Brief Original Article

Serologic evidence and risk factors for Helicobacter pylori infection in

animals and humans

Mahmoud Elhariri1, Rehab Elhelw1, Dalia Hamza2, Heba Sayed El-Mahallawy3

1 Department of Microbiology, Faculty of Veterinary Medicine, Cairo University, Cairo, Egypt
2 Department of Zoonoses, Faculty of Veterinary Medicine, Cairo University, Cairo, Egypt
3 Department of Animal Hygiene, Zoonoses, and Animal Behaviour and Management, Faculty of Veterinary

Medicine, Suez Canal University, Ismailia, Egypt

Abstract
Introduction: Helicobacter pylori (H. pylori) is one of the most common bacterial infections among humans worldwide. Although many records
imply its interfamilial acquisition, the role of animals remains poorly understood. This study was undertaken to investigate the seroprevalence
of H. pylori in animals and their human contacts in Cairo and Giza governorates, Egypt.
Methodology: Commercial enzyme-linked immunosorbent assay (ELISA) kits were used to detect IgG antibodies to H. pylori in dogs, cattle,
and humans.
Results: Seropositive dogs (35/94; 37.2%), cattle (24/80; 30%) and humans (40/90; 44.4%) were found. Seroprevalence in animals significantly
varied in different areas of sample collection, but there was no association with sex or age. Human seropositivity rates were associated with
increasing age; moreover, seropositive dog owners (51.7%; 15/29), had seropositive dogs. However, infection was not associated with subject's
sex, occupation, or history of animal contact.
Conclusions: Our findings indicate H. pylori is widely distributed in cattle and dogs and their human contacts in Cairo and Giza, Egypt. Further
studies to determine infection in other occupational groups are needed. This study provides baseline information on the seroprevalence of H.
pylori, which may be required to begin prevention control programs in our area.

Key words: dogs; cattle; human; Egypt; ELISA; Helicobacter pylori.

J Infect Dev Ctries 2017; 11(5):414-419. doi:10.3855/jidc.9339

(Received 23 August 2016 – Accepted 13 january 2017)

Copyright © 2017 Elhariri et al. This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction The prevalence rate of H. pylori varies greatly by

Helicobacter pylori (H. pylori) is one of the most the geographic area, age, and socioeconomic status.
common bacterial infections among humans, and has Infection appears to be more common in developing
worldwide distribution. The causative agent is a helical, than in developed countries [8,9]. Modes of infection
microaerophilic, flagellated Gram-negative bacterium are yet not clearly understood. Although spread can
that inhabits and adapts to the acidic human gastric occur through the environment or via reservoirs or
mucosa [1]. The organism colonizes about 50% of the vectors, little is known about the main route of
world population’s upper gastrointestinal tracts [2], dissemination from an infected individual [10].
which makes the infection a public health concern Transmission from person to person, through gastro-
worldwide [3]. Although infected individuals usually oral, oral-oral, fecal-oral routes, and through exposure
never encounter clinical symptoms except chronic to contaminated food or water is highly controversial;
gastritis, acute infections can cause acute gastritis with furthermore, close and intense human contact with
abdominal pain or nausea [4,5]. The ability of the animals has been identified as a risk factor [11-13]. The
organism to hydrolyze urea leads to gastric ulcers and possibility of zoonotic transmission from animals has
increases the risk of developing duodenal and stomach been previously suggested [14]. Moreover, detection of
cancer to the level that the World Health Organization anti-H. pylori antibodies in abattoir workers in France
(WHO) classifies as a class I carcinogen, where the and in northern Sardinian shepherds, at higher levels
infection is found in 80%–90% of patients with gastric than their siblings inhabiting the same house [15,16],
ulcers [6,7]. demonstrates the zoonotic importance of the organism.
Elhariri et al. – Seroprevalence of H. pylori in animals and humans J Infect Dev Ctries 2017; 11(5):414-419.

However, the exact role of animals as a reservoir of some of the sampled dogs (n = 29). Demographic data
infection remains unclear. on age and sex were also obtained.
Most data about the rates of H. pylori infection in Following collection, samples were transported on
different geographical and demographic populations ice box to Cairo University, Faculty of Veterinary
comes from seroprevalence studies [17]. Serological Medicine, where whole blood samples were
tests using enzyme-linked immunosorbent assay centrifuged, and aliquots of sera were separated and
(ELISA) are preferred as a noninvasive alternative stored at -20°C for ELISA.
method to endoscopy and biopsy for rapid diagnosis of
H. pylori. Thus, serological tests have been used Serological assay
extensively in screening humans in clinics and for The canine, bovine, and human H. pylori IgG (Hp-
epidemiologic studies [18]. Unfortunately, in Egypt, IgG) indirect ELISA kits (MyBioSource, San Diego,
very little epidemiological data are available about the USA) were used according to the manufacturer’s
situation of H. pylori infection in humans and animals. instructions to detect IgG antibodies against H. pylori
To provide further information, the present study was in sera of dogs, cattle, and humans, respectively.
undertaken to address the occurrence of H. pylori The sample optical densities (OD) were measured
infection in apparently healthy humans and animals, using a microplate reader (CLINDIAG, Orange, USA)
including their owners. at 450 nm, and the sample-to-negative ratio was
determined. As recommended by the manufacturer, for
Methodology human kits, samples were considered to be ELISA
Ethics statement positive if the OD sample/OD negative ≥ 2.1, while if
Protocols for the collection of samples were OD sample/OD negative less than 2.1, the sample was
reviewed and approved by the Scientific Research considered as negative. For canine and bovine H. pylroi
Committee and Bioethics Board of Suez Canal IgG ELISA kits, the cut-off was calculated based on the
University, Faculty of Veterinary Medicine, Ismailia, following formula: average of negative control + 0.15.
Egypt (No. 2016086). Samples exceeding the calculated cut-off value were
considered positive.
Sample collection
Whole blood was collected from convenience Statistical analysis
samples of apparently healthy cattle and dogs. Cattle PASW Statistics, SPSS version 18.0 software
were randomly sampled from farms in El-Badrasheen (SPSS Inc., Armonk, USA) was used to analyze the
and Mazghona and Gameeit Ahmed Orabi of Giza and data. Chi-squared (χ2) and Fisher's exact tests were
Cairo governorates of Egypt, respectively. Domestic performed to analyze H. pylori antibody positivity
dogs were those mostly kept indoor and admitted with between various groups. Differences were considered
their owners to small animal veterinary clinics in El- statistically significant if the P value was < 0.05.
Haram and Heliopolis and El-Maadi for other purposes.
Stray dogs were those had been captured roaming in Results
rural and suburban areas in Giza and Cairo Serologic detection of anti-H. pylori antibodies in dogs
governorates. Human whole blood samples (n = 90) Overall, a total of 264 whole blood samples from
were collected from consenting apparently healthy dogs (n = 94), cattle (n = 80), and people (n = 90) were
people (n = 61) attending the Giza and Cairo hospitals tested. Generally, there was no statistically significant
for routine health examinations and from owners of difference in the seroprevalence in dogs (37.2%;
35/94), cattle (30%; 24/80), and humans (p = 0.151). A

Table 1. Seroprevalences of IgG antibodies to H. pylori by ELISA in dogs from Cairo and Giza governorates.
Dogs Positive dogs
Source of sample Male Female Total positive belonging to
collection No. No. of H. pylori No. No. of H. pylori (No., %) positive dog
examined + (%) examined + (%) owners
Stray dogs 7 3 (42.9%) 11 2 (18.2%) 5 (18, 27.8%) -
El-Maadi 14 3 (21.4%) 10 4 (40%) 7 (24, 29.2%) 5
Heliopolis 21 4 (19%) 7 1 (14.3%) 5 (28, 17.9%) 2
El-Haram 13 12 (92.3%) 11 6 (54.5%) 18 (24, 75%) 8
Total 55 22 (40%) 39 13 (33.3%) 35 (94, 37.2%) 15

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Elhariri et al. – Seroprevalence of H. pylori in animals and humans J Infect Dev Ctries 2017; 11(5):414-419.

relatively large percentage of dogs were found to have Figure 1. Seroprevalence of H. pylori in people by age and
antibodies to H. pylori in the ELISA test (37.2%; 35/94) gender using ELISA. Seropositivity was associated with
(Table 1). Prevalence significantly varied by the area of increasing age but not with gender. Individuals in the third
decade of life were more likely to have a higher seroprevalence
sample collection, with the highest found in dogs from than those under 20 years of age.
El-Haram (75%; 18/24), El-Maadi (29.2%; 7/24), and
Heliopolis (17.9%; 5/28) (p < 0.05). There was no
significant difference in seropositivity in male (22/55)
and female dogs (13/39) (p > 0.05) (Table 1).

Serologic detection of anti-H. pylori antibodies in cattle

Cattle from three different farms were examined:
one in Cairo (Gameet Ahmed Orabi) and two in Giza
governorates (Badrashen and Mazghona), in addition to
sporadic cases bred by individual farmers (Table 2).
Thirty percent of the total examined cattle were
seropositive (24/80). Prevalence significantly varied by
the area of sample collection, with the highest found in
Badrashen in Giza governorates (52%, 13/25) and
Gameet Ahmed Orabi in Cairo governorate (30%,
6/20); the lowest was in Mazghona in Giza governorate
(14.3%, 5/35) (p < 0.05). Seropositivity was not 15/29) and people with no history of animal contact
associated with age or type of animal production (p > (41%; 25/61) (p = 0.338) (Table 4).
0.05) (Table 2).
Discussion
Serologic detection of anti-H. pylori antibodies in This study was undertaken as an attempt to evaluate
humans the distribution and possible zoonotic relationship of H.
A total of 44.4% (40/90) of humans were found to pylori infection in Giza and Cairo governorates, Egypt.
have antibodies to H. pylori. There was no statistically Overall, the differences of seroprevalence in the
significant difference in the seropositivity in men examined dogs, cattle, and humans was not statistically
(17/44) and women (23/46), while there was significant significant (p = 0.151). Seroprevalence in dogs was
difference among different age groups (p < 0.05) (Table 37.2% (Table 1). Generally, serodiagnosis in dogs
3, Figure 1). Although 15 seropositive dog owners had represents a big challenge, since they might be infected
seropositive dogs, there was no statistically significant with several Helicobacter species [19-21].
difference in seropositivity in dog owners (51.7%; Thirty percent of the examined cattle were
seropositive (Table 2), whereas lower seroprevalence

Table 2. Seroprevalences of IgG antibodies to H. pylori by ELISA in cattle from Cairo and Giza governorates.
Cairo Giza
Source of Gameet Ahmed Total number
sample Purpose of animal Badrashin Mazghona examined
Orabi
collection No. examined No. examined No. examined (+, %)
(+, %) (+, %) (+, %)
Meat production
Adults 7 (4, 57.1%) --- 15 (5, 33.3%) 22 (9, 40.9%)
Calves and heifers 13 (2, 15.4%) --- --- 13 (2, 15.4%)
Total 20 (6, 30%) --- 15 (5, 33.3%) 35 (11, 31.4%)
Farms
Milk production
Adults --- --- --- ---
Calves and heifers --- 15 (9, 60%) --- 15 (9, 60%)
Total --- 15 (9, 60%) --- 15 (9, 60%)
Adults --- 10 (4, 40%) 15 (0, 0.0%) 25 (4, 16%)
Sporadic
Calves and heifers --- --- 5 (0, 0.0%) 5 (0, 0.0%)
cases
Total --- 10 (4, 40%) 20 (0, 0.0%) 30 (4, 13.3%)
Total 20 (6, 30%) 25 (13, 52%) 35 (5, 14.3%) 80 (24, 30%)

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Elhariri et al. – Seroprevalence of H. pylori in animals and humans J Infect Dev Ctries 2017; 11(5):414-419.

Table 3. Seropositivity of IgG antibodies to H. pylori by ELISA among humans of different age groups.
Male Female
Total examined
Age group (years) No. of subjects No. of H. pylori No. of subjects No. of H. pylori (positive, %)
examined + (%) examined + (%)
Up to 15 20 4 (20%) 15 7 (46.7%) 35 (11, 31.4%)
16–30 8 7 (87.5%) 10 6 (60%) 18 (13, 72.2%)
31–45 12 5 (41.7%) 8 4 (50%) 20 (9, 45%)
More than 45 4 1 (25%) 13 6 (46.2%) 17 (7, 41.2%)
Total 44 17 (38.6%) 46 23 (50%) 90 (40, 44.4%)

Table 4. Seropositivity of IgG antibodies to H. pylori by ELISA in dog owners and subjects with no history of animal contact.
Male Female
Occupation of human
No. of subjects No. of H. pylori No. of subjects No. of H. pylori Total (positive, %)
subjects
examined + (%) examined + (%)
Apparently healthy 28 11 (39.3%) 33 14 (42.4%) 61 (25, 41%)
Dog owners 16 6 (37.5%) 13 9 (69.2%) 29 (15, 51.7%)
Total 44 17 (38.6%) 46 23 (50%) 90 (40, 44.4%)

was reported in other studies [22,23]. Previous on ELISA had seropositive dogs (Table 4). Although
detection of H. pylori from bovine feces [23,24] and/or there was no significant difference in the seropositivity
milk [23,25] and seroconversion in farm workers between dog owners and the other group, contact with
[26,27], however, might suggest the probable role of dogs was identified as a risk factor for acquiring H.
this animal species in transmission of infection to pylori infection in other studies [36,37]. Similar to our
humans in case of inappropriate farm management findings, in other seroepidemiological studies, the exact
practices. relationship between pet ownership and human
In our investigation, the overall seroprevalence in seropositivity cannot be clearly established [38,39].
humans was relatively high (44.4%) (Table 3). This was It is worth mentioning that an association had been
somehow higher than results shown in previous studies reported between animal contact and seropositivity in
from other countries: United Kingdom (27.6%) [28], abattoir workers and veterinarians working in abattoirs
Australia 15.4% [29], and United State (36.3%) [30], and meat processing plants in New Zealand [40,41].
while it was lower than reports in Uganda (87%) [31], However, the cross-reactivity with antibodies to other
China (62%) [32], and neighboring Arabian countries, gastrointestinal organisms which might be acquired
mainly Libya (94%) [33] and Sudan (65%) [34]. The from slaughtered animals was not excluded in those
diversity of crowding, socioeconomic status, and studies. Thus, these findings are questionable, and it
environmental and hygiene factors may play an was suggested that this higher prevalence was due to
important role in increased rates of H. pylori infection cross-reactivity to Campylobacter jejuni [14]. In
in developing countries. another study, high seroprevalence was reported in
Results showed an association between shepherds from northern Sardinia in comparison to their
seroprevalence and increasing age of the examined siblings inhabiting the same house who had no contact
subjects (Table 3, Figure 1). Similarly, this was with sheep. Authors claimed that contact with sheep
reported in other studies [29,35]. Individuals in the third and sheepdogs was a risk factor for infection [16].
decade of life were more likely to have a higher However, other authors failed to isolate H. pylori and/or
seroprevalence than those under 20 years of age. This to detect its antibodies due to natural infection from
may be because Egyptian youth in such age groups like stray and pet cats [42,43] and pigs in abattoirs [44].
to have food away from home during their outside These questionable data suggest doubtful zoonotic
activities in trips or camps; thus, they might be infected transmission of such agent, and whether animals are
from consumption of contaminated food or water true reservoir hosts for H. pylori or not is still not
sources. Generally, it is estimated that colonization of obvious. It seems that infection might be contracted
H. pylori in gastric mucosa is associated with old age, from a common source (e.g., drinking water,
male sex, and low socioeconomic status [11,12]. consumption of raw vegetables) or might suggest that
The controversial finding is that around fifty H. pylori infection could be an anthroponosis
percent (51.7%; 15/29) of the dog owners who reacted

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Elhariri et al. – Seroprevalence of H. pylori in animals and humans J Infect Dev Ctries 2017; 11(5):414-419.

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race, and socioeconomic status. Gastroenterology 100: 1495- Corresponding author
1501. Heba S El-Mahallawy Department of Animal Hygiene, Zoonoses,
36. Lindo JF, Lyn-Sue AE, Palmer CJ, Lee MG, Vogel P, and Animal Behaviour and Management
Robinson RD (1999) Seroepidemiology of Helicobacter pylori Faculty of Veterinary Medicine, Suez Canal University
infection in a Jamaican community. Trop Med Int Health 4: Ring Rd., Kilo 4.5, 41522, Ismailia, Egypt
862-866. Phone: +20 100 294 2291
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Realdi G (2002) Risk Factors Associated with Helicobacter Heba_elmahalawi@vet.suez.edu.eg
pylori Infection among Children in a Defined Geographic
Area. Clin Infect Dis 35: 240-245.
Conflict of interests: No conflict of interests is declared.

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