Cryptosporidiosis As Threatening Health Problem: a Review

Asian Pac J Trop Biomed 2013; 3(11): 916-924 916

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Nurul Fariza Rossle*, Baha Latif Faculty of Medicine, Universiti Teknologi MARA, Jalan Hospital, 47000 Sungai Buloh, Selangor, Malaysia

PEER REVIEW ABSTRACT

Peer reviewer Cryptosporidium The protozoa under the genus is a zoonotic apicomplexan oCryptosporidiumbligate intracellular Dr. Xue-jie Yu, Professor, University parasite. Cryptosporidiosis, the term used to designate infection caused by sp., of Texas Medical Branch, Galveston, is considered as one of the most common food and waterborne diseases with worldwide spread, 409 772 1786 - , USA. Professor and Dean, Cryptosporidiumacting as a common cause of diarrhoea in animals and man. In immunocompetent individuals, School of Public Health, Shandong typically induces self-limiting diarrhoea, which may resolve on its own after 2-3 University, Jinan, China. d. However, cryptosporidiosis may turn life-threatening and subsequently lead to death in small E AIDS -mail: [email protected] chilCryptosporidiumdren, the elderly and immunocompromised person, especially in patient. The diagnosis Comments for infection is uμsually carried out through examination of stool for the presence of oocysts which measured 4-6 m with spherical appearance. Morphometric identification is This is a nice review article that often difficult because of thCryptosporidiume diminutive size and obscure internal structure of the protozoa. has summarized information on Often, the identification of is realised through the combination of methods cryptosporidiosis including classic incorporating data from morphometrics, molecular techniques, and host specificity. However, microbiology, epidemiology, clinical limitations to some of these techniques still exist whether because of cost, duration, expertise, or manifestations, diagnosis and reliability. Drugs combination is implemented in treatmen tStreptomyces of cryptosporidiosis. The efficiency treatments based on articles published of paromomycin, an aminocyclitol antibiotic isolated from , can be effective when from 1907 to 2013. Information in this 12 combined use with proteaCryptosporidiumse inhibitors or recombinant IL- . Since there is no drug that achieves article will give physicians and young the complete removal of from the host, supportive therapy was preferred in both scientists a comprehensive overview human and domestic animals. on cryptosporidiosis and this article will be helpful in controlling and KEYWORDS prevention of cryptosporidiosis. Cryptosporidium Details on Page 920 , Prevalence, Taxonomy, Outbreak, Diagnosis

1. Introduction [7] human casesCryptosporidium of cryptosporidiosis . Initially, sp. was reported by Tyzzer as C [8] ryptosporidiosis is a zoonotic proCryptosporidiumtozoal disease infective in mice , and then was pushed to the background caused by coccidial species of the genus until the first human case noted in 1976[9,10]. Afterwards, and which is reported in more than 40 countries in the more concerns over cryptosporidiosis have arisen since [1] I AIDS [11] world . n stool surveys of pCryptosporidiumatients with gastroenteritis, it was determined to cause death in one patient . the reported prevalence of is 1%-4% Mainly, cryptosporidiosis is responsible for acute self- in Europe and North America and 1%-37% in Africa, limiting diarrhoea in immunocompetent persons and life- A A S C A [2-6] sia, ustralia,Cryptosporidium and outh and entral merica . threatening diarrhoea in immunocompromised persons, In most cases, infection results in particularly in persons receiving immunosuppressive drugs AIDS [12] gastrointestinal problems such as severe diarrhoea in both and patients . C. hominis A A ( immunocompromiseCryptosporidiumd and immunocompetent people. mong mong all iC.de nparvumtified species, previously I) tCryptosporidiumhe five commo nparvum C. parvum specCryptosporidiumies in humans, known as the C. parvum genotype almost exclusiveC.ly ( ) ( hominis C. hominis and parvuminfects humans. previously known as the ( ) are responsible for more than 90% of genotype II) has a wide range of hosts including

*Corresponding author: Nurul Fariza Rossle, Institute of Medical Molecular Article history: Biotechnology, Faculty of Medicine, Universiti Teknologi MARA, Jalan Hospital, 47000 Received 20 Aug 2013 Sungai Buloh, Selangor, Malaysia. Received in revised form 27 Aug, 2nd revised form 5 Sep, 3rd revised form 10 Sep 2013 Tel: +603 6126 7396 Accepted 20 Oct 2013 Fax: +603 6126 7073 Available online 28 Nov 2013 E-mail: [email protected] Foundation Project: This study was part of the project funded by MARA University of Technology Excellence Fund [Grant No. 600-RMI/ST/DANA 5/3/Dst (334/2011)]. Nurul Fariza Rossle and Baha Latif/Asian Pac J Trop Biomed 2013; 3(11): 916-924 917

II I humans and animals and has Cryptosporidiumbeen considere dcanis, as a into type meront or complete another cycle of type zoonotic species. Furthermore, meronts[25]. Type II meronts produce four merozoites which Cryptosporidium meleagridis, Cryptosporidium felis, [24,26] Cryptosporidium andersoni, Cryptosporidium muris become microgamonts or macrogamonts . F Cryptosporidium suis , ertilization between gamonts results in formation and have also been isolated from of a zygote which develops into oocyst containing four immunocompetent humans[13-15]. sporozoites[24,27]. Two types of oocysts are produced, thick- Cryptosporidiosis has a higher incidence in developing walled oocysts which are excreted in the faeces and thin- countries, especially in children, institutionalized patients, walled oocysts which re-circulate in the intestinal tract (AIDS) [11,24,26] T malnCryptosporidiumourished, and immunocompromised individuals causing autoinfection . his phenomenon may explain [16]. mostly infects children less than five the mechanism of persistent infection in AIDS patients in the years old and peaks for children less than two years old[17]. absence of subsequent oocyst exposure[2]. In industrialised countries, cryptosporidiosis also occurs [7,18] in adults due to foodborne or waterborne outbreaks . 3. Taxonomy Currently, nitazoxanide (Alinia) is approved for treatment of cryptosporidiosis in children and immunocompetent adults USA H I 1907 T in the . owever, nitazoxanide is not effective without an Cryptosporidium n , yzzer was the first to discover the genus appropriate immune response and is therefore ineffective who described it as a coccidian- [19] against immunocompromised individuals . lCryptosporidiumike organism in thmurise stomach of mice, which he named [8,28]. Later, Tyzzer discovered 2. Morphology and life cycle a second isCryptosporidiumolate in the sma lparvuml intestine of mice, which [29] H he named Cryptosporidium. ence, species Cryptosporidium nomenclature within the genus was initially O 4 6 60 µ ocysts of sp. are small, measuring - based on host occurrence, which led to more than [20] T [24] T m in diameCryptosporidiumter and are spherical-to-ovoid in shape . he species being described . he claCryptosporidiumssification based only on life cycle of is completed in a single host. It morphology has been difficult as species T involves both asexual and sexual stages. here are six major are morphologicaCryptosporidiumlly identical. developmental stages as described by Tzipori and Ward[2], Until recently, was classified as belonging which are excystation, merogony, gametogony, fertilization to the family Cryptosporidiidae, suborder Eimeriorina and E [30] and zygote development, formation of environmentally oToxoplasma,rder ucocc iCyclospora,diorida , w Isosporahich also inclSarcocystisudes in its ranks resistant oocyst wall, and sporogony (Figure 1)[21]. and [31]. To b S Cryptosporidium j Thick-walled porozoite c Trophozoite T I M a Ocyst d ype eront e date, over 20 species and 60 genotypes of oocyst (spourlated) exits host have been classified with invalidation of somCryptosporidiume old ones and introduction of new others[15,32]. Of these, Auto-infection parvum Cryptosporidium hominis Asexual Cycel k and are the most common Thin-walled [33] oogyst species causing the disease in human (Table 1). (sporulated) Eerozoite Table 1 Microgamont Cryptosporidium Microgametes f Recognized species in the genus . Undifferentiated g Gamont Type II Meront Species Host Reference C. hominis Merozoites Human [34] Macrogamont Sexual Cycle C. parvum [35] h Cattle, human i C. andersoni Cattle [36] Figure 1. Cryptosporidium C. muris Life cycle of sp. consisting of asexual and sexual Rodent [37] C. suis stages. Pig [38,39] C. felis Infection starts with the ingestion of the oocysts by Cat [40] C. canis the host. Oocyst is the exogenous stage, containing four Dog [41] C. wrairi Guinea pig [42] sporozoites within a tough two-layered wall excreted in C. baileyi [22] O Poultry [43] the faeces . ocyst stage is environmentally stable, able C. meleagridis Turkey, human, zoo birds [13,40,44-45] to survive through routine wastewater treatment and is C. bovis Cattle, sheep [46] resistant to inactivation by commonly used drinking water C. galli [23] Finches, chicken [47] disinfectants . C. serpentis Reptile [48] After oocysts are ingested via contaminated food or water, C. saurophilum Lizard, snake [14,49] from fomites, or from direct contact with infected persons C. molnari or animals, the oocyst undergoes excystation, releasing four Fish [50] C. scophtalmi [51] sporozoites in the small intestine (ileum) which invades Fish C. xiaoi [52] epithelial cells[24]. The sporozoites affix to the luminal Sheep, yak, goat C. fragile [53] surface of epithelial cells and differentiate asexually into Frog C. ryanae [54] trophozoites which to produce two different types of meront Cattle C. marcopodum [55] by merogony[11,24]. Type I meronts form eight merozoites, Kangaroo C. fayeri [57] which enter neighbouring epithelial cells and either develop Kangaroo Nurul Fariza Rossle and Baha Latif/Asian Pac J Trop Biomed 2013; 3(11): 916-924 918 4. Pathology and clinical manifestations [16] A water, food and possibCryptosporidiumly via air . nimals were considered Cryptosporidium to be a reservoir of , with potential for has been recognized as a cause of the contamination of household water sourcesC. a nparvumd most gastrointestinal illness in both immunocompetent and humC.an hominiscryptosporiodiosis is associated with C. [11,20] C [65,66] I immunodeficient people . linical manifestations ahominisnd . n addition, children infected with of cryptosporidiosis typically include persistent watery shed higher levels of oocysts because they have diarrhoea, nausea, vomiting, abdominal cramps, and underdeveloped immune system and oocysts can proliferate [58] fever . easier, possibC.ly hominiscontributing to the increased prevalence Clinical history and physical examination are quite and spread of within these communities[13,67]. valuable as preliminary screening for the aetiology of Infectious oocysts could be excreted with the stool for up diarrhoea. Food and water consumption could be the source to 5 weeks even after diarrhoeal illness ends, which means of infection if patients have history of travelling to endemic that the absence of diarrhoea does not necessarily mean or epidemic places prior to illness. Acute diarrhoea may that the infection had subsided[68]. Numerous nosocomial point more to rotavirus while Cryptosporidiumpersistent diarrhoea isGiardia usually outbreaks of cryptosporidiosis have occurred among caused by protozoa such as aSalmonelland . healthcare workers as well as patients in bone marrow D HIV Shigellaysentery or bloody diarrhoea may be due to , transplant units, paediatric hospitals, and wards with - [69,70] F , or trauma to the gastrointestinal tract such as infected patients . urtheCryptosporidiumrmore, elderly hospitalized ulcer and irritable bowel syndrome. Nevertheless, these patients may also be at risk for infection[71]. F classifications are not concrete and sometimes mixed arm animals hC.av eparvum long been implicated as sources of infection is detected in patients, particularly in endemic human infection. has been the most prevalent I arCryptosporidiumeas with poor hygiene and sanitation practices. species in farm animals particularly in calves. n sheep, infects tissue on the superficial surface of the prevalence ranges from 10% to 68%[72,73] and between 11 0% 35 2% [74,75] I UK the intestinal epithelium in the ileum and causes destruction . C. a nparvumd . in goats . n the , human infection to the epithelial layer[59]. Extensive studies in a piglet model with dramatically declined after applying several of cryptosporidiosis demonstrate the loss of vacuolated intervention measures that lessened human contact with villus tip epithelium accompanied witCryptosporidiumh reduction in livestock, which has been previously accounted as a risk glucose-coupled sodium co-transport[60]. factor of cryptosporidiosis[76]. Livestock has also been C [16] disrupts the intestinal barrier function and increases its inferred as the source of waterC.bo parvumrne outbreaks in anada permeability, causing impaired absorption and increased and England[67]. Furthermore, was the aetiological secretion of fluid and electrolytes, and nutrients, which pathogen in 84% of sporadic cases detected in Scotland, leads to malnutrition and watery diarrhoea[61]. Persistent supporting livestock faecal pollution of water sources infection in the absence of subsequent exposure to oocysts as the leading cause of sporadic cryptosporidiosis[77]. is quite common, especially among the immunosuppressed Associations between animal contact with transmission patients. Thin-walled oocysts excyst in the intestinal tract of cryptosporidiosis in humans have been documented. without ever leaving the host and have the ability to cause Outbreaks have been reported in veterinary students autoinfection[2]. Moreover, attachment of motile sporozoites and animal researchers working with infected calves; to the gastric epithelium induced the formation of agricultural camps and fairs; and case control studies of [77-79] parasitophorouCryptosporidiums vacuole and this unique structure provides human cryptosporidiosis . I protection for from the harsh environment mplicating domestic pets as potential souCryptosporidiumrce of infection of the host gastrointestinal tract. meleagridisfor human starts gaining deliberation when In developing countries, where children are more , a parasite originally described in turkeys, susceptible to infection, cryptosporidiosis in early has been detected in human in the UK[67], Thailand[80] and P [65] D childhood may be associated with subsequent impaired eru . ogs and cats seem to be most coCryptosporidiummmonly infected physical and cognitive development, even in the absence wcanisith the pCryptosporidiumredominantly h felisost-adapted of diarrhoea[62,63]. Cryptosporidiosis is one of the most and [81] and may act as zoonotic AIDS A AIDS [82] serious opportunistic infections in patients. n reservoirs for human cryptospCryptosporidiumoridiosis . patient with CD4 T-cell counts of <150/mL can develop During the last decade, has emerged 150 persistent infection, often with profound and life- as an important enteriCryptosporidiumc pathogen and over potentially threatening diarrhoea[12]. The parasite can also spread from waterborne pathogens. is the most notorious the intestines to the hepatobiliary and the pancreatic ducts, in developed countries, responsible for laCryptosporidiumrge waterborne causing cholangiohepatitis, cholecystitis, choledochitis or disease outbreaks[83,84]. The significance of pancreatitis[2,64]. to water authorities resulted in introduction of specific regulations and guidelines to deal with this parasite. Many 5. Transmission and outbreaks waterborne outbreaks of cryptospoCryptosporidiumridiosis have been reported in different countries[85,86]. sp. Cryptosporidium has been responsible for waterborne outbreaks associated can be transmitted directly via person to with water intended for drinking in the United States[58,87]. person, animal to human, animal to animal, or indirectly by These outbreaks have occurred in water systems that used Nurul Fariza Rossle and Baha Latif/Asian Pac J Trop Biomed 2013; 3(11): 916-924 919 well and spring water treated solely by chlorination and more hazardous[108]. Overexposure of ozone can give rise to in surface water systems that have been filtered. The first formation of high concentrations of possibly genotoxic by- reported waterborne outbreak of cryptosporidiosis was in products. Oocysts can survive for months in surface water the summer of 1984 in San Antonio, Texas[88]. The largest and soil and still remain viable for infection[109,110]. documented waterborne disease outbreak was in 1993, 403 000 100 which infected people and more than died with 6. Diagnosis M [58] S weakened immune systems in ilwaukee . ubsequeC.nt M ahominisnalysis revealed that the ilwaukee outbreak was due to [89]. Although cattle have been repeatedly implicated A wet mount using saline and/or iodine is the basis as sources of waterborne cryptosporidiosis outbreaks, of all microscopic technique. Routine diagnosis of genotyping the contaminating isolates in Milwaukee cryptosporidiosis in most countries has been based on outbreak has implicated human effluent as the source of microscopic detection of oocysts after staining of faecal contamination[89]. Swimming pool-associated outbreaks of smears. Concentration methods using the principals of cryptosporidiosis have also been widely reported[83,90]. flotation and sedimentation have been widely used, with Foodborne outbreaks of cryptosporidiosis have solutions such as sucrose, salt, zinc sulphate and formol- been accounted worldwide. The main sources of food ether[111,112]. The staining methods of most commonly used contamination comes from consumption of improperly are the m’odified Ziehl-Neelson acid-fast stain and modified cleaned raw fruits, vegetables and shellfish; faulty Kinyoun s acid-fast stain[113,114]. Differential staining processing of meat, beverages and other foodstuffs; methods such as safranin-methylene blue are also used[115]. unhygienic food handlers; and contamination via vectors Negative staining techniques with nigrosin[116], light green, such as insects and birds (Table 2)[91,92]. merbromide[117] and malachite green[118] stains yeasts and Table 2 bacteria but not oocysts. These techniques, despite being Food-borne outbreaks of cryptosporidiosis. easy to use with lowCryptosporidium cost, unfortunately can not distinguish Country Source No. of cases Reference between species of [56](Figure 2). ’ Mexico Cow s milk 22 [93] A B USA Chicken salad 15 [94] ’ UK Cow s milk 50 [95] USA Apple cider 154 [96] USA Green onions 54 [97] USA Apple cider 31 [97] Spain Clams/mussels/oysters - [98] μm Spain Mussels/cockles - [35] 20 USA Fruit/vegetables 148 [99] C D ’ Australia Cow s milk 8 [100] USA - 24 [101] USA - 88 [101] S S S EO USA Mussels - [102] USA Apple cider 23 [97] S Japan Raw meat and raw liver dish 4 [103] Denmark Salad buffet 99 [104] Figure 2. Cryptosporidium Finland Salad 72 [105] Microscopic observation of sp. Chile Snails - [106] (A) Modified acid-fast staining 100伊, (B) Wet mount 40伊, (C) Wet mount 40伊 , Sweden Fresh herbs - [39] (D) Fluorescent monoclonal antibody staining 20伊. O=oocyst, S=sporozoites, EO=empty oocyst. (Source: Latif B, unpublished data). -: Unknown. G USA I enotypinC.g aparvumnalysis of outbreaks in from apple cider mmunological based antigen detection methods identified which revealed that the outbreak that use antibodies to detect intact oocysts have been may have been due to dropped apples on the ground developed. Monoclonal antibody test is preferable to contaminated with cattle faeces[96]. A recent investigation of polyclonal antibody since it showed no cross-reactivity D [119] I C.foo dhominis handler contamination of a salad in enmark identified with other species . mmunofluorescence-based kits, [104] A J . nother foodborne outbreak in apan wC.as uCryptosporidiumsing a fluorescein isothiocyanate-conjugated anti- caused by eating raw beef and liver contaminated with monoclonal antibody that recognises parvum[103] . Cryptosporidium exposed surface epitopes oCryptosporidiumf oocysts are more specific and The nature of sp. oocyst makes it quite also sensitive for detecting oocysts. Indirect resistant to the changes in the environment. It is extremely fluorescence antibody tests show superior sensitivity resistant to chemical disinfection and not effected by compared to modified acid-fast stain[120]. However, it is chlorine, chloramines, and chlorine dioxide permissible expensive and needs specific equipment like fluorescence [107] O A in drinking water treatmeCryptosporidiumnt . zone is quite potent as microscope. ntigen detection using enzyme linked chemical disinfectant for oocyst, but also immunosorbent assays and passive agglutination has also Nurul Fariza Rossle and Baha Latif/Asian Pac J Trop Biomed 2013; 3(11): 916-924 920

[121] been developed . However, antibody cross-reaction and tongs or utensils should be always us’ed at a sala’d bar to the costs associated with such techniques have limited their prevent contamination from handlers or patrons hands. use[14]. Although enzyme linked immunosorbent assays Water, especially untreated surface water, should be boiled showed sensitivities ranging from 66% to 100%, false positive before drinking to kill any oocysts in it. Water treatment results have been reported[114]. plants have to be monitored regularly to prevent defective The introduction of polymerase chain reaction technology treatment and subsequent outbreak to houses receiving provides specific diagnosis to the species level with the water supply. Hands must be washed after contact with high sensitivity. Polymerase chain reaction allows swift, uncooked meat, soil, or animals before eating or touching repeatable and highly accurate examination, with the ability around the mouth area. Pastures need to be fenced properly to analyse large number of samples[16]. A variety of gene and the water bodies inside pastures (ponds or lakes) must DNA Cryptosporidiumloci are used in current diagnostics and taxonomy of never mix with the municipal water sources or reservoirs in , including the small subunit rRNA (also order to prevent cross-contamination. 18S RNA)[33,47,56,122] (HSP 70 O known as Cryptosporidium r , heat shock protein utbreaks of cryptosporidiosis should be investigated gene)[123], outer wall protein gene[122], quickly and the source isolated or quarantined to prevent B gCryptosporidiumene for thrombospondin-related adhesive protein of further infection. abies, toddlers, and diarrheic individuals -1[124], and actin gene[125]. must limit their contact with recreational water or use only pools made specifically for them. Train pets to defecate 7. Treatment outside the house and bath them regularly, especially if there is any children teething and crawling around in the house. These measures may seem trivial at first glance, In 2006, the only drug approved by the US Food and but they are in reality very important in minimising the Drug Administration for treatment of cryptosporidiosis in risk of getting cryptosporidiosis, particularly in those with children and immunocompetent adults is the anti-protozoal underdeveloped or immunocompromised immune system agent nitazoxanide (Alinia)[25]. However, nitazoxanide is like children, the sick, and the elderly. not effective without an appropriate immune response and is therefore ineffective against immunocompromised Conflict of interest statement individuals[19]. Recovery and survival rates has been dramatically improved with the use of highly active antiretroviral We declare that we have no conflict of interest. therapy, which cause increased CD4+ T-lymphocyte counts [25] in immunocompromised individuals . The introduction of Acknowledgements protease inhibitors in highly active antiretroviral therapy also has additional benefits, as protease inhibitors appear to directly interfere with the life cycle of the parasite[126]. This study was part of the project funded by MARA Drugs combination is implemented in treatment of University of Technology Excellence Fund [Grant No. 600- T RMI ST DANA 5 3 D (334 2011) cryptosporidiosis. he efficiency o Streptomycesf paromomycin, an / / / / st / ]. aminocyclitol antibiotic isolated from , can be [126] effective when combined use with protease inhibitors or Comments recombinant IL-12[127]. S Cryptosporidiumince there is no drug that achieves the complete removal Background of from the host, supportive therapy was T C preferred in both human and domestic animals. his consists ryptosporidiosis isCryptosporidium a parasitic disease caused by coccidial of replacement of fluid and electrolytes, nutritional support, species of the genus . Cryptosporidiosis has and anti-diarrhoeal drugs[128]. become recognized as one of the most common causes of waterborne disease in humans in every region of the world 8. Prevention, control and conclusion including developed and undeveloped countries. Research frontiers Cryptosporidium sp. could infect its host by three main This review article has overviewed the pathogenesis, routes. The first is through contamination of raw food distribution, diagnosis and treatment of cryptosporidiosis. ingredients from farms or abattoirs. The second is through Information in this article will give physicians and young contaminated water whether from unprocessed sources scientists a comprehensive overview on cryptosporidiosis (rivers, wells) or from water treatment plants. The third and this article will be helpful in controlling and prevention is transfered from infected host such as unhygienic food of cryptosporidiosis. [129,130] handlers, pets, or pests like flies and cockroaches . Related reports T Cryptosporidium aking preventive measures is the best way to manage sp. infection. Raw vegetables and food This article has selectively reviewed 132 articles selected must be washed thoroughly before consumption. Clean from a large number of original articles and review articles Nurul Fariza Rossle and Baha Latif/Asian Pac J Trop Biomed 2013; 3(11): 916-924 921

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The information is based on Cryptosporidium 1907 2013 Identification of 5 types of parasites in children articles published from to . J Infect Dis 183 in Lima, Peru. 2001; : 492- 497. Applications Cryptosporidium [14] X iao L, Fayer R, Ryan U, Upton SJ. taxonomy: Clin T recent advances and implications for public health. his article provided information on the research on Microbiol Rev 17 2004; : 72-97. cryptosporidiosis. The updated information in the article Cryptosporidium [15] F ayer R. Taxonomy and species delimitation in . including pathogenesis, diagnosis and treatment of Exp Parasitol 124 2010; (1): 90-97. cryptosporidiosis will be very helpful to physicians who do Cryptosporidium [16] F ayer R, Morgan U, Upton SJ. Epidemiology of : not have time to go through large quantities of articles. Int J Parasitol 30 transmission, detection and identification. 2000; : Peer review 1305-1322. 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