The effect of diabetes mellitus on clinical symptoms and esophageal injury in patients with gastroesophageal reflux disease
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original papers
Małgorzata Krakowska-Stasiak1
Dorota Cibor2
The effect of diabetes mellitus on clinical
Kamil Kozioł2
Iwon Grys1
symptoms and esophageal injury in patients
Tomasz Mach2
Danuta Owczarek2
with gastroesophageal reflux disease
Wpływ cukrzycy na obraz kliniczny i endoskopowy
u pacjentów z chorobą refluksową przełyku
Department of Internal Medicine and
1 Introduction: In recent years atten- Wprowadzenie: W ostatnich la-
Gastroenterology, 5th Military Hospital tion has been paid to the increased tach zwraca się uwagę na zwiększo-
Cracow, Poland incidence of gastroesophageal reflux ną częstość występowania choroby
Head: disease (GERD) among patients with refluksowej przełyku (ChRP) wśród
Prof. nadzw. dr hab. Iwon Grys
diabetes, however, the relationship chorych z cukrzycą, jednak związek
2
Department of Gastroenterology Hepatology
between glycaemic control and GERD pomiędzy wyrównaniem glikemii
and Infectious Diseases, Jagiellonian remains unclear. a ChRP pozostaje niejasny.
University Medical College, Cracow, Poland Aim: The aim of the study is to as- Cel: Celem pracy jest ocena wpły-
Head: sess the impact of diabetes on clini- wu cukrzycy na prezentację klinicz-
Prof. dr hab. Tomasz Mach cal presentation and the occurrence ną i występowanie zmian zapalnych
of inflammatory changes in the oeso- w przełyku u chorych z ChRP.
phagus in patients with GERD. Materiał i Metodyka: Do badania
Additional key words: Material and Methods: The study włączono 77 pacjentów z ChRP roz-
gastroesophageal reflux disease comprised 77 patients with GERD poznaną na podstawie typowych ob-
diabetes mellitus diagnosed on the basis of typical cli- jawów klinicznych w oparciu o skalę
gastroscopy nical symptoms assessed in the fre- częstości występowania objawów
quency scale for symptoms of GERD ChRP (frequency scale for symptoms
Dodatkowe słowa kluczowe:
(FSSG). To evaluate the complica- of gastroesophageal reflux disease -
choroba refluksowa przełyku
cukrzyca
tions, gastroscopy was performed, FSSG). Dla oceny powikłań wykona-
zapalenie przełyku classifying inflammatory changes in no gastroskopię, klasyfikując zmia-
the oesophagus based on the Los ny zapalne w przełyku na podstawie
Angeles scale. The diagnosis of Bar- skali Los Angeles. Rozpoznanie
rett’s oesophagus was based on the przełyku Barretta ustalono w oparciu
Prague classification and histological o klasyfikację praską i badanie histo-
examination. Anthropometric data logiczne. Analizie poddano dane an-
(including body mass index (BMI) and tropometryczne (w tym indeks masy
waist-hip ratio (WHR)) and results of ciała (body mass index - BMI) i stosu-
routine biochemical tests (glycemia, nek obwodu talii do obwodu bioder
glycated haemoglobin (HgbA1c), lipid (waist-hip ratio – WHR) oraz wyniki
profile, protein) were analysed. rutynowych badań biochemicznych
Results: In the examined group, (glikemia, hemoglobina glikowana
27 patients had diabetes (DM), while (HgbA1c), profil lipidów, białko całko-
50 people were non-diabetic (nDM). wite)
Patients with GERD and DM were ol- Wyniki: W badanej grupie 27 cho-
der than nDM (66.89 ± 9.44 vs 59.63 rych miało cukrzycę (DM), natomiast
± 15.5 years, p = 0.029), had a higher 50 osób stanowiła grupa bez cukrzycy
BMI (31.21 ± 4.89 vs. 26.57 ± 4.84 kg (nDM). Pacjenci z grupy DM byli starsi
/ m2, pmatory changes in the oesophagus were significantly more 6,49 punktów; p=0,06) oraz częściej skarżyły się na zgagę
frequent (59.3 vs. 34%, p=0.03). po posiłkach (p=0,018). U pacjentów z DM znamiennie czę-
Conclusions: Patients with GERD and concomitant ściej stwierdzono zmiany zapalne w przełyku (59,3 vs. 34%;
diabetes more often complain of postprandial heartburn p=0,03).
than non-diabetic ones. DM in patients with GERD predi- Wnioski: Pacjenci z ChRP oraz współistniejącą DM
sposes to oesophageal inflammatory changes, however częściej skarżą się na poposiłkową zgagę niż chorzy bez
further studies on a larger group of patients are necessary DM. DM wśród chorych z ChRP predysponuje do zmian
to confirm this thesis. zapalnych przełyku, jednak dalsze badania na większej
grupie pacjentów są konieczne dla potwierdzenia tej tezy.
Introduction ties, Kusano et al. developed a question- GERD was evaluated based on the FSSG
Diabetes mellitus (DM) is a chronic di- naire, the Frequency Scale for the Symp- that included 12 questions with 5 possible
sease that compromises the functions of toms of GERD (FSSG), which addresses answers grading the frequency of each of
almost all organs and is associated with 12 symptoms most commonly experienced the symptom as presented in the table I [8].
various gastrointestinal symptoms and by GERD patients, represented not only by All patients were asked to complete the
complications that are usually attributed heartburn and acid taste, but also by other FSSG questionnaire, and the cutoff score
to neurological impairment, especially au- dyspeptic symptoms, such as the sensa- at 8 points or more was considered as po-
tonomic neuropathy. Heartburn, nausea or tion of excessive fullness, especially after sitive for the GERD diagnosis. Gastrosco-
belching are widely recognized upper ga- meals [8]. FSSG has been validated to be py was performed to assess the presence
strointestinal symptoms commonly obse- clinically useful for the initial diagnosis of and severity of the esophageal injury and
rved in patients with DM [1]. GERD and patients with FSSG scores of erosion lesions were evaluated according
Gastroesophageal reflux disease more than 8 have been considered positive to the Los Angeles esophagitis classifica-
(GERD) is a condition characterized by for its diagnosis [7]. tion, graded from A to D [12]. Depending on
reflux symptoms and/or esophageal injury The aim of our study was to assess the the gastroscopy results, the patients were
such as esophagitis, strictures or Barrett’s influence of DM on the clinical presentation classified as NERD when no mucosal inju-
esophagus (BE) resulted from an abnormal and occurrence of inflammatory lesions in ry was found, Erosive Esophagitis (EE) if
acid or bile reflux into the esophagus. The the esophagus in patients with GERD. the typical erosions were present, and BE
known risk factors are obesity, pregnancy, if biopsy results confirmed the presence of
hiatal hernia, medications that relax lower Patients and Methods intestinal metaplasia according to the Pra-
esophageal sphincter (LES), and stress [2]. Seventy-seven patients from the De- gue classification [13].
In previous studies, various pathophysiolo- partment of Gastroenterology and Hepato- In the patients with DM, a thorough me-
gical factors such as insulin resistance, hy- logy, University Hospital in Cracow, Poland, dical history was taken. The anthropomor-
perinsulinemia, peripheral neuropathy and and from the Department of Internal Medi- phic data were collected, including weight,
metabolic syndrome were suggested as cine and Gastroenterology, 5th Military Ho- height, abdomen and waist circumferences.
the possible risk factors for the high preva- spital in Cracow, Poland, were involved in The body mass index (BMI), and the waist-
lence of the typical GERD symptoms in the the prospective study. The inclusion criteria -hip-ratio (WHR) were calculated. Routine la-
type 2 DM patients [3]. The recent scarce comprised: age above 18 years and GERD boratory tests were performed in all subjects.
studies have highlighted that complications diagnosed on the basis on the FSSG qu- Biochemical analyses included: complete
of GERD are more common in patients with estionnaire. The exclusion criteria were: blood cells count, and blood level of fasting
DM; however, the link between glycemic concomitant severe acute diseases (such glucose, glycated hemoglobin (HbA1c), li-
control and GERD is still unclear [1,4-6]. as myocardial infarction, stroke, pulmona- pids [(total cholesterol (TC), high-density
According to studies based on 24-h ry embolism, cirrhosis, severe infections), lipoprotein (HDL), low-density lipoprotein
pH monitoring, insulin-dependent diabetic malignancies, and pregnancy. The study (LDL), triglycerides (TG)], total protein and
patients may have a higher prevalence of group consisted of 27 diabetic patients albumin. All tests were performed using stan-
asymptomatic reflux than the general popula- (DM) and 50 non-diabetic (nDM) subjects. dard methodology in the clinical practice.
tion [9]. Visceral neuropathy may reduce the
perception of typical gastrointestinal symp-
Table I
toms in DM patients [10]. This may be the FSSG – Frequency Scale for the Symptoms of GERD.
reason for difficulties in determining the fre- Skala częstości objawów ChRP.
quency of GERD-related disorders, such as
erosive esophagitis, in a diabetic population
since the diabetic subjects may not present
with symptoms leading to initiation of an en-
doscopic evaluation [11]. On the other hand,
some studies have suggested that diabetic
patients may be more susceptible to acid
injury and severe acute gastric inflammation
since peptic ulcer disease occurs with a high
prevalence in patients with DM presenting
few or no dyspeptic symptoms [10].
Although 24-h pH-impedance moni-
toring is a gold standard to diagnose ga-
stroesophageal reflux disease, GERD is
commonly diagnosed based on the frequ-
ency of typical symptoms. However, most
patients with reflux symptoms have no
evidence of esophageal injury and the non-
-erosive GERD (NERD) may be difficult to
diagnose while based on patient reported Abbreviations: BE – Barrett’s esophagus; BMI – body mass index; DM – diabetes mellitus; EE – erosive esophagitis;
symptoms. Even typical, the reflux symp- FSSG – Frequency Scale for the Symptoms of GERD; GERD – gastroesophageal reflux disease; HgbA1c – glycated
toms depend on the patient’s description hemoglobin; HDL – high-density lipoprotein; LDL – low-density lipoprotein; LES – lower esophageal sphincter, nDM
and might be difficult to define in various – non-diabetic patients; NERD – non-erosive reflux disease; SD – standard deviation; TC – total cholesterol; TG –
populations [7]. To overcome these difficul- triglycerides; WHR – waist-hip-ratio.
Przegląd Lekarski 2018 / 75 / 09 437Statistical analysis The patients with GERD and DM were than in nDM GERD group, but the differ-
Continuous variables were presented significantly older as compared to the nDM ence was not statistically significant (20.75
as means and standard deviation or me- (66.89 ± 9.44 vs. 59.63 ± 15.5 years, p = ± 7.48 vs. 17.62 ± 6.49 points, p = 0.06).
dian and interquartile range (q1-q3). The 0.029). In the both DM and nDM groups, The distribution of responses to the FSSG
distribution of variables was tested us- most subjects were females (59.3% and in the DM and nDM patients is presented
ing the Shapiro-Wilk test. The Student’s t 62%, respectively). The diabetic patients in table IV.
test (ANOVA more than two groups) or the were more obese (BMI 31.21 ± 4.89 vs. The comparison of the response distri-
Mann-Whitney U (Kruskal-Wallis more than 26.57 ± 4.84 kg/m2, p < 0.001) and demon- bution in patients with esophageal injury ss
two groups) test were used for continuous strated a higher level of fasting glycemia, including EE and BE, and without esopha-
variables to assess differences between HgbA1c, total protein and triglycerides, geal injury (NERD) is presented in table V.
the groups. Categorical variables were but the significantly lower level of LDL and The frequency of the responses to qu-
reported as the number and percentages. HDL than in the nDM group as presented estions did not demonstrate statistical si-
The chi-square test was used to compare in table II. No differences were observed in gnificance both in the DM and nDM groups
categorical variables or as appropriate. total cholesterol and albumin levels in the and in the NERD and EE + BE subjects.
The statistical analyses were performed both studied groups (Tab. II). The only difference was that a significantly
using SPSS 23.0 (SPSS Inc., Chicago, IL, higher number of the DM subjects suffered
USA). P-valuesTable IV
The distribution of responses to the FSSG in the DM and nDM patients.
Rozkład odpowiedzi na pytania w skali FSSG wśród pacjentów z DM oraz nDM.
Question DM nDM P-value
0 1 2 3 4 0 1 2 3 4
1. 0.98
6.9% 20.7% 24.1% 37.9% 10.3% 18% 16% 36% 28% 2%
0 1 2 3 4 0 1 2 3 4
2. 0.17
20.7% 0% 17.2% 51.7% 10.3% 14% 10% 26% 48% 2%
0 1 2 3 4 0 1 2 3 4
3. 0.13
6.9% 17.2% 24.1% 41.4% 10.3% 20% 8% 36% 34% 2%
0 1 2 3 4 0 1 2 3 4
4. 0.12
48.3% 13.8% 17.2% 20.7% 0% 60% 12% 24% 4% 0%
0 1 2 3 4 0 1 2 3 4 0.2
5.
24.1% 20.7% 27.6% 27.6% 0% 36% 18% 36% 10% 0%
0 1 2 3 4 0 1 2 3 4
6. 0.018
44.8% 13.8% 13.8% 24.1% 3.4% 34% 14% 44% 8% 0%
0 1 2 3 4 0 1 2 3 4
7. 0.49
13.8% 20.7% 41.4% 17.2% 6.9% 28% 14% 38% 18% 2%
0 1 2 3 4 0 1 2 3 4
8. 0.11
31% 17.2% 17.2% 17.2% 17.2% 30% 12% 30% 26% 2%
0 1 2 3 4 0 1 2 3 4
9. 0.13
62.1% 17.2% 3.4% 17.2% 0% 54% 16% 18% 6% 6%
0 1 2 3 4 0 1 2 3 4
10. 0.56
10.3% 24.1% 44.8% 20.7% 0% 22% 16% 38% 20% 4%
0 1 2 3 4 0 1 2 3 4
11. 0.98
10.3% 24.1% 27.6% 34.5% 3.4% 14% 28% 26% 30% 2%
0 1 2 3 4 0 1 2 3 4
12. 0.14
24.1% 13.8% 27.6% 27.6% 6.9% 46% 14% 18% 22% 0%
Abbreviations: DM – diabetic patients, FSSG – frequency scale for symptoms of GERD, nDM – non-diabetic patients.
Table V
The distribution of responses to the FSSG in the NERD group and EE + BE group.
Rozkład odpowiedzi na pytania w skali FSSG wśród chorych z NERD i w grupie EE + BE.
Question NERD EE + BE P-value
0 1 2 3 4 0 1 2 3 4
1. 0.76
11.4% 15.9% 34.1% 36.4% 2.3% 18.2% 18.2% 30.3% 27.3% 6.1%
0 1 2 3 4 0 1 2 3 4
2. 0.45
18.2% 6.8% 18.2% 47.7% 9.1% 15.2% 6.1% 27.3% 51.5% 0%
0 1 2 3 4 0 1 2 3 4
3. 0.23
13.6% 4.5% 38.6% 38.6% 4.5% 18.2% 18.2% 21.2% 36.4% 6.1%
0 1 2 3 4 0 1 2 3 4
4. 0.13
54.5% 15.9% 25% 4.5% 0% 60.6% 9.1% 12.1% 18.2% 0%
0 1 2 3 4 0 1 2 3 4
5. 0.9
31.8% 20.5% 29.5% 18.2% 0% 33.3% 18.2% 36.4% 12.1% 0%
0 1 2 3 4 0 1 2 3 4
6. 0.73
31.8% 13.6% 34.1% 18.2% 2.3% 42.4% 15.2% 33.3% 9.1% 0%
0 1 2 3 4 0 1 2 3 4
7. 0.77
22.7% 15.9% 34.1% 22.7% 4.5% 24.2% 15.2% 45.5% 12.1% 3%
0 1 2 3 4 0 1 2 3 4
8. 0.46
22.7% 13.6% 29.5% 27.3% 6.8% 39.4% 15.2% 21.2% 15.2% 9.1%
0 1 2 3 4 0 1 2 3 4
9. 0.59
52.3% 15.9% 13.6% 11.4% 6.8% 63.6% 18.2% 12.1% 6.1% 0%
0 1 2 3 4 0 1 2 3 4
10. 0.64
15.9% 15.9% 38.6% 25% 4.5% 21.2% 21.2% 42.4% 15.2% 0%
0 1 2 3 4 0 1 2 3 4
11. 0.14
11.4% 18.2% 34.1% 36.4% 0% 15.2% 33.3% 18.2% 27.3% 6.1%
0 1 2 3 4 0 1 2 3 4
12. 0.76
36.4% 15.9% 15.9% 29.5% 2.3% 42.4% 12.1% 24.2% 18.2% 3%
Abbreviations: BE – Barrett’s esophagus, EE – erosive esophagitis, FSSG – frequency scale for symptoms of GERD, NERD – non-erosive reflux disease.
Przegląd Lekarski 2018 / 75 / 09 439and nodular esophageal carcinoma deve- higher total protein value and lover HDL the motor, sensory and autonomic nerves,
lopment [14-23]. Additionally, publications level when compared to the patients with retinopathy or nephropathy. Esophageal
report that complications of GERD are as- GERD, but without DM. Interestingly, the dysfunction in patients with DM is caused
sociated with arterial hypertension, insulin DM patients demonstrated a significan- largely by autonomic neuropathy, espe-
resistance and lipid disorders [7,24]. Some tly lower LDL cholesterol level. Similar cially the vagal nerve damage [37]. As
authors suggest that the symptoms and results were observed by Domaradzki et DM duration increases, esophageal motor
complications of GERD are more common al. in patients hospitalized due to pulmo- function deteriorates, what predisposes the
in patients with DM 2 as compared to sub- nary embolism episode - patients with DM subject to develop GERD [37]. It was sug-
jects without glycemia disturbances [1,4- had a better lipid profile as compared to gested that increased abnormal gastroeso-
6]. In the study performed in 2008, patients nDM ones [31]. One might only speculate phageal acid reflux in patients with DM was
with long-term DM 2, obesity and high on the effect of LDL cholesterol-reducing caused by impaired acid clearance and im-
HgbA1c levels more commonly demonstra- medications (e.g. statins) that are more pairment of effective esophageal peristal-
ted the symptoms of gastrointestinal reflux often taken by obese patients upon the sis which is related to diabetic neuropathy
as compared to the controls [25]. In turn, symptoms of GERD, but nevertheless, [25,33,37,38].
Rubenstein et al. [23] showed that in the further analyses are necessary to explain Based on endoscopy results we de-
population of patients with DM 2, esopha- the phenomenon. Horikawa et al. demon- monstrated that esophageal erosion le-
gitis was more common than in non-DM strated that patients with DM presenting sions were more frequently present in
subjects, while the serum insulin levels with symptoms of GERD were more rarely the DM patients as compared to the nDM
positively correlated with BE prevalence administered calcium channel blockers, subjects. A higher percentage of NERD
also among patients without glycemia di- thiazolidinediones and antiplatelet drugs was observed in the nDM group. However,
sorders. The same authors demonstrated [32]. The use of insulin or oral anti-diabe- there was no difference in the frequency
a positive correlation between increased tes agents did not affect the occurrence of of BE. Similar results, i.e. a higher preva-
levels of ghrelin and leptin, obesity-asso- GERD [32]. On the other hand, the authors lence of esophagitis, was observed in the
ciated hormones, and the prevalence of of another report demonstrated that in pa- previous studies [11]. The results suggest
BE in patients with GERD symptoms [23]. tients with DM and GERD, treatment with that DM predisposes patients with GERD
Thus, intensity of reflux symptoms in pa- proton-pump inhibitors more often ended to develop inflammatory lesions in the eso-
tients with DM 2 may also be associated in a failure [33]. In the analysis carried out phagus.
with a fully-developed metabolic syndrome in 2018 and including more than twelve Diabetes and insulin resistance are
[26]. Visceral adipose tissue is a precursor thousand subjects, Smith et al. observed among the risk factors of carcinoma de-
of increased lipolysis and free fatty acids symptoms of GERD and esophagitis more velopment [4,39]. Insulin may act directly
levels, leading to insulin resistance, a pri- frequent in patients on statins [34]. on tumor cells as a mitogen, and indirec-
mary factor in the mechanisms of metabolic The DM subjects achieved higher tly by promoting tumor growth via aberra-
syndrome [7,27-29]. Visceral adipose tis- average scores in the FSSG scale, that tions in the insulin-like growth factor axis
sue is also metabolically active and stron- suggests a higher intensity of reflux symp- [6,39,40]. In addition, chronic inflamma-
gly associated with elevated serum levels toms in this group. However, no significant tory state plays a significant role in BE
of proinflammatory adipokines, which may differences were demonstrated in the re- etiology, with BE being a precancerous
play a role in the development of GERD sponse distribution of most of questions. state predisposing the patient to develop
[29]. These humoral mediators released Only post-prandial heartburn occurred esophageal adenocarcinoma [27,29]. Evi-
by visceral fat tissue might alter the lower more frequent in the DM as compared to dence suggests that chronic inflammation
esophageal sphincter pressure or affect the nDM patients. Quite contradictory re- triggered by GERD not only predispo-
esophageal clearance [7]. sults were achieved by Holub et al, who ses to developing BE, but that the ensu-
On the other hand, Sun et al. did not showed that DM patients less often com- ing proinflammatory state and oxidative
demonstrate that BMI, WHR, lipid profile, plained of heartburn; however, the authors stress have roles in malignant transforma-
arterial hypertension and insulin therapy did not use validated forms for assessing tion [29]. In the study of Koppert et al. [41],
affected the prevalence of GERD in pa- GERD symptoms [11]. Nishida et al, inve- patients with esophageal carcinoma more
tients with DM [3]. Similarly, tobacco smo- stigated patients with DM 2; to evaluate frequently presented with DM as opposed
king, alcohol consumption and diabetes in the intensity of GERD symptoms, the au- to subjects with esophageal squamous
family history showed no significant effect thors employed the QUEST questionnaire cell carcinoma. In a large population-ba-
on GERD occurrence [3]. In a large po- and concluded that reflux symptoms were sed case-control study, DM 2 was a risk
pulation study including 65,333 patients, more common in the DM 2 group [35]. In factor for BE, independent of obesity and
a positive correlation was demonstrated this study, the prevalence of symptoms other risk factors (e.g. smoking) [4]. The
between ischemic heart disease, myocar- increased with an increasing duration of above results contradict the findings of
dial infarct and cerebral stroke, and GERD DM, the presence of complications (such Rubenstein et al. [42], where no correla-
presence, yet no correlation was noted for as nephropathy, neuropathy, retinopathy) tion was proven between the occurrence
DM [30]. Fujiwara et al. (2015) observed and when oral anti-diabetes medications of DM and esophageal adenocarcinoma.
that patients with DM and GERD were were employed [35]. Additionally, Natalini Our data demonstrate a more frequent oc-
younger, had shorter duration of DM and et al. demonstrated that the mean dura- currence of esophageal injury in patients
showed no difference in BMI [1]. There tion of diabetes was longer by 2.5 years with DM, but in view of the small number
was no significant association between in patients with concomitant symptomatic of the investigated subjects, further analy-
the presence of concurrent GERD and GERD [36]. With the increasing duration of ses are necessary.
diabetic complications, including periphe- DM, the response to anti-reflux treatment Summing up, the present study is
ral neuropathy [1]. As presented above, with proton pump inhibitors deteriorated among the few reports in which the diagno-
the results of the previously reported stu- [30]. However, the authors of the above- sis of GERD was established based on the
dies are contradictory; thus, further inve- -cited studies did not perform endoscopic noninvasive and validated symptoms sca-
stigations are needed to explain the as- evaluation thus asymptomatic GERD rela- le. Moreover, in all the patients gastrosco-
sociation between carbohydrate and lipid ted esophageal injury could not have been py was performed, that allowed us to deta-
metabolism and functioning of the upper assessed [35]. Examination of the upper iled evaluation of the esophageal mucosa
gastrointestinal tract. gastrointestinal tract in patients with DM is and possible GERD complications.
In the present study, we demonstrated significant, since GERD was demonstrated The study also has several limita-
that patients presenting with symptoms to show a high prevalence in asymptomatic tions. One of them, as mentioned above is
of GERD and DM were more obese as patients with abnormalities of carbohydrate a small sample of patients. No evaluation
compared to the controls. The diabetic metabolism [9-11]. With an increasing DM was also performed for the effect of medi-
patients showed significantly higher level duration, complications develop increasin- cations and duration of DM that might have
of fasting glycemia, HgbA1c, triglycerides, gly more commonly, such as neuropathy of affected the presented symptoms.
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