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Italian Journal of Food Safety logoLink to Italian Journal of Food Safety
. 2024 May 16;13(3):12176. doi: 10.4081/ijfs.2024.12176

Review of foodborne helicobacteriosis

Contributions: all the authors made a substantial intellectual contribution, read and approved the final version of the manuscript, and agreed to be accountable for all aspects of the work.: Dhary Alewy Almashhadany 1,✉, Mustafa Abdulmonam Zainel 2, Taha Talal AbdulRahman 2
PMCID: PMC11411406  PMID: 39301146

Abstract

Helicobacteriosis is a common bacterial infection caused by Helicobacter pylori. It affects the stomach and small intestines, leading to inflammation. Bacteria can spread through contaminated food or water. This review explores the role of food in the transmission of H. pylori, drawing on research from the past three decades. People commonly acquire the infection during childhood, often from close family members. Crowded living conditions can also contribute to the spread. This review also discusses various risk factors and highlights the challenges of detecting H. pylori, particularly in its dormant form. Techniques like ribotyping and restriction fragment length polymorphism hold promise for tracing transmission routes, but more long-term studies are needed to account for potential confounding factors.

Key words: Helicobacter pylori, gastritis, chronic, peptic ulcer, Helicobacter infections

Introduction

Helicobacteriosis, the infection caused by Helicobacter pylori, is recognized as the most prevalent human infection worldwide (Shaaban et al., 2023). Its incidence is notably higher in regions characterized by poor hygiene and low economic status, resulting in higher rates of infection in Africa, South America, and Asia in comparison to Western Europe, North America, and Australia (Tonkic et al., 2012; Hooi et al., 2017; Bashir and Khan, 2023). The prevalence of H. pylori infection is influenced by various factors, including living conditions, dietary habits, and geographic location (Sjomina et al., 2018; Al-Mashhadany, 2020). Infected individuals serve as the primary reservoir for H. pylori, facilitating transmission of the infection to others since most infections are asymptomatic (Denic et al., 2020).

The belief that the human stomach was sterile and unsuitable for microorganisms due to its highly acidic conditions changed decades ago. In 1982, H. pylori bacteria were successfully isolated from gastric biopsies by Marshall and Warren, demonstrating their ability to survive in patients with active chronic gastritis, gastric ulcers, or duodenal ulcers (Elbehiry et al., 2023). H. pylori is now classified by the World Health Organization as a group 1 carcinogen and the causative agent of gastric diseases, including gastritis, ulcers, and gastric cancer (Al-Mashhadany et al.,2018; Denic et al., 2020). It is estimated that approximately half of the global population is infected with H. pylori (Denic et al., 2020; Qasim et al., 2023). New H. pylori infections are believed to result from direct human-to-human transmission, which can occur through oral-oral or fecal-oral routes or both. The presence of bacteria has been detected in various bodily fluids, including stool, saliva, vomitus, and gastric refluxate (Mégraud et al., 2007). Typically, the infection occurs during early childhood and is often transmitted by close family members. Premastication of food by a parent has been suggested as a potential risk factor for H. pylori transmission; however, the certainty of this association remains uncertain, and further evidence is needed. Additionally, a higher prevalence of H. pylori has been positively associated with crowding during childhood, both within and outside the family (Almashhadany et al., 2023). Other potential sources of transmission include contaminated water and food (Aziz et al., 2015).

There are several methods for detecting H. pylori in human clinical specimens (Sabbagh et al., 2018; Godbole et al., 2020). These methods can be broadly categorized as invasive or non-invasive. Invasive methods require endoscopy with biopsies of gastric tissues for histology, culture, and rapid urease testing. Non-invasive tests include the urea breath test and fecal antigen tests, which are quick diagnostic procedures with comparable accuracy to biopsy-based techniques and are the methods of choice in the test and treatment setting (Sabbagh et al., 2018). Serological methods to detect immunoglobulin G antibodies to H. pylori can also show as high accuracy as other non-invasive and invasive biopsies but do not differentiate between current or past H. pylori infections (Cardos et al., 2022). Polymerase chain reaction (PCR) is an emerging option that can be categorized as both invasive and non-invasive tests. The PCR approach is beneficial for detecting H. pylori from gastric biopsies without the need for cultures (Sohrabi et al., 2021).

Due to its fastidious growth requirements and ability to enter a viable but nonculturable state under stressful conditions, the detection of H. pylori in food and water can be challenging. Consequently, molecular methods that rely on the identification of H. pylori-specific DNA or RNA sequences are commonly employed to assess the presence of H. pylori in food and water samples. Numerous epidemiological studies have highlighted drinking water sources as a significant risk factor for H. pylori infection (Quaglia et al., 2008; Al-Mashhadany and Mayass, 2017; Durazzo et al., 2021).

H. pylori has been detected in drinking water, seawater, vegetables, and foods of animal origin. It can survive in complex foodstuffs such as milk, vegetables, and ready-to-eat foods. In general, the survival of H. pylori is better in filtered water than in auto-claved water. It has been reported that H. pylori can survive several days in water at 5°C, supporting the observation that H. pylori survive better at 5°C than at higher temperatures (Quaglia and Dambrosio, 2018). Certainly, detecting H. pylori in food and water is crucial for preventing its transmission and potential health risks. There are several diagnostic methods available for detecting H. pylori infections, all of which can be broadly classified as either invasive or non-invasive. Invasive methods necessitate upper endoscopy and the analysis of gastric biopsy samples. If the patient necessitates upper endoscopy, various diagnostic approaches can be employed to diagnose H. pylori infection, including histological analysis, rapid urease testing, molecular methods, or culture. Non-invasive testing options encompass immunological methods such as serology and stool antigen testing, as well as the 13C-urea breath test and molecular methods. Preferential consideration should be given to non-invasive diagnostic techniques (Bessède et al., 2017; Bordin et al., 2021). This review aimed to address H. pylori infection in terms of its epidemiology and potential transmission by food and water. The preventive measures at the personal and community levels were discussed.

Taxonomy and pathogenic Helicobacter species

The Helicobacteraceae family consists of gram-negative, spiral-shaped bacteria known for their helical or curved morphology. The family Helicobacteraceae, which lies within the Epsilon subdivision of the Proteobacteria, consists of five Helicobacter genera: Sulfuricurvum, Sulfurimonas, Sulfurovum, Thiovulum, and Wolinella (Mitchell et al., 2014; Garrity et al., 2015). This family is dominated by the Helicobacter genus, which currently consists of 33 validated named species and several candidates and unclassified organisms (Mitchell et al., 2014). Helicobacter is the representative genus and H. pylori is the type species of this family (Taillieu et al., 2022). Species belonging to Helicobacter and Wolinella are commonly associated with animal and/or human hosts and typically colonize the oral and gastrointestinal tracts (Varon et al., 2022).

The Helicobacter genus is commonly classified into two groups: gastric and enterohepatic (non-gastric) species (Romo-Gonzalez et al., 2022). These groups exhibit a high level of organ specificity, with gastric helicobacters typically unable to colonize the intestine or liver, and vice versa. Gastric species are known to colonize the stomachs of humans and a wide range of animals, including cattle, sheep, goats, dogs, cats, cheetahs, rhesus monkeys, ferrets, whales, and dolphins (On et al., 2015). This group includes H. pylori, H. felis, H. mustelae, H. acinonychis, and H. heilmannii. H. acinonychis is associated with chronic gastritis and ulceration in big cats, such as cheetahs and tigers, and is a common cause of death in cheetahs (On et al., 2015). In humans, H. heilmannii infection can lead to gastritis and dyspeptic symptoms, and in rare cases, even ulcer disease. However, the inflammation is typically less severe compared to individuals infected with H. pylori (Husnik et al., 2022).

Enterohepatic species of the Helicobacter genus colonize the lower gastrointestinal tract, including the biliary tree, in humans and other mammals. These persistent infections are associated with chronic inflammation and hyperproliferation of epithelial cells, which can lead to neoplastic and hepatobiliary diseases in humans (Verhoef et al., 2003). There are nineteen named non-gastric Helicobacter species that colonize the lower intestinal tract of animals, many of which can also colonize humans. These species include H. canadensis, H. rodentium, H. pullorum, H. fennelliae, H. trogontum, H. muridarum, H. hepaticus, H. canis, H. bilis, H. rappini, H. cinaedi, H. westmeadii, H. pametensis, H. winghamensis, H. mesocricatorum, H. aurati, H. typhlonius, H. cholecystus, and H. trogontum (On et al., 2015; Romo-Gonzalez et al., 2022). These Helicobacter species naturally colonize the intestinal crypts and are often associated with diarrhea. They can also cause bacteremia and systemic disease, including cholecystitis, colonization of the biliary tract, hepatitis, and in some cases, hepatic cancer. Eight of these enterohepatic Helicobacter species (H. canis, H. pullorum, H. cinaedi, H. fennelliae, H. canadensis, H. winghamensis, H. westmeadii, and H. rappini) have been isolated from humans with diarrhea and/or bacteremia (Garrity et al., 2015; On et al., 2015; Husnik et al., 2022).

Bacteriology of Helicobacter pylori

H. pylori is a microaerophilic, gram-negative bacterium with an average length ranging from 0.5 to 5 μm and a tuft of 5 to 7 polar sheathed flagella, each approximately 3 μm in length. The helical or curved rod shape of H. pylori enables it to move through the mucus lining of the stomach. The ability of H. pylori to live, swim, grow, and move within the acidic environment of the stomach is facilitated by its shape, size, and flagellation (On et al., 2015).

The complex cell wall structure of H. pylori, similar to that of other gram-negative bacteria, comprises an outer membrane, a thin peptidoglycan layer, and an inner cytoplasmic membrane. The presence of a capsule, a slimy layer outside the cell wall, may or may not be observed in H. pylori. Under specific circumstances, such as exposure to antibiotics or harsh environments, a morphological transformation from the characteristic spiral shape to coccoid forms can occur in H. pylori. It is noteworthy that the morphology of H. pylori is subject to variation and can adapt to its surroundings and growth conditions. Additionally, the species exhibits a high degree of diversity, leading to potential differences in morphology among various strains (On et al., 2015; Al-Mashhadany, 2018).

Epidemiology

In 2015, a total of 4.4 billion cases of H. pylori were estimated via a meta-analysis of epidemiological surveys (Hooi et al., 2017; Bashir and Khan, 2023). A higher prevalence of H. pylori is observed in unsanitary and economically poor regions, particularly in Asia, Africa, and South America, compared to regions such as Australia, North America, and Western Europe (Sjomina et al., 2018; Al-Mashhadany, 2020; Almashhadany et al., 2022; Balas et al., 2022). It is worth noting that a significant proportion of infected individuals remain asymptomatic, serving as potential carriers and unknowingly transmitting the infection to others (Denic et al., 2020).

The geographical variation of H. pylori frequency has been documented with over 80% of the population in certain developing countries being positive for H. pylori, while the prevalence in industrialized countries generally remains below 40% (Sjomina et al., 2018). Moreover, the prevalence of H. pylori tends to be lower in children and adolescents compared to adults and elderly individuals (Al-Moayad, 2012). In terms of regional distribution, developing countries exhibit an occurrence below 50%, whereas developed countries have a prevalence rate of around 35% (Zamani et al., 2018). Specifically, the prevalence of H. pylori is 63.5% in India, 81.0% in Pakistan, 77.2% in Western Asia, and 70.1% in Africa (Khoder et al., 2019). In contrast, the frequency of H. pylori in North America is approximately 20-30%, while in the United States of America, it ranges from 30-40% (Willems et al., 2020).

The relationship between H. pylori infection and certain living habits remains uncertain. However, studies have shown that the infection rate of H. pylori is lower in the elderly who have higher education, engage in significant mental work, or reside in more economically developed regions (Nurgalieva et al., 2002; Matsuhisa et al., 2015). In an early epidemiological survey conducted in Beijing, China, the prevalence of H. pylori infection among the elderly was reported to be 83.4% (Zhang et al., 2005). However, a recent investigation found a lower rate of 46.5%, with males exhibiting a higher infection rate than females (51.8% versus 42.5%), and an increase in infection rate with age (Zhu et al., 2020). Previous studies have also examined the infection rate of H. pylori in the elderly with peptic ulcer disease. These studies reported infection rates ranging from 58% to 78%. However, it is worth noting that only 40% to 56% of these individuals were tested for H. pylori infection, and among those with a positive test, only 50% to 73% received antibiotic treatment (Pilotto and Franceschi, 2014). Furthermore, there is evidence suggesting a decreasing trend in H. pylori infection rates among both adults and children in certain countries (Bureš et al., 2012; Tonkic et al., 2012).

Transmission of Helicobacter pylori

The transmission dynamics of H. pyloriare crucial to understand for effective prevention and control strategies. The precise mechanism of transmission remains poorly understood. It is postulated that the bacterium can be transmitted either directly from person to person, as the primary route, or indirectly from the environment to individuals (Zamani et al., 2018; Almashhadany et al., 2022). Person-to-person transmission is considered to be the primary mode of transmission, particularly in developed countries. However, in developing countries with inadequate sanitation, transmission through contaminated food and water is likely to occur, leading to a more rapid spread of H. pylori(Vale and Vítor, 2010; Zamani et al., 2017; Al Mashhadany and Mayass, 2018). Not all individuals exposed to H. pyloriwill manifest symptoms or experience complications. Other factors, such as the host immune response, individual susceptibility, and bacterial strain, significantly influence the outcome of the infection (Sukri et al., 2020). However, Figure 1 illustrates the transmission routes of H. pylorito humans.

Figure 1.

Figure 1.

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Transmission of Helicobacter pylori. Transmission routes with direct evidence are drawn in black arrows, while gray arrows indicate suspected transmission as evidenced only by the detection of bacteria or its DNA in non-human samples. Oral-oral transmission can occur during the sharing of food utensils or between mothers and their newborns.

Oral-oral transmission

H. pylori is primarily considered a gastric organism; however, research has indicated that infected individuals may harbor H. pylori in their mouth and saliva, either on a permanent or transient basis. The transmission of H. pylori through oral-oral routes can occur when the bacterium is directly transmitted to another individual via activities such as kissing, sharing utensils, or engaging in close personal contact (Wang et al., 2019). The oral cavity has been identified as a reservoir for microorganisms, including H. pylori, as demonstrated by Miyabayashi et al. (2000), who found that the presence of H. pylori in the oral cavity constitutes a risk factor for recurrent gastric infection. Additionally, it has been recommended that adjunctive periodontal treatment enhances the efficacy of H. pylori therapy and reduces the recurrence of gastric infection (Tongtawee et al., 2019).

Gastro-oral and fecal transmission

The transmission of H. pylori from the gastrointestinal tract to the oral cavity is referred to as the gastro-oral route. This route is facilitated by the presence of the bacterium in the stomach and duodenum, and through mechanisms such as regurgitation or vomiting, the bacteria can be transferred to the mouth and potentially disseminated to others through oral contact. Both oral-oral and gastro-oral routes play a role in the transmission of H. pylori and significantly contribute to its prevalence among individuals (Zamani et al., 2017; Mezmale et al., 2020).

The presence of H. pylori in the feces of infected individuals has been documented (Tonkic et al., 2012; Godbole et al., 2020). Transmission through the fecal-oral route can occur when contaminated fingers come into contact with shared food or food utensils. Such contamination is often associated with poor sanitation or improper food handling practices, particularly in regions where inadequate hygiene practices are prevalent (Kayali et al., 2018).

Sexual routes

It has been indicated by several studies that non-gut organs such as the vagina, ears, and nasopharyngeal sinus cavities can be inhabited by H. pylori (Eslick, 2000; Dimitriadi, 2014; Shishegar et al., 2015;). The transmission of H. pylori through sexual contact has been observed, with the vagina potentially serving as a reservoir for the bacterium, either permanently or temporarily (Eslick, 2000; Dimitriadi, 2014). Studies have demonstrated that when one partner in a sexual relationship is infected with H. pylori, the non-infected partner faces an increased risk of acquiring the infection. H. pylori can colonize yeast in the vagina and has been associated with the formation of biofilms, which can contribute to treatment-resistant bacterial vaginosis (Sánchez-Alonzo et al., 2021). Vaginal yeasts are more favorable to H. pylori colonization compared to oral yeasts, which facilitate transmission to infants during vaginal delivery.

Risk factors

Several risk factors contribute to an increased likelihood of acquiring H. pylori infection (Balas et al., 2022; Bashir and Khan, 2023). It is noteworthy that many of these risk factors can be avoided through the acquisition of adequate knowledge and the implementation of appropriate practices. The general community appears to lack adequate knowledge regarding H. pylori, particularly regarding its mode of transmission (Hafiz et al., 2021). However, a study conducted by Alaridah et al. (2023) revealed the presence of misconceptions and highlighted the need for further expansion and support in knowledge dissemination concerning H. pylori.

Personal hygiene and socioeconomic status

The probability of acquiring H. pylori infection can be increased by poor hygiene practices, including inadequate hand-washing, particularly after using the restroom or before eating (Che et al., 2023). A higher risk of H. pylori infection has been associated with lower socioeconomic status, potentially attributable to factors such as inadequate sanitation, limited healthcare access, and suboptimal living conditions (Balas et al., 2022; Meliţ et al., 2022).

Living in crowded or unsanitary conditions

In regions characterized by overcrowded living conditions or limited access to hygienic water and proper sanitation, the prevalence of H. pylori infection is further amplified. These findings underscore the importance of the fecal-oral route and the influence of crowded living conditions in facilitating the transmission of H. pylori (Bashir and Khan, 2023). Consequently, the implementation of preventive protocols should prioritize the dissemination of instructions about sanitation practices, especially in densely populated areas (Che et al., 2023).

Close contact with diseased people

Transmission of H. pylori infection within families is facilitated by intrafamilial frequent contacts, particularly in cases of repeated exposure to the same infected individuals (Khoder et al., 2019). The bacteria are known to be transmitted through person-toperson contact, with childhood being the typical transmission period. Acquisition of this infection predominantly occurs during infancy or childhood, with close person-to-person contact serving as the primary route of transmission (Balas et al., 2022). Notably, the prevalence of H. pylori within the same household increases progressively with age, ranging from 10% to 30% in adolescents to 40% to 60% in the elderly (Kayali et al., 2018).

Consumption of contaminated food or water

While direct evidence is insufficient to definitively establish the role of food products in the environmental transmission of H. pylori, numerous studies have successfully isolated H. pylori or identified its DNA in samples of food and water. Consequently, the consumption of improperly prepared food contaminated with H. pylori can potentially result in infection. Additionally, regions characterized by limited access to clean water may be associated with an elevated risk of H. pylori infection (Bashir and Khan, 2023; Che et al., 2023). The bacterium Helicobacter pylori has been studied as a potential foodborne pathogen, particularly in relation to its spread through contaminated meat products (Akhlaghi et al., 2024). While researchers have explored this possibility, the degree to which H. pylori transmission via meat contributes to overall infection rates remains an area of ongoing investigation.

Age

In developing countries, the acquisition of H. pylori infection at a younger age is attributed to close contact with infected individuals, including family members, and unless treated, it typically persists as a lifelong infection in most individuals. The infection is commonly acquired by children before reaching 10 years of age (Balas et al., 2022). Conversely, in developed countries, the prevalence of infection among children is lower. However, the infection rate increases with age, and by the time individuals reach 60 years of age, approximately 50% of the population is infected (Venero-Fernández et al., 2020).

Smoking

A significant association between cigarette smoking and residing in the same household as H. pylori-positive families was observed in H. pylori positivity (Monno et al., 2019). Additionally, Itskoviz et al. (2017) reported that smoking was found to significantly elevate the likelihood of ineffective first-line treatment for H. pylori infection.

Role of food and water in transmission

The role of food in the transmission of H. pylori has been investigated, with milk, meat, and vegetables being the most commonly analyzed food products (Vale and Vítor, 2010). Among these, milk products have received the most attention, likely because H. pylori infection is primarily acquired during childhood when milk is a common dietary component (Vale and Vítor, 2010). However, individuals who consume raw vegetables have been found to have a higher likelihood of acquiring H. pylori (Zamani et al., 2017). This association between H. pylori infection and the consumption of raw vegetables indirectly suggests that the bacterium may be present in the water used for irrigating these vegetables (Aziz et al., 2015; Zamani et al., 2017). It is important to acknowledge the challenges in determining the exact modes of transmission, as H. pylori is difficult to culture from environmental samples, and association does not necessarily imply causation (Almashhadany et al., 2022).

Previous studies have examined the survival of H. pylori by testing various samples such as water, meat, seafood, vegetables, and milk (Guner et al., 2011; Quaglia et al., 2007; Quaglia et al., 2020). For example, Quaglia et al. (2007) conducted a study where artificially contaminated pasteurized and ultrahigh temperature (UHT) milk samples were stored aerobically at 4°C. The results showed that the bacterial load progressively decreased, with a median survival of 9 days in pasteurized milk and 12 days in UHT milk. The initial inoculum was approximately 105 and 106 CFU/mL for pasteurized and UHT milk, respectively. In contrast, it was found that H. pylori did not grow at refrigeration temperature on vegetable substrates but remained viable and culturable for up to 5 days at 20°C (Pina-Pérez et al., 2018).

Consumption of contaminated food

H. pylori infections can potentially originate from food sources (Vale and Vítor, 2010). However, the fastidious growth requirements of this species, coupled with its ability to enter a viable but nonculturable state under stressful conditions, pose challenges in isolating H. pylori from various food samples. Consequently, molecular methods that rely on the detection of H. pylori-specific DNA or RNA sequences are frequently employed to assess the presence of H. pylori in food (Meng et al., 2008; Quaglia et al., 2008; Almashhadany et al., 2022). H. pylori was found in human and animal samples. Additionally, glmM was discovered in both milk and human samples. The findings by Shaaban et al. (2023) imply that domestic and agricultural animals may transfer H. pylori infection to people.

Drinking of contaminated water

A positive association between the prevalence of H. pylori infection and untreated or fecally contaminated drinking water has been reported in several epidemiological studies (Mezmale et al., 2020). Families utilizing non-flush toilets, outdoor toilets, outdoor water taps, and river water have been found to have a higher prevalence of H. pylori infection. These findings suggest that an increased frequency of microorganisms is positively associated with poor hygiene. The survival of H. pylori in water can extend for several weeks, with factors such as temperature, salt content, and nutrient levels influencing its persistence (Aziz et al., 2015).

Using contaminated kitchen instruments

Sharing plates, glasses, and other utensils with an individual infected with H. pylori can potentially lead to transmission. The bacteria can survive on these surfaces and be transferred to another individual if proper cleaning and disinfection are not followed (Mezmale et al., 2020; She et al., 2023) (Table 1) (Dore et al., 1999; Stevenson et al., 2000; Dore et al., 2001; Fujimura et al., 2002; Turutoglu and Mudul, 2002; Quaglia et al., 2008; Meng et al., 2008; Angelidis et al., 2011; Safaei et al., 2011; Rahimi and Kheirabadi, 2012; Momtaz et al., 2014; Mousavi et al., 2014; Atapoor et al., 2014; Yahaghi et al., 2014; Esmaeiligoudarzi et al., 2015; Talaei et al., 2015; Bianchini et al., 2015; Osman et al., 2015; Abdel-Latif et al., 2016; Saeidi and Sheikhshahrokh, 2016; Hemmatinezhad et al., 2016; Ghorbani et al., 2016; Eldairouty et al., 2016; Gilani et al., 2017; Al-Mashhadany and Mayass, 2017; Khaji et al., 2017; Talimkhani and Mashak, 2017; Ranjbar et al., 2018; Hamada et al., 2018; Elhariri et al., 2018; Guessoum et al., 2018; Mashak et al., 2020; Kareem and Maaly, 2021; Elrais et al., 2022; Al-Shrief and Thabet, 2022; Almashhadany et al., 2022; Asadi et al., 2023; Shaaban et al., 2023; Piri-Gharaghie et al., 2023).

Signs and symptoms of helicobacteriosis

Several individuals infected with H. pylori may not show any symptoms, but the infection can lead to different gastrointestinal diseases and complications (Pina Dore et al., 2022). It is important to note that these symptoms can also be associated with other gastrointestinal conditions, so a proper diagnosis by a healthcare professional is essential.

H. pylori infection is primarily associated with abdominal pain, which is often described as a burning or distressing sensation (Marzio et al., 2003). The pain is typically felt in the upper abdomen and worsens when fasting, with nocturnal episodes being common. Nausea is a common symptom experienced by certain individuals, and in some cases, it may progress to vomiting with the presence of coffee ground-like or blood-tinged material. The infection can also lead to abdominal distension, bloating, and frequent burping owing to increased gas production. Even without visible distention, individuals may experience a subjective feeling of a bloated stomach. The black, tarry stool is a characteristic sign of H. pylori gastritis. Some individuals may also experience heartburn and acid reflux, with a burning sensation in the chest, which can be chronic or intermittent (Ceylan et al., 2007; Al Mashhadany and Mayass, 2018; Mărginean et al., 2022).

H. pylori infection has been linked to halitosis, a malodor characterized by a foul odor due to elevated levels of hydrogen sulfide due to the putrefactive action of H. pylori. The infection may also increase the risk of erosive changes in the stomach, potentially leading to the production of volatile sulfur compounds (Pina Dore et al., 2022). In cases where H. pylori infection causes stomach bleeding, the presence of black, tarry stools may indicate the presence of blood (Bashir and Khan, 2023).

Chronic H. pylori infection can lead to continuous stomach bleeding, potentially causing iron deficiency anemia. It may also result in decreased appetite due to discomfort and chronic inflammation, which can contribute to weight loss. The infection can cause a general feeling of weakness and fatigue. Patients may also experience fatigue and a sensation of fullness even after eating a small amount of food (Pina Dore et al., 2022).

Prevention and control of helicobacteriosis

Prevention of H. pylori infection can be achieved through various techniques. The most effective measure is to avoid the risk factors associated with H. pylori infection and practice good hygiene. However, it is important to note that these preventive measures may help reduce the risk of infection, but they are not guaranteed to be completely effective.

Personal hygiene

Practicing good sanitation, including regular handwashing, is crucial in preventing the transmission of H. pylori. Since bacteria can be spread through contaminated hands, it is important to wash hands thoroughly with soap and water after using the restroom, before eating, and after contact with potentially contaminated surfaces (Mezmale et al., 2020). When traveling, especially to areas with lower hygiene standards, it is important to be extra cautious about food safety, handwashing, and avoiding contaminated water sources to reduce the risk of H. pylori infection and other infectious diseases (Yin et al., 2009; Almashhadany, 2019, 2020, 2021).

Table 1.

Studies that detected Helicobacter pylori in different food types.

Year Country Detection method Food type Reference
1999 Italy PCR Sheep milk Dore et al., 1999
2000 USA Culture Retail beef Stevenson et al., 2000
2001 Italy Culture & PCR Sheep milk and gastric tissue Dore et al., 2001
2002 Japan PCR, culture, EM Raw and pasteurized cow milk Fujimura et al., 2002
Turkey Culture Raw sheep milk Turutoglu and Mudul, 2002
2008 Italy Nested-PCR Raw goat, sheep, and cow milk Quaglia et al., 2008
USA Multiplex PCR Raw chicken and ready-to-eat raw tuna Meng et al., 2008
2011 Greece FISH Raw cow milk Angelidis et al., 2011
Iran ELISA & PCR. Cow’s milk Safaei et al., 2011
2012 Iran PCR Raw milk from cows, sheep, goats, buffalo and camel Rahimi and Kheirabadi, 2012
2014 Iran PCR Rumen (cow, sheep, and goat) in slaughterhouse Momtaz et al., 2014
Iran Culture & PCR Milk and traditional dairy products Mousavi et al., 2014
Iran Culture & PCR Vegetables and salad Atapoor et al., 2014
Iran Culture & PCR Washed and unwashed vegetables Yahaghi et al., 2014
2015 Iran Culture & PCR Milk and dairy products Esmaeiligoudarzi et al., 2015
Iran PCR Raw cow, sheep, goat, buffalo, and, camel milk Talaei et al., 2015
Italy Culture &PCR Bulk tank milk of dairy cattle Bianchini et al., 2015
Sudan Culture &PCR Raw cow milk Osman et al., 2015
2016 Egypt PCR Cow’s milk Abdel-Latif et al., 2016
Iran Culture & PCR Raw cow, sheep, goat, buffalo, and camel milk and meats Saeidi and Sheikhshahrokh, 2016
Iran Culture & PCR Ready-to-eat food Hemmatinezhad et al., 2016
Iran PCR Fish, ham, chicken, vegetable, meat sandwiches, minced meat Ghorbani et al., 2016
Egypt Culture Raw meat, raw poultry meat, and luncheon meat samples, Eldairouty et al., 2016
2017 Iran Culture & PCR Hamburger and minced meat Gilani et al., 2017
Yemen Culture Red meat, poultry meat, salad Al-Mashhadany and Mayass, 2017
Iran PCR Milk and dairy samples Khaji et al., 2017
Iran Culture & PCR Meat, milk, and vegetables Talimkhani and Mashak, 2017
2018 Iran PCR Raw milk Ranjbar et al., 2018
Egypt PCR Chicken samples Hamada et al., 2018
Egypt PCR Cows, buffaloes, and sheep milk Elhariri et al., 2018
Algeria ELISA & PCR Milk Guessoum et al., 2018
2020 Iran PCR Raw meat Mashak et al., 2020
2021 Iraq PCR Meat samples Kareem and Maaly, 2021
2022 Egypt PCR Chicken meat, swabs Elrais et al., 2022
Egypt Culture & PCR Cows’ milk Al-Shrief and Thabet, 2022
Yemen Culture Chicken meat Almashhadany et al., 2022
2023 Iran PCR Raw poultry meat Asadi et al., 2023
Iran PCR Animal milk samples Shaaban et al., 2023
Iran Culture & PCR Raw poultry meat Piri-Gharaghie et al., 2023
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EM, electron microscopy, FISH, fluorescence in situ hybridization; PCR, polymerase chain reaction; ELISA, enzyme-linked immunosorbent assay.

Water and food safety

Practicing good water and food safety techniques is crucial. H. pylori can be transmitted through contaminated water and food if they are not prepared and handled properly (She et al., 2023). To prevent H. pylori infection, it is important to ensure that drinking water comes from a reliable source and is safe for consumption. Moreover, consuming properly cooked food and avoiding the consumption of raw or undercooked shellfish and meat also reduces the likelihood of infection. It is also important to wash vegetables and fruits thoroughly, as they can be a potential source of H. pylori infection. Additionally, it is worth noting that post-processed contaminated milk may have a higher risk of transmitting H. pylori due to its ability to survive for up to a week (Quaglia et al., 2007).

Avoiding close contact with infected individuals

To prevent the transmission of the infection, it is imperative to exercise caution and refrain from close contact with individuals within one’s household or immediate social circle who have been diagnosed with H. pylori. This is because H. pylori can be transmitted through saliva and vomit. Consequently, it is advisable to abstain from sharing personal items, such as utensils, drinking glasses, and other belongings, with individuals who may be infected or have a history of H. pylori infection (Sjomina et al., 2018; Mezmale et al., 2020).

Awareness of the infection

Acquiring knowledge regarding the risk factors, symptoms, and modes of transmission of H. pylori is crucial for individuals to safeguard themselves and make informed decisions. Patient education serves as a cost-effective, safe, and convenient approach in this regard. In a recent study, it was suggested that implementing enhanced educational interventions led to positive outcomes in terms of both the eradication rate of H. pylori and the adherence of infected patients to treatment regimens (Zha et al., 2022). Zhou et al. (2022) observed that efforts to address risk factors at not only the individual level but also within the family and school environments were crucial in advancing knowledge, attitudes, and practices among children, family members, and teachers, thereby fostering a healthier society. Consequently, such interventions would serve as valuable complements to clinical treatment programs.

Maintaining a clean environment

The preservation of a clean environment is deemed necessary for the promotion of overall health and serves as a fundamental measure in preventing the transmission of various infectious pathogens, including H. pylori. Nevertheless, the prevention of H. pylori infection can be achieved through the modification of lifestyles and behaviors, as well as the enhancement of environmental sanitation through hygiene interventions targeted towards vulnerable populations (Sjomina et al., 2018; Mezmale et al., 2020).

Rational administration of medications

When taking non-steroidal anti-inflammatory drugs (NSAIDs), it is vital to be cautious and utilize these drugs at the lowest effective dosage and for the shortest duration possible. This is due to the potential of NSAIDs to induce irritation of the stomach lining and increase the likelihood of peptic ulcer progression, thereby facilitating H. pylori infection (Alexander et al., 2021). Moreover, the unnecessary and excessive use of antibiotics has the potential to disrupt the normal balance of gut flora, potentially encouraging the proliferation of H. pylori. Therefore, it is advised to only take antibiotics when necessary.

Quitting smoking and alcohol

Smoking can irritate and damage the stomach lining, making it easier for H. pylori to colonize and cause complications, so the improvement of stomach lining health by quitting smoking allows the stomach lining to heal and decreases the risk of additional problems (Wu et al., 2020). Furthermore, excessive alcohol consumption can irritate the stomach lining, necessitating the limitation of alcohol intake to promote optimal digestive health.

Role of probiotics in preventing Helicobacter pylori

Probiotics are live microbes that can provide health benefits when consumed in specific quantities. They are known for their positive effects on gut health and have been studied for their potential role in managing several gastrointestinal disorders, including H. pylori infection. Some studies suggest that certain probiotics may help inhibit the growth of H. pylori and promote a healthy balance of gut microbiota (Zhang et al., 2015). Other studies have investigated the potential benefits of using probiotics in combination with standard antibiotic treatments for H. pylori eradication. However, research on the role of probiotics in treating or preventing H. pylori infection is still ongoing (Keikha and Karbalaei, 2021).

Regular screening and treatment

Screening tests are of paramount importance, especially in cases where a family history of H. pylori infection or when gastrointestinal symptoms are suspected. It is worth emphasizing that early detection plays a pivotal role in facilitating prompt treatment. However, cross-sectional studies revealed that only a limited number of participants had undergone a screening test for H. pylori, with the majority possessing minimal knowledge regarding this infection (Wang et al., 2019; Teng et al., 2021). Lastly, studies have demonstrated that H. pylori vaccines have proven ineffective in reducing microbial load and have only provided limited immunity (Stubljar et al., 2018). Vaccination holds promise as a preventive measure against H. pylori infection on a global scale. However, previous attempts to develop an H. pylori vaccine have yielded disappointing results (Li et al., 2023). While certain vaccine candidates have shown potential for prophylactic use, none have demonstrated clinical applicability (Zhang et al., 2022).

Conclusions

Concerns about H. pylori are widespread due to its problematic nature as a pathogen that infects more than the world population. The stomach lining is commonly infected by H. pylori, which can cause gastritis, peptic ulcers, and other gastrointestinal manifestations. Person-to-person transmission is thought to occur through oral-oral, fecal-oral, gastric-oral, or sexual routes. Two routes of transmission exist: i) direct routes (oral-oral, gastro-oral, fecal-oral, and sexual routes); and ii) indirect routes (drinking of contaminated water, consumption of contaminated food, and using contaminated utensils). Although H. pylori is unlikely to grow in food, it may survive in a viable but nonculturable form. This might lead to an underestimation of its prevalence in food and water. It is not clear how the conversion from a viable nonculturable state to a viable state occurs. This remains to be resolved, particularly since it is not known whether coccoid forms of H. pylori can infect humans. Molecular-typing techniques such as ribotyping or restriction fragment length polymorphism are expected to help trace the route of transmission in future epidemiological studies of transmission that should be longitudinal and adequately controlled for the likely confounders of the association between risk factors and H. pylori infection.

Funding Statement

Funding: none.

Availability of data and materials

Available from the corresponding author.

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