ABSTRACT

OBJECTIVES: to analyze the correlation between oral stimulation, the sucking pattern and feeding performance of premature newborns.
METHODS: systematic review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Statement guidelines. The databases consulted included PubMed-Central, Cielo, LILACS, and via EBSCOHost, with no temporal or language restrictions. The research process was carried out from October to November 2023. The selection, screening, and integration of studies were conducted using the Rayyan^® software, in collaboration with another researcher. Evidence analysis was performed using the Quality Assessment Tool for Quantitative Studies instrument.
RESULTS: 358 articles were found, of which 13 were selected after eliminating duplicates and application of the qualification criteria. Three additional articles were included through reference analysis, totaling a sample of 16 original studies. Evidence levels varied, with one study classified as weak, three as moderate, and twelve as strong. The results obtained demonstrated that oral stimulation improved the sucking pattern and feeding performance, contributing to early hospital discharge.
CONCLUSION: the literature supports that oral stimulation techniques, non-nutritive sucking and Premature Infant Oral Motor Intervention have beneficial effects on the premature newborns' feeding process.

Keywords: Infant premature, Feeding methods, Sucking, Sucking behavior, Deglutition

RESUMO

OBJETIVOS: analisar a relação entre a estimulação oral, o padrão de sucção e o desempenho alimentar de recém-nascidos prematuros.
MÉTODOS: revisão sistemática seguindo as diretrizes do Preferred Reporting Items for Systematic Reviews and Meta-Analyses Statement. Foram consultadas as bases PubMed-Central, SciELO, LILACS e CINA-HL Complete, Cochrane Collection Plus, Nursing & Allied Health Collection e Medic Latina via EBSCOHost, sem restrições temporais ou de idioma. A pesquisa foi realizada entre outubro a novembro de 2023. O processo de seleção, triagem e integração dos estudos foi conduzido no programa Rayyan^®, em colaboração com outro pesquisador. A análise de evidências foi feita através do instrumento Quality Assessment Tool For Quantitative Studies.
RESULTADOS: foram encontrados 358 artigos, dos quai 13 foram selecionados após eliminação de duplicados e aplicação dos critérios de qualificação. Três artigos adicionais foram incluídos pela análise de referências, totalizando uma amostra de 16 estudos originais. O nível de evidência variou de fraco (n=1), moderado (n=3) e forte (n=12). Os resultados obtidos demonstraram que a estimulação oral melhorou o padrão de sucção, o desempenho alimentar e contribuiu para alta hospitalar precoce.
CONCLUSÃO: a literatura apoia que técnicas de estimulação oral, sucção não nutritiva e a Premature Infant Oral Motor Intervention têm efeitos benéficos no processo alimentar de recém-nascidos prematuros.

Palavras-chave: Recém-nascido prematuro, Métodos de alimentação, Sucção, Comportamento de sucção, Deglutição

Introduction
Prematurity refers to all live newborns who are younger than 37 weeks.¹ A premature newborn has an underdeveloped nervous system as a result of neurological immaturity, and for this reason, changes in the coordination of the sucking-swallowing-breathing pattern.² As the sucking pattern is usually reduced, oral motor skills will be compromised and consequently oral feeding can become challenging for these children.²
It is important to note that clinical practice has shown that premature infants do not suddenly start sucking efficiently, and there is a need for preparation and training so that their sucking and swallowing patterns become coordinated. This training period must be constantly evaluated and stimulated, with the aim of preparing the newborn for more robust and effective sucking.³ The proper coordination of sucking, swallowing and breathing is a determining factor in ensuring safe feeding. Compromising any of these three functions can put the newborn at risk, specifically aspiration, pneumonia, oxygen desaturation, apnea and bradycardia.⁴
Due to the use of an alternative feeding route, these newborns often present difficulties and alterations in oro-motor functions, hindering the safe and efficient transition to the oral route.⁵
The stimulation for nutritive and non-nutritive sucking are forms of oral sensorimotor stimulation. The framework for their use is related to the development of the phonoarticulatory organs, which occurs due to the occurrence of muscular pressure during the babies' sucking function.⁶ By performing nutritive or non-nutritive sucking, the newborn will be developing the phonoarticulatory organs properly, thus promoting the correct functioning of the oromotor structures due to the relationship that exists between the stomatognathic system and the other organs and functions.⁷
The technique of non-nutritive sucking with the gloved little finger⁸ is one of the most common routine in the neonatal intensive care units, followed by non-nutritive sucking with a pacifier.⁸ This technique can be used alone or combined with other strategies in specific intervention programs.
The oral stimulation program⁹ can be implemented for this purpose. This program includes 15 minutes of intervention, in which the first 12 minutes consist of stimulating the cheeks, lips, gums and tongue, and the last three minutes consist of non-nutritive sucking on a pacifier commonly used in the nursery.⁹ Oral sensorimotor stimulation in premature newborns accelerates the maturation process of oral reflexes, helping to develop the ability to feed orally in a safe and effective way.¹⁰
In particular, the Premature Infant Oral Motor Intervention (PIOMI) is an oral stimulation program created by Lessen¹¹ that provides (i) assisted movements to activate muscle contraction of the phonoarticulatory organs (ii) against resistance to increase strength.¹¹ Given the difficulties that prematurity brings, it is important to understand how different techniques can facilitate the feeding pattern on premature newborns, since it is essential for them to be able to make the feeding transition in a safe and effective way.
Therefore this study aims to examine the effects of oral stimulation on the feeding performance of premature newborns. The aim is to analyze the relationship among oral stimulation, the sucking pattern and the feeding performance of these newborns.
Methods
This study is of a methodological nature and consists of a systematic review of the literature that aims to analyze the importance of oral stimulation in the performance of the premature newborns' on feeding pattern and sucking. This review has been registered on the International Platform of Registered Systematic Review and Meta-analysis Protocols (INPLASY) under the registration number INPLASY2024100083.
The question of the present study was carried out in PICO format, i.e. Population (P), Intervention (I), Comparator (C) and Outcome (O), considering the question: "What is the importance of oral stimulation (I) compared to the standard procedure (C) in the feeding performance (O) of preterm newborns (P)?". In particular, for the outcome under study (i.e. feeding performance), measures of i) milk transfer rate, ii) overall milk intake volume, iii) feeding performance/sucking pattern, iv) oral feeding initiation time, v) independent oral feeding, vi) effective breastfeeding and vii) early hospital discharge were analyzed.
Eligibility criteria were established for this study, as follows. Regarding the inclusion criteria, primary studies were included with premature newborns who presented feeding difficulties, born between 25-36 weeks of gestation who were stable and did not require mechanical ventilation, subject to oral stimulation programs and non-nutritive sucking. Articles duplicated in the database, letters to the editor, gray literature articles, case reports, secondary reports, studies integrating newborns with primary diagnoses and studies that did not answer the research question were excluded. Articles were not excluded based on the level of evidence.
The search for the present investigation was carried out by two independent researchers through the PubMed Central, SciELO, LILACS databases and a search of the following databases through the EBSCOHost platform: CINA-HL Complete, Cochrane Collection Plus, Nursing & Allied Health Collection and Medic Latina. No time or language restrictions were set. The specific descriptors and search keys for each database are shown in Table 1. Four key terms were used for the search key: speech therapy, premature newborns and sucking pattern. The Medical Subject Headings (MeSH term) "speech therapy" and the natural language term "stimulation" were used for the concept "speech therapy". For "premature newborns", the MeSH term "infant, premature" and the natural language terms "preterm infant" and "infant, preterm" were used. For "sucking pattern", the MeSH terms "sucking behavior", "breast feeding", "feeding behavior" and the natural language terms "breastfeeding", "breast fed" and "wet nursing" were used. The descriptors were combined with Boolean operators AND and OR and proximity operators "" and (). To increase comprehensiveness during the search, no filters were used in the databases (e.g. time period of publication, type of study).
 


Following the literature search, it was necessary to remove duplicates and assess the titles and abstracts of the remaining results, in order to judge whether they should be included. At this stage, the program Rayyan^Ò was used,¹² thus facilitating the organization of the studies and the screening process. This selection was carried out independently by two researchers. Studies that met the inclusion criteria were selected and those that did not fit the topic under study were removed after reading the titles and abstracts. This program also made it possible to obtain basic bibliometric information, helping to reduce bias among researchers, attach full texts, resolve duplicates and justify the exclusion of studies through labeling.¹² In the event of non-consensus, the collaboration of a third researcher was predicted.
Once all the studies that met the previously defined criteria had been included, their bibliographic references were consulted in order to examine possible additional sources of information that had not been detected in the initial search. Subsequently, the studies selected after a consensus meeting were read in full by a researcher and a detailed analysis was carried out.
The selection of studies was described in a flowchart, following the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Statement (PRISMA)¹³ (Appendix 1). The evidence analysis was carried out for each study according to the Quality Assessment Tool For Quantitative Studies.¹⁴ This tool allows the final classification of the quality of studies by assigning sub-classifications (strong, moderate or weak) to a set of six topics: sample representativeness, study design, confounding factors, blinding, data collection and retention (dropouts). An overall classification was determined based on the sub-classifications assigned: strong if there were no weak sub-classifications; moderate if there was one weak sub-classification; weak if there were more than two weak sub-classifications.¹⁴ The results obtained are organized in Table 2, which includes the reference of each one, the types of study, the population, the methodology, the results, the conclusions and the evidence analysis.¹⁴ Table 3 organizes the different outcomes studied at the end of each investigation.
 



 


Results
Figure 1 shows the flowchart that integrates the process of integrating the studies for the present investigation, which contains information on the process of identifying and screening studies. It also shows the reasons for excluding records. The results of the search in the different databases (n=358) were imported into the program Rayyan^Ò. Secondary reports (n=33), case reports (n=11) and those that did not answer the study question (n=231) were then excluded, with the titles first being analyzed and, if there were any doubts, the abstract. Articles which could not be accessed in full were also excluded (n=2). The researchers of these studies were contacted, but no reply was received. As a result, 13 studies were integrated and three were added by analyzing the bibliographical references of the studies already selected, giving a total of 16 articles as a sample of original studies. When the sample of original studies was reviewed with a second researcher, there was total consensus and agreement.
 


Of the 16 studies analyzed, one had a weak level of evidence, three had a moderate level of evidence and 12 were classified as having a strong level of evidence. The evidence analysis is present in all the columns of Table 1. All the integrated studies made comparisons with control groups that were made up of sham (simulated procedures) or standard neonatal care, which refers to the set of practices and interventions carried out to promote the health and well-being of newborns. This care includes medical assistance, monitoring and support for newborns, focusing on the prevention, early diagnosis and treatment of conditions that may threaten their life or development.
The 16 studies selected for this investigation date from between 2002 and 2022, with the majority originating from the United States (Fucile et al.⁹; Fucile et al.¹⁵; Lessen¹¹; Fucile et al.¹⁶), with some from Brazil (Rocha et al.,¹⁷ Costa et al.¹⁸), India (Arora et al.¹⁹; Thakkar et al.,²⁰; Kore and Mathew²¹), Iran (Ghomi et al.²²; Mahmoodi et al.²³; Ostadi et al.²⁴), Luxembourg (Bache et al.²⁵), China (Lyu et al.²⁶), Thailand (Lessen et al.,²⁷), and Spain (Aguilar-Rodríguez et al.²⁸).
As mentioned above, in order to better organize the integrated studies and the results, three tables were drawn up: Table 1 contains the different results of each study and Table 2 presents a compilation of the outcomes studied in all the articles analyzed.
Discussion
Considering that this study aimed to study the importance of oral stimulation in the sucking/feeding process of premature newborns, it should be noted that the vast majority of the articles included showed that the oral stimulation program,¹⁰ non-nutritive sucking⁸ and PIOMI¹¹ had a beneficial effect not only on the feeding performance of premature newborns, but also on independent oral feeding. The studies by Fucile et al.,⁹ Fucile et al.,¹⁵ Rocha et al.,¹⁷ and Lyu et al.²⁶ showed positive effects through the oral stimulation program¹⁰ and non-nutritive sucking. With the intervention of the oral stimulation program alone, the studies by Bache et al.,²⁵ Fucile et al.,¹⁶ Aguilar-Rodríguez et al.,²⁸ and Kore and Mathew²¹ proved that the application of this program brings benefits to premature newborns. Through the implementation of PIOMI, the studies by Lessen,¹¹ Arora et al.,¹⁹ Thakkar et al.,²⁰ Ghomi et al.,²² Lessen et al.,²⁷ and Mahmoodi et al.,²³ demonstrated significant improvements with the use of this program. When interpreting the results of the studies analyzed, more outcomes were visible that are directly related to the programs under study. Thus, in addition to the outcomes initially studied (i.e. improved feeding performance and feeding independence of premature babies), the rate and volume of milk ingested, time to first feeding, breastfeeding rate and early hospital discharge were also analyzed. Therefore, these outcomes will be considered for this discussion.
i)Milk transfer rate
With regard to the milk transfer rate (i.e. the volume of milk ingested in relation to the duration of oral feeding session), one of the results found in the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ showed that the oral stimulation program and non-nutritive sucking had a beneficial effect, causing these newborns to have a higher milk transfer rate precisely because of the improved sucking pattern. On the other hand, in the studies by Costa et al.,¹⁸ Lyu et al.²⁶ and Thakkar et al.,²⁰ this same effect could not be observed and there was no increase in the milk transfer rate. Regarding this relationship, the literature has shown that there is an increase in the rate of milk transfer in newborns who undergo an oral stimulation program, suggesting that these babies are better able to suck more effectively.²⁹ These findings are congruent with the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ which point to a benefit of these techniques.
ii)Volume of milk swallowed
Regarding the increase in the volume of milk swallowed (i.e. the volume consumed as a percentage of the prescribed volume) by premature newborns, the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ Thakkar et al.,²⁰ and Lessen et al.,²⁷ showed favorable results, with a greater amount of milk volume swallowed by babies who received the stimulation program. However, the study by Costa et al.¹⁸ did not show any changes in the volume of milk swallowed by the babies, which may be due to the fact that the experimental group weighed less at the different assessment times than the control group. The literature also attests to the positive relationship between the oral stimulation program and the increase in the volume of milk swallowed by these newborns, which is justified by the improvement in the sucking pattern, allowing the babies to swallow more milk due to stronger and more effective sucking.³⁰ This is in line with the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ Thakkar et al.,²⁰ and Lessen et al.,²⁷ analyzed in this study.
iii)Feeding performance/sucking pattern
With regard to feeding performance/sucking pattern, one of the outcomes to be studied in this study, the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ Rocha et al.,¹⁷ Bache et al.,²⁵ Lyu et al.,²⁶ Arora et al.,¹⁹ Thakkar et al.,²⁰ Ghomi et al.,²² Lessen et al.,²⁷ Ostadi et al.²⁴ and Kore and Mathew²¹ have shown that an oral stimulation program has promising results in relation to the feeding performance and sucking pattern of premature babies. According to the information found in other studies, it was possible to conclude that the feeding performance of these babies improved because the techniques used helped to coordinate the sucking-breathing-deglutition pattern during the different sucks, providing a maturation of the different structures.³¹ This information is in line with the results obtained in the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ Rocha et al.,¹⁷ Bache et al.,²⁵ Lyu et al.,²⁶ Arora et al.,¹⁹ Thakkar et al.,²⁰ Ghomi et al.,²² Lessen et al.,²⁷ Ostadi et al.²⁴ and Kore and Mathew²¹ demonstrating that the stimulation program effectively shows beneficial results in relation to the feeding performance of these premature infants.
iv)Time to start oral feeding
With regard to the time taken to start oral feeding, the studies by Rocha et al.,¹⁷ Ghomi et al.,²² Lessen et al.,²⁷ Mahmoodi et al.²³ and Aguilar-Rodríguez et al.²⁸ and Ostadi et al.²⁴ showed that the stimulation program reduced the time normally required for premature newborns to start oral feeding. This information is in line with the results found in the literature, in particular in the study by Neiva and Leone³² which aimed to investigate and analyze the effects of non-nutritive sucking stimulation on the age of onset of oral feeding in premature newborns, and showed that this technique accelerated the process of starting the first oral feeding. These results are similar to those obtained in the studies by Rocha et al.,¹⁷ Ghomi et al.,²² Lessen et al.,²⁷ Mahmoodi et al.,²³ Aguilar-Rodríguez et al.²⁸ and Ostadi et al.,²⁴ which show that the stimulation program plays an important role in anticipating the first oral feeding of premature babies without the presence of a feeding tube.
v)Independent oral feeding
Independent oral feeding was studied by the authors Fucile et al.,⁹ Fucile et al.,¹⁵ Rocha et al.,¹⁷ Costa et al.,¹⁸ Lessen,¹¹ Bache et al.,²⁵ Lyu et al.,²⁶ Fucile et al.,¹⁶ Thakkar et al.,²⁰ Ghomi et al.,²² Mahmoodi et al.²³ and Aguilar-Rodríguez et al.²⁸ who obtained the results of earlier total oral feeding by premature newborns who benefited from the stimulation program. However, Costa et al.¹⁸ and Bache et al.²⁵ who also studied this factor, obtained different results, and there were no differences in the time needed to transition from tube feeding to independent oral feeding. According to the literature, as can be seen in the study by Pereira et al.³³ which aimed to assess the effect of the oral stimulation program on oral feeding performance and the transition time from the tube to total oral intake, this program showed important results with regard to the time needed to make the transition from the tube to independent oral feeding, with a reduction in time having been demonstrated in this study. In this way, the studies by Fucile et al.,⁹ Fucile et al.,¹⁵ Rocha et al.,¹⁷ Lessen,¹¹ Lyu et al.,²⁶ Fucile et al.,¹⁶ Thakkar et al.,²⁰ Ghomi et al.,²² Mahmoodi et al.,²³ and Aguilar-Rodríguez et al.²⁸ are supported by the results obtained in the research by Pereira et al.³³ in which the oral stimulation program revealed that babies who were submitted to this technique showed a reduction in the transition time between the feeding tube and independent oral feeding. This may be related to the improvement in the sucking pattern of premature newborns which, because it is more efficient, allows babies to make the transition from the feeding tube to independent oral feeding sooner.
vi)Breastfeeding rates
With regard to breastfeeding rates, Bache et al.²⁵ and Fucile et al.¹⁶ found that the oral stimulation program helped to improve breastfeeding rates. In this context, the study by Balci et al.³⁴ which aimed to understand the benefits of oromotor stimulation in relation to the transition to breastfeeding, concluded that the oral stimulation program has beneficial effects on feeding skills and the transition to breastfeeding in premature newborns. These data are in line with the results obtained in the studies by Bache et al.²⁵ and Fucile et al.,¹⁶ demonstrating once again that oral stimulation of babies provides a number of benefits.
vii) Early hospital discharge
Early hospital discharge was one of the outcomes studied in the different studies analyzed in this investigation. It should be noted that this result is linked to the different results studied so far, since hospital discharge is directly related to oral feeding independence and also to feeding performance.In this way, different authors have studied this factor, Rocha et al.,¹⁷ Arora et al.,¹⁹ Fucile et al.,¹⁶ Thakkar et al.,²⁰ Ghomi et al.,²² Mahmoodi et al.²³ and Aguilar-Rodríguez et al.²⁸ showing that the oral stimulation program has positive effects on hospital discharge, and where the newborns studied were discharged earlier than those who were not subjected to this technique. Authors such as Song et al.³⁵ reported that newborns who had the oral stimulation program as an intervention had fewer days in hospital than the control group who did not have any type of intervention. However, in the studies by Fucile et al.,⁹ Bache et al.²⁵ and Lyu et al.²⁶ the same results were not found, showing that babies who underwent the oral stimulation program had no differences in the length of stay until hospital discharge. These results may be due to the fact that the experimental group studied had a lower birth weight, which may have biased the effects.According to Medeiros et al.,³⁶ more premature newborns with lower birth weights stay in hospital longer because they need more care and specific interventions.
Thus, after analyzing the results and comparing them with the literature, we can highlight a beneficial effect of the oral stimulation program in improving the feeding performance of premature newborns and the early transition between tube and total oral feeding, information that answers the initial question of this research. Newborns submitted to this program show improvements related to feeding, which is decisive for their development and growth.
Study limitations
It is important to recognize some limitations regarding this work, especially those inherent to primary studies. Some methodological weaknesses (i.e. small samples, variability in the type of control group) influenced the analysis of the evidence. In addition, there were difficulties related to the heterogeneity of the studies which made it difficult to synthesize the data, especially as the analysis measures varied significantly. As an example of this factor, it can be seen that the sample size varied from 19 to 112 premature newborns and their characteristics were not homogeneous, namely in terms of gestational age and birth weight. Another limitation observed was the time and frequency of administration of the different stimulation techniques. In some studies it was administered for five minutes once a day, while in others it was administered more times a day. In some studies, the intervention was carried out for seven days, while in others, it was prolonged until the baby began to feed himself or herself orally. It should also be noted that when interpreting the outcomes of the studies, the technique used was not always the same, and it was possible to verify the use of oral stimulation, PIOMI and non-nutritive sucking. This heterogeneity made it difficult to carry out a more comprehensive analysis and generalize the results found. There were no studies excluded because they were in a language not mastered by the researchers, so it is considered that there was no risk of language bias.
Conclusion
The literature supports the notion that oral sensorimotor stimulation has beneficial effects on the feeding process of premature newborns. This study underlines its relevance to clinical practice by demonstrating that oral sensorimotor stimulation is associated with an improvement in feeding patterns and promotes autonomy in newborns, which supports the recommendation to implement it in neonatal units. In addition, the results indicate a trend towards a reduction in the length of stay, which could contribute to a reduction in the costs associated with managing neonatal care services. The combination of different techniques could enhance the therapeutic effect in terms of the feeding transition, but more studies are needed to consolidate this statement.
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Authors' contribution: Figueiredo IF: conceptualization, data collection and analysis, research, visualization and writing of the manuscript. Grilo M: supervision, validation and revision of the manuscript. Campos SG: data collection and analysis, revision of the manuscript. Rodrigues IT: project management, methodology, supervision, validation and revision of the manuscript. All the authors have approved the final version of the article and declare no conflict of interest.

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Received on April 22, 2024
Final version presented on November 11, 2024
Approved on December 13, 2024

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Associated Editor: Raphael Perrier-Melo