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Mohammad S. Mubarak
Abstract The effect of garlic (Allium sativum) and cab- Keywords Garlic (Allium sativum)
bage (Brassica oleracea var. capitata) extracts on the Cabbage (Brassica oleracea var. capitata) juice
healing of gastric ulcer in experimental rats has been Aspirin ulcer Histopathological changes pH value
investigated. Thirty-three albino male rats (115 ± 4 g Bacterial count Gastric juice
B.Wt. each) were used and divided into 6 groups (n = 6
rats); one was used as a negative control while the others
were given aspirin orally (200 mg/kg B.Wt.). One of these Introduction
groups was employed as a positive control and the others
were administrated with 150 or 300 mg/kg B.Wt. doses of Peptic ulcers are erosions or open sores in the mucous
garlic and cabbage juice for 7 days. The length of the lining of the stomach or duodenum (the first part of the
gastric ulcer, the volume of gastric juice, the total acidity, small intestine). The term ‘‘peptic’’ distinguishes peptic
the pH value, the total bacterial count, and the histopa- ulcers from ulcerations that affect other parts of the body
thological changes of the stomach were examined. Results (e.g., diabetic leg ulcers). Peptic ulcer should never be
revealed that oral administration with both tested plant treated without proper diagnosis, since they are usually
extracts reduced the length of gastric ulcer, the total acid- caused by infection from Helicobacter pylori (H. pylori).
ity, the volume of gastric juice, the bacterial count, and the Patients with peptic ulcer due to infection should receive
histopathological changes caused by aspirin. On the other conventional treatment directed toward eradicating the
hand, both aqueous plants extract increased the pH value of organism. This treatment consists of various combinations
gastric juice. It is concluded that, garlic and cabbage of antibiotics, acid blockers, and bismuth-under medical
extract could be used for healing acute gastric ulcer. supervision. In addition, ulcers can also be caused or
E. A. M. Header
Clinical Nutrition, Faculty of Applied Medical Sciences, Umm
Al Qura University, Makkah, Saudi Arabia
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Med Chem Res
aggravated by stress, alcohol, smoking, and dietary factors Materials and methods
(Suadicani et al., 1999).
The symptoms of peptic ulcer are occasionally painless. Material and rats
However, the most common symptom is a dull ache in the
upper abdomen that usually occurs 2–3 h after a meal; Garlic (Allium sativum L.) and cabbage (Brassica oleracea
eating relieves the ache. Other common symptoms include var. capitata) were purchased as crude dried material from
weight loss, bloating, belching, and nausea. Untreated, local markets in Egypt. Garlic and cabbage were ground
peptic ulcers often bleed and may cause sharp burning pain using a porcelain grinder to pass through sieve-mesh pores
in the area of the stomach or just below it (David et al., of 1 mm in diameter. Extracts were prepared by mixing
2002). 1 gm of powdered leaves with 100 mL of distilled water.
Many years ago, researchers reported that cabbage juice The mixture was boiled for 10 min and left to cool for
accelerates healing of peptic ulcers. According to some 15 min. The aqueous extract was filtered, using filter paper,
reports, daily intake of a quart of cabbage juice led to to remove the particulate matter (0.2 mm) and the filtrate
symptom relief. Although only preliminary research sup- was freely dried (Lyophilized) and reconstituted in 1.5 mL
ports this approach of treatment, many doctors claim of distilled water (100 mg/kg body weight) (Shin, 2005).
considerable success using one quart per day for Aspirin was obtained as Aspegic from the Amirya
10–14 days, with ulcer symptoms frequently decreasing in Pharmaceutical Industries (Cairo, Egypt). Injections were
only a few days; carrot juice may be added to improve the prepared by dissolving one vial’s content in 25 mL of
flavor (Cheney, 1949; Noess, 1984). distilled water. A volume of 1 mL of this solution was
On the other hand, garlic has been reported to have anti- given orally (at the level 200 mg/kg body weight) for 1 day
Helicobacter activity in test-tube studies. In a preliminary to induce acute gastric ulcer in Albino male rats. Rats were
trial, garlic added as supplement (300 mg in tablets three fed on a ration (a basal diet devoid from starch) composed
times daily for 8 weeks) failed to eradicate H. pylori in of wheat bran, soya bean powder 44 %, fish meal, molas-
participants with active infections (Sivam et al., 1997; ses, fibers 3.3 %, sodium chloride, calcium carbonate,
Chung et al., 1998). Similarly, addition of 10 sliced cloves calcium phosphate, methionine, and ash (net protein 22 %
of garlic to the meals of participants with active H. pylori and fats 4.7 %). The diet was fed and water was provided
infections failed to inhibit the growth of the organism ad libitum for the experimental period. This ready to use
(Jensen et al., 1992). Further trials using garlic extracts are ration for Sprague–Dawley rats was made by the Cairo
needed to validate the anti-Helicobacter activity observed Agric. Dev. Company (Giza, Egypt). Albino male rats
in test tubes. Therefore, there is weak evidence to support (115 ± 4 g B.Wt.) of Sprague–Dawley strain were
the use of garlic for H. pylori-related peptic ulcers (Graham obtained from the Laboratory of Animal Colony, Faculty of
et al., 1999). Home Economics, Minufiya University, Egypt. Two
Garlic oil, however, was evaluated for gastro protective microbial cultures were employed, the first was nutrient
activity against ethanol-induced ulcers. Reactive oxygen agar for recording the total count of bacteria and the second
species are involved in the pathogenesis of these ulcers. was potato dextrose agar for counting the molds and yeasts.
The possible involvement of garlic oil in restraining the
oxidation process produced in gastric tissues was also Methods
investigated. Effect of garlic oil on ulcer index, lipid per-
oxidation, and antioxidant enzyme activity (GPx, catalase, Grouping design and feeding of rats
SOD) was undertaken. Pretreatment with garlic oil in doses
of 0.25 and 0.5 mg/kg, 30 min before administration of The experiment was performed in the Animal House of the
ethanol (1 mL of 100 %) caused a decrease in ulcer index Faculty of Home Economics, Minufiya University. Rats
and lipid peroxidation and improved the decrease in anti- were housed in wire cages in a room maintained at
oxidant enzyme levels caused by ethanol. This result sug- 25 ± 2 °C and kept under normal healthy conditions. All
gests that garlic oil possesses antioxidant properties and rats were kept on basal diet for a week before treatment.
provides protection against ethanol-induced gastric injury After 1 week, rats were divided into two main groups. The
(Khosla et al., 2004). first group (n = 6 rats) was fed on the basal diet only as a
In view of the wide interest in the treatment of ulcer, we negative control (healthy rats) while rats in the second
present, herein, data pertaining to the anti-ulcer activity of group (n = 30 rats) were treated orally with 200 mg/kg
garlic (Allium sativum) and cabbage (Brassica oleracea B.Wt. of aspirin solution for induction of acute gastric
var. capitata) juice in experimental rats. These natural ulcer according to a procedure previously described
foods may be used as starting points in the development of (Agrawal et al., 2000). Rats with aspirin-induced gastric
new ulcer drugs. ulcers were divided into five groups (n = 6 rats in each
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Med Chem Res
group). One group was left as a positive control while the described (Chapman et al., 1959) using the following
other groups were administrated with garlic and cabbage equation:
juice at doses of 150 and 300 mg/kg B.Wt for 7 days. Relative organ’s weight ðROWÞ
¼ ðOrgan weight=Total body weightÞ 100:
Measurement of the length of gastric ulcer
Histopathological study
On the last day of experimental period, all rats were starved
for 12–14 h and only allowed to drink water. Next morn- Specimens from stomachs were collected from rats of all
ing, all rats were sacrificed, and their stomachs were tied experimental groups, fixed in 10 % neutral buffered for-
around both openings (cardiac & pyloric sphincters) and malin (pH 7.0), dehydrated in ethyl alcohol, cleared in xylol,
injected with distilled water (3 mL). The gastric juice was and embedded in paraffin. Four to six microns thick sections
then collected in sterilized tubes. The stomachs were were prepared and stained with hematoxylin and eosin for
opened longitudinally, washed with saline and examined examination of both fore and glandular parts of the stomach
under dissecting microscope for ulcer. The length of gastric according to a procedure outlined by (Carleton, 1976).
ulcer was measured and expressed as mean ± SD for each
group. The curative ratio was then calculated for each Statistical analysis
treated group according to the method described by Akhtar
and Ahmad (1995), using the following equation: Data were analyzed by means of one-way analysis with a
Curative ratio ðCRÞ ¼ ðLC LT=LCÞ 100; program at the Scientific Computer Center, Faculty of Home
Economics, Minufiya University, using the statistical ana-
where LC is the length of ulcer in positive control group lysis software (Duncan Multiple Range Test, one-way
and LT is the length of ulcer in treated group. ANOVA test) according to Armitage and Berry (1987). Data
are expressed as the mean ± SD, and P \ 0.05 was con-
Measurement of the volume of gastric juice sidered statistically significant.
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Med Chem Res
Table 1 Effect of garlic (Allium sativum L.) and cabbage (Brassica Table 2 Effect of garlic (Allium sativum L.) and cabbage (Brassica
oleracea var. capitata) extract at two doses on the length of gastric oleracea var. capitata) extract at two doses on the volume of gastric
ulcer in rats juice collected from stomachs of rats
Groups Aspirin and Doses Gastric ulcer CR Groups Aspirin and Doses Volume of DR
extracts (mg/kg B.Wt.) length (mm) (%) extracts (mg/kg B.Wt.) gastric juice (mL) (%)
Mean ± SD Mean ± SD
These results are in agreement with those obtained by (positive control group) at a dose of 200 mg/kg B.Wt.
Block (1985), who concluded that garlic has an important Results revealed that the mean length of gastric ulcer in
dietary and medicinal role. Most of its prophylactic and positive control was 0.8 ± 0.14 mL compared with
therapeutic effects are ascribed to specific oil- and water- 0.26 ± 0.05 mL in normal rats (negative control group).
soluble organosulfur compounds, which are responsible for Oral administration with garlic extract at a dose of 300 mg/
the typical odor and flavor of garlic. Meanwhile, Jain kg B.Wt. and cabbage juice at the same dose for 7 days to
(1993) reported that garlic oil preparation has a good anti- the positive control group (200 mg/kg B.Wt.) caused the
tuberculosis activity in guinea pigs with an intra-peritoneal highest decrease in the volume of gastric extract in rats. On
dose of 0.5 mg/kg. In addition, complete lack of resistance the other hand, oral administration with garlic extract at a
of bacteria to garlic has been found; as a result of this dose of 150 mg/kg B.Wt. and cabbage extract at the same
bactericidal activity of garlic, toxin production by the dose for 7 days to the same positive control group
bacteria is prevented. (200 mg/kg B.Wt.) caused the lowest decrease in the vol-
Similarly, Gowsala(2001) found in a study that garlic ume of gastric juice in rats. It was reported that the increase
juice has been used worldwide to fight bacterial infections. of acid secretion leads to gastric damage and is associated
Allium vegetables, particularly garlic (Allium sativum L.) with the greater acid back-diffusion, oxygen radical gen-
exhibits a broad antibiotic spectrum against both gram- eration, and lower mucosal glutathione and mucus pro-
positive and gram-negative bacteria. On the other hand, duction (Chen-Road and Su-Lin, 1997).
Thaly (1965) reported that cabbage is one of the most Gastric cancer is the major cancer in the developing
highly anti-inflammatory, antibacterial, antirheumatic, world and one of the top two worldwide. H. pylori are
heals tissues by encouraging cells to proliferate, a liver bacteria implicated in the etiology of stomach cancer
decongestant, and protects the stomach from gastric (Fuchs and Mayer, 1995). It was found that incidence of
hydrochloric acid. Fresh juices can be used as a diuretic stomach cancer is lower in individuals with a high intake of
and antiseptic for the urinary tract and to ease fluid reten- allium vegetables in developed and developing (high risk)
tion and to reduce or prevent kidney stones, arthritis, and countries, due to the antibiotic activity allium vegetables
gout. particularly garlic (Sivam et al., 1997). This is in agree-
ment with results obtained by (Cellini et al., 1996). They
Effect of garlic and cabbage extract on the volume tested 16 clinical isolates of H. pylori and showed 90 %
of gastric juice in rats inhibition of the isolates with aqueous garlic extract at
5 mg/mL. The concentration used in that study is the total
Shown in Table 2 are the data pertaining to the effect of weight of garlic per milliliter. However, calculations show
garlic and cabbage extract on the volume of gastric juice that the minimum inhibitory concentrations reported in the
obtained from rats with aspirin-induced gastric ulcer two studies are comparable. It is plausible that the
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Table 3 Effect of garlic (Allium sativum L.) and cabbage (Brassica Table 4 Effect of garlic (Allium sativum L.) and cabbage (Brassica
oleracea var. capitata) extract at two doses on the PH of gastric juice oleracea var. capitata) extract at two doses on the total acidity of
collected from stomachs of rats gastric juice collected from stomachs of rats
Groups Aspirin and Doses pH of IR Groups Aspirin Doses Total DR
extracts (mg/kg B.Wt.) gastric juice (%) and (mg/kg acidity (%) (%)
Mean ± SD extracts B.Wt.) Mean ± SD
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Med Chem Res
Table 5 Effect of garlic (Allium sativum L.) and cabbage (Brassica garlic was administered at a dose of 300 mg/kg B.Wt.; this
oleracea var. capitata) extract at two doses on the total bacterial dose caused the lowest T.B.C (0.31 9 103 C.F.U/mL).
count (T.B.C) of gastric juice in rats
Oral administration of cabbage at the same dose also
Groups Aspirin and Doses T.B.C Correction caused a decrease of T.B.C which was 3.6 9 102 C.F.U/
extracts (mg/kg C.F.U/mL (%) mL. These results are in agreement with those obtained by
B.Wt.)
Baibekov and Mavlian (1986) who found that chronic
Control –ve gastric ulcer was associated with a rise in the relative
1 – – 0.113 9 103f – amounts of parietal microflora. In the same time, Mahachai
Control ?ve et al., (2004) reported that infection with bacteria, espe-
2 Aspirin (Asp) 200 0.78 9 103a – cially H. pylori increases the risk of peptic ulcer recur-
Treated groups with plant extracts rences and bleeding complications.
3 (Asp) ? garlic 150 0.43 9 103bc 44.87 The antibacterial effect of aqueous garlic extract (AGE)
4 (Asp) ? garlic 300 0.31 9 103d 60.25 was investigated against Helicobacter pylori. Sixteen
5 (Asp) ? cabbage 150 0.46 9 103b 41.02 clinical isolates and three reference strains of H. pylori
6 (Asp) ? cabbage 300 0.36 9 103c 53.84 were studied. Two different varieties of garlic were used.
The concentration of AGE required to inhibit the bacterial
Means with different superscript letters in the column denote high
significant differences (P \ 0.01), while similar superscript letters
growth was between 2 and 5 mg mL-1. The concentration
denote non- significance for both AGE types, which inhibited 90 % (MIC90) of
isolates, was 5 mg mL-1. The minimum bactericidal con-
centration (MBC) was usually equal to or two fold higher
extracts at two doses on the total acidity of gastric juice in than minimum inhibitory concentration (MIC). Heat
rats. Data reveal that oral administration of garlic at a dose treatment of extracts reduced the inhibitory or bactericidal
of 300 mg/kg B.Wt., for 7 days after aspirin (200 mg/kg activity against H. pylori; the boiled garlic extract showed
B.Wt.) caused a significant decrease in total acidity of a loss of efficacy from two to four fold the values of MIC
gastric juice compared with positive control (0.41 ± 0.12 and MBC obtained with fresh AGE. The antibacterial
and 0.75 ± 0.1 for positive and negative control, respec- activity of garlic was also studied after combination with a
tively). Data presented also reveal that both aqueous plant proton pump-inhibitor (omeprazole) in a ratio of 250:1. A
extracts reduced the total acidity of gastric juice compared synergistic effect was found in 47 % of strains studied; an
with positive control. antagonistic effect was not observed Cellini et al. (1996).
Very few studies have dealt with chemically character- Didry et al. (1992) reported on the combinations of
ized garlic. The composition of garlic depends on the antibiotics and known antimicrobial natural products,
source, age, storage conditions, and type of processing and naphthoquinones ,and Allium extracts. The chessboard
method of consumption. Unfortunately, the different forms broth method was applied to assess the activity of these
of garlic are frequently referred to as ‘‘garlic’’ in both the combinations against aerobic and anaerobic bacteria. If no
lay and scientific literature. Additionally, it was showed antagonism was observed, the combinations studied lead
that the amount and composition of organosulfur com- from partial to total synergism, mainly against aerobic
pounds vary within the different strains of garlic (Lawson, bacteria. Gowsala (2001) demonstrated in vitro that H.
1996), and the problem is compounded by the volatile and pylori are susceptible to garlic extract at a fairly moderate
reactive nature of these compounds. Hence, there is a clear concentration. Even some antibiotic-resistant H. pylori
necessity for standardization of garlic preparations, espe- strains are susceptible to garlic. Clinical trials are necessary
cially for use in biological studies. to explore the possibility of using garlic as a low-cost
remedy against H. pylori.
Effect of garlic and cabbage extract on the total Garlic tested in this study had bactericidal and/or anti-
bacterial count (T.B.C) of gastric juice in rats adhesive effects on H. pylori. Ingestion of the plants with
anti-adhesive properties could provide a potent alternative
Displayed in Table 5 are the results pertaining to the effect therapy for H. pylori infection, which overcomes the
of garlic (Allium sativum L.) and cabbage (Brassica oler- problem of resistance associated with current antibiotic
acea var. capitata) extracts at two doses on the total bac- treatment (Mahony, 2005). Propolis and Zingiber officinal
terial count (T.B.C) of gastric juice in rats. It was found have been shown to be specifically targeted against H.
that gastric juice of ulcerated rats (positive control group), pylori strains, to possess anti-inflammatory, antioxidant
has higher T.B.C compared with normal rats (negative and antitumoral activity ,and to be used in traditional
control); 7.8 9 102 compared to 1.13 9 102 C.F.U/mL, medicine for the treatment of gastrointestinal ailments
respectively. It is evident that the best treatment was when Nostro (2006). Reuter et al. (1996) have recently reviewed
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Med Chem Res
the therapeutic effects of garlic, on the cardiovascular growth than in uninhibited controls, and (iv) an entry into
system, as antibacterial, anticancer, antioxidant, immuno- stationary phase at a lower culture density. Whereas DNA
modulatory, anti-inflammatory, hypoglycemic ,and hor- and protein syntheses showed a delayed and partial inhi-
mone-like effects. This review focuses on recent research bition by allicin, inhibition of RNA synthesis was imme-
on protective effects of garlic against H. pylori and other diate and total, suggesting that this is the primary target of
bacterial infections. allicin action (Feldberg et al., 1988).
There is extensive literature on the antibacterial effects Aspirin and related drugs (non-steroidal anti-inflamma-
of fresh garlic juice, aqueous and alcoholic extracts, tory drugs), alcohol, coffee (including decaf), and tea can
lyophilized powders, steam distilled oil ,and other com- aggravate or interfere with the healing of peptic ulcers.
mercial preparations of garlic. Fenwick and Hanley (1985) Smoking is also known to slow ulcer healing. Whether or
undertook a thorough review of the antibacterial effects of not an ulcer is caused by infection, patients with peptic
garlic and other allium vegetables up to mid-1984; more ulcer should avoid use of these substances (Allison et al.,
recently, the antibacterial effects of garlic have been 1992). Vitamin A is needed to heal the linings of mucous
reviewed by Reuter et al. (1996). Garlic has been reported membranes of the stomach and intestines. In one controlled
to inhibit several strains of gram ?ve and gram -ve bac- trial, vitamin A supplement facilitated healing in a small
teria. Noteworthy among the reported findings are as fol- group of patients with stomach ulcer. The amount used in
lows: (1) Garlic exhibits a broad antibiotic spectrum that study (150,000 IU per day) can be toxic and may also
against gram-positive and gram-negative bacteria. Entero- cause birth defects. Such a high dose should not be taken
toxic coli strains and other pathogenic intestinal bacteria, by a pregnant woman, by a woman who could become
which are responsible for diarrhea in humans and animals, pregnant, or by anyone else without careful supervision
are more easily inhibited by garlic than the normal intes- from a doctor (Patty et al., 1982). Objective evidence of
tinal flora (Caldwell and Danzer, 1988; Rees et al., 1993). ulcer healing from taking vitamin A has been reported by
Garlic is active even against organisms that have become the same research group. The effect of lower amounts of
resistant to antibiotics. The combination of garlic extracts vitamin A has not been studied in people with peptic ulcer
with antibiotics leads to partial or total synergism (Didry (Patty et al., 1984).
et al., 1992). Zinc is also needed for the repair of damaged tissue and
Diallyl thiosulfinates play an important role in the has protected against stomach ulceration in animal studies.
antibiotic activity of garlic. Hughes and Lawson (1991) In Europe, zinc combined with acexamic acid, an anti-
showed that the antimicrobial activity of garlic is com- inflammatory substance, is used as a drug in the treatment
pletely abolished when the thiosulfinates (e.g., allicin) are of peptic ulcers. In a small controlled trial, high amounts of
removed from the extract. Also, upon reduction of allicin to zinc accelerated the healing of gastric ulcers compared
diallyl disulfide, the antibacterial activity is greatly reduced with placebo. Some doctors suspect that such an excep-
(Reuter et al., 1996). Feldberg et al. (1988) reported that tionally high intake of zinc may be unnecessary, suggesting
allicin exhibits its antimicrobial activity mainly by imme- instead that people with ulcers wishing to take zinc sup-
diate and total inhibition of RNA synthesis, although DNA plements use only 25 to 50 mg of zinc per day. Even at
and protein synthesis are also partially inhibited, suggest- these lower levels 1–3 mg of copper per day must be taken
ing that RNA is the primary target of allicin action. The to avoid copper deficiency that would otherwise be induced
structural differences of the bacterial strains may also play by the zinc supplement (Jimenez et al., 1992).
a role in the bacterial susceptibility to garlic constituents.
The cell membrane of Escherichia coli contains 20 % Effect of garlic and cabbage juice on relative organs
lipid, whereas that of Staphylococcus aureus contains only weight in rats
2 % lipid. The lipid content of the membranes will have an
effect on the permeability of allicin and other garlic con- Organs weight analysis revealed that oral administration of
stituents. On the basis of this hypothesis, it is interesting to water garlic (Allium sativum L.) and cabbage (Brassica
attribute the difference in susceptibility we observed oleracea var. capitata) juice significantly decreased the
between gram-negative H. pylori (40 lg/mL) and gram- liver, spleen ,and kidneys weights and did not significantly
positive Staphylococcus aureus ([160 lg/mL) to garlic change the heart and lungs weights.
extract (Sivam et al., 1997). A pattern of inhibition char-
acterized by: (i) a lag of approximately 15 min between Histopathological results
addition of allicin and onset of inhibition, (ii) a transitory
inhibition phase whose duration was proportional to allicin Examined sections of control rat showed the normal his-
concentration and inversely proportional to culture density, tology of stomach, which consists of mucosa, submucosa
(iii) a resumed growth phase which showed a lower rate of musculosa, and serosa (Fig. 1). On the other hand, stomach
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Med Chem Res
Fig. 2 Stomach of rat from (control ?ve) showing ulcer of the Fig. 4 Stomach of rat from group 4 (garlic 300 mg/kg B.Wt.)
glandular stomach characterized by marked necrosis and sloughing of showing no histopathological alterations (H and E 9200)
lamina epithelial associated with leucocyte cells infiltration in the
necrotic glands and hemorrhage (H and E 9200)
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