Methodological procedures for ultrasonographic assessment of the tongue during sucking in full-term infants: A scoping review

Abstract

Background

This scoping review aimed to identify methodological procedures for acquiring and analyzing ultrasound images of the tongue during sucking in full-term infants. The Participants, Concept, and Context strategy was used to define the inclusion criteria: population (full-term infants); concept (ultrasound assessment); and context (assessment of tongue movements during sucking).

Methods

It included observational, experimental, descriptive, and analytical studies, and excluded those unavailable in full, with premature infants, babies with craniofacial changes and syndromes, studies on animals, in vitro, letters to the editor, errata, and using ultrasound for other purposes. There were no language or time restrictions. Two blinded professionals independently selected 20 articles that met the inclusion criteria from different databases.

Results

The most evaluated parameters were related to the morphometric and kinematic aspects of the tongue, considering the physical behavior of the nipple and bottle nipple; sucking, swallowing, and breathing; distance from the tip of the nipple to the hard-soft palate junction; and milk flow. An endocavity transducer was positioned in the submental region at 5 MHz to 8 MHz.

 Conclusions

The studies present the acquisition and static analysis of ultrasound images of the tongue, hard and soft palate, nipple, and bottle nipple, and of kinematic measurements of the tongue, nipple, bottle nipple, and hyoid bone. They evaluated quantitative and qualitative parameters. Frequency adjustment depended on the child’s age (the B mode was the most used), with babies reclined on the mother’s lap to feed from the mother’s breast and/or bottle.

Introduction

Nutritive sucking is a complex oral sensorimotor activity, essential for adequate growth and development in infants. It includes the coordination of sucking, swallowing, and breathing, which require movements of the tongue and jaw [1]. The complexity of tongue development and its functional role during breastfeeding generates controversy regarding criteria for monitoring, evaluation, diagnosis, treatment indications, and clinical interventions [2, 3]. During the first half of the sucking cycle, the baby moves the tongue downwards, creating a stronger vacuum (average: − 122 to − 163 mmHg) that coincides with the removal of milk from the breast. During the second half of the sucking cycle, the tongue rises, and the milk is transported from the oral cavity to the pharynx to be swallowed. The vacuum returns to its baseline, thus completing a suction cycle [4].

Sucking stimulates nerve impulses through the efferent arc of the milk ejection reflex to the hypothalamus, which prompts the posterior pituitary gland to release oxytocin into the maternal circulation. Oxytocin binds to receptors on the myoepithelial cells surrounding the alveoli, causing them to contract, ejecting milk toward the nipple (milk ejection). Thus, negative pressure (intraoral vacuum) combined with positive pressure, caused by milk ejection, are the driving forces for the flow of milk from the breast to the baby during breastfeeding. As the breast empties, the rate of milk flow changes with subsequent milk ejections, suggesting that babies may modify their sucking patterns as breastfeeding progresses[4].

Some clinical tools allow observing and diagnosing sucking patterns in babies, such as the Neonatal Oral Motor Assessment Scale (NOMAS), which distinguishes between a normal, disorganized, and dysfunctional sucking pattern, and the Digital Swallowing Workstation (DSW, KayPentax, USA), which quantitatively measures a disorganized sucking pattern, characterized by difficulties in coordinating sucking, swallowing, and breathing during feeding [1, 3]. Ultrasonography (US), among clinical tools, has been described as an image evaluation method that allows the acquisition and analysis of biomechanical parameters of the tongue during sucking [5,6,7]. US provides different modes of static and dynamic images through a transducer, from the reflection or scattering of a pulsed low to high-frequency sound beam (1 to 16 MHz) [5]. In the assessment of tongue movements during sucking, ultrasound B-mode provides a real-time, two-dimensional image, allowing qualitative and quantitative analyses of its movements in a sagittal plane.

Studies used US to analyze the tongue kinematics of healthy and post-frenotomy babies during sucking. They observed the number of sucking cycles, the amplitude of tongue movements, its distance in relation to the hard and soft palate junction (HSPJ), the amplitude and elasticity of the nipple, and the speed of milk transfer from the oral cavity to the pharynx [8, 9]. The advantage of US over other imaging exams for evaluating tongue movements during sucking is that it does not use contrast media, does not expose to ionizing radiation, is non-invasive, with low cost, and captures dynamic, real-time images, focusing on the visualization of soft tissues, the number of cycles during the baby’s feeding. Although studies indicate the US is an easy resource, it is challenging to maintain the transducer in the submandibular plane, to standardize images for comparison, to establish measurements with reliable parameters, and to maintain the mother/infant’s positioning during the US evaluation (ELAD 2014) [5, 8, 10].

Thus, US has numerous advantages and clinical applicability for evaluating tongue movements during sucking in normal individuals and those with anatomical and functional changes. However, studies describe the methodological procedures for using US individually, which makes it difficult to compare and analyze results. They differed regarding the transducer type, frequency, and positioning; US image acquisition mode and analysis; instructions to the mother/baby; and evaluator’s experience. Hence, this study carried out a scoping review to identify the procedures performed during US assessment of sucking during breastfeeding in full-term infants. This study design seeks to explore the main findings of the topic in question, investigate the dimension, scope, and nature of the studies, condense the data, and make it possible, based on their findings, to identify gaps that direct questions to be answered by systematic reviews and assist in the development of a protocol for US evaluation of sucking during breastfeeding for infants.

The research question was guided by the PCC mnemonic elements (population, concept, and context) suggested by the Joanna Briggs Institute (JBI) scoping review guide [11]. The population comprised full-term infants, up to 180 days old, without risk factors such as syndromes, craniofacial malformations, and oropharyngeal dysphagia; the concept consisted of the methodological procedures for acquiring and analyzing US images related to tongue movements during sucking; and the context encompassed aspects of tongue assessment during sucking. Therefore, the research question of this scoping review was, “What are the methodological procedures for acquiring and analyzing US images of the tongue during sucking in full-term infants?”.

Methods

This research is a scoping review, with a structured protocol registered in the Open Science Framework (OSF). The protocol is available from: https://www.osf.io/d7cyr/ and was published in the CEFAC journal https://doiorg.publicaciones.saludcastillayleon.es/10.1590/1982-0216/20232551223s‘Human Ethics and Consent to Participate declarations: not applicable’.

Eligibility criteria

Participants

This scoping review included primary studies that used US to assess measures related to tongue mobility during sucking in full-term babies up to 180 days old, of both sexes. The scope of this review did not include studies with premature babies, with craniofacial malformations, syndromes, or swallowing disorders, studies that used US for therapy, to assess facial muscles, or to assess only swallowing.

Concept

The concept of this review consisted of describing the methodological procedures for US acquisition and analysis of tongue movements during sucking. A standardized protocol for quantifying tongue movements in US videos could lead to more efficient and reproducible measurements by different researchers and clinicians. US has been described as an image evaluation clinical tool that acquires and analyzes biomechanical parameters of the tongue during sucking [5,6,7]. US obtains different modes of static and dynamic images through a transducer, from the reflection or scattering of a pulsed low to high-frequency sound beam (1 to 16 MHz) [5]. In the assessment of tongue movements during sucking, US B-mode provides a real-time, two-dimensional image, allowing qualitative and quantitative analyses of its movements in a sagittal plane.

Context

This scoping review included literature evidence published in scientific journals or other means of scientific dissemination (e.g., dissertations, theses) that assessed tongue movements during sucking in full-term infants with US. This made it possible to identify the procedures used to assess tongue movements with US and the available evidence on the topic. Furthermore, studies that used US as a tool for acquiring and analyzing images related to sucking in full-term infants were included.

Source types

Observational, experimental, descriptive, and analytical studies were included, and published in English, Portuguese, and Spanish, without restrictions on the date of publication. Expert opinion studies, letters to the editor, errata, annals, study protocols, and studies that could not be acquired in full, animal studies, and in vitro studies were excluded, as they did not approach the population in question.

Search strategy

The search strategy (Fig. 1) was applied individually to each database, namely: MEDLINE (via PubMed), EMBASE, Web of Science, and Scopus. This strategy was developed based on a guiding search (ultrasonic AND sucking behavior). To validate the guiding research terms, Medical Subject Headings (MeSH) were used for the MEDLINE, Scopus, and Web of Science databases, while the “EMTREE terms” were used in Embase. Two professionals blindly and independently screened the studies based on the eligibility criteria.

Fig. 1

Individualized search strategy per database.The review included studies published from the date of insertion until April 2024

Selection of studies/sources of evidence

All identified citations were collated using Rayyan software (Qatar Computing Research Institute, Doha, Qatar). Relevant studies with full texts available in English, Portuguese, and Spanish were imported into the software; disagreements that arose between reviewers were resolved through discussion or with a third reviewer for eligibility.

Data extraction

Two independent reviewers extracted data from the articles included in the scoping review, using a structured Microsoft Excel spreadsheet developed by the reviewers. This mapping allowed the data to be synthesized and interpreted, generating a detailed description for the review (Fig. 2). Thus, the results were separated, summarized, and reported to present an overview of all the material through specific categories.

Fig. 2

Data extracted from the studies selected to map the ultrasound assessment procedures of tongue movements during sucking in full-term infants

Data analysis/presentation

The article analysis protocol considered the year of study, study design, number of babies assessed, age, sucking assessment method, US sucking image acquisition method, and US sucking analysis method.

Results

The review mapped 770 studies, of which 280 were excluded due to duplication, leaving 490 for reading titles and abstracts. Of these, 467 articles were excluded for not meeting the inclusion criteria established for this review, leaving 23 articles for reading in full. After reading the studies in full text, only 20 articles were eligible for analysis in this review (Fig. 3). Two blind evaluators carried out the selection process, with a Kappa coefficient of 0.96. Fig. 4.

Fig. 3

Flowchart of the search and selection phases of the scoping review of ultrasound assessment of the tongue during sucking in infants

The studies [4, 6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24] were published between 1986 and 2023, with a greater concentration in the last 10 years. Between 1986 and 1988, studies focused on evaluating the behavior of the nipple and tongue during breastfeeding [12, 21]; between 1990 and 1997, they focused on the morphological evaluation of the nipple during sucking and tongue movements during sucking based on breastfeeding with a bottle nipple [22,23,24]; between 2001 and 2023, they evaluated the distance between the nipple and the hard/soft palate, the movement of the tongue before and after lingual frenotomy, and the kinematics of the tongue during feeding in the mother’s breast and bottle nipple [4, 6,7,8,9,10, 13, 15, 17,18,19,20]. The number of publications on the topic differed between countries; Australia had the most publications (48%), followed by the United States (28%), England (12%), Japan (8%), Turkey (3%) and Israel (1%).

The designs of the mapped studies consisted of observational (descriptive and analytical) [4, 7, 9, 13, 14, 17, 22, 25] and experimental (nonrandomized clinical trials) [8, 10, 15, 20, 23] However, seven studies did not present their methodological designs [6, 12, 16, 18, 19, 21, 24]. The studies analyzed samples ranging from four to 50 babies, aged 2 to 120 days, including healthy babies and those with ankyloglossia, and mothers who complained of pain during breastfeeding. They were assessed in the office/outpatient clinic and at home, although some studies did not inform the location.

Table 1 presents the general overview of the methodological procedures for acquiring and analyzing US images of the babies’ sucking from different breastfeeding methods (only breastfeeding, breastfeeding and bottle, and only bottle). It also shows the equipment used to acquire US images, the acquisition method, previous instructions, positioning of the transducer, US image adjustments, analysis mode, and evaluation time.

Table 1 Parameters for acquisition and analysis of ultrasound images during feeding

The examinations were performed with different US equipment models (portable and mechanical). The endocavitary transducer was the most used for having a wide frequency range (4–10 MHz) and being more anatomically adjustable to the baby’s submental region. Several studies do not describe the positioning when the baby was feeding. The ones describing it followed breastfeeding position protocols such as the LATCH and International Board Certified Lactation Consultant guidelines. Those that described bottle use suggested sitting the baby on the lap with the head reclined slightly back. The examination should use the transducer in the midline, centered in the submental region, in the sagittal plane, with the nipple to the left to obtain more accurate images. This enables better visualization of the anatomical structures of the baby’s oral cavity and the dynamics of the tongue and nipple movements during suction.

The authors used the following biomarkers: distance from the nipple to the HSPJ (mm); physical behavior of the nipple (nipple diameter, nipple compression, nipple stretching) (mm); tongue position during the sucking cycle (tongue up and down, nutritive and nonnutritive suction); suction rates; distance between tongue and palate. Even though the studies addressed the same biomarkers, analyzing all or some, the results may differ according to the evaluator’s expertise in applying the technique, identifying the target biomarkers during the examination, associating them, and analyzing data Fig. (4)

Fig. 4

Ultrasound imaging of the tongue at rest to identify anatomical structures

The authors aimed to investigate the distance from the tip of the nipple to the HSPJ; the physical behavior of the nipple during sucking; the correlation with intraoral vacuum [6,7,8,9, 12, 13, 16, 19, 25] and tongue movement during breastfeeding before and after lingual frenotomy [14]; tongue kinematics and morphology during breastfeeding in babies with and without ankyloglossia [20, 21, 24]; sucking patterns during breastfeeding over time; secretory activation [4, 7, 8, 10, 16,17,18] and tongue action during breastfeeding and bottle feeding [7, 22, 23].

On US, the hard palate appears as an echogenic line visualized in white. Although the articles have not described it, the contour of the hard palate on US is visible when the tongue presses against it, as in swallowing/sucking milk, and is no longer visible when the tongue moves away from it. Because it is a rigid structure, the hard palate can be used as a reference point to eliminate noise induced by non-breastfeeding movements[10]. The HSPJ location on the polar coordinates was identified where the band becomes wider than 5 pixels[10]. The soft palate appears as a gray structure (3–4 mm) with an echogenic border and was identified where the band widens. The nipple appears as a gray, soft tissue structure, and the ducts within the nipple appear as hypoechoic (black), shaped like tubular structures. Milk flow was visualized as a hypoechoic fluid containing echogenic spots [14, 16]. Echogenic spots are described as fat and globules in milk [14, 16].

Other landmarks were used as measurement markers, such as distance (mm) between the tip of the nipple and the beginning of the HSPJ was measured from a transverse mark on the tip of the nipple to the transverse mark on the distal end of the hard palate adjacent to the soft palate in the sagittal plane; distance (mm) the nipple traveled in the entire gray structure presented cylindrically in the image; the sucking cycle, from when the middle of the tongue was attached to the palate (tongue up), followed by a downward tongue excursion, the middle tongue reaching its lowest point (tongue down), until the tongue attached to the palate again. Some authors measured with a caliper on the device’s screen, whereas others used the device’s measurements (which can bias the analysis of the results).

Discussion

This scoping review aimed to map the procedures for acquiring and analyzing US images of tongue movements during sucking of full-term infants at the mother’s breast and bottle. It presents the possibilities of US assessment of sucking, based on the analysis of acquisition methods, image modes, milk ejection and flow, association with the evaluation of intraoral vacuum, weight gain, and limitations inherent to the exam. In this way it will help understand US image acquisition methods and guide the basic principles for examinations of full-term infants’ sucking. Hence, studies should indicate the oral cavity structures that can be evaluated in this population. Moreover, the mapped studies show that examiners must know how US images are formed, tissue differences, and structure echogenicity.

Real-time US is a lower-cost imaging modality free from ionizing radiation and other associated risks [5, 26]. It has been used since the 1980 s to describe events that occur in full-term babies’ oral cavity and nipple behavior during breastfeeding [12, 21]. The most recent studies explore the validity and reliability of new US technologies for morphometric and kinematic assessment of the tongue [4,5,6];distance from the nipple to the HSPJ [8, 9]; physical behavior of the nipple and bottle nipple[8, 12, 13], associating milk ejection [17, 18] and intraoral vacuum [9] during the sucking of infants at the mother’s breast and bottle, seeking to establish the temporal sequences of the events of suction identified with US in the wave-like movement of the tongue during breastfeeding [4, 6,7,8,9,10, 12,13,14,15,16,17,18,19,20,21,22,23,24,25]. It makes it possible to understand patterns considered typical of sucking and the possible variations of these patterns [27, 28] and correlate tongue movements before and after lingual frenotomy and maternal pain scale to verify the effectiveness of the surgical technique [14] and the displacement of the hyoid bone as a marker for swallowing and reference for sucking cycles [4].

US provides more detailed, static, and dynamic images of the soft tissues of the infant’s mouth, human nipple, and bottle nipple, showing the milk flow in the oral cavity with various US devices, such as B-mode, endocavity transducer, at 7 MHZ, with a gain of 55 dB and a dynamic range of 60 dB [6, 7, 9, 13, 15, 19]. Such parameters can be adjusted according to the baby’s age by reducing the frequency to 5 MHz [6, 9, 16, 17], using two foci to narrow the US beam, one on the hard palate and the other on the nipple-tongue attachment [6,7,8,9, 13, 14, 16,17,18,19,20].

Currently, the infant’s sucking patterns are clinically assessed through visual and digital inspection (with a gloved finger while the baby sucks), using protocols with qualitative and empirical measures [3, 25], with no objective method to assess tongue movement during sucking on the mother’s breast or bottle for clinical speech-language-hearing pathologists to more accurately assess tongue movements and draw up a more assertive and individualized therapeutic plan. Thus, more studies are needed to understand the reliability, sensitivity, and specificity of US for this objective. This corroborates the need to develop a protocol for evaluating tongue movements during sucking in full-term babies during breastfeeding and bottle feeding.

Even though the US is a potential evaluation instrument likely used in these individuals’ clinical follow-up, the studies do not address the challenges faced in acquiring and analyzing US images. They must detail the evaluator’s experience and training and whether the intrarater and interrater reliability was analyzed. Most articles do not mention the preparation of the mother and baby for the assessment, the position of the baby for milk supply, the place where babies were assessed, the details of the acquisition mode, and US calibration parameters. There was variability in the parameters and methods of US image analysis to determine the quantitative measures and interpret the qualitative ones. Furthermore, for the same variable, the authors differ between units of measurement in millimeters [12] and percentages [23].

Moreover, some standardization difficulties are expected in US assessment of sucking, such as the change in the sucking rhythm that occurs naturally according to the baby’s alert state and sucking time, anatomical differences between nipples in the breastfeeding assessment, variations in the entry and exit movement of the bottle nipple during sucking [22], the difficulty in maintaining the transducer stabilized, centered, and positioned in the submandibular region without interfering with the natural breastfeeding process, and the quality of US image resolution to enable more accurate analysis.

This scoping review observes a need for detailing the US image acquisition method to make the studies more robust and homogeneous. It also found that they overvalued sonographic analysis results but undervalued the biases from image formation.

Conclusion

The studies mapped in this review present the acquisition and static analysis of US images of the tongue muscles, hard and soft palate, nipple, and bottle nipple, and kinematic measurements of the tongue, nipple, bottle nipple, and hyoid bone. They assessed quantitative and qualitative parameters, mostly amplitude (mm), distance (mm), duration (number of sucking cycles), and description of the displacement of the tongue, nipple, and bottle nipple. They used endocavitary transducers at various frequencies, depending on the depth and the child’s age. B-mode was the most used among the studies. Babies were generally placed reclined on their mother’s lap to breastfeed or feed from a bottle, and mothers were instructed to breastfeed on demand and/or until the bottle was emptied. The brightness, depth, and gain settings were modified to acquire quality images according to the equipment’s and the baby’s characteristics. However, there is a significant gap in knowledge, such as detailed information on the evaluator’s training and expertise, standardized mother-infant management during feeding, methodological accuracy in acquiring images and identifying and analyzing biomarkers. Clinical practice can use US to assess infants, identify the cause of feeding difficulties, and define individualized care plans. Thus, more detailed and standardized studies are needed, as well as the development of a US protocol to evaluate tongue movements while sucking on the bottle or the mother’s breast.