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Ansari, S.;  Yamaoka, Y. Animal Models and Helicobacter pylori Infection. Encyclopedia. Available online: https://encyclopedia.pub/entry/25083 (accessed on 18 May 2024).
Ansari S,  Yamaoka Y. Animal Models and Helicobacter pylori Infection. Encyclopedia. Available at: https://encyclopedia.pub/entry/25083. Accessed May 18, 2024.
Ansari, Shamshul, Yoshio Yamaoka. "Animal Models and Helicobacter pylori Infection" Encyclopedia, https://encyclopedia.pub/entry/25083 (accessed May 18, 2024).
Ansari, S., & Yamaoka, Y. (2022, July 13). Animal Models and Helicobacter pylori Infection. In Encyclopedia. https://encyclopedia.pub/entry/25083
Ansari, Shamshul and Yoshio Yamaoka. "Animal Models and Helicobacter pylori Infection." Encyclopedia. Web. 13 July, 2022.
Animal Models and Helicobacter pylori Infection
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This entry is adapted from the peer-reviewed paper 10.3390/jcm11113141

Helicobacter pylori colonize the gastric mucosa of at least half of the world’s population. Persistent infection is associated with the development of gastritis, peptic ulcer disease, and an increased risk of gastric cancer and gastric-mucosa-associated lymphoid tissue (MALT) lymphoma. 

Helicobacter pylori infection animal model Mongolian gerbils

1. Animal Models

Helicobacter pylori (H. pylori) is well adapted for colonizing the human stomach, but the natural history of infection in animals is unknown, and it does not easily infect the gastric mucosa of animals. This is because of the complex interaction of H. pylori with the human gastric epithelium, which takes decades to develop into gastric cancer. It is difficult to determine the pathogenesis of H. pylori infection and the immune response generated by this pathogen. Therefore, considerable efforts are being made to identify suitable animal models to understand the natural history of H. pylori infection and its immune response. It has been suggested that animals, including dogs, cats, pigs, monkeys, mice, Mongolian gerbils, and guinea pigs, could be potential habitats for H. pylori [1][2]. H. pylori does not easily infect the gastric mucosa of other animals, and in the search for more suitable animal models, experimental infection studies have been widely conducted in Mongolian gerbils, mice, guinea pigs, and rhesus monkeys.
In the human stomach, H. pylori mostly colonize the antrum, a pyloric part of the stomach found throughout the gastric mucosa from the pylorus to the cardia [3]. The gastric topological locations of most animal models are also preferentially colonized by H. pylori [4][5][6][7], emphasizing their widespread use for understanding the role of several bacterial virulence factors, host constituents, and environmental factors involved in H. pylori-mediated gastric pathogenicity.
Mongolian gerbils are small rodents that develop similar infection symptoms, such as appetite and weight loss, and recapitulate many features of H. pylori-induced gastric colonization, inflammation, ulceration, and carcinogenesis, as seen in humans [8][9][10][11][12]. Several other studies demonstrated the development of H. pylori-induced gastric ulcers, duodenal ulcers, and IM following an experimental bacterial challenge in Mongolian gerbils [13][14][15][16][17]. Therefore, Mongolian gerbils work as a suitable animal model and are the most commonly used animal model for establishing H. pylori infection. They also represent an efficient and cost-effective rodent model. Colonization of the gastric mucosa by H. pylori produces a similar mixed inflammatory infiltrate in the lamina propria as elicited in human diseases consisting of neutrophils and mononuclear leukocytes [18][19]. Over time, severe inflammation in gerbils causes the loss of parietal and chief cells, usually accompanied by the hyperplasia of mucous neck cells, sometimes referred to as mucous metaplasia, and the base of fundic glands may show features of spasmolytic polypeptide-expressing metaplasia (SPEM), also referred to as pseudopyloric metaplasia [18].
A mouse model infected with the H. pylori Sydney strain (HpSS1) displayed CG and gastric atrophy [20]. However, wild-type mouse models, such as C57BL/6 [21], BALB/c [22], and C3H [23], infected with H. pylori commonly develop mild gastritis or slow progressing diseases and provide less information about H. pylori pathogenicity [24][25][26]. Infecting mice models with H. pylori and H. felis resulted in lymphocytic gastritis without progression to severe pathologies, such as peptic ulcers or gastric cancer [7][27][28]. Moreover, the architecture of the murine stomach differs from that of the human stomach and lacks the components necessary for the development of severe gastric pathologies. Furthermore, the murine stomach may contain other bacteria that may influence the outcome of H. pylori infection [7][27][28]. These disadvantages limit the use of wild-type mouse models for experimental H. pylori infections. Therefore, several knockout or transgenic mouse models, such as insulin-gastrin (INS-GAS) [29], interferon gamma (IFN-γ), tumor necrosis factor alpha (TNF-α) knockout [30], interleukin (IL)-1 beta (IL-1β) transgenic [31], IL-10 knockout [32], Fas antigen transgenic [33], p27-deficient [34], and cytotoxin-associated gene A (CagA)-transgenic mice [35], are prone to develop gastric cancer when given a high-salt diet or chemical carcinogens of H. pylori infection [28][36]. Rodent animal models have been extensively used as in vivo models for studying the virulence characteristics of H. pylori [37][38].
H. pylori strains have been found to infect nonhuman primates [39][40][41][42][43], and macaques have been used as experimental models for H. pylori infection. However, it is unclear whether macaques carry H. pylori as a natural reservoir in wildlife or whether they are transmitted from humans to macaques after capture. Rhesus macaques are a suitable alternative for animal models that have several advantages over conventional small animal models, such as anatomical and physiological similarities with humans, while socially housed rhesus macaques are naturally infected with H. pylori [40][41]. Moreover, all infected macaques develop CG, and some may develop gastric atrophy [42], the histological precursor of gastric adenocarcinoma [44]. However, studies on non-human primates are time-consuming, tedious, labor-intensive, and extremely expensive, making it difficult to evaluate the degree of H. pylori virulence. Although H. pylori naturally infects the human gastric mucosa, observations indicate that some macaques reared in captivity were naturally infected with this bacterium [38][39][40].
The guinea pig model of H. pylori infection was first described in the late 1990s [5][45]. The guinea pig is a small laboratory animal with a stomach structure similar to that of humans, prone to developing an inflammatory response due to IL-8 secretion by gastric epithelial cells. Similar to the mouse model, the guinea pig models exhibit the ease of husbandry owing to the small animal size. In addition, the guinea pig stomach possesses several features in common with the human stomach, such as the presence of a cylindrical epithelium, maintenance of sterile conditions, the ability to produce IL-8, and the lack of a non-glandular region [46][47][48]. However, the studies are from 2001 to 2003, and there was no openness to metagenomics studies that show the opposite in humans, and I would suppose that in other models as well. Furthermore, like humans, guinea pigs require vitamin C [49].
These animals are considered an optimal model because they possess several similarities with human hormonal and immunologic responses, innate immunity and complement systems, and thymus, bone marrow, and pulmonary physiology. They also demonstrate a delayed type of hypersensitivity, major histocompatibility complex similarity, and possess numerous homologs of human group 1 cluster of differentiation (CD) 1 proteins and IFN-γ expression similarity [50][51][52][53][54][55][56]. These animals are not naturally infected with different Helicobacter spp., making them advantageous as an infection animal model to evaluate the role of several virulence factors in pathogenicity [57].

2. Animal Models to Evaluate Therapeutics against H. pylori Infection and Cancer Progression

In the 1990s, the standard triple-therapy (STT), which consists of protein pump inhibitors (PPI), amoxicillin, clarithromycin, or metronidazole, was developed. Owing to its substantially higher eradication rate, STT is recommended as the first-line eradication therapy for H. pylori [58][59]. It has been found that eradication therapy for H. pylori combined with endoscopic resection of early gastric cancer significantly reduces the development of metachronous gastric cancer [60]. However, in recent times, STT’s efficacy has been decreasing due to the increasing development of antimicrobial resistance, mainly to clarithromycin. Therefore, the increased demand for safe and effective non-antibiotic compounds capable of eliminating H. pylori has become a public concern [61][62][63]. Several studies have been conducted using animal models to evaluate the eradication efficacy of numerous compounds (Table 1). A study utilizing H. pylori infection mouse models evaluated the potent antimicrobial efficacy of H-002119-00-001, a β-caryophyllene. H-002119-00-001 showed potent efficacy in eradicating the bacteria in H. pylori-infected animals compared with the animals treated with antimicrobials [64].
Table 1. Animal models in evaluating therapeutics.
Animal Models Evidence Found References
Mongolian gerbils Hydrogen peroxide eliminates H. pylori and prevents H. pylori infection recurrence [8]
5-ethyl-2-hydroxybenzylamine (EtHOBA) prevents gastric cancer development [65]
Mouse model H-002119-00-001, a β-caryophyllene, shows a potent efficacy in bacterial eradication [64]
The graphitic nanozyme PtCo@Graphene (PtCo@G) exerts antibacterial activity against H. pylori [66]
A mucoadhesive system (Mucolast®) loaded with amoxicillin and clarithromycin improves antibacterial efficacy against H. pylori [67]
The gentamicin-intercalated smectite hybrid (S-GM) proves to be an effective therapeutic agent against H. pylori [68]
Blockage of the Toll-like receptor 4 (TLR4) signaling pathway could play a role in controlling the H. pylori infection [69]
Tilapia piscidin 4 (TP4), a peptide, inhibits the growth of antibiotic-resistant and sensitive H. pylori [70]
Similarly, a study evaluated the role of hydrogen peroxide in eradicating H. pylori using a Mongolian gerbil model. The animal models were orally administered the H. pylori ATCC 43504 strain to successfully establish the infection. Hydrogen peroxide doses of 1 mg/mL, 2 mg/mL, and 4 mg/mL were administered after 14 days, and H. pylori counts were determined. There was no significant difference in the bacterial count between the control and hydrogen peroxide groups, indicating that hydrogen peroxide had eliminated the bacteria. Moreover, the bacterial counts of H. pylori in the triple-drug group were higher than those in the hydrogen peroxide group and lower than those in the H. pylori-infected control group. Overall, the results of the research indicated a higher efficacy of hydrogen peroxide in eliminating and preventing the recurrence of H. pylori than that of triple-drug therapy [8]. Moreover, the study found no toxicity or damage due to hydrogen peroxide in the gastric mucosa. Hydrogen peroxide can disrupt bacterial cell membranes, and the oxygen-enriched environment provided by hydrogen peroxide eradicates and prevents H. pylori recurrence, thus providing an attractive candidate for treating H. pylori infection [8].
A study utilizing transgenic FVB/N INS-GAS mice and Mongolian gerbils evaluated the role of 5-ethyl-2-hydroxybenzylamine (EtHOBA) against H. pylori-induced gastric cancer development [65]. EtHOBA, a potent scavenger of all dicarbonyl electrophiles that react with amines, prevents cancer development in these animal models. Similarly, a mouse model developed an in vivo activatable pH-responsive graphitic nanozyme, PtCo@Graphene (PtCo@G), to selectively treat H. pylori. The results showed high antibacterial activity against H. pylori and negligible side effects on normal tissues and other symbiotic bacteria [66]. Several other studies have also attempted to potentiate the efficacy of existing antibiotics by combining them with other compounds, as the current treatment usually requires high doses and frequent administration to succeed. A similar study proposed that an innovative mucoadhesive system (Mucolast®) loaded with amoxicillin and clarithromycin could improve the efficacy of treatment against H. pylori [67]. Treatment of H. pylori-infected C57BL/6 mice with Mucolast® loaded with antibiotics showed superior efficacy than treatment with antibiotics only, as evidenced by the bacterial count in stomach tissues and histopathological evaluations. Similarly, another study analyzing the fecal microbiome composition in H. pylori-infected mice evaluated the efficacy of a gentamicin-intercalated smectite hybrid (S-GM)-based treatment [68]. The results showed that a H. pylori polymerase chain reaction (PCR) of the gastric mucosa was significantly lower in the STT and S-GM-based treatment group than in the non-treatment group. The results also showed that S-GM-based therapy could reduce IL-8 levels and atrophic changes in the gastric mucosa. Stool microbiome analysis revealed that mice treated with S-GM-based therapy showed microbiome diversity and abundant microorganisms at the phylum level compared to STT-treated mice. Overall, these results suggested that S-GM-based treatment may be a promising and effective therapeutic agent against H. pylori infection [68].
Other studies have used animal models to evaluate immunological events in the control of H. pylori infections. A study using a mouse model suggested that blocking the TLR4 signaling pathway could downregulate MyD88 expression; reduce NF-κB activation; increase CD4+, IL-2 receptor alpha chain (CD25+), forkhead box protein 3 (FOXP3+), and Treg numbers [69]; and consequently depress the Th1 and Th17 immune response, exacerbate H. pylori colonization density, and reduce the degree of inflammation in the gastric mucosa infected with H. pylori. As a result, the interaction between the TLR signaling pathway and Tregs might be an important factor in reducing H. pylori colonization and suppressing the inflammatory response. This mechanism was suggested to provide a new strategy for designing effective preventive and therapeutic treatment regimens against H. pylori colonization [69]. The antibacterial therapeutic potential of peptides, such as tilapia piscidin 4 (TP4), against multidrug-resistant H. pylori was evaluated in vivo in murine models (mice and rabbits). TP4 was found to inhibit the growth of antibiotic-sensitive and antibiotic-resistant H. pylori by causing membrane depolarization and the extravasation of cellular constituents. TP4 treatment suppresses the Treg subset population of pro- and anti-inflammatory cytokines. H. pylori maintains a high Treg subset and a low Th17/Treg ratio during gastric epithelium colonization, resulting in the expression of both pro- and anti-inflammatory cytokines [70].

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Subjects: Infectious Diseases; Gastroenterology & Hepatology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Shamshul Ansari
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Yoshio Yamaoka
View Times: 479
Entry Collection: Gastrointestinal Disease
Revisions: 3 times (View History)
Update Date: 14 Jul 2022
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