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Year : 2009  |  Volume : 15  |  Issue : 3  |  Page : 201-207
Helicobacter pylori infection in developing countries: The burden for how long?


Department of Biology, Fatih University, Faculty of Science, Istanbul, Turkey

Click here for correspondence address and email

Date of Submission03-Apr-2009
Date of Acceptance25-May-2009
Date of Web Publication24-Jul-2009
 

   Abstract 

Approximately 50% (over 3 billion) of the world populations are known to be infected with Helicobacter pylori , mainly in the developing countries . Among those, hundreds of millions of people develop peptic ulceration during their lifetime and still tens of millions might progress to gastric cancer. Possible modes of H. pylori transmission generally described are through direct contact between family members and also through contaminated water and food. Because the high prevalence of infection occurs mainly in developing countries and because the test-and-treat strategy puts a huge economic burden on many of these countries, it is time to take an immediate action toward this bacterial infection and adopt a strategy to prevent it. To address this issue, an updated prevalence of infection, modes of transmission, economics of infection and preventative measures to block the infection process have been discussed.

Keywords: Helicobacter pylori , modes of transmission, preventative measures, prevalence of infection

How to cite this article:
Salih BA. Helicobacter pylori infection in developing countries: The burden for how long?. Saudi J Gastroenterol 2009;15:201-7

How to cite this URL:
Salih BA. Helicobacter pylori infection in developing countries: The burden for how long?. Saudi J Gastroenterol [serial online] 2009 [cited 2019 May 26];15:201-7. Available from: http://www.saudijgastro.com/text.asp?2009/15/3/201/54743


Helicobacter pylori infection is well known to be the most common human infection worldwide on the basis of the fact that approximately 50% of the world's populations are infected and that human beings are the main reservoir. [1],[2] The pattern of infection is an early childhood acquisition of H. pylori (30%-50%) that reaches over 90% during adulthood in developing countries. This has been attributed to the poor socioeconomic status and overcrowded conditions. [3],[4],[5] Infection in developed countries is less common in young children and reaches up to 60% in older ages. [1],[6],[7] In the United States, a 20% infection rate among adolescents is being reported, [7] and recently an overall prevalence of 36% was reported, suggesting rapidly improving socioeconomic conditions. [8] While the prevalence of infection has decreased significantly in many parts of North America and Western Europe, no such decline has been noted in the majority of the developing world. [7]

H. pylori is the causative agent of chronic gastritis and peptic ulcer diseases and is an important risk factor for the development of gastric cancer and mucosal-associated lymphoid tissue (MALT) lymphoma. [9],[10],[11]

Although the world health organization (WHO) estimates indicate high infection rates among the world populations , most infected subjects develop no clinical symptoms or peptic ulceration and continue their life with superficial chronic gastritis. [12],[13],[14],[15] However, still high percentages (approximately 17%) of the infected subjects will develop peptic ulcers and one-quarter of such patients (approximately 4.25%) even experience ulcer complications, [16] and still fewer (1%) will progress to gastric cancers. [10],[16] If we consider these percentages in terms of numbers, then it is expected that several hundreds of millions (approximately 500 million) sooner or later will suffer from severe gastric pathology (peptic ulceration) and tens of millions (approximately 30 million) might progress to gastric cancer. A majority of these patients are within the populations of the developing countries.


   Prevalence of Infection Top


All reports on the prevalence of infection indicate that subjects are infected with H. pylori early in childhood (<5 years of age) and that the risk of infection declines rapidly after that. [1],[2],[3],[4],[16],[17] In developed countries [Table 1], Granstrom et al . [18] have monitored a cohort of Swedish children of age ranging from 6 months to 11 years and found that 13.6% were infected between 18 and 24 months of age; however, at age 11, only 3% of children were seropositive. Prevalence rates of 8.6% [19] and 2.4% [20] were reported for children aged 3 years in Ireland and in Germany, respectively. Recently, Okuda et al . [21] reported an overall rate of 3.7% in Japanese children aged <2 years. While in developing countries [Table 1] a prevalence rate of 22.6% was reported in Vietnamese children aged <3 years, [22] 46.7% in Mexican children <5 years, [23] 33% in Egyptian children <6 years, [24] 80% in Bangladeshi children <5 years, [25] 57% in Indian children <5 years, [26] 40% in Brazilian children <6 years, [27] 32.4% in Saudi children <10 years [28] and 41% in Turkish children <6 years. [29],[30] Infection of subjects with H. pylori after this period continues but at much lower rate. [16] A seroconversion rate of 1.8% per year for children and 1.5% for adults was reported. [31] In another study, a reinfection rate of 2.0% per year was reported for children older than 5 years. [19] It was also shown that reinfection with H. pylori after treatment occurs rarely in children older than 5 years regardless of socioeconomic group or number of infected family members. [16] This might suggest that continuous contact between family members is required for the acquisition of H. pylori because children older than 5 years (school age) who spend less time at home are less commonly infected.

In adults, the H. pylori infection rates are even higher and increase with age. A recent report from India indicates that almost 80% of the population is infected with H. pylori. [32] Similarly, Mishra et al . [26] indicated that earlier report showed 80-90% infection rates by the age of 20 years. In another recent report, the overall prevalence of H. pylori was detected to be 80% that reached 90% in subjects aged 70-79 years. [33] Considering the current population of India, which is 1.15 billion according to the United States Census Bureau, [34] around 918 million people (80%) are currently infected and the rates are not different from those reported in 1991. In China, an early report (1995) showed an overall 61% prevalence rate of H. pylori infection, [35] and in 2008, 2 reports showed similar percentages of 62% [36] and 60-70%, [37] indicating no changes in the prevalence of H. pylori , but on the contrary an increase in the infected population had occurred. The current population of China is 1.33 billion, [34] which also indicates that approximately 824 million people are infected. Reports from other highly populated developing countries showed similar infection rates. In Brazil, an overall prevalence rate of 65% was reported in healthy individuals. [38] In Bangladesh, H. pylori prevalence of more than 90% was reported in asymptomatic adults. [25] We have also found an overall 70% infection rate in asymptomatic Turkish subjects that reached up to 100% in subjects aged 60-69 years. [30]

Recently, a study on children aged 2-19 years in St. Petersburg, Russia, showed an overall decline in H. pylori prevalence rate from 44% in 1995 to 13% in 2005. The prevalence decreased from 30% among children younger than 5 years in 1995 to 2% after 10 years in the same age group. The authors correlated these findings with the improvements in the standards of living. [39] Similarly, reports from South Korea showed an overall H. pylori infection rate of 75% in adults in 1996, [40] 66.9% in 1998 that decreased to 59.6% in 2005 [41] and, more recently, [42] a decline from 64.7% to 40.0% in the 8-year period (1998-2005) has been reported. Whether this drop is a local phenomenon or a national trend has to be investigated in those countries. However, there is a common consensus that the risk of acquisition and transmission of H. pylori can be minimized and prevented to a large extent by implementation of household hygiene, boiling water for drinking purposes and proper cleaning of vegetables.


   Modes of Transmission Top


Several modes of transmission of H. pylori have been described in the literature; these included direct contact between subjects, which is considered the most common mode, [2],[43],[44],[45] contaminated water sources and food [2],[46],[47],[48] and, less commonly, iatrogenic transmission (during endoscopies and dental care) [2] and zoonotic transmission. [2],[48]

Direct contact

For several years now researchers have attempted to define the exact mode of transmission of H. pylori and the role of subjects in this process.

Role of mother-to-child

Many investigators have studied the role of familial clustering in the spread of H. pylori infection and the majority indicated that mothers play the key role in transmission of H. pylori to their children and spouses. [43],[44],[45],[49],[50],[51],[52],[53],[54],[55],[56],[57],[58] In a study conducted on children of the Canadian First Nations community who were negative for H. pylori at entry, 16% acquired H. pylori over 1 year period from their positive mothers. [48] Malaty et al . [55] examined the longitudinal changes in H. pylori infection monitored from 1986-1994 within 46 families with children living in Japan. At study entry, prevalence of H. pylori in children with positive mothers was 23% versus 5% in children with negative mothers. Their data strongly support the key role of the infected mothers in the transmission within families and also indicated that seroconversion rate of 1.5% per year was evident only among children living with positive mothers that did not differ among adults living with or without children.

Tindberg et al . [49] compared the risk of H. pylori infection between family members and extraneous child-to-child transmission among Swedish school children with varying family backgrounds. They found 2% seroprevalence among children with Scandinavian parents and 55% among children with origin in high prevalence areas (Middle East and Africa). They concluded that intrafamilial transmission is far more important than child-to-child transmission outside the family. In a study from Eastern Turkey, it was shown that seroprevalence was also higher in children (49%) whose mothers were infected than in children (22.6%) of uninfected mothers. [51] Malaty [16] reported that if one index parent is positive for H. pylori then 40% of children were found to turn positive, while if both parents are negative only 3% of children turn positive. In China, it was also reported that in families with at least one infected parent, 85% of children were H. pylori positive, while in families with both parents uninfected, only 22% of children were H. pylori positive. [59] Similarly, investigators from Brazil reported that seropositivity was higher in family members of infected symptomatic index subjects than family members of uninfected index subject, especially mothers and siblings. They emphasized the role of mothers and siblings but not fathers in the transmission of H. pylori. [53] In a community-based cross-sectional study in 533 participants from 135 household members, with multiple generations living in the same house in Vietnam, H. pylori infection in children was found significantly associated with infection of the mothers, which supports the hypothesis of intrafamilial transmission. [60]

It appears that in developing countries, overcrowded conditions that create closer contacts between mothers and children and between siblings sharing the same bed might be the main reason for the high infection rates reported. In addition, in these countries working fathers had little contact with their children and that is why transmission of H. pylori was mostly linked to the mother.

Role of spouse-to-spouse

In a recent study in Germany, prevalence of infection was 34.9% among women whose partners were infected and 14.5% when the partner was not infected. [61] Malaty [16] reported that if one spouse is positive for H. pylori then 68% of spouses turn positive, while if negative 9% of spouses were found positive. We also found in Turkey that H. pylori infection was significantly higher among married subjects and those with low socioeconomic status. [30] It was also reported that the risk of infection increases with the number of years lived with an infected partner. A 42% of subjects were found positive when living with an infected partner, while only 7% were infected when living with an uninfected partner. [62] These results support the hypothesis of a major role of spouse-to-spouse transmission of H. pylori infection and that continuous contact is required for the establishment of such infection.

Transmission among non-family members

Triantafillidis et al . [63] investigated whether medical or non-medical staff in a large acute care hospital was at increased risk of acquiring H. pylori infection over a 5-year period. They observed an annual seroconversion rate of 4.95% and found that nursing staff had a significantly higher risk of infection compared with administrative and technical staff. The person-to-person mode of transmission is supported by the higher incidence of infection among institutionalized children and adults and the clustering of H. pylori infection within families. Also in support to this concept is the detection of H. pylori DNA in vomitus, saliva, dental plaque, gastric juice and feces. [2] The abovementioned data suggest that transmission of H. pylori can occur between individuals irrespective of their close relations provided that they maintain close contact for long periods.

Contaminated water sources and food

Klein et al . [46] reported earlier that the municipal water supply seems to be an important source of H. pylori infection among Lima children from families of both low and high socioeconomic status. Consumption of uncooked vegetables has also been described as a mode for transmission of H. pylori . [47] Goodman et al . [48] also reported that children swimming in rivers or pools as did using streams as a drinking water source and those who frequently consumed raw vegetables were more likely to have the infection.

For the general population, it appears that the most likely mode of transmission is direct contact, by either the oral-oral route (through vomitus and saliva) or perhaps the fecal-oral route. Waterborne transmission, probably due to fecal contamination, may also be an important source of infection, especially in parts of the world in which untreated water is common. [2] Overall, inadequate sanitation practices, low socioeconomic status and overcrowded or high-density living conditions seem to be related to higher prevalence of H. pylori infection. [2] These studies suggest that the main critical period of life for acquiring H. pylori infections is the first 5 years of childhood and at adulthood were married couples living together.


   Economics of H Pylori Infection Top


Health care is becoming more and more expensive as accompanied by the increase in the standards of living. More importantly, the increase in population size mainly in developing countries makes coverage for health insurance a big burden on governments. The economics of H. pylori infection have been analyzed using the test and treat strategy and evidence for effectiveness gained from randomized controlled trials suggested that treating H. pylori is also more effective and less expensive than continuous PPI therapy, and is therefore the dominant strategy in treating peptic ulcer disease. [64]

Ladabaum et al . [65] have estimated the cost per dyspeptic patient managed by the test and treat strategy ($545) or by the PPI ($529) and recommended the first strategy. Delaney et al . [66] also found the test and treat strategy to be more effective than acid suppression alone and reported a mean additional cost of US$401 for endoscopy. Ebell et al . [67] have investigated the cost per quality-adjusted life year (QALY) and reported that two strategies are reasonable for patients presenting with dyspepsia: (1) empiric H. pylori eradication that costs $1198 per QALY, and (2) use of a serum H. pylori titer to identify patients who might benefit from H. pylori eradication at a cost of $1214 per QALY. In China, comparison of the incremental costs per ulcer treatment using the test and treat strategy, endoscopy and empirical PPI therapy showed US$1778, US$1797 and US$2158, respectively. [68] In Finland, Farkkila et al . [69] indicated that the test and treat strategy significantly reduced peptic ulcer disease and improved dyspeptic symptoms and quality of life but did not reduce the number of endoscopies. Mason et al . [70] in their randomized controlled trial using economic model suggested that population H. pylori screening and treatment for 1,000,000 45-year-olds would save over 6,000,000 pounds sterling and 1300 years of life. In another study, the cost-effectiveness of performing routine biopsies for the detection of H. pylori in non-ulcer dyspepsia patients showed an incremental cost of $10,716 per 100 treated patients. [71]

Most of these estimates came from studies conducted in developed countries and unfortunately no sufficient data is available yet from developing countries. Owing to the huge number of infected subjects in those countries, the number of routine upper endoscopies conducted is also very high. We have reported on such numbers in our recent study. On average 1500 endoscopies are being conducted in one year by a single clinician in a state hospital in Istanbul. [72]

From the abovementioned studies it is obvious that the health economics of managing H. pylori infection to prevent the occurrence of peptic ulcer and gastric cancer is highly expensive. With the enormous and continuous increase in the world population size, it is going to be very difficult to deal with such an infection even in the immediate future, particularly in developing countries. According to the United States Census Bureau [34] the world population will reach 7.5 billion in the year 2020, which indicates that an additional several hundred millions of infected subjects will be added to the already currently infected over 3 billion subjects . Such an increase will have an even greater impact on the economic burden that is already being overloaded. With all evidence being pointed toward the familial clustering of H. pylori, the main focus then is to block the process among family members and improve sanitary measures.


   Preventative Measures Top


Establish a campaign for educating people, particularly infected mothers and newlywed couples about familial clustering of H. pylori infection and the risk of infecting others by direct contact and exchange of saliva.

Implementation of sanitary measures among family members (hand and mouth wash, brushing teeth, no sharing of food plates or drinking glasses, no sharing of spoons in feeding children, no bed sharing between siblings).

Routine testing of newlywed couples (depends on the availability of equipments and cost of the test). If they are found to be H. pylori positive, recommendations should be provided for strict implementation of sanitary measures to prevent partner infection and also future infection of their children. Marshall et al . [73] have indicated earlier that in low-risk asymptomatic patients with dyspepsia, testing for H. pylori using serology appears to be economical and that 13 C-labeled urea breath test (13 C-UBT) may also be a cost-effective alternative to serology depending on the current cost of each test. In a study on patient acceptance of tests, it was reported that the stool test would be less popular than a blood test or UBT and may have less compliance. Patients might not come back to bring the stool specimen; however, the blood test or UBT can be done before they leave. [74]

Recommendations for adopting the 13 C-UBT test as an additional mandatory test together with the already existing mandatory tests (HIV, HBV, HCV and Syphilis) required for all newlywed couples before registration. This will help partners in applying strict sanitary measures so as to not transfer infection between each other and to their future children and also in future follow-up of subjects who develop dyspepsia for treatment recommendation.

Test-and-treat strategy for mothers with recurrent dyspepsia; if found H. pylori positive, a recommendation for testing family members.

Routine testing of drinking water sources for H. pylori contamination, especially in poor communities and recommendations for boiling water before drinking.

The issue of vaccination and the status of vaccine against H. pylori is currently still under development. According to Kabir [75] who indicated that although extensive studies in the mouse model have demonstrated the feasibility of both therapeutic and prophylactic immunizations, the mechanism of vaccine-induced protection is poorly understood as several factors such as immunoglobulin and various cytokines do not contribute to protection. Svennerholm et al . [76] also reported that there is still a strong need to clarify the main protective immune mechanisms against H. pylori and to identify a cocktail of strong protective antigens, or recombinant bacterial strains that express antigens that could be administered by a regimen that gives rise to effective immune responses in humans.


   Conclusions Top


Because most H. pylori infections acquired during early childhood, particularly in children aged less than 5 years, a continuous contact is required for the establishment of a real infection that can last lifelong. Infection rates are lower after this period due to the fact that less contact occurs between mothers and children. This is because children start their school year and spent more time outside their home. Infection with H. pylori continues to be acquired by children after that but at lower rates depending on the mode of transmission. During adult life, however, married couples are also at high risk of infection if one spouse is infected. Keeping this in mind, serious measures should be taken immediately to advocate the implementation of sanitary conditions and education against the transmission of H. pylori to block the infection process.

 
   References Top

1.Go MF. Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 2002;16:3-15.   Back to cited text no. 1    
2.Brown LM. Helicobacter pylori epidemiology and routes of transmission. Epidemiol Rev 2000;22:283-97.  Back to cited text no. 2  [PUBMED]  [FULLTEXT]
3.Megraud F. Epidemiology of Helicobacter pylori infection. In Helicobacter pylori and gastrointestinal disease. In Rathbone BJ, Heatley RV. Editors. Oxford: Blackwell Scientific; 1992. p. 107-23.   Back to cited text no. 3    
4.Bardhan PK. Epidemiological features of Helicobacter pylori infection in developing countries. Clin Infect Dis 1997;25:973-8.  Back to cited text no. 4  [PUBMED]  
5.Cheng H, Hu F, Zhang L, Yang G, Ma J, Hu J, et al . Prevalence of Helicobacter pylori infection and identification of risk factors in rural and urban Beijing, China. Helicobacter 2009;14:128-33.  Back to cited text no. 5  [PUBMED]  [FULLTEXT]
6.Axon AT. The transmission of Helicobacter pylori : which theory fits the facts? Euro J Gastroenterol Hepatol 1996;8:1-2.  Back to cited text no. 6    
7.Frenck RW Jr, Clemens J. Helicobacter in the developing world. Microbes Infect 2003;5:705-13.  Back to cited text no. 7  [PUBMED]  [FULLTEXT]
8.Smith JG, Li W, Rosson RS. Prevalence, clinical and endoscopic predictors of Helicobacter pylori infection in an urban population. Conn Med 2009;73:133-7.  Back to cited text no. 8  [PUBMED]  
9.Maeda S, Mentis AF. Pathogenesis of Helicobacter pylori infection. Helicobacter 2007;12:10-4.  Back to cited text no. 9  [PUBMED]  [FULLTEXT]
10.McGee DJ, Mobley HL. Pathogenesis of Helicobacter pylori infection. Current Opin Gastroenterol 2000;16:24-31.  Back to cited text no. 10    
11.Mbulaiteye SM, Hisada M, El-Omar EM. Helicobacter pylori associated global gastric cancer burden. Front Biosci 2009;14:1490-504.  Back to cited text no. 11  [PUBMED]  [FULLTEXT]
12.Moss SF, Malfertheiner P. Helicobacter and gastric malignancies. Helicobacter 2007;12:23-30.  Back to cited text no. 12  [PUBMED]  [FULLTEXT]
13.Hunt RH. The role of H. pylori in pathogenesis: the spectrum of clinical outcomes. Scand J Gastroenterol 1996;31:3-9.  Back to cited text no. 13    
14.Blaser MJ. Medical significance of H. pylori . In Helicobacter pylori protocols. In: Clayton CL, Mobley HL, editors. New Jersey: Humana Press; 1997. p. 1-6.  Back to cited text no. 14    
15.Rothenbacher D, Brenner H. Burden of Helicobacter pylori and H. pylori -related diseases in developed countries: recent developments and future implications. Microbes Infect 2003;5:693-703.  Back to cited text no. 15    
16.Malaty HM. Epidemiology of Helicobacter pylori infection. Best Prac Res Clin Gastroenterol 2007;21:205-14.   Back to cited text no. 16    
17.Rowland M, Daly L, Vaughan M, Higgins A, Bourke B, Drumm B. Age-specific incidence of Helicobacter pylori . Gastroenterol 2006;130:65-72.  Back to cited text no. 17    
18.Granstrom M, Tindberg Y, Blennow M. Seroepidemiology of Helicobacter pylori infection in a cohort of children monitored from 6 months to 11 years of age. J Clin Microbiol 1997;35:468-70.  Back to cited text no. 18    
19.Rowland M, Kumar D, Daly L, O′Connor P, Vaughan D, Drumm B. Low rates of Helicobacter pylori reinfection in children. Gastroenterol 1999;117:336-41.  Back to cited text no. 19    
20.Weyermann M, Adler G, Brenner H, Rothenbacher D. The mother as source of Helicobacter pylori infection. Epidemiol 2006;17:332-4.  Back to cited text no. 20    
21.Okuda M, Miyashiro E, Booka M, Tsuji T, Nakazawa T. Helicobacter pylori Colonization in the First 3 Years of Life in Japanese Children. Helicobacter 2007;12:324-7.  Back to cited text no. 21  [PUBMED]  [FULLTEXT]
22.Nguyen BV, Nguyen KG, Phung CD, Kremp O, Kalach N, Dupont C, et al . Prevalence of and factors associated with Helicobacter pylori infection in children in the north of Vietnam. Am J Trop Med Hyg 2006;74:536-9.   Back to cited text no. 22  [PUBMED]  [FULLTEXT]
23.Nares-Cisneros J, Jaramillo-Rodrνguez Y, Martνnez-Ordaz VA, Velasco-Rodrνguez VM, Madero A, Mena-Arias G, et al . Immunochromatographic Monoclonal Test for Detection of Helicobacter pylori Antigen in Stool is Useful in Children from High-Prevalence Developing Country. Helicobacter 2007;12:354-8.  Back to cited text no. 23    
24.Frenck RW Jr, Fathy HM, Sherif M, Mohran Z, El Mohammedy H, Francis W, et al . Sensitivity and specificity of various tests for the diagnosis of Helicobacter pylori in Egyptian children. Pediatrics 2006;118:1195-202.  Back to cited text no. 24    
25.Ahmad MM, Ahmed DS, Rowshon AH, Dhar SC, Rahman M, Hasan M, et al . Long-term re-infection rate after Helicobacter pylori eradication in Bangladeshi adults. Digestion 2007;75:173-6.  Back to cited text no. 25  [PUBMED]  [FULLTEXT]
26.Mishra S, Singh V, Rao GR, Dixit VK, Gulati AK, Nath G. Prevalence of Helicobacter pylori in asymptomatic subjects-A nested PCR based study. Infect Genet Evol 2008;8:815-9.  Back to cited text no. 26  [PUBMED]  [FULLTEXT]
27.Braga AB, Fialho AM, Rodrigues MN, Queiroz DM, Rocha AM, Braga LL. Helicobacter pylori colonization among children up to 6 years: results of a community-based study from Northeastern Brazil. J Trop Pediatr 2007;53:393-7.  Back to cited text no. 27  [PUBMED]  [FULLTEXT]
28.Marie MA. Seroprevalence of Helicobacter pylori infection in large series of patients in an urban area of Saudi Arabia. Korean J Gastroenterol 2008;52:226-9.  Back to cited text no. 28  [PUBMED]  [FULLTEXT]
29.Ertem D, Harmanci H, Pehlivanoπlu E.Helicobacter pylori infection in Turkish preschool and school children: role of socioeconomic factors and breast feeding. Turk J Pediatr 2003;45:114-22.   Back to cited text no. 29    
30.Abasiyanik MF, Tunc M, Salih BA. Enzyme immunoassay and immunoblotting analysis of Helicobacter pylori infection in Turkish asymptomatic subjects. Diag Microbio Infect Dis 2004;50:173-7.  Back to cited text no. 30    
31.Kumagai T, Malaty HM, Graham DY, Hosogaya S, Misawa K, Furihata K, et al . Acquisition versus loss of Helicobacter pylori infection in Japan: results from an 8-year birth cohort study. J Infect Dis 1998;178:717-21.  Back to cited text no. 31  [PUBMED]  
32.Poddar U, Yachha SK. Helicobacter pylori in children: an Indian perspective. Indian Pediatr 2007;44:761-70.  Back to cited text no. 32  [PUBMED]  [FULLTEXT]
33.Ahmed KS, Khan AA, Ahmed I, Tiwari SK, Habeeb A, Ahi JD, et al . Impact of household hygiene and water source on the prevalence and transmission of Helicobacter pylori : a South Indian perspective. Singapore Med J 2007;48:543-9.  Back to cited text no. 33  [PUBMED]  [FULLTEXT]
34.The United States Census Bureau. World population (International data base). Available from: http://www.census.gov/ipc/www/idb/worldpopinfo.html. [cited on 2008 Oct 10].  Back to cited text no. 34    
35.Zhou D, Yang H. Epidemiology of Helicobacter pylori infection in the People′s Republic of China. Chin Med J (Engl) 1995;108:304-13.  Back to cited text no. 35  [PUBMED]  
36.Shi R, Xu S, Zhang H, Ding Y, Sun G, Huang X, et al . Prevalence and risk factors for Helicobacter pylori infection in Chinese populations. Helicobacter 2008;13:157-65.  Back to cited text no. 36  [PUBMED]  [FULLTEXT]
37.Zhang Z, Zheng Q, Chen X, Xiao S, Liu W, Lu H. The Helicobacter pylori duodenal ulcer promoting gene, dupA in China. BMC Gastroenterol 2008;8:49.  Back to cited text no. 37  [PUBMED]  [FULLTEXT]
38.Zaterka S, Eisig JN, Chinzon D, Rothstein W. Factors related to Helicobacter pylori prevalence in an adult population in Brazil. Helicobacter 2007;12:82-8.  Back to cited text no. 38  [PUBMED]  [FULLTEXT]
39.Tkachenko MA, Zhannat NZ, Erman LV, Blashenkova EL, Isachenko SV, Isachenko OB, et al . Dramatic changes in the prevalence of Helicobacter pylori infection during childhood: a 10-year follow-up study in Russia. J Pediatr Gastroenterol Nutr 2007;45:428-32.  Back to cited text no. 39  [PUBMED]  [FULLTEXT]
40.Malaty HM, Kim JG, Kim SD, Graham DY. Prevalence of Helicobacter pylori infection in Korean children: inverse relation to socioeconomic status despite a uniformly high prevalence in adults. Am J Epidemiol 1996;143:257-62.  Back to cited text no. 40  [PUBMED]  [FULLTEXT]
41.Do MY, Lee YC, Choi CH, Kim SJ, Mun CS, Moon HJ, et al . The changes in prevalence and the related factors of Helicobacter pylori infection in Korean health check-up subjects during 8 years. Korean J Gastroenterol 2009;53:76-83.  Back to cited text no. 41  [PUBMED]  [FULLTEXT]
42.Yim JY, Kim N, Choi SH, Kim YS, Cho KR, Kim SS, et al . Seroprevalence of Helicobacter pylori in South Korea. Helicobacter 2007;12:333-40.  Back to cited text no. 42  [PUBMED]  [FULLTEXT]
43.Kivi M, Johansson AL, Reilly M, Tindberg Y. Helicobacter pylori status in family members as risk factors for infection in children. Epidemiol Infect 2005;133:645-52.  Back to cited text no. 43  [PUBMED]  
44.Malaty HM, Graham DY, Klein DG, Evans DG, Adam E, Evans DJ. Transmission of Helicobacter pylori infection: studies in families of health individuals. Scand J Gastroenterol 1991;26:927-32.  Back to cited text no. 44    
45.Farrell S, Doherty GM, Milliken I, Shield MD, McCallion WA. Risk factors for Helicobacter pylori infection in children: an examination of the role played by intrafamilial bed sharing. Pediatr Infect Dis J 2005;24:149-52.  Back to cited text no. 45  [PUBMED]  [FULLTEXT]
46.Klein PD, Graham DY, Gaillour A, Opekun AR, Smith EO. Water source as risk factor for Helicobacter pylori infection in Peruvian children. Gastrointestinal Physiology Working Group. Lancet 1991;337:1503-6.  Back to cited text no. 46    
47.Hopkins RJ, Vial PA, Ferreccio C, Ovalle J, Prado P, Sotomayor V, et al . Seroprevalence of Helicobacter pylori in Chile: vegetables may serve as one route of transmission. J Infect Dis 1999;168:222-6.  Back to cited text no. 47    
48.Goodman KJ, Correa P, Tengana Aux HJ, Ramirez H, DeLany JP, et al . Helicobacter pylori infection in the Colombian Andes: a population-based study of transmission pathways. Am J Epidemiol 1996;144:290-9.  Back to cited text no. 48    
49.Tindberg Y, Bengtsson C, Granath F, Blennow M, Nyren O, Granstrom M. Helicobacter pylori infection in Swedish school children: lack of evidence of child-to-child transmission outside the family. Gastroenterol 2001;121:310-6.  Back to cited text no. 49    
50.Al-Knawy BA, Ahmed ME, Mirdad S, ElMekki A, Al-Ammari O. Intrafamilial clustering of Helicobacter pylori infection in Saudi Arabia. Can J Gastroenterol 2000;14:772-4.  Back to cited text no. 50  [PUBMED]  [FULLTEXT]
51.Yilmaz E, Dogan Y, Gurgoze MK, Unal S. Seroprevalence of Helicobacter pylori infection among children and their parents in eastern Turkey. J Paediatr Child Health 2002;38:183-6.  Back to cited text no. 51    
52.Sinha SK, Martin B, Gold BD, Song Q, Sargent M, Bernstein CN. The incidence of Helicobacter pylori acquisition in children of a Canadian First Nations community and the potential for parent-to-child transmission. Helicobacter 2004;9:59-68.   Back to cited text no. 52  [PUBMED]  [FULLTEXT]
53.Escobar ML, Kawakami E. Evidence of mother-child transmission of Helicobacter pylori infection. Arq Gastroenterol 2004;41:239-44.  Back to cited text no. 53  [PUBMED]  [FULLTEXT]
54.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;319:537-40.  Back to cited text no. 54  [PUBMED]  [FULLTEXT]
55.Malaty HM, Graham DY, Isaksson I Engstrand L, Pedersen NL. Are genetic and environmental components of peptic ulcer disease: a study of twins reared apart and twins reared together? Arch Intern Med 2000;160:105-9.  Back to cited text no. 55    
56.Wizla-Derambure N, Michaud L, Ategbo S, Vincent P, Ganga-Zandzou S, Turck D, et al . Familial and community environmental risk factors for Helicobacter pylori infection in children and adolescents. J Pediatr Gastroenterol Nutr 2001;33:58-63.  Back to cited text no. 56  [PUBMED]  [FULLTEXT]
57.Zhou H, Chan KL, Chu KM, Tam PK. Intrafamilial spread of Helicobacter pylori : a prospective study using urea breath test. J Pediatr Surg 2000;35:1672-5.  Back to cited text no. 57  [PUBMED]  [FULLTEXT]
58.Rothenbacher D, Winkler M, Gonser T, Adler G Brenner H. Role of infected parents in transmission of Helicobacter pylori to their children. Pediatr Infect Dis J 2002;21:674-9.  Back to cited text no. 58    
59.Ma JL, You WC, Gail MH, Zhang L, Blot WJ, Chang YS, et al . Helicobacter pylori infection and mode of transmission in a population at high risk of stomach cancer. Int J Epidemiol 1998;27:570-3.  Back to cited text no. 59  [PUBMED]  [FULLTEXT]
60.Nguyen VB, Nguyen GK, Phung DC, Okrainec K, Raymond J, Dupond C, et al . Intra-familial transmission of Helicobacter pylori infection in children of households with multiple generations in Vietnam. Eur J Epidemiol 2006;21:459-63.  Back to cited text no. 60  [PUBMED]  [FULLTEXT]
61.Brenner H, Weyermann M, Rothenbacher D. Clustering of Helicobacter pylori infection in couples: differences between high- and low-prevalence population groups. Ann Epidemiol 2006;16:516-20.  Back to cited text no. 61  [PUBMED]  [FULLTEXT]
62.Brenner H, Rothenbacher D, Bode G, Dieudonne P, Adler G. Active infection with Helicobacter pylori in healthy couples. Epidemiol Infect 1999;122:91-5.  Back to cited text no. 62    
63.Triantafillidis JK, Gikas A, Hyphantis T, Cheracakis P, Rokkas T, Konstantellou E, et al . Helicobacter pylori infection in hospital workers over a 5-year period: correlation with demographic and clinical parameters. J Gastroenterol 2002;37: 1005-13.  Back to cited text no. 63  [PUBMED]  [FULLTEXT]
64.Moayyedi P. The health economics of Helicobacter pylori infection. Best Pract Res Clin Gastroenterol 2007;21:347-61.  Back to cited text no. 64  [PUBMED]  [FULLTEXT]
65.Ladabaum U, Chey WD, Scheiman JM, Fendrick AM. Reappraisal of non-invasive management strategies for uninvestigated dyspepsia: a cost-minimization analysis. Aliment Pharmacol Ther 2002;16:1491-501.  Back to cited text no. 65  [PUBMED]  [FULLTEXT]
66.Delaney B, Ford AC, Forman D, Moayyedi P, Qume M. Initial management strategies for dyspepsia. Cochrane Database Syst Rev 2005;4:CD001961.  Back to cited text no. 66  [PUBMED]  [FULLTEXT]
67.Ebell MH, Warbasse L, Brenner C. Evaluation of the dyspeptic patient: a cost-utility study. J Fam Pract 1997;44:545-55.  Back to cited text no. 67  [PUBMED]  
68.You JH, Wong PL, Wu JC. Cost-effectiveness of Helicobacter pylori "test and treat" for patients with typical reflux symptoms in a population with a high prevalence of H. pylori infection: a Markov model analysis. Scand J Gastroenterol 2006;41:21-9.  Back to cited text no. 68    
69.Farkkila M, Sarna S, Valtonen V, V, Sipponen P; PROSPER Study Group. Does the ′test-and-treat′ strategy work in primary health care for management of uninvestigated dyspepsia? A prospective two-year follow-up study of 1552 patients. Scand J Gastroenterol 2004;39:327-35.   Back to cited text no. 69    
70.Mason J, Axon AT, Forman D, Duffett S, Drummond M, Crocombe W, et al . The cost-effectiveness of population Helicobacter pylori screening and treatment: a Markov model using economic data from a randomized controlled trial. Aliment Pharmacol Ther 2002;16:559-68.  Back to cited text no. 70  [PUBMED]  [FULLTEXT]
71.Makris N, Crott R, Fallone CA, Bardou M, Barkun A. Cost-effectiveness of routine endoscopic biopsies for Helicobacter pylori detection in patients with non-ulcer dyspepsia. Gastrointest Endosc 2003;58:14-22.  Back to cited text no. 71  [PUBMED]  [FULLTEXT]
72.Bayyurt N, Abasiyanik MF, Sander E, Salih BA. Canonical correlation analysis of factors involved in the occurrence of peptic ulcers. Digest Dis Sci 2007;52:140-6.  Back to cited text no. 72  [PUBMED]  [FULLTEXT]
73.Marshall JK, Armstrong D, O′Brien BJ. Test and treat strategies for Helicobacter pylori in uninvestigated dyspepsia: a Canadian economic analysis. Can J Gastroenterol 2000;14:379-88.  Back to cited text no. 73  [PUBMED]  [FULLTEXT]
74.McNulty C, Freeman E, Delaney B. Helicobacter pylori test and treat strategy for dyspepsia: a qualitative study exploring the barriers and how to overcome them. Fam Pract 2006;23:203-9.   Back to cited text no. 74  [PUBMED]  [FULLTEXT]
75.Kabir S. The current status of Helicobacter pylori vaccines: a review. Helicobacter 2007;12:89-102.  Back to cited text no. 75  [PUBMED]  [FULLTEXT]
76.Svennerholm AM, Lundgren A. Progress in vaccine development against Helicobacter pylori . FEMS Immunol Med Microbiol 2007;50:146-56.  Back to cited text no. 76  [PUBMED]  [FULLTEXT]

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Correspondence Address:
Barik A Salih
Department of Biology, Fatih University, Faculty of Science, Istanbul
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1319-3767.54743

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