Early Neonatal Pain-A Review of Clinical and Experimental Implications on Painful Conditions Later in Life

Morika D Williams, B Duncan X Lascelles, Morika D Williams, B Duncan X Lascelles

Abstract

Modern health care has brought our society innumerable benefits but has also introduced the experience of pain very early in life. For example, it is now routine care for newborns to receive various injections or have blood drawn within 24 h of life. For infants who are sick or premature, the pain experiences inherent in the required medical care are frequent and often severe, with neonates requiring intensive care admission encountering approximately fourteen painful procedures daily in the hospital. Given that much of the world has seen a steady increase in preterm births for the last several decades, an ever-growing number of babies experience multiple painful events before even leaving the hospital. These noxious events occur during a critical period of neurodevelopment when the nervous system is very vulnerable due to immaturity and neuroplasticity. Here, we provide a narrative review of the literature pertaining to the idea that early life pain has significant long-term effects on neurosensory, cognition, behavior, pain processing, and health outcomes that persist into childhood and even adulthood. We refer to clinical and pre-clinical studies investigating how early life pain impacts acute pain later in life, focusing on animal model correlates that have been used to better understand this relationship. Current knowledge around the proposed underlying mechanisms responsible for the long-lasting consequences of neonatal pain, its neurobiological and behavioral effects, and its influence on later pain states are discussed. We conclude by highlighting that another important consequence of early life pain may be the impact it has on later chronic pain states-an area of research that has received little attention.

Keywords: animal models; chronic pain; consequences; early life; mechanisms; neonatal pain; neurobiology.

Copyright © 2020 Williams and Lascelles.

References

    1. Howson CP, Kinney MV, Lawn JE. (editors). Born too Soon: the Global Action Report on Preterm Birth. Geneva: World Health Organization; (2012). 126 p.
    1. Dimes M PMNCH Children St WHO Born Too Soon: The Global Action Report on Preterm Birth. Geneva: World Health Organization; (2012).
    1. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, et al. . National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. (2012) 379:2162–72. 10.1016/S0140-6736(12)60820-4
    1. Slattery MM, Morrison JJ. Preterm delivery. Lancet. (2002) 360:1489–97. 10.1016/S0140-6736(02)11476-0
    1. Behrman R, Butler A. Institute of Medicine (US) Committee on Understanding Premature Birth and Assuring Healthy Outcomes. Preterm Birth: Causes, Consequences, and Prevention. Washington, DC: National Academies Press; (2007).
    1. March of Dimes Perinatal Data Center: Special Care Nursery Admissions White Plains, NY: National Perinatal Information System/Quality Analytic Services (2011).
    1. Lee HC, Bennett MV, Schulman J, Gould JB. Accounting for variation in length of NICU stay for extremely low birth weight infants. J Perinatol. (2013) 33:872–6. 10.1038/jp.2013.92
    1. Carbajal R, Rousset A, Danan C, Coquery S, Nolent P, Ducrocq S, et al. . Epidemiology and treatment of painful procedures in neonates in intensive care units. JAMA. (2008) 300:60–70. 10.1001/jama.300.1.60
    1. Hall RW, Anand KJ. Pain management in newborns. Clin Perinatol. (2014) 41:895–924. 10.1016/j.clp.2014.08.010
    1. Bower AJ. Plasticity in the adult and neonatal central nervous system. Br J Neurosurg. (1990) 4:253–64. 10.3109/02688699008992734
    1. Ochiai M, Kinjo T, Takahata Y, Iwayama M, Abe T, Ihara K, et al. . Survival and neurodevelopmental outcome of preterm infants born at 22–24 weeks of gestational age. Neonatology. (2014) 105:79–84. 10.1159/000355818
    1. Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. (2008) 371:261–9. 10.1016/S0140-6736(08)60136-1
    1. Brummelte S, Grunau RE, Chau V, Poskitt KJ, Brant R, Vinall J, et al. . Procedural pain and brain development in premature newborns. Ann Neurol. (2012) 71:385–96. 10.1002/ana.22267
    1. Duerden EG, Grunau RE, Guo T, Foong J, Pearson A, Au-Young S, et al. . Early procedural pain is associated with regionally-specific alterations in thalamic development in preterm neonates. J Neurosci. (2018) 38:878–86. 10.1523/JNEUROSCI.0867-17.2017
    1. Grunau RE. Neonatal pain in very preterm infants: long-term effects on brain, neurodevelopment and pain reactivity. Rambam Maimonides Med J. (2013) 4:e0025. 10.5041/RMMJ.10132
    1. Beggs S, Currie G, Salter MW, Fitzgerald M, Walker SM. Priming of adult pain responses by neonatal pain experience: maintenance by central neuroimmune activity. Brain. (2012) 135:404–17. 10.1093/brain/awr288
    1. Walker SM, Melbourne A, O'Reilly H, Beckmann J, Eaton-Rosen Z, Ourselin S, et al. . Somatosensory function and pain in extremely preterm young adults from the UK EPICure cohort: sex-dependent differences and impact of neonatal surgery. Br J Anaesth. (2018) 121:623–35. 10.1016/j.bja.2018.03.035
    1. Grunau RE, Holsti L, Peters JW. Long-term consequences of pain in human neonates. Semin Fetal Neonatal Med. (2006) 11:268–75. 10.1016/j.siny.2006.02.007
    1. Johnston C, Barrington KJ, Taddio A, Carbajal R, Filion F. Pain in Canadian NICUs: have we improved over the past 12 years? Clin J Pain. (2011) 27:225–32. 10.1097/AJP.0b013e3181fe14cf
    1. Simons SH, van Dijk M, Anand KS, Roofthooft D, van Lingen RA, Tibboel D. Do we still hurt newborn babies? A prospective study of procedural pain and analgesia in neonates. Arch Pediatr Adolesc Med. (2003) 157:1058–64. 10.1001/archpedi.157.11.1058
    1. Johnston CC, Collinge JM, Henderson SJ, Anand KJ. A cross-sectional survey of pain and pharmacological analgesia in Canadian neonatal intensive care units. Clin J Pain. (1997) 13:308–12. 10.1097/00002508-199712000-00008
    1. Anand KJ, International Evidence-Based Group for Neonatal P. Consensus statement for the prevention and management of pain in the newborn. Arch Pediatr Adolesc Med. (2001) 155:173–80. 10.1001/archpedi.155.2.173
    1. Farmer D, Sitkin N, Lofberg K, Donkor P, Ozgediz D. Surgical interventions for congenital anomalies. In Debas HT, Donkor P, Gawande A, Jamison DT, Kruk ME, Mock CN. editors. Essential Surgery: Disease Control Priorities. The International Bank for Reconstruction and Development. Washington, DC: The World Bank; (2015). p. 129–49. 10.1596/978-1-4648-0346-8_ch8
    1. Mitul AR, Sarin YK. Minimal access surgery in neonates. J Neonatal Surg. (2017) 6:59. 10.21699/jns.v6i3.614
    1. Courtois E, Droutman S, Magny JF, Merchaoui Z, Durrmeyer X, Roussel C, et al. . Epidemiology and neonatal pain management of heelsticks in intensive care units: EPIPPAIN 2, a prospective observational study. Int J Nurs Stud. (2016) 59:79–88. 10.1016/j.ijnurstu.2016.03.014
    1. Shah VS, Ohlsson A. Venepuncture versus heel lance for blood sampling in term neonates. Cochrane Database Syst Rev. (2011) CD001452. 10.1002/14651858.CD001452.pub4
    1. Ma P, Liu J, Xi X, Du B, Yuan X, Lin H, et al. . Practice of sedation and the perception of discomfort during mechanical ventilation in Chinese intensive care units. J Crit Care. (2010) 25:451–7. 10.1016/j.jcrc.2009.11.006
    1. Friesen RH, Honda AT, Thieme RE. Changes in anterior fontanel pressure in preterm neonates during tracheal intubation. Anesth Analg. (1987) 66:874–8. 10.1213/00000539-198709000-00012
    1. Gitto E, Aversa S, Salpietro CD, Barberi I, Arrigo T, Trimarchi G, et al. . Pain in neonatal intensive care: role of melatonin as an analgesic antioxidant. J Pineal Res. (2012) 52:291–5. 10.1111/j.1600-079X.2011.00941.x
    1. Krishnan L. Pain relief in neonates. J Neonatal Surg. (2013) 2:19. 10.21699/jns.v2i2.59
    1. Qiu J, Zhao L, Yang Y, Zhang JH, Feng Y, Cheng R. Effects of fentanyl for pain control and neuroprotection in very preterm newborns on mechanical ventilation. J Matern Fetal Neonatal Med. (2019) 32:3734–40. 10.1080/14767058.2018.1471593
    1. Rozé JC, Denizot S, Carbajal R, Ancel PY, Kaminski M, Arnaud C, et al. . Prolonged sedation and/or analgesia and 5-year neurodevelopment outcome in very preterm infants: results from the EPIPAGE cohort. Arch Pediatr Adolesc Med. (2008) 162:728–33. 10.1001/archpedi.162.8.728
    1. Zimmerman KO, Smith PB, Benjamin DK, Laughon M, Clark R, Traube C, et al. . Sedation, analgesia, and paralysis during mechanical ventilation of premature infants. J Pediatr. (2017) 180:99–104.e1. 10.1016/j.jpeds.2016.07.001
    1. Anand KJ, Aranda JV, Berde CB, Buckman S, Capparelli EV, Carlo W, et al. . Summary proceedings from the neonatal pain-control group. Pediatrics. (2006) 117:S9–22. 10.1542/peds.2005-0620C
    1. Doyle LW, Cheong JL, Burnett A, Roberts G, Lee KJ, Anderson PJ, et al. . Biological and social influences on outcomes of extreme-preterm/low-birth weight adolescents. Pediatrics. (2015) 136:e1513–20. 10.1542/peds.2015-2006
    1. Fitzgerald M, Millard C, McIntosh N. Cutaneous hypersensitivity following peripheral tissue damage in newborn infants and its reversal with topical anaesthesia. Pain. (1989) 39:31–6. 10.1016/0304-3959(89)90172-3
    1. Knaepen L, Patijn J, van Kleef M, Mulder M, Tibboel D, Joosten EAJ. Neonatal repetitive needle pricking: Plasticity of the spinal nociceptive circuit and extended postoperative pain in later life. Dev Neurobiol. (2013) 73:85–97. 10.1002/dneu.22047
    1. Woolf CJ. Central sensitization: implications for the diagnosis and treatment of pain. Pain. (2011) 152:S2–15. 10.1016/j.pain.2010.09.030
    1. Woolf CJ, Thompson SW, King AE. Prolonged primary afferent induced alterations in dorsal horn neurones, an intracellular analysis in vivo and in vitro. J Physiol (Paris). (1988) 83:255–66.
    1. Bellieni CV, Johnston CC. Analgesia, nil or placebo to babies, in trials that test new analgesic treatments for procedural pain. Acta Paediatr. (2016) 105:129–36. 10.1111/apa.13210
    1. Hatfield LA. Neonatal pain: what's age got to do with it? Surg Neurol Int. (2014) 5:S479–89. 10.4103/2152-7806.144630
    1. Roofthooft DW, Simons SH, Anand KJ, Tibboel D, van Dijk M. Eight years later, are we still hurting newborn infants? Neonatology. (2014) 105:218–26. 10.1159/000357207
    1. Johnston CC, Stevens BJ. Experience in a neonatal intensive care unit affects pain response. Pediatrics. (1996) 98:925–30.
    1. Kaur H, Negi V, Sharma M, Mahajan G. Study of pain response in neonates during venipuncture with a view to analyse utility of topical anaesthetic agent for alleviating pain. Med J Armed Forces India. (2019) 75:140–5. 10.1016/j.mjafi.2017.12.009
    1. Maitre NL, Key AP, Chorna OD, Slaughter JC, Matusz PJ, Wallace MT, et al. . The dual nature of early-life experience on somatosensory processing in the human infant brain. Curr Biol. (2017) 27:1048–54. 10.1016/j.cub.2017.02.036
    1. Burnett AC, Cheong JLY, Doyle LW. Biological and social influences on the neurodevelopmental outcomes of preterm infants. Clin Perinatol. (2018) 45:485–500. 10.1016/j.clp.2018.05.005
    1. Hunt RW, Hickey LM, Burnett AC, Anderson PJ, Cheong JLY, Doyle LW, et al. . Early surgery and neurodevelopmental outcomes of children born extremely preterm. Arch Dis Child Fetal Neonatal Ed. (2018) 103:F227–32. 10.1136/archdischild-2017-313161
    1. Chau CMY, Ranger M, Bichin M, Park MTM, Amaral RSC, Chakravarty M, et al. . Hippocampus, amygdala, and thalamus volumes in very preterm children at 8 years: neonatal pain and genetic variation. Front Behav Neurosci. (2019) 13:51. 10.3389/fnbeh.2019.00051
    1. Abernethy LJ, Cooke RW, Foulder-Hughes L. Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm. Pediatr Res. (2004) 55:884–93. 10.1203/01.PDR.0000117843.21534.49
    1. Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, et al. . Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain. (2001) 124:60–6. 10.1093/brain/124.1.60
    1. Ranger M, Zwicker JG, Chau CM, Park MT, Chakravarthy MM, Poskitt K, et al. . Neonatal pain and infection relate to smaller cerebellum in very preterm children at school age. J Pediatr. (2015) 167:292–8.e1. 10.1016/j.jpeds.2015.04.055
    1. Jaekel J, Eryigit-Madzwamuse S, Wolke D. Preterm Toddlers' inhibitory control abilities predict attention regulation and academic achievement at age 8 years. J Pediatr. (2016) 169:87–92.e1. 10.1016/j.jpeds.2015.10.029
    1. Linsell L, Johnson S, Wolke D, O'Reilly H, Morris JK, Kurinczuk JJ, et al. . Cognitive trajectories from infancy to early adulthood following birth before 26 weeks of gestation: a prospective, population-based cohort study. Arch Dis Child. (2018) 103:363–70. 10.1136/archdischild-2017-313414
    1. Olsen A, Dennis EL, Evensen KAI, Husby Hollund IM, Løhaugen GCC, Thompson PM, et al. . Preterm birth leads to hyper-reactive cognitive control processing and poor white matter organization in adulthood. Neuroimage. (2018) 167:419–28. 10.1016/j.neuroimage.2017.11.055
    1. Skiöld B, Alexandrou G, Padilla N, Blennow M, Vollmer B, Adén U. Sex differences in outcome and associations with neonatal brain morphology in extremely preterm children. J Pediatr. (2014) 164:1012–8. 10.1016/j.jpeds.2013.12.051
    1. Schneider J, Duerden EG, Guo T, Ng K, Hagmann P, Bickle Graz M, et al. . Procedural pain and oral glucose in preterm neonates: brain development and sex-specific effects. Pain. (2018) 159:515–25. 10.1097/j.pain.0000000000001123
    1. Anand KJS, Coskun V, Thrivikraman KV, Nemeroff CB, Plotksy PM. Long-term behavioral effects of repetitive pain in neonatal rat pups. Physiol Behav. (1999) 66:627–37. 10.1016/S0031-9384(98)00338-2
    1. Dührsen L, Simons SHP, Dzietko M, Genz K, Bendix I, Boos V, et al. . Effects of repetitive exposure to pain and morphine treatment on the neonatal rat brain. Neonatology. (2013) 103:35–43. 10.1159/000341769
    1. Nuseir KQ, Alzoubi KH, Alhusban A, Bawaane A, Al-Azzani M, Khabour OF. Sucrose and naltrexone prevent increased pain sensitivity and impaired long-term memory induced by repetitive neonatal noxious stimulation: Role of BDNF and beta-endorphin. Physiol Behav. (2017) 179:213–9. 10.1016/j.physbeh.2017.06.015
    1. Nuseir KQ, Alzoubi KH, Alabwaini J, Khabour OF, Kassab MI. Sucrose-induced analgesia during early life modulates adulthood learning and memory formation. Physiol Behav. (2015) 145:84–90. 10.1016/j.physbeh.2015.04.002
    1. Henderson YO, Victoria NC, Inoue K, Murphy AZ, Parent MB. Early life inflammatory pain induces long-lasting deficits in hippocampal-dependent spatial memory in male and female rats. Neurobiol Learn Mem. (2015) 118:30–41. 10.1016/j.nlm.2014.10.010
    1. Ranger M, Tremblay S, Chau CMY, Holsti L, Grunau RE, Goldowitz D. Adverse behavioral changes in adult mice following neonatal repeated exposure to pain and sucrose. Front Psychol. (2018) 9:2394. 10.3389/fpsyg.2018.02394
    1. Ranger M, Grunau RE. Early repetitive pain in preterm infants in relation to the developing brain. Pain Manag. (2014) 4:57–67. 10.2217/pmt.13.61
    1. Hall RW, Anand KJS. Short- and long-term impact of neonatal pain and stress. Neoreviews. (2005) 6:e69–75. 10.1542/neo.6-2-e69
    1. Bhutta AT, Rovnaghi C, Simpson PM, Gossett JM, Scalzo FM, Anand KJ. Interactions of inflammatory pain and morphine in infant rats: long-term behavioral effects. Physiol Behav. (2001) 73:51–8. 10.1016/S0031-9384(01)00432-2
    1. Butkevich IP, Mikhailenko VA, Vershinina EA, Aloisi AM, Barr GA. Long-term effects of chronic buspirone during adolescence reduce the adverse influences of neonatal inflammatory pain and stress on adaptive behavior in adult male rats. Front Behav Neurosci. (2017) 11:11. 10.3389/fnbeh.2017.00011
    1. Burke NN, Finn DP, McGuire BE, Roche M. Psychological stress in early life as a predisposing factor for the development of chronic pain: clinical and preclinical evidence and neurobiological mechanisms. J Neurosci Res. (2017) 95:1257–70. 10.1002/jnr.23802
    1. Burt KB, Obradović J, Long JD, Masten AS. The interplay of social competence and psychopathology over 20 years: testing transactional and cascade models. Child Dev. (2008) 79:359–74. 10.1111/j.1467-8624.2007.01130.x
    1. Bauminger N, Solomon M, Rogers SJ. Externalizing and internalizing behaviors in ASD. Autism Res. (2010) 3:101–12. 10.1002/aur.131
    1. Vinall J, Miller SP, Synnes AR, Grunau RE. Parent behaviors moderate the relationship between neonatal pain and internalizing behaviors at 18 months corrected age in children born very prematurely. Pain. (2013) 154:1831–9. 10.1016/j.pain.2013.05.050
    1. Loe IM, Lee ES, Luna B, Feldman HM. Behavior problems of 9–16 year old preterm children: biological, sociodemographic, and intellectual contributions. Early Hum Dev. (2011) 87:247–52. 10.1016/j.earlhumdev.2011.01.023
    1. Schmidt LA, Miskovic V, Boyle M, Saigal S. Frontal electroencephalogram asymmetry, salivary cortisol, and internalizing behavior problems in young adults who were born at extremely low birth weight. Child Dev. (2010) 81:183–99. 10.1111/j.1467-8624.2009.01388.x
    1. Talge NM, Holzman C, Wang J, Lucia V, Gardiner J, Breslau N. Late-preterm birth and its association with cognitive and socioemotional outcomes at 6 years of age. Pediatrics. (2010) 126:1124–31. 10.1542/peds.2010-1536
    1. Walker SM, O'Reilly H, Beckmann J, Marlow N, Group ES. Conditioned pain modulation identifies altered sensitivity in extremely preterm young adult males and females. Br J Anaesth. (2018) 121:636–46. 10.1016/j.bja.2018.05.066
    1. Hussong AM, Jones DJ, Stein GL, Baucom DH, Boeding S. An internalizing pathway to alcohol use and disorder. Psychol Addict Behav. (2011) 25:390–404. 10.1037/a0024519
    1. Winters KC, Stinchfield RD, Latimer WW, Stone A. Internalizing and externalizing behaviors and their association with the treatment of adolescents with substance use disorder. J Subst Abuse Treat. (2008) 35:269–78. 10.1016/j.jsat.2007.11.002
    1. Pearl RL, White MA, Grilo CM. Weight bias internalization, depression, and self-reported health among overweight binge eating disorder patients. Obesity (Silver Spring). (2014) 22:E142–8. 10.1002/oby.20617
    1. Relland LM, Gehred A, Maitre NL. Behavioral and physiological signs for pain assessment in preterm and term neonates during a nociception-specific response: a systematic review. Pediatr Neurol. (2019) 90:13–23. 10.1016/j.pediatrneurol.2018.10.001
    1. Green G, Hartley C, Hoskin A, Duff E, Shriver A, Wilkinson D, et al. . Behavioural discrimination of noxious stimuli in infants is dependent on brain maturation. Pain. (2019) 160:493–500. 10.1097/j.pain.0000000000001425
    1. Donia AE-S, Tolba OA. Effect of early procedural pain experience on subsequent pain responses among premature infants. Egypt Pediatr Assoc Gazette. (2016) 64:74–80. 10.1016/j.epag.2016.03.002
    1. Evans JC, McCartney EM, Lawhon G, Galloway J. Longitudinal comparison of preterm pain responses to repeated heelsticks. Pediatr Nurs. (2005) 31:216–21.
    1. Grunau RE, Oberlander TF, Whitfield MF, Fitzgerald C, Lee SK. Demographic and therapeutic determinants of pain reactivity in very low birth weight neonates at 32 weeks' postconceptional age. Pediatrics. (2001) 107:105–12. 10.1542/peds.107.1.105
    1. Slater R, Cantarella A, Franck L, Meek J, Fitzgerald M. How well do clinical pain assessment tools reflect pain in infants? PLoS Med. (2008) 5:e129. 10.1371/journal.pmed.0050129
    1. Slater R, Cantarella A, Gallella S, Worley A, Boyd S, Meek J, et al. . Cortical pain responses in human infants. J Neurosci. (2006) 26:3662–6. 10.1523/JNEUROSCI.0348-06.2006
    1. Guinsburg R, de Araújo Peres C, Branco de Almeida MF, de Cássia Xavier Balda R, Cássia Berenguel R, Tonelotto J, et al. . Differences in pain expression between male and female newborn infants. Pain. (2000) 85:127–33. 10.1016/S0304-3959(99)00258-4
    1. Gao H, Li M, Xu G, Li F, Zhou J, Zou Y, et al. . Effect of non-nutritive sucking and sucrose alone and in combination for repeated procedural pain in preterm infants: a randomized controlled trial. Int J Nurs Stud. (2018) 83:25–33. 10.1016/j.ijnurstu.2018.04.006
    1. Bartocci M, Bergqvist LL, Lagercrantz H, Anand KJ. Pain activates cortical areas in the preterm newborn brain. Pain. (2006) 122:109–17. 10.1016/j.pain.2006.01.015
    1. Schwaller F, Fitzgerald M. The consequences of pain in early life: injury-induced plasticity in developing pain pathways. Eur J Neurosci. (2014) 39:344–52. 10.1111/ejn.12414
    1. Schmelzle-Lubiecki BM, Campbell KA, Howard RH, Franck L, Fitzgerald M. Long-term consequences of early infant injury and trauma upon somatosensory processing. Eur J Pain. (2007) 11:799–809. 10.1016/j.ejpain.2006.12.009
    1. Walker SM, Franck LS, Fitzgerald M, Myles J, Stocks J, Marlow N. Long-term impact of neonatal intensive care and surgery on somatosensory perception in children born extremely preterm. Pain. (2009) 141:79–87. 10.1016/j.pain.2008.10.012
    1. Buskila D, Neumann L, Zmora E, Feldman M, Bolotin A, Press J. Pain sensitivity in prematurely born adolescents. Arch Pediatr Adolesc Med. (2003) 157:1079–82. 10.1001/archpedi.157.11.1079
    1. Taddio A, Goldbach M, Ipp M, Stevens B, Koren G. Effect of neonatal circumcision on pain responses during vaccination in boys. Lancet. (1995) 345:291–2. 10.1016/S0140-6736(95)90278-3
    1. Taddio A, Katz J, Ilersich AL, Koren G. Effect of neonatal circumcision on pain response during subsequent routine vaccination. Lancet. (1997) 349:599–603. 10.1016/S0140-6736(96)10316-0
    1. Peters JW, Schouw R, Anand KJ, van Dijk M, Duivenvoorden HJ, Tibboel D. Does neonatal surgery lead to increased pain sensitivity in later childhood? Pain. (2005) 114:444–54. 10.1016/j.pain.2005.01.014
    1. Valeri BO, Ranger M, Chau CM, Cepeda IL, Synnes A, Linhares MB, et al. . Neonatal invasive procedures predict pain intensity at school age in children born very preterm. Clin J Pain. (2016) 32:1086–93. 10.1097/AJP.0000000000000353
    1. Butkevich IP, Mikhailenko VA, Vershinina EA, Aloisi AM. Effects of neonatal pain, stress and their interrelation on pain sensitivity in later life in male rats. Chin J Physiol. (2016) 59:225–31. 10.4077/CJP.2016.BAE412
    1. Low LA, Fitzgerald M. Acute pain and a motivational pathway in adult rats: influence of early life pain experience. PLoS ONE. (2012) 7:e34316. 10.1371/journal.pone.0034316
    1. van den Hoogen NJ, Patijn J, Tibboel D, Joosten BA, Fitzgerald M, Kwok CHT. Repeated touch and needle-prick stimulation in the neonatal period increases the baseline mechanical sensitivity and postinjury hypersensitivity of adult spinal sensory neurons. Pain. (2018) 159:1166–75. 10.1097/j.pain.0000000000001201
    1. Walker SM, Beggs S, Baccei ML. Persistent changes in peripheral and spinal nociceptive processing after early tissue injury. Exp Neurol. (2016) 275:253–60. 10.1016/j.expneurol.2015.06.020
    1. Walker SM, Tochiki KK, Fitzgerald M. Hindpaw incision in early life increases the hyperalgesic response to repeat surgical injury: critical period and dependence on initial afferent activity. Pain. (2009) 147:99–106. 10.1016/j.pain.2009.08.017
    1. Walker SM. Biological and neurodevelopmental implications of neonatal pain. Clin Perinatol. (2013) 40:471–91. 10.1016/j.clp.2013.05.002
    1. Huang QT, Gao YF, Zhong M, Yu YH. Preterm birth and subsequent risk of acute childhood leukemia: a meta-analysis of observational studies. Cell Physiol Biochem. (2016) 39:1229–38. 10.1159/000447828
    1. Vinall J, Miller SP, Chau V, Brummelte S, Synnes AR, Grunau RE. Neonatal pain in relation to postnatal growth in infants born very preterm. Pain. (2012) 153:1374–81. 10.1016/j.pain.2012.02.007
    1. Ibáñez L, Ong K, Dunger DB, de Zegher F. Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab. (2006) 91:2153–8. 10.1210/jc.2005-2778
    1. Greer FR. Long-term adverse outcomes of low birth weight, increased somatic growth rates, and alterations of body composition in the premature infant: review of the evidence. J Pediatr Gastroenterol Nutr. (2007) 45:S147–51. 10.1097/01.mpg.0000302961.01170.29
    1. Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. (2000) 320:967–71. 10.1136/bmj.320.7240.967
    1. Alexeev EE, Lönnerdal B, Griffin IJ. Effects of postnatal growth restriction and subsequent catch-up growth on neurodevelopment and glucose homeostasis in rats. BMC Physiol. (2015) 15:3. 10.1186/s12899-015-0017-5
    1. Juonala M, Cheung MM, Sabin MA, Burgner D, Skilton MR, Kähönen M, et al. . Effect of birth weight on life-course blood pressure levels among children born premature: the cardiovascular risk in Young Finns Study. J Hypertens. (2015) 33:1542–8. 10.1097/HJH.0000000000000612
    1. Raju TNK, Buist AS, Blaisdell CJ, Moxey-Mims M, Saigal S. Adults born preterm: a review of general health and system-specific outcomes. Acta Paediatr. (2017) 106:1409–37. 10.1111/apa.13880
    1. DiLorenzo M, Pillai Riddell R, Holsti L. Beyond acute pain: understanding chronic pain in infancy. Children (Basel). (2016) 3:26. 10.3390/children3040026
    1. Pillai Riddell RR, Stevens BJ, McKeever P, Gibbins S, Asztalos L, Katz J, et al. . Chronic pain in hospitalized infants: health professionals' perspectives. J Pain. (2009) 10:1217–25. 10.1016/j.jpain.2009.04.013
    1. van Ganzewinkel CJ, Anand KJ, Kramer BW, Andriessen P. Chronic pain in the newborn: toward a definition. Clin J Pain. (2014) 30:970–7. 10.1097/AJP.0000000000000056
    1. Vanegas H, Schaible HG. Descending control of persistent pain: inhibitory or facilitatory? Brain Res Brain Res Rev. (2004) 46:295–309. 10.1016/j.brainresrev.2004.07.004
    1. Ossipov MH, Morimura K, Porreca F. Descending pain modulation and chronification of pain. Curr Opin Support Palliat Care. (2014) 8:143–51. 10.1097/SPC.0000000000000055
    1. Dantzer R. Neuroimmune interactions: from the brain to the immune system and vice versa. Physiol Rev. (2018) 98:477–504. 10.1152/physrev.00039.2016
    1. Grace PM, Hutchinson MR, Maier SF, Watkins LR. Pathological pain and the neuroimmune interface. Nat Rev Immunol. (2014) 14:217–31. 10.1038/nri3621
    1. Marchand F, Perretti M, McMahon SB. Role of the immune system in chronic pain. Nat Rev Neurosci. (2005) 6:521–32. 10.1038/nrn1700
    1. Ren K, Dubner R. Interactions between the immune and nervous systems in pain. Nat Med. (2010) 16:1267–76. 10.1038/nm.2234
    1. Beggs S. Long-term consequences of neonatal injury. Can J Psychiatry. (2015) 60:176–80. 10.1177/070674371506000404
    1. Beggs S, Torsney C, Drew LJ, Fitzgerald M. The postnatal reorganization of primary afferent input and dorsal horn cell receptive fields in the rat spinal cord is an activity-dependent process. Eur J Neurosci. (2002) 16:1249–58. 10.1046/j.1460-9568.2002.02185.x
    1. Fitzgerald M, Walker SM. Infant pain management: a developmental neurobiological approach. Nat Clin Pract Neurol. (2009) 5:35–50. 10.1038/ncpneuro0984
    1. Anand KJ, Scalzo FM. Can adverse neonatal experiences alter brain development and subsequent behavior? Biol Neonate. (2000) 77:69–82. 10.1159/000014197
    1. Grunau R. Early pain in preterm infants. A model of long-term effects. Clin Perinatol. (2002) 29:373–94, vii–viii. 10.1016/S0095-5108(02)00012-X
    1. Fitzgerald M. The development of nociceptive circuits. Nat Rev Neurosci. (2005) 6:507–20. 10.1038/nrn1701
    1. Rodkey EN, Pillai Riddell R. The infancy of infant pain research: the experimental origins of infant pain denial. J Pain. (2013) 14:338–50. 10.1016/j.jpain.2012.12.017
    1. Anand KJ. Clinical importance of pain and stress in preterm neonates. Biol Neonate. (1998) 73:1–9. 10.1159/000013953
    1. Fitzgerald M, Shaw A, MacIntosh N. Postnatal development of the cutaneous flexor reflex: comparative study of preterm infants and newborn rat pups. Dev Med Child Neurol. (1988) 30:520–6. 10.1111/j.1469-8749.1988.tb04779.x
    1. Goksan S, Hartley C, Emery F, Cockrill N, Poorun R, Moultrie F, et al. fMRI reveals neural activity overlap between adult and infant pain. Elife. (2015) 4:e6356 10.7554/eLife.06356
    1. Steeds CE. The anatomy and physiology of pain. Surgery (Oxford). (2009) 27:507–11. 10.1016/j.mpsur.2009.10.013
    1. Zouikr I, Karshikoff B. Lifetime modulation of the pain system via neuroimmune and neuroendocrine interactions. Front Immunol. (2017) 8:276. 10.3389/fimmu.2017.00276
    1. Tahayori B, Koceja DM. Activity-dependent plasticity of spinal circuits in the developing and mature spinal cord. Neural Plast. (2012) 2012:964843. 10.1155/2012/964843
    1. Wolpaw JR, Tennissen AM. Activity-dependent spinal cord plasticity in health and disease. Annu Rev Neurosci. (2001) 24:807–43. 10.1146/annurev.neuro.24.1.807
    1. Smith CC, Paton JFR, Chakrabarty S, Ichiyama RM. Descending systems direct development of key spinal motor circuits. J Neurosci. (2017) 37:6372–87. 10.1523/JNEUROSCI.0149-17.2017
    1. Ruda MA, Ling QD, Hohmann AG, Peng YB, Tachibana T. Altered nociceptive neuronal circuits after neonatal peripheral inflammation. Science. (2000) 289:628–31. 10.1126/science.289.5479.628
    1. Ren K, Anseloni V, Zou SP, Wade EB, Novikova SI, Ennis M, et al. . Characterization of basal and re-inflammation-associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult. Pain. (2004) 110:588–96. 10.1016/j.pain.2004.04.006
    1. Yam MF, Loh YC, Tan CS, Khadijah Adam S, Abdul Manan N, Basir R. General pathways of pain sensation and the major neurotransmitters involved in pain regulation. Int J Mol Sci. (2018) 19:E2164. 10.3390/ijms19082164
    1. Leinekugel X, Khalilov I, McLean H, Caillard O, Gaiarsa JL, Ben-Ari Y, et al. . GABA is the principal fast-acting excitatory transmitter in the neonatal brain. Adv Neurol. (1999) 79:189–201.
    1. Baccei ML, Bardoni R, Fitzgerald M. Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol. J Physiol. (2003) 549:231–42. 10.1113/jphysiol.2003.040451
    1. Baccei ML, Fitzgerald M. Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. J Neurosci. (2004) 24:4749–57. 10.1523/JNEUROSCI.5211-03.2004
    1. Bremner L, Fitzgerald M, Baccei M. Functional GABA(A)-receptor-mediated inhibition in the neonatal dorsal horn. J Neurophysiol. (2006) 95:3893–7. 10.1152/jn.00123.2006
    1. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain. (2009) 10:895–926. 10.1016/j.jpain.2009.06.012
    1. Hathway GJ, Vega-Avelaira D, Fitzgerald M. A critical period in the supraspinal control of pain: opioid-dependent changes in brainstem rostroventral medulla function in preadolescence. Pain. (2012) 153:775–83. 10.1016/j.pain.2011.11.011
    1. Fitzgerald M, Millard C, MacIntosh N. Hyperalgesia in premature infants. Lancet. (1988) 1:292. 10.1016/S0140-6736(88)90365-0
    1. Walker SM, Fitzgerald M, Hathway GJ. Surgical injury in the neonatal rat alters the adult pattern of descending modulation from the rostroventral medulla. Anesthesiology. (2015) 122:1391–400. 10.1097/ALN.0000000000000658
    1. Zhang YH, Wang XM, Ennis M. Effects of neonatal inflammation on descending modulation from the rostroventromedial medulla. Brain Res Bull. (2010) 83:16–22. 10.1016/j.brainresbull.2010.07.007
    1. Huang H, Zhang J, Wakana S, Zhang W, Ren T, Richards LJ, et al. . White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage. (2006) 33:27–38. 10.1016/j.neuroimage.2006.06.009
    1. Volpe JJ. The encephalopathy of prematurity–brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol. (2009) 16:167–78. 10.1016/j.spen.2009.09.005
    1. Plomgaard AM, Andersen AD, Petersen TH, van de Looij Y, Thymann T, Sangild PT, et al. . Structural brain maturation differs between preterm and term piglets, whereas brain activity does not. Acta Paediatr. (2019) 108:637–44. 10.1111/apa.14556
    1. Anand KJ, Garg S, Rovnaghi CR, Narsinghani U, Bhutta AT, Hall RW. Ketamine reduces the cell death following inflammatory pain in newborn rat brain. Pediatr Res. (2007) 62:283–90. 10.1203/PDR.0b013e3180986d2f
    1. Gwak YS, Kang J, Unabia GC, Hulsebosch CE. Spatial and temporal activation of spinal glial cells: role of gliopathy in central neuropathic pain following spinal cord injury in rats. Exp Neurol. (2012) 234:362–72. 10.1016/j.expneurol.2011.10.010
    1. Verriotis M, Chang P, Fitzgerald M, Fabrizi L. The development of the nociceptive brain. Neuroscience. (2016) 338:207–19. 10.1016/j.neuroscience.2016.07.026
    1. Crair MC, Malenka RC. A critical period for long-term potentiation at thalamocortical synapses. Nature. (1995) 375:325–8. 10.1038/375325a0
    1. Pape HC, Stork O. Genes and mechanisms in the amygdala involved in the formation of fear memory. Ann N Y Acad Sci. (2003) 985:92–105. 10.1111/j.1749-6632.2003.tb07074.x
    1. Kalanjati VP, Wixey JA, Miller SM, Colditz PB, Bjorkman ST. GABAA receptor expression and white matter disruption in intrauterine growth restricted piglets. Int J Dev Neurosci. (2017) 59:1–9. 10.1016/j.ijdevneu.2017.02.004
    1. Janak PH, Tye KM. From circuits to behaviour in the amygdala. Nature. (2015) 517:284–92. 10.1038/nature14188
    1. McGaugh JL, Cahill L, Roozendaal B. Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci USA. (1996) 93:13508–14. 10.1073/pnas.93.24.13508
    1. Goenka A, Kollmann TR. Development of immunity in early life. J Infect. (2015) 71:S112–20. 10.1016/j.jinf.2015.04.027
    1. Totsch SK, Sorge RE. Immune system involvement in specific pain conditions. Mol Pain. (2017) 13:1744806917724559. 10.1177/1744806917724559
    1. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. (1990) 39:151–70. 10.1016/0306-4522(90)90229-W
    1. Verney C, Monier A, Fallet-Bianco C, Gressens P. Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J Anat. (2010) 217:436–48. 10.1111/j.1469-7580.2010.01245.x
    1. Burke NN, Fan CY, Trang T. Microglia in health and pain: impact of noxious early life events. Exp Physiol. (2016) 101:1003–21. 10.1113/EP085714
    1. Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci. (2007) 10:1361–8. 10.1038/nn1992
    1. Ding X, Liang YJ, Su L, Liao FF, Fang D, Tai J, et al. . BDNF contributes to the neonatal incision-induced facilitation of spinal long-term potentiation and the exacerbation of incisional pain in adult rats. Neuropharmacology. (2018) 137:114–32. 10.1016/j.neuropharm.2018.04.032
    1. Hathway GJ, Vega-Avelaira D, Moss A, Ingram R, Fitzgerald M. Brief, low frequency stimulation of rat peripheral C-fibres evokes prolonged microglial-induced central sensitization in adults but not in neonates. Pain. (2009) 144:110–8. 10.1016/j.pain.2009.03.022
    1. Vega-Avelaira D, Ballesteros JJ, López-García JA. Inflammation-induced hyperalgesia and spinal microglia reactivity in neonatal rats. Eur J Pain. (2013) 17:1180–8. 10.1002/j.1532-2149.2013.00308.x
    1. Sorge RE, Mapplebeck JC, Rosen S, Beggs S, Taves S, Alexander JK, et al. . Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat Neurosci. (2015) 18:1081–3. 10.1038/nn.4053
    1. Kim JJ, Foy MR, Thompson RF. Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci USA. (1996) 93:4750–3. 10.1073/pnas.93.10.4750
    1. Brennan TJ, Vandermeulen EP, Gebhart GF. Characterization of a rat model of incisional pain. Pain. (1996) 64:493–501. 10.1016/0304-3959(95)01441-1
    1. Brennan TJ, Zahn PK, Pogatzki-Zahn EM. Mechanisms of incisional pain. Anesthesiol Clin North Am. (2005) 23:1–20. 10.1016/j.atc.2004.11.009
    1. Castel D, Sabbag I, Meilin S. The effect of local/topical analgesics on incisional pain in a pig model. J Pain Res. (2019) 10:2169–75. 10.2147/JPR.S144949
    1. Chu YC, Chan KH, Tsou MY, Lin SM, Hsieh YC, Tao YX. Mechanical pain hypersensitivity after incisional surgery is enhanced in rats subjected to neonatal peripheral inflammation: effects of N-methyl-D-aspartate receptor antagonists. Anesthesiology. (2007) 106:1204–12. 10.1097/01.anes.0000267604.40258.d1
    1. Gilchrist HD, Allard BL, Simone DA. Enhanced withdrawal responses to heat and mechanical stimuli following intraplantar injection of capsaicin in rats. Pain. (1996) 67:179–88. 10.1016/0304-3959(96)03104-1
    1. Kang S, Wu C, Banik RK, Brennan TJ. Effect of capsaicin treatment on nociceptors in rat glabrous skin one day after plantar incision. Pain. (2010) 148:128–40. 10.1016/j.pain.2009.10.031
    1. Roizenblatt S, Andersen ML, Bignotto M, D'Almeida V, Martins PJ, Tufik S. Neonatal arthritis disturbs sleep and behaviour of adult rat offspring and their dams. Eur J Pain. (2010) 14:985–91. 10.1016/j.ejpain.2010.03.008
    1. Walker SM, Meredith-Middleton J, Cooke-Yarborough C, Fitzgerald M. Neonatal inflammation and primary afferent terminal plasticity in the rat dorsal horn. Pain. (2003) 105:185–95. 10.1016/S0304-3959(03)00201-X
    1. Anseloni VC, He F, Novikova SI, Turnbach Robbins M, Lidow IA, Ennis M, et al. . Alterations in stress-associated behaviors and neurochemical markers in adult rats after neonatal short-lasting local inflammatory insult. Neuroscience. (2005) 131:635–45. 10.1016/j.neuroscience.2004.11.039
    1. Davis SM, Rice M, Rudlong J, Eaton V, King T, Burman MA. Neonatal pain and stress disrupts later-life pavlovian fear conditioning and sensory function in rats: evidence for a two-hit model. Dev Psychobiol. (2018) 60:520–33. 10.1002/dev.21632
    1. Torsney C, Fitzgerald M. Spinal dorsal horn cell receptive field size is increased in adult rats following neonatal hindpaw skin injury. J Physiol. (2003) 550:255–61. 10.1113/jphysiol.2003.043661
    1. Victoria NC, Inoue K, Young LJ, Murphy AZ. A single neonatal injury induces life-long deficits in response to stress. Dev Neurosci. (2013) 35:326–37. 10.1159/000351121
    1. Butkevich IP, Mikhailenko VA, Vershinina EA, Ulanova NA. Differences in adaptive behaviors of adolescent male and female rats exposed at birth to inflammatory pain or stress. J Evol Biochem Physiol. (2015) 51:305–15. 10.1134/S0022093015040067
    1. Doenni VM, Song CM, Hill MN, Pittman QJ. Early-life inflammation with LPS delays fear extinction in adult rodents. Brain Behav Immun. (2017) 63:176–85. 10.1016/j.bbi.2016.11.022
    1. Paluch LR, Lieggi CC, Dumont M, Monette S, Riedel ER, Lipman NS. Developmental and behavioral effects of toe clipping on neonatal and preweanling mice with and without vapocoolant anesthesia. J Am Assoc Lab Anim Sci. (2014) 53:132–40.
    1. Schaefer DC, Asner IN, Seifert B, Bürki K, Cinelli P. Analysis of physiological and behavioural parameters in mice after toe clipping as newborns. Lab Anim. (2010) 44:7–13. 10.1258/la.2009.009020
    1. Schellinck HM, Stanford L, Darrah M. Repetitive acute pain in infancy increases anxiety but does not alter spatial learning ability in juvenile mice. Behav Brain Res. (2003) 142:157–65. 10.1016/S0166-4328(02)00406-0
    1. Page GG, Blakely WP, Kim M. The impact of early repeated pain experiences on stress responsiveness and emotionality at maturity in rats. Brain Behav Immun. (2005) 19:78–87. 10.1016/j.bbi.2004.05.002
    1. Catré D, Lopes MF, Cabrita AS. Lasting developmental effects of neonatal fentanyl exposure in preweanling rats. Anesthesiol Res Pract. (2012) 2012:180124. 10.1155/2012/180124
    1. Chen M, Xia D, Min C, Zhao X, Chen Y, Liu L, et al. . Neonatal repetitive pain in rats leads to impaired spatial learning and dysregulated hypothalamic-pituitary-adrenal axis function in later life. Sci Rep. (2016) 6:39159. 10.1038/srep39159
    1. Ririe DG, Bremner LR, Fitzgerald M. Comparison of the immediate effects of surgical incision on dorsal horn neuronal receptive field size and responses during postnatal development. Anesthesiology. (2008) 109:698–706. 10.1097/ALN.0b013e3181870a32
    1. Howard RF, Walker SM, Mota PM, Fitzgerald M. The ontogeny of neuropathic pain: postnatal onset of mechanical allodynia in rat spared nerve injury (SNI) and chronic constriction injury (CCI) models. Pain. (2005) 115:382–9. 10.1016/j.pain.2005.03.016
    1. Ririe DG, Eisenach JC. Age-dependent responses to nerve injury-induced mechanical allodynia. Anesthesiology. (2006) 104:344–50. 10.1097/00000542-200602000-00021
    1. Vega-Avelaira D, Géranton SM, Fitzgerald M. Differential regulation of immune responses and macrophage/neuron interactions in the dorsal root ganglion in young and adult rats following nerve injury. Mol Pain. (2009) 5:70. 10.1186/1744-8069-5-70
    1. Vega-Avelaira D, McKelvey R, Hathway G, Fitzgerald M. The emergence of adolescent onset pain hypersensitivity following neonatal nerve injury. Mol Pain. (2012) 30:30 10.1186/1744-8069-8-30
    1. Blom JM, Benatti C, Alboni S, Capone G, Ferraguti C, Brunello N, et al. . Early postnatal chronic inflammation produces long-term changes in pain behavior and N-methyl-D-aspartate receptor subtype gene expression in the central nervous system of adult mice. J Neurosci Res. (2006) 84:1789–98. 10.1002/jnr.21077
    1. Lim EJ, Back SK, Kim MA, Li C, Lee J, Jeong KY, et al. Long-lasting neonatal inflammation enhances pain responses to subsequent inflammation, but not peripheral nerve injury in adult rats. Int J Dev Neurosci. (2009) 27:215–22. 10.1016/j.ijdevneu.2009.01.005
    1. Hohmann AG, Neely MH, Pina J, Nackley AG. Neonatal chronic hind paw inflammation alters sensitization to intradermal capsaicin in adult rats: a behavioral and immunocytochemical study. J Pain. (2005) 6:798–808. 10.1016/j.jpain.2005.07.009
    1. Laprairie JL, Johns ME, Murphy AZ. Preemptive morphine analgesia attenuates the long-term consequences of neonatal inflammation in male and female rats. Pediatr Res. (2008) 64:625–30. 10.1203/PDR.0b013e31818702d4
    1. LaPrairie JL, Murphy AZ. Female rats are more vulnerable to the long-term consequences of neonatal inflammatory injury. Pain. (2007) 132:S124–33. 10.1016/j.pain.2007.08.010
    1. Lidow MS, Song ZM, Ren K. Long-term effects of short-lasting early local inflammatory insult. Neuroreport. (2001) 12:399–403. 10.1097/00001756-200102120-00042
    1. Wang G, Ji Y, Lidow MS, Traub RJ. Neonatal hind paw injury alters processing of visceral and somatic nociceptive stimuli in the adult rat. J Pain. (2004) 5:440–9. 10.1016/j.jpain.2004.07.003
    1. Mikhailenko VA, Butkevich IP, Vershinina EA, Ulanova NA. Long-term changes in adaptive behavior of rats after neonatal inflammatory pain. Zh Evol Biokhim Fiziol. (2015) 51:108–14. 10.1134/S0022093015020052
    1. Moss A, Beggs S, Vega-Avelaira D, Costigan M, Hathway GJ, Salter MW, et al. . Spinal microglia and neuropathic pain in young rats. Pain. (2007) 128:215–24. 10.1016/j.pain.2006.09.018
    1. Knaepen L, Patijn J, Tibboel D, Joosten EA. Sex differences in inflammatory mechanical hypersensitivity in later life of rats exposed to repetitive needle pricking as neonates. Neurosci Lett. (2012) 516:285–9. 10.1016/j.neulet.2012.04.012
    1. Johnston CC, Walker CD. The effects of exposure to repeated minor pain during the neonatal period on formalin pain behaviour and thermal withdrawal latencies. Pain Res Manag. (2003) 8:213–7. 10.1155/2003/305409
    1. van den Hoogen NJ, Tibboel D, Honig WM, Hermes D, Patijn J, Joosten EA. Neonatal paracetamol treatment reduces long-term nociceptive behaviour after neonatal procedural pain in rats. Eur J Pain. (2016) 20:1309–18. 10.1002/ejp.855
    1. Walker CD, Kudreikis K, Sherrard A, Johnston CC. Repeated neonatal pain influences maternal behavior, but not stress responsiveness in rat offspring. Dev Brain Res. (2003) 140:253–61. 10.1016/S0165-3806(02)00611-9
    1. Moriarty O, Tu Y, Sengar AS, Salter MW, Beggs S, Walker SM. Priming of adult incision response by early life injury: neonatal microglial inhibition has persistent but sexually dimorphic effects in adult rats. J Neurosci. (2019) 39:3081–93. 10.1523/JNEUROSCI.1786-18.2019
    1. Moriarty O, Harrington L, Beggs S, Walker S. Opioid analgesia and the somatosensory memory of neonatal surgical injury in the adult rat. Br J Anaesth. (2018) 121:314–24. 10.1016/j.bja.2017.11.111
    1. Gibson CL, Arnott GA, Clowry GJ. Plasticity in the rat spinal cord seen in response to lesions to the motor cortex during development but not to lesions in maturity. Exp Neurol. (2000) 166:422–34. 10.1006/exnr.2000.7511
    1. Smith C, Nordstrom E, Sengupta JN, Miranda A. Neonatal gastric suctioning results in chronic visceral and somatic hyperalgesia: role of corticotropin releasing factor. Neurogastroenterol Motil. (2007) 19:692–9. 10.1111/j.1365-2982.2007.00949.x
    1. Victoria NC, Karom MC, Murphy AZ. Analgesia for early-life pain prevents deficits in adult anxiety and stress in rats. Dev Neurosci. (2015) 37:1–13. 10.1159/000366273
    1. McKelvey R, Berta T, Old E, Ji RR, Fitzgerald M. Neuropathic pain is constitutively suppressed in early life by anti-inflammatory neuroimmune regulation. J Neurosci. (2015) 35:457–66. 10.1523/JNEUROSCI.2315-14.2015
    1. Giminiani PD, Edwards SA, Malcolm EM, Leach MC, Herskin MS, Sandercock DA. Characterization of short- and long-term mechanical sensitisation following surgical tail amputation in pigs. Sci Rep. (2017) 7:1–9. 10.1038/s41598-017-05404-y
    1. Sandercock DA, Barnett MW, Coe JE, Downing AC, Nirmal AJ, Di Giminiani P, et al. . Transcriptomics analysis of porcine caudal dorsal root ganglia in tail amputated pigs shows long-term effects on many pain-associated genes. Front Vet Sci. (2019) 6:314. 10.3389/fvets.2019.00314
    1. van den Hoogen NJ, Patijn J, Tibboel D, Joosten EA. Repetitive noxious stimuli during early development affect acute and long-term mechanical sensitivity in rats. Pediatr Res. (2019) 87:26–31. 10.1038/s41390-019-0420-x
    1. Fehrenbacher JC, Vasko MR, Duarte DB. Models of inflammation: Carrageenan- or complete Freund's Adjuvant (CFA)-induced edema and hypersensitivity in the rat. Curr Protoc Pharmacol. (2012) Chapter 5:Unit5.4. 10.1002/0471141755.ph0504s56
    1. McKeon GP, Pacharinsak C, Long CT, Howard AM, Jampachaisri K, Yeoman DC, et al. . Analgesic effects of tramadol, tramadol–gabapentin, and buprenorphine in an incisional model of pain in rats (Rattus norvegicus). J Am Assoc Lab Anim Sci. (2011) 50:192–7.
    1. Peters CM, Hayashida K, Suto T, Houle TT, Aschenbrenner CA, Martin TJ, et al. . Individual differences in acute pain-induced endogenous analgesia predict time to resolution of postoperative pain in the rat. Anesthesiology. (2015) 122:895–907. 10.1097/ALN.0000000000000593
    1. Institute of Medicine Committee on Advancing Pain Research CE The National Academies Collection: Reports funded by National Institutes of Health. Relieving Pain in America: A Blueprint for Transforming Prevention, Care, Education, and Research. Washington, DC: National Academies Press; National Academy of Sciences; (2011).
    1. Jones GT. Psychosocial vulnerability and early life adversity as risk factors for central sensitivity syndromes. Curr Rheumatol Rev. (2016) 12:140–53. 10.2174/1573397112666151231113438
    1. Littlejohn C, Pang D, Power C, Macfarlane GJ, Jones GT. Is there an association between preterm birth or low birthweight and chronic widespread pain? Results from the 1958 Birth Cohort Study. Eur J Pain. (2012) 16:134–9. 10.1016/j.ejpain.2011.05.015
    1. Pyhala R, Wolford E, Kautiainen H, Andersson S, Bartmann P, Baumann N, et al. . Self-reported mental health problems among adults born preterm: a meta-analysis. Pediatrics. (2017) 139:e20162690. 10.1542/peds.2016-2690
    1. Burma NE, Leduc-Pessah H, Fan CY, Trang T. Animal models of chronic pain: advances and challenges for clinical translation. J Neurosci Res. (2017) 95:1242–56. 10.1002/jnr.23768
    1. Gregory NS, Harris AL, Robinson CR, Dougherty PM, Fuchs PN, Sluka KA. An overview of animal models of pain: disease models and outcome measures. J Pain. (2013) 14:1255–69. 10.1016/j.jpain.2013.06.008
    1. Williams M, Meyers R, Lascelles B. PS19 long-term impacts of early life injury on monoiodoacetate induced osteoarthritis in adult rats. J Am Assoc Lab Anim Sci. (2018) 57:610 Available online at:
    1. Cope PJ, Ourradi K, Li Y, Sharif M. Models of osteoarthritis: the good, the bad and the promising. Osteoarthritis Cartilage. (2019) 27:230–9. 10.1016/j.joca.2018.09.016
    1. Knazovicky D, Helgeson ES, Case B, Thomson A, Gruen ME, Maixner W, et al. X. Replicate effects and test-retest reliability of quantitative sensory threshold testing in dogs with and without chronic pain. Vet Anaesth Analg. (2017) 44:615–24. 10.1016/j.vaa.2016.08.008
    1. Uilenreef J, van der Staay FJ, Meijer E. A monosodium iodoacetate osteoarthritis lameness model in growing pigs. Animals (Basel). (2019) 9:405. 10.3390/ani9070405
    1. Wilkes D, Li G, Angeles CF, Patterson JT, Huang LY. A large animal neuropathic pain model in sheep: a strategy for improving the predictability of preclinical models for therapeutic development. J Pain Res. (2012) 5:415–24. 10.2147/JPR.S34977
    1. Lascelles BDX, Brown DC, Maixner W, Mogil JS. Spontaneous painful disease in companion animals can facilitate the development of chronic pain therapies for humans. Osteoarthritis Cartilage. (2018) 26:175–83. 10.1016/j.joca.2017.11.011
    1. Eiby YA, Wright LL, Kalanjati VP, Miller SM, Bjorkman ST, Keates HL, et al. . A pig model of the preterm neonate: anthropometric and physiological characteristics. PLoS ONE. (2013) 8:e68763. 10.1371/journal.pone.0068763
    1. Gobina I, Villberg J, Välimaa R, Tynjälä J, Whitehead R, Cosma A, et al. . Prevalence of self-reported chronic pain among adolescents: evidence from 42 countries and regions. Eur J Pain. (2019) 23:316–26. 10.1002/ejp.1306
    1. Kennedy J, Roll JM, Schraudner T, Murphy S, McPherson S. Prevalence of persistent pain in the U.S. adult population: new data from the 2010 national health interview survey. J Pain. (2014) 15:979–84. 10.1016/j.jpain.2014.05.009
    1. Nahin RL. Estimates of pain prevalence and severity in adults: United States, 2012. J Pain. (2015) 16:769–80. 10.1016/j.jpain.2015.05.002
    1. Pitcher MH, Von Korff M, Bushnell MC, Porter L. Prevalence and profile of high-impact chronic pain in the United States. J Pain. (2019) 20:146–60. 10.1016/j.jpain.2018.07.006
    1. Victoria NC, Murphy AZ. Exposure to early life pain: long term consequences and contributing mechanisms. Curr Opin Behav Sci. (2016) 7:61–8. 10.1016/j.cobeha.2015.11.015
    1. Walker SM. Translational studies identify long-term impact of prior neonatal pain experience. Pain. (2017) 158:S29–42. 10.1097/j.pain.0000000000000784

Source: PubMed

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