El-Gohary et al.

, Biol Med (Aligarh) 2015, 7:5

Biology and Medicine

http://dx.doi.org/10.4172/0974-8369.1000251

Case Report Open Access

Epidemiological Study on H. pylori in Cattle and Its Milk with Special

Reference to its Zoonotic Importance
Adel H El-Gohary1*, Mohamed A Yousef2, Amro A Mohamed1, Waleed E Abou El-Amaiem3 and Lobna M Abdel-Kareem3
1
Department of Hygiene and Zoonoses, Department of Internal Medicine, Egypt
2
Infectious and fish Diseases, Faculty of Veterinary Medicine, Mansoura University, Egypt
3
Aga District in EL-Dakahlia Veterinary Authority, General Organization for Veterinary Medical Services, Egypt

Abstract
This study was carried out to investigate some epidemiological aspects on the occurrence of Helicobacter pylori in
cattle, milk and humans at Dakahlia province, Egypt during the period from February 2014 to June 2015. A total of 304
samples including 117 rectal swabs (53 cows and 64 buffaloes) and 85 milk samples (36 cows and 49 buffaloes) sand
102 humans stools were collected and subjected to bacteriological examination by culturing on Columbia Blood Agar
(CBA) and biochemically identified. The results showed that the overall occurrence of H. pylori were 21.7% in collected
samples. The occurrence in cattle faeces was 18.8% (11.9% in cows and 6.9% in buffaloes). However, the isolation rate
from cattle milk was 28.2% (10.5% in cows and 17.7% in buffaloes). Moreover, the frequency distribution of H. pylori
from human stool was 19.6%. Concerning animal breed, native breed of cattle and their milk showed higher occurrence
(5.2% in cow's faeces, 11.9% in buffalo's faeces, 7% of cow's milk and 17.7% of buffalo's milk). Regarding animal age,
the occurrence of H. pylori was increased with increasing age. On the other hand, the frequency distribution of H. pylori
was more prevalent in the samples (faeces and milk) collected from Mansoura center. In relation to human samples, with
respect to gender, males showed higher isolation rate (11.7%) than females (7.8%). Whereas, frequency of H. pylori in
adults (4.9%) was higher than young (1.96%). On the other hand, H. pylori was more frequently isolated from patients
(8.8%) with gastrointestinal disorders. Moreover, the occurrence of H. pylori was higher in human samples collected
from persons of occupations related to animals such as veterinarians (6.8%), dairy workers, and farmers (3.92% each)
than others. It could be concluded that H. pylori could be isolated from cattle, milk and humans with recognizable
percentages, suggesting its zoonotic significance and role played by cattle especially buffaloes and its milk as potential
reservoir and source of human infection. The zoonotic significance for H. pylori as well as the recommended preventive
measures which should be taken to avoid the risk of contamination of milk and human infection were fully discussed.

Keywords: Epidemiology; Zoonosis; H. pylori importance and role of cattle and its milk which act as reservoir and
source of human infection in Egypt are scarce or absent. So, this work was
Introduction conducted to carry out some epidemiological studies on the occurrence
of H. pylori in cattle and their milk. Also, the epidemiological aspects of
The Helicobacter genus consists of a group of microaerophilic,
H. pylori in man were investigated.
none sporulating, Gram-negative rods that colonize on the mucus
layer covering the epithelial surface of the gastrointestinal tract of Materials and Methods
humans and a variety of animal species. There are currently 6 validated
Helicobacter species isolated from gastric tissue and 16 validated entero A total of 304 cattle, milk and human samples were collected from
hepatic species. Some Helicobacter species may be commonly (H. Mansoura and Aga centers, at Dakahlia province, Egypt. From cattle, 117
aurati) or occasionally (H. bilis and H. muridarum) isolated from both faecal samples including (53 cows faeces, 64 buffaloes faeces ) of different
gastric and entero hepatic sites [1]. ages and breeds were taken directly from the rectum of animals using sterile
swabs, The swabs then directly immersed in tubes containing Tryptone
Although H. pylori is present in the stomachs of about half of soya broth and immediately transported to the laboratory in ice box under
world’s population, the routes of transmission are still unclear and non- complete aseptic conditions. The detailed data concerning locality, age,
human reservoirs have not been identified. The prevalence of H. pylori sex, breed, housing, health status, number of parturition, stage of lactation,
infection increases with age and is inversely related to socio-economic water supply, feeding pattern and hygienic disposal of animal wastes. From
and hygiene status, suggesting person-to person transmission. Several raw milk, 85 milk samples consisting of (36 cows and 49 buffaloes) were
studies have shown high prevalence of antibodies against H. pylori
in abattoir workers, such as veterinarians, butchers and slaughterers,
suggesting that H. pylori might be transmitted from animals to man.
Dogs and sheep have also been implicated in the transmission of *Corresponding author: Adel H El- Gohary, Department of Hygiene and
Zoonoses, Department of Internal Medicine, Egypt, Tel: 201-060-849-47; E-mail:
Helicobacter infection [2]. waleedabouelamaim@gmail.com
From the zoonotic point of view and public health importance Received July 08, 2015; Accepted September 30, 2015; Published October 07,
of H. pylori, recently recovery of H. pylori from cows by Dore et al. 2015
[3] supported this idea. Milk (especially raw milk) and its products Citation: El-Gohary AH, Yousef MA, Mohamed AA, El-Amaiem WEA, Abdel-
are indicated as an important vehicle for transmission of pathogenic Kareem LM (2015) Epidemiological Study on H. pylori in Cattle and Its Milk with
microorganisms, where, milk is considered as cultural and growth Special Reference to its Zoonotic Importance. Biol Med (Aligarh) 7: 251. doi:
10.4172/0974-8369.1000251
media for such organism [4].
Copyright: © 2015 El-Gohary AH, et al. This is an open-access article distributed
Little information about the epidemiology of H. pylori in dairy under the terms of the Creative Commons Attribution License, which permits
animals in Egypt are known , also the reports dealing with its zoonotic unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.

Biol Med (Aligarh)

ISSN: 0974-8369 BLM, an open access journal Volume 7 • Issue 5 • 1000251
Citation: El-Gohary AH, Yousef MA, Mohamed AA, El-Amaiem WEA,Abdel-Kareem LM (2015) Epidemiological Study on H. pylori in Cattle and Its Milk
with Special Reference to its Zoonotic Importance. Biol Med (Aligarh) 7: 251. doi: 10.4172/0974-8369.1000251

Page 2 of 5

collected in sterile cups. From human stool specimens, 102 represented under low level of hygienic practices (Table 2).
(45 apparently healthy, 35 with gastrointestinal disorders, and 22
The frequency distribution of H. pylori in animal faecal samples in
diarrheal stool specimens) were obtained. All samples were collected
relation to age was illustrated in Table 2. There were various frequency
in sterile cups and transported to laboratory in ice box under complete
distribution of H.pylori with different age group in cattle (from 0-6
aseptic conditions. The data including age, gender, health status, socio-
months, from 6-12 month, from 12-18 month, from 18-24 month
economic level, hygienic practices, occupations and previous suffering
and over 2 years), the frequency distribution of H. pylori were 1.7%,
from dyspepsia. All collected samples were cultured within six hours
0.85%, 0.85%, 0.85%, and 2.65%, respectively, whereas their respective
from collection.
frequency distribution of H. pylori in buffaloes were 0.85%, 0.85%,
Isolation and Identification of H. pylori 1.7%, 1.7% and 6.8% (Table 3).

All collected animal rectal swabs were directly streaked on CBA It was obvious from recorded results in Table 2 that the highest
supplemented with antibiotic (Vancomycin, Trimethoprim and Incidence (6.8% and 2.65%) of H. pylori was in buffaloes and cows over
Cefsulodin). A loopful from each collected milk sample was plated than 2 years, respectively. The most examined over than 2 years. Females
on CBA. A sterile swab was taken from each human stool sample and are kept for lactation and breeding for old ages which they were more
directly cultured on CBA. All cultured plates were incubated under exposed to H. pylori infection. However, the present results showed that
microaerophilic conditions (5% O2, 15% Co2 and 80% N2) using small or young ages were with low frequency rates (1.7%) in cows and
generating kits (Campygen TM 2.5 L) (Oxoid CN0025A) for creation (0.85%) in buffaloes. This explained that the age may be considered as
of microaerophilic atmosphere at 37°C for one week (5-7 days). a risk factor for H. pylori infection. This result suggesting the old age
After the incubation, the suspected growing colonies (tiny, small and of cows and buffaloes are more exposed to harbor H. pylori infection
translucent) were picked up and inoculated on CBA slope, incubated (Table 4).
microaerophilically at 37°C for 5-7 days for further identifications [5]. The results showed that the examination of the faecal samples
The tests used for identification of H. pylori isolates were Gram collected from various localities showed variable frequency distribution
staining, oxidase, catalase, urease, TSI, growth at 1% glycine and rates from one area to another (Table 3). In cows the samples collected
resistance to Nalidixic acid and cephalothin [6]. from Aga district, Nawasa Al-Bahr village, Mitishna village, Mansoura
district, Awish Al-Hagar village were showed occurrence of 0.85%, 1.7%,
Results and Discussion 0.85%, 2.65% and 0.85%, respectively, while the respective occurrence
frequency distribution in buffaloes were 1.7%, 0.85%, 2.6%, 5.9% and
Helicobacter pylori, is well established as a major cause of gastritis,
0.85%. The recorded results revealed that higher frequencies (5.9% and
peptic ulcer, duodenal ulcer and chronic gastritis. It is also implicated
in the development of gastric cancer. Consequently, the detection of
H. pylori infection has become important, due to fastidious and slow
Number of Number of Percentage
growing nature of H. pylori, great care was needed in the collection,  
Breed of the
examined Positive of Positive
animal
transport and culture [7]. However, the origin and transmission of samples Samples samples
this bacterium has not been obviously explained. One of the suggested
Holstein 12 2 1.7
modes of transmission is cattle milk consumed by human beings [8].
Native breed
H. pylori is one of the most common bacterial infectious agents Cows 41 6 5.2
cow (Baladi)
inhabits the stomach of more than half of world's population. The
Total 53 8 6.9
presence of H. pylori antigens in faeces of cows which contaminates the
cow's milk and might be a transmission route of H. pylori infection to Native breed
Buffaloes 64 14 11.9
buffaloes
man. Moreover, faecal contamination to milk due to improper hygienic
practice during production and management processing could transfer Total   117 22   18.8
H. pylori to milk consumers. From the zoonotic point of view, it was
Table 1: Frequency distribution of H. Pylori in animal faecal samples in relation to breed.
utmost of importance to study the role of cattle and its milk as reservoir
and source of human infection with H. pylori. According to available Percentage Number of Number of
Age of the
data and literatures, there was no previous studies in Egypt dealing with of Positive Positive examined
animal
samples Samples samples
zoonotic importance of H. pylori, moreover, the articles investigated
and discussed the epidemiology of H. pylori in cattle in Egypt are scarce 1.7 2 4 0-6 month

or absent. 0.85 1 7 6-12 month

0.85 1 2 12-18 month
Cows
In the present study, the frequency distribution of H. pylori from 0.85 1 4 18-24month
Holstein cows was 1.7% (Table 1). In a previous study carried out on 92 2.65 3 36 Over 2 years
lactating Holstein cows in Shahrekord, Iran found that the prevalence
6.9 8 53 Total
of H. pylori antigens in faeces of cows were 10.8%. The recorded results
in Table 1 showed that the native or Baladi breeds of cows had higher 0.85 1 2 0-6 month
frequency distribution of H. pylori (5.2%) While the buffaloes native 0.85 1 4 6-12 month
breed were showed a percentage of (11.9%). From the results recorded 1.7 2 6 12-18 month Buffaloes
in Table 1, it could be notice that the examined native breeds of cows 1.7 2 3 18-24month
and buffaloes showed higher isolation rates of H. pylori than the 6.8 8 49 Over 2 years
examined Holstein breeds. This might be suggested that either native or 11.9 14 64 Total
Baladi breeds are more susceptible to exposed to carry H. pylori in their 18.8 22 117 Total
gut and shedding in their faeces or the native breeds might be reared Table 2: Frequency distribution of H. Pylori in animal faecal samples in relation to age.

Biol Med (Aligarh)

ISSN: 0974-8369 BLM, an open access journal Volume 7 • Issue 4 • 1000251
Citation: El-Gohary AH, Yousef MA, Mohamed AA, El-Amaiem WEA,Abdel-Kareem LM (2015) Epidemiological Study on H. pylori in Cattle and Its Milk
with Special Reference to its Zoonotic Importance. Biol Med (Aligarh) 7: 251. doi: 10.4172/0974-8369.1000251

Page 3 of 5

2.65%) were found in buffaloes and cows in Mansoura district (Table 5). Number of
Percentage of Number of Breed of the
examined
This might be due to the examined farms in Mansoura district were Positive samples Positive Samples animal
samples
mixed herds of cows and buffaloes of low hygienic conditions in farms, 3.5 3 13 Holstein
which facilitate the contact between buffaloes and cows and give the Native breed
7 6 23 Cows
opportunities to harbor the H. pylori microorganism. cow(Baladi)
10.5 9 36
In the present study, the frequency distribution of H. pylori from Native breed
Holstein cow's milk was 3.5%, while from the native breed or Baladi 17.7 15 49 Buffaloes
buffalo
breed was 7%. On the other hand the frequency distribution of buffalo's 28.2 24 85 Total
milk from the examined native breed (which is the only buffalo breed
Table 4: Frequency distribution of H. pylori in raw milk samples in relation to breed.
in Egypt) was 17.7% which was higher than Holstein cows and native
breed cows. Lower frequency distribution from raw samples from Percentage Number of Number of Locality of
Holstein cows in different geographic areas of Japan was previously of Positive Positive examined collected raw
detected by Fujimura et al. [4] who found that 72.2% were positive for samples Samples samples milk samples
H. pylori from raw milk samples and 55% commercial pasteurized milk. 2.3 2 7 Aga district
Nawasa Al-
3.55 3 7 Aga
It was found that the frequency distribution of H. pylori in cow's Bahr village
Center
milk from different localities of Aga district, Nawasa Al-Bahr village, Mitishna
1.2 1 2
Mitishna village, Mansoura district, Awish Al-Hagar village were village
Cows
2.3%, 3.55%, 1.2%, 4.7% and 2.3%, respectively, while their respective Mansoura
4.7 4 13
district
frequency distribution of buffaloes milk were 3.55%, 3.55%, 1.2%, 8.2% Mansoura
Awish Al-
and 1.2%. The highest frequency distribution of H. pylori (8.2% and 2.3 2 9
Hagar village
Center
4.7%) was from cow's milk and buffalo milk in relation to locality was 10.5 9 36 Cows
found in Mansoura district. The lowest frequency distribution was 3.55 3 11 Aga district
found in Mitishna village which was 1.2% in both cows and buffaloes Nawasa Al-
(Table 5). 3.55 3 7 Aga
Bahr village
Center
Mitishna
The overall isolation rate of H. pylori from human stool samples was 1.2 1 2
village
19.6%. The isolation rates were 11.7 % and 7.8% in males and females, Mansoura Buffaloes
respectively. In a study higher isolation rates (48.27%) were recorded 8.2 7 20
district
of patients with hydatid liver diseases were positive, of which were Awish Al- Mansoura
1.2 1 9 Center
32.7% and 15.5% were in males and females, respectively. in another Hagar District
study carried out by Uemura et al. [9] who detected H. pylori in 445 17.7 15 49 Buffaloes
28.2 24 85 Total
Table 5: Frequency distribution of H. pylori in raw milk samples in relation to locality
Locality of
Percentage Number of Number of collected
of Positive Positive examined animal non ulcer dyspeptic patients with the percentage of 46.2% in males
samples Samples samples faecal and 53.7% in females, moreover in patients with duodenal ulcers,
samples
the isolation rates in males were 72% and 28% in females. In patients
0.85 1 8 Aga district with gastric ulcer, the isolation rates of H. pylori were 76% and 24% in
males and females, respectively. Furthermore, in patients with gastric
Nawasa Al- polyps, the results were 36.6% and 64.4% in males and females. The
1.7 2 14
Bahr village Aga Center higher isolation rates were also previously reported by Rasheed et al.
[10] who found the overall percentage of H. pylori was 74.4%, moreover
Mitishna
0.85 1 9
village Cows the incidence of H. pylori was 73.5% in males and 75.4% in females. The
Mansoura isolation rate of H. pylori from females (7.8%) was almost similar to the
2.65 3 12 isolation rate of a study previously reported by Ahmed et al. [11] who
district
Mansoura found the isolation rates of the examined females percentage was 7.4%,
Awish Al-
0.85 1 10 Center
Hagar village while their isolation in males was 28%. The recorded results revealed
6.9 8 53 Total that H. pylori was slightly higher in examined males than females, this
1.7 2 13 Aga district could illustrate that males which are more susceptible than females to
0.85 1 6
Nawasa Al- carrying and infection with H. pylori (Tables 6 and 7).
Bahr village Aga Center
Mitishna This conviction was fully supported by the idea of Klein [12] who
2.6 3 21
village
Buffaloes
stated that males which are more susceptible than females to infections
5.9 7 16
Mansoura caused by bacteria, viral, fungi and parasites due to males generally
district
Mansoura exhibit reduced immune responses fully compared to females. These
Awish Al-
0.85 1 8
Hagar village
Center differences are usually attributed to socio-ecological, physiological
11.9 14 64 Total
(hormonal in origin), and occupational (referred to animal contact),
18.8 22 117 Total
so, the females less susceptible to infection than males, not only because
of the androgenic hormones which reduce the immunity but also sex
Table 3: Frequency distribution of H. pylori in animal faecal samples in relation to locality.

Biol Med (Aligarh)

ISSN: 0974-8369 BLM, an open access journal Volume 7 • Issue 4 • 1000251
Citation: El-Gohary AH, Yousef MA, Mohamed AA, El-Amaiem WEA,Abdel-Kareem LM (2015) Epidemiological Study on H. pylori in Cattle and Its Milk
with Special Reference to its Zoonotic Importance. Biol Med (Aligarh) 7: 251. doi: 10.4172/0974-8369.1000251

Page 4 of 5

Number of who reported that H. pylori isolated was more frequently isolated from
Percentage of Number of positive
Positive samples samples
examined Gender of human patients with gastrointestinal disorders. H.pylori had been isolated
samples from patients with upper gastrointestinal symptoms of peptic disease,
11.7 12 59 Male in patients with gastritis and peptic ulcer [17] (Table 8).
7.8 8 43 Female
19.6 20 102 Total The occurrences of H. pylori in human stool samples with respect
Table 6: Isolation rate of H. Pylori from Human stool concerning to gender.
to occupation in Table 9 are illustrated. The occurrence of H. pylori in
children, farmers, veterinarians, officers, Housewives and dairy workers
Number of were 1.96%, 3.92%, 6.8%, 0.98%, 1.96% and 3.92%, respectively. The
Percentage of Number of
Positive samples positive samples
examined Age of human highest occurrence 6.8% was found in veterinarians and the lowest
samples occurrence 0.98% were found in officers the dairy worker group
2.95 3 15 1-10 years showed occurrence of 3.92%. It could be concluded that H. pylori could
1.96 2 17 10-20 years be isolated from cattle faeces, their milk and humans in the examined
3.92 4 22 20-30 years area reflecting the important role of cattle especially buffaloes as new
3.92 4 20 30-40 years potential zoonotic reservoir. So, the recommended measures to reduce
1.96 2 15 40-50 years and avoid the risk of H. pylori are standard hygienic practices in animal
4.9 5 13 50-60 years management, feeding, hygienic disposal of animal wastes, preparation
19.6 20 102 Total of silage, and periodical cleaning and disinfection must be applied to
Table 7: Frequency of H. pylori from human stool with regard to age. reduce H. pylori carriages in cattle. Avoid faecal contamination for milk.
All raw milk and its products must be efficiently heat treated to avoid
steroid hormones affect disease resistant genes and behavior which
risk of H. pylori for milk consumers. Gastroenterology hospitals must
make males more susceptible to infection.
be provided with a rapid urease test kits, all patients with peptic ulcers
Regarding frequency of H. pylori from human stool with regard to disease and other gastric disease must be monitored for detection of
age, there were various frequency distribution of H. pylori with different H. pylori by rapid tests then confirming with culturing or PCR assays.
age groups in humans, the frequency distribution of H. pylori in human The positive H. pylori cases must be treated to avoid development of
were 2.95%, 1.96%, 3.92%, 3.92%, 1.96 % and 4.9%, respectively. The age gastric cancers. Persons had occupations related to animals such as
groups varied (From 1-10 years, from 10-20years, from 20-30, from 30- veterinarian, dairy worker and farmers must be healthy educated to
40, from 40-50, from 50-60). The highest rate (4.9%) was found in the avoid the risk of H. pylori from cattle by application strictly personal
age group from 50-60 years old, while the lowest frequency distribution hygienic practices. Further research in needed to explain the role of
rate (1.96%) was found in 2 age groups from 10-20 years and from 40- other domestic animals such as horses, sheep, goats and pet animals
50 years. In a study performed by Windsor et al. [13] recorded that the as reservoir for H. pylori. Also, the effect of ecology, seasons and other
males under age group less than 10 years showed highest prevalence risk factors on isolation rates of H. pylori must be studied in different
(11%), whereas, females aged from 11 to 20 years showed that the geographic areas in Egypt to obtain clear picture on the epidemiology
highest prevalence (14%) in rural community. In urban community, the of H. pylori in animals and man.
males aged from 11to 20 years was highest (9%), however in females,
the highest prevalence was in age group from 31-40 years with (13%).
Incidence rate of H. pylori detected in adults in the present study agreed
Percentage of Number of
with the previous reports of Malaty et al. [14] who carried out a study Number of Healthy state of
Positive samples Examined
positive samples human
on a total of 413 person (161 adults and 252 children) adult age range % samples
from 20 to 75 years and the children from 1 to 19 years. The overall 5.8 6 45 Apparently healthy
seropositivity rate of H. pylori was 75% among adults and 22% among Patients with
children. Higher frequency of isolation of H. pylori in young age was 8.8 9 35 gastrointestinal
disorders
also recorded in another study carried out by Naficy et al. [15] who
Diarrheal stool
reported that 42 % children aged from 6-17 months were positive for 4.9 5 22
samples
H.pylori infection. 19.6 20 102 Total
It was obvious that adults showed higher prevalence of H. pylori Table 8: Results of bacteriological examination of human stool samples for H.
than young. This indicated that the prevalence increases with increasing pylori in relation to healthy state.
the age, this conviction was previously supported by Rasheed et al. [10]
who mentioned that the prevalence of H. pylori in human population Percentage Number of Number of Source
increased with increasing age and presence of household animals and of Positive positive examined Occupation of
size of family and members of family. samples samples samples samples
Children less than 10
Concerning results of bacteriological examinations of human stool 1.96 2 17
years
samples for H. pylori in relation to healthy state, the highest occurrence 3.92 4 15 Farmers
(8.8%) had been showed in the patients with gastrointestinal disorders, 6.8 7 22 Veterinarians Human
the lowest percentage (4.9%) was found in the diarrheal patients, while 0.98 1 15 Officers stool
the apparently healthy persons showed a percentage of (5.8%) (Table 8). 1.96 2 13 Housewives
3.92 4 20 Dairy workers
From the achieved results, it was obvious that H. pylori isolated was
19.6 20 102 Total
more frequently isolated from patients with gastrointestinal disorders;
Table 9: The occurrence of H. pylori in human stool samples with respect to
this conviction was fully supported by the results of Javed et al. [16]
occupation.

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ISSN: 0974-8369 BLM, an open access journal Volume 7 • Issue 4 • 1000251
Citation: El-Gohary AH, Yousef MA, Mohamed AA, El-Amaiem WEA,Abdel-Kareem LM (2015) Epidemiological Study on H. pylori in Cattle and Its Milk
with Special Reference to its Zoonotic Importance. Biol Med (Aligarh) 7: 251. doi: 10.4172/0974-8369.1000251

Page 5 of 5

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