professional relationship, and for professionals themselves. The most serious consequences are that symptoms of pain behavior and the sequelae of pain are undetected, minimized, or denied, and that changes in neonatal pain management are resisted. Such outcomes result in unnecessary suffering for neonates, with further possible health trauma as a result of physiologic distress and with the potential for long-term sensitization to pain. Most parents approach a sick neonate naı¨vely, expecting the infant to be as responsive to pain as an older baby. Parents have a strong emotional investment in wanting to love, nurture, and protect this new baby and will be especially observant of behaviors in the neonate that may be indicative of pain. Parents will assume that their neonates are given pain relief for invasive procedures. If neonates do not receive adequate analgesia, parents may feel they have failed in protecting their child [13,19,40]. If parents also observe that professionals are not perceptive to symptoms of pain behavior in the neonate or that they do not provide adequate pain relief, hostility or, ironically, acceptance of professional denial of neonatal pain may occur. Increased public awareness of controversy in neonatal pain [18,19] may exacerbate the friction between parents and professionals. Such early negative experiences between parents and health care professionals may have deleterious effects on future health care for the child and the family. Unfortunately, for some parents, the resultant feelings of guilt (that as parents, they were unable to protect their child from unnecessary pain) might be very stressful and may lead to oversensitization and hostility toward health professionals. Health professionals who are convinced by the scientific evidence and their clinical experience in an NICU that neonates do feel pain but who are unable to provide relief because they either do not have the authority to do so or they believe they cannot challenge or change current practices of their unit may feel increasingly helpless, depressed, and disillusioned about neonatal care. In addition, those who recognize pain are presented with another problem. Although there are good strategies of pain management for some procedures, there remains significant scientific uncertainty about how to control pain from some of the most common procedures in neonates (eg, heel sticks). The inability to provide adequate pain relief may cause internal conflict or arouse feelings of guilt or helplessness.

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Changes in pain management per se have worked in concert with widespread efforts to change the environment of NICUs. The most comprehensive approach is that of developmentally sensitive care developed by Heidi Als [41] and her collaborators. More effort is being made to decrease noxious stimuli in the neonatal environment by decreasing light intensity and auditory stimulation, by providing more opportunity for uninterrupted sleep, and by comforting infants using positioning and swaddling.

The neonate’s learning about pain It is possible that the social environment affects the pain perception of the neonate. Social factors have a major impact on adults’ and children’s pain responses. As Craig [3,4] and his colleagues demonstrated in numerous carefully controlled laboratory experiments with adults, models that tolerate pain will increase pain tolerance in subjects and models that are intolerant reduce pain tolerance. There is also some evidence that reinforcement will similarly alter tolerance. It is plausible and commonly believed (but only now being proved) that families teach their children how to cope with pain [42]. Pain does aggregate in families [43]. The mechanisms that may explain familial pain aggregation are thought to be modeling, reinforcement, and instruction. In the case of the neonate, teaching and learning about pain responses have had little time to occur; however, such learning may be important in some contexts. It is part of the folklore of most NICUs that neonates who are subjected to numerous invasive procedures soon develop the tendency ‘‘to go off’’ when their incubator is approached by anyone. If this is true, these neonates might well have developed a classically conditioned response because of the repeated pairing of pain with human presence. The one study [44] to examine classical conditioning of pain in the neonate used rubbing of the foot as the conditioned stimulus and a heel prick as the unconditioned stimulus. Only one trial was used and no conditioning was detected. Other approaches using repeated stimuli or a stronger unconditioned stimulus might demonstrate conditioning. Work with infant pain [45,46] has shown that the social context both at the time of the pain and at other times very significantly alters the response to pain in infants as young as 6 months of age.

Standards of care in neonatal pain Institutions (in their general standards) and professional associations (in their ethical standards) seldom detail exact procedures but rather expect a standard of care that should be provided. Detailed protocols in many different forms are in place in some institutions for specific aspects of neonatal pain. In addition, professional associations or other organizations may develop specific practice guidelines. Practice guidelines and institutional protocols are intended to guide

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behavior but they are phrased to allow professional judgment on most issues. Along with research articles, professional articles, and material in widely used textbooks, these documents combine with actual practice to set a standard of care. Although often invoked in a nonlegal context, standard of care has been most widely discussed in the legal literature, especially the negligence literature. The nonlegal notion of standard of care is very similar to the concepts involved in civil negligence, with one important difference. Institutional and professional standards may be designed to provide both a minimum acceptable level and present goals to be attained. Standards of care in negligence law are minimum standards. An important question is What is the standard of care against which a specific physician or nurse dealing with a specific infant should be ethically and legally judged? Clearly, it is not good enough for a physician or nurse just to do his or her best if it is below what is an acceptable standard of care. On the other hand, the law and ethical guidelines are concerned with reasonably good care rather than the best possible care. Standard of care has received many interpretations. Sharpe [47] outlined four levels of standard of care. These levels are 1. Common practice in the immediate locality of the professional accused of negligence. 2. Common practice in similar locations. 3. Common practice in relation to the medical resources available to the health professional. 4. National minimum standard of a reasonable and prudent practitioner. Sharpe [47] suggested that both American and Canadian courts tended to use the third level to determine standard of care in negligence. This approach is also likely to be true of professional ethical bodies. The third level requires the appropriate use of consultation and referral to a major medical center if one is available. Due to the rapid dispersal of medical knowledge and the ready access to consultation and referral, it is no longer accepted that standards of care should vary across most geographic areas. It is unlikely that a person practicing in an NICU in one setting could claim to be held to a different, lower standard of care than someone practicing in any other NICU. They might, however, be legitimately practicing at a lower level than the most advanced unit. The concept of standard of care does not necessarily mean that the average standard of care is acceptable if that average is deficient. The standard of care that the courts or ethical boards would expect is that of a reasonable and prudent professional. In rapidly changing areas such as neonatal pain, one might argue that the reasonable and prudent professional should not rely on past practice or standard texts that may be out of date. Furthermore, it is always open to a court or ethical board to raise the standard of care if the court feels it is appropriate. Although it is clear that standards of neonatal pain care are sometimes violated, the authors know of no legal or ethics cases on this topic. Institutional disciplinary actions may have occurred, but these actions are seldom reported.

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Still, standards of care are helpful in prompting behavior outside of the legal and ethical domains. Statements and guidelines of professional or governmental agencies play an important role in determining what a reasonable physician or nurse should do and, consequently, determining the standard of care. Three important documents have influenced the standard of care in neonatal pain. The first is the joint statement of the American Academy of Pediatrics, Fetus and Newborn Committee, Section on Anesthesiology, Section on Surgery [48] and the American Society of Anesthesiologists [49]. This statement includes the following opinion: Local or systemic pharmacologic agents are now available to permit relatively safe administration of anesthesia or analgesia to neonates undergoing surgical procedures, and that such administration is indicated according to the usual guidelines for the administration of anesthesia to high-risk, potentially unstable patients. . . . [Any decision to withhold analgesia or anesthesia] should be based on the same medical criteria used for older patients. The decision should not be based solely on the child’s age or perceived degree of cortical maturity. [49]

The second document is the Clinical Practice Guideline for acute pain management published by the US Agency for Health Care Policy and Research [50]. This guideline discusses the measurement, strategies for treatment, and institutional responsibility for pain management. Although there is not great detail in the methods used for measurement and treatment of neonates, the importance of this document for neonatal pain lies in the unequivocal endorsement of the need for neonatal pain management by a blue ribbon panel who has studied and reviewed the research literature at the request of the US Department of Health and Human Services. The most recent policy statement, a joint statement by the American Academy of Pediatrics and the Canadian Paediatric Society [23] provides a series of recommendations about the general approach to pain management in the neonate and the need for institutional support for better pain management. These documents have provided official sanction for the necessity of pain management in neonates and have had an important influence on legitimizing practice. There is no evidence that in themselves, they change practice. A recent consensus document that was developed by an ad hoc international group (Anand, 2001) based on a series of systematic reviews and consensus meetings provides detailed procedure-specific recommendations and guidance, with citations for the evidence. Although not sanctioned by any formal organization, the stellar reputation of the participants and the international representation may provide more weight for the recommendations.

Research in neonatal pain Research on neonatal pain has advanced quickly and the social climate that supports this research has strengthened. Researchers are well aware that the quality of an idea and the competence of the research team only partially

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determine whether research is done. Before research can flourish, a social structure that supports that research must be built. Major research-funding agencies including national agencies in the United States, Canada, the Netherlands, and the United Kingdom have supported neonatal pain research programs, and there is now a small cadre of researchers around the world who are expert in neonatal pain. Research on neonatal pain, however, suffers from significant problems that are common in emerging areas of research. There are very few training opportunities for the next generation of researchers. Individual researchers struggle to provide mentoring and training for a few trainees, but there are few, if any, fellowships dedicated to this area. There are no training grants dedicated to this area and no funding agency that has neonatal pain as a top priority. There are still fewer researchers competent to provide peer review of research or fellowship applications. The tendency of research in this area continues to be labeled as unimportant or obvious by reviewers who do not have expertise. Although research on neonatal pain is not limited to any one discipline, there are few centers that have truly transdisciplinary research teams. Most research on neonatal pain is built around a single researcher. Studies that require large numbers of participants cannot be readily undertaken because there are no established multicenter collaborative groups with the distributed expertise to provide the necessary infrastructure.

Summary Neonatal pain and neonatal pain management occurs in a social context and is influenced by this context. Changes in the practice of pain management have clearly occurred over the last 20 years. Changes have occurred because of the confluence of scientific research and lobbying, primarily by parents. Although the standard of care for neonatal pain has risen dramatically in the past 20 years, much remains to be done. Procedure pain appears to be a continuing issue, and pain in the cognitively handicapped neonate has not been addressed. Research on the social context of pain is almost entirely lacking. References [1] Butler NC. The NICU culture versus the hospice culture: can they mix? Neonatal Netw 1986; 5(2):35 – 42. [2] Johnston CC, Collinge JM, Henderson SJ, et al. A cross-sectional survey of pain and pharmacological analgesia in Canadian neonatal intensive care units. Clin J Pain 1997;13:308 – 12. [3] Craig KD. Social disclosure, coactive peer companions, and social modeling determinants of pain communications. Can J Behav Sci 1978;10:91 – 104. [4] Craig KD. The facial display of pain. In: Finley GA, McGrath PJ, editors. Measurement of pain in infants and children. Seattle (WA): IASP Press; 1998. p. 103 – 21. [5] Purcell-Jones G, Dormon F, Sumner E. Pediatric anaesthetists perceptions of neonatal and infant pain. Pain 1988;33:181 – 7. [6] de Lima J, Lloyd-Thomas AR, Howard RF, et al. Infant and neonatal pain: anaesthetists’ perceptions and prescribing patterns. BMJ 1996;313:707.

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