sensors-18-04240
sensors-18-04240
Article
Bowel Sounds Identification and Migrating Motor
Complex Detection with Low-Cost Piezoelectric
Acoustic Sensing Device
Xuhao Du 1, * , Gary Allwood 1 , Katherine Mary Webberley 1 , Adam Osseiran 2 and
Barry J. Marshall 1
1 The Marshall Centre for Infectious Diseases Research and Training (M504),
The University of Western Australia, Crawley, WA 6009, Australia; [email protected] (G.A.);
[email protected] (K.M.W.); [email protected] (B.J.M.)
2 School of Engineering, Edith Cowan University, Joondalup, WA 6027, Australia; [email protected]
* Correspondence: [email protected]; Tel.: +61-08-6457-2516
Received: 26 October 2018; Accepted: 29 November 2018; Published: 3 December 2018
Abstract: Interpretation of bowel sounds (BS) provides a convenient and non-invasive technique to
aid in the diagnosis of gastrointestinal (GI) conditions. However, the approach’s potential is limited
by variation between BS and their irregular occurrence. A short, manual auscultation is sufficient to
aid in diagnosis of only a few conditions. A longer recording has the potential to unlock additional
understanding of GI physiology and clinical utility. In this paper, a low-cost and straightforward
piezoelectric acoustic sensing device was designed and used for long BS recordings. The migrating
motor complex (MMC) cycle was detected using this device and the sound index as the biomarker
for MMC phases. This cycle of recurring motility is typically measured using expensive and invasive
equipment. We also used our recordings to develop an improved categorization system for BS.
Five different types of BS were extracted: the single burst, multiple bursts, continuous random sound,
harmonic sound, and their combination. Their acoustic characteristics and distribution are described.
The quantities of different BS during two-hour recordings varied considerably from person to person,
while the proportions of different types were consistent. The sensing devices provide a useful tool for
MMC detection and study of GI physiology and function.
1. Introduction
For centuries, auscultation has been used as a non-invasive technique in medicine [1]. The most
commonly studied organs were, and still are, the lungs and the heart, with doctors long using sounds
to diagnose disease in the cardiovascular and respiratory systems [2–4]. Sounds have more recently
been exploited as biomarkers in fields as diverse as joint ageing and degeneration [5], and placental
pathophysiology [6].
Doctors have also listened to gut noises to diagnose conditions such as bowel obstructions and
paralytic ileus based on the nature or absence of bowel sounds (BS) [4]. In 1905, the first scientific study
of bowel auscultation was reported by Cannon [7]. Cannon found that the gut produced rhythmic
noises, most likely from the peristaltic movement of the intestines, plus continuous random noises
varying in location and intensity. His study prompted many researchers to try to understand the
relationship between BS and gastrointestinal (GI) physiology and disease. To date, automatic or
computerized gut-noise-based diagnosis and prognosis has not been widely developed or adopted.
However, detected BS are known to have distinctive characteristics, indicating that they are generated
by different bowel movements. Therefore, BS must contain meaningful information about the processes
inside the bowel which could be analyzed systematically [8,9]. The irregular pattern and occurrence of
BS means that the potential of short recordings is limited and that methods allowing longer recordings
of BS are required to fully exploit this approach.
BS generation is linked with gastrointestinal motility and a key physiological phenomenon
underlying motility, the migrating motor complex (MMC) [10]. The MMC is a cyclic, recurring motility
pattern that occurs in the stomach and small bowel during fasting. It has a housekeeping role, ensuring
contents move forward through the gastrointestinal tract. The MMC repeats every 80 to 150 min [10]
with three different phases. The detection of MMC cycle can have significant clinical importance [11,12].
During the fasting state, the absence of MMC might indicate small intestinal bacterial overgrowth, due
to a motility disorder. It is also commonly measured during clinical trials of new drugs developed
to alter motility [10]. Although monitoring of the MMC is important, detection of the MMC and
other measure of motility involves expensive, invasive, and uncomfortable procedures [12,13].
For example, the MMC is usually detected using antropyloroduodenal manometry. The method
typically uses water-perfused manometric catheters or solid-state sensors mounted on motility
catheters. Tube placement usually requires upper GI endoscopy and skilled technical support [12].
The relationship between MMC and BS was first proposed by Tomomasa et al. in 1999 [10].
They found that the sound index, which is the sum of absolute signal amplitudes, links with the MMC
cycle due to the BS generation mechanism. Within a five-hour recording, they observed two MMC
cycles. Thus, this sound index shows potential as a biomarker for clinical use. The BS can be divided
into small popping sounds and huge gurgling sounds, which are significantly different in amplitude.
Therefore, we hypothesize that the sound index might be dominated by the gurgling sounds due to
their large amplitude. Also, it is important to identify different kinds of BS in the different phases of
MMC to better understand if the sound index could act as a reliable biomarker for the MMC. This paper
proposes to use the sound duration for indicating either the popping sound or large sound and identify
the dominant sound during MMC phases. We also demonstrate the effectiveness of our simple and
low-cost acoustic sensing device designed for long recordings of BS.
Microphone-based sensors are popular for BS recording [14–20]. In 2013, Sakata et al. developed
a silicon microphone-based sensor for long-term BS recording [15]. They studied sound occurrence
over time before and after eating. Kim et al. used a similar microphone-based sensor attached to
the abdomen for long-term BS recordings [16,21]. They extracted the jitter and shimmer from BS for
gut motility estimation. Spiegel et al. built a microelectronic microphone for gut motility monitoring
via BS [17]. Their sensor and associated algorithm can distinguish healthy controls from patients
recovering from abdominal surgery and predict which patients will develop postoperative ileus. Use of
a microphone for BS recording is straightforward. However, it requires a power supply, which could
cause inconvenience. Since microphone-based sensors are sensitive to airborne noise, the ambient
noise might easily contaminate the BS signal. Emoto et al. proposed a non-contact microphone for BS
recorded and used their system to identify gut motility before and after soda intake [19,20]. However,
their participants were required to lie down on a bed for recordings, which is inconvenient for long
recordings. A piezoelectric-based sensor is another choice for passively recording physiology focused
sound and vibration [22,23]. Dimoulas et al. have done much research using long recording of BS
signals, which were recorded by piezoelectric-based sensor [24,25]. However, the exact structure of
their sensor is never mentioned, and their studies mainly focused on signal processing and BS types
classification. Due to the way BS are conducted through the abdomen, a piezoelectric-based sensing
device is suitable for BS recording as it is more sensitive to vibration trigger signals and can sit on
the skin to pick these up. Furthermore, it is much less sensitive to ambient air borne noise. In this
study, a piezoelectric acoustic sensing device was developed and decomposed for demonstration.
Its design makes it low cost, easy to make, less noise contaminated, and accurate enough for longer BS
recordings, making it suitable for research and probably clinical use.
Sensors 2018, 18, 4240 3 of 12
The proposed device can be evaluated by comparing the observed BS with previous studies.
Different BS classification methods have been investigated, although no standard definitions or classes
of BS have been established. In 1967, Watson and Knox described three different types of BS by
analyzing the sounds from three participants [26], including BS with a regular pattern, rising pitch and
crescendo intensity, BS with unregulated patterns, and tinkling BS. Dalle et al. also reported three types
of BS, using their durations as the basis of a classification index [27]. Dalle et al. are also noteworthy
because they pioneered the use of computers to analyze BS. Dimoulas et al. classified BS into five
different categories based on their waveforms and perceived characteristics [25]. These five types
comprised solitary clicks, repeated clicks, sequences of irregularly concatenated segments, crepitating
sweeps, and whistling sweeps. The authors also linked them to different gut activities. Ulusar
recognized BS as single bursts and multiple bursts based on their waveform to build a BS classification
model using Bayesian theory. Du et al. also proposed a mathematical model for BS generation to
explain different types of BS [28]. As summarized above, there are several classifications of BS based
on different sound characteristics, and the quantities of different types of BS were not studied in
their work. However, the quantities may be important for gut motility detection. The most common
classification indexes include duration, frequency, waveform, auditory perception, and mechanisms for
the production of BS. This paper will also summarize different types of BS based on our observations.
We also analyzed the quantities of the BS types across and within participants.
This study presents a low-cost and straightforward piezoelectric acoustic sensing device that can
effectively allow detection of BS and MMC cycle with a personal computer and commercial software
Audacity. This offers the potential of greater understanding of the physiology of the gastrointestinal
tract and possible clinical use. BS from ten participants were recorded for two hours for identification
and characterization of BS types. The observed BS were classified in a fundamental way with two
physical indexes, waveform, and spectrogram. Five different types of BS were systematically analyzed
including the duration, spectral flatness, spectral bandwidth, and mean-crossing ratio. The quantities
of different types of BS were also counted from these long-term recordings, and their quantities
proportion of different types within each participant were found to be stable. Also, in eight- and
four-hour recordings from a healthy participant, several MMC cycles and different phases were
observed under the fasting state using the sound index, and longer BS are more likely to occur in Phase
III using sound duration as another index. As expected, the cycles disappeared when the participant
consumed food.
similar performance. A stretchy tubi-grip belt was used to hold the sensor head at the right location.
This low-cost and straightforward piezoelectric sensing device can effectively detect the BS with high
accuracy compared to sensors used in previous research. Multiple bio-indexes can be observed such as
sound index, sound duration, and the MMC.
(a) (b)
Figure 1. (a) Decomposition of the real sensor and (b) its corresponding consistence including the top
lid, housing, foam, piezoelectric disk, and the membrane.
skip breakfast and recorded under fasting conditions for eight hours to see the MMC cycle. Both the
sound duration and sound index over the eight hours of recording were documented in this stage.
Another four hours recording after a meal was conducted to investigate how the MMC changed after
the meal.
(a) (b)
The most frequent type of BS in the recordings was the SB, which is a simple pulse probably caused
by a single contraction of the bowel muscle [25,28,29]. An SB, with its distinctive peak frequencies,
is noticeable in the time domain. An example of a SB is presented in Figure 2a with both the time and
frequency domain representations.
In Figure 2a, the top figure represents the time domain signal and the lower figure represents
its frequency spectrogram. The duration of the single burst is short, only 10–30 ms and no other
SB is present within 100 ms on either side. There is usually a distinct peak frequency of the SB.
The frequency of this example was around 400 Hz, but it can vary from 200 to 1000 Hz for different SB.
Sensors 2018, 18, 4240 6 of 12
The SB is comprehensively reported in the literature [27,29,32]. Since the SB occurs the most frequently,
it therefore makes up the largest proportion of the total quantity of BS.
MB can be described as a repetitive SB with a shorter interval time between adjacent components.
Figure 2b gives an example of this type of BS. Each component in the MB looks quite similar in
the spectrogram with slight differences in bandwidth and amplitude, which indicates that the MB
consists of several similar individual components. The quantities of the repetitive components are
not consistent in MB, as they vary from two to dozens within a single MB. There are clear silent gaps
between the adjacent components in the time domain and the length of these silent gaps are also
inconsistent. The spectrogram of the MB is similar to the SB, although the duration of MB is much
longer than the SB and ranges from 40 to 1500 ms. The MB is also comprehensively described in
the literature [25,29].
The CRS is shown in Figure 2c. The waveform of the CRS is usually continuous over long periods
of time ranging from 200 ms to 4000 ms without any defined silent gaps. The CRS is usually recognized
as a random sound because it has no clear rhythm or pattern. The CRS waveform is also less regular
compared to other types of BS although it occurs more often than the HS and CS. It is also clear that
the CRS often appears in a combination of other types of BS to construct a CS. It appears that CRS are
reported elsewhere in the literature references [7,25,33] with the names continuous random noises,
crepitating sweeps, and prolonged sounds.
Another typical BS is the HS, which is a whistling-like sound and is presented in Figure 2d. Three
to four clear frequency components appear in the spectrogram of the HS such as the harmonic sound,
which causes the whistling-like sound. Those peak frequencies are multiples of the fundamental
frequency, which is usually relatively low, around 200 Hz. The highest harmonics recorded in our
experiment were up to 3000 Hz. The duration of the HS ranges from 50 ms to 1500 ms. In the time
domain, a few peaks could be observed in the HS with no defined silent gaps between each peak.
Sounds of the HS type infrequently occur (see below). HS have been described in other studies [7,25,26]
with the descriptions: rhythmic noises, whistling sweeps, and regular pattern.
In addition to the above four separate types of BS, many detected BS often appear as a combination
of the types described above. Figure 2e is from a BS where the first part is a CRS, while the end contains
typical HS characteristics. The CRS and HS are not the only possible combination, every combination
of the five BS described above are possible, and all were collected during the 20 h of recordings.
These types of BS will usually last for a long time. They appear to have been previously described
by Dimoulas et al. [25] with the name “irregularly concatenated segments”. Due to their inconsistent
characteristics, their quantity and acoustic features were not directly counted and analyzed.
Table 1. The quantities and their corresponding proportion of different types of BS of 10 participants.
Although the quantity ratios across these four types of BS vary, their proportions were consistent.
The consistency can be represented by CV, which is the ratio between the standard deviation and the
mean value. It is clear that the CV of proportion is much smaller than the CV of quantities. Table 1
indicates that the most common type is SB, which makes up 87.8% of sounds on average (mean value)
with only 5.4% SD. The second most abundant type is MB, which makes up on average 7.8% of sounds
with 3.5% SD. The least type is HB, average only 0.9% and below 2% for all participants.
Several typical acoustic features were studied for different types of BS including the duration,
spectral bandwidth, spectral flatness, and mean-crossing ratio. The BS acoustic features from first and
third quadratic are shown in Table 2, and the distributions are shown in Figure 3. The amplitudes are
normalized so that in all cases the area under the curve is equal to one.
(a) (b)
(c) (d)
Figure 3. Normalized distribution (area under curve equals to one) of acoustics characteristics of four
types of BS including (a) duration; (b) mean-cross ratio; (c) spectral bandwidth; and (d) spectral flatness.
Sensors 2018, 18, 4240 8 of 12
For the duration, it is common that the SB is typically short and the duration of the other four
types of BS have a similar distribution. However, the CRS has some extra-long BS beyond 4000 ms.
The second longest type of BS is the MB, which can last up to 3000 ms. In this study, the longest
duration observed for the HS was 1800 ms. The spectral centroid is the “center of mass” of the spectrum,
where all five types of BS share similar distribution and values. The spectral bandwidth is defined as
the wavelength interval in which a radiated spectral amplitude is not less than half its maximum value.
The mean value of spectral bandwidth decreases from MB, SB, HS to CRS. The spectral bandwidth
distribution of the CRS type of BS is the narrowest at low spectral bandwidth. The spectral flatness
is a measure used in digital signal processing to characterize an audio spectrum to show how tonal
the signal is. It is interesting to note that the CRS has the smallest spectral flatness. As with spectral
bandwidth, the mean values of spectral flatness decrease from MB, SB, HS to CRS. The SB and HS
share the same distribution with different mean values, and the CRS has the narrowest distribution
again. This order is observed in the spectral bandwidth and mean-crossing ratio. The mean-crossing
ratio value is the number of times the waveform crosses its mean value. The distributions of these
five types of BS have the most significant difference among all other characteristics. The MB tend
to have a higher value with narrower distribution. The lowest mean value is that of the HS with
wide distribution.
was much larger than under the fasting state. The long BS are also spread uniformly, which indicates
high gut motility during this time. This is reasonable according to the mechanism of MMC [13].
In addition, the MMC pattern was also observed in the other ten participants from their two-hour
recording based on the sound index. As shown in Figure 5b, the peaks of Phase III were presented
from the sound index of the first three participants and the same observation of the sound duration
was obtained. Also, two Phase III peaks with 77.2 min interval time were observed in Participant
No. 2. The preliminary tests further demonstrate the utility of our simple, non-invasive acoustic
sensing device.
(a)
(b)
Figure 4. The scaled sound index of BS every three minutes (black curve) and sound duration
(red curve) over eight hours under fasting at (a) upper quadrant and (b) lower quadrant.
(a)
Figure 5. Cont.
Sensors 2018, 18, 4240 10 of 12
(b)
Figure 5. The scaled sound index of BS and the sound duration at lower quadrant (a) over four hours
after meal from participant L and (b) over two hours under fasting stage from participant No. 1 to 3.
We also studied the mean BS quantities before and after the meal over the eight- and four-hour
recording. The means were 3.09 and 7.12 BS per minute for the upper and lower abdomens respectively,
from the first eight hours of recording. From the recording after meal, there were on average 4.59 and
45.88 BS per minute detected at the upper and lower abdomen, respectively. These quantities indicate
a significant increase in gut activity in the lower abdomen after eating.
4. Conclusions
A low-cost and straightforward acoustic sensing device was proposed in this paper to enable long
duration BS recordings. The sensor head consisted of only a piezoelectric sensor, housing, membrane,
and a piece of foam. The performance of the device has been tested with two hours of recording from
each of the ten participants and an eight- and four-hour recording from one participant. We undertook
analysis of BS from ten volunteers with the proposed sensing device. Our simple sensor heads were
able to pick up previously described BS types. However, we were also able to improve characterization
of BS types and produce a standard categorization system. Based on our analysis, we found five
different characteristic types of BS based on their waveform and spectrogram. The first four separate
types of BS comprise the single burst, multiple bursts, CRS, tone sound, harmonic sound, and the
last one is their combination. Their behavior and characteristics were described, and the quantities
of different types recorded from each participant were counted. These quantities varied significantly
from person to person, from 0.04 to 0.7 per second. However, the proportions of different types of
BS were reasonably stable. The mean proportion of SB sounds was 87.8% ± 5.4%, mean multiple
bursts proportion was 7.8% ± 3.5%, mean continues random sound proportion was 3.5% ± 2.0%,
and the mean proportion harmonic sound was 0.9% ± 0.5%. Also, from the eight- and four-hour
recording, six MMC cycles were successfully observed based on the sound index with clear phases
identifiable under the fasting state, and, as expected, the MMC disappeared once the participant
consumed food. The MMC cycle was also observed from the two-hour-long recordings taken from
ten other participants. This study also shows that when the gut enters MMC Phase II and III, longer
BS were generated due to the increased gut activity by looking at the sound duration. This result
shows that this simple and low-cost acoustic sensing device can effectively detect the MMC cycle by
using the sound index as its biomarker. This work will help in further bowel sound studies with long
recordings by providing guidance on the design of an effective acoustic sensing device and may aid in
the development of new methods for understanding GI physiology.
Author Contributions: Conceptualization, B.J.M., A.O. and K.M.W.; methodology, X.D., K.M.W. and G.A.;
software, X.D.; Hardware: G.A.; validation, X.D., K.M.W. and G.A.; formal analysis, X.D.; investigation,
X.D., K.M.W. and G.A.; resources, B.J.M., A.O. and K.M.W.; data curation, X.D., K.M.W. and G.A.; writing—original
draft preparation, X.D.; writing—review and editing, K.M.W. and G.A.; visualization, X.D..; supervision, K.M.W.;
project administration, K.M.W.; funding acquisition, B.J.M.
Funding: The study was funded by the McCusker Charitable Foundation, who played no role in the study design
or analysis.
Acknowledgments: We are also grateful to Andrisha-Jade Inderjeeth for bowel sound verification.
Sensors 2018, 18, 4240 11 of 12
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.
Abbreviations
The following abbreviations are used in this manuscript:
BS Bowel Sound
SB Single Burst
MB multiple bursts
CRS Continue Random Sound
HS Harmonic Sound
MMC Migrating Motor Complex
SD Standard Deviation
CV Coefficient of Variation
References
1. Hanna, I.R.; Silverman, M.E. A history of cardiac auscultation and some of its contributors. Am. J. Cardiol.
2002, 90, 259–267. [CrossRef]
2. Kim, J.W.; Kim, J.; Kim, T.; Lee, K.; Kim, S.; Bae, M. Extraction of acoustic biomarkers from PSG to detect osa.
Sleep Med. 2017, 40, e160. [CrossRef]
3. Kim, T.; Kim, J.W.; Lee, K. Detection of sleep disordered breathing severity using acoustic biomarker and
machine learning techniques. Biomed. Eng. Online 2018, 17, 16. [CrossRef] [PubMed]
4. Talley, N.J.; O’Connor, S. Clinical Examination: A Systematic Guide to Physical Diagnosis; Elsevier Health
Sciences: Amsterdam, The Netherland, 2013.
5. Shark, L.K.; Chen, H.; Goodacre, J. Knee acoustic emission: A potential biomarker for quantitative assessment
of joint ageing and degeneration. Med. Eng. Phys. 2011, 33, 534–545. [CrossRef] [PubMed]
6. Riknagel, D.; Al Humaidan, P.H.; Farlie, R.; Zimmermann, H.; Ramsing, M.; Struijk, J. Acoustic biomarker of
placental pathophysiology and adverse fetal outcome. Placenta 2015, 36, A6. [CrossRef]
7. Cannon, W.B. Auscultation of the rhythmic sounds produced by the stomach and intestines. Am. J.
Physiol.-Leg. Content 1905, 14, 339–353. [CrossRef]
8. Inderjeeth, A.J.; Webberley, K.M.; Muir, J.; Marshall, B.J. The potential of computerised analysis of bowel
sounds for diagnosis of gastrointestinal conditions: A systematic review. Syst. Rev. 2018, 7, 124. [CrossRef]
[PubMed]
9. Du, X.; Allwood, G.; Webberley, K.M.; Inderjeeth, A.J.; Osseiran, A.; Marshall, B.J. Tu2017-Non-Invasive
Diagnosis of Irritable Bowel Syndrome via Novel Bowel Sound Features: Proof of Principle. Gastroenterology
2018, 154, S1370. [CrossRef]
10. Tomomasa, T.; Morikawa, A.; Sandler, R.H.; Mansy, H.A.; Koneko, H.; Masahiko, T.; Hyman, P.E.; Itoh, Z.
Gastrointestinal sounds and migrating motor complex in fasted humans. Am. J. Gastroenterol. 1999, 94, 374.
[CrossRef] [PubMed]
11. Takahashi, T. Interdigestive migrating motor complex—Its mechanism and clinical importance. J. Smooth
Muscle Res. 2013, 49, 99–111. [CrossRef] [PubMed]
12. Camilleri, M.; Linden, D.R. Measurement of gastrointestinal and colonic motor functions in humans and
animals. Cell. Mol. Gastroenterol. Hepatol. 2016, 2, 412–428. [CrossRef] [PubMed]
13. Medhus, A.; Sandstad, O.; Bredesen, J.; Husebye, E. The migrating motor complex modulates intestinal
motility response and rate of gastric emptying of caloric meals. Neurogastroenterol. Motil. 1995, 7, 1–8.
[CrossRef] [PubMed]
14. Ulusar, U.D.; Canpolat, M.; Yaprak, M.; Kazanir, S.; Ogunc, G. Real-time monitoring for recovery of
gastrointestinal tract motility detection after abdominal surgery. In Proceedings of the 2013 7th International
Conference on Application of Information and Communication Technologies (AICT), Azerbaijan, Baku,
23–25 October 2013; pp. 1–4.
15. Sakata, O.; Suzuki, Y.; Matsuda, K.; Satake, T. Temporal changes in occurrence frequency of bowel sounds
both in fasting state and after eating. J. Artif. Organs 2013, 16, 83–90. [CrossRef] [PubMed]
Sensors 2018, 18, 4240 12 of 12
16. Kim, K.S.; Seo, J.H.; Ryu, S.H.; Kim, M.H.; Song, C.G. Estimation algorithm of the bowel motility based
on regression analysis of the jitter and shimmer of bowel sounds. Comput. Methods Programs Biomed. 2011,
104, 426–434. [CrossRef]
17. Spiegel, B.M.; Kaneshiro, M.; Russell, M.M.; Lin, A.; Patel, A.; Tashjian, V.C.; Zegarski, V.; Singh, D.;
Cohen, S.E.; Reid, M.W.; et al. Validation of an acoustic gastrointestinal surveillance biosensor for
postoperative ileus. J. Gastrointest. Surg. 2014, 18, 1795–1803. [CrossRef] [PubMed]
18. Kaneshiro, M.; Kaiser, W.; Pourmorady, J.; Fleshner, P.; Russell, M.; Zaghiyan, K.; Lin, A.; Martinez, B.;
Patel, A.; Nguyen, A.; et al. Postoperative gastrointestinal telemetry with an acoustic biosensor predicts
ileus vs. uneventful GI recovery. J. Gastrointest. Surg. 2016, 20, 132–139. [CrossRef] [PubMed]
19. Sato, R.; Emoto, T.; Gojima, Y.; Akutagawa, M. Automatic Bowel Motility Evaluation Technique for
Noncontact Sound Recordings. Appl. Sci. 2018, 8, 999. [CrossRef]
20. Emoto, T.; Abeyratne, U.R.; Gojima, Y.; Nanba, K.; Sogabe, M.; Okahisa, T.; Akutagawa, M.; Konaka, S.;
Kinouchi, Y. Evaluation of human bowel motility using non-contact microphones. Biomed. Phys. Eng. Express
2016, 2, 045012. [CrossRef]
21. Kim, K.S.; Seo, J.H.; Song, C.G. Non-invasive algorithm for bowel motility estimation using
a back-propagation neural network model of bowel sounds. Biomed. Eng. Online 2011, 10, 69. [CrossRef]
[PubMed]
22. Rao, A.; Ruiz, J.; Bao, C.; Roy, S. Tabla: A Proof-of-Concept Auscultatory Percussion Device for Low-Cost
Pneumonia Detection. Sensors 2018, 18, 2689. [CrossRef] [PubMed]
23. Farooq, M.; Sazonov, E. Automatic measurement of chew count and chewing rate during food intake.
Electronics 2016, 5, 62. [CrossRef] [PubMed]
24. Dimoulas, C.; Kalliris, G.; Papanikolaou, G.; Kalampakas, A. Novel wavelet domain Wiener filtering
de-noising techniques: Application to bowel sounds captured by means of abdominal surface vibrations.
Biomed. Signal Process. Control 2006, 1, 177–218. [CrossRef]
25. Dimoulas, C.A.; Papanikolaou, G.; Petridis, V. Pattern classification and audiovisual content management
techniques using hybrid expert systems: A video-assisted bioacoustics application in abdominal sounds
pattern analysis. Expert Syst. Appl. 2011, 38, 13082–13093. [CrossRef]
26. Watson, W.; Knox, E. Phonoenterography: The recording and analysis of bowel sounds. Gut 1967, 8, 88.
[CrossRef] [PubMed]
27. Dalle, D.; Devroede, G.; Thibault, R.; Perrault, J. Computer analysis of bowel sounds. Comput. Biol. Med.
1975, 4, 247–256. [CrossRef]
28. Du, X.; Allwood, G.; Webberley, K.M.; Osseiran, A.; Wan, W.; Antonina, V.; Marshall, B.J. A mathematical
model of bowel sound generation. J. Acoust. Soc. Am. 2018, 144, EL485–EL491.
29. Ulusar, U.D. Recovery of gastrointestinal tract motility detection using Naive Bayesian and minimum
statistics. Comput. Biol. Med. 2014, 51, 223–228. [CrossRef]
30. Ranta, R.; Louis-Dorr, V.; Heinrich, C.; Wolf, D.; Guillemin, F. Digestive activity evaluation by multichannel
abdominal sounds analysis. IEEE Trans. Biomed. Eng. 2010, 57, 1507–1519. [CrossRef]
31. Allwood, G.; Du, X.; Webberley, M.; Osseiran, A.; Marshall, B. Advances in Acoustic Signal Processing
Techniques for Enhanced Bowel Sound Analysis. IEEE Rev. Biomed. Eng. 2018. [CrossRef]
32. Dimoulas, C.; Kalliris, G.; Papanikolaou, G.; Petridis, V.; Kalampakas, A. Bowel-sound pattern analysis
using wavelets and neural networks with application to long-term, unsupervised, gastrointestinal motility
monitoring. Expert Syst. Appl. 2008, 34, 26–41. [CrossRef]
33. Ching, S.S.; Tan, Y.K. Spectral analysis of bowel sounds in intestinal obstruction using an electronic
stethoscope. World J. Gastroenterol. 2012, 18, 4585. [CrossRef] [PubMed]
34. Craine, B.L.; Silpa, M.; O’toole, C.J. Computerized auscultation applied to irritable bowel syndrome.
Dig. Dis. Sci. 1999, 44, 1887–1892. [CrossRef] [PubMed]
35. Ozawa, T.; Saji, E.; Yajima, R.; Onodera, O.; Nishizawa, M. Reduced bowel sounds in Parkinson’s disease
and multiple system atrophy patients. Clin. Auton. Res. 2011, 21, 181–184. [CrossRef] [PubMed]
c 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).