Esophageal body motility in people with diabetes: Comparison with non-diabetic healthy individuals

diabetes research and clinical practice 97 (2012) 77–81

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Diabetes Research and Clinical Practice journ al h ome pa ge : www .elsevier.co m/lo cate/diabres

Esophageal body motility in people with diabetes: Comparison with non-diabetic healthy individuals§ Joa˜o Xavier Jorge a,*, Edgard Augusto Pana˜o b, Ma´rio Amaral Simo˜es a, Cla´udia Iracema Cardoso Borges c, Fernando Jorge Delgado d, A´lvaro Correia Coelho d, Amı´lcar Lima Silva d, Carlos Costa Almeida a a

Faculty of Medicine, University of Coimbra, Portugal Service of Gastroenterology, Hospital Centre of Coimbra, Portugal c Service of Internal Medicine, Hospital of Leiria, Portugal d Service of Internal Medicine, Hospital Centre of Coimbra, Portugal b

article info

abstract

Article history:

Aims: The aim of this study was to compare esophageal motor characteristics between

Received 15 November 2011

diabetics and healthy individuals.

Received in revised form

Methods: Esophageal manometry was performed in 34 type 2 diabetics and 32 healthy

23 January 2012

individuals. Waves were evaluated in the 3 thirds of the esophagus (P1 = upper, P2 = middle,

Accepted 30 January 2012

and P3 = distal).

Published on line 2 March 2012

Results: In diabetics vs. controls, wave distribution was as follows: peristaltic waves,

Keywords:

p < 0.01; no transmitted waves, 10.62  20.7% vs. 2.75  3.0%, p < 0.002; and retrograde

83.5  22.2% vs. 96.3  4.4%, p < 0.002; simultaneous waves, 3.26  5.8% vs. 0.53  1.3%, Esophagus

waves, 2.68  4.0% vs. 0.31  1.1%, p < 0.03. Wave amplitude was similar between groups.

Motility

Average upstroke (mmHg/s) in diabetics vs. non-diabetics was P2, 33.8  13.9 vs. 40.2  17.7,

Diabetes

p < 0.03; and P3, 29.8  15.3 vs. 41.3  14.0, p < 0.002.

Healthy individuals

Conclusions: (1) Simultaneous waves, no transmitted waves, and retrograde esophageal waves were significantly more frequent in diabetics. (2) Average upstroke was significantly lower within the middle and distal esophagus of diabetic individuals. (3) Wave amplitude was similar in both groups. # 2012 Elsevier Ireland Ltd. All rights reserved.

1.

Introduction

Esophageal dysmotility, as well as gastroparesis, appears to be common in patients with diabetes [1–6], particularly those with gastrointestinal symptoms [7–9]. However, some such patients may have no esophageal or gastrointestinal symptoms [10,11]. Alterations in the motor activity of the esophagus have been observed in healthy individuals in several studies. §

The presence of ineffective or simultaneous esophageal waves appears to be common in healthy individuals and, within specific limits, can be considered normal [12,13]. Further, it has been observed that maximum active tension in healthy individuals deteriorates as a function of age and that the esophagus becomes stiffer with age. Changes such as increased stiffness and reduced primary and secondary peristalsis have been observed in the esophagus of healthy

Grant support: This study was supported by the Enterprise Sonangol. * Corresponding author at: Urbanizac¸a˜o Nova Conı´mbriga II, lote B1, r/c posterior, 3150-220 Condeixa-a-Velha, Portugal. Tel.: +351 239100907; fax: +351 239100907. E-mail address: [email protected] (J.X. Jorge). 0168-8227/$ – see front matter # 2012 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.diabres.2012.01.036

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diabetes research and clinical practice 97 (2012) 77–81

individuals, with deterioration of esophageal function evident after the age of 40 years [14]. In patients with diabetes, the magnitude of these alterations is unclear, as is the correlation with gastrointestinal symptoms and the impact on quality of life. Studies have verified that, in diabetic patients, alterations in esophageal motility may be associated with slow gastric emptying [15], in individuals with or without neuropathy [16–19]. On the other hand, other studies have shown that symptoms of gastroesophageal reflux may not be correlated with esophageal dysmotility in diabetic patients [20]. Some authors believe that the alterations in the biomechanical properties of the esophagus observed in diabetics reflect, to some extent, intra-structural tissue alterations caused by the disease [21]. Reduced sensitivity to esophageal stimulation [22] and an increased frequency of distension-induced contractions have been shown to correlate with the duration of the disease, and diminution of longitudinal and radial compressive stretch [23] have been described. In diabetics with neuropathy, increased esophageal sensory thresholds have been observed compared to controls, evidencing altered central processing to visceral stimulation with involvement of both peripheral and central mechanisms [24]. Some authors have argued that the effect of acute hyperglycemia itself does not influence the esophageal sensitivity in patients with longstanding diabetes and autonomic neuropathy [25]. A decrease in the amplitude of esophageal contractions, the absence of primary peristalsis, high-frequency simultaneous or repetitive body contractions, and a decrease in the velocity of peristalsis are some of the many esophageal alterations that have been revealed [26,27]. However, 1 study comparing diabetics and non-diabetics showed no difference in the rate of acid reflux and the risk of esophageal mucosa damage [28]. Moreover, only few differences in esophageal motility have been observed between diabetics and healthy individuals [29]. Therefore, the aim of this study was to compare specific esophageal body motor characteristics of type 2 diabetic patients with those of nondiabetic healthy individuals.

2.

Materials and methods

2.1.

Subjects

A group of 34 type 2 diabetic patients (15 women and 19 men) with a mean age of 57.5  7.9 years and 32 non-diabetics (12 women and 20 men) with a mean age of 58.8  10.7 years underwent stationary computed esophageal manometry. All individuals participated voluntarily and provided written informed consent. The study was approved by the Ethical Committee of the hospital where it took place. The mean duration of diabetes was 12.6  8.5 years. The HbA1c (mean  SD) was 8.21%  2.05; the fasting plasma glucose was 8.69  3.16%. The mean body mass index (BMI) was 30.9 in diabetics and 26.6 in non-diabetics, with a very significant difference ( p < 0.002). At the time of the investigation, diabetic patients were taking oral hypoglycemics (metformin, 13 patients or gliclazide, 7 patients), insulin, 6 patients, or insulin plus an oral hypoglycemic 8 patients. No patient was taking dipeptidil peptidase inhibitors. On the day of the examination,

diabetic patients took their medications only after the procedure. Pregnant women, patients who had undergone anterior gastrointestinal surgery and those with signs of autonomic neuropathy according to the coefficient of variation of the R–R interval (CVRR) by electrocardiography were excluded from the study. The CVRR was obtained according the methods descript by Castro et al. [30] and the normal range of RR interval during the expiration divided by RR interval during the expiration, >1.1, referred by Castro et al. [31]. No patient was taking medications that altered gastrointestinal motility. The number of individuals with symptoms of heartburn or reflux was 9 (26.67%) in diabetics and 6 (21.87%) in non-diabetics with no significant difference observed between groups, any patient related difficulty in swallowing. No patient had a diabetic nephropathy or retinopathy. No esophageal endoscopy, pHmetry or motor nerve conduction velocity (MCV) was performed to any participant, and it could be considered a limitations.

2.2.

Procedure

Stationary computed esophageal manometry with a water perfusion system from Medical Measurement System (MMS), UPS 2020 ULGI, Netherlands, 2000, was performed in all participants. The examination was conducted using a 6channel catheter based on the manometric technique and normality criteria of Katz et al. [32] and Richter et al. [33]. During the manometric examination, participants were in the decubitus dorsal position. The catheter was inserted through the nose into the stomach; it was then adjusted so that the last channel was positioned on the inferior esophageal sphincter. Because the sphincter has a higher pressure than the stomach and esophageal body lumen, we ensured that the 3 proximal catheter doors (P1, P2, and P3) were positioned in the lumen of the esophageal body. The distance between the 3 proximal channels or catheter doors was 5 cm. Participants were encouraged to relax for approximately 1 min before we began the examination. The participants were then asked to drink 5 mL of natural water. The computed system automatically registered manometric waves during swallowing, which was repeated 10 times for each individual. Each of 3 proximal catheter doors registered the activity of one-third of the esophagus (P1: proximal esophagus, P2: middle esophagus, and P3: distal esophagus, 2.5 cm above the inferior esophageal sphincter IOS). The esophageal waves registered by the 3 proximal channels were evaluated based on their characteristics, amplitude, average and maximum upstroke, velocity, and duration, all of which were automatically calculated by the computer. Data were analyzed with SPSS using the Student’s t-test and Mann–Whitney test-for non-parametric variables, and are presented as mean  standard deviation.

3.

Results

The wave distribution in diabetic vs. control participants was as follows: peristaltic waves, 83.5  22.2% vs. 96.3  4.4%, p < 0.002; simultaneous waves 3.26  5.8% vs. 0.53  1.3%,

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diabetes research and clinical practice 97 (2012) 77–81

Table 3 – The velocity of esophageal waves (in cm/s) in type 2 diabetic patients and non-diabetic controls in the upper to middle (P1–P2), middle to lower (P2–P3), and upper to lower (P1–P3) esophagus. Group

Fig. 1 – Distribution of esophageal waves in diabetic and control participants. Values are expressed as mean. Peristaltic waves (PW) were more frequent in control participants ( p < 0.002). All other wave types were significantly more frequent in type 2 diabetic patients: simultaneous waves = SW ( p < 0.01); no transmitted waves = NTW ( p < 0.002), and retrograde waves = RW ( p < 0.03).

Table 1 – The percentage of diabetic and non-diabetic participants with a wave distribution up to the normal range. Group Diabetics Controls p-Value

Simultaneous waves

No transmitted waves

Retrograde waves

5.8% 3.1% >0.05

14.7% 12.5% >0.05

38.2% 18.7% <0.01

The percentage of patients with retrograde waves was significantly higher in the diabetic than the control group, p < 0.01 (the normal range is: simultaneous waves, <20%; no transmitted waves, <20%; retrograde waves, 0%).

Diabetics Controls p-Value

P2–P3

P1–P3

3.5  2.9 4.9  2.7 <0.04

3.2  3.4 4.2  2.1 >0.05

Values are expressed as mean  standard deviation. The velocity was significantly higher in control than diabetic participants in P2– P3, p < 0.04.

mean values tended to be lower in diabetic vs. non-diabetic participants in all parts of the esophageal body; amplitude values were: P1, 31.9  11.5 vs. 36.2  14.7, p > 0.05; P2, 51.8  22.1 vs. 58.2  34.2, p > 0.05; and P3, 55.9  26.7 vs. 65.9  21.6, p > 0.05; mean amplitude was 46.7  17.7 vs. 52.8  16.3, p > 0.05. Average upstroke (in mmHg/s) was significantly higher in non-diabetic participants compared with diabetic patients in the middle and distal esophagus, as was mean average upstroke, as can be seen in Table 4. Maximum upstroke was significantly lower in the distal third of the esophagus in diabetic vs. non-diabetic individuals; in the other 2 proximal thirds, values were statistically similar: P1, 39.9  16.1 vs. 41.8  18.9, p > 0.05; P2, 57.7  21.8 vs. 61.8  20.0, p > 0.05; and P3, 56.9  27.7 vs. 71.6  22.5, p < 0.02; mean maximum upstroke was 51.6  17.9 vs. 59.2  16.7, p > 0.05.

4. p < 0.01; no transmitted waves 10.6  20.7% vs. 2.7  3.0%, p < 0.002; and retrograde waves, 2.7  4.0% vs. 0.3  1.1%, p < 0.03 (Fig. 1). According to the software of the MMS used, the normal distribution of waves in healthy individuals is as follows: peristaltic waves, >80%; simultaneous waves, <20%; no transmitted waves, <20%; and retrograde waves, 0%. In diabetic vs. non-diabetic participants, the percentage of individuals with a wave distribution up to this normal range was as follows: simultaneous waves, 5.8% vs. 3.1%, p > 0.05; no transmitted waves, 14.7% vs. 12.5%, p > 0.05; and retrograde waves, 38.2% vs. 18.7%, p < 0.01 (Table 1). Wave duration (in s) was higher in diabetics than in the control group, with significant differences in the middle esophagus ( p < 0.04) and the distal esophagus ( p < 0.02) (Table 2). Wave velocity was higher in non-diabetic participants compared with diabetic patients, with a significant difference seen in the middle to distal esophagus ( p < 0.04) (Table 3). Wave amplitude (in mmHg) did not differ significantly between groups, although

P1–P2 3.1  3.7 3.8  3.6 >0.05

Discussion

Most studies have shown alterations in esophageal motility in diabetic patients compared with healthy individuals. A reduction in the amplitude and frequency of effective esophageal peristalsis, a prolonged duration of peristalsis, decreased wave propagation velocity, and an increased number of simultaneous contractions in the esophageal body have been observed in diabetic individuals [9,27]. However, some authors have also recorded waves with a higher amplitude and broader wave peristalsis [16] or a decrease in the duration of contractions in such patients [34]. Our results, in general, show that diabetic individuals demonstrate alterations in esophageal body motility during swallowing. The frequency of effective peristalsis was reduced in diabetic participants, and the frequency of simultaneous waves, no transmitted waves, and retrograde waves was significantly higher in diabetic vs. non-diabetic participants, in accordance with previous reports [9,16,26]. However, we

Table 2 – The duration of esophageal waves (in s) in type 2 diabetic patients and non-diabetic controls. Group Diabetics Controls p-Value

Upper esophagus

Middle esophagus

Lower esophagus

Mean duration

4.0  1.0 3.8  0.9 >0.05

4.5  1.3 3.9  0.8 <0.04

5.4  1.4 4.7  1.0 <0.02

4.6  0.9 4.1  0.75 <0.04

Values are expressed as mean  standard deviation. Wave duration in the middle and lower esophagus and mean wave duration were significantly higher in diabetic than control participants.

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diabetes research and clinical practice 97 (2012) 77–81

Table 4 – Average wave upstroke (in mmHg/s) in the esophagus of diabetic and non-diabetic participants. Group Diabetics Controls p-Value

Upper esophagus

Middle esophagus

Lower esophagus

Mean upstroke

24.1  13.9 24.5  13.0 >0.05

33.8  13.9 40.2  17.7 <0.03

29.8  15.3 41.3  14.0 <0.002

29.3  10.6 35.3  11.8 0.03

Values are expressed as mean  standard deviation. The value in the middle and lower esophagus and the mean average upstroke were significantly higher in the control group than in type 2 diabetic patients.

observed that wave amplitude, although higher in nondiabetic participants, did not differ significantly between groups. This observation differs from that of some studies [9,27], but is in accordance with others [29]. In this study, wave duration and velocity were lower in diabetic patients compared with healthy controls, particularly in the middle and distal esophagus, which showed a statistically significant difference between groups. Average and maximum wave upstroke were also significantly lower in diabetic than in control participants. Kinekawa et al. [17] registered that a significant correlation was found between esophageal dysfunction and MCV. The same authors showed that esophageal alterations in patients with diabetes are unrelated to signs of autonomic neuropathy, as based on the CVRR. A similar observation was made by Annese et al. [18] and Hu¨ppe et al. [34]. Innocenti and Castagnoli [19] also found no correlation between esophageal motor changes and peripheral neuropathy, duration of diabetes, or insulin dependence. Similarly, the diabetic patients we studied showed no signs of neuropathy according to the CVRR, revealing that esophageal alterations in diabetic patients appear not to be related to the presence of neuropathy. Nevertheless, in a group of type 1 diabetic patients, it was observed that esophageal transit time was slower in 68.7% of patients with cardiovascular autonomic neuropathy compared with only 15.4% of patients without neuropathy [35]. Usai et al. [6] believe that some unspecific alterations in esophageal motility such as spontaneous motor activity characterized by repetitive segmentary waves may be indicative of autonomic neuropathy. The mean BMI was significantly higher in diabetic patients than in control. According to the observations of different authors, its influence on the esophageal motility is controversial. Fornari et al. [36] observed that obese patients showed stronger esophageal peristalsis than non-diabetics. However, Ku¨per et al. [37] registered an esophageal waves with higher amplitude in non obese than obese individuals. For Merrouche et al. [38] the BMI was not related to LES tone or esophageal dyskinesia. Our data support the idea that esophageal motor alterations are more frequent in type 2 diabetic patients than in nondiabetic healthy individuals. Thus, medical examinations are required to identify any esophageal perturbations that diabetic patients may experience, followed by appropriate interventions. In conclusion, we observed that type 2 diabetic patients showed more frequent alterations in the motor activity of the esophagus than healthy individuals, as based on the manometric registry. The frequency of peristaltic waves was significantly higher in healthy individuals, whereas simultaneous waves, retrograde waves, and non-transmitted waves

were significantly more frequent in diabetic patients. The duration of esophageal waves and wave velocity were also higher in non-diabetic healthy individuals, with a significant difference observed in the middle and distal esophageal body. Wave amplitude was similar between groups, but wave upstroke was higher in non-diabetic participants compared with diabetic patients, with a significant difference seen in the middle and distal esophageal body.

Conflict of interest The authors declare that they have no conflict of interest.

Acknowledgments We would like to thank our patients and the group of volunteers who participated in this study. We also thank Dr. Cristina Martins and Dr. Ba´rbara Oliveiros for their contribution to the statistical analysis, and Editage for the writing assistance received. Dr. Joa˜o X. Jorge and Dr. Cla´udia IC Borges are supported by the enterprise Sonangol. The authors declare no conflicts of interest in relation to this investigation.

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