ZMIANY PROFILU LIPIDOWEGO U OSÓB Z BEZOBJAWOWYM I OBJAWOWYM ZAKAŻENIEM HELICOBACTER PYLORI

Marta Mędrek-Socha1,2, Jan Chojnacki1, Janusz Śmigielski3, Paulina Konrad1, Cezary Chojnacki1

1DEPARTMENT OF CLINICAL NUTRITION AND GASTROENTEROLOGICAL DIAGNOSTICS, MEDICAL UNIVERSITY OF LODZ, LODZ, POLAND 

2DEPARTMENT OF GASTROENTEROLOGY, MEDICAL UNIVERSITY OF LODZ, LODZ, POLAND 

3PAŃSTWOWA WYŻSZA SZKOŁA ZAWODOWA W KONINIE STATE HIGHER VOCATIONAL SCHOOL IN KONIN, KONIN, POLAND

Abstract

Introduction: Helicobacter pylori ( H. pylori) infection often coexists with coronary artery disease, but the causal relationship is not clear as yet.

The aim: to assess the lipidogram of patients with asymptomatic and symptomatic H. pylori infection.

Material and methods: The study included 30 healthy subjects (group I), 40 patients with asymptomatic (group II) and 40 with symptomatic (group III) H. pylori infection. The diagnosis of infection was based on the results of the urea breath test (13C-UBT) and the concentration of specific IgG antibodies. Serum concentration of: total cholesterol (TC), low density lipoprotein (LDL) fraction, high density lipoprotein fraction (HDL), non-HDL cholesterol (TC-LDL) and triglycerides (TG) were tested.

Results: Mean total cholesterol concentration was in group I-170,1±14,9 mg/dl, in group II – 173,0±13,1 mg/dl (p>0,05), in group III – 192,9±20,1 mg/dl (p<0,001). The concentration of LDL fraction was in group I – 111,6±12,5 mg/dl, in group II – 130,2±13,1 mg/dl (p<0,001) and in group III-151,3±14,6 mg/dl (p<0,001). The concentration of HDL fraction was in group I – 55,1±7,1 mg/dl, in group II-40,7±6,4 mg/dl (p<0,001), in group III-40,0±4,9 mg/dl (p<0,001). The concentration of non-HDL (TC-HDL) was in group I – 114,5±12,4 mg/dl, in group II – 132,2±13,8 mg/dl (p<0,001), in group III – 152,8±15,6 mg/dl (p<0,001). Triglycerides were in group I-133,3±24,2 mg/dl, in group II – 132,1±23,4 mg/dl (p>0.05), in group III – 154,75±17,2 mg/dl (p<0,001). Moreover, in group III a positive correlation was demonstrated between total cholesterol, LDL, HDL, triglycerides, non-HDL cholesterol and 13C-UBT.

Conclusion: In H.pylori-infected patients there are observed changes in the lipidogram, particularly adverse ones in the proportion of LDL to HDL.

STRESZCZENIE

Wstęp: Zakażenie Helicobacter pylori (H. pylori) często współistnieje z chorobą niedokrwienną serca, ale związek przyczynowy nie jest jasny.

Cele pracy: Ocena lipidogramu u osób z bezobjawowym i objawowym zakażeniem H. pylori.

Materiał i metody: Do badań włączono 30 osób zdrowych (grupa I), 40 osób z bezobjawowym (grupa II) i 40 osób z objawowym (grupa III) zakażeniem H. pylori. Rozpoznanie zakażenia oparto na wynikach mocznikowego testu oddechowego (UBT-13C) oraz stężenia swoistych przeciwciał IgG. w surowicy. W surowicy badano stężenia: cholesterolu całkowitego (TC), frakcji cholesterolu o niskiej gęstości (LDL), frakcji cholesterolu o wysokiej gęstości (HDL), cholesterolu nie-HDL (TC-LDL) oraz trójglicerydów.

Wyniki: Średnie stężenie cholesterolu całkowitego wynosiło odpowiednio w grupie I 170,1±14,9 mg/dl, w grupie II 173,0±13,1 mg/dl (p>0,05), w grupie III 192,9±20,1 mg/dl (p<0,001). Stężenie frakcji LDL wynosiło w grupie I 111,6±12,5 mg/dl, w grupie II 130,2±13,1 mg/dl (p<0,001) i w grupie III 151,3±14,6 mg/dl (p<0,001). Stężenie frakcji HDL wynosiło w grupie I 55,1±7,1 mg/dl, w grupie II 40,7±6,4 mg/dl (p<0,001), w grupie III 40,0±4,9 mg/dl (p<0,001). Stężenie nie-HDL (TC-HDL) wynosiło w grupie I 114,5±12,4mg/dl, w grupie II 132,2±13,8 mg/dl (p<0,001), w grupie III 152,8±15,6mg/dl (p<0,001). Trójglicerydy w grupie I 133,3±24,2 mg/dl, w grupie II 132,1±23,4 mg/dl (p>0,05), w grupie III 154,75±17,2 mg/dl (p<0,001). Ponadto w grupie III wykazano dodatnią korelację cholesterolu całkowitego, LDL, HDL, trójglicerydów, cholesterolu nie-HDL a UBT-13C.

Wnioski: U osób zakażonych H. pylori występują zmiany w lipidogramie, szczególnie niekorzystne zmiany proporcji LDL/HDL.

Wiad Lek 2018, 71, 8, -1473

INTRODUCTION

Helicobacter pylori (H. pylori) infection occurs in 50-80% of adults in different populations and is still a serious epidemiological and medical problem. For many years, the attention of researchers was focused mainly on inflammatory changes in the stomach. It has been established that this infection always leads to chronic destructive gastric mucosal lesions and secondarily to metaplasia and dysplasia, which may initiate a neoplastic process. The infection was classified as risk factor for the development of gastric cancer also in subjects without clinical symptoms [1]. In recent decades, it has been pointed out that H. pylori infection often coexists with diseases of other organs [2]. Particular attention was paid to the coexistence of cardiovascular diseases, including the younger age subjects [3]. Many researchers believe that H. pylori infection is a risk factor of coronary artery disease [4, 5], but not everyone shares this opinion [6] and the role of other atherogenic factors in this group of patients is indicated [7].

In search of a causal relationship between H. pylori infection and changes in the blood vessels the inflammatory and immune response is considered [8]. IgM antibody develops first, followed by IgA and IgG. In the gastric mucosa there are mainly found IgA antibodies and a small amount of IgM and IgG and the IgG fraction dominates in the serum [9]. It is believed that the presence of these antibodies and proinflammatory cytokines in the peripheral blood may promote immune and inflammatory changes in the blood vessel wall [10]. This suggestion is confirmed by the presence of H. pylori specific DNA in coronary atherosclerotic plaques [11]. However, the reference of inflammatory changes in the gastric mucosa to changes in the blood vessels is questionable. Moreover, lipoproteins are an essential element of the atherosclerotic process, which has been pointed out by many researchers.

Rasmi et al. [12] found higher serum levels of total and LDL cholesterol as well as apolipoproteins A and B in patients with angina pectoris and H. pylori infection compared to healthy subjects. Similarly, Pohjanen et al. [13] and Hoffmeister et al. [14] detected the decrease in HDL with simultaneous increase in LDL levels in H.pylori infected patients.

In most studies on this issue, the diagnosis of H. pylori infection was based only on serological tests, which raises reservations and doubts and inspires to conduct further research.

The aim of the study was to assess the lipidogram changes in patients with asymptomatic and symptomatic H. pylori infection in relation to the intensity of bacterial colonization.

MATERIAL AND METHODS

Patients

The study was carried out in a group of 110 patients, aged 21-40 years observed in the years 2014-2016 at the Department of Gastroenterology and at the Department of Clinical Nutrition and Gastroenterological Diagnostics, Medical University of Łódź, Poland.

Three groups were distinguished for the purpose of the study:

Group I (n=30) – clinically healthy subjects, without H. pylori infection – control group,

Group II (n=40) – patients with asymptomatic H. pylori infection,

Group III (n=40) – patients with symptomatic H. pylori infection in the form of chronic epigastric pain mainly between meals and at night.

The diagnosis of infection was based on the urea breath test (13C-UBT) and the concentration of specific anti-H.pylori IgG antibodies.

Criteria of inclusion

Only patients in whom an increase in the concentration of hydrogen in the exhaled air exceeded 8.0 ‰ (ppm) and the IgG antibody concentration was over 10 U/ml were enrolled in the study. The control group included individuals whose result of the 13C-UBT breath test was below 1.0 ‰ (ppm) and no specific antibodies were found in the blood.

Criteria of exclusion:

– body mass index 30 kg/m2 ,

– high-energy or vegetarian diet,

– cardiac diseases and arterial hypertension,

– endocrine, metabolic and mental diseases,

– history of peptic ulcers,

– allergy or IgG-dependent food intolerance,

– viral hepatitis,

– alcohol abuse and smoking,

– taking hypolipemic and sedative agents.

Methods

Endoscopy of the upper gastrointestinal tract and the following routine laboratory tests were performed in all the subjects:

blood cell count, bilirubin, glucose, urea, creatinine, TSH, triiodothyronine, thyroid hormones and activity of amylase, lipase, aspartate aminotransferase, alanine aminotransferase, gamma-glutamyl transpeptidase, alkaline phosphatase,

serum concentration of C-reactive protein (CRP) and glycated hemoglobin (HbA1c) determined by turbidometric method (Cobas-Integra 400 analyzer),

serum concentration of cholesterol and its high (HDL) and low density lipoprotein fraction (LDL) and triglycerides were determined by spectrophotometric method (Cobas-Integra 800 analyzer),

urea breath test was performed using 13C-labeled urea and FANci 2 analyzer (Fisher Analysen Instrumente GmbH),

serum concentration of anti-H.pylori IgG antibodies were determined by immunoenzymatic method using Simcus tests and Immulite analyzer,

blood was collected in fasting after previous 14-day balanced diet of 1600-2100 kcal, depending on the type of performed professional work.

Ethics

Written consent was obtained from all study participants and the study protocol was approved by the Bioethics Committee of the Medical University in Lodz (No RNN/458/14/KB).

The study was performed in accordance with the Declaration of Helsinki and with the principles of Good Clinical Practice.

Statistical analysis

The nonparametric Kruskal-Wallis test was used in the statistical analysis to compare involved features between groups. The Mann-Whitney test was applied for median comparison.

The correlation between intensity of H. pylori infection and laboratory results was assessed by the Pearson’s correlation coefficient and linear regression equation. Statistica 12.0 was used for the correlation. The differences between results were regarded as significant when “P” value < 0.05-0.001.

RESULTS

Group I, II and III participants were matched properly as regards age and gender and they did not differ statistically. Compared to the control group, the body mass index was higher in both groups of patients with symptomatic and asymptomatic H. pylori infection (Tab. 1). The concentration of CRP (p<0.05) and HbA1c (p<0.01) was higher in the group of patients with symptomatic infection. The groups of infected patients differed as regards the results of the urea breath test (p<0.001) and the serum concentration of specific antibodies (p<0.01) (Tab. 1).

In the control group, serum total cholesterol level was 170.1±14.9 mg/dl, whereas in H. pylori infected patients in the asymptomatic group it was 173.0±13.1 mg/dl (p> 0.05) and in the symptomatic group it was 192.9±20.1 mg/dl (p <0.001) (Fig. 1).

The concentration of LDL fraction was higher in both H. pylori-infected groups than in non-infected subjects and it was respectively: in group I – 111.6±12.5 mg/dl, in group II – 130.2±13.1 mg/dl (p <0.001) and in group III – 151.3±14.6mg/dl (p <0.001) (Fig. 2).

The concentration of HDL fraction was lower in H. pylori-infected patients and it was respectively: in group II – 40.7±6.4 mg/dl (p <0.001) and in group III – 40.0 ± 4.9 mg/dl (p <0.001) (Fig.3).

Similar differences between groups were found when assessing non-HDL cholesterol. In group I – 114.5±12.4 mg/dl, in group II – 132.2±13.8mg/dl (p <0.001) and in group III -152.8±15.6 mg/dl (p <0.001) (Fig.4).

The ratio of cholesterol fractions was significant. The total cholesterol/HDL ratio (TC/HDL-Castelli index) was in the control group- 3.10±0.42, in group II – 4.35±0.81 (p <0.001), in group III – 4.83±0.22 (p<0.001).

Similar differences were found when assessing the LDL/HDL ratio. In group I it was – 2.04± 0.36, in group II – 3.30±0.79 (p <0.001) and in group III – 3.80± 0.22 (p <0.01).

The serum concentration of triglycerides was similar in the control group and in the group with asymptomatic infection and it was: 133.5±24.2 mg/dl vs. 132.1±23.4 mg/dl (p>0.05), whereas in the group with symptomatic infection it was higher – 154.7±17.2 (p<0.001) (Fig.5).

No correlation was found between the value of the breath test and the concentration of investigated lipid fractions in the group of patients with asymptomatic infection. Such a correlation of high statistical significance was found in the group of patients with symptomatic H. pylori infection (Tab. 2).

Discussion

The pathogenesis of lipid disorders and atherosclerosis is a complex process. The presented study included only individuals younger than 40 years of age to limit the participation of many factors affecting lipid metabolism. Therefore, the obtained results can be related to H. pylori infection. Attention is drawn to the statistically significant low concentration of HDL cholesterol with the simultaneous increase in LDL cholesterol in both infected groups. Other researchers found similar changes. Jia et al. [15] in a large group of patients with coronary artery disease demonstrated lower concentration of HDL cholesterol in infected patients compared to those non-infected. Mokhtare et al. [16] found a reduction in LDL and an increase in HDL after H. pylori eradication. Similarly, beneficial effect of H. pylori eradication on the lipid profile was confirmed by Gen. et al. [17] and Pellicano et al. [18]; they also admitted that the mechanism of these changes was not clear.

Most researchers see the cause of dyslipidemia in the effect of proinflammatory cytokines, which can inhibit the activity of lipoprotein lipase and stimulate the generation of reactive oxygen species [8].

However, the influence of other factors is not excluded, especially in patients with symptomatic infection, in the form of epigastric pain, including hunger and night pain, which is accompanied by an increase in appetite due to changes in the secretion of enterohormones, particularly gastrin. Divergent results were obtained in the assessment of other hormones.

Ulasoglu et al. [19] found a decrease in serum ghrelin concentration with a simultaneous increase in obestatin level after eradication of H. pylori. In turn, Deng et al. [20] found an increase in ghrelin concentration and Osawa et al. [21] observed an increase in ghrelin concentration in some patients (37.3%) and in the remaining individuals (62.3%) the decrease in the concentration of this hormone after eradication of this bacterium.

Francois et al. [22] studied postprandial concentrations of ghrelin and found 6-fold higher levels prior to bacterial eradication as well as a leptin increase by 20%.

Russo et al. [23] reported significantly higher serum gastrin and TNF-α concentrations in half of the patients with asymptomatic H. pylori infection compared to uninfected subjects.

Increased appetite and eating too frequently, especially without checking the caloric value, can lead to weight gain and lipid metabolism disorders. Numerous studies point to such a pathogenetic chain but the conclusions from the research vary [24].

The majority of researchers indicated positive correlation between H. pylori infection and metabolic syndrome, obesity, insulin resistance and dyslipidemia [24−26]. Other researchers found no association of this infection with lipid profile disturbances and body mass index [27].

The results of most studies indicate that body mass index is higher in patients with symptomatic H. pylori infection than in non-infected subjects. Moreover, the level of HbA1c was also higher in this group which indicates the co-existence of carbohydrate metabolism disorders. Due to the small group of respondents, it is difficult to draw more representative conclusions.

An important observation is the occurrence of lipid profile disorders also in patients with asymptomatic H. pylori infection which indicates that this infection is not neutral to the body.

Many researchers tried to find out which factors determine that the infection is asymptomatic in some and causes symptoms in others , but no definitive answers have been found so far. However, it is known that an asymptomatic infection leads to the damage of gastric mucosa and to peptic ulcers [28]. Oxygen metabolism disorders are an essential gastrotoxic factor. All H. pylori strains stimulate macrophages to generate reactive oxygen species that cause oxidative damage to gastric mucosa cells and may affect the integrity of DNA regardless of the presence of clinical symptoms [29]. Furthermore, bacterial urease activates lipoxygenation in blood platelets [30] and acts proinflammatory [31] similarly to secondary ammonia [32]. These mechanisms can also be an important element in the carcinogenesis. These indicate guidelines for therapeutic management and prevention of gastric cancer. The currently valid in Europe Maastricht V Consensus [33] does not recommend the treatment of asymptomatic H. pylori infection with the exception of individuals with a family history of gastric cancer and those with hypochromic anemia and immune thrombocytopenia purpura. In turn, in the Kyoto Consensus [34], it was considered that every infection requires H. pylori eradication which includes the idea of gastric cancer prevention.

CONCLUSION

The obtained own results indicate a possible role of H. pylori also in the lipid metabolism disorders, although the causal relationship is crucial but it needs confirmation in further studies. In the case of symptomatic infection, this relationship is indicated by a positive correlation between the activity of bacterial colonization in the gastric mucosa and disturbances of all fractions of the lipid profile. In patients with asymptomatic infection, no such correlation was found, which indicates the involvement of other factors in the pathogenesis of dyslipidemia. However, it seems purposeful to test H. pylori infection in all young people who present lipid disorders. In these cases, after excluding other causes of dyslipidemia, H. pylori eradication is justified also in asymptomatic infections.

Praca finansowana przez Uniwersytet Medyczny w Łodzi z zadania badawczego o numerze 502-03/5-006-02/502-54-163.

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Conflict of interest:

The Authors declare no conflict of interest.

Corresponding author

Marta Mędrek-Socha

Department of Clinical Nutrition and Gastroenterological Diagnostics, Medical University of Lodz, Lodz, Poland

e-mail: martamedrek@gmail.com

Received: 03.10.2018

Accepted: 24.10.2018

Fig. 1. Serum total cholesterol level (TC[mg/dl]) in healthy subjects (group I) and with asymptomatic (group II) and symptomatic (group III) H. pylori infection; X±SD. Differences between groups: I vs. II p>0,05, I vs. III p<0,001, II vs. III p<0.001.

Fig. 2. Serum concentration of low density lipoprotein (LDL[mg/dl]) in healthy subjects (group I) and in patients with asymptomatic (group II) and symptomatic (group III) H. pylori infection. X ±SEM. Differences between groups: I vs. II p<0.001, I vs. III p<0.001, II vs. III p<0.001.

Fig. 3. Serum concentration of high density lipoprotein (HDL[mg/dl]) in healthy subjects (group I) and in patients with asymptomatic (group II) and symptomatic (group III) H. pylori infection. X ±SD. Differences between groups: I vs. II p< 0.001, I vs. III p<0.001, II vs III p>0.05

Fig. 4. Serum concentration of non-HDL [mg/dl]) in healthy subjects (group I) and in patients with asymptomatic (group II) and symptomatic (group III) H. pylori infection. X±SEM. Differences between groups: I vs. II p<0.001, I vs. III p<0.001, II vs. III p<0.001.

Table 1. Clinical characteristics of the investigated subjects: Group I – healthy subjects, group II – patients with asymptomatic H. pylori infection, group III – patients with symptomatic H. pylori infection. BMI – body mass index, UBT – urea breath test, IgG – anti-H. pylori antibodies, CRP – C-reactive protein, HbA1c – glycated hemoglobin. X± SD, p<0.05, p<0,01, p<0.001

Parameters

Group I (n=30)

Group II (n=40)

Group III (n=40)

Age

28.9±5.4

28.8±4.8

28.7±4.9

Gender M

F

16

14

23

17

21

19

BMI (kg/m2)

21.0±1.6

22.2±1.9

24.4±1.9

UBT (‰)

(-)

12.4±4.0

20,9±7,5

IgG (U/ml)

(-)

17.7±6.3

22.8±7.6

CRP (mg/L)

1.8±1.1

1.6±0.8

2.6±1.5

HbA1c (%)

5.1±0.2

5.0±0.3

5.5±0.6

Table 2. Correlation between the value of the urea breath test (13C-UBT) and serum total cholesterol (TC), fraction of low density (LDL) and of high density (HDL), non-HDL cholesterol (TC-HDL) and triglycerides (TG) in asymptomatic (group II) and symptomatic (group III) H. pylori infection.

13C-UBT/lipids

Group II

Group III

Spearman correlation coefficient (r)

P value

Spearman correlation coefficient (r)

P value

TC

0.228

>0.05

0.819

<0.001

LDL

0.72

>0.05

0.835

<0.001

HDL

0.123

>0.05

0.764

<0.001

TC-HDL

0,. 91

>0.05

0.822

<0.001

TG

-0.157

>0.05

0.546

<0.001

Fig. 5. Serum concentration of triglycerides (TG) [mg/dl] in healthy subjects (group I) and in patients with asymptomatic (group II) and symptomatic (group III) H. pylori infection. X±SD. Differences between groups: I vs. II p>0.05, I vs. III p<0.001, II vs III p<0.001.