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| ORIGINAL ARTICLE |
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| Year : 2016 | Volume
: 9
| Issue : 1 | Page : 7-12 |
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Anti-Giardia lamblia activity of ginger (Zingiber officinale) extract in an improved modified axenic culture
Ekhlas H. A. Abdel-Hafeez MD, PhD, Assistant Professor 1, Azza K Ahmad1, Amany M Kamal1, Usama S Belal1, Nawras M El-Saghier Mowafy2
1 Department of Parasitology, Faculty of Medicine, Minia University, Minia, Egypt
2 Department of Parasitology, Faculty of Medicine, Minia University, Minia, Egypt; Department of Medical Parasitology, College of Medicine, Female Sector, Umm Al-Qura University, Makkah, KSA
| Date of Submission | 27-Jun-2015 |
| Date of Acceptance | 18-Oct-2015 |
| Date of Web Publication | 25-Oct-2016 |
Correspondence Address:
Dr. Ekhlas H. A. Abdel-Hafeez
Department of Parasitology, Faculty of Medicine, Minia University, Minia 61519
Egypt
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/1687-7942.192990
Background
Giardiasis is an important common intestinal infection that occurs as a result of ingestion of cysts of the protozoan parasite Giardia lamblia. Several medications are available to treat giardiasis. Metronidazole and other chemical drugs currently used for treatment cause side effects, whereas ginger has been used for centuries as a herbal medicine, without harmful side effects.
Objective
With regard to the above-mentioned properties of ginger we were prompted to evaluate its anti-Giardia activity, as compared with nitazoxanide (NTZ) and phosphate buffer saline (PBS) as controls, and to establish a G. lamblia axenic culture that yields a large number of trophozoites.
Materials and methods
Fresh clinical isolates of G. lamblia were obtained from different patients with acute giardiasis. Trophozoites were cultured using Stone’s modification of Locke’s solution as an axenic culture medium modified by supplementing with bovine bile and heat-inactivated bovine serum. Ginger extract was prepared to give a final concentration of 20 mg/ml. In vitro assessment of effect of ginger was carried out after 24 and 48 h. For post-treatment evaluation, the viability of G. lamblia trophozoites was tested by their morphological criteria and dye staining (eosin stain 0.01%).
Results
The culture yielded a rich growth of G. lamblia trophozoites. Dead trophozoites stained pink with eosin and showed loss of morphological criteria. NTZ treatment significantly lowered the number of the parasites after 48 h (mean: 42.5±3.53/ml; P≤0.002), with a reduction rate of 92.93%, compared with PBS. Ginger treatment significantly lowered the number of the parasites after 48 h (mean: 55±7.07/ml, P≤0.004), with a reduction rate of 94.4%, compared with PBS.
Conclusion
The present study confirmed that ginger extract is equally active against G. lamblia as NTZ. More research studies are needed to highlight the physiological and molecular mechanisms of action of ginger and provide more scientific evidence of its effectiveness. Moreover, this simple G. lamblia axenic culture medium proved beneficial for evaluation of the susceptibility of isolates to antiparasitic drugs. Keywords: Giardia lamblia, ginger, in vitro effects, nitazoxanide
How to cite this article:
Abdel-Hafeez EH, Ahmad AK, Kamal AM, Belal US, El-Saghier Mowafy NM. Anti-Giardia lamblia activity of ginger (Zingiber officinale) extract in an improved modified axenic culture. Parasitol United J 2016;9:7-12 |
How to cite this URL:
Abdel-Hafeez EH, Ahmad AK, Kamal AM, Belal US, El-Saghier Mowafy NM. Anti-Giardia lamblia activity of ginger (Zingiber officinale) extract in an improved modified axenic culture. Parasitol United J [serial online] 2016 [cited 2023 Dec 3];9:7-12. Available from: http://www.new.puj.eg.net/text.asp?2016/9/1/7/192990 |
| Introduction | |  |
Giardia lamblia is one of the most common intestinal flagellates that infects a wide array of mammalian hosts [1]. Infection is characterized by colonization of the small intestine by trophozoites. The symptoms of giardiasis include abdominal cramps, nausea, and acute or chronic diarrhea, with malabsorption. In addition, failure of children to thrive may occur in both subclinical and symptomatic disease [2]. Untreated giardiasis in children can last several months and is characterized by continued exacerbations of diarrheal symptoms. Chronic illness, malabsorption of fat, lactose, vitamin A, and vitamin B12, and growth deficiency are also reported [3],[4],[5]. Because the trophozoites are noninvasive, the variation in clinical outcome of giardiasis was questioned [6]. However, host factors (such as immune status, nutritional status, and age), as well as differences in the virulence and pathogenicity of Giardia assemblages, are recognized as important determinants for the severity of infection [7]. The prevalence rates of G. lamblia in humans range from 2 to 7% and from 20 to 30% in developed and developing countries, respectively [2]. Of the many protozoa species associated with diarrhea in HIV-infected patients [8], G. lamblia has been reported in 8–50% of cases worldwide [9]. Many culture media have been developed to facilitate the in vitro growth of G. lamblia. One of the first axenic cultures used was HSP-1 medium supplemented with heat-inactivated human serum [10]. TYI-S-33, which was first developed for axenic culture of Entamoeba histolytica trophozoites, was later supplemented with bovine serum for axenic culture of G. lamblia trophozoites [11]. The efficacy of many drugs against G. lamblia trophozoites cultured axenically has been published [12],[13].
Nitazoxanide (NTZ) is a relatively new antimicrobial drug that is active against G. lamblia, in addition to E. histolytica, Cryptosporidium spp., Trichomonas vaginalis, and some bacteria including Helicobacter pylori [14],[15]. It is proposed to work as a noncompetitive inhibitor of the pyruvate–ferredoxin oxidoreductase reaction [16], perhaps by inhibiting the binding of pyruvate to the thiamine pyrophosphate cofactor [15]. Consequently, NTZ proved effective as an antiprotozoan drug [17]. Three-day courses of NTZ have been studied in children, yielding response rates of about 70–80%, when given at a dose of 100–500 mg twice daily for 3–7 days [18]. Therapeutic failure occurred more frequently in human giardiasis, due to reinfection or parasite resistance to metronidazole (MTZ) and/or NTZ-related compounds [19]. Development of resistant strains indicates the importance of using alternative traditional medicines that have many positive aspects [20],[21].
Ginger (Zingiber officinale) is known worldwide as a spice and flavoring agent [22]. It has an antioxidant effect that enhances the immune response, allowing the body to naturally fight infections. Moreover, ginger has other activities that may help in parasite clearance, such as its ability to increase digestive fluids and absorb and neutralize toxins and stomach acid. Furthermore, ginger increases bile secretion, as well as the action and tone of the bowels [22]. Few investigations were conducted on the anthelmintic activity of ginger and its constituents [23]. Lin et al. [24] showed that hexahydrocurcumin, a constituent isolated from ginger, might be used as a larvicidal agent against Angiostrongylus cantonensis. In another publication, the same investigators [25] investigated its anthelmintic activity against the nematode worm Anisakis simplex, and Mostafa et al. [26] demonstrated its antischistosomal activities.
The present research was carried out to assess the in vitro effects of ginger on G. lamblia, in the presence of a modified axenic culture to yield large numbers of trophozoites of G. lamblia.
| Materials and methods | | |
This case control study was conducted during the period from April 2015 to June 2015 in the Parasitology Department, Faculty of Medicine, Minia University, Minia, Egypt.
Parasite preparation
Fresh clinical isolates of G. lamblia were obtained from different patients with acute giardiasis. Stool samples from different patients were delivered to the Parasitology Department, Minia University, for examination. Positive samples for G. lamblia trophozoites were immediately cultured using 50 mg of feces for each culture tube. Wet mount was performed to confirm diagnosis of these isolates.
Axenic culture medium
The culture medium was prepared using Stone’s modification of Locke’s solution [27], which is the main component of Locke’s egg medium. Locke’s solution composed of various salts, including 600 mg/ml bovine bile salts (Sigma-Aldrich, St. Louis, Missouri, USA), with a final pH adjusted to 6.8–7, was sterilized by autoclaving for 20 min at 121°C and stored in 500 ml bottles at 4°C until use. Under sterile hood conditions, 10% heat-inactivated (56°C for 30 min) bovine serum (Sigma-Aldrich, St. Louis, Missouri, USA), 100 UI/ml penicillin, and 100 μg/ml streptomycin (Sigma-Aldrich, St. Louis, Missouri, USA) were added to the cooled medium [28]. Before use, the medium was distributed in 5 ml sterile screw-capped tubes. The culture was used to maintain the trophozoites for longer periods of time by supplementing Locke’s solution with bovine bile instead of homogenized egg and with heat-inactivated bovine serum instead of horse serum, both of which were documented as growth factors for G. lamblia trophozoites [11],[29]. This successfully maintained the trophozoite growth for more than 1 month.
Culture of G. lamblia trophozoites
A 50 mg sample of positively detected stool sample for G. lamblia trophozoites was inoculated immediately in the axenic medium and incubated at 37°C for 2–3 days. The cultures were screened for G. lamblia with standard light microscopy every 12 h and subcultured every 72 h in fresh media [30].
Preparation of ginger extract
Ginger extract was prepared as previously described [31],[32]. The concentration of ginger extract was adjusted to a final concentration of 20 mg/ml.
In vitro assessment of effect of ginger
In vitro susceptibility assays were performed. In addition to the ginger extract, NTZ was used as a positive control at a concentration of 500 mg/ml. PBS was used as a negative control. Six tubes were prepared, each containing 1×103 trophozoites/ml media. NTZ, PBS, and ginger were added in the calculated doses. Two sets, each composed of three tubes, were prepared and incubated at 37°C, the first for 24 h and the second for 48 h. At the end of each incubation period, the supernatant from each tube was carefully removed without disturbing the pellet at the bottom. The sediment was then gently agitated to obtain a uniform distribution of trophozoites. The parasite numbers were determined by counting in a hemocytometer under a light microscope. The procedure was repeated three times.
Evaluation of trophozoite viability
Trophozoite viability was evaluated microscopically in eosin-stained (0.01%) preparations [33]. In addition, their morphological criteria were observed.
Statistical analysis
Statistical significance was determined using t-tests (Mann–Whitney). Data were presented as means±SD using SPSS (version 15.8 for Windows; SPSS Inc., Chicago, Illinois, USA), with P-value less than 0.05 considered significant.
| Results | | |
Cultured fecal samples of G. lamblia trophozoites in Stone’s modification of Locke’s solution supplemented with bovine bile and heat-inactivated bovine serum produced profuse numbers of trophozoites (1–2×103/ml) at 48 h. The viable forms appeared pear-shaped ([Figure 1]a) and showed the characteristic jerky rotational movement of the projecting flagellae. The viable forms also maintained their ‘clown face’ look with two nuclei outlined by adhesive discs above dark median bodies that form the clown’s mouth [34]. | Figure 1 Photomicrographs of Giardia lamblia trophozoites (arrows) using light microscopy (×1000). Unstained viable G. lamblia trophozoites in the culture treated with PBS (a). Stained dead trophozoites in the culture treated with ginger (b) and nitazoxanide (NTZ) (c).
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The treatment of cultured trophozoites with PBS, ginger, and NTZ showed variable features of mortality more evident with ginger and NTZ ([Figure 1]b and [Figure 1]c, respectively). Loss of viability of trophozoites was portrayed as loss of the characteristic pear shape, immobility, loss of caudal flagellae, and of their refractory quality. Dead trophozoites stained red with 0.01% eosin. Treatment of cultured trophozoites with ginger and NTZ significantly reduced the viability compared with PBS. NTZ treatment significantly (P<0.002) lowered the number of parasites/ml after 48 h (mean: 42.5±3.53/ml) ([Figure 2] and [Table 1]). The reduction rate after 48 h compared with PBS was 92.93%. Ginger treatment significantly (P<0.004) lowered the number of parasites/ml after 48 h (mean: 55±7.07/ml). The reduction rate after 48 h compared with PBS was 94.4% ([Figure 2] and [Table 1]). | Figure 2 Giardia lamblia trophozoite intensity in the culture treated with phosphate buffered saline (PBS), nitazoxanide (NTZ), and ginger at different intervals. Black columns represent the culture treated with PBS after 24 and 48 h. Grey columns represent the culture treated with NTZ after 24 and 48 h. White columns represent the culture treated with ginger after 24 and 48 h. Data are expressed as parasite load/ml.
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 | Table 1 Giardia lamblia parasite intensity in the culture treated with phosphate buffer saline, nitazoxanide, and ginger at different intervals
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| Discussion | | |
The use of culture methods for intestinal protozoa allows study of their biology and growth rate, investigation of their virulence factors, susceptibility to new drugs, and development of resistant strains [35]. In this study, we used an axenic culture medium (Stone’s modification of Locke’s solution), which is a solution of multiple salts and heat-inactivated serum as a source of lipids, to improve growth of the parasite. Using Stone’s modification of Locke’s solution with bovine bile instead of homogenized egg and with heat-inactivated bovine serum instead of horse serum was the modified procedure used in our study. This modification was for economic purposes and to facilitate the in vitro susceptibility studies. Supplementing the culture medium with bovine serum instead of horse serum was described in the preparation of modified PEHSP medium [36]. It was possible to maintain the parasites in axenic condition at 37°C with subculture every 72 h for more than 30 days.
Despite the recognition of G. lamblia as an important human pathogen causing diarrheal illness throughout the world, relatively few agents have been used in therapy. The greatest clinical experience is with the nitroimidazole drugs such as MTZ, tinidazole, and ornidazole, which are highly effective. A 5-day to 7-day course of MTZ can be expected to cure over 90% of individuals, and a single dose of tinidazole or ornidazole will cure a similar proportion [37]. Relevant side effects, treatment failures, and an increasing incidence of drug resistance are associated with current drugs. Recently, fumagillin, carbadox, and tioxidazole were identified with equal or better anti-G. lamblia activities compared with MTZ, as determined in in vitro assays. Moreover, omeprazole was effective in vitro against drug-resistant and drug-sensitive strains. Further studies are still needed for evaluation of some of the alternative treatments [38],[39].
In this research, we evaluated the in vitro effect of the dietary herb, ginger, on G. lamblia trophozoite viability at 24 and 48 h. NTZ was used as a suitable alternative to MTZ for its known antigiardial effect. MTZ significantly reduced the number of G. lamblia trophozoites at 24 h (P=0.002) and at 48 h (P=0.004). Ginger significantly reduced the number of G. lamblia trophozoites at 24 h (P=0.002) and at 48 h (P=0.004). This result indicates that ginger has an effect similar to that of NTZ in suppressing the growth of the parasite (P=0.12 at 48 h). The reduction rates after 48 h compared with PBS was 93.33%. Our results confirm previously reported antigiardial activity of ginger extract [40]. In brief, the researchers evaluated the antigiardial activity of chloroform, methanol, and water extracts of 12 medicinal plants (39 extracts, (including ginger), commonly used as self medication by AIDS patients in southern Thailand. The plant extracts and MTZ were incubated with 2×105 trophozoites of G. lamblia/ml of growth medium in 96-well tissue culture plates under anaerobic conditions for 24 h. The cultures were examined with an inverted microscope and the minimum inhibitory concentration and the IC50 value for each extract were determined. The chloroform extracts from ginger were classified as ‘active’ with an IC50 greater than 100 µg/ml, proving that extracts of this medicinal plant have potential for use as therapeutic agent against G. lamblia infections. The same researchers reported that ginger also exhibited antiamebic activity [40]. In the traditional system of medicine in India, a formulation was prescribed for intestinal disorders. The in vitro amebicidal activity was studied to determine the minimal inhibitory concentration values of all constituting extracts, as well as the whole formulation. The formulation had a minimal inhibitory concentration of 1000 µg/ml compared with 10 µg/ml for MTZ. There were varying degrees of inhibition of DNase, RNase, aldolase, alkaline phosphatase, acid phosphatase, α-amylase, and protease enzyme activities of crude extracts of axenically cultured amoebae [41].
Moreover, ginger is effective in vitro against Blastocystis spp. significantly (P<0.002) lowering the number of the cultured forms after 48 h (mean: 335±7.07/ml) [32] and it is effective in vivo in infected mice, reducing the shedding of cysts significantly compared with the infected untreated group. In addition, histopathological examination revealed that Blastocystis was frequently observed within the lumen, at the tip of the epithelium, and/or infiltrated in an enterocyte in the infected group without treatment compared with the infected treated one [42].
Ginger has been reported as an antioxidant [43], potent antibacterial [44],[45], and potent antifungal [46]. Furthermore, many studies have shown that ginger exhibits anthelmintic activity against Dirofilaria immitis [47], Anisakis larvae [48], Schistosoma mansoni [49], and gastrointestinal nematodes [23]. Furthermore, Moazeni and Nazer [50] have reported that ginger has an in vitro lethal effect on protoscolices of hydatid cysts from sheep liver.
| Conclusion | | |
The present study confirmed that ginger extract is equally active against G. lamblia as NTZ. More research studies are needed to highlight the physiological and molecular mechanisms of action of ginger and provide more scientific evidence of its effectiveness. Moreover, this simple G. lamblia axenic culture medium proved beneficial for evaluation of the susceptibility of isolates to antiparasitic drugs.
Acknowledgements
The authors thank Professor Dr Nabil S. Gabr, Professor of Parasitology, Faculty of Medicine, Minia University, for providing excellent technical expertise. They also appreciate his generous cooperation.
Authors contribution
Authors contributed equally to the research.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1]
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