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1 CHAPTER II LITERATURE REVIEW 2.1 GIARDIA I TESTI ALIS Introduction Giardia is an ubiquitous enteric flagellate protozoan parasite affecting humans and a range of domestic and wild mammals. The infection is transmitted by the ingestion of cysts, the infective stage, directly through faecal-oral contact or indirectly through contaminated water or food. Human giardiasis is a common cause of parasitic gastroenteritis and is a major health concern worldwide. Clinical manifestations vary from asymptomatic infection to acute diarrhoeal illness (Astiazara n-garcı a et al. 2000; Meyer and Jarroll, 1980). Although giardiasis is usually self-limited, it can develop into chronic and life-threatening disease. Chronic giardiasis in the early childhood has been significantly associated with malnutrition disorders (Gendrel et al. 2003). In developed countries, G. intestinalis has been considered as a re-emerging infectious pathogen because of its role in outbreaks of diarrhoea in day-care centres and in foodborne and waterborne outbreaks (Thompson, 2000). In developing nations, in Asia, Africa, and Latin America, approximately 200 million people have symptomatic giardiasis with 500,000 new cases each year (WHO, 1996).

2 Genotyping and phylogenetic analyses have shown that G. intestinalis comprises at least seven deeply rooted lineages, designated as Assemblages A G. Assemblage A and assemblage B, the zoonotic potential assemblages, have a broad host range including human and animals. The other assemblages, assemblages C-G, appear to be hostadapted and have not represented potential public health concerns (Monis et al. 1999) Morphology G. intestinalis is an eukaryotic organism which has a distinct nucleus and nuclear membrane, cytoskeleton, and endomembrane system. In contrast, it lacks nucleoli and peroxisome organelles that are nearly universal in eukaryotes. In addition, G. intestinalis is anaerobic, lacking mitochondria or any of the components of oxidative phosphorylation (Thompson et al. 1994). A. Trophozoite Trophozoite is pear-shaped and is approximately 12 to 15 µm in length and 5 to 9 µm in width. The cytoskeleton includes a median body, four pairs of flagella and a ventral disk. Trophozoite has also two nuclei without nucleoli that are located interiorly and symmetrically to the long axis (Figure 2.1). Both nuclei are transcriptionally active containing approximately the same number of genes and the same amount of DNA (Kabnick and Peattie, 1990) and they replicate at the same time (Wiesehahn et al. 1984). Trophozoites inhabit the small intestine of their host attaching by ventral adhesive disk to the intestinal wall. 7

3 B. Cyst Cysts are the infective stage of G. intestinalis. Cysts are approximately 5 x 7-10 µm in dimension, covered by a thick wall and contain four nuclei (Figure 2.1). The cyst wall is about 0.3 to 0.5 µm in thickness and composed of an outer filamentous layer and an inner membranous layer with two membranes Life cycle Life cycle of G. intestinalis species includes two major steps; excystation and encystation. The excystation starts when susceptible host ingests the cysts (infective stage). After ingestion, cysts are exposed to the acidic environment of the stomach and pass to the proximal small intestine where they excyst and develop to trophozoites. The trophozoite is the vegetative form which causes the disease (pathogenic stage). When trophozoites are exposed to the jejunum and duodenum environment, they are encysted and passed in the faeces, allowing the completion of the life cycle by infecting a new host (Figure 2.1). A. Excystation Excystation occurs in the proximal small intestine after passage through the acidic environment of the stomach. After the initiation of excystation, one or two pairs of preventral flanges develop into the ventral flange (Hetsko et al. 1998). The peritrophic space and the preventral flange enlarge as the emerging trophozoite separates from the cyst wall. Externally, the emergence of flagella through the opening cyst wall is followed by the entire trophozoite (Buchel et al. 1987). The oval trophozoite becomes more rounded and then undergoes cytokinesis, so that two trophozoites are formed from one cyst. 8

4 B. Encystation Encystation processes occur in the jejunum and factors promoting the encystation have been controversial. In vitro studies formed cysts by exposing trophozoites to mildly alkaline ph of 7.8 and conjugated bile salts plus fatty acids (Gillin et al. 1988). In contrast, cholesterol was reported as inhibiting factor. Encystation can be divided into two phases; early and late phases. The early phase consists of the intracellular synthesis and transport of cyst wall components. The late phase of encystation consists of the appearance on the trophozoite plasmalemma of sites for initiation of the assembly of cyst wall filaments followed by the assembly of the filamentous portion of the cyst wall. 9

5 Organisms in man Multiplication by binary fission in small intestine Excystation in upper small intestine INGESTED disintegrates Trophozoites on mucosa of small intestine cyst EXCRETED cyst Trophozoite Organisms in external environment Excreted form diagnostic stage Figure 2.1 Life cycle and morphology of Giardia intestinalis Source: Meyer (1974) 10

6 2.1.4 Taxonomy Giardia was used as a genus name for the first time. In 1888, the name Lamblia intestinalis was suggested (Blanchard, 1888) and changed to Giardia duodenalis in 1902 (Stiles, 1902). Subsequently, Kofoid and Christiansen proposed the names Giardia lamblia in 1915 and Giardia enterica in 1920 (Kofoid and Christiansen, 1915; 1920). Giardia intestinalis, Giardia duodenalis and Giardia lamblia are currently used as synonyms and there is no taxonomic basis on which to justify using any name. Based on morphological differences using light microscopy, Giardia has been classified into Giardia agilis (long and slender), Giardia intestinalis (pear-shaped), and Giardia muris (nearly round) (Filice, 1952). The application of electron microscopy has assigned additional species based on differences from G. intestinalis which are Giardia ardeae, Giardia psittaci, and Giardia microti (Erlandsen et al. 1990; Erlandsen and Bemrick, 1987; Feely, 1988). Further genetically distinct assemblages, assemblage A- G, within G. intestinalis have also been reported which are likely to represent different species (Table 2.1). Furthermore, assemblage A consists of isolates that can be grouped into two distinct clusters; assemblage A-I and assemblage A-II. Assemblage A-I may be implicated in zoonotic transmission as it has a broad range of hosts. In contrast, assemblage A-II has been considered as human isolate. Assemblage B comprises a genetically diverse group of predominantly human and animal isolates (Thompson et al. 2000). Assemblages A and B correspond, respectively, to the Polish and Belgian genotypes that were previously reported in Europe (Homan et al. 1992) and groups (1/2) and group 3, stated in north America (Nash and Mowatt, 1992; Nash and Keister, 1985; Nash et al. 1985). 11

7 Table 2.1 Giardia species and Giardia intestinalis assemblages and their hosts (Modified from Cacciὸ et al. (2005)) Giardia species Host Giardia intestinalis Assemblage A Assemblage B Assemblage C & D Assemblage E Assemblage F Assemblage G Giardia muris Giardia agilis Giardia ardeae Giardia psittaci Giardia microti Human, livestock Human Dog Cattle, other hoofed livestock Cats Rats Rodents Amphibians Herons Psittacine birds Muskrats 12

8 2.1.5 Pathology and clinical manifestation Giardiasis is most often asymptomatic. Symptomatology of giardiasis differs from person to person, depending on factors such as number of cysts ingested, duration of infection, host immune status and perhaps parasitic factors (Faubert, 2000). Acute giardiasis, which lasts 3 or 4 days, is characterized by nausea, anorexia and some times low-grade fever and chills followed by symptoms that may include explosive, watery and foul-smelling diarrhoea. Upper or mid-epigastric cramps may also occur. Although some acute infection is self-limited, chronic infection may develop which may last for 2 or more years. During this chronic phase, patients may suffer intermittent diarrhoea and persistent or recurrent mild to moderate symptoms. Chronic giardiasis in early childhood is associated with poor cognitive function and failure to thrive (Berkman et al. 2002). Giardiasis causes malabsorption and significant association of giardiasis with protein energy malnutrition and micronutrient deficiency particularly iron deficiency and vitamin B12 deficiency has been reported (Gendrel et al. 2003). The pathogenesis of Giardia is still not clearly understood and appears to involve villous atrophy and damage to the microvilli. These changes may result from interaction between parasite products and host inflammatory and immunological responses (Scott et al. 2000; 2004; Rosenthal, 1999). Villous atrophy and microvilli damage are correlated with brush border enzyme deficiencies and impaired absorption which return to the normal level of activity after the infection disappears (Buret et al. 1990a; 1991). G. intestinalis assemblages have been shown to differ in their pathogenicity, virulence and other biological characters. However, few studies have correlated between G. 13

9 intestinalis genotypes and clinical symptoms. Homan and Mank, (2001) observed that persons with intermittent diarrhoeal complaints were only infected with isolates belonging to Assemblage A, whereas those with persistent diarrhoeal complaints were only infected with isolates belonging to Assemblage B. This finding was supported by a recent study, carried out in Ethiopia, which indicated that symptomatic infection was significantly more associated with assemblage B than with assemblage A (Gelanew et al. 2007). In contrast, Read et al. (2002) stated a strong correlation between assemblage A and diarrhoea in children under 5 years of age. The significant association between assemblage A and symptoms has also been reported in India (Paintlia et al. 1998). Other studies, carried out in Turkey and Bangladesh, showed that assemblage A was significantly associated with diarrhoeal symptoms (Haque et al. 2005; Aydin et al. 2004). It must be noted that the association of an assemblage with diarrhoea does not necessary mean that this assemblage is more virulent than the assemblage which was not associated with diarrhoea. Although chronic giardiasis is not always associated with the presence of diarrhoea, it has been significantly associated with malnutritional disorders, particularly among those children in community setting (Gendrel et al. 2003) Epidemiology Prevalence and demographic distribution G. intestinalis has a global distribution and is the most common intestinal protozoan parasite of humans in developed countries. Prevalence varies between 2% and 5% in industrialized countries and up to 20 30% in developing countries. In Asia, Africa and Latin America, about 200 million people have symptomatic giardiasis with some 500, 000 new cases reported each year (WHO, 1996). The prevalence of G. intestinalis 14

10 assemblages A and B isolated from humans, vary from one country to another (Table 2.2). Children have been reported to be significantly at higher risk of giardiasis worldwide (Laupland and Church, 2005; Norhayati et al. 1998; Lim et al. 1997). The possible reasons for this age dependent pattern are probably related to children's habits (e.g. sharing things among themselves, putting objects into the mouth) and exposure to sources of faecal contamination because of their poor personal hygiene practices. Another reason for higher infections in children may also be related to the lack of effective immunity. Giardiasis also does not seem to be gender dependent and most studies have reported no significant difference between male and female and Giardia infection (Norhayati et al. 1998; Lim et al. 1997). However, some studies stated that males were at slightly higher risk for developing Giardia infection compared to females (Laupland and Church, 2005; Clavel et al. 1996; Addiss et al. 1992). 15

11 Table 2.2 Prevalence of assemblage A and assemblage B isolated from human faecal samples worldwide Assemblages Country N A B Mixed References USA (100) - - Van Keulen et al USA 2-2 (100) - Sulaiman et al UK (22%) 843 (71%) 77 (7%) Cacciὸ et al Italy (43%) 10 (27%) 11 (30%) Lalle et al Italy (80%) 6 (20%) - Caccio` et al. 2002b Japan 3 2 (67%) 1 (23%) - Abe et al Australia 23 6 (26%) 11 (74%) - Read et al Australia 23 7 (30%) 16 (70%) - Read et al Albania (45%) 12 (55%) - Berrilli et al Turkey (43%) 25 (57%) - Aydin et al Mexico (100%) - - Eligio-García et al India (100%) - Sulaiman et al Ethiopia (53%) 13 (22%) 15 (25%) Gelanew et al Peru 25 6 (24%) 19 (76%) - Sulaiman et al N = the total of genotyped samples 16

12 Transmission A. Person-to-person transmission In environments where the infection rate of G. intestinalis is high with poor personal hygiene, faecal-oral is the most common route of transmission (Núñez et al. 2003). In developed countries, large numbers of children are placed in day care centres due to social and workforce changes. Diarrhoea is a common disease in these types of institutes and Giardia has been considered one of the most common faecal-oral transmitted pathogens causing diarrhoea especially among children who are not toilettrained and toddlers (Thompson, 1994). Day care centres may also act as focus points for Giardia infection which may spread to day care staff, parents and community; 20-25% of staff and family who were in a close contact with the infected children have been reported to be asymptomatically infected (CDC, 1995). Person-to-person transmission has also been suggested in developing countries and disadvantaged communities in developed countries. In Australian aboriginal communities, the prevalence rate of giardiasis is 50% among children under five years causing acute or persistent diarrhoea. In these communities, overcrowding together with poor hygiene are factors which enhance the transmission (Reynoldson et al. 1998; Meloni et al. 1993). Furthermore, an epidemiological study identified large family size as risk factor of giardiasis in Malaysia, hence, supporting the faecal-oral transmission (Norhayati et al. 1998). 17

13 B. Waterborne transmission G. intestinalis is a waterborne protozoan which has been responsible for 130 reported waterborne outbreaks worldwide. In the United States of America, giardiasis caused approximately 80 waterborne outbreaks in the period from 1955 to 2001, affecting approximately 85,000 cases (Karanis et al. 2007). In Canada, fourteen waterborne outbreaks of giardiasis have been reported since 1981 (Karanis et al. 2007). G. intestinalis has some features that enhance the possibility of the waterborne transmission; its cysts are sufficiently small to penetrate the physical barriers of water treatment and are insensitive to some disinfectants used in the water industry and they can survive in water for 1-2 months. Low host specificity and the ability of G. intestinalis to infect wide spectrum of domestic and wildlife animals increases the sources of water contamination. The large numbers of excreted cysts by infected hosts and low infectious dose of cysts are other factors that increase the risk of waterborne transmission. Genotyping of Giardia isolated from waterborne outbreaks could help water health authorities in determining the sources of infection (Cocciὸ et al. 2005). C. Zoonotic transmission Zoonotic transmission of G. intestinalis is in the forefront of the public health interest and has been controversial for several years. A number of studies carried out in north America and Australia have shown high prevalence of G. intestinalis in dairy calve, with infection rate of 100% in some animal groups (O'Handley et al. 2000; 1999; Xiao and Herd, 1994). These high rates raise question about the potential of zoonotic transmission. Although the majority of isolates were genetically identical and conformed to the livestock genotype (assemblage E), small herds of animals may 18

14 harbour assemblage A, the most zoonotic genotype affecting human. Buret et al. (1990b) isolated G. intestinalis from domestic ruminants which was morphologically and antigenically similar to G. intestinalis isolated from human. Furthermore, Traub et al. (2005) found that horses can be infected with assemblages AI and AII, constituting a potential zoonotic risk to humans. Domestic dogs are susceptible to infection with both host-adapted (G. intestinalis assemblage C) and zoonotic Giardia genotypes. A molecular epidemiological study, carried out in Giardia endemic area in India where dogs are living closely with human, isolated similar genotypes from human and dogs, thus supporting the zoonotic transmission (Traub et al. 2004). Although wildlife is commonly infected with zoonotic Giardia genotypes, there is little evidence to support the implication of these animals as a source of human disease. It would seem that wildlife, particularly aquatic mammals have been infected from the water contaminated with Giardia cysts from human origin or domestic animals. This suggestion has been confirmed by genotyping studies indicating that the source of Giardia infection in beavers was likely to be from human origin (Sulaiman et al. 2003; Appelbee et al. 2002). In summary, the risk of zoonotic transmission should be from those zoonotic assemblages A and B that can infect human and animal (Table 2.3). The host-adapted assemblages such as assemblages C and D (dog), assemblage G (rats), assemblage F (cat), and assemblage E (calves) may not represent any risk to human as they have not been isolated from human (Thompson et al. 2000; Ey et al. 1997). Furthermore, the isolation of identical genotypes from human and animal is not a conclusive evidence of 19

15 zoonotic transmission unless the identical genotypes are isolated from the same endemic focus and direct experimental cross-transmission of these Giardia genotypes between humans and animals is carried out. However, direct experimental cross-transmission studies have been difficult to design because of the uncertainty about the Giardia-free status of experimental animals and the common use of high doses of cysts that are unlikely to represent natural infection (Thompson, 2004). 20

16 Table 2.3 Giardia intestinalis assemblages isolated from animals worldwide Assemblages Animals Country A B C D E F References Dogs USA Sulaiman et al Canada van Keulen et al Japan a Itagaki et al Italy b Berrilli et al Italy c Lalle et al Australia Read et al Mexico Eligio-García et al Calves USA Trout et al Canada Appelbee et al Canada van Keulen et al Italy d Lalle et al Italy Berrilli et al Australia Read et al Japan Itagaki et al Cats Canada van Keulen et al Italy Berrilli et al Australia Read et al Japan Itagaki et al Horses USA Traub et al Sheep Italy Giangaspero et al Monkey Japan Itagaki et al Beavers USA Sulaiman et al Muskrats USA Sulaiman et al Rabbit China Sulaiman et al N, total genotyped samples (a) 3 was A/D (b) 2 A/C, 1 C/D (c) 1 A/D (d) 2 A/B, 2 A/E 21

17 Risk factors The epidemiology of giardiasis in industrial nations is different from low income countries. Many studies have been conducted to determine risk factors of giardiasis in developed countries (Table 2.4). In a case-control study conducted in UK, the main risk factors were accidental swallowing of water while swimming, drinking contaminated treated tap water, contact with contaminated recreational fresh water and eating contaminated lettuce (Stuart et al. 2003). Previous studies in UK have also identified travelling to developing countries as a risk factor of giardiasis (Gray and Rouse, 1992). In New Zealand, drinking water from New Zealand supplies was seven times higher risk of giardiasis compared to water from sources outside New Zealand. Housewives and nursing mothers, occupational groups exposed to human wastes, swimming and travelling were additional risk factors (Hoque et al. 2002). In addition to the previous risk factors of giardiasis in New Zealand, children wearing nappies were at thirty times higher risk of the disease (Hoque et al. 2003). Only one study reported that contact with animal was a risk factor (Warburton et al. 1994). In contrast, in developing countries, risk factors of giardiasis seem to be more related to personal hygiene and environmental sanitation (Table 2.5). The main risk factors are households without piped water, improper sewage disposal, large family size, not using toilet, not washing hands and insufficient washing of vegetables (Cifuentes et al. 2004; Prado et al. 2003). Giardiasis has been reported to be highly prevalent in day care centres worldwide and many studies have been carried out for identifying risk factors which included high duration of attendance, low family income, and large family size (Novotny et al. 1990). Furthermore, lack of hand-washing before eating and after defecation has also been stated as a risk factor (Núñez et al. 2003). 22

18 Table 2.4 The main risk factors of giardiasis reported in developed countries (Modified from Hunter and Thompson (2005)) Risk factor OR 95% CI Country References Drinking treated water UK Stuart et al New Zealand Hoque et al Drinking non-treated water Canada Isaac-Renton and Philion, New Hampshire Dennis et al Swimming UK Stuart et al UK Gray et al New Zealand Hoque et al New Zealand Hoque et al New Hampshire Dennis et al Travelling New Zealand Hoque et al New Zealand Hoque et al UK Gray et al Canada Isaac-Renton and Philion, 1992 Eating raw vegetables (lettuce) UK Stuart et al Nappy handling 4 - New Zealand Hoque et al New Zealand Hoque et al Contact with farm animals UK Warburton et al Contact with pets UK Warburton et al

19 Table 2.5 The main risk factors of giardiasis reported in developing countries (Modified from Hunter and Thompson (2005)) Risk factor OR 95% CI Country References Not-using toilet Egypt Mahmud et al Brazil Prado et al Improper sewage disposal Mexico Cifuentes et al Brazil Prado et al Large family size Brazil Prado et al Malaysia Norhayati et al Unsafe food hygiene Mexico Cifuentes et al Poor hand washing Mexico Cifuentes et al

20 2.1.7 Genotyping The development of genotyping techniques marked a new phase in the epidemiology of Giardia. It is required to determine the significance of zoonotic potential of Giardia especially in endemic foci and where human are living closely to companion animals. Genotyping could also help public health authorities to detect the sources of water contamination in waterborne outbreaks, and whether human pathogenic genotypes are present. Many environmentally derived strains, which may occur in the water, are of species that are not normally associated with human infection (Cacciò et al. 2005; Thompson and Monis, 2004). In addition, genetic mechanism of drug resistance and assemblage-linked sensitivity to metronidazole can also be achieved using molecular typing tools. Several genes have been targeted for genotyping Giardia such as small subunit ribosomal RNA (SSU rrna), triosephosphate isomerise (TPI), glutamate dehydrogenase (GDH), ß-giardian, elongation factor 1 a (EF-1a) and G. lamblia open reading frame C4 (GLORF-C4). Most of the studies that characterized Giardia have been based on analysis of a single genetic locus (Aydin et al. 2004; Read et al. 2004; Traub et al. 2004; Sulaiman, et al. 2003; Amar et al. 2002; Caccio` et al. 2002; Graczyk et al. 2002; Van Keulen et al. 2002; Read et al. 2002; Yong, et al. 2002; Yong, et al. 2000; Hopkins, et al. 1997). Although the analysis of at least two loci for determining assemblages and species has been recommended (Caccio et al. 2005), the single polymorphic marker analysis is still considered valid (Sulaiman et al. 2003). The SSU rrna gene and the EF-1a gene can be used to distinguish major assemblages, whereas the TPI gene, β-giardin gene, and the GDH gene, allow different subgenotypes 25

21 to be identified within each assemblage. In addition, restriction fragment length polymorphism (RFLP) genotyping tool has been developed for TPI (Amar et al. 2002), GDH (Read et al. 2004) and β-giardian (Cacciὸ et al. 2002b). TPI-based RFLP can differentiate between assemblage AI, assemblage AII and assemblage B (Aydin et al. 2004; Amar et al. 2002). Using GDH-based RFLP, all the major assemblages can be differentiated. The protocol is also capable of discriminating between assemblages AI and AII and between assemblages BIII and BIV (Read et al. 2004). An RFLP assay on the β-giardin gene allowed the identification of three genotypes within assemblage A and four genotypes within assemblage B. Although the RFLP protocol could be useful for routine examination as it is a rapid and cheaper genotyping tool, it does not replace DNA sequencing. DNA sequencing is the most common genotyping tool used for typing G. intestinalis (Anthony et al. 2007; Cacciὸ et al.2007; Nantavisai et al. 2007; Papini et al. 2007; Robertson et al. 2007; Berrilli et al. 2006; Lalle et al. 2005; Traub et al. 2005; Trout et al. 2005; Appelbee et al. 2003). The superiority of DNA sequencing could be attributed to several factors including the information on the genetic diversity it gives, discovering a new genotypes and additional analysis such as phylogenetic analysis could be applied. Many genotyping methods have been published (Table 2.6). The sensitivity of these techniques depends on DNA extraction methods, primers and type of the targeted gene. The efficiency of these protocols has not been compared except in one study, carried out in Thailand, which compared 16s rrna-based nested PCR (Read et al. 2002), GDHbased nested PCR (Read et al. 2004), ß-giardin-based nested PCR (Lalle et al. 2005), TPI-based nested PCR (Sulaiman et al. 2003), and EF1-α-based nested PCR (Monis et al. 1999). The study showed that nested PCR, using the two primer pairs (RH 4, RH 11 and GiarR, GiarF), which amplify SSU rrna was the most sensitive protocol. This 26

22 superior sensitivity could be attributed to the high copy number of the SSU rrna gene in the organism. Boothroyd et al. (1987) reported that approximately 60 to 130 copies of the SSU rrna gene are present per nucleus of G. intestinalis, arranged in tandem repeats. DNA extraction is a critical step in molecular identification of pathogens and plays a major role in the sensitivity of PCR protocol. The presence of PCR inhibitors in faeces and the difficulty of cysts to rupture make the use of an effective extraction method very important in increasing PCR sensitivity. A wide variety of extraction methods have been used for extracting DNA from stool. However, no intensive study has been carried out to evaluate the sensitivity of these methods. Nantavisai et al. (2007) has compared the efficiency of three extraction techniques i.e. phenol-chloroform, QIAgen stool Mini Kit and FTA filter paper. They concluded that FTA filter paper was the most sensitive technique. This finding could not be generalized as many techniques were not included in their comparison. 27

23 Table 2.6 Giardia genotyping protocols Target gene Primers PCR assay References 16S rrna RH-4, RH-11 PCR Hopkins et al RH 4, RH 11 + GiarR, Nested PCR Read et al GiarF AL4303, AL AL4304, AL4306 Nested PCR Sulaiman et al G18S2, G18S3 PCR Monis et al GDH GDH1, GDH4 PCR Homan et al GDHeF, GDHiR + Nested PCR Read et al GDHiF ß-Giardin G7, G759 PCR Giangaspero et al G7, G759 + Forward, Nested PCR Lalle et al Reverse TPI AL3543, AL AL3544, AL3545 Nested PCR Sulaiman et al EF-1a EF1AR/GLONGF and RTef1-αF/ RTef1-αR Nested PCR Monis et al

24 2.1.8 Diagnosis Microscopic identification of G. intestinalis trophozoites or cysts using permanent staining such as trichrome staining technique after concentration method has been considered the gold standard diagnostic method. It is sensitive, specific and reliable. An additional advantage is the applicability for the assessment of parasite morphology. However, this method is time consuming and impractical under circumstances where rapid diagnosis is required for large numbers of specimens. The sensitivity of microscopic examination could be affected by sampling issues related to the intermittent excretion of intestinal parasites which can be overcome by examining triple faeces samples collected in three consecutive days (van Gool et al. 2003). An alternative approach was to develop antigen based detection. The two most common antigen detection assays are immunoflourescent assay which targets the intact parasite and needs immunoflourescence microscope, and ELISA test which detect soluble antigens in the faeces. A non-enzymatic solid-phase qualitative immunochromatographic assay for detecting soluble antigen has also been developed (Garcia et al. 2003). Although these techniques are sensitive and specific, the interpretation of results from serological tests detecting soluble Giardia antigens should be carefully interpreted because they may be positive even after a person stops shedding intact organisms. They could thus give false positive results in individuals who may actually be cured of infection (Ali and Hill, 2003). PCR assays are more specific and sensitive. However, they are expensive, time consuming and the laboratory technologists need to be trained. Discovering a difference in the pathogenicity and drug resistance of Giardia assemblages may lead to improving PCR based technology for routine diagnosis. However, the cost will still be an important deciding factor especially in low income countries. 29

25 2.1.9 Treatment Several drugs for the treatment of giardiasis have been produced such as metronidazole, tinidazole, ornidazole, quinacrine, nitazoxanide, tizoxanide, furazolidone, albendazole and paromomycin (Gardener and Hill, 2001; Abboud et al. 2001; Heyworth, 1996). Metronidazole has been the drug of choice of giardiasis at a single high dose (2g) regimen or multiple low doses (250mg three times a day for 5 to 7 days). Tinidazole is an alternative drug being easiest to be used as single dose (2g) for adult which shows 90-98% efficacy. It could also be given as multiple doses (100mg three times a day for 5 to 7 days) (Gardener and Hill, 2001). Single-dose of ornidazole showed 94-97% efficacy in children in Turkey (Ozbilgin et al. 2002). Although quinacrine at multiple doses (100mg three times a day for 5 to 7 days) indicated up to 90% efficacy, it has been discontinued in USA since 1992 (Ali and Hill, 2003). Albendazole, the drug of choice for helminthiasis, has been found to be effective for the treatment of giardiasis in vitro (Cruz et al. 2003) and in vivo (Gardener and Hill, 2001). Taking albendazole at 400mg four times a day for 5 days has been reported to be as effective as metronidazole (Misra et al. 1995). Nitazoxanide appears to be as effective as metronidazole and tinidazole (Adagu et al. 2002; Abboud et al. 2001) for treating giardiasis even for cases resistant to metronidazole and albendazole therapy (Abboud et al. 2001). Nitazoxanide has also been approved in United States for the treatment of diarrhoea caused by Cryptosporidium in children aged 1 11 years (Anonymous, 2003). Tizoxanide parallel the effectiveness of nitazoxanide. Paromomycin is the drug of choice of giardiasis during pregnancy (Gardner and Hill, 2001). 30

26 2.2 CRYPTOSPORIDIUM Introduction Cryptosporidium is an intracellular coccidian opportunistic protozoan parasite which has a worldwide distribution infecting humans, farm animals, companion animals, laboratory animals as well as wild mammals (Fayer, 2004). Although Cryptosporidium was initially reported in mice in 1907 by Tyzzer, (1907), the first human case was described in 1976 (Meisel et al. 1976; Nime et al. 1976). In the 1980s, Cryptosporidium was reported as the cause of death in an AIDS patient, highlighting the public health significance of this parasite (Current et al. 1983). Cryptosporidiosis is responsible for acute self-limiting diarrhoea in immunocompetent persons and life-threatening diarrhoea in immunocompromised persons, particularly in persons receiving immunosuppressive drugs and AIDS patients (Flanigan et al. 1992). In the early childhood, the infection is associated with malnutrition disorder (Agnew et al. 1998; Checkley et al. 1998, 1997; Molbak et al. 1994). Cryptosporidiosis is a major public health problem in developing and developed countries. In industrialized countries, Cryptosporidium has been identified as the cause of numerous waterborne, foodborne and daycare outbreaks (Fayer, 2004). In developing nations, the disease is probably sporadic affecting paediatric health. The epidemiology of this parasite is complicated and Cryptosporidium species cannot be distinguished morphologically, creating many problems to water industry and water health authorities. In addition, the oocyst stage is environmentally stable, able to survive and penetrate routine wastewater treatment and is resistant to inactivation by commonly used drinking water disinfectants (Rose and Gerba, 1991). The application of genotyping tools has therefore great merit to help water health authorities to manage water contamination and 31

27 to identify the source of infection. Thus far, approximately 16 species and more than 30 genotypes of Cryptosporidium have been recognized. Of these, C. parvum and C. hominis are the most common species causing the disease in human. Furthermore, C. canis, C. meleagridis, and C. felis have also been isolated from immunocompetent children (Xiao et al. 2001). Although humans have been considered the main source of infection (anthroponotic transmission), animals have been implicated as the source of water contamination and human infection (zoonotic transmission) Morphology Cryptosporidium, like Giardia, has no recognizable Golgi apparatus and previously regarded as primary amitochondriate organisms. The discovery of the Giardia and Cryptosporidium mitosome has changed this view. Rather than the amitochondrial state being primitive, it is suggestive of reductive evolution. Cryptosporidium has different stages; oocyst, trophozoite, schizont, merozoite and sexual stages including micro- and macrogamont. Oocysts are the exogenous stage, consisting of four sporozoites within a tough two-layered wall (Fayer, 1997) Life cycle The life cycle of Cryptosporidium is shown diagrammatically in Figure 2.2. There is no intermediate host in Cryptosporidium and the life cycle takes place in a single host. The life cycle starts with the ingestion of the infective stage oocysts by the host. After excystation, four naked sporozoites are released in the small intestine, infecting the epithelial cells and initiating asexual development. They become internalized, differentiate into spherical trophozoites and undergo two successive generations of merogony (schizogony), releasing eight and four merozoites, respectively. Each mature 32

28 merozoite released from the first schizont, theoretically, infects another host cell and develops into another type I or into type II schizont which produces four merozoites. The merozoites released from the type II schizont infect a new host cells and initiate sexual multiplication by differentiating into either a micro- or macrogamete. The release of microgametes, and their union with macrogametes, gives rise to the zygote, which, after two asexual divisions, forms the environmentally resistant oocyst containing four sporozoites (Tzipori and Ward, 2002). Thin wall oocysts may also develop and can excyst in the intestinal tract causing autoinfection. This phenomenon may explain the mechanism of persistent infection in AIDS patients in the absence of successive oocyst exposure (Current and Gracia, 1991). Although Cryptosporidium infection is localized to gastrointestinal tract especially in infected immunocompetent individual, extraintestinal infection should not be ruled out (Yang and Healy, 1994). The prepatent period ranges from one to three weeks, whereas the patent period may persist for years, depending on the parasite species and the immune status of the hosts (Sturdee et al. 1999). 33

29 Figure 2.2 Life cycle and morphology of Cryptosporidium Source : Fayer (1997) 34

30 2.2.4 Taxonomy Describing species within the genus Cryptosporidium was initialy based on host occurrence which led to a large number of species being described and a history of confusion and controversy (Thompson, 2002; O Donoghue, 1995). The classification based on morphology has been difficult as Cryptosporidium species are morphologically identical. Molecular tools have indicated that Cryptosporidium species are phenotypically and genotypically heterogeneous and 16 species of Cryptosporidium have thus far been identified (Lim et al. 2008) (Table 2.7). Among all identified species, C. hominis (previously known as the C. parvum genotype I) almost exclusively infects humans. C. parvum (previously known as the C. parvum genotype II) has a wide range of hosts including humans, ruminants and perhaps a few other animals and has been considered as zoonotic species. Furthermore, other species that are known as animal parasites such as C. meleagridis, C. canis, C. felis, C. suis, C. muris and the cervine and monkey genotypes of Cryptosporidium have been reported in immunocompetent (Learmonth et al. 2004; Ryan et al. 2003; Wu et al. 2003; Enemark et al. 2002; Ong et al. 2002; Xiao et al. 2001) and immunocompromised humans (Matos et al. 2004; Cama et al. 2003; Mallon et al.2003; Caccio` et al. 2002a; 2000; Gatei et al. 2002; Guyot et al. 2001; Leav et al. 2002;; Tiangtip and Jongwutiwes, 2002; Morgan et al. 2000; Pieniazek et al. 1999; Sulaiman et al. 1998; Bonnin et al. 1996). 35

31 Table 2.7 Cryptosporidium species and their hosts. Species Hosts References Cryptosporidium hominis Human, monkey Morgan-Ryan et al Cryptosporidium parvum Cattle, other ruminants, humans Tyzzer, 1912 Cryptosporidium meleagridis Turkeys, humans Slavin, 1955 Cryptosporidium canis Dogs Fayer et al Cryptosporidium felis Cats Iseki, 1979 Cryptosporidium suis Pigs Ryan et al Cryptosporidium fayeri Red Kangaroo Ryan et al Cryptosporidium pestis Cattle Slapeta, 2006 Cryptosporidium muris Rodents Tyzzer, 1907 Cryptosporidium andersoni Cattle Lindsay et al Cryptosporidium wrairi Guinea pigs Vetterling et al Cryptosporidium bailey Poultry Current et al Cryptosporidium serpentis Reptiles Levine, 1980 Cryptosporidium galli Birds Pavlásek, I Cryptosporidium saurophilum Lizard Koudela and Modry, 1998 Cryptosporidium molnari Fish Alvarez-Pellitero and Sitja-Bobadilla

32 2.2.5 Pathology and clinical manifestation Cryptosporidium species are opportunistic pathogens which cause severe and lifethreatening diarrhoea in immunocompromised hosts. It also induces diarrhoea in immunocompetent persons. Other clinical manifestations of cryptosporidiosis include nausea and vomiting, abdominal cramps, and fever. In developing countries, where children are prone to infection, cryptosporidiosis in early childhood may be associated with subsequent impaired physical and cognitive development (Guerrant et al. 1999), even in the absence of diarrhoea (Agnew et al. 1998; Checkley et al. 1998, 1997; Molbak et al. 1994). In AIDS patients, cryptosporidiosis is one of the most serious opportunistic infections. An AIDS patient with CD4 T-cell counts of < 150/ml who is infected with C. parvum can develop persistent infection, with profound and life-threatening diarrhoea (Flanigan et al. 1992). The parasite can also spread from the gut to the hepatobiliary and the pancreatic ducts, causing cholangiohepatitis, cholecystitis, choledochitis or pancreatitis. Crypt abscessation in the gut of chronically infected AIDS patient has been reported (Tzipori et al. 1995). There is limited correlation between C. hominis and C. parvum and disease severity and morbidity. A case-controlled study aimed at differentiating symptoms and severity of illness between C. hominis and C. parvum found that the variation in duration of symptoms was significantly greater with C. hominis than in C. parvum (Hunter et al. 2004). Another study, conducted in Brazil, reported that children infected with C. hominis were worse than those infected with C. parvum. In addition, asymptomatic C. hominis infected children had greater long-term growth shortfalls than those who were 37

33 symptomatic. In contrast, growth shortfall in children infected with C. parvum was associated with being symptomatic, degree of oocysts shedding and lactoferrin positivity (inflammation). Authors have concluded that even in asymptomatic children, C. hominis is associated with heavy infection, growth shortfalls and lactoferrin positivity (Bushen et al. 2007). Although C. canis, C. meleagridis, and C. felis have been isolated from immunocompetent children whom some of them had diarrhoea (Xiao et al. 2001), there is no data available about the pathogenecity of these species Epidemiology Prevalence and demographic distribution Cryptosporidiosis is distributed worldwide. The mean prevalence rate for Cryptosporidium infection is between 1 and 3% in Europe and North America but is considerably higher in underdeveloped continents, ranging from 5% in Asia to approximately 10% in Africa (Bushen et al. 2006; Current, 1994). In developing nations, cryptosporidiosis occurs mostly in children younger than 5 years (Samie et al. 2006; Sulaiman et al. 2005; Simango and Mutikani, 2004; Xiao et al. 2001; McLauchlin et al. 2000). this could be attributed to the short-lived or incomplete acquired immunity to Cryptosporidium infection (Xiao et al. 2001; Newman et al. 1999). The prevalence of C. hominis and C. parvum, the major causes of human cryptosporidiosis, varies from one country to another. C. hominis is more prevalent in North and South America, and Africa (Learmonth et al. 2004; Cama et al. 2003; Gatei et al. 2003; Peng et al. 2003a; Leav et al. 2002; Ong et al. 2002), whereas C. parvum causes more human infections in Europe, especially in the UK (Mallon et al. 2003; 38

34 McLauchlin et al. 2000). Geographical variation has also been reported within countries; C. parvum infection rate in human is higher in rural than in urban areas compared to C. hominis (Learmonth et al. 2004; McLauchlin et al. 2000; Ong et al. 1999). Seasonal pattern of human cryptosporidiosis has been documented in several countries. In UK, two peaks were reported; one peak during the spring which was exclusively due to C. parvum and the second peak during late summer to early autumn and was caused by both C. parvum and C. hominis (McLauchlin et al. 2000). In South Africa, the highest prevalence of cryptosporidiosis was in the summer months (Moodley et al. 1991) Transmission Cryptosporidium infection can be transmitted directly from person-to-person or indirectly through contaminated water or food. Although animals were considered to be a reservoir of Cryptosporidium, with potential for the contamination of household water sources (Newman et al. 1993), the dominance of C. hominis in several communities (Samie et al. 2006; Learmonth et al. 2004; Cama et al. 2003; Gatei et al. 2003; Peng et al. 2003a; Leav et al. 2002; Ong et al. 2002) indicates the importance of the anthroponotic transmission cycle since humans are a predominant recognised host of C. hominis. In addition, children infected with C. hominis shed higher levels of oocysts, possibly contributing to the increased prevalence and spread of C. hominis within these communities (Samie et al. 2006; Xiao et al. 2001; McLauchlin et al. 2000). 39

35 A. Zoonotic transmission Farm animals have been implicated as sources of human cryptosporidiosis. C. parvum has been the most prevalent species in farm animals particularly in calves. In sheep, the prevalence ranges from 10% to 68% (Causape et al. 2002; Majewska et al. 2000; Abd- El-Wahed, 1999; Olson et al. 1997) and between 11.0% and 35.2% in goats (Watanabe et al. 2005; Noordeen et al. 2000; Rossanigo et al. 1987). In the UK, human infection with C. parvum dramatically declined after applying several intervention measures that reduced human contact with livestock, which has been previously reported as a risk factor of cryptosporidiosis (Hunter et al. 2003). Livestock has also been implicated as the source of waterborne outbreaks in Canada (Fayer et al. 2000) and England (McLauchlin et al. 2000). Furthermore, C. parvum was the aetiological pathogen in 84% of 67 sporadic cases detected in Scotland, supporting livestock faecal pollution of water sources as the leading cause of sporadic cryptosporidiosis (Goh et al. 2004). However, detection of C. parvum in humans is not a conclusive evidence for zoonotic transmission. Genetic variants of C. parvum isolated from human that are rarely found in animals have been identified using subgenotyping analysis, suggesting that human infection with C. parvum might have originated from human themselves (Xiao et al. 2004). Subtyping of C. parvum (species that has been considered zoonotic) showed that of the two most common C. parvum subtype families, the IIa family is zoonotic, seen in humans and ruminants, whereas the IIc subtype family is anthroponotic and is found only in humans (Xiao et al. 2007; Sulaiman et al. 2005; Xiao and Ryan, 2004; Alves et al. 2003; Mallon et al. 2003). 40

36 C. meleagridis, a parasite originally described in turkeys (Xiao et al. 2004), has been detected in human in the UK (McLauchlin et al. 2000), Thailand (Tiangtip and Jongwutiwes, 2002; Gatei et al. 2002) and Peru (Cama et al. 2003), implicating domestic pets as potential source of infection for human. Dogs and cats seem to be most commonly infected with the predominantly host-adapted C. canis and C. felis (Abe et al. 2002) and may not represent important zoonotic reservoirs. B. Waterborne transmission During the last decade, Cryptosporidium has emerged as an important enteric pathogen. Of the > 150 potentially waterborne pathogens (Karanis et al. 2007; WHO, 2004), Cryptosporidium is the most notorious in developed countries, responsible for large waterborne disease outbreaks (Insulander et al. 2005; Rose et al. 1997). The significance of Cryptosporidium to water authorities resulted in introduction of specific regulations and guidelines to deal with this parasite. Many waterborne outbreaks of cryptosporidiosis have been reported in different countries (Kuroki et al. 1996; Barer and Wright, 1990; Brown et al. 1989). Cryptosporidium spp. have been responsible for eight waterborne outbreaks associated with water intended for drinking in United States (Berkelman, 1994; Moore et al. 1993). These outbreaks have occurred in water systems that used well and spring water treated solely by chlorination and in surface water systems that have been filtered. The first reported waterborne outbreak of cryptosporidiosis was in the summer of 1984 in Braun Station, 32 km from San Antonio, Texas (D'Antonio et al. 1985). The largest documented waterborne disease outbreak in the US history was in 1993, which infected 403,000 out of 1,610,000 people in greater Milwaukee (Mackenzie et al. 1994). 41

37 Swimming pool-associated outbreaks of cryptosporidiosis have also been widely reported (CDC, 1994; McAnulty et al. 1994; Bell et al. 1993; Sorvillo et al. 1992; Joce et al. 1991). Genotyping methods of discriminating pathogens isolated from water borne outbreaks could help epidemiologist to assess the source of contamination. They also provide information about the public health significance of Cryptosporidium oocysts in watersheds (Thompson, 2000). Although cattle have been repeatedly implicated as sources of waterborne cryptosporidiosis outbreaks, genotyping the contaminating isolates in Milwaukee outbreak has implicated human effluent as the source of contamination (Zhou et al. 2003) Risk factors Currently, infections with Cryptosporidium are either those detected in outbreaks or sporadic cases. It has been stated that cases detected in outbreaks represent 10% of all the diagnosed cases (Nichols et al. 2003). Immunocompromised patients especially AIDS patients have been identified to be at high risk and several case-control studies have been carried out to determine the most common predictors of cryptosporidiosis in this high risk group (Hunter and Nichols, 2002). The highlighted risk factor was sexual behaviour (Pedersen et al. 1996; Sorvillo et al. 1994). Furthermore, HIV-positive patient who owned dogs had two fold higher risk of cryptosporidiosis (OR = 2.19, 95% CI = , p = 0.05) (Glaser et al. 1998). On the other hand, risk factors of sporadic cryptosporidiosis among immunocompetent in developed countries included children with diarrhoea, contact with farm animals especially calves, swimming in public swimming pool and fresh water and travelling 42

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