Abstract
OBJECTIVES:
Helicobacter pylori is a gram-negative, spiral-shaped, urease-producing bacterium with multiple unipolar flagella. Humans are a major reservoir for H. pylori; however, there are no data on the prevalence of H. pylori among dyspeptic patients who have experienced natural disasters. Therefore, the aim of this study was to examine the prevalence of H. pylori in dyspeptic patients who survived a recent natural disaster and to compare the data between the pre-disaster and post-disaster periods.
METHODS:
Between December 2011 and February 2012 (∼ one month following an earthquake), 209 dyspeptic patients who underwent gastroscopy were included in the study. For microorganism identification, gastric biopsy materials from the 209 disaster survivors with dyspeptic complaints were tested for urease activity in a medium containing urea and a pH indicator. The obtained results were compared with pre-disaster data from dyspeptic patients in the same city during the corresponding period of the previous year. Furthermore, the current H. pylori prevalence was evaluated among 139 dyspeptic patients between January 2014 and May 2014.
RESULTS:
We found a significantly higher prevalence of H. pylori in disaster survivors with dyspepsia compared with dyspeptic patients in the pre-disaster period (p<0.005). Interestingly, the current H. pylori prevalence was found to be significantly higher than the prevalence in both the disaster and pre-disaster periods (p<0.005).
CONCLUSION:
These results suggest that a recent earthquake could contribute to the development of H. pylori infection in subjects who live in the disaster-stricken area. These data also highlight the exceptionally high H. pylori prevalence in dyspeptic patients. Regional variations require further analyses.
Helicobacter pylori ; Earthquake; Van City
INTRODUCTION
Since it was first isolated from gastric mucosa in 1990, Helicobacter
pylori has been reported to be the cause of a variety of
gastrointestinal (GI) diseases, including dyspeptic ulcers and gastric cancer. The
vast majority of cases are the result of the ingestion of H.
pylori-infected foods. Nonetheless, person-to-person transmission is
currently considered to be the main route of contagiousness H.
pylori infection and the proposed routes are mainly oral-oral and
fecal-oral (11. Delport W. The transmission of Helicobacter pylori: The effects
of analysis method and study population on inference. Best Pract Res Clin
Gastroenterol. 2007;21(2):215-36,
http://dx.doi.org/10.1016/j.bpg.2006.10.001.
http://dx.doi.org/10.1016/j.bpg.2006.10....
). The prevalence of H.
pylori infection is higher in developing countries than in developed
countries, mostly due to a lack of safe drinking water and a lack of basic hygiene;
this high prevalence may also be due to poor diet and overcrowded living conditions.
Turkey reportedly has a high prevalence of H. pylori infection as
well (22. World Gastroenterology Organisation. World Gastroenterology
Organisation Global Guideline: Helicobacter pylori in developing countries.
J Clin Gastroenterol. 2011;45(5):383-8.). Although there may be geographical
differences in prevalence, the majority of patients with H. pylori
infection have been found to live under poor hygienic conditions, including poor
urban infrastructure. It is generally accepted that this infection is mainly
prevalent among lower social classes as well as in poor countries, likely due to the
favorable circumstances for contagion between persons living under overcrowded and
unhygienic conditions. Relatively socially deprived populations may also harbor
H. pylori infection (33. Woodward M, Morrison C, McColl K. An investigation into factors
associated with Helicobacter pylori infection. J Clin Epidemiol.
2000;53(2):175-81,
http://dx.doi.org/10.1016/S0895-4356(99)00171-7.
http://dx.doi.org/10.1016/S0895-4356(99)...
).
Natural disasters are one of the most common causes of social turmoil, particularly
in the developing world. Disaster-related conditions may also be associated with
poor hygienic conditions, leading to dyspeptic complaints. Indeed, a strong
relationship between gastric disorders and disasters has recently been reported. In
addition, a number of previous studies have suggested an association between GI
disorders and natural disasters (44. Kurokawa M, Nukina M, Nakanishi H, Miki K, Tomita S, Tohdo A. The
relationship between hemorrhagic gastric ulcers often appearing among in the
great Hanshin-Awaji earthquake sufferers and Helicobacter pylori infections.
Kansenshogaku Zasshi. 1996;70(9):970-5,
http://dx.doi.org/10.11150/kansenshogakuzasshi1970.70.970.
http://dx.doi.org/10.11150/kansenshogaku...
). A
large-scale Japanese study that explored whether earthquakes affect gastric
disorders revealed that earthquake-related conditions not only triggered but also
exacerbated gastric ulcers, particularly in the elderly (55. Aoyama N, Kinoshita Y, Fujimoto S, Himeno S, Todo A, Kasuga M, et
al. Peptic ulcers after the Hanshin-Awaji earthquake: increased incidence of
bleeding gastric ulcers. Am J Gastroenterol.
1998;93(3):311-6.). In developing countries, a lack of hygienic conditions and
overcrowded living conditions may also be two of the main risk factors for
developing H. pylori infection (66. Dominici P, Bellentani S, Di Biase AR, Saccoccio G, Le Rose A,
Masutti F, et al. Familial clustering of Helicobacter pylori infection:
population based study. BMJ. 1999;319(7209):537-40,
http://dx.doi.org/10.1136/bmj.319.7209.537.
http://dx.doi.org/10.1136/bmj.319.7209.5...
).
On October 23, 2011, a 7.2-magnitude earthquake killed more than 1,000 people in the eastern Anatolian city of Van; this was one of Turkey's worst natural disasters. More than 60,000 residents of the city lived in make-shift houses and containers under unfavorable climatic conditions (77. Tolon M, Yazgan U, Ural DN, Goss KC. Overview of the critical disaster management challenges faced during Van 2011 earthquakes. J Emerg Manag. 2014;12(1):82-96.). Furthermore, people in the disaster-stricken areas faced many health problems, mostly due to overcrowding in temporary, make-shift dwellings and other unfavorable accommodations. Van city's socioeconomic situation, which has further deteriorated due to a series of earthquakes of great magnitude, has also facilitated and contributed to a higher prevalence of such conditions and these types of areas have been considered to yield useful data for epidemiological studies on H. pylori infection.
Therefore, we conducted a prospective study to evaluate the effects of the recent earthquake on the frequency of H. pylori in dyspeptic patients who live in the disaster-affected area.
MATERIALS AND METHODS
In total, 209 dyspeptic patients (100 female and 109 male, aged 18-88 years) who experienced the recent disaster were evaluated at our clinic from December 2011 to February 2012. According to the most recent consensus committee, or Rome III, dyspepsia was defined as the presence of any bothersome symptom, postprandial fullness, early satiation, epigastric pain, or epigastric burning, with no evidence of structural disease that is likely to explain the symptoms. The criteria had to be fulfilled for the last three months, with symptom onset at least 6 months prior to diagnosis. The symptoms and their rates are shown in the Table 1. The study subjects were recruited from the residents of Van city, where, together with its environs, a recent earthquake caused massive devastation (Figure 1). Patients using antibiotics or anti-ulcer drugs, four weeks before initial admission were excluded from the study. All the patients provided informed consent to participate in the study. Esophagogastroscopy with antral biopsy was performed for each patient. The gastric biopsy samples were tested for urease activity using a commercial, rapid H. pylori test (GI Supply¯, Camp Hill, PA, USA), which includes a urea-containing medium and a pH indicator. Medical data were obtained from 97 dyspeptic patients (57 women and 40 men, aged 18-75 years) who underwent GI endoscopy before the earthquake. Between January 2014 and May 2014, 139 dyspeptic patients (60 female, mean age 48±4 years) were also selected in the same region to evaluate the current status of H. pylori infection. Antral biopsies obtained from the endoscopic evaluation of patients who were examined before the disaster were assessed for H. pylori by the same method. H. pylori positivity was defined as positivity in the rapid urease test (RUT).
Statistical analysis: Comparisons between three groups were performed using the Mann-Whitney U-test. The differences were considered statistically significant at p<0.05. Calculations were performed using conventional software (SPSS 12 for Windows).
RESULTS
The mean age was 45.96±1.61 in the pre-disaster group and 48.49±1.97 in the disaster group. H. pylori infection was observed in 118 of 209 (56.5%) disaster survivors with dyspepsia. In the pre-disaster group, H. pylori infection was found in 40 of 97 (41.2%) patients. We found significantly more frequent H. pylori infection in disaster survivors with dyspepsia compared with the pre-disaster data obtained from hospital records (p = 0.02). In the group of subjects who experienced the disaster, there were 112 (80.6%) patients with H. pylori infection. There was a statistically significant difference between the current H. pylori status of the dyspeptic patients and that of the disaster and pre-disaster groups (p<0.005). However, there was no gender difference among the groups (p>0.05). The data for H. pylori status are shown in Figure 2.
DISCUSSION
Our study clearly demonstrates a statistically significant association between the recent earthquake and the prevalence of H. pylori infection. Furthermore, this is the first study demonstrating higher rates of H. pylori infection due to and exacerbated by an earthquake. The results also show that the prevalence of H. pylori infection in dyspeptic patients who experienced the recent Van earthquake was as high as 57%.
Dyspepsia is characterized by the presence of postprandial fullness, early satiation,
epigastric pain, and epigastric burning, and eradication of the bacterium has been
demonstrated to be an effective and tolerable first-line treatment for dyspeptic
patients infected with H. pylori. According to the American
Gastroenterological Association, the most common organic causes in dyspeptic
patients are peptic ulcer disease, gastroesophageal reflux disease and gastric
cancer. However, non-ulcer dyspepsia is the most common cause on average and is
defined as the presence of dyspepsia, with no evidence of organic disease, for at
least 12 weeks (which do not have to be consecutive) within the last 12 months.
Upper GI tract endoscopy is one of the most useful invasive methods for the
exclusion of organic causes of dyspepsia (88. Tack J1, Talley NJ, Camilleri M, Holtmann G, Hu P, Malagelada JR,
et al. Functional gastroduodenal disorders. Gastroenterology.
2006;130(5):1466-79,
http://dx.doi.org/10.1053/j.gastro.2005.11.059.
http://dx.doi.org/10.1053/j.gastro.2005....
).
Natural disasters have had a great impact on human history, killing numerous
populations and devastating extensive residential areas. It has been shown that
natural disasters, including earthquakes, contribute to the spread of water- and
food-borne illnesses as well as GI infections (99. Ligon BL. Infectious Diseases that Pose Specific Challenges After
Natural Disasters: A Review. Semin Pediatr Infect Dis. 2006;17(1):36-45,
http://dx.doi.org/10.1053/j.spid.2006.01.002.
http://dx.doi.org/10.1053/j.spid.2006.01...
). Natural disasters are also associated with a higher prevalence of
dyspepsia (1010. Honarkar Z, Baladast M, Khorram Z, Akhondi Sh, Antikchi M,
Masoodi M, et al. An analysis of gastrointestinal symptoms in causalities of
catastrophic earthquake of Bam, Iran. SEMJ. 2005;6:1-2.), though the effect of
earthquakes on the H. pylori profile of clinically apparent
dyspepsia is not known. A limited number of epidemiological studies have revealed a
very strong association between GI disorders and natural disasters (44. Kurokawa M, Nukina M, Nakanishi H, Miki K, Tomita S, Tohdo A. The
relationship between hemorrhagic gastric ulcers often appearing among in the
great Hanshin-Awaji earthquake sufferers and Helicobacter pylori infections.
Kansenshogaku Zasshi. 1996;70(9):970-5,
http://dx.doi.org/10.11150/kansenshogakuzasshi1970.70.970.
http://dx.doi.org/10.11150/kansenshogaku...
). In a recent study from Iran, it was
reported that approximately 20% to 40% of earthquake survivors suffered from GI
complaints, including dyspepsia; however, the presence of H. pylori
infection was not evaluated (1010. Honarkar Z, Baladast M, Khorram Z, Akhondi Sh, Antikchi M,
Masoodi M, et al. An analysis of gastrointestinal symptoms in causalities of
catastrophic earthquake of Bam, Iran. SEMJ. 2005;6:1-2.).
An increased rate of bleeding gastric ulcers, particularly in the elderly population
has been reported in earthquake-stricken areas in Japan (55. Aoyama N, Kinoshita Y, Fujimoto S, Himeno S, Todo A, Kasuga M, et
al. Peptic ulcers after the Hanshin-Awaji earthquake: increased incidence of
bleeding gastric ulcers. Am J Gastroenterol.
1998;93(3):311-6.). Researchers have postulated that emotional stress is a
contributing factor in the development of gastric ulcers in such cases (1111. Kanno T, Iijima K, Abe Y, Koike T, Shimada N, Hoshi T, et al.
Peptic ulcers after the Great East Japan earthquake and tsunami: possible
existence of psychosocial stressulcers in humans. J Gastroenterol.
2013;48(4):483-90, http://dx.doi.org/10.1007/s00535-012-0681-1
http://dx.doi.org/10.1007/s00535-012-068...
). However, only a few studies have examined
the prevalence of H. pylori in earthquake-stricken areas and all of
these studied involved measurements of serum anti-H. pylori
antibodies among patients with gastric ulcers. The researchers found that the
seroprevalence of H. pylori in disaster-stricken areas was not
different from that in less-devastated surrounding areas. In addition, they found a
significant association between H. pylori infection and the
development of gastric ulcers (44. Kurokawa M, Nukina M, Nakanishi H, Miki K, Tomita S, Tohdo A. The
relationship between hemorrhagic gastric ulcers often appearing among in the
great Hanshin-Awaji earthquake sufferers and Helicobacter pylori infections.
Kansenshogaku Zasshi. 1996;70(9):970-5,
http://dx.doi.org/10.11150/kansenshogakuzasshi1970.70.970.
http://dx.doi.org/10.11150/kansenshogaku...
,1212. Matsushima Y, Aoyama N, Fukuda H, Kinoshita Y, Todo A, Himeno S,
et al. Gastric ulcer formation after the Hanshin-Awaji earthquake: a case study
of Helicobacter pylori infection and stress-induced gastric ulcers.
Helicobacter. 1999;4(2):94-9,
http://dx.doi.org/10.1046/j.1523-5378.1999.98290.x.
http://dx.doi.org/10.1046/j.1523-5378.19...
).
To establish a specific diagnosis, endoscopic biopsy samples from the antral mucosa
should be obtained for the detection of H. pylori infection by RUT
or histological testing (1313. Malfertheiner P, Chan FK, McColl KE. Peptic ulcer disease.
Lancet. 2009;374 (9699):1449-61,
http://dx.doi.org/10.1016/S0140-6736(09)60938-7.
http://dx.doi.org/10.1016/S0140-6736(09)...
). RUT is based on
the detection of H. pylori urease activity and has a high
sensitivity (85%) and specificity (>95%) in detecting H.
pylori infection. As this test is considered to be cost-effective and
suitable for endoscopy units (1414. Onders RP. Detection methods of Helicobacter pylori: accuracy
and costs. Am Surg. 1997;63(8):665-8.), we used
RUT to establish H. pylori infection. However, because our
pathology unit was demolished by the earthquake, we were not able to examine the
gastric specimens by light microscopy.
H. pylori infection is increasingly prevalent in the eastern part of
Turkey, though there are few data on the modern epidemiology and the changes in the
presentation of the disease, particularly its association with socioeconomic
deprivation due to the recent Van city earthquake. Previous studies have also shown
that the eastern part of Turkey has one of the highest rates of H.
pylori infection. In the present study, the prevalence of H.
pylori in infection gastric biopsy specimens from normal subjects in
the Van region was also found to be as high as 36%. Low educational and
socioeconomic statuses, consumption of smoked, salty, hot, and fatty foods,
overconsumption of hot tea and well water, cigarette smoking, poor intake of fresh
fruits and vegetables and poor hygienic conditions are probable key factors for the
presence of H. pylori infection in the eastern part of Turkey
(1515. Türkdoğan M. Kürşad, Alıcı
Süleyman, İlhan Mahmut, Dilek Hüsniye, Akman Emel, et al.
Helicobacter pylori infection in gastric carcinoma in the Van region of Turkey.
Turk J Gastroenterol. 1999;10(1):36-9.,1616. Türkdoğan MK, Akman N, Tuncer I, Tuncer I, Dilek FH,
et al. The high prevalence of esophageal and gastric cancers in Eastern Turkey.
Med Biol Environ. 1998;26:79-84.). Mounting evidence indicates that disaster survivors are more likely
to experience a lower health-related quality of life compared with their normal
counterparts. In addition to the epidemiologic studies that have shown a strong link
between poor hygienic conditions and GI infections, the effects of increased lower
socioeconomic status during natural disasters also appear to have an impact on
H. pylori infection in patients who live in disaster-stricken
areas. Possible reasons include increased person-to-person transmission of
H. pylori and a lack of hygienic conditions (1717. Waring SC, Brown BJ. The threat of communicable diseases
following natural disasters: a public health response. Disaster Manag Response.
2005;3(2):41-7, http://dx.doi.org/10.1016/j.dmr.2005.02.003.
http://dx.doi.org/10.1016/j.dmr.2005.02....
).
H. pylori infection is a topic of growing importance in developing countries, as a higher prevalence of infection has been described in disaster-stricken areas. Natural disasters, including earthquakes, have also been identified as a key promoting factor for the spread of H. pylori infection, the production of CagA protein and the presence of hemorrhagic gastric ulcers (1818. Yamanaka K, Miyatani H, Yoshida Y, Asabe S, Yoshida T, Nakano M. Hemorrhagic gastric and duodenal ulcers after the Great East Japan Earthquake Disaster. World J Gastroenterol. 2013;19(42):7426-32.).
In this study, the prevalence of H. pylori in dyspeptic patients seeking routine primary care was 80% in recent months, a huge difference between the disaster and current periods. This phenomenon may be linked to worsening socioeconomic conditions in our region in the post-disaster era. This gap needs to be investigated in further studies.
It can be concluded that H. pylori infection is prevalent in dyspeptic patients who live in disaster-hit areas. Our data also indicate that recent earthquake-related conditions may play an important role in the development of H. pylori infection. In addition, there is a close correlation between the recent earthquake and the presence of H. pylori infection. Although the mechanism for this phenomenon is presently unknown, it may be related to the devastating effects of the recent earthquake. Further characterization of disaster-related mechanisms might provide a broader application of novel strategies for preventing H. pylori infection.
REFERENCES
-
1Delport W. The transmission of Helicobacter pylori: The effects of analysis method and study population on inference. Best Pract Res Clin Gastroenterol. 2007;21(2):215-36, http://dx.doi.org/10.1016/j.bpg.2006.10.001.
» http://dx.doi.org/10.1016/j.bpg.2006.10.001 -
2World Gastroenterology Organisation. World Gastroenterology Organisation Global Guideline: Helicobacter pylori in developing countries. J Clin Gastroenterol. 2011;45(5):383-8.
-
3Woodward M, Morrison C, McColl K. An investigation into factors associated with Helicobacter pylori infection. J Clin Epidemiol. 2000;53(2):175-81, http://dx.doi.org/10.1016/S0895-4356(99)00171-7.
» http://dx.doi.org/10.1016/S0895-4356(99)00171-7 -
4Kurokawa M, Nukina M, Nakanishi H, Miki K, Tomita S, Tohdo A. The relationship between hemorrhagic gastric ulcers often appearing among in the great Hanshin-Awaji earthquake sufferers and Helicobacter pylori infections. Kansenshogaku Zasshi. 1996;70(9):970-5, http://dx.doi.org/10.11150/kansenshogakuzasshi1970.70.970.
» http://dx.doi.org/10.11150/kansenshogakuzasshi1970.70.970 -
5Aoyama N, Kinoshita Y, Fujimoto S, Himeno S, Todo A, Kasuga M, et al. Peptic ulcers after the Hanshin-Awaji earthquake: increased incidence of bleeding gastric ulcers. Am J Gastroenterol. 1998;93(3):311-6.
-
6Dominici P, Bellentani S, Di Biase AR, Saccoccio G, Le Rose A, Masutti F, et al. Familial clustering of Helicobacter pylori infection: population based study. BMJ. 1999;319(7209):537-40, http://dx.doi.org/10.1136/bmj.319.7209.537.
» http://dx.doi.org/10.1136/bmj.319.7209.537 -
7Tolon M, Yazgan U, Ural DN, Goss KC. Overview of the critical disaster management challenges faced during Van 2011 earthquakes. J Emerg Manag. 2014;12(1):82-96.
-
8Tack J1, Talley NJ, Camilleri M, Holtmann G, Hu P, Malagelada JR, et al. Functional gastroduodenal disorders. Gastroenterology. 2006;130(5):1466-79, http://dx.doi.org/10.1053/j.gastro.2005.11.059.
» http://dx.doi.org/10.1053/j.gastro.2005.11.059 -
9Ligon BL. Infectious Diseases that Pose Specific Challenges After Natural Disasters: A Review. Semin Pediatr Infect Dis. 2006;17(1):36-45, http://dx.doi.org/10.1053/j.spid.2006.01.002.
» http://dx.doi.org/10.1053/j.spid.2006.01.002 -
10Honarkar Z, Baladast M, Khorram Z, Akhondi Sh, Antikchi M, Masoodi M, et al. An analysis of gastrointestinal symptoms in causalities of catastrophic earthquake of Bam, Iran. SEMJ. 2005;6:1-2.
-
11Kanno T, Iijima K, Abe Y, Koike T, Shimada N, Hoshi T, et al. Peptic ulcers after the Great East Japan earthquake and tsunami: possible existence of psychosocial stressulcers in humans. J Gastroenterol. 2013;48(4):483-90, http://dx.doi.org/10.1007/s00535-012-0681-1
» http://dx.doi.org/10.1007/s00535-012-0681-1 -
12Matsushima Y, Aoyama N, Fukuda H, Kinoshita Y, Todo A, Himeno S, et al. Gastric ulcer formation after the Hanshin-Awaji earthquake: a case study of Helicobacter pylori infection and stress-induced gastric ulcers. Helicobacter. 1999;4(2):94-9, http://dx.doi.org/10.1046/j.1523-5378.1999.98290.x.
» http://dx.doi.org/10.1046/j.1523-5378.1999.98290.x -
13Malfertheiner P, Chan FK, McColl KE. Peptic ulcer disease. Lancet. 2009;374 (9699):1449-61, http://dx.doi.org/10.1016/S0140-6736(09)60938-7.
» http://dx.doi.org/10.1016/S0140-6736(09)60938-7 -
14Onders RP. Detection methods of Helicobacter pylori: accuracy and costs. Am Surg. 1997;63(8):665-8.
-
15Türkdoğan M. Kürşad, Alıcı Süleyman, İlhan Mahmut, Dilek Hüsniye, Akman Emel, et al. Helicobacter pylori infection in gastric carcinoma in the Van region of Turkey. Turk J Gastroenterol. 1999;10(1):36-9.
-
16Türkdoğan MK, Akman N, Tuncer I, Tuncer I, Dilek FH, et al. The high prevalence of esophageal and gastric cancers in Eastern Turkey. Med Biol Environ. 1998;26:79-84.
-
17Waring SC, Brown BJ. The threat of communicable diseases following natural disasters: a public health response. Disaster Manag Response. 2005;3(2):41-7, http://dx.doi.org/10.1016/j.dmr.2005.02.003.
» http://dx.doi.org/10.1016/j.dmr.2005.02.003 -
18Yamanaka K, Miyatani H, Yoshida Y, Asabe S, Yoshida T, Nakano M. Hemorrhagic gastric and duodenal ulcers after the Great East Japan Earthquake Disaster. World J Gastroenterol. 2013;19(42):7426-32.
-
No potential conflict of interest was reported.
Publication Dates
-
Publication in this collection
Jan 2015
History
-
Received
19 Sept 2014 -
Reviewed
29 Aug 2014 -
Accepted
12 Nov 2014