The Journal of Pain, Vol 14, No 4 (April), 2013: pp 338-350 Available online at www.jpain.org and www.sciencedirect.com
Critical Review The Infancy of Infant Pain Research: The Experimental Origins of Infant Pain Denial Elissa N. Rodkey and Rebecca Pillai Riddell Department of Psychology, York University, Toronto, Ontario, Canada.
Abstract: Skepticism toward infant pain characterized much of 20th century research and clinical practice, with infant surgery routinely conducted with minimal or no anesthesia into the 1980s. This paper offers a historical exploration of how this view became common by reviewing and analyzing the experimental infant pain research of the 19th and early 20th centuries that contributed to the development of infant pain denial. These experiments used pinprick and electric shock, and the results were generally interpreted as evidence of infants’ underdeveloped pain perception, attributed to their lack of brain maturation. Even clear responses to noxious stimuli were often dismissed as reflex responding. Later these experimental findings were used by anesthesiologists to support the lessened use of anesthesia for infants. Based on the reviewed literature, this paper suggests that 4 interrelated causes contributed to the denial of infant pain: the Darwinian view of the child as a lower being, extreme experimental caution, the mechanistic behaviorist perspective, and an increasing emphasis on brain and nervous system development. Ultimately this history can be read as a caution to modern researchers to be aware of their own biases, the risks of null hypothesis testing, and a purely mechanistic view of infants. Perspective: This article reviews the history of 19th and early 20th century infant pain research, tracing how the widely accepted belief that infants could not feel pain developed in the period prior to the growing acceptance of infant pain. Four interrelated causes are posited to help explain the tolerance of infant pain denial until recent times. ª 2013 by the American Pain Society Key words: History, neonate, infant pain, pediatric pain.
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ain research’s most famous infant, Jeffrey Lawson, was born prematurely February 1985 and underwent open heart surgery shortly thereafter.26 What made this particular surgery noteworthy was the fact that Jeffery was awake and conscious throughout the entire procedure. The anesthesiologist had administered only Pavulon, a paralytic that has no effect on pain. Only after Jeffrey died 5 weeks later did his mother, Jill, learn the truth about his surgery. Jeffrey had been too young to tolerate anesthesia, the anesthesiologist said, and anyway, ‘‘It had never been demonstrated to her
Work was funded by a Canadian Institutes of Health Research New Investigator Award to Rebecca Pillai Riddell. There were no conflicts of interest related to this research. Address reprint requests to Rebecca Pillai Riddell, The O.U.C.H. Lab, Department of Psychology, Faculty of Health, 119 Behavioural Sciences Building, Toronto, ON M3J 1P3. E-mail:
[email protected] 1526-5900/$36.00 ª 2013 by the American Pain Society http://dx.doi.org/10.1016/j.jpain.2012.12.017
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that premature babies feel pain.’’26(p.125) This was not the case of a rogue anesthesiologist; textbooks at the time taught that the surgery Jeffrey underwent ‘‘could be safely accomplished with only oxygen and a paralytic’’69(p.580) when performed on infants. In her advocacy work Lawson questioned how such a belief developed: ‘‘If I had been told by a physician, no matter how senior, that infants don’t feel pain, I would never have believed it. What constitutes the difference between my reaction and that of the thousands of physicians who did believe it?’’27(p.1198) Decades later, the question of how such medical practice could evolve still plagues us. This paper offers a historical response to this question by analyzing the early infant pain research that contributed to the development of infant pain denial. Skepticism toward infant pain characterized much of 20th century research and clinical practice, with infant surgery routinely conducted with no or minimal anesthesia well into the 1980s.51 It was not until the emergence of parent activism and the rapid growth of pediatric pain
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research in the 1980s that the denial of infant pain began to be challenged. Anand and Hickey’s seminal article1 was particularly important in refuting many of the earlier beliefs about infant pain perception, such as the claim that the lack of myelination of the nervous system prevented infant pain perception.
Historical Methods A historical review of the infant pain literature of 19th and early 20th centuries can reveal the particular attitudes, assumptions, and research findings that played a causal role in establishing the later erroneous scientific consensus that newborns do not experience pain. Establishing the original causes of infant pain denial through the historical record is critical because vestiges of this skeptical attitude persist to the present day and bias modern research. Discovering how these views arose requires a thorough review of the historical experimental work on infant pain. Unfortunately, published works that review the history of infant pain research are limited to the following: Chamberlain9 reviews 20th century infant pain research from an anticircumcision perspective, McGrath30 reviews the history of infant pain research in the 1980s, and Pabis et al37 and Unruh64 review the ancient and medieval views of infant pain. While these publications offer useful literature reviews, they do not evaluate infant pain experiments in any depth. In contrast, this paper gives careful attention to the assumptions and design of the historical infant pain experiments, gleaning from their language and structure evidence of the views and motivations of early infant pain researchers. Additionally, given that these experiments were conducted across nearly 2 centuries and arose in diverse contexts and theoretical systems, we interpret these experiments in light of their social and scientific contexts. This project involved an extensive literature search for historical publications on infant pain, which began with database searches of PsycINFO, Pubmed, and ProQuest. However, because most historical experimental articles are not indexed in modern databases, these initial searches uncovered only a handful of relevant sources: a historical review of infant pain experimentation,9 a 1954 review of literature on the neonate,44 a history of pain,48 and a history of anesthesia.42 The reference sections of these sources formed the basis for further snowball searching, which resulted in 24 articles or books dealing with infant pain published from 1848 to 1974 (see Table 1). Because this paper expands the number of historical experiments beyond the scope of previous reviews, we decided to focus only on experiments that clearly test infant pain and to exclude borderline cases of experiments on infant reactions to other ‘‘noxious stimuli,’’ such as temperature, unpleasant tastes, or tactile pressure, even though such experiments may well have been conducted with the same motivations.10,23,37,45 These exclusions resulted in a total of 20 articles for analysis. Taken together, these articles provide a rough chronology for the development of infant pain denial.
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In what follows we review those experiments that were important in establishing views of infant pain, as judged by their influence on successive researchers, or that demonstrate the experimental design typical of a particular time period. In addition, based on these articles and what is known about their historical contexts, we have identified 4 factors that appear to have played a causal role in the development of infant pain skepticism. These are 1) the Darwinian view of the child as a lower being; 2) extreme experimental caution; 3) the mechanistic behaviorist perspective; and 4) an increasing emphasis on brain and nervous system development. To some degree these factors implicate the modern scientific method, as we show in the discussion. But first, we turn to the context in which experimentation on infant pain began: the 19th century.
Nineteenth Century Developments in Pain The modern view that pain is negative and that alleviating it is the goal of medical intervention was not shared by earlier periods. Although by the time of the Enlightenment the general trend was toward a more secular, physiological understanding of pain, pain was still often seen as beneficial.48 Since pain often occurred in the natural course of illness, it was seen to be useful not only in diagnosis but also in treatment. Well into the 19th century doctors might induce pain in order to bring on the crisis of the illness, since pain was associated with the body’s healthy, healing reaction to illness or surgery, whereas loss of sensation often indicated a nearness to death. For example in 1826, American doctor Felix Pascalis wrote in his treatise on pain, ‘‘Painful.sensations all require sound and healthy organs. It is therefore our axiom, that the greater the pain, the greater must be our confidence in the power and energy of life.’’48(p.43) The reality that medical options for alleviating pain at the time were limited doubtless contributed to this more positive evaluation of pain. Nevertheless, the view of pain as beneficial was sufficiently powerful that it inspired some resistance to ether and chloroform when they were pioneered around 1846.42 Traditional religious attitudes of pain as divinely ordained and natural (particularly for childbirth), in combination with the very real risks of early forms of anesthesia, gave some reason to question whether anesthesia was actually a medical advance.42 This ambivalence toward pain and the relatively recent invention of anesthesia helps to explain why infant pain sensitivity was not explored earlier than the 19th century. If preventing pain was not seen as an unqualified good and if there were few medical means of alleviating pain available, the question of whether infants felt pain was largely irrelevant. In addition, infants’ lack of agency and limited self-expression meant the concerns about infant pain were largely drowned out in discussions of maternal pain driven by their more vocal mothers.42 This concern over maternal pain was also the result of the common view that different demographics differed
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Table 1.
METHOD
CONCLUSIONS
Review
Discusses use of ether in infant surgery
Infants can be successfully operated on early after birth; they do not feel or remember pain.
Medical record
Harelip [cleft palate] surgery on 6 conscious infants 6-12 hours old
Genzmer A: Untersuchugen Ueber die Sinneswahrhehumugen des Neugeborenen Menschen. Inaugural € tzche Dissertation, Plo Buchhandlung, Halle, 187318 Preyer W: The Mind of the Child: The development of the intellect. Arno Press, New York, 188946
Experiment
Pokes approximately 60 infants with pins on their noses, upper lips and hands
Sensitivity to pain is limited in early hours of life, but increases with age, therefore surgeries should be conducted as close to birth as possible. Infants show no sign of discomfort in response to pinprick, they are insensitive to pain.
Observations
Records sensitivity of son to non-painful touch, reviews Genzmer’s work
Blanton MG: The behavior of the human infant in the first 30 days of life. Psychol Rev 24:456-483, 19177 Sherman M, Sherman IC: Sensorimotor responses in infants. J Comp Psychol 5:53-68, 192553
Experiment
Observations from pricking of toe, lancing of infected finger, circumcision; pricked 21 2–26 day old sleeping infants on the wrist 96 infants 1 hour–12 days old poked with a pin on cheeks, thighs, calves
€tigkeit des Peiper A: Die hirntu neugeborenen. Jahrbuch fur Kinderheilkunde 29:290-314, 1926a38
Experiment
1852
1873
1889
1917
1925
1926
TYPE
Experiment
Measures the latency of response to pinprick (2–4 mm depth) and electric shock in older new newborns
CITES
Son is surprisingly sensitive to light touch at a young age, but Genzmer says that infant are insensitive to pain. This may be because nerves are not mature in infants and so they require a pinch rather than a pinprick to activate nerves. 8 out of 21 infants did not respond to wrist prick.
Genzmer, 187318
The sensorimotor responses studied (including pain) are imperfect at birth, and increase in adequacy with age. Infants do feel pain and newborns are not less sensitive (may even be more sensitive); typical response is movement and screaming with a latency similar to adult pain response.
Blanton, 19177
Preyer, 188946
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TITLE Bigelow J: Ether and chloroform: Their discovery and physiological effects. Ether and Chloroform: A Compendium of their History, Surgical Use, Dangers and Discovery. David Clapp, Boston, 18486 Peirson AL: Early operation for harelip. Am J Med Sci 24:576, 185241
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DATE 1848
Continued
DATE
TITLE
1927
Wolowick AB: Uber die gegenseitige wirkung der schmerz- und nahrungsreflexe bei kindern. €r Kinderheilkunde und Jahrbuch fu Physische Erziehung 115:185-193, 192770 Dockeray FC, Rice C: Responses of newborn infants to pain stimulation. Ohio State University Studies Contributing to Psychology 12: 82-93, 193416 McGraw M: Growth: A study of Johnny and Jimmy. Appleton Century Crofts, New York, 193531
1936
1941
1934
1935
1954
1956
TYPE
CONCLUSIONS
Experiment
18 children of varying ages shocked on foot before, during, and after food intake. Measured strength of shock necessary to produce defense response
Food intake results in less sensitivity to pain stimulus, especially in infants.
Experiment
40 infants 4 hours–5 days old poked with pin in cheek, forearm, palm, leg and toe
There seems to be no change in response over age, responses appear to be undifferentiated (unrelated to where the infant was stimulated).
Experiment
Twins poked with a safety pin on head, trunk, and upper and lower extremities
Sherman M, Sherman I, Flory CD: Infant behavior. Comp Psychol Monogr 12:1-107, 193652
Experiment
317 infants shocked or pricked on the face and leg with special algometers
McGraw M: Neural maturation as exemplified in the changing reactions of the infant to pin prick. Child Dev 12:31-42, 194132 Pratt KC: The neonate. In: Manual of Child Psychology, 2nd edition, (Carmichael, L., Ed.), Wiley, New York, 1954, pp 215-29144
Experiment
75 children birth–4 years old poked with safety pin on head, trunk, upper and lower extremities, resulting in 2008 observations Chapter on the neonate reviews research on pain stimuli
Reflex withdrawal and crying accompanied by diffuse body movement is typical of first 2 months, in later developmental stages the infants engage in successful escape and defense from the pain stimulus. The face is more sensitive to pinprick than the legs; older infants more sensitive to pain than younger infants. Infants cannot localize cutaneous irritation, probably the result of limited brain development.
Graham FK, Matarazzo RG, Caldwell BM: Behavioral differences between normal and traumatized newborns: II. Standardization, reliability, and validity. Psychol Monogr 70(21): 17-33, 195619
Experiment
Review
Electric shock to back and back of leg in ascending and descending voltages in 110 traumatized and nontraumatized infants 7 days old or younger
It has been demonstrated that infants are sensitive to pain, however there is disagreement among researchers over whether the sensitivity increases with age. Infant response to pain a reliable indicator of brain damage.
CITES
Sherman & Sherman, 192553
Sherman & Sherman, 192553
Dockeray & Rice, 1934,16 Genzmer, 1873,18 Peiper, 1926b,39 Preyer, 1889,46 Sherman, Sherman & Flory, 1936,54 Wolowick, 192770 Dockeray & Rice, 1934,16 Sherman, Sherman & Flory, 193654 The Journal of Pain
METHOD
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Table 1.
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Continued
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Table 1.
TITLE
1957
Graham FK, Pennoyer MM, Caldwell BM, Greenman M, Hartmann AF: Relationship between clinical status and behavior test performances in a newborn group with histories suggesting anoxia. Pediatrics 50:177, 195720 Lipsitt LP, Levy N: Electrostatic threshold in the neonate. Child Dev 30:547554, 195929 Peiper A: Cerebral Function in Infancy and Childhood. Consultants Bureau, New York, 1961/196339
Experiment
60 infants under 24 hours old were given electric shocks behind their knee
Impaired pain response on a ‘‘pain threshold test’’ in anoxic infants.
Experiment
36 infants 4 hours–24 days old shocked on back of calf and big toe
Review
Reviews recent research on infant sensitivity to pain, including his own
1968
Swafford LL, Allan D: Pain relief in the pediatric patient. Med Clin North Am 52:131-136, 196860
Hospital report
Discusses the limited use of analgesics in surgery recovery for children and infants in their hospital
1969
McGraw M: The Neuromuscular Maturation of the Human Infant. Hafner Publishing, New York, 196933
Review
Reviews the findings of McGraw, 194132
1974
Rich EC, Marshall RE, Volpe JJ: The normal neonatal response to pinprick. Dev Med Child Neurol 16:432434, 197449
Experiment
130 infants tested with needle prick to the lower leg
Pain sensitivity increases over course of first 4 days of life, grimacing or crying not often exhibited. Infants respond to pinprick and engage in protective skin reflexes. Previous researchers’ findings’ inconsistency with these findings is due to variations in infants’ readiness to react. Children and infants generally do not need pain relief following surgery, suggestion and distraction can be substituted for medication. Infant response to pinprick becomes more localized and differentiated with age. This should be understood in the context of their still developing cerebral cortex. The normal response to pinprick in infants is movement of the limbs, sometimes accompanied by crying and grimacing.
1959
1961
TYPE
METHOD
CONCLUSIONS
CITES Graham, Matarazzo & Caldwell, 195619
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DATE
Genzmer, 1873,18 Sherman, Sherman & Flory, 1936,54 Wolowkick, 192770
McGraw, 1941,32 McGraw, 1969,33 Peiper, 196340
McGraw, 194132
Pieper, 196340
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Rodkey and Pillai Riddell in their pain sensitivity. It was widely held that women were more sensitive to pain, as Dr. Wendell Holmes commented in 1867, ‘‘She [woman] is so much more fertile in capacities of suffering than a man. She has so many varieties of headache.’’42(p.149) In contrast, ‘‘lower’’ races and classes were thought to be less sensitive to pain. Age was a more complicated factor. While most agreed that old age diminished the ability to feel pain, there was controversy over whether children were more or less sensitive than women.63 Given infants’ limited mental capacity, they were often classed with the lower animals. Some argued for this based on empirical evidence, such as Dr. Abel Peirson of Salem, Massachusetts, who in 1852 reported on 6 successful harelip (cleft palate) surgeries that led him to recommend surgery as close to birth as possible. Peirson reports ‘‘the sensibility to pain is less distinctly marked at first, than after a few days. In the last-mentioned case of harelip operation, the child actually slept while the lip was being dissected from the maxillary bone.’’41(p.576) Similarly, Henry Bigelow, in his 1848 history of anesthesia, argued that infants’ limited memory capacity rendered them incapable of suffering: Though I have operated on a child of three months who was so far inebriated [with ether] that its cries were modified into a sort of moan, yet I know of no case in which a young infant has been completely narcotized after its birth. Indeed the facility of controlling a child of this age, together with the fact that it has neither the anticipation or remembrance of suffering, however severe, seems to render this stage of narcotism unnecessary.6(p.15) Despite the attendant dangers, children and infants were sometimes anesthetized for surgery during the 1840s and 50s, although they were not the demographic most likely to receive anesthesia.42 However, the use of anesthesia on children was not necessarily a recognition of their pain, but an attempt to immobilize difficult patients, as is shown by an 1854 report of an infant who was ‘‘rolled firmly in a sheet as a substitute for ether’’ during harelip surgery.42(p.229) Alongside practical medical advances, physiologists pursued more theoretical lines of pain research. Ernst Weber investigated tactile thresholds and localization but left the details of pain vague.67,68 However, his pioneering research on physical senses and establishing perceptual thresholds for each of the senses influenced the direction of 19th century psychophysics research.48 The growth of science programs in German universities coincided with this psychophysical interest and supported the growth of experimental physiology, which led to an increasingly sophisticated understanding of the nervous system. However the partial knowledge of the nervous system meant that there was significant potential for disagreement; there was debate over whether pain depended on the central nervous system or the peripheral nervous system and whether pain receptors and pathways were exclusively dedicated to pain perception or had a more generalized function.8,48
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Darwin’s Theory of Evolution Another trend that paved the way for infant pain research was the stimulating effect Darwin’s evolutionary theory had on the scientific study of children. In his writing Darwin regularly used the behavior of infants as evidence of inherited traits or reflexes, and recapitulationist theory emphasized the importance of understanding children’s development.34 This led to an increased scientific interest in children, culminating in the child study movement in the 1890s, which deplored the lack of developmental knowledge and advocated the scientific investigation of children’s physical and mental development.56 In its popular form, parents and educators were encouraged to keep detailed records of the development of their own children, which were inspired by Darwin’s brief ‘‘Biographical Sketch of an Infant’’11 and considered a legitimate source of scientific data. Although parents recorded detailed observations of their infants’ senses, they exhibited a natural reluctance to experiment on infant pain, so little discussion of infant pain took place in these baby biographies. However, Darwin’s theory of evolution would ultimately contribute to infant pain denial. In Darwin’s view children were lumped together with animals, savages, and the insane as primitives whose emotional expression was simply reflex actions reinforced by habit, making them less reliable markers of pain.12,48 Initially, however, the Darwinianinfluenced interest in infant senses and sorting responses into reflexes and instincts simply helped to pave the way for later experimental investigations.
Extreme Experimental Caution The first to combine these lines of research and conduct an experimental test of infants’ pain sensitivity was Alfred Genzmer, who published Investigations on the Psychic Function of the Newborn18 in 1873, while a doctoral candidate in medicine and surgery at HalleWittenberg University. Genzmer was interested in the sensory perception of children and followed the lead of Adolf Kussmaul,25 a well-respected internist who had tested newborns’ senses, including the sensitivity to touch of the tongue, lips, nasal membranes, and eyelashes. But while Kussmaul had used a feather and a thin glass rod and cut short his taste experiments because they appeared to cause infant discomfort, Genzmer tested, with pins, ‘‘almost 60 children’’18(p.12) at a Leipzig training school for midwives. According to Genzmer, During the first days I pricked premature infants with fine pins in the most sensitive parts [of their] noses, upper lips and hands so intensely that small drops of blood oozed from these openings. They gave no evidence of discomfort—not even a slight quivering.18(p.12) Although Genzmer acknowledged that the ‘‘wetness of their eyes’’ sometimes increased when pricked, he dismissed this as unrelated, concluding that pain is ‘‘exceptionally poorly developed in the neonate.’’18(p.12) It was not uncommon in this era for researchers to be skeptical of children’s senses: 2 of the best-known baby
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biographers of the time concluded that babies did not develop their sense of hearing until several days after birth, thanks to their lack of response to sound stimuli.46,55 The assumption of lesser abilities was in part due to the Darwinian view of infants as more primitive beings, but another contributor was the fact that the idea of the scientific method was still evolving.52,71 In this earlier period when the term ‘‘scientist’’ was still new (coined in 1833) and scientific authority not universally accepted, scientists emphasized strict methodology to bolster their credibility.71 In this context researchers such as Genzmer were so concerned with establishing their scientific credibility that they practiced an extreme experimental caution, which although meant to keep them from unwarranted assumptions in fact biased them toward skepticism of certain phenomena. Infant pain was one such phenomenon, given the appeal of scientifically debunking the common sense assumption of infant pain combined with the often ambiguous evidence that infant pain researchers encountered. Genzmer’s work was obscure enough that it would likely have been forgotten had it not been cited by physiologist Wilhelm Preyer in his 1882 Die Seele des Kindes or The Mind of the Child.46 Preyer’s baby biography was far more comprehensive than any previous observational record of child development and, as a result, became a classic, influential in child psychology research well into the 20th century. Since The Mind of the Child was a record of Preyer’s son Axel’s growth, he predictably did not experiment on Axel’s pain sensitivity, only recording that ‘‘in the case of my boy’’ the sensitivity of the skin was ‘‘surprisingly great; for the child reacted by movements upon the slightest touches of his face.’’46(p.105) Instead, Preyer relied upon Genzmer extensively as an authority on infant pain, and therefore came to similar conclusions regarding infant sensitivity, stating that the infant . . . in the first days does not feel pain at many kinds of treatment that would cause pain to older children—treatments confined to a small area of skin; for example, pricks of a needle, cooling with ice, sewing up of wounds after operations (Genzmer)— for he often keeps perfectly quiet under such treatment and even falls asleep.46(p.148) Still, Preyer thought that infants were capable of experiencing pain since they enjoyed breastfeeding and gave evidence of experiencing pain, which he called ‘‘unmistakable for every diligent observer. Above all, crying is characteristic: it is piercing and persistent in pain.’’46(p.147) Rather than dismissing Genzmer’s work, Preyer used recent knowledge of nerve development to interpret Genzmer’s results, arguing that the nonresponsivity need not mean that infants are insensible to pain, but merely that in experiments using a fine needle the painful stimuli only reaches a few nerves.46 Preyer surmised that coarse receptive fields might account for the nonresponsivitiy of infants and a different stimulus, such as a slap or a pinch, which would reach more cutaneous
The Infancy of Infant Pain nerves might bring out a ‘‘pain reflex’’ in a newborn46(p.233) Preyer’s conclusion is mixed; he both denies that infants experience adult-level pain and yet maintains that this does not mean they do not experience pain at all since ‘‘screaming and movements can be elicited from children and animals just born . . . by pinching the skin.’’46(p.97) Preyer’s understanding of the pain response as primarily a reflex is important in the context of infant pain denial. Preyer articulates a concern with discovering the infant reflexes that was common in the 19th and early 20th centuries: ‘‘It would be of great interest to draw up a list, as complete as possible, of the reflex movements of the newly-born.’’46(p.233) This avid interest in children’s reflexes had its origins in Darwinism, as part of a larger project of explaining behavior in adaptive terms. In the late 19th century, interest in reflexes, the developing scientific method, and the Darwinian view of the infant as a primitive lower being all contributed to a mechanistic perspective of the child that made infant pain experimentation both more common and more accepted.
The Influence of Behaviorism While Darwinism set the stage for infant pain experimentation, its heyday was the first half of the 20th century as it was caught up in an increasingly reductionist conception of human psychology: behaviorism. Behaviorism became the dominant paradigm in psychology following J. B. Watson’s 1913 Behaviorist Manifesto66 and remained influential throughout the 20th century.2 As a result of Watson’s blackboxing of consciousness and cognition, psychologists focused exclusively on observable behavior. Pain research fit particularly well into this ethos—pain could be read as nothing but a mechanical stimulus-response. While Preyer could describe pain as a reflex and still affirm the infant’s experience of pain based on his observations, as psychology became more behaviorist, researchers came to understand even a clear pain response as irrelevant for the question of whether infants experienced pain; it was simply a reflex, an automatic response to stimuli. Watson’s claims that psychology was a ‘‘purely objective experimental branch of natural science’’66(p.158) resulted in the continuation of extreme methodological caution in which researchers were unwilling to make causal claims even in the face of clear pain responses. An early example of this behaviorist trend is Margaret Gray Blanton’s 1917 publication on the behavior of newborns.7 Not only does Blanton describe the infant behavior overwhelmingly in terms of reflexes, but her observations of infants’ response to ‘‘noxious stimuli’’7(p.458) were conducted at Johns Hopkins, under the supervision of Watson. Blanton records crying in response to the deep pricking of big toe, lancing an infected finger, and circumcision, yet in each case she resists concluding that the medical procedure was what caused the crying. When the infants regularly raised the opposite foot in response to the toe prick Blanton responds ‘‘As this is also one of the motions of kicking no conclusion could be drawn.’’7(p.472) and notes similar possible
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confounds for the other 2 procedures. Blanton also records an experiment in which she pricked 21 sleeping infants on the wrist with a pin, with a pressure that ‘‘when tried on my own wrist it aroused a pain response’’7(p.473) According to Blanton, 8 of the sleeping infants did not respond to pinprick. Indicating the lasting influence of Preyer, Blanton cites his conclusion that ‘‘Sensibility to contact is, in the first hour of life, much inferior to what it is later’’46(p.183) in her interpretations of these results. Since behaviorists viewed infant pain as a case of simple stimuli and response, their experiments emphasized exact control of the experimental situation. This in turn resulted in the introduction of electric shock to infant pain experiments (with electric shock the confound of pressure from a pricking needle could be eliminated). Experiments by Mandel and Irene Sherman, who were associated with Northwestern University, University of Chicago, and several Chicago hospitals, demonstrate this trend. Their 1936 ‘‘Infant Behavior’’ summarizes the status of the question of infant pain: General observation has shown that some infants cry when they are pricked with a needle. Carefully controlled observation, on the other hand, demonstrated that some infants to do not respond to a needle prick even though the stimulus be repeated. . .54(p.8) Sherman et al54 believed this problem could be solved with sufficiently carefully controlled experimental conditions and pain stimulus. Thus, much of ‘‘Infant Behavior’’ focuses on the apparatus used to administer the painful stimulus and was aimed at developing a reliable algometer, or an apparatus used to produce precise painful stimuli, used to detect pain thresholds. The Shermans introduced 2 such algometers: a penlike instrument whose protective cap carefully controlled the depth of the needle prick and an electrical algometer that would deliver up to a 12.5-milliampere shock. The Shermans found that the needle algometer produced a stereotyped movement of the opposite hand that they concluded indicated a ‘‘crossed flexion reflex . . . carried out at brain stem level and mediated through the spinal fifth track and the cervical cord segments.’’54(p.31) This they took as evidence that the infant ought to be regarded as a ‘‘sub-cortical animal’’—dependent for its senses and responses to pain on the most primitive part of the brain.54(p.92) While both algometers produced infant responses, like Blanton, Sherman et al54 emphasized caution in the interpretation of results. Precise control of the stimulus, site of stimulation, and circumstances of stimulation was required ‘‘before interpretations can be made regarding the relationship between a given stimulus and the consequent response.’’54(pp.38 39) Even with their own methodological precision, Sherman et al were hesitant to draw conclusions about infant pain from their own experiment: ‘‘Perhaps the responses of infants to pain stimuli cannot be called ‘pain‘ responses, as their psychological nature is unknown.’’54(p.38) They go on to assert that because the psychological complications of
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adults are eliminated and only physical stimuli are involved for infants, their pain responses represent a more ‘‘pure’’ test of pain than tests of adults. Yet since the infant cannot speak, the interpretation of his actual pain experience remains unknowable, and ultimately irrelevant. The fact that the Shermans’ experiments were published in The Journal of Comparative Psychology and Comparative Psychology Monographs in the context of similar experiments using shock on animals and recording the resulting ‘‘reflexes’’ (eg, Liddell, James and Anderson28) suggests the dominant mechanistic view of infants. Along with animals, infants provided the perfect passive subjects for experiments that took a reductionist behaviorist perspective, for researchers searching for reflexes rather than consciousness. In this context the Shermans’ interpretation of their results as evidence for the decorticate infant went unchallenged, clearing the way for routine experimentation on infant pain thresholds, with no special ethical justification required.
Emphasis on Brain Development The Shermans’ introduction of the decorticate infant was a sign of things to come; as behaviorism lost its monopoly on psychological thinking, brain maturation became the dominant focus of infant pain research. The researcher who pioneered this emphasis was psychologist Myrtle McGraw, best known for her longitudinal study of twins Jimmy and Johnny, who received differential physical stimulation, leading, most famously, to Johnny learning to roller skate at 13 months old.31 What is less well known is that McGraw also tested Jimmy and Johnny for their pain reactions during their regular examinations, ‘‘stimulating the infants with a blunted pin-point’’ in their leg, forearm, trunk, and cheek.31(p.111) McGraw commented ‘‘Many parunates and infants just a few hours old manifest no overt response to cutaneous irritation of the type just described. So far as can be determined by observation, many newborn babies are insensible to peripheral irritation of this sort.’’31(p.111) However, McGraw acknowledged that by the time infants were about a week old, they showed ‘‘decided irritability to such stimulation’’ and might exhibit a reflex withdrawal of the stimulated member.31(p.111) McGraw saw development as the result of interaction between brain growth and behavior and therefore rather than looking for a pain threshold, she was looking for evidence of maturation. In later research she would interpret the changing responses of infants to pinprick as evidence of neural maturation. ‘‘Neural Maturation as Exemplified in the Changing Reactions of the Infant to Pin Prick’’32,33 records a staggering number of observations: 75 infants were poked with a safety pin at repeated intervals from birth to 4 years old, resulting in a total of 2,008 observations. Based on this data McGraw concludes: In view of these findings it is reasonable to assume that the sensori-motor reactions of the newborn infant do not extend appreciably beyond the level of
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the thalamus. Observations on the overt behavior of the infant support this assumption.32(p.39) It was McGraw’s conclusions about infant brain development that would be particularly important for later infant pain research. Based on histological studies indicating limited function of infant cerebral cortex, McGraw interpreted her data to mean that newborn sensorimotor reactions took place at a subcortical level, resulting in ‘‘a period of diminished neuromuscular activity, and possibly diminished sensory experience.’’32(p.40) McGraw’s work would be frequently cited by later infant pain writers, and her tentative conclusions about brain development used as statements of fact. But as popular as McGraw’s findings became, there was a dissenting view. The eminent German pediatrician Albrecht Peiper had also turned his attention to the question of infant pain in 2 publications in the 1920s38,39 that he later summarized in his book Cerebral Function in Infancy and Childhood.40 In 1 of these papers Peiper describes how he pricked newborns on the heel, finding that a needle prick between 2 to 4 mm deep resulted in a clear reaction of movement and screaming.39 Although premature babies had a slower response time, he emphasized that they did eventually respond, and there was a wide range of reactions possible, including ‘‘protective skin reflexes,’’ movements related to the irritated site. Peiper did not hesitate to challenge the findings of previous researchers, starting with Genzmer: ‘‘The reaction time cited by Genzmer is too long.’’40(p.30) Based on his investigations Peiper staunchly asserted the existence of infant pain: ‘‘Actually, there is no normal or immature newborn who could not be easily aroused by pinprick. I could elicit by pinprick twitching in the facialis area of a human fetus 23 cm long.’’40(p.30) In fact, Peiper says, he would interpret a lack of reaction as a sign of pathology or illness on the part of the child—healthy as well as premature infants always have a measurable sign of pain.37 In accounting for the difference between his own findings and those of others, Peiper emphasizes individual differences as well as the potentially wide variation in the infant’s state that affects its ‘‘readiness to react.’’40 Sleep, hunger, poor health, feeding, and distraction could incline infants to not respond to pain stimulus. Although Peiper, whose specialty was neurology, acknowledged that the infant’s brain was still developing, he asserted that ‘‘Protective skin reflexes do not depend on functioning cerebral hemispheres,’’40(p.33) arguing that pain responses relied on the brainstem. Based on his reading of the clear evidence for infant pain Peiper ends his discussion of infant pain in Cerebral Function in Infancy and Childhood with the ethical implications of his findings: The adult reserves for himself the right to be protected against pain during surgical interventions. Because of their sensitivity to pain, newborns and infants have the same right but, contrary to the adult, they are defenseless when their rights are violated. Surgeons who declare infants to be insensitive to pain and—as I have
The Infancy of Infant Pain witnessed—perform operations for pylorospasm without anesthesia, do so contrary to everyday experience and scientific knowledge.40(p.33) In this unprecedented rhetorical broadside Peiper clearly targets not only the medical establishment but by extension the researchers who had closed their eyes to obvious evidence of infant pain. Sadly his ethical challenge would go largely unheeded.
Post-1950 Research and Practice The influence of the infant pain research from the first half of the 20th century on the research in the second half was facilitated by Karl Pratt’s 1954 chapter on the neonate. Genzmer, Preyer, the Shermans, and early Peiper are all cited in Pratt’s literature review of infant response to ‘‘noxious (pain) stimuli.’’44(p.221) Based on this review Pratt concluded that although neonatal sensitivity to pain had been demonstrated there was disagreement ‘‘regarding the degree of pain sensitivity in the just-born infant as compared with that found at later age periods.’’44(p.223) In this period infant pain researchers were motivated by using pain as a diagnostic tool. For example, a pair of experiments by Frances Graham et al19,20 tested the pain sensitivity of traumatized infants, as compared to normal infants using electric shock. They found that traumatized infants showed impaired functioning, including pain responses. According to Graham, 1 reason they picked pain as a measure of trauma was their assumption that ‘‘sensitivity to pain has not reached a maximum at birth.’’19(p.4) The post-1950 shift away from investigating infant pain for its own sake and toward researching it as a means for diagnosis portended decreasing interest in the subject. The only experimental test of infant pain conducted between 1960 and 1980 we could find was the 1974 ‘‘The Normal Neonatal Response to Pinprick,’’49 which reported that the normal response for infants given a series of pricks in the knee area is ‘‘movement of the upper and lower limbs, usually accompanied by grimace and/or cry.’’49(p.433) Interestingly, Rich, Marshall, and Volpe appear to be almost entirely ignorant of the preceding tradition of research, citing only Peiper.40 The decreasing interest in infant pain may have indicated the matter was considered settled—there was enough scientific skepticism of infant pain for medical authorities to feel justified in withholding anesthesia from their youngest patients. Supporting this theory is Pabis et al37 and Chamberlain’s9 assertion that McGraw’s work was the most influential for medical authorities post-1950. No doubt the popularity of her work was due in part to the extensive nature of her investigations and the relatively recent date of the research, but another important factor seems to have been the nature of her findings and the ease with which it could be made to agree with standard medical practice. For example, in 1968 Swafford and Allen cited McGraw to support their conclusion that ‘‘Pediatric patients seldom need medication for the relief of pain after general
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surgery. They tolerate discomfort well.’’ Lida Swafford and David Allen were professors of anesthesia at Northwestern University School of Medicine and Associate Attending and Chief of Anesthesia at Children’s Memorial Hospital, Chicago, and reported that in their pediatric intensive care unit, out of 180 patients only 26 received any form of postsurgical narcotics.60 As justification, Swafford and Allen invoked McGraw’s findings that infants do not respond to pain stimuli: Although variation exists it seems reasonable to believe that the infant’s perception of pain is determined by the degree of cortical development. The response and cortical activity of the baby may be compared to that of a patient receiving thiopental anesthesia. A baby with an undeveloped cortex and a deeply anaesthetized patient may both lack cortical activity, and both are unable to feel pain. A baby with partial cortical development and a patient under light thiopental anesthesia will show mass, undirected responses, still without ‘consciousness’ of pain. When a baby cries on stimulation and the patient first complains, the pain may be felt but not remembered, whereas complete cortical development of the baby and full awakening are necessary for normal consciousness and remembrance of pain.60(p.132) Swafford and Allen’s paper shows how earlier studies of infant pain affected later medical practice in creating an abiding skepticism regarding infants’ perception of pain. Despite acknowledging that ‘‘from their first injection in the delivery room, active full-term infants react to the stimulation of needle punctures’’ Swafford and Allen still conclude ‘‘The age at which pain is first perceived is unknown.’’60(p.131) With this sort of determined skepticism it appears that there is little that infants could do to demonstrate their perception of pain. A similar perspective is taken in Stephen, Ahlgren, and Bennett’s Elements of Pediatric Anesthesia,57 an anesthesia textbook published in 1970. In their discussion of the central nervous system, the authors state that infants under 1 month appear to be less sensitive to pain and ‘‘There is now anatomic evidence to reinforce this clinical impression. At birth the infant has a well-developed brain up to the midbrain level but not including the higher cortical regions.’’57(p.21) While they do not cite any source for this statement, it coincides with McGraw’s claims about pain in relation to brain development. Although the authors acknowledge that young infants do respond to painful stimuli, they persist in viewing these responses as mere reflexes: Whether pain can be perceived in the first months of life is indeed a moot point. However, there is no doubt that patients react, often in a nonspecific manner, to external stimuli, and that these repeated reactions prevent surgery from being accomplished. Perhaps what one is really accomplishing in this age group by the administration of anesthesia is a reduction of the reflex response to stimuli.57(p.21)
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This view of infant pain response as a reflex revealing nothing about infant experience of pain, and simply a disruption of surgery, must have affected anesthesia decisions. Even though Stephen, Ahlgren and Bennett condemn the ‘‘willy-nilly’’ use of muscle-relaxant drugs ‘‘to cover up inadequate anesthesia,’’57(p.13) it is not unreasonable to assume that student anesthesiologists would interpret their dismissal of infant pain as implicit permission not to anesthetize infants. This seems particularly likely given the many serious problems in anesthetizing young infants that the textbook covers. Writing in 1987, in their article ‘‘Do premature infants require anesthesia for surgery?’’ Berry and Gregory review the numerous challenges involved in anesthetizing premature infants in the early 1970s and conclude that given these risks ‘‘it is understandable why some anesthesiologists chose to ‘anesthetize’ premature infants with muscle relaxants.’’5(p.292) Swafford and Allen’s use of McGraw’s research illustrates how influential her research was: they adopt her experimental findings and explanations regarding cortical development with little criticism and even interpret her work in ways that move beyond her conclusions. Similarly, Elements of Pediatric Anesthesia’s embrace of the McGraw-influenced notions of cortical development shows how her ideas gained enough legitimacy to be treated as facts, with no citation necessary. The identity of the authors of both publications as respected anesthesiologists and professors of anesthesia demonstrates how early infant pain research in general, and McGraw’s work in particular, came to have a real impact on medical practice. The popularity of McGraw’s research is in striking contrast to the neglect of Peiper’s work, which raises the question of why McGraw’s findings came to predominate over Peiper’s. One explanation is that Peiper’s German identity caused his work to be less well known, which is plausible given that only his 1961 book Cerebral Function in Infancy and Childhood was translated into English. Yet this alone cannot explain Swafford and Allen’s preference for McGraw, because they cite Peiper’s Cerebral Function, surprisingly including the whole of his most passionate passage decrying infant surgery without anesthesia. As the inclusion of Peiper’s quote demonstrates, Swafford and Allen’s paper is a strange mix of infant pain denial and acceptance. Although they are strongly skeptical of infant and childhood pain postsurgery, they do evince some uncertainty about the necessity of anesthesia for infant surgery, based on the different rates of brain myelinzation and comment on the ‘‘restraint required for the alert newborn infant undergoing simple operative procedures without general anesthesia.’’60(p.134) Yet their article concludes: ‘‘Infants and children below the age of 10 rarely require narcotics. They are very amenable to suggestion, want to get well and are trusting.’’60(p.135) Instead of adopting the presumption of infant pain championed by Peiper, Swafford and Allen, apparently concerned about drug addiction and respiratory depression, advocate using suggestion
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and distraction rather than analgesics to deal with children’s complaints. Swafford and Allen’s response to the evidence of earlier infant pain research appears to be representative of midcentury medical opinion. Adopting the skepticism of McGraw and her predecessors, medical authorities largely ignored inconvenient contradictory evidence. Although these authorities, like Swafford and Allen, may have acknowledged that the existence of infant pain was ‘‘open to question,’’ in practice they acted as though it was settled. It was not until the 1980s that these questions were reopened, motivated by humanitarian concerns and a new certainty that infant pain could be detected and systematically studied. New ethical concerns and mandates such as the Declaration of Helsinki in 1974 led to the embrace of infant pain research using necessary medical procedures only.35,36 Yet the profound and long-lasting results of experimental skepticism can be clearly seen in the underprescription of anesthesia and analgesia for infant surgery that lasted into the 1980s. As late as 1988, well into the renaissance of infant pain research, when 80% of pediatric anesthetists surveyed believed that neonates experienced pain, the same survey found a widespread reluctance to prescribe analgesics to infants.47 Work since the late 1980s has generally debunked most myths related to infant pain, such as that infants and toddlers show no evidence of memory for pain,65 that conducting painful procedures in infancy without proper analgesic/anesthetic does not cause anticipatory anxiety and sensitization,61,62 and that there are no reliable ways of assessing59 nor safe ways of managing infant pain.4,43 Infant pain skepticism is in stark contrast to the information put forth by pain scientists and influential health organizations22,24 who have clearly articulated not only that infants, despite being preverbal, are capable of feeling pain, but that evidence suggests that immature inhibitory capacities may make the pain experience more intense for infants. Yet there is recent evidence that pediatric patients continue to receive inadequate analgesics postsurgery and during painful medical procedures,50,58 and some researchers continue to question infants’ capacity for pain.13-15 For example, a recent publication, ‘‘A Shift in Sensory Processing that Enables the Developing Human Brain to Discriminate Touch from Pain,’’ puts a modern twist on the historical denial of infant pain, using electroencephalogram evidence to argue that premature infants are not able to distinguish touch from pain until approximately 35 weeks.17 Rather than suggest that the sensitive state of the premature infant could render non-noxious touch noxious, the discussion clearly implied the inverse: that noxious touch was perceived as non-noxious. This choice of interpretation seems a clear legacy of infant pain research dating back to the mid-19th century. To sum up the basic causal trajectory of this research, skepticism about pain, which had initially only been the result of experimental caution and
limitations, eventually solidified into scientific fact and common knowledge. A few important studies (ie, Genzmer, McGraw) influenced later ones, and even though many of these studies were inconclusive, since skepticism about infant pain was more in tune with the widespread mechanistic views of the infant, they were eventually interpreted into scientific consensus.
Discussion An ultimate cause of the denial of infant pain is difficult to deduce from this complicated mixture of historical factors. However, taking a broad historical perspective, one must consider why skepticism about infant pain emerged only in the modern era. Unruh64 and Pabis, Kowalczyk, and Kulik37 have shown that infant pain was widely acknowledged by ancient and medieval physicians and philosophers, as evidenced by the abundant medical advice and pain-relieving practices, including opiates for infants. In 1656, Franz Wiertz wrote: If the 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 a tender new 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?64(p.248) The contrast with the subsequent research of the 19th and early 20th centuries is striking. In this light, the sad history of infant pain research reads as an indictment of the modern scientific perspective; the transformation of the infant into a mechanistic scientific object resulted in medical insensitivity and experimental bias. Although certain aspects of this history are perversions of scientific method or temptations particular to a certain time (ie, the desire to appear objective and scientific when science’s credentials were less well established), others (ie, the exclusively mechanistic view of the infant) appear equally relevant in any era. One lesson that seems particularly applicable to the modern researcher is that a strict adherence to accepted research methodology can actually cloak bias, rather than prevent it. For example, unthinking adherence to null hypothesis testing, with its requirement that the scientist disprove the assertion that nothing has happened as a result of the experimentation, undoubtedly contributed to infant pain skepticism. Faced with a research subject who in response to painful experimentation could not express pain like a verbal adult (eg, latency to response, specificity of response), scientists, bound by their chosen methodology, could not reject their null hypothesis. A number of established scientists zealously guarded their methodological purity, yet remained blind to the possibility that their own hypotheses were adultbiased, their mechanistic view of the infant prejudiced toward pain skepticism.
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As we continue to explore infant pain, the field’s history should serve as a powerful reminder to pay attention to infants’ pain experience and beware the limitations of the scientific method in the pursuit of science.
Acknowledgment
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