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DOI:10.2214/AJR.04.1114
AJR 2005; 185:1322-1327
© American Roentgen Ray Society


Original Research

Assessment of Fetal Swallowing with Gray-Scale and Color Doppler Sonography

Roberto Grassi1, Roberto Farina2, Irene Floriani3, Francesco Amodio2 and Stefania Romano2

1 Institute of Radiology, Second University of Naples, Naples, Italy.
2 Department of Diagnostic Imaging, "A. Cardarelli" Hospital, Viale Cardarelli, 9, Naples 80131, Italy.
3 Dipartimento di Oncologia, Istituto di Ricerche Farmacologiche "Mario Negri," Milan, Italy.

Received July 15, 2004; accepted after revision November 23, 2004.

 
Address correspondence to S. Romano (stefromano{at}libero.it)


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Our study was focused on the evaluation of fluid dynamics to assess the value of gray-scale and color Doppler sonography for evaluating the development of fetal swallow-related movements from early gestation until birth.

MATERIALS AND METHODS. We examined 56 fetuses from weeks 15–39 of gestation. Each fetus was examined throughout four distinct periods of gestation: weeks 15–18, 22–25, 30–34, and 37–39. During the examination, seven gray-scale sonography or color Doppler sonography patterns and their prevalence were considered.

RESULTS. Mandibular and/or labial movements ({chi}2 = 56.4, p < 0.0001) and their rhythmic activity ({chi}2 = 41.4, p < 0.0001) were seen on gray-scale sonography in an increasing percentage of fetuses as gestational age increased. Doppler findings showed an increase for nose–mouth flow signals ({chi}2 = 57.6, p < 0.0001), larynx–esophagus flow signals ({chi}2 = 13.2, p = 0.0003), and effective swallowing ({chi}2 = 36.0, p < 0.0001) as gestational age increased.

CONCLUSION. There is a trend in the fetus toward development of increased coordinated movement and more functional nose–mouth flow with increasing gestational age: 32.1% of the 56 fetuses in our series achieved effective swallowing at 37–39 weeks, on the basis of gray-scale and Doppler evaluations. Knowledge of the physiologic mechanism involving swallowing development may allow identification of altered swallow-related movements in fetuses with malformations of the digestive tract or with neurologic disorders.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The human fetus shows swallowing movements as early as week 11 of gestation, whereas more complex sucking movements can be identified during weeks 18–20 [1].

In the past, swallow-related movement was usually regarded as a mere acquiring of a mechanism necessary for postnatal life. However, recently it was proven that such function is necessary to the development of the gastrointestinal tract and to fetal growth [2, 3]: experimental studies, in which esophagus ligations in rabbit [46] and in sheep [7, 8] fetuses were performed, confirmed these views by documenting severe atrophy of the gastroenteric mucous membrane.

Sonography allows direct visualization of the anatomic structures involved in the swallowing process in the fetus [913] as well as in the neonate and adult [14]. More recently, color Doppler sonography has been used for investigating swallowing mechanisms in human fetuses at 36–41 weeks of gestation [15]; however, our study was focused on the evaluation of fluid dynamics in relation to swallowing activity from week 15 of gestation with the purpose of describing the evolution of fetal swallowing dynamics from early gestational age until birth to better assess the progression of these physiologic movements.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Eighty-two consecutive pregnant women underwent gray-scale and color Doppler sonography examinations during weeks 15–39 of gestation. After the initial study, 26 of the 82 fetuses were excluded from further evaluation because of low physiologic weight, physical malformations, or both. Thus, the remaining 56 healthy subjects were enrolled in our study. The 56 mothers had a median age of 26.5 years, ranging from 21 to 33.

Each fetus was examined throughout four distinct periods of gestation: weeks 15–18, 22–25, 30–34, and 37–39. Postnatal follow-up sonography examinations of swallowing function were performed 6 and 12 months after birth to document any eventual abnormality

All examinations were performed using a sonography unit equipped with a 3.5–5-MHz multifrequency convex probe (Logic 500 MD, GE Healthcare). The mean time needed for the examination was 30 min. Our study protocol included gray-scale sonography to investigate morphologic and biometric parameters and color Doppler sonography to evaluate fetus–placenta perfusion. Then, the sonography studies focused on the orohypopharyngeal region to reveal the movements related to swallowing. During the examination, seven gray-scale sonography or color Doppler sonography patterns and their prevalence were considered: first, the presence of labial, lingual, and/or mandibular movements at gray-scale sonography; second, the presence of rhythmic labial, lingual, or mandibular movements at gray-scale sonography; third, evidence of flow signals in the oral or nasal cavity or in both cavities at color Doppler sonography; fourth, detection of flow signals indicating fluid passage in the nose–mouth direction at color Doppler sonography; fifth, evidence of flow signals indicating fluid passage in the mouth–nose direction at color Doppler sonography; sixth, contemporary flow signals in the esophagus and in the larynx at color Doppler sonography; and seventh, effective swallow-related movement at color Doppler sonography. Swallowing was described as "effective" when oronasal regurgitation was either absent or very slight and fluid flow was shown in the hypopharynx.

At gray-scale sonography in the sagittal plane, the hypopharynx was identified as a triangle with its apex downward that was anechoic and distended according to the quantity of fluid swallowed, and it was visualized on color Doppler sonography as craniocaudally directed flow signals. A median vertical line tangent to the base of the tongue was adopted as a criterion to distinguish the hypopharynx from the laryngeal area situated posteriorly and anteriorly to the median axis, respectively.

Scans obtained in the sagittal and axial planes were always included in our study protocol. For sagittal scanning, the probe was oriented directly toward the face of the fetus: A technically correct scan may accurately reproduce the entire fetus profile from forehead to chin. Serial axial scans were also used for integrating visualization on the sagittal plane. Color Doppler sonography allowed identification of flow in the oral or nasal cavity or in both cavities, but it could not show the passage through the pharynx or esophagus and was not able to depict reflux phenomena.

Doppler sonography examination has been set at values of low-velocity flow (postrepetition frequency [PRF] values between 0.6 and 1.0 kHz) to identify phenomena of amniotic liquid suction from the mouth or nose and fluid ejection from the same tract. The focal point of the probe, and thus the Doppler zero-shift value, was placed on a plane slightly posterior to the proximal pharynx segment to accurately identify the flow direction.

All gray-scale and color Doppler sonography examinations were recorded; as soon as rhythmic mandibular or labial movements were visible, color Doppler imaging was activated and the examination was recorded by a video recorder (S-VHS, Sony) or a magneto-optical unit on a 125-MB cartridge (MTO, Mitsubishi). We prefer the cartridge system, despite its lower frame rate, because it provides better resolution on a single image than VHS film.

All the examinations were performed and reviewed by three radiologists with proven experience in obstetric and fetal sonography. The examination was performed in real time by one, and the images were reviewed by the others. The final annotation of the imaging findings for the study was made by consensual agreement of all the observers.

The trend over time of the studied variables was described by means of the Kaplan-Meier method and analyzed with the Mantel-Haenszel chi-square test for the linear and quadratic trend. All reported p values are two-sided. Analyses were performed using an SAS system (version 8.20, SAS Institute).


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The results of the present study are summarized in Table 1 and described in Figures 1A, 1B, 1C, 1D, and 1E.


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TABLE 1: Prevalence of Gray-Scale and Color Doppler Sonography Patterns in 56 Examined Fetuses

 


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Fig. 1A Graphs show Kaplan-Meier curves for trend over time. Mandibular and/or labial movements ({chi}2 = 56.4, p < 0.0001).

 


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Fig. 1B Graphs show Kaplan-Meier curves for trend over time. Rhythmic mandibular and/or labial movements ({chi}2 = 41.4, p < 0.0001).

 


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Fig. 1C Graphs show Kaplan-Meier curves for trend over time. Nose–mouth flow signals ({chi}2 = 57.6, p < 0.0001).

 


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Fig. 1D Graphs show Kaplan-Meier curves for trend over time. Larynx–esophagus flow signals ({chi}2 = 13.2, p = 0.0003).

 


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Fig. 1E Graphs show Kaplan-Meier curves for trend over time. Effective swallowing ({chi}2 = 36.0, p < 0.0001). Oronasal flow signal presented quadratic trend, so it is impossible to visualize as cumulative incidence.

 

Mandibular and/or labial movements ({chi}2 = 56.4, p < 0.0001) and their rhythmic activity ({chi}2 = 41.4, p < 0.0001) were seen on gray-scale sonography in an increasing percentage of fetuses as gestational age increased. Doppler findings (Figs. 2, 3, 4A, 4B, 5A, and 5B) showed an increase for nose–mouth flow signals ({chi}2 = 57.6, p < 0.0001), larynx–esophagus flow signals ({chi}2 = 13.2, p = 0.0003), and effective swallowing ({chi}2 = 36.0, p < 0.0001) as the gestational age increased. A statistically significant quadratic trend was detected for oronasal flow signals ({chi}2 = 8.17, p = 0.0168).



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Fig. 2 Sagittal sonogram of fetus at gestational age of 24 weeks shows evidence of fluid flow signals in nasal cavity (arrow) with moderate reflux back from oral cavity (asterisk).

 


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Fig. 3 Sagittal color Doppler sonogram of fetus at gestational age of 26 weeks shows evidence of fluid flow signals in oral cavity (arrow) and distention of hypopharynx without visualization of flow (arrowheads). Other flow areas in image correspond to umbilical artery (white asterisk) and aortic arch (black asterisk).

 


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Fig. 4A Sagittal oblique sonograms of fetus at gestational age of 25 weeks. Oropharynx region is on left and heart is on right. Fluid distention of larynx (asterisk, B) is probably due to immaturity.

 


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Fig. 4B Sagittal oblique sonograms of fetus at gestational age of 25 weeks. Oropharynx region is on left and heart is on right. Fluid distention of larynx (asterisk, B) is probably due to immaturity.

 


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Fig. 5A Sagittal sonograms of fetus at gestational age of 22 weeks. Distention of hypopharynx (diamond) without visualization of flow.

 


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Fig. 5B Sagittal sonograms of fetus at gestational age of 22 weeks. Visualization of fluid flow in hypopharyngeal triangle (diamond) and in esophagus not accompanied by oronasal regurgitation, defined as "effective" swallowing.

 
At the postnatal follow-up sonography evaluations of swallowing function, no abnormalities or evidence of reflux were observed in the infants, all of whom were asymptomatic.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Studies have shown that the sheep fetus swallows approximately 500 mL daily of a liquid composed of amniotic fluid and oronasal and pulmonary secretions [16, 17]. Moreover, the human fetus normally swallows about 700 mL of fluid at the end of gestation [18]. Sonography examination allows an analytic study of fetal swallow movements. Improvements in sonography equipment and techniques of examination since the early 1980s have made this possible. Rhythmic lingual and mandibular movements demonstrating suction have been identified from week 11 of gestation and have been shown to increase as pregnancy progressed [19, 20]. Since 1985, it has been possible to directly visualize amniotic fluid flow in fetal cavities, combining gray-scale sonography examination with Doppler spectrum, particularly with color Doppler sonography [10, 21, 22]. Petrikovsky et al. [15] first used the combination of gray-scale sonography and color Doppler sonography for evaluating fetal swallowing mechanisms. They studied fetuses from 36 to 41 weeks of gestation.

In our study, we extended the observation period from 15 weeks of gestation with the purpose of following the evolution of fetal swallowing dynamics from an early gestational age until birth in term newborns in whom no swallowing disorders were seen at birth. Using the new color Doppler machines now available, which allow easier detection of low-velocity and low-frequency flow, we noted that the rhythmic mandibular and/or labial movements, considered in the past as sucking movements [19, 20], are not always related to fluid passage into the oral or nasal cavity or into both cavities, unless fluid quantity is large enough to produce color flow signals.

From our observations, we should consider the suction mechanism only when rhythmic mandibular and/or labial movements are followed by evidence of flow signals in oronasal cavities. We noted that the mouth–nose flow, which can be regarded as a regurgitation mechanism, occurs rarely compared with nose–mouth flow; it cannot be visualized from week 37 of gestation in the normal fetus. Our data may suggest that swallow-related movement—that is, antiregurgitation reflex mechanisms—appears from week 15 of gestation and can be considered complete at the end of a normal pregnancy.

Nose–mouth flow movements occur more frequently than mouth–nose movements, and their number tends to increase as the pregnancy proceeds. These flow movements can be partially related to the progressive development of respiratory functions.

Effective swallowing-related movements have not been documented before week 18 of gestation to our knowledge, but its visualization becomes increasingly frequent. Such movement was recorded in 32.1% of the fetuses after week 37 of gestation in our study.

Visualization of the hypopharynx is important to study swallowing activity. Richards and Farah [11] observed a positive correlation between the size of the fluid-filled pharynx and gestational age, and Petrikovsky et al. [12] postulated that dilated appearance of the fetal pharynx is a cyclic event that is related to swallowing activity.

We consider the triangular depiction of the hypopharynx on combined gray-scale and color Doppler sonography, which has not been described before, as evidence that swallowing has occurred when no evidence of flow-inverted direction phenomena, which can be ascribed to regurgitation toward the oral cavity, is seen at the level of this hypopharyngeal triangle. When this triangle is well shown on color Doppler sonography, we consider that finding to indicate the presence of an effective swallow-related movement. Rarely, the subsequent flow passage into the esophagus can be noted as a progression of the color signal, probably because of the limited flow velocity. A simultaneous signal in the respiratory tract and esophagus appears rarely: we did not identify any color signal below the larynx. The simultaneous flow, probably due to poor coordination caused by immaturity, has never been visualized either before week 21 or after week 27 of gestation, to our knowledge. We documented effective swallow-related movements in fetuses between weeks 22 and 25 of gestation.

Before week 11 of gestation, neither real-time gray-scale sonography nor color Doppler sonography has identified any movement related to fetal swallowing. From week 11 to 18 of gestation, real-time sonography examination shows phenomena related to swallowing (suction), whereas color Doppler sonography usually does not show them. Occasionally, color Doppler sonography shows swallowing as rare color spots in the oral or nasal cavity or in both cavities. From week 19 to 28 of gestation, color Doppler imaging shows swallowing movements that often are uncoordinated and, for the most part, present regurgitation phenomena. During this gestational age, color Doppler sonography allows visualization of the hypopharyngeal triangle. From week 29 of gestation to the end of pregnancy, color Doppler sonography shows swallow-related movements becoming increasingly coordinated while regurgitation phenomena decrease in frequency. These findings confirm that fetal swallowing mechanisms are developing gradually during gestation, having partly existed in the first weeks of gestation.

Sonography evaluation may have an important role in prenatal indexes of emerging aerodigestive skills [13]. The current color Doppler technology allows visualization of flow in the esophageal lumen only occasionally and never within trachea. In the future, if power Doppler imaging is performed as a useful adjunct in addressing ingestive and respiratory functions in the developing fetus, as has been proposed [23], it will be interesting to consider the increasing importance of 3D sonography for the assessment of this fetal mechanism.

Fetal swallowing activity contributes importantly to fetal and amniotic fluid homeostasis and to fetal and gastrointestinal development. Our study includes an extended observation period from week 15 of gestation until birth and shows the development of fetal swallowing dynamics. Our results, based on gray-scale and color Doppler evaluations, show that there is a trend in the fetus toward development of increasingly coordinated movement and more functional nose–mouth flow with increasing gestational age, with 32.1% of the fetuses in our series of 56 fetuses achieving effective swallowing at 37–39 weeks of gestation.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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