Effects of implementing non-nutritive sucking on oral feeding progression and outcomes in preterm infants: A systematic review and meta-analysis

Shuliang Zhao; Huimin Jiang; Yiqun Miao; Wenwen Liu; Yanan Li; Yuanyuan Zhang; Aihua Wang; Xinghui Cui

doi:10.1371/journal.pone.0302267

. 2024 Apr 16;19(4):e0302267. doi: 10.1371/journal.pone.0302267

Effects of implementing non-nutritive sucking on oral feeding progression and outcomes in preterm infants: A systematic review and meta-analysis

Shuliang Zhao ^1,^2,^‡, Huimin Jiang ^2,^‡, Yiqun Miao ³, Wenwen Liu ⁴, Yanan Li ², Yuanyuan Zhang ², Aihua Wang ^2,^*, Xinghui Cui ^1,^*

Editor: Mona Nabulsi⁵

PMCID: PMC11020483 PMID: 38626172

Abstract

Background

Preterm infants have imperfect neurological development, uncoordinated sucking-swallowing-breathing, which makes it difficult to realize effective oral feeding after birth. How to help preterm infants achieve complete oral feeding as soon as possible has become an important issue in the management of preterm infants. Non-nutritive sucking (NNS), as a useful oral stimulation, can improve the effect of oral feeding in preterm infants. This review aimed to explore the effect of NNS on oral feeding progression through a meta-analysis.

Methods

We systematically searched PubMed, CINHAL, Web of Science, Embase, Cochrane databases, China’s National Knowledge Infrastructure (CNKI), Wanfang and VIP database from inception to January 20, 2024. Search terms included ’non-nutritive sucking’ ’oral feeding’ and ’premature.’ Eligibility criteria involved randomized controlled studies in English or Chinese. Studies were excluded if they were reviews, case reports, or observational studies from which valid data could not be extracted or outcome indicators were poorly defined. The meta-analysis will utilize Review Manager 5.3 software, employing either random-effects or fixed-effects models based on observed heterogeneity. We calculated the mean difference (MD) and 95% confidence interval (CI) for continuous data, and estimated pooled odds ratios (ORs) for dichotomous data. Sensitivity and publication bias analyses were conducted to ensure robust and reliable findings. We evaluated the methodological quality of randomized controlled trials (RCTs) utilizing the assessment tool provided by the Cochrane Collaboration.

Results

A total of 23 randomized controlled trials with 1461 preterm infants were included. The results of the meta-analysis showed that NNS significantly shortened time taken to achieve exclusive oral feeding (MD = -5.37,95%CI = -7.48 to-3.26, p<0.001), length of hospital stay(MD = -4.92, 95% CI = -6.76 to -3.09, p<0.001), time to start oral feeding(MD = -1.41, 95% CI = -2.36 to -0.45, p = 0.004), time to return to birth weight(MD = -1.72, 95% CI = -2.54 to -0.91, p<0.001). Compared to the NNS group, the control group had significant weight gain in preterm infants, including weight of discharge (MD = -61.10, 95% CI = -94.97 to -27.23, p = 0.0004), weight at full oral feeding (MD = -86.21, 95% CI = -134.37 to -38.05, p = 0.0005). In addition, NNS reduced the incidence of feeding intolerance (OR = 0.22, 95% CI = 0.14 to 0.35, p<0.001) in preterm infants.

Conclusion

NNS improves oral feeding outcomes in preterm infants and reduces the time to reach full oral feeding and hospitalization length. However, this study was limited by the relatively small sample size of included studies and did not account for potential confounding factors. There was some heterogeneity and bias between studies. More studies are needed in the future to validate the effects on weight gain and growth in preterm infants. Nevertheless, our meta-analysis provides valuable insights, updating existing evidence on NNS for improving oral feeding in preterm infants and promoting evidence-based feeding practices in this population.

Introduction

Preterm birth, defined as delivery before 37 weeks of gestation, poses a significant global health burden and is recognized as a primary risk factor for children mortality under the age of five [1, 2]. Preterm birth is linked to a spectrum of adverse short- and long-term outcomes, including compromised health and growth during infancy, intellectual and psychiatric disabilities later in life, and an increased risk of chronic diseases developing at an earlier age [3]. The implications of preterm birth extend beyond the initial period following birth and can have lasting impacts on the individual’s overall well-being across their lifespan. Oral feeding and swallowing problems in preterm infants are common medical problems in neonatal intensive care units (NICUs) and families of preterm infant [4]. Preterm birth presents many challenges to infants, including neurodevelopmental immaturity, physiological instability, and disturbed behavioral states [5, 6]. Preterm infants are prone to oral feeding difficulties due to delayed development of oral motor skills and poor suck-swallow-breathe coordination [5–7]. In addition, sucking and swallowing dysfunction in preterm infants affects the availability of nutrients and may affect their growth, development and neurological function [8, 9]. The transition from tube-feeding to full oral feeding is a huge challenge for infant caregivers [10]. Early difficulties with oral feeding can affect the ability of preterm infants to achieve independent oral feeding, prolong hospitalization, and cause long-term feeding problems such as malnutrition, growth retardation, and cognitive deficits [5, 11, 12]. Therefore, providing optimal nutritional feeding support for preterm infants, improving sucking and feeding behaviors in infants less than 30 weeks of age, and increasing the ability to feed independently through the mouth are key to the early care and survival of preterm infants [13].

Non-nutritive sucking (NNS) and nutritive sucking (NS) serve as indices of an infant’s oral motor skills and feeding behavior [14]. The Neonatal Oral-Motor Assessment Scale (NOMAS) is an instrument utilized for appraising the oral motor abilities of infants [15]. By using the NOMAS scale, healthcare professionals can identify potential oral motor problems in infants and provide appropriate intervention and support. NNS refers to a pacifier is placed in an infant’s mouth to increase sucking action, but there is no milk or other fluid intake [16]. NNS creates an oral feeding experience and promotes self-organization and soothing. Oral feeding not only necessitates the components of NNS but also requires suck–swallow–breathe coordination to manage a bolus for consumption [17]. Numerous studies have demonstrated that NNS offers clinical advantages, such as enhancing feeding performance and reducing the duration of hospital stays, and accelerating the transition to oral feeding [18, 19]. Effective NNS interventions not only decrease the incidence of adverse events like oxygen desaturation, apnoea, and bradycardia but may also lessen long-term issues such as feeding or eating aversion [20].

The meta-analysis by Schwartz et al. [21] in 1987 indicated that non-nutritive sucking shortened the time to first bottle feed and reduced hospital stay duration. Both the systematic reviews by Pinelli et al. [22] in 2005 and Barlow et al. [10] in 2008 concurred that NNS could enhance feeding skills in preterm infants and reduce hospitalization time. Foster et al.’s [23] meta-analysis in 2016 demonstrated significant effects of NNS on the transition from tube to full oral feeding, from the start of oral feeding to full oral intake, and on hospital stay duration. Despite a consensus reached by previously published meta-analyses on the promotion of feeding performance in preterm infants through NNS, numerous randomized controlled trials have been conducted in recent years. Therefore, we decided to carry out a more comprehensive and systematic literature review and meta-analysis. The objective of our meta-analysis was to examine the effects of implementing NNS versus no NNS on the initiation of oral feeding, the attainment of full oral feeding, hospital stay duration, and weight progression in preterm infants. This study aimed to synthesize existing evidence to provide an updated understanding of the efficacy of NNS interventions in neonatal intensive care units (NICUs).

Materials and methods

Systematic search and strategy

The review protocol was developed using the Cochrane Handbook for Systematic Reviews of Interventions. Our meta-analysis was conducted according to the preferred reporting items in the guide of systematic review and meta-analysis (PRISMA) [24]. The PRISMA checklist is presented in S1 Checklist. A comprehensive search was performed in MEDLINE (via PubMed), CINHAL, Web of science, Embase, Cochrane Library, CNKI, VIP and Wanfang databases to identify randomized controlled trials (RCT) from inception to January 20, 2024. The following search terms were used:("Sucking Behavior" OR "Pacifiers" OR (non-nutritive AND suck*) OR (non-nutritive sucking) OR (Non-nutritional sucking) OR pacifier OR dummy OR soother OR nipple) AND ("Infant, Newborn" OR "Infant, Premature" OR newborn OR neonate OR neonatal OR premature OR (very low birth weight) VLBW OR (low birth weight) LBW OR (extremely low birth weight) ELBW) AND (randomized controlled trial OR controlled clinical trial OR RCT). Detailed search strategies for each database are shown in S1 Table. Only research involving human beings is included in the selection. Moreover, language limitations are English or Chinese. Our meta-analysis was registered with the PROSPERO database (CRD42023457646).

Inclusion and exclusion criteria

Studies included in this systematic review and meta-analysis must meet the following inclusion criteria: ① Preterm infants with gestational age < 37 weeks and birth weight < 2500g; ② Randomized controlled studies; ③ The language is published in Chinese or English; ④Preterm infants in the intervention group received NNS (The intervention can occur before, during or after gavage feeding. NNS involving the use of a pacifier or nipple.) and preterm infants in the control group were implemented on routine feeding. ⑤At least one of the parameters was included in the outcome measures: Time taken to achieve exclusive oral feeding, Length of hospital stay, Time to start oral feeding, Weight of discharge, Weight at full oral feeding, Time to return to birth weight, Gastrointestinal complications. Time taken to achieve exclusive oral feeding was defined as when the infant ingests all nutrient volumes in a 24hour period without any gavage [25]. Length of hospitalization is described as the number of days from admission to hospital discharge [26]. Time to start oral feeding is defined as transition from gavage feeding to oral feeding, measured in days [27]. Weight of discharge is described as infant’s weight on discharge from hospital, measured in grams [28]. Weight at full oral feeding is described as infant’s weight at full oral intake, measured in grams [29]. Time to return to birth weight is described as the time it takes for a newborn to lose weight after birth and then gradually return to its birth weight, measured in days [30]. Feeding intolerance (FI) is a disorder of milk digestion after enteral feeding, resulting in abdominal distension, vomiting and gastric retention [27], and the diagnostic criteria are based on the Clinical Guidelines on Feeding Intolerance in Preterm Infants [31], with the incidence rate of FI serving as the unit of measurement.

Any study that met the exclusion criteria was excluded from the systematic review and meta-analysis: ① Reviews, case reports, observational studies or animal trials. ② Full text was unavailable ③ Studies with insufficient information for extraction data ④ Unclear or inappropriate definition of exposure/results ⑤ NNS was implemented in the control group.

Data extraction

Two researchers (ZSL and JHM) screened through the literature independently and completed the extraction of data. If there is a disagreement, a third researcher (MYQ) should be called in to adjudicate. Initial screening was done first by reading the title and abstract, followed by selecting the final compliant literature by reading the full text. The extracted information includes the following aspects: first author’s name, year of publication, country, sample size, details of the intervention, and the data of outcome indicators. If the units of the outcome indicators in the study are inconsistent, they should be converted to harmonized units prior to subsequent processing.

Methodological quality assessment

We assessed the methodological quality of RCTs using the Cochrane risk of bias tool [32], which included seven evaluation items: sequence generation, allocation concealment, blinding of participants, outcome evaluator, incomplete outcome data, and selective outcome reporting. The studies were evaluated for unclear, low or high risk of bias. In addition, we entered the assessment data into Cochrane Review Manager software (Revman version 5.3, Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, Denmark) to obtain a risk of bias assessment table. This was done independently by two assessors (LWW and LYN), and when disagreements arose, they were resolved in consultation with a third researcher (ZSL)until agreement was reached.

Data synthesis and analysis

The data was analyzed by Review Manager 5.3 software. The mean difference (MD) and confidence interval (CI) of 95% were calculated for continuous data, while the pooled odds ratios (ORs) and confidence interval (CI) of 95% were estimated for dichotomous data. Heterogeneity was assessed by using I² statistics. Random-effects models were employed in instances where there was substantial heterogeneity among the studies (I² > 50%), whereas fixed-effects models were utilized when the heterogeneity was low (I² ≤50%) [33]. Sensitivity analysis was conducted by changing the analytical model, i.e., selecting the opposite model according to the original analytical model and conducting the combined analysis of effect sizes again. If the results of the two models were consistent, it indicated that the sensitivity was lower, suggesting that the results of the meta-analysis were stable, and vice versa, suggesting that the sensitivity was higher and the results of the meta-analysis were unstable. After individual studies were sequentially excluded, the data were reanalyzed and sensitivity analyses were performed by comparing the excluded results with the original results. Subgroup analyses were used when necessary to address heterogeneity. Funnel plot was performed to evaluate publication bias. p < 0.05 was considered to be statistically significant.

Results

Search results

The initial search yielded 3238 potentially eligible records for eight databases: PubMed (n = 367), EMBASE (n = 339), CINAHL (n = 169), Web of Science (n = 177), Cochrane Library (n = 671), CNKI (n = 349), Wanfang database (n = 708) VIP (n = 458). Following the removal of 1385 duplicate records, a total of 1,853 unique records were assessed. Based on title and abstract screening, 72 studies were selected for full-text review. At this stage, 44 studies were excluded due to various reasons: being reviews, case reports, conference abstracts, animal trials (n = 30), absence of full text (n = 3), or having unclear or inadequate outcome definitions (n = 11). Twenty—eight studies [19, 26–30, 34–55] were identified for inclusion in the systematic review (qualitative synthesis). Four studies [51–54] did not meet our inclusion criteria because the control preterm infants underwent breast or pacifier NNS; data could not be extracted from one additional study [55], so only 23 studies were included in the meta-analysis. The PRISMA flow diagram in Fig 1 shows the study selection process.

Table 1 shows the detailed characteristics of the included literature. These articles included were published from 1982 to 2023. Ten studies [26, 27, 34–41] were conducted in China, three studies [42–44] in the United States, three studies [45–47] in Iran, five studies [28, 30, 48–50] in Turkey, and one each in Canada [29] and Brazil [19]. Figs 2 and 3 depict the risk-of-bias assessment in minute detail. Only six studies [19, 26, 45–47, 50] showed a low risk of bias, and seventeen studies [27–30, 34–44, 48, 49] showed a higher risk of bias. Because it is difficult to implement double-blinding for NNS implementation, only six [19, 26, 45–47, 50] of the included papers were better blinded.

Table 1. Characteristics of the included studies.

Study	Year	Country	Number		Intervention		Outcomes
Study	Year	Country	NNS	Control	NNS group	Control group	Outcomes
Shaki [45]	2022	Iran	50	50	Sucking on a pacifier 3 times/day followed by gavage for ten days of intervention.	routine ward care	①②③
Ostadi [46]	2021	Iran.	15	15	provided with NNS twice a day, for 10 days during two consecutive weeks	not provided with any intervention	①②③
Say [30]	2018	Turkey	45	45	Use the pacifiers for 15 minutes before and after feeding, 4 times/day.	not provided with any intervention	①②④⑥⑦
Fucile [29]	2018	Canada	16	15	The intervention was a 15-minute program consisting of 5 minutes of preparatory oral stimulation of the cheeks and lips, 5 minutes of tongue exercises, and 5 minutes of NNS. 1x/day for 10 days.	15 minutes of pseudo-intervention	①②⑤
Kaya [49]	2017	Turkey	34	36	Sucking 3 times a day to soothe	Not using pacifiers	②③④⑤
Asadollahpour [47]	2015	Iran	11	11	NNS 3 times/day for 15 minutes each time. Place little finger in infant’s mouth and stroke palate for 5 min/times to elicit sucking.	pseudo-intervention	①②④
Zhang [34]	2014	China	25	27	Suck on the pacifier 7–8 times/day for 5 minutes.	not provided with any intervention	①②③⑤
Yildiz [48]	2012	Turkey	30	30	3x/day sucking on a pacifier until oral feeding is initiated	Routine gavage feeding without NNS	①②④
Rocha [19]	2007	Brazil	49	49	NNS 15min/dose for 10 days until oral feeding is initiated	15 minutes of pseudo-intervention	①②③④⑤
Lau [42]	2012	USA	25	23	NNS, 15 minutes/day, 5 days per week.	Routine feeding care	①②③④
Field [43]	1982	USA	30	27	infants in the treatment group were given a pacifier during all tube feedings.	Control infants were tube-fed only until oral feeding	②③
Bernbaum [44]	1983	USA	15	15	Infants in the intervention group were given rubber nipples for NNS during the entire feeding process	Control infants were tube-fed only until oral feeding	①②
Xu [27]	2022	China	57	57	Breast milk olfactory stimulation combined with NNS.	Routine feeding care	①②③ ④⑦
Feng [35]	2022	China	44	46	Early swallowing function training combined with NNS	Routine feeding care	①③⑦
Ling [36]	2008	China	26	21	NNS was given before each nasogastric tube feeding and sucked for 10min every 2-3h/time.	No NNS	②③⑥⑦
Zhang [37]	2003	China	22	21	NNS every 3h with 10min sucking for 2 weeks.	No NNS	②③⑥
Yue [38]	2003	China	18	20	Preterm infants were given a non-porous rubber nipple to suck for 5 min before, during and after each nasogastric tube feeding for 2 weeks.	No NNS	③⑥⑦
Ma [39]	2019	China	43	43	NNS was given for 5 min before each feeding until the preterm infant was able to complete 8 sucks/d for 3 h/suck for 7 d of continuous intervention.	No NNS	①②
Jiang [40]	2009	China	50	48	Preterm infants were given a non-porous rubber nipple to suck for 5 min before, during and after each feeding, 7–8 times/24h, for a period of 1 week.	Routine gavage feeding without NNS	③⑥⑦
Kang [41]	2009	China	36	36	Sucking on a non-porous rubber nipple for 10 min before each feeding, 8 times/d.	Routine gavage feeding without NNS	③⑥⑦
Lyu [26]	2014	China	32	31	Implemented an oral stimulation program consisting of 12 minutes of oral stimulation and 3 minutes of NNS. administered 15–30 minutes before feeding, once a day.	Routine feeding care in the NICU	①④⑤⑥
Berber Çiftci [50]	2024	Turkey	47	47	NNS was continued until discharge for 5 days a week, once a day, until transition from tube feeding to full oral feeding.	Routine feeding care	④⑤
Calik [28]	2019	Turkey	14	14	Using a pacifier, each feeding lasts about 10 minutes and continues until complete oral feeding.	not given the pacifiers	①②④
Li [51]	2023	China	74	74	Non-nutritive breast sucking once a day, 5 min each time, and sucking pacifier for 5 min before each tube feeding.	Suck pacifier for 5 min before each tube feeding	①
John [52]	2019	India	4	5	standard care and suckle on the mother’s emptied breast for 5 to 10 minutes 3 times a day	Use fingers for NNS	②④
Khodagholi [53]	2018	Iran	16	16	NNS paired with olfactory stimuli was administered during the initial 5 minutes of each gavage feeding, thrice daily for 10 days	NNS was administered as in the intervention group with untreated cotton pads	③④
Fucile [54]	2021	Canada	16	17	Empty Breast Group NNS, once a day for 15 min	For the NNS on a pacifier Group, once a day for 15 min	①②③④⑤
Kamhawy [55]	2014	Egypt	23	24	Placed pacifiers in preterm infants’ mouths for 15 minutes of NNS around feeding times, NNS for four consecutive feedings per day for the total of 10 continuous days.	Not using pacifiers	③④

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Note: NNS: Non-nutritive sucking

①Time taken to achieve exclusive oral feeding(days) ②Length of hospital stay(days) ③Time to start oral feeding(days) ④Body weight of discharge(g) ⑤Weight at full oral feeding (g) ⑥Time to return to birth weight(days) ⑦ Feeding intolerance

Meta analysis results

Primary outcomes

Time taken to achieve exclusive oral feeding

Time taken to achieve exclusive oral feeding(days) was included as an outcome between the two groups in fifteen studies [19, 26–30, 34, 35, 39, 42, 44–48] that involved 942 premature infants. We observed that the time to transition to full oral feeding in the NNS group was significantly shorter compared to the control group (MD = -5.37,95%CI = -7.48 to -3.26, p<0.001) (Fig 4). Heterogeneity between studies was high (I² = 93%, p < 0.001), so a random-effect model was used.

Length of hospital stay

Seventeen studies [19, 27–30, 34, 36, 37, 39, 42–49] involving 1006 premature infants examined the effect of NNS on length of hospital stay and contributed data to the meta-analysis. Meta-analysis showed a statistically significant shorter length of hospital stay for infants in the NNS compared to the control infants (MD = - 4.92, 95% CI = -6.76 to -3.09, p<0.001). Significant heterogeneity existed among these studies (I² = 83%, p<0.001).Subgroup analyses was performed based on gestational age of preterm infants (Fig 5). Heterogeneity was significantly reduced in preterm infants with gestational age >33 weeks (I² = 0%, p = 0.94), and statistical differences between the NNS and control groups remained after grouping.

Time to start oral feeding

Fourteen studies [19, 27, 34–38, 40–43, 45, 46, 49] involving 957 premature infants included time to start oral feeding as an outcome. Compared to the control group, we found a statistically significant reduction in transition from gavage to start oral feeding in the NNS group (MD = -1.41, 95% CI = -2.36 to -0.45, p = 0.004) (Fig 6), and there was greater heterogeneity (I² = 59%, p = 0.003). Heterogeneity was reduced after one article [42] was removed from the sensitivity analysis (I² = 40%, p = 0.07).

Fig 6 — Forest plot for time to start oral feeding.

The secondary outcomes

Weight of discharge

Ten studies [19, 26–28, 30, 42, 47–50] including 687 patients were included to assess weight of discharge. The result of random-effect model demonstrated that there was not a significant difference in weight at discharge between the two groups (MD = -22.61, 95% CI = -84.92 to -39.69, p = 0.48). Heterogeneity was significantly reduced after excluding two articles [28, 47] from the sensitivity analysis (I² = 0%, p = 0.45). This adjustment revealed a statistically significant difference between the two groups (MD = -61.10, 95% CI = -94.97 to -27.23, p = 0.004) (Fig 7).

Time to return to birth weight

Time to return to birth weight was included as an outcome between the two groups in seven studies [26, 30, 36–38, 40, 41] that involved 451 infants. Compared to the control group, preterm infants in the NNS group had a shorter time to return to birth weight (MD = -1.72, 95% CI = -2.54 to -0.91, p<0.001) (Fig 8). Significant heterogeneity existed among these studies (I² = 51%, p = 0.06), so the random-effect model was used.

Weight at full oral feeding

Six studies [19, 26, 29, 34, 49, 50] involving 408 premature infants reported the weight at full oral feeding as an outcome. The meta-analysis revealed a statistically significant difference between the two groups, with preterm infants in the NNS group exhibiting reduced weight as compared to control group (MD = -86.21, 95% CI = -134.37 to -38.05, p = 0.0005) (Fig 9). There was no significant heterogeneity between these studies (I² = 0%, p = 0.87), so a fixed-effects model was used.

Feeding intolerance

Seven studies [27, 30, 35, 36, 38, 40, 41] involving 549 premature infants reported the feeding intolerance as an outcome. According to our meta-analysis, feeding intolerance in preterm infants were significantly less in the NNS group than in the control group(OR = 0.22, 95% CI = 0.14 to 0.35, p<0.001) (Fig 10). There was no significant heterogeneity between these studies (I² = 0%, p = 0.86), so a fixed-effects model was used.

Sensitivity analysis and publication bias

Sensitivity analysis by converting the effect sizes of the fixed-effects model and the random-effects model to each other revealed that the differences in the combined effect sizes of the two were small, indicating that the results of the meta-analysis were generally stable (Table 2). In addition, the source of heterogeneity was further explored using a study-by-study approach to exclude individual studies. We drew funnel plots for the indicators of the number of 10 or more articles included in the literature and evaluated the publication bias. The results showed that the funnel plots were all largely symmetrical, with no obvious publication bias (S1 Fig).

Table 2. Results of sensitivity analysis.

Outcome indicator	Fixed effect model OR(95%CI)	random effect model OR(95%CI)
Time taken to achieve exclusive oral feeding	-5.91 (-4.73, -3.64)	-5.37 (-7.48, -3.26)
Length of hospital stay	-4.90 (-5.49, -4.32)	-4.92 (-6.76, -3.09)
Time to start oral feeding	-1.39 (-1.88, -0.90)	-1.41 (-2.36, -0.45)
Weight of discharge	-61.10 (-94.97, -27.23)	-61.10 (-94.97, -27.23)
Weight at full oral feeding	-86.21 (-134.37, -38.05)	-86.21(-134.37, -38.05)
Time to return to birth weight	-1.67 (-2.17, -1.17)	-1.72 (-2.54, -0.91)
Feeding intolerance	0.22 (0.14, 0.35)	0.22 (0.14, 0.35)

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Discussion

Recent investigations have demonstrated that NNS not only enables nasogastric tube-fed preterm infants to transition to oral feeding as soon as possible, but also has a significant effect on both behavioral patterns and growth and development of preterm infants [53, 56]. Antecedent study has identified the advantages of NNS in improving sucking skills, shortening transition to full breastfeeding, and time to hospital discharge in preterm infants [49]. It has also been shown that the use of pacifiers can negatively affect the health of infants and lead to nipple confusion [57]. At the same time, NNS provided by a pacifier might elicit different physiological, pharyngeal, and esophageal motility events, potentially affecting gastroesophageal reflux [58]. Therefore, the present study conducted a more comprehensive and systematic meta-analysis aimed at investigating the impact of NNS on the effectiveness of oral feeding in preterm infants. Infants in the NNS group demonstrated a significantly reduced duration necessary to achieve exclusive oral feeding, a shorter length of hospital stay, an earlier commencement of oral feeding, and a quicker recovery to birth weight when compared to the control group. Preterm infants in the NNS group weighted less at hospital discharge and at full oral feeding. In addition, this review demonstrated that NNS reduced the incidence of feeding intolerance in preterm infants.

First of all, our meta-analysis found that the premature infants in NNS group had significantly shorter time taken to reach exclusive oral feeding and time to start oral feeding than those in the control group, which was consistent with the Cochrane analysis of Foster et al. [23]. Preterm infant perioral and oral receptors are highly sensitive to stimulation, mechanical stimulation of the lips or tongue can cause a non-specific reflex in the orbicularis oris muscle, thus initiating sucking behavior [59]. The sensory experience generated by NNS can trigger sucking in preterm infants through the input-feedback mechanism of the central pattern generator (CPG), prompting an increase in the number of active sucks, a faster rate of sucking, an increase in the negative pressure of sucking, and a shortening of the stopping time, thus promoting the maturation of the sucking reflex [59]. In addition, NNS motor training of preterm infants’ oral muscles promotes the coordination of sucking, swallowing, and respiration, thus accelerating the transition from tube-feeding to transoral feeding [56]. The meta-analysis by Tolppola et al. [60] in 2022 was also in agreement with our findings, confirming the reduction in time from gavage to total mouth feeding in preterm infants in the NNS group, and suggesting that the use of NNS in hospitalized preterm infants is beneficial and should be carried out in clinical practice.

Adequate nutrition increases the rate of development of premature infant bodies, leading to shorter hospital stays. Consistent with the results of a previous meta-analysis [10, 21, 22], our study demonstrates that NNS significantly reduces the length of hospitalization for preterm infants. Say et al. [30], Kaya et al. [49] and Shaki et al. [45] studies also showed that preterm infants in the NNS group were discharged earlier, and these results are consistent with the present study. Analyzing the reasons, this may be related to the fact that NNS not only promotes the maturation of sucking reflex in preterm infants and shortens the time from tube feeding to complete oral feeding [61], but also prompts hepatic, biliary and pancreatic activities through the vagus nerve, regulates gastrointestinal peptide levels, and stimulates gastrointestinal growth and development and maturation, which in turn improves feeding tolerance in preterm infants and shortens the length of hospital stay [37]. Clinical experience has demonstrated that the length of hospitalization of preterm infants is largely dependent on the time taken to achieve complete oral feeding. However, the reality is that when a preterm infant is discharged from the NICU after a stay in the NICU is related to a number of complex factors, such as: stable weight gain, mature and stable cardiorespiratory function as well as assessment of nutritional risk, neurodevelopmental and neurobehavioral assessments, and more [62]. It is also important to ensure that the family and community health care system is adequately prepared to care for the infant safely outside of the hospital after discharge.

Our study showed that preterm infants in the NNS group had lower body weights at hospital discharge compared to the control group, a finding that is consistent with the findings of Lyu et al. [26] and different from those of Asadollahpour et al. [47] and Calik et al. [28]. The difference in discharge weight between the different studies in preterm infants may be related to the baseline weight of the study. The improvement in weight of preterm infants at discharge by NNS may also be related to the following factors: NNS can stimulate the vagus nerve excitation in the oral cavity of preterm infants, and then stimulate the secretion of gastric motility and gastrin, regulate gastrointestinal motility, promote the development of gastrointestinal function, so that preterm infants eat more [63], but also cause vagus nerve excitation, accelerate the digestion and absorption of nutrients, and promote the growth of physical development [61]. In addition, NNS training can stimulate the orofacial and lingual muscles of preterm infants, improve the strength of oropharyngeal muscles, improve the function of swallowing reflexes, enhance the sucking ability of children, shorten the time of feeding through the mouth, and promote weight gain [64].Other studies [27, 30, 49] have also found that preterm infants in the NNS and control groups had similar weight measurements at discharge, and the difference was not statistically significant, but it does not indicate that NNS does not promote body mass growth in preterm infants. This is because there are many other factors involved in the weight gain and growth of preterm infants. The variability in the effect of NNS on discharge weight of preterm infants between studies may be related to the different methods of intervention, and there are differences in the timing as well as duration of NNS use that can affect the effectiveness of the intervention, so this result should be interpreted with caution.

Successful oral feeding has been defined as the ability of preterm infants to complete the prescribed amount of milk and gain the expected weight. However, our study found that the mean weight of preterm infants in the NNS group was lower than that of the control group at the time of achieving independent oral feeding, which is consistent with the findings of Lyu et al. [26]. In contrast, the findings of Rocha et al. [19] found that NNS had no significant effect on the weight of preterm infants at the time of independent mouth-feeding. The study by Rocha et al. [19] documented the average weekly weight gain, whereas most of the studies that we included measured the rate of weight gain over the entire period of hospitalization. Different measurements can affect the results of the study, in addition to the fact that the weight of preterm infants is influenced by other factors. The maximum degree of physiologic weight loss and the time to regain birth weight reflect nutrient availability and physical development. In our study, we found that the difference in time to regain birth weight between the two groups of preterm infants was statistically significant, which is consistent with the results of Zhang et al. [37] and Yue et al. [38]. NNS accelerates the maturation of the sucking reflex in preterm infants, improves the ability to suck, and facilitates oral gratification, which leads to an increase in the amount of milk ingested by the infants. In addition, the pituitary gland increased the secretion of various hormones, especially growth hormone secretion reached the highest level, which is conducive to the growth and development of preterm infants [65]. Hwang et al. [66] concluded that NNS can modulate pre-feeding behavior in preterm infants, increase feeding efficiency during the first 5 min of feeding, and help infants regulate pre-feeding agitation.

In the present study, the incidence of feeding intolerance in preterm infants in the NNS group was significantly less than those in the control group, which is consistent with the findings of Say et al. [30] and Feng et al. [35]. The possible explanation for this is that NNS helps to establish rhythmic sucking and swallowing patterns in preterm infants, promotes gastrointestinal growth and development and the maturity of gastrointestinal function, and reduces feeding intolerance and gastrointestinal complications by stimulating the sensory nerve fibers in the oral cavity and stimulating the G-cells to release gastric motility, gastrin, and gastric acid secretion [67].

This review conducted an extensive literature search to refine the evidence base supporting the use of NNS to improve oral feeding outcomes in preterm infants and to promote evidence-based feeding practices. The findings of this study underscore the benefits of NNS for oral feeding in preterm infants, which can inform the development of structured oral feeding programs in NICUs. Such programs have the potential to provide preterm infants with positive early feeding experiences, thereby enhancing their overall care and development. Moving forward, there is a need for large-scale multicenter randomized controlled trials to further investigate the efficacy of NNS in improving oral feeding in preterm infants, and to assist in the development of individualized feeding patterns and evidence-based clinical guidelines for oral feeding in preterm infants.

Nonetheless, this study has several limitations that must be acknowledged. First, although we conducted a relatively comprehensive search, we may have missed some eligible studies. Only articles written in English or Chinese were included, and gray literature was not considered. Second, some articles did not clearly describe randomization and blindness, which may lead to biased reports. Finally, there was some heterogeneity in the interventions, with some using a combination of oral stimulation and NNS, and some using only NNS, but as the results were similar across all studies, this should not have been an issue in the analysis.

Conclusions

In conclusion, NNS significantly reduces the time required for preterm infants to achieve exclusive oral feeding, as well as shortening their length of hospital stay and the time to both initiate oral feeding and return to birth weight. Although we observed that the weight at discharge and at the achievement of full oral feeding was lower in the NNS group compared to the control group, this does not negate the potential for NNS to positively influence weight gain in preterm infants. In the future, it is necessary to further explore the effect of NNS on weight gain of preterm infants, and to establish a standardized evidence-based management method for oral feeding of preterm infants. Importantly, NNS also appears to decrease the incidence of feeding intolerance, which supports its consideration for widespread use in NICUs.

Supporting information

S1 Checklist. PRISMA 2020 checklist.

(DOCX)

pone.0302267.s001.docx^{(27.5KB, docx)}

S1 Table. Search strategy.

(DOCX)

pone.0302267.s002.docx^{(14.8KB, docx)}

S1 Fig. Funnel plot of publication bias.

((a): Time taken to achieve exclusive oral feeding; (b): Length of hospital stay; (c): Time to start oral feeding).

(ZIP)

pone.0302267.s003.zip^{(145.6KB, zip)}

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

The author(s) received no specific funding for this work.

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PLoS One. doi: 10.1371/journal.pone.0302267.r001

Decision Letter 0

Mona Nabulsi

16 Jan 2024

PONE-D-23-30243Effectiveness of non-nutritive sucking on oral feeding of preterm infants: a systematic review and meta-analysisPLOS ONE

Dear Dr. cui,

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: I Don't Know

Reviewer #3: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for the opportunity to review the manuscript “Effectiveness of non-nutritive sucking on oral feeding of preterm infants: a systematic review and meta-analysis” presented in PLOS ONE

The systematic review is very interesting and will be a good contribution to share the findings once the manuscript is revised and professionally edited for English grammar and addressing the multiple sections including the recommendations for revisions and comments about the content. In the attached pdf, the feedback is detailed and specific and intended to assist with moving the manuscript to publication. Below, there is a summary of the feedback.

Best of luck

1. The title includes information about the interventions used in the systematic review, it may be added value to consider the design of included studies

2. The abstract is well defined, you may include the methods used to assess risk of bias and the synthesis of results and state the study limitations

3. Introduction:

a. Please provide an overview of preterm births in a one paragraph

b. Please provide the next section with the content specific to NNS and its benefits for premature infants

4. The aims and objectives: Please rewrite your aim and objectives based on the research questions

5. Methods:

a. The inclusion and exclusion criteria are well stated

b. Search data bases: You may refer to other databases for more studies like CINHAL

c. The outcomes measures may need to be specify as primary and secondary outcomes. Some outcomes need to be well defined along with the units of measures

6. Discussion: Please revise the discussion part, you may need to summarize it. there are too many information which may be not pertinent to the study aims.

7. Figures: Needs labelling

8. References: Please verify the citation for “Vildan 2017”, it refers to

GENERAL COMMENT

The manuscript needs to be edited to improve the flow and the content. Please refer to the feedback in the attached pdf

Reviewer #2: PONE-D-23-30243

Effectiveness of non-nutritive sucking on oral feeding of preterm infants: a systematic review and meta-analysis

PLOS ONE

Thank you for asking me to review this study.

1. Please adjust the keywords according to the mesh.

2. The most important criteria for entering and exiting the study should be mentioned in the method section of the abstract.

3. Please add the search thermals key words in the method section of the abstract if there is no word limit.

4. The time period of the search (from the beginning to the end) should be fully stated.

5. The title or research question of a systematic review should be designed based on PICO, so the comparison group, which is the same as the control group, should be added in the title.

Reviewer #3: This is a well-formed systematic review and meta-analysis focused on the fruitful subject of the effects of NNS on feeding-dependent outcomes in NICU-infants. However, there are some points which should be met before any decision for publication. These are as follows:

Abstract

1- Although the authors provided a background for the ways established for the preterm infants to achieve complete oral feeding with an implicit emphasis on Non-nutritive sucking (NNS), it seems necessary to provide a clear statement of the main questions the review addresses.

2- Also it seems necessary to provide the eligibility criteria in the method section of the abstract.

3- I propose that the PROSPERO registration be transferred inside the manuscript (may be as a footnote) out of the abstract.

4- Please provide the date of your last search for each database.

5- How did you assess risk of bias of the included studies? This needs to be clarified in the method section of the abstract.

6- Also we need specification of the methods of synthesizing the results of the systematic review.

7- Was there any risk of bias, contradiction, or ill-formed designs in the included studies which limited your conclusion? If yes, please provide a description in the conclusion of the abstract section.

Introduction

1- Page 3- line 60: I think it is better to eliminate “Currently” from the sentence, because this is not a new issue in the NICUs.

2- Page 5-line 90: In the sentence, “Although a few published meta-analyses have reached a consensus, in recent years, additional randomized controlled trials have been conducted, so we decided to carry out a more comprehensive and systematic literature review…” the authors tried to show the gap in existing knowledge of reviewed and synthesized data, however, they do not specify what agreement the previous works have reached. It is necessary to clarify this.

Methods

1- The time range of searching for sources has not been specified. We know the end not the beginning date of search.

2- Page 5-line 105: Please eliminate “were conducted”; it does make confusion in the meaning.

3- What were the eligibility criteria for the systematic review? It is described just for the meta-analysis phase.

4- Please clarify how two authors (ZSL and JHM) extracted the information like first author’s name, etc. Was it done independently too? Did they work together?

5- Page 8-line 175: the authors did not specify that how they chose 26 studies for qualitative analysis and then how they decided to do quantitative synthesis on the 21 finalized studies. On the other words, by what criteria did the authors select 21 final studies for meta-analysis? Why was 5 study excluded and 21 studies included?

6- Some of outcomes like time taken to achieve exclusive oral feeding and length of hospitalization are operationally defined. However, the others like gastrointestinal complications, time to return to birth weight, and weight at full oral feeding need a definition. We need to know the unit of their measurement (day, pound, etc.) in addition to a description of the concept. For “time to return to birth weight” specifically it is necessary to elucidate the days, as we encounter premature not term newborns.

7- The authors stated that I2≥50% indicated significant heterogeneity between studies, this is while references like Cochrane consider I2 >75% as evidence for considerable heterogeneity. Would you please cite your source?

8- Did the authors assess confidence (certainty) of the evidence for the measured outcomes?

Results

1- We do not see any trace of the qualitative analysis of the 26 chosen studies. We should have a demographic table for 26 articles first. Then the authors may go to the next step, i.e., meta-analysis of the 21 final studies. We have a missing circle here: systematic review results. Also it is necessary to explain why these 5 studies were removed from the synthesis.

2- For figures 3 to 9, I propose to mention “favors NNS-favors control” instead of “NNS-control” beneath the figures.

3- Page 10-line 212: For “weight at discharge” outcome, why didn’t the authors include references number 31, 34, and 48 in meta-analysis? These studies had calculated this secondary outcome either. Please clarify the reason of the drop out of these references from the meta-analysis.

Discussion

1- You have noted about the controversies regarding negative impact of NNS on infant health. Please explain about it. What are the probable side effects of NNS?

2- The authors attribute the lower weight of NNS group to their earlier discharge from NICU. As far as I am involved in Asadollahpour et al. (2015) study, the mean weight of the NNS group had been higher than the other groups from the baseline measurement. This may be the reason for their higher weight at discharge. This might be controlled through weight-adjustment of the groups at baseline (which was not considered at that time). Yet, as the baseline information is available in the paper, the authors may refer to it.

3- What are the probable impacts of the present review on the future research, clinical work and health policies?

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

**********

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Attachment

Submitted filename: PONE-D-23-30243_SM.pdf

pone.0302267.s004.pdf^{(3.1MB, pdf)}

Attachment

Submitted filename: Report.docx

pone.0302267.s005.docx^{(13KB, docx)}

PLoS One. 2024 Apr 16;19(4):e0302267. doi: 10.1371/journal.pone.0302267.r002

Author response to Decision Letter 0

24 Feb 2024

Dear Reviewers and Editor,

Thank you very much for your reviews on our manuscript submitted to PLOS ONE and the opportunity to revise and resubmit the manuscript for further publication consideration.

We would like to thank for your time and effort to help us improve the manuscript. Each comment brought important help to improve and refine this paper. We have revised the manuscript in response to your comments and have highlighted the changes in the manuscript. Here, we respond to the reviewers' comments point by point after the comments.

Best regards,

All authors

Review Comments to the Author

Response: We thank the reviewer’s positive comment. We would like to express our sincere gratitude to you for detailed and constructive comments. Here, we respond to the comments point by point and reply in blue after the comments.

1. The title includes information about the interventions used in the systematic review, it may be added value to consider the design of included studies

Response: Thanks to the reviewer's comment. We have amended the title “Effects of non-nutritive sucking on developmental progress and oral feeding outcomes in preterm infants: a systematic review and meta-analysis”.

2. The abstract is well defined, you may include the methods used to assess risk of bias and the synthesis of results and state the study limitations

Response: We have refined the abstract by adding methods for assessing risk of bias and outcome synthesis and explaining the limitations of this study.

3. Introduction:

a. Please provide an overview of preterm births in a one paragraph

Response: Thanks to the reviewer's comment. We have added an explanation of the circumstances of preterm birth. (Lines75-82)

b. Please provide the next section with the content specific to NNS and its benefits for premature infants

Response: We further added specifics about the benefits of NNS for preterm infants.

4.The aims and objectives: Please rewrite your aim and objectives based on the research questions

Response: We rewrite the aim and objectives of the study based on the research questions. (Lines123-128)

5. Methods:

a. The inclusion and exclusion criteria are well stated

Response: We further refined and clarified the inclusion and exclusion criteria

b. Search data bases: You may refer to other databases for more studies like CINHAL

Response: We referenced the CINHAL database and updated our search times.

c. The outcomes measures may need to be specify as primary and secondary outcomes. Some outcomes need to be well defined along with the units of measures

Response: The primary and secondary outcomes of the study we defined and added units of measurement.

6. Discussion: Please revise the discussion part, you may need to summarize it. there are too many information which may be not pertinent to the study aims.

Response: Thank you for your suggestion, we have made changes to the discussion section to remove some of the information as appropriate.

7. Figures: Needs labelling

Response: We added labelling to the figures.

8. References: Please verify the citation for “Vildan 2017”, it refers to

Response: After checking, "Vildan" is a reference to "Kaya", which we have modified.

GENERAL COMMENT The manuscript needs to be edited to improve the flow and the content. Please refer to the feedback in the attached pdf

Respond to comments in the PDF

Abstract Please add the aim of the study Response: we add the aim of study: "This review article aimed to explore the effect of NNS on developmental progress and oral feeding in preterm infants through a meta-analysis. "

Please review the total is 1339

Response: We have re-conducted a systematic and comprehensive search of the database, which has been extended until January 2024. A total of 23 randomized controlled trials with 1461 preterm infants were included.

Introduction

You may need to revise this sentence, it is better to start with general introduction about preterm infants and after you will specify about problems of prematurity among those feeding difficulties

Response: We have modified the first paragraph of the preface to provide a general introduction to preterm infants, followed by a specific description of oral feeding difficulties in preterm infants. (lines75-90)

Schneider summarized in this article the importance of nutrition on the brain and cognitive development. You may need to refer to other studies to elaborate about the cardiopulmonary system and other systems

Response: We have revised this sentence and referenced other references to make it more informative. (lines84-88)

what do you mean by motion? you may explain here the NOMAS scale

Response: "Motion" refers to oral motor skills and is usually used to describe the coordination of the muscles of an infant while sucking, swallowing, and breathing.

We explain the NOMAS scale, the tool used to assess sucking ability in newborns.

You may need to redefine the process sine it is unclear as stated

Response: We have redefined NNS to make its expression clearer. " NNS refers to a pacifier is placed in an infant's mouth to increase sucking action, but there is no milk or other fluid intake. "

You may elaborate this sentence

Response: We've made changes.

It is better to discuss the type of in-consensus and support with evidence

Response: Based on your suggestions, we have made modifications, discussed the types of opinions that are consistent with this study, and given evidence to support them.

To compare to what

Response: NNS vs. no NNS compared

Please can you define gastrointestinal complications and related conditions

Response: Our research indicators for this study are defined in the “Materials and Methods” section. (lines161-169)

Materials and methods

You may need to look at other databases for inclusion of related studies like CINHAL, Medline and other

Response: Based on your suggestions, we searched CINHAL, Medline, and re-searched other databases.

Please add the full words for abbreviation

Response: We've added the full name of the abbreviation

the population is preterm infants less than 33 weeks of gestation, you can include in search terms the Extreme low birth weight

Response: Our study was not limited to preterm infants <33 weeks of gestation; the inclusion criterion was preterm infants <37 weeks of gestation.

please add the definition for remaining outcomes and specify the unit of measures weight at discharge, weight at full oral feeding, time to return to birth weight and GI complications

Response: We defined the outcomes "weight at discharge, weight at full oral feeding, time to return to birth weight, and feeding intolerance" and added units of measurement.

Results

Please review the number of studies 15 or 16

Response: We read references 15 and 16 and reevaluated the quality of the studies included in this review

please review the total

Response: A total of 15 studies involving 942 preterm infants were included in the "time taken to achieve exclusive oral feeding”.

Subgroup analyses was performed based on gestational age of preterm infants

Please can you justify why the subgroup analyse was done based on < 33 weeks not less?

Response: The choice of subgroup analyses to be performed based on < 33 weeks gestational age rather than a younger gestational age was determined by a number of reasons. ① Infants with a gestational age of < 33 weeks are considered extremely preterm. They represent a group of particularly biologically immature infants with underdeveloped organ systems that require specialized medical care. This gestational age group is an important cut-off point for identifying very high-risk infants in clinical practice. ②For less heterogeneity. Including all preterm infants together in the analysis resulted in a study with higher heterogeneity. Therefore, by focusing on a more homogenous subgroup, researchers can reduce this heterogeneity, which can result in clearer and more precise study conclusions.

“Lighter” You may use another used for better clarity

Response: We made changes to make the expression more fluent and clearer:” The meta-analysis revealed a statistically significant difference between the two groups, with preterm infants in the NNS group exhibiting reduced weight as compared to control group.”

Discussion

You may need to refer to the article to review the result of the study about the benefit of NNS in improving sucking skills and shortening the time to transition to full breastfeeding

Response: Thanks to the reviewer's comment. We made reference to this literature and revised the sentence.

“pure” Please can you explain what does it mean?

Response: Thanks to the reviewer's comment. " pure " means "exclusive oral feeding ".

“Tolppola et al” Add year here like Tolppola et al (2022)

Response: We have added year of Tolppola et al.

Please check the citation for the author's name

Response: We've changed "Vaildan" to "Kaya".

nasal feeding

Response: We've changed "nasal feeding" to "tube feeding".

“There should be good communication between hospitals, communities and families to safeguard the lives and health of preterm infants.” I think this sentence is abrupt, you may need to elaborate more and add citation

Response: Thanks to the reviewer's comment. After discussion in our team group, we also felt that this sentence appeared out of place and was therefore deleted.

You may need to define the ideal behavior state

Response: NNS can help infants shift from a state of restlessness before eating to a state of quiet alertness.

You may need to review the article since sedation was not studied

Response: We incorporated new research and revised this sentence.

You may add the strengths of the study

Response: We added the strengths of this study. (lines403-413)

Reviewer #2:

1. Please adjust the keywords according to the mesh.

Response: Thanks to the reviewer's comment. We have adapted the keywords to the Mesh subject word.

2. The most important criteria for entering and exiting the study should be mentioned in the method section of the abstract.

Response: We mentioned the most important criteria for inclusion and exclusion in the methods section of the abstract, including:" Eligibility criteria involved randomized controlled studies in English or Chinese. Studies were excluded if they were reviews, case reports, or observational studies from which valid data could not be extracted or outcome indicators were poorly defined. "

3. Please add the search thermals key words in the method section of the abstract if there is no word limit.

Response: We added keywords for the search in the methods section of the abstract: 'non-nutritive sucking' 'Oral feeding' and 'premature.'

4.The time period of the search (from the beginning to the end) should be fully stated.

Response: We refined the search time of the databases in the methods section of the abstract: the search period for each database was from the creation of the database until January 20, 2024.

5.The title or research question of a systematic review should be designed based on PICO, so the comparison group, which is the same as the control group, should be added in the title.

Response: Thanks to the reviewer's comment. We have made changes to the article title: "Effects of non-nutritive sucking on developmental progress and oral feeding outcomes in preterm infants: a systematic review and meta-analysis".

Abstract

Response：Thanks to the reviewer's comment. This review aimed to explore the effect of NNS on developmental progress and oral feeding in preterm infants through a meta-analysis.

2- Also it seems necessary to provide the eligibility criteria in the method section of the abstract.

Response：We provide some of the eligibility and exclusion criteria in the methods section of the abstract.

3- I propose that the PROSPERO registration be transferred inside the manuscript (may be as a footnote) out of the abstract.

Response：We have removed the PROSPERO registration from the abstract, which can be found under "Materials and methods" in the manuscript .(line146)

4- Please provide the date of your last search for each database.

Response：All databases last searched on January 20, 2024

5- How did you assess risk of bias of the included studies? This needs to be clarified in the method section of the abstract.

Response: "We evaluated the methodological quality of randomized controlled trials (RCTs) utilizing the assessment tool provided by the Cochrane Collaboration. " Readers can understand the methods and standards of studying bias risk assessment when reading the abstract.

6- Also we need specification of the methods of synthesizing the results of the systematic review.

Response: We describe this in the methods section of the abstract. " The meta-analysis will utilize Review Manager 5.3 software, employing either random-effects or fixed-effects models based on observed heterogeneity. We calculated the mean difference (MD) and 95% confidence interval (CI) for continuous data, and estimated pooled odds ratios (ORs) for dichotomous data. "

Response: Yes, there are some limitations in this study. We describe it in the conclusion of the abstract. " The study, hampered by a small sample size, did not account for potential confounders. High heterogeneity and notable bias among studies were observed. "

Introduction

1- Page 3- line 60: I think it is better to eliminate “Currently” from the sentence, because this is not a new issue in the NICUs.

Response: We have eliminated “Currently”.

Response: We interpret the consensus reached in previously published review studies that non-nutritive sucking improves feeding skills and reduces hospitalization time in preterm infants.

Methods

1- The time range of searching for sources has not been specified. We know the end not the beginning date of search.

Response: The search time frame for each database ranged from its inception date until January 20, 2024.

2- Page 5-line 105: Please eliminate “were conducted”; it does make confusion in the meaning.

Response: We have eliminated “were conducted”.

3- What were the eligibility criteria for the systematic review? It is described just for the meta-analysis phase.

Response: The eligibility criteria for the systematic review were consistent with those for the meta-analysis, and we have refined them.

4- Please clarify how two authors (ZSL and JHM) extracted the information like first author’s name, etc. Was it done independently too? Did they work together?

Response: The two authors (ZSL and JHM) extracted general information for inclusion in the study independently, and they did not work together and did not interfere with each other.

Response: To ensure the comprehensiveness and up-to-date nature of our research, we have updated the literature search cutoff date to incorporate a newly published study. This article offers a detailed account of the selection process for the final 22 studies included. In the ultimate phase of this process, five studies were excluded due to insufficient quality.

Response: We defined time to return to birth weight and weight at full oral feeding, as well as feeding intolerance, and added their units of measurement.

7- The authors stated that I2 ≥50% indicated significant heterogeneity between studies, this is while references like Cochrane consider I2 >75% as evidence for considerable heterogeneity. Would you please cite your source?

Response: We refer to the research of Foreman et al and think that I2≥50% indicated significant heterogeneity between studies.

(Foreman J, Salim AT, Praveen A, et al. Association between digital smart device use and myopia: a systematic review and meta-analysis. Lancet Digit Health. 2021;3(12):e806-e818. doi:10.1016/S2589-7500(21)00135-7)

8- Did the authors assess confidence (certainty) of the evidence for the measured outcomes?

Response: Yes, the authors assessed confidence (certainty) of the evidence for the measured outcomes. We assessed the methodological quality of RCTs using the Cochrane risk of bias tool, which included seven evaluation items: sequence generation, allocation concealment, blinding of participants, outcome evaluator, incomplete outcome data, and selective outcome reporting. The studies were evaluated for unclear, low or high risk of bias.

Results

Response: We qualitatively analyzed the 28 studies in Table 1 and provided detailed explanations for these 5 studies that were removed from the review. (See Table 1 for details.) Four of the five studies that were deleted were because the control group also received NNS or pacifier interventions, and one study was deleted because the study metrics could not be converted for data.

2- For figures 3 to 9, I propose to mention “favors NNS-favors control” instead of “NNS-control” beneath the figures.

Response: We have revised figures 3 to 9 to “favors NNS-favors control” based on your suggestions.

Response: Reference 31, which measured from "admission to weight of 2 kg," did not match our indicator of "weight at discharge" and was deleted.

References 34 and 48, although they had "weight at discharge" results, were included in the analysis and found to be the main source of heterogeneity, and were deleted. We have explained this in the manuscript in the "weight at discharge" results. (lines262-268)

Discussion

1- You have noted about the controversies regarding negative impact of NNS on infant health. Please explain about it. What are the probable side effects of NNS?

Response: NNS provided by pacifiers tend to cause nipple confusion and may also cause different physiological, pharyngeal, and esophageal motility events, potentially affecting gastroesophageal reflux.

Response: Thanks to the reviewer's suggestion, we reviewed the baseline data of the included studies and found that the reason for the difference in "weight at discharge" between the studies may be related to weight at baseline. We have made changes in the "Discussion" section of the manuscript.

3- What are the probable impacts of the present review on the future research, clinical work and health policies?

Response: This review conducted an extensive literature search to refine the evidence base supporting the use of NNS to improve oral feeding outcomes in preterm infants and to promote evidence-based feeding practices. The findings of this study underscore the benefits of NNS for oral feeding in preterm infants, which can inform the development of structured oral feeding programs in NICUs. Such programs have the potential to provide preterm infants with positive early feeding experiences, thereby enhancing their overall care and development. Moving forward, there is a need for large-scale multicenter randomized controlled trials to further investigate the efficacy of NNS in improving oral feeding in preterm infants, and to assist in the development of individualized feeding patterns and evidence-based clinical guidelines for oral feeding in preterm infants.

Attachment

Submitted filename: Response to Reviewers.docx

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PLoS One. doi: 10.1371/journal.pone.0302267.r003

Decision Letter 1

Mona Nabulsi

22 Mar 2024

PONE-D-23-30243R1Effects of non-nutritive sucking on developmental progress and oral feeding outcomes in preterm infants: a systematic review and meta-analysisPLOS ONE

Dear Dr. cui,

Please submit your revised manuscript by May 06 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Mona Nabulsi, MD, MS

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

Reviewer #3: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: I Don't Know

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Reviewer #1: Review 16/3/2024

Thank you for your extensive work and addressing the suggestions and comments. The manuscript demonstrated thorough and diligent efforts

Kindly find below minor suggestions for your kind follow up best of luck

1- Abstract :

a. Title : Based on your research question you may need to modify the title as: “Effects Of Implementing Non-Nutritive Sucking On Oral Feeding Progression And Outcomes In Preterm Infants: A Systematic Review And Meta-Analysis”

b. Aim: Line 34-35 You may need to review the aim “to explore the effect of NNS on oral feeding progression through a meta-analysis”.

c. Conclusion: Line 64 you may need to modify the sentence to “reduces the time to reach full oral feeding”

2- Introduction: Line 88-90 the cited reference discusses the effect of oxygen therapy on altering the oral sensory, motor, and the development of coordinated NNS in preterm infants. I may suggest reviewing another reference to support your point.

3- Materials and methods

a. Systematic search and strategy

Line 143 -1 44 “Detailed search strategies for each database are shown in S2 Table” you may need to modify to S1 table as stated in the section of supporting information.

b. Inclusion and exclusion criteria: Line 157-165: You may need to put references for the definition of outcome measures and add the full word of the unit “g” as grams

4- Results: Line 215 - 227: Please review the values in the related section and match with ones stated in Fig1. PRISMA flow diagram

5- Discussion:

a. Line 325, please review the citation, it is more pertinent for the reference (57)

“Barlow SM, Finan DS, Rowland SG. Mechanically evoked perioral reflexes in infants. Brain research. 651 1992;599(1):158-60. Epub 1992/12/18. doi: 10.1016/0006-8993(92)90865-7. PubMed PMID: 1493544.”

b. Line 347, The author Chorna et al studied the outcome for the development of sucking ability and decrease the length of hospitalization. I may suggest looking at this reference instead which elaborates the complex factors for discharge “Committee on Fetus and Newborn. (2008). Hospital discharge of the high-risk neonate. Pediatrics, 122(5), 1119-1126.”

Reviewer #2: PONE-D-23-30243

Effectiveness of non-nutritive sucking on oral feeding of preterm infants: a systematic review and meta-analysis

PLOS ONE

Thank you for asking me to review this study. The authors' answers were acceptable to me and convincing.

Thank you

Reviewer #3: (No Response)

**********

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Reviewer #1: Yes: Saadieh Masri

Reviewer #2: No

Reviewer #3: No

**********

Attachment

Submitted filename: Report - 2.docx

pone.0302267.s007.docx^{(12.5KB, docx)}

PLoS One. 2024 Apr 16;19(4):e0302267. doi: 10.1371/journal.pone.0302267.r004

Author response to Decision Letter 1

25 Mar 2024

Reviewer #1: Review 16/3/2024

Thank you for your extensive work and addressing the suggestions and comments. The manuscript demonstrated thorough and diligent efforts

Kindly find below minor suggestions for your kind follow up best of luck

Response: Once again, we express our appreciation for your constructive comments. Here, we have responded to the comments individually in blue.

1- Abstract:

a. Title: Based on your research question you may need to modify the title as: “Effects Of Implementing Non-Nutritive Sucking On Oral Feeding Progression And Outcomes In Preterm Infants: A Systematic Review And Meta-Analysis”

b. Aim: Line 34-35 You may need to review the aim “to explore the effect of NNS on oral feeding progression through a meta-analysis”.

c. Conclusion: Line 64 you may need to modify the sentence to “reduces the time to reach full oral feeding”

Response: Thanks to the reviewer's comment.

a.As per your suggestion, I have revised the title to " Effects Of Implementing Non-Nutritive Sucking On Oral Feeding Progression And Outcomes In Preterm Infants: A Systematic Review And Meta-Analysis."

b.The purpose of the study in the abstract section has been revised to: "This review aimed to explore the effect of NNS on oral feeding progression through a meta-analysis. "

c.The first sentence of the conclusion has been modified as per your suggestion to read " NNS improves oral feeding outcomes in preterm infants and reduces the time to reach full oral feeding and hospitalization length."

Response: We have added other references to support our argument.

(9. Samara M, Johnson S, Lamberts K, Marlow N, Wolke D. Eating problems at age 6 years in a whole population sample of extremely preterm children. Developmental medicine and child neurology. 2010;52(2):e16-22. Epub 2009/10/17. doi: 10.1111/j.1469-8749.2009.03512.x. PubMed PMID: 19832883.)

3- Materials and methods

a. Systematic search and strategy

Line 143 -1 44 “Detailed search strategies for each database are shown in S2 Table” you may need to modify to S1 table as stated in the section of supporting information.

b. Inclusion and exclusion criteria: Line 157-165: You may need to put references for the definition of outcome measures and add the full word of the unit “g” as gram

Response: Thanks to the reviewer's comment.

a. See S1 Table for detailed search strategies for each database, which we have modified.

b. We have added references to all the definitions for the outcome measures and modified the unit "g" to "gram". (lines 159-168)

4- Results: Line 215 - 227: Please review the values in the related section and match with ones stated in Fig1. PRISMA flow diagram

Response: Lines 216-228, we checked this section well compared to the values in Figure 1 (PRISMA flow diagram) and verified that there were no errors.

5- Discussion:

a. Line 325, please review the citation, it is more pertinent for the reference (57)

Response: We amend the citation in line 325 to read "59. Barlow SM, Finan DS, Rowland SG. Mechanically evoked perioral reflexes in infants. Brain research. 1992;599(1):158-60. Epub 1992/12/18. doi: 10.1016/0006-8993(92)90865-7. PubMed PMID: 1493544."

Response: As you suggested, we have carefully read and quoted from the article (62. Hospital discharge of the high-risk neonate. Pediatrics. 2008;122(5):1119-26. Epub 2008/11/04. doi: 10.1542/peds.2008-2174. PubMed PMID: 18977994.) and have refined this section of the manuscript. (lines 346-352)

Reviewer #2: Thank you for asking me to review this study. The authors' answers were acceptable to me and convincing.

Response: We are pleased to learn that you found our response acceptable and convincing. Thank you again for your interest in and support of our research, and good luck.

We would like to thank the reviewer again for your time and efforts to provide the comments for us to improve the manuscript.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0302267.s008.docx^{(20KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0302267.r005

Decision Letter 2

Mona Nabulsi

1 Apr 2024

Effects Of Implementing Non-Nutritive Sucking On Oral Feeding Progression And Outcomes In Preterm Infants: A Systematic Review And Meta-Analysis

PONE-D-23-30243R2

Dear Dr. cui,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Mona Nabulsi, MD, MS

Academic Editor

PLOS ONE

PLoS One. doi: 10.1371/journal.pone.0302267.r006

Acceptance letter

Mona Nabulsi

4 Apr 2024

PONE-D-23-30243R2

PLOS ONE

Dear Dr. Cui,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

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Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Mona Nabulsi

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Checklist. PRISMA 2020 checklist.

(DOCX)

pone.0302267.s001.docx^{(27.5KB, docx)}

S1 Table. Search strategy.

(DOCX)

pone.0302267.s002.docx^{(14.8KB, docx)}

S1 Fig. Funnel plot of publication bias.

((a): Time taken to achieve exclusive oral feeding; (b): Length of hospital stay; (c): Time to start oral feeding).

(ZIP)

pone.0302267.s003.zip^{(145.6KB, zip)}

Attachment

Submitted filename: PONE-D-23-30243_SM.pdf

pone.0302267.s004.pdf^{(3.1MB, pdf)}

Attachment

Submitted filename: Report.docx

pone.0302267.s005.docx^{(13KB, docx)}

Attachment

Submitted filename: Response to Reviewers.docx

pone.0302267.s006.docx^{(29.6KB, docx)}

Attachment

Submitted filename: Report - 2.docx

pone.0302267.s007.docx^{(12.5KB, docx)}

Attachment

Submitted filename: Response to Reviewers.docx

pone.0302267.s008.docx^{(20KB, docx)}

Data Availability Statement

All relevant data are within the manuscript and its Supporting Information files.

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PERMALINK

Effects of implementing non-nutritive sucking on oral feeding progression and outcomes in preterm infants: A systematic review and meta-analysis

Shuliang Zhao

Huimin Jiang

Yiqun Miao

Wenwen Liu

Yanan Li

Yuanyuan Zhang

Aihua Wang

Xinghui Cui

Roles

Abstract

Background

Methods

Results

Conclusion

Introduction

Materials and methods

Systematic search and strategy

Inclusion and exclusion criteria

Data extraction

Methodological quality assessment

Data synthesis and analysis

Results

Search results

Fig 1. PRISMA flow diagram.

Table 1. Characteristics of the included studies.

Fig 2. Risk of bias graph about each risk of bias item presented as percentages across all included studies.

Fig 3. Summary of risk of bias for each trial.

Meta analysis results

Primary outcomes

Time taken to achieve exclusive oral feeding

Fig 4. Forest plot for time taken to achieve exclusive oral feeding.

Length of hospital stay

Fig 5. Forest plot for length of hospital stay.

Time to start oral feeding

Fig 6.

The secondary outcomes

Weight of discharge

Fig 7. Forest plot for weight of discharge.

Time to return to birth weight

Fig 8. Forest plot for time to return to birth weight.

Weight at full oral feeding

Fig 9. Forest plot for weight at full oral feeding.

Feeding intolerance

Fig 10. Forest plot for feeding intolerance.

Sensitivity analysis and publication bias

Table 2. Results of sensitivity analysis.

Discussion

Conclusions

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Mona Nabulsi

Roles

Author response to Decision Letter 0

Decision Letter 1

Mona Nabulsi

Roles

Author response to Decision Letter 1

Decision Letter 2

Mona Nabulsi

Roles

Acceptance letter

Mona Nabulsi

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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