Effects of gustatory stimulation on oral readiness and behavioral states of newborns

Andréa Monteiro Correia Medeiros Vinicius do Nascimento Santi Felipe Batista Santos Thalyta Prata Leite de Sá Íkaro Daniel Carvalho Barreto Luana Ramos de Aquino Stella Andrade Alves Rogeris Kayque Barreto do Nascimento Ricardo Queiroz Gurgel About the authors

RESUMO

Objetivo

investigar e comparar comportamentos específicos de prontidão oral e estados comportamentais de recém-nascidos a termo (RNT) e pré-termo (RNPT), a partir da estimulação gustativa (água e sacarose).

Métodos

estudo experimental, analítico, duplo-cego, caso controle. Participaram 152 recém-nascidos de uma maternidade pública, sendo 68 a termo e 84 pré-termo, subdivididos conforme estímulo gustativo (água ou sacarose). O teste durou 15 minutos, dividido em três períodos de cinco minutos. Foram analisados estados comportamentais e comportamentos específicos.

Resultados

foram observadas diferenças significativas, comparando os estímulos, com maior tempo nos comportamentos mão-boca direita (p=0,042) e esquerda (p=0,037), e diminuição no tempo de sono (p=0,019) nos RNT estimulados com sacarose. Nos RNPT houve maior tempo de sucção de mão direita (p=0,043) e esquerda (p=0,001) e de sucção (p<0,001), com aumento no tempo de alerta (p=0,025), quando estimulados com sacarose. Houve diminuição de tempo de agitação (p=0,018) em RNPT estimulados com água. RNT apresentaram maior tempo em sono do que os RNPT (p=0,032). A estimulação da sacarose no estado alerta foi mais evidente em RNPT (p=0,047).

Conclusão

A sacarose eliciou respostas motoras referentes à prontidão para alimentação e estado comportamental favorável para alimentação, independentemente da idade gestacional. Os achados são importantes para a clínica fonoaudiológica, possibilitando ampliar condutas de estimulação da alimentação.

Descritores:
Recém-nascido; Recém-nascido prematuro; Percepção gustatória; Sacarose; Comportamento de sucção

ABSTRACT

Purpose

To investigate and compare specific oral readiness behavior and behavioral states of term newborns (TNB) and preterm newborns (PTNB) based on taste stimulation (water and sucrose).

Methods

Experimental, analytical, double-blind, case-control study: 152 newborns from a public maternity hospital participated, 68 of them were term newborns and 84,preterm , divided according to taste stimulus (water or sucrose). The test lasted 15 minutes, divided into three periods of 5 minutes. We evaluated behavioral states and specific behaviors.

Results

We observed significant difference by comparing stimulations and longer periods of right (p=0.042) and left (p=0.037) hand suction for mouth behavior, shorter sleeping periods (p=0.019) in TNB stimulated with sucrose. In PTNB, we observed longer periods of right hand (p=0.043) and left hand (p=0.001) suction, suction (p<0.001) and alert state (p=0.025) when stimulated with sucrose. We found a decrease in agitation (p=0.018) in PTNB stimulated with water. The TNB were asleep for longer periods of time than PTBN (p=0.032). Sucrose stimulation in alert state is more evident in PTNB (p=0.047).

Conclusion

Sucrose elicited motor responses related to food readiness and favorable behavioral status for food regardless of gestational age. The findings are important for the speech therapy clinic, enabling broader feeding stimulation approaches.

Keywords:
Newborn; Infant premature; Taste perception; Sucrose; Sucking behavior

INTRODUCTION

Human beings have a vast behavioral repertoire at birth, showing learning capacities and social interaction at an extremely early age(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
). Studies have investigated the existence of functional systems initiated in the intrauterine period (11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
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,22 Hayes JE, Johnson SL. Sensory aspects of bitter and sweet tastes during early childhood. Nutr Today. 2017 Mar;52(2):S41-51. http://dx.doi.org/10.1097/NT.0000000000000201.
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), considering the development of the senses still in pregnancy(33 Clark-Gambelunghe MB, Clark DA. Sensory development. Pediatr Clin North Am. 2015 Apr;62(2):367-84. http://dx.doi.org/10.1016/j.pcl.2014.11.003. PMid:25836703.
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,44 Grigore M, Gafitanu D, Socolov D, Grigore AM, Nemeti G, Micu R. The role of 4D US in evaluation of fetal movements and facial expressions and their relationship with fetal neurobehaviour. Med Ultrason. 2018;20(1):88-94. http://dx.doi.org/10.11152/mu-1350. PMid:29400374.
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).

Behaviors such as putting your hands into your mouth appear in the intrauterine period. Since the 15th week of gestation, fetuses have been observed sucking the right thumb and showing oromanual integration, preferably on the right side of the body(55 Reissland N, Francis B, Aydin E, Mason J, Exley K. Development of prenatal lateralization: evidence from fetal mouth movements. Physiol Behav. 2014 May;131:160-3. http://dx.doi.org/10.1016/j.physbeh.2014.04.035. PMid:24768644.
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). Taste activation starts around the 30th week of pregnancy(66 Paglia L. Taste development and prenatal prevention. Eur J Paediatr Dent. 2019;20(4):257. PMid:31850766.).

Considering that it has been reported as preferential(22 Hayes JE, Johnson SL. Sensory aspects of bitter and sweet tastes during early childhood. Nutr Today. 2017 Mar;52(2):S41-51. http://dx.doi.org/10.1097/NT.0000000000000201.
http://dx.doi.org/10.1097/NT.00000000000...
), sweet taste stimuli is addressed when investigating early-life development(77 Forestell CA, Mennella JA. The ontogeny of taste perception and preference throughout childhood. In: Doty RL, editor. Handbook of olfaction and gustation. Hoboken, NJ: John Wiley & Sons, Inc; 2015. p. 795-828. http://dx.doi.org/10.1002/9781118971758.ch36.
http://dx.doi.org/10.1002/9781118971758....
). A study shows that the calming effect of sucrose reflects in the function of central stress regulating systems, which are dependent on opioids(88 Barr RG, Young SN, Wright JH, Gravel R, Alkawaf R. Differential calming responses to sucrose taste in crying infants with and without colic. Pediatrics. 1999 May;103(5):e68. http://dx.doi.org/10.1542/peds.103.5.e68. PMid:10224212.
http://dx.doi.org/10.1542/peds.103.5.e68...
).

Studies have demonstrated various effects caused by stimulation with sucrose, from evoking facial patterns and smiles to sucking and protruding tongue movements in newborns (NBs)(99 Forestell CA. Flavor perception and preference development in human infants. Ann Nutr Metab. 2017;70(Suppl. 3):17-25. http://dx.doi.org/10.1159/000478759. PMid:28903110.
http://dx.doi.org/10.1159/000478759...
,1010 Ayres C, Ferreira CF, Bernardi JR, Marcelino TB, Hirakata VN, Silva CH, et al. A method for the assessment of facial hedonic reactions in newborns. J Pediatr. 2017 May;93(3):253-9. http://dx.doi.org/10.1016/j.jped.2016.06.011. PMid:27886807.
http://dx.doi.org/10.1016/j.jped.2016.06...
). There is an effect on the incidence of hand-mouth contact(1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
), with higher frequency and suction strength of preterm newborns (PTNB), in latex or not, comparing with newborns who were not stimulated with a sweet taste(1212 Mennella JA. Ontogeny of taste preferences: basic biology and implications for health. Am J Clin Nutr. 2014 Mar;99(3):704S-11S. http://dx.doi.org/10.3945/ajcn.113.067694. PMid:24452237.
http://dx.doi.org/10.3945/ajcn.113.06769...
,1313 Milbrandt T, Kryscio R, Muchow R, Walker J, Talwalkar V, Iwinski H Jr. Oral sucrose for pain relief during clubfoot casting: a double-blinded randomized controlled trial. J Pediatr Orthop. 2018 Set;38(8):430-5. http://dx.doi.org/10.1097/BPO.0000000000000845. PMid:27636913.
http://dx.doi.org/10.1097/BPO.0000000000...
).

In addition, sweet stimulus has also been used as a treatment to minimize pain in newborns in the context of different types of procedures(1313 Milbrandt T, Kryscio R, Muchow R, Walker J, Talwalkar V, Iwinski H Jr. Oral sucrose for pain relief during clubfoot casting: a double-blinded randomized controlled trial. J Pediatr Orthop. 2018 Set;38(8):430-5. http://dx.doi.org/10.1097/BPO.0000000000000845. PMid:27636913.
http://dx.doi.org/10.1097/BPO.0000000000...
1515 Stevens B, Yamada J, Ohlsson A, Haliburton S, Shorkey A. Sucrose for analgesia in newborn infants undergoing painful procedures. Cochrane Database Syst Rev. 2016 Jul;(7):CD001069.). From a neurophysiological point of view, evidence point out that glucose oral administration in newborns interferes with the response associated with pain at the cortical level by attenuating it(1616 Bembich S, Cont G, Baldassi G, Bua J, Demarini S. Maternal holding vs oral glucose administration as nonpharmacologic analgesia in newborns. JAMA Pediatr. 2015 Mar;169(3):284-5. http://dx.doi.org/10.1001/jamapediatrics.2014.3052. PMid:25599227.
http://dx.doi.org/10.1001/jamapediatrics...
). (A study shows or studies shows [in general]) Study shows that the soothing effect of sucrose lingers on the behavioral state even after behaviors of sucking and putting hands in mouth cease(1717 Barr RG, Quek VSH, Cousineau D, Oberlander TF, Brian JA, Young SN. Effects of intra-oral sucrose on crying, mouthing and hand-mouth contact in newborn and six-week-old infants. Dev Med Child Neurol. 1994 Nov;36(7):608-18. http://dx.doi.org/10.1111/j.1469-8749.1994.tb11898.x. PMid:8034123.
http://dx.doi.org/10.1111/j.1469-8749.19...
).

Actions such as bringing your hands into your mouth and sucking them in the face of gustatory stimulation, as well as sucking and protruding tongue movements, point respectively to the existence of an integrated sensorimotor system(1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
) and a feeding system(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
) present at an early age. Such behaviors can be influenced by the behavioral state(1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.) and the type of sensory stimulation(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
).

The behavioral state considered as a central factor in the readiness for feeding and suction performance(1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.) is correlated with the tone of the NB and ability to respond to the environment. NBs can respond by changing their behavioral state according to external or internal stimuli(1919 Lima RO, Estevam LD, Leite FMC, Almeida MVS, Nascimento L, Amorim MHC, et al. Intervenção de enfermagem-primeiro banho do recém-nascido: estudo randomizado sobre o comportamento neonatal. Acta Paul Enferm. 2020 Mar;33:e-APE20190031.).

When related to hunger, crying may indicate readiness for food. A study shows an increase in the suction of newborns who started feeding after crying versus those who were in a sleep state(2020 Medoff‐Cooper B, Bilker W, Kaplan JM. Sucking patterns and behavioral state in 1‐ and 2‐day‐old full‐term infants. J Obstet Gynecol Neonatal Nurs. 2010 Set;39(5):519-24. http://dx.doi.org/10.1111/j.1552-6909.2010.01173.x. PMid:20919998.
http://dx.doi.org/10.1111/j.1552-6909.20...
). Authors point out that healthy full-term newborns (TNB) are ready to suck in the first hours of life showing good suction frequency when in an active behavioral state(2121 Calegari FL, Barbieratto BJ, Fujinaga CI, Fonseca LMM, de Oliveira CR, Leite AM. Full-term newborns’ readiness during the first breastfeeding in rooming-in. Rev da Rede Enferm do Nord. 2016 Oct;17(4):444.).

Previous research found that gustatory stimulation decreases the occurrence of behavioral states of agitation and crying(2222 Medeiros AMC, Sá TPL, Alvelos CL, Raposo OFF. Efeitos da estimulação gustativa nos estados comportamentais de recém-nascidos prematuros. Audiol Commun Res. 2013 Mar;18(1):50-6. http://dx.doi.org/10.1590/S2317-64312013000100010.
http://dx.doi.org/10.1590/S2317-64312013...
) related to stress(2323 Brasil, Ministério da Saúde. Atenção humanizada ao recém-nascido - método canguru - manual técnico. Ministério da Saúde; Brasília; 2017.), leading to higher occurrence of alertness, the behavioral state that most favors interaction(2323 Brasil, Ministério da Saúde. Atenção humanizada ao recém-nascido - método canguru - manual técnico. Ministério da Saúde; Brasília; 2017.) and consequently readiness for feeding(1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.).

The study hypothesis is that regardless of the corrected gestational age (CGA), newborns may present a higher frequency of readiness behaviors for feeding upon a behavioral state regarded as favorable for feeding (alert) in the presence of sweet eliciting taste stimulus (sucrose).

Our objective was to investigate the specific behaviors related to oral readiness and behavioral states present in TNB and PTNB by establishing a comparison from gustatory stimulation with water and sucrose.

METHODS

Participants

This is an experimental, analytical, double-blind, case-control study carried out with 152 newborns, preterm (N=84) and term (N=68), of both genders, divided according to corrected gestational age (CGA) at the time of assessment, and subdivided according to the taste stimulus offered (sucrose or water).

We followed the prematurity classification by the Brazilian Ministry of Health (2323 Brasil, Ministério da Saúde. Atenção humanizada ao recém-nascido - método canguru - manual técnico. Ministério da Saúde; Brasília; 2017.), which classifies as term newborns born with gestational ages between 37 to 42 weeks and as preterm those born between 28 to 36 weeks and 6 days (2323 Brasil, Ministério da Saúde. Atenção humanizada ao recém-nascido - método canguru - manual técnico. Ministério da Saúde; Brasília; 2017.).

Procedure

Gustatory stimulation was performed within the first 36 hours of life for newborns, while PTNBs were tested within a 35-week CGA hospital stay (ranging from 30 to 36 weeks).

After being randomly chosen to receive stimulation, 34 newborns received water, while the remaining 34 received sucrose. 44 out of the 84 PTNBs received water and 40 were stimulated with sucrose. The bottles were numbered by a single researcher, who did not managed the substance.

The study followed the same methodological design proposed by Medeiros(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
,2424 Medeiros AMC. Contato das mãos com a região oral, protrusão de língua e movimentos de sucção em recém-nascidos humanos, a partir da estimulação oro gustativa [tese]. São Paulo: Universidade de São Paulo; 2002.). Inclusion criteria were: intrauterine growth curve suitable for gestational age (GA), clinical stability at the time of testing, and consent of the person responsible for the test.

Exclusion criteria were: newborns with respiratory support who used an orogastric tube at the time of the test and presence of a clinical history of major neurological and/or cardiac complications and syndromes and/or malformations diagnosed or to be clarified. Newborns who entered into a state of intense crying without ceasing due to gustatory stimulation were also disregarded.

Since no specific data were collected on the newborns' feeding, we were not able to state whether they had any previous feeding experience. However, both groups showed similar results in this regard; in addition, we were careful to consider the diet schedule before performing the test to avoid regurgitation.

The stimulation was proceeded by positioning the newborn in a transport cradle, supine, with a naked body and free upper limbs. The procedure was recorded by a digital camera (Panasonic Compact - VHS Palmcorder) positioned on a tripod, keeping the face and upper limbs properly framed.

Different researchers, who had no prior knowledge of the solution offered (double-blind procedure), administered water or sucrose , only the number of the bottle used for each participant was known. The researchers had been trained by the research coordinator to homogenize the procedure.

Sucrose was used as an agent that elicits motor behaviors and water as a control stimulus. It is worth mentioning that the data were collected from the database previously organized by Medeiros(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
,1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.,2424 Medeiros AMC. Contato das mãos com a região oral, protrusão de língua e movimentos de sucção em recém-nascidos humanos, a partir da estimulação oro gustativa [tese]. São Paulo: Universidade de São Paulo; 2002.).

The test duration was 15 minutes, divided into three periods of five minutes. The first five minutes corresponded to the initial baseline (BL1), without gustatory stimulation and with the NB resting without receiving any stimulation.

In the intermediate five minutes, gustatory stimulation was performed using a disposable syringe (without a needle) with 12% sucrose solution or water. During this period, the examiner administered 0.2 ml of solution every one minute, totaling 1 ml per newborn tested. As in other studies(1212 Mennella JA. Ontogeny of taste preferences: basic biology and implications for health. Am J Clin Nutr. 2014 Mar;99(3):704S-11S. http://dx.doi.org/10.3945/ajcn.113.067694. PMid:24452237.
http://dx.doi.org/10.3945/ajcn.113.06769...
), we chose to use a syringe and not a pacifier, since the maternity hospital in study follows the precepts of the Baby Friendly Hospital Initiative (BFHI).

In the final baseline (BL2), referring to the last five minutes, once again no stimulation was applied (as in the initial baseline) or any intervention occurred.

It is worth mentioning that during the test, the behavioral states and specific behaviors presented by the newborns were not observed or analyzed, which only occurred later on, by filming. Three independent judges analyzed the occurrence of these behaviors per second , recording was performed only upon agreement between at least two of them.

Behavioral states

The observation of behavioral states was adapted from the classification of Medeiros(2424 Medeiros AMC. Contato das mãos com a região oral, protrusão de língua e movimentos de sucção em recém-nascidos humanos, a partir da estimulação oro gustativa [tese]. São Paulo: Universidade de São Paulo; 2002.) and Brazelton's Neonatal Behavioral Assessment Scale(2525 Brazelton TB. Neonatal behavioral assessment scale. London: Willian Heinemann Medical Books; 1973.).

  • Sleep (includes deep sleep, light sleep, and sleepy sleep): eyes should be closed and immobile or half-open and open, without any specific appearance. Spontaneous motor activity is usually absent or mild, with the presence of short-term spasms, such as jerks and/or tremors. There may be an occasional reaction to stimuli.

  • Alert: Eyes open with the presence of a bright look, or eyes closed with clear activity of concentration. Demonstrates attention to the source of stimulation. Being concentrated, the global motor activity is low, and there is a reaction to stimuli.

  • Agitation (includes agitation, irritation, and crying): Eyes can be open, closed, or narrowed. High level of global motor activity with spasms and frequent impulsive movements in the extremities. Occurrence of grumbling, vocalizations or crying.

Specific behaviors

We described the specific oral readiness behaviors based on the characterization of Medeiros(2424 Medeiros AMC. Contato das mãos com a região oral, protrusão de língua e movimentos de sucção em recém-nascidos humanos, a partir da estimulação oro gustativa [tese]. São Paulo: Universidade de São Paulo; 2002.). The oral region ranged lips (red zone), delimited by the red margin, mouth cavity, tongue and mouth cavity floor.

  • Hand over mouth (HOM) - right (RHOM) or left (LHOM): contact of one hand in the oral region; the hand may have been placed or only supported on the oral region; there is no type of suction movement.

  • Hand suction (HS) - right (RHS) or left (LHS): contact of one hand or both with the oral region, simultaneously or alternately, concomitant with the presence of suction movements; the lips are usually open; often rhythmic movements are observed in the buccal region (cheeks) and protruding movements and jaw retraction; the movements observed can occur in an intense or subtle way, at a short or prolonged duration.

  • Suction (SU): occluded or rounded lips; visualization of the retracted angle of the mouth, corresponding to the buccinator muscle action; rhythmic oral movements (cheeks), with or without jaw protrusion and retraction.

  • Tongue protrusion (TP): lips not occluded (separated); visualization of the tongue apex between the upper and lower lips; presence of tongue movement back and forth.

Ethical procedures

This study was approved by the Research Ethics Committee of the Federal University of Sergipe, under No. CAAE 0027.0.107.000-11. Those responsible for the newborns signed the Free and Informed Consent Form (FICF).

Statistical analysis

We described the categorical variables as absolute and relative percentage frequency and the counting variables as means and standard deviations.

When assessing the experiment, we used a mixed generalized linear model with zero inflated negative binomial distribution (2626 Brooks ME, Kristensen K, Benthem KJ, Magnusson A, Berg CW, Nielsen A, et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 2017;9(2):378-400. http://dx.doi.org/10.32614/RJ-2017-066.
http://dx.doi.org/10.32614/RJ-2017-066...
). Dependent variables refer to the number of seconds in which the NB performed the specific behaviors (RHOM, LHOM, RHS, LHS, SU and TP), while independent variables are the CGA (TNB or PTNB) and type of gustatory stimulation (water or sucrose) as fixed effects and stages (BL1, stimulation phase, and BL2), as well as behavioral states (sleep, alertness, and agitation) as random effects.

In all models, at least 90% of test power was achieved(2727 Green P, MacLeod CJ. SIMR: an R package for power analysis of generalized linear mixed models by simulation. Methods Ecol Evol. 2016 Apr;7(4):493-8. http://dx.doi.org/10.1111/2041-210X.12504.
http://dx.doi.org/10.1111/2041-210X.1250...
). We used the level of significance of 5% and the lme4 package of the R Core Team 2020 software to analyze the models.

RESULTS

The group stimulated with water corresponded to 51% of the sample, while the group stimulated with sucrose represented 49%. The TNB and PTNT groups corresponded to 45% and 55%, respectively.

Specific behaviors

In BL1, preterm infants in the sucrose group already had a higher SU time percentage than those in the water group.

At the stimulation stage, PTNBs from the sucrose group had longer RHS, LHS, and SU behaviors than those from the water group. TNBs from the sucrose group, at the same stage, had a higher percentage of time for hand-mouth behaviors – RHOM (5.64) and LHOM (1.46).

In BL2, PTNB in the sucrose group continued to show a higher percentage of SU behavior time than those in the water group. TNB from the sucrose group maintained a higher percentage of RHOM and LHOM time.

Table 1 shows the descriptive statistics of the average time percentage characterization in which the NBs performed each specific behavior, grouped by stage, CGA and stimulus.

Table 1
Characterization of the percentage of specific behavior time per stage, corrected gestational age and stimulus

Behavioral state

In BL1, TNB in the water group already presented longer time range on alert and agitation than those in the sucrose group.

Comparing with the BL1, the comparison between stages indicated higher percentage of alert time (+ 10%) and less sleep time (-14%) in the newborns stimulated with sucrose during the stimulation stage. In addition, PTNBs stimulated with water had lower percentage of agitation time (-6%) at step BL1 for stimulation.

Table 2 shows the descriptive statistics of the average time percentage characterization in which the NBs were in each behavioral state, grouped by stage, CGA, and stimulus.

Table 2
Characterization of the percentage of behavioral state time per stage, corrected gestational age and stimulus

Stimulation and corrected gestational age

In relation to the offered stimulus, significant results were observed regarding LHS and SU, in which the sucrose group had a longer average time than the water group.

As for gestational age, we found that the LHOM time in TNB was shorter than in PTNB (B<1). In turn, the behaviors of RHS, LHS, and SU showed an inverse relationship, since TNB executed these behaviors for a longer time range.

When observing the interaction between stimulus and gestational age, we found significantly less SU and LHS time in the sucrose group comparing with water in TNB versus PTNB. This means that sucrose stimulation in the specific behaviors of SU and LHS was more evident in PTNB.

Table 3 shows the mixed generalized linear model for the number of seconds of specific behavior as a function of corrected gestational age and controlled stimulus for stage and behavioral state.

Table 3
Mixed generalized linear model for the number of seconds of specific behavior as a function of corrected gestational age and controlled stimulus for stage and behavioral state

Behavioral status as a function of stimulus, CGA, and stage

We observed that the TNB had longer sleep time than the PTNB. By comparing TNB and PTNB for the interaction between stimulus and gestational age, we found shorter alert time in the sucrose group than in the water group, that is, sucrose stimulation in the alert state was more evident in PTNB.

Table 4 shows the models involving behavioral status as a function of the stimulus, gestational age (fixed effects) and stage (random effects).

Table 4
Mixed generalized linear model for the number of seconds of behavioral status as a function of corrected gestational age and controlled stimulus for stage

DISCUSSION

The analysis of the results allowed to observe that the gustatory stimuli elicited behaviors related to the oral readiness, both in the TNB and PTNB.

TNBs stimulated with sucrose showed longer time range with hand over mouth (RHOM and LHOM) than those stimulated with water, even after the stimuli ceased (BL2), showing the influence of the sweet on the hand-mouth coordination(1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
). Sucrose had an effect on both sides, but with a higher incidence of behavior on the body right side, indicating manual preference for that side, as reported in the literature(55 Reissland N, Francis B, Aydin E, Mason J, Exley K. Development of prenatal lateralization: evidence from fetal mouth movements. Physiol Behav. 2014 May;131:160-3. http://dx.doi.org/10.1016/j.physbeh.2014.04.035. PMid:24768644.
http://dx.doi.org/10.1016/j.physbeh.2014...
,1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
,1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.).

PTNBs already had a higher frequency of sucking behavior in BL1 even before receiving gustatory stimulation. Even so, sucrose proved to be an elicitor of suction behaviors, not only in line with previous reports in the literature(99 Forestell CA. Flavor perception and preference development in human infants. Ann Nutr Metab. 2017;70(Suppl. 3):17-25. http://dx.doi.org/10.1159/000478759. PMid:28903110.
http://dx.doi.org/10.1159/000478759...
,1010 Ayres C, Ferreira CF, Bernardi JR, Marcelino TB, Hirakata VN, Silva CH, et al. A method for the assessment of facial hedonic reactions in newborns. J Pediatr. 2017 May;93(3):253-9. http://dx.doi.org/10.1016/j.jped.2016.06.011. PMid:27886807.
http://dx.doi.org/10.1016/j.jped.2016.06...
,1212 Mennella JA. Ontogeny of taste preferences: basic biology and implications for health. Am J Clin Nutr. 2014 Mar;99(3):704S-11S. http://dx.doi.org/10.3945/ajcn.113.067694. PMid:24452237.
http://dx.doi.org/10.3945/ajcn.113.06769...
,2828 Murray RD. Savoring sweet: sugars in infant and toddler feeding. Ann Nutr Metab. 2017;70(Suppl. 3):38-46. http://dx.doi.org/10.1159/000479246. PMid:28903112.
http://dx.doi.org/10.1159/000479246...
), but with an increase in this behavior, both in isolated form (SU) and in oromanual coordination (RHS and LHS) during the stimulation, still maintaining an increase in SU after the stimulus supply ceases (BL2). The higher suction frequency for both sides indicates that the preterm newborns population in this study did not have preference for laterality.

It is worth mentioning that for both PTNB and TNB, sucrose was more effective than water at eliciting readiness behaviors for feeding, which corroborates previous research(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,2222 Medeiros AMC, Sá TPL, Alvelos CL, Raposo OFF. Efeitos da estimulação gustativa nos estados comportamentais de recém-nascidos prematuros. Audiol Commun Res. 2013 Mar;18(1):50-6. http://dx.doi.org/10.1590/S2317-64312013000100010.
http://dx.doi.org/10.1590/S2317-64312013...
) and our hypothesis regarding the influence of the sweet taste stimulus on the frequency of readiness behaviors for food, regardless of CGA.

Regarding the behavioral states, the newborns in the sucrose group showed lower percentage of time in the sleep state and higher in the alert state at the stimulation stage, corroborating studies addressing sucrose as eliciting states of greater attention(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.,2222 Medeiros AMC, Sá TPL, Alvelos CL, Raposo OFF. Efeitos da estimulação gustativa nos estados comportamentais de recém-nascidos prematuros. Audiol Commun Res. 2013 Mar;18(1):50-6. http://dx.doi.org/10.1590/S2317-64312013000100010.
http://dx.doi.org/10.1590/S2317-64312013...
). When stimulated with water, PTNBs had a lower percentage of agitation time than BL1, with no significant correlation to sucrose, demonstrating that oral stimulation had an effect on the preterm infants studied here, regardless of the stimulus used, as found in previous research(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
,2222 Medeiros AMC, Sá TPL, Alvelos CL, Raposo OFF. Efeitos da estimulação gustativa nos estados comportamentais de recém-nascidos prematuros. Audiol Commun Res. 2013 Mar;18(1):50-6. http://dx.doi.org/10.1590/S2317-64312013000100010.
http://dx.doi.org/10.1590/S2317-64312013...
).

Regardless of gestational age, stimulation with sucrose provided LHS and SU for a longer time (on average) than water, confirming studies that address the sweet stimulus as eliciting motor responses(99 Forestell CA. Flavor perception and preference development in human infants. Ann Nutr Metab. 2017;70(Suppl. 3):17-25. http://dx.doi.org/10.1159/000478759. PMid:28903110.
http://dx.doi.org/10.1159/000478759...
1212 Mennella JA. Ontogeny of taste preferences: basic biology and implications for health. Am J Clin Nutr. 2014 Mar;99(3):704S-11S. http://dx.doi.org/10.3945/ajcn.113.067694. PMid:24452237.
http://dx.doi.org/10.3945/ajcn.113.06769...
,1717 Barr RG, Quek VSH, Cousineau D, Oberlander TF, Brian JA, Young SN. Effects of intra-oral sucrose on crying, mouthing and hand-mouth contact in newborn and six-week-old infants. Dev Med Child Neurol. 1994 Nov;36(7):608-18. http://dx.doi.org/10.1111/j.1469-8749.1994.tb11898.x. PMid:8034123.
http://dx.doi.org/10.1111/j.1469-8749.19...
,2828 Murray RD. Savoring sweet: sugars in infant and toddler feeding. Ann Nutr Metab. 2017;70(Suppl. 3):38-46. http://dx.doi.org/10.1159/000479246. PMid:28903112.
http://dx.doi.org/10.1159/000479246...
). It is worth emphasizing the importance of this finding, since sucking is an important function already present at birth and serves to guarantee not only breastfeeding, but also to contribute to the newborns’ self-regulating behavior(2929 Lubbe W, Ham-Baloyi W. When is the use of pacifiers justifiable in the baby-friendly hospital initiative context? A clinician’s guide. BMC Pregnancy Childbirth. 2017 Dez;17(1):130. http://dx.doi.org/10.1186/s12884-017-1306-8. PMid:28449646.
http://dx.doi.org/10.1186/s12884-017-130...
).

When comparing TNB and PTNB regarding specific behaviors, we observed that TNB spent less time with LHOM than PTNB, probably because newborns display, in general, more hand behaviors on the right side of the body (RHOM and RHS)(55 Reissland N, Francis B, Aydin E, Mason J, Exley K. Development of prenatal lateralization: evidence from fetal mouth movements. Physiol Behav. 2014 May;131:160-3. http://dx.doi.org/10.1016/j.physbeh.2014.04.035. PMid:24768644.
http://dx.doi.org/10.1016/j.physbeh.2014...
,1111 Medeiros AMC. A existência de “sistema sensório-motor integrado” em recém-nascidos humanos. Psicol USP. 2007 Jun;18(2):11-33. http://dx.doi.org/10.1590/S0103-65642007000200002.
http://dx.doi.org/10.1590/S0103-65642007...
,1818 Medeiros AMC, Leite de Sá TP, Raposo OFF. Relação entre os estados comportamentais do recém-nascido prematuro e a prontidão para mamada. Temas Sobre Desenvolv. 2013;19(105):125-9.), due to their lateral preference, whereas PTNB did not show such preference.

In addition, TNBs spent more time performing RHS, LHS and SU than PTNBs, possibly due to the complexity of this behavior, since sucking hands is more complex than just bringing them to the mouth, demonstrating that TNB are probably more competent in this sense than PTNB.

Sucrose stimulation in the specific behaviors of SU and LHS appeared more clearly in PTNB, as observed in a previous study(11 Medeiros AMC, Alvelos CL, Sá TPL, Barros AD, Raposo OFF. Investigação de um sistema de alimentação em recém-nascidos prematuros a partir de estimulação gustativa. Rev CEFAC. 2014 Jun;16(3):929-40. http://dx.doi.org/10.1590/1982-0216201415912.
http://dx.doi.org/10.1590/1982-021620141...
), since the sweet stimulus proved to be an important elicitor of sucking behaviors(99 Forestell CA. Flavor perception and preference development in human infants. Ann Nutr Metab. 2017;70(Suppl. 3):17-25. http://dx.doi.org/10.1159/000478759. PMid:28903110.
http://dx.doi.org/10.1159/000478759...
,1010 Ayres C, Ferreira CF, Bernardi JR, Marcelino TB, Hirakata VN, Silva CH, et al. A method for the assessment of facial hedonic reactions in newborns. J Pediatr. 2017 May;93(3):253-9. http://dx.doi.org/10.1016/j.jped.2016.06.011. PMid:27886807.
http://dx.doi.org/10.1016/j.jped.2016.06...
,1212 Mennella JA. Ontogeny of taste preferences: basic biology and implications for health. Am J Clin Nutr. 2014 Mar;99(3):704S-11S. http://dx.doi.org/10.3945/ajcn.113.067694. PMid:24452237.
http://dx.doi.org/10.3945/ajcn.113.06769...
,2828 Murray RD. Savoring sweet: sugars in infant and toddler feeding. Ann Nutr Metab. 2017;70(Suppl. 3):38-46. http://dx.doi.org/10.1159/000479246. PMid:28903112.
http://dx.doi.org/10.1159/000479246...
). However, as already mentioned, the right lateral preference in the TNB may have influenced the smaller number of responses of this behavior on the left side.

The results showed that TNB spent more time in a sleep state than PTNB. A previous study reports that TNBs usually sleep 16 to 18 hours a day, which is positive for neurological development. According to the authors, longer sleeping time reflects the crucial role that sleep plays in promoting optimal development, cognition, and behavior for the brain(3030 Grigg-Damberger MM. The visual scoring of sleep in infants 0 to 2 months of age. J Clin Sleep Med. 2016 Mar 15;12(3):429-45. http://dx.doi.org/10.5664/jcsm.5600. PMid:26951412.
http://dx.doi.org/10.5664/jcsm.5600...
).

Sucrose stimulation in the alert state was more evident in PTNB, as observed in previous research, in which this stimulus was effective at keeping the premature infants in a behavioral state considered favorable – alert –, and decreasing the presence of less favorable states – agitation, irritation and crying(2222 Medeiros AMC, Sá TPL, Alvelos CL, Raposo OFF. Efeitos da estimulação gustativa nos estados comportamentais de recém-nascidos prematuros. Audiol Commun Res. 2013 Mar;18(1):50-6. http://dx.doi.org/10.1590/S2317-64312013000100010.
http://dx.doi.org/10.1590/S2317-64312013...
) –, demonstrating a possible calming effect of sucrose(1313 Milbrandt T, Kryscio R, Muchow R, Walker J, Talwalkar V, Iwinski H Jr. Oral sucrose for pain relief during clubfoot casting: a double-blinded randomized controlled trial. J Pediatr Orthop. 2018 Set;38(8):430-5. http://dx.doi.org/10.1097/BPO.0000000000000845. PMid:27636913.
http://dx.doi.org/10.1097/BPO.0000000000...
1515 Stevens B, Yamada J, Ohlsson A, Haliburton S, Shorkey A. Sucrose for analgesia in newborn infants undergoing painful procedures. Cochrane Database Syst Rev. 2016 Jul;(7):CD001069.,1717 Barr RG, Quek VSH, Cousineau D, Oberlander TF, Brian JA, Young SN. Effects of intra-oral sucrose on crying, mouthing and hand-mouth contact in newborn and six-week-old infants. Dev Med Child Neurol. 1994 Nov;36(7):608-18. http://dx.doi.org/10.1111/j.1469-8749.1994.tb11898.x. PMid:8034123.
http://dx.doi.org/10.1111/j.1469-8749.19...
).

Among the limitations of this study, it is worth mentioning that the experiment could not be performed on newborns who were using an orogastric tube at the time of the test, since this circumstance per se would already be configured as an intraoral proprioceptive stimulus.

Further research should be carried out in this scope to expand the profile of the population studied and include different clinical conditions, such as inadequation of neonates regarding the growth pattern for gestational age, or even those who present neurological changes that do not interfere with the risk of oral stimulation.

CONCLUSIONS

This study demonstrated that sucrose is a gustatory stimulus that elicits motor responses at an early age, since it increased behaviors for food readiness in all newborns, regardless of CGA. It can interfere with the behavioral states of newborns, providing a longer sleep time range and a shorter alertness time range, which is important to promote interaction and readiness for food. The influence of sucrose appeared more clearly in preterm infants in the alertness state, demonstrating the stimulus effect when keeping preterm infants in a favorable behavior state.

Our findings are important to deepen the current understanding and develop intervention with neonates regarding the speech-language aspects involved, especially orofacial motricity, thus enabling to expand guidelines for feeding stimulation.

  • Study carried out at Speech and Language Therapy course, Universidade Federal de Sergipe – UFS – São Cristóvão (SE), Brasil.
  • Funding: None.

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    » http://dx.doi.org/10.5664/jcsm.5600

Publication Dates

  • Publication in this collection
    16 Aug 2021
  • Date of issue
    2021

History

  • Received
    01 Sept 2020
  • Accepted
    26 Mar 2021
Academia Brasileira de Audiologia Rua Itapeva, 202, conjunto 61, CEP 01332-000, Tel.: (11) 3253-8711, Fax: (11) 3253-8473 - São Paulo - SP - Brazil
E-mail: revista@audiologiabrasil.org.br