This is the first attempt, to the best of our knowledge, to describe the feasibility of using a facial expression–based tool, which was originally developed for newborns, in a human fetus under an acute pain condition. We have described the fetal facial changes seen after acute pain by using high-resolution 4D ultrasound. In this model, we have used the rest condition before the injection of analgesics as a control, to explore the facial expressions that were present exclusively during the painful anaesthetic puncture. Should this approach be confirmed in future larger validation studies, it could be a way to monitor acute pain–related facial expression in human fetuses in an inexpensive and straightforward fashion. Indeed, the possibility to assess pain-related behaviours intrauterus would allow not only for the monitoring of the efficacy of anaesthetic procedures in the fetus but would also open the way to explore the evolution of pain-related facial responses during the fetal neurodevelopment. One could explore when the pain-related facial expressions actually begin during the development, and which are their core components.25 It could also open the way to the development of a potential biological markers of pain/pain behaviours in fetus,22 which can have ethical and legal consequences. However, no human studies have directly reported on the development of thalamocortical circuits associated with pain perception in fetuses.20 From the theoretical point of view, one frequently associates the presence and qualities of facial expressions in pain with the social-adaptative development of nonverbal communication.11,27 Since fetuses express a plethora of facial movements in the dark uterus, one could ask whether this energy-consuming and apparently socially vital behaviour is being trained for extrauterine life (such as other behaviours such as sucking and stretching), or would it be serving another function. The presence of such facial movements would actually favour the model,5 proposing that feelings are indeed a coupling of the sensory discriminant perception with an “output” behavioural drive and reflex response. In this view, facial expressions may constitute the motor reflexive expression of the emotional motor system and could exist in the absence of a socially interacting observer.21 The aim of this report was to provide the description of an acute pain model and a potentially useful way to measure it. Should this approach endure the processes of validation, it could bring to life practical as well as theoretical new insights into the mechanisms of pain expression in humans.
There are no conflicts of interests in this study.
This study was funded by the Pain Center and Department of Obstetrics and Gynecology.
The authors are thankful to Esther Minorescu and Marly dos Santos for technical assistance.
Supplemental digital content
Supplemental digital content associated with this article can be found online at http://links.lww.com/PR9/A27.
. Anand KJ, Hickey PR. Pain and its effects in the human neonate and fetus. N Engl J Med 1987;317:1321–9.
. Andonotopo W, Kurjak A. The assessment of fetal behavior of growth restricted fetuses by 4D sonography. J Perinat Med 2006;34:471–8.
. Andrade DC, Faria JW, Caramelli P, Alvarenga L, Galhardoni R, Siqueira SR, Yeng LT, Teixeira MJ. The assessment and management of pain in the demented and non-demented elderly patient. Arq Neuropsiquiatr 2011;69:387–94.
. Bellieni CV, Buonocore G. Is fetal pain
a real evidence? J Matern Fetal Neonatal Med 2012;25:1203–8.
. Craig (Bud) AD. How do you feel? An interoceptive moment with your neurobiological self. Princeton: Princeton University Press, 2015. p. 21–2.
. Deli T, Szeyerényi P. Fetal pain
and intrauterine analgesia/anesthesia—long-term pathologic effects, causes and alleviation of intrauterine pain [in Hungarian]. Orv Hetil 2010;151;702–6.
. DiPietro JA, Costigan KA, Voegtline KM. Studies in fetal behavior: revisited, renewed, and reimagined. Monogr Soc Res Child Dev 2015;80:VII; 1–94.
. Ekman P, Friesen WV. Manual for the facial action coding system. Palo Alto: Consulting Psychologists Press, 1978.
. Grunau RE, Oberlander T, Holsti L, Whitfield MF. Bedside application of the Neonatal Facial Coding System in pain assessment of premature neonates. PAIN 1998;76:277–86.
. Grunau RVE, Craig KD. Facial activity as a measure of neonatal pain expression. In: Tyler DC, Krane EJ, editors. Advances in pain research and therapy. Vol. 15. New York: Raven, 1990. p. 147–55.
. Hadjistavropoulos HD, Craig KD, Grunau RE, Whitfield MF. Judging pain in infants: behavioural, contextual, and developmental determinants. PAIN 1997;73:319–24.
. Hadjistavropoulos T, Craig KD, Duck S, Cano A, Goubert L, Jackson PL, Mogil JS, Rainville P, Sullivan MJ, Williams ACC, Vervoort T, Fitzgerald TD. A biopsychosocial formulation of pain communication. Psychol Bull 2011;137:910–39.
. Hevner RF. Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol 2000;59:385–92.
. Karmann AJ, Lautenbacher S, Bauer F, Kunz M. The influence of communicative relations on facial responses to pain: does it matter who is watching? Pain Res Manag 2014;19:15–22.
. Kostovic I, Goldman-Rakic PS. Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 1983;219:431–47.
. Kostovic I, Rakic P. Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 1984;4:25–42.
. Kostovic I, Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 1990;297:441–70.
. Lamm C, Porges EC, Cacioppo JT, Decety J. Perspective taking is associated with specific facial responses during empathy for pain. Brain Res 2008;1227:153–61.
. Lautenbacher S, Kunz M. Facial pain expression in dementia: a review of the experimental and clinical evidence. Curr Alzheimer Res 2017;14:501–5.
. Lee SJ, Ralston HJ, Drey EA, Partridge JC, Rosen MA. Fetal pain
: a systematic multidisciplinary review of the evidence. JAMA 2005;294:947–54.
. Libet B, Gleason CA, Wright EW, Pearl DK. Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 1983;106:623–42.
. Petrikovsky B, Kaplan G, Holsten N. Fetal yawning activity in normal and high-risk fetuses: a preliminary observation. Ultrasound Obstet Gynecol 1999;13:127–30.
. Platt MW. Fetal awareness and fetal pain
: the Emperor's new clothes. Arch Dis Child Fetal Neonatal Ed 2011;96:F236–F237.
. Reissland N, Francis B, Mason J, Lincoln K. Do facial expressions develop before birth? PLoS One 2011;6:e24081.
. Reissland N, Francis B, Mason J. Can healthy fetuses show facial expressions of “Pain” or “Distress”? PLoS One 2013;8:e65530.
. Steinbock B. Life before birth: the moral and legal status of embryos and fetuses. New York: Oxford University Press, 1992. p. 400.
. Yan F, Dai SY, Akther N, Kuno A, Yanagihara T, Hata T. Four-dimensional sonographic assessment of fetal facial expression early in the third trimester. Int J Gynaecol Obstet 2006;94:108–13.
. Yigiter AB, Kavak ZN. Normal standards of fetal behavior assessed by four-dimensional sonography. J Matern Fetal Neonatal Med 2006;19:707–21.