Journal of the Egyptian Society of Parasitology, Vol.44, No.1, April 2014 J. Egypt. Soc. Parasitol. (JESP), 44(1), 2014: 161 - 171

SOME STUDIES ON PHILIPINENSIS AND ITS MYSTERIOUS TRIP FROM PHILIPPINES TO EGYPT (REVIEW ARTICLE) By REFAAT M.A. KHALIFA AND RAGAA A. OTHMAN Department of Medical Parasitology, Faculty of Medicine, Assiut University (e-mail correspondence: [email protected]) Abstract Capillaria philippinensis is a mysterious parasite and intestinal is a mysterious disease. It is now more than half a century since the discovery of the first case in Philippines without answering many questions concerning the parasite's , morphology, life cycle, diagnosis, pathology, clinical symptoms, mode of transmission as well as how it was transported to Egypt and how it started to spread and progressed in most Egyptian Governorates; particularly those of Middle Egypt. This article is a trial to overview all these aspects of the parasite. Key words: Egypt, Capillaria philipinensism, Egypt, comments, recommendations. Introduction with sporadic cases were reported from The caused by Japan (Mukai et al,1983), Korea(Lee et Capillaria philippinensisis a life-threa- al,1993; Hong et al,1994), Taiwan(Chen et tening disease in humans that causes severe al, 1989, Bair et al,2004, Lu et al,2006), enteropathy (Cross, 1998).The outcome of India Kang et al,1994;Vasantha et al, 2012), the disease may be fatal if untreated in due Iran (Hoghooghi-Rad et al,1987; Rokni, time (Abd-ElSalam et al, 2012). Small 2008), Egypt (Youssef et al,1989; Mansour freshwater and brackish-water fish are the et al,1990, Khalifa et al,2000), Indonesian in source of infection and probably fish-eating Italy(Chichino et al,1992), Egyptians in the birds the reservoir host (Cross, 1998). United Arab Emirates (El-Hassan and Although more than 250 Capillaria species Mikhail, 1992; Austin et al, 1999) and Spain have been found in fish, amphibians, (Dronda et al,1993). reptiles, birds and mammals, only 3 species The first outbreak was in a small village in have been found in humans: C. philippi- Thailand in 1981 involving 20 patients and 9 nensis, C. hepatica and C. aerophila (Eucol- deaths. Most of the cases were adults who eusaerophilus). Reports of human infections were over 20 years of age and 80% of them with C. hepatica, C. aerophila are rare, but habited in the same household with a wrong reports of C. philippinensis infections are belief of man to man transmission (Kunara- increasing and appear to be spreading tanapruk et al, 1981). Kunaratanapruk et al. geographically (Cross, 1992). (1983) reported that 100 cases of C. The first human case of intestinal philippinensis infection had occurred from capillariasis was reported in the Philippines 1979 to 1981. Out of them 15 cases died. in 1963 (Chitwood et al, 1964) while the Later on other case records were re-ported first record of the disease in Thailand was in (Benjanuwattar et al, 1990; Chunlertrith et 1973 (Pradatsundarasar et al, 1973), then al, 1992; Sangcha et al, 2007). more and more cases were detected from No doubt, Capillaria philippinensis is a both Philippines and Thailand (Sanpakit et mysterious parasite and intestinal al., 1974; Bhaibulaya, 1975; Cross and capillariasis is a mysterious disease. It is Bhaibulaya, 1983). Now more than 2,000 now about half a century since the discovery cases of intestinal capillariasis have been of the first case of the disease in Philippines reported from the Philippines and Thailand, without answering many questions con-

161 cerning the parasite's taxonomy, morpho- (females may produce larvae; adults in logy, life cycle, diagnosis, pathology, warm-blooded ; larvae in fishes). clinical symptoms, mode of transmission as Sukontason et al. (2006), Nunez et al. well as how it was transported to Egypt and (2010) accepted the classification and named how it started to spread and progressed in it P. Crossicapillaria philippinensis. In the most Egyptian governorates; particularly present authors’ opinion, these differences those of Middle Egypt. This article is a trial are not sufficient to create a new or to overview all these aspects of the parasite. subgenus and we should not mix between Classification and Taxonomy: According to human capillarids and those of birds, fishes, Chitwood et al. (1968) this parasite belongs reptiles and amphibians as the latter to Phylum Nematoda Class Adenophorea, parasites have different morphology, mode Subclass Enoplia, Order Trichocephalida, of transmission and life cycles. Moreover, C. Family , Genus Capillaria, philippinensis is the name given to the species philippinensis. On basis of the parasite by the majority of medical inaccurate original description given by parasitologists. Chitwood et al. (1968), Moravec (1982) Description of the parasite: Although C. assigned this parasite provisionally to philippinensis has been extensively studied Anochotheca LopezNeyera, 1947 whereas over the past 50 years, the only existing Anderson (1992) without giving a reason description of this nematode is that named it Colodium philippinensis. Until originally made by Chitwood et al. (1968). recently, the species have generally been Chitwood et al. (1964) described the parasite reported as Capillaria philippinensis in the from specimens collected at autopsy from medical literature (e.g. Hong et al, 1994; the first person known to have the infection Kang et al, 1994; Vilairatauna, 1994; Anis et and in material obtained from several al, 1998; Hwang, 1998), but Moravec (2001) subsequent autopsies. More specimens were redescribed the parasite and found his examined by other investigators, and the description fully corresponding that of initial findings were confirmed. As most of Paracapillaria, Mendonaca, 1963 as refined the laboratory investigators used to find by Moravec (1982) that included calliparids eggs, larvae and adults in the patient's stools, of fishes, amphibians and reptiles. As they should be familiar with the detailed compared to the known Paracapillaria spp morphological features of all the stages of known from cold-blooded hosts, C. phili- the parasite. ppinensis is unique in that its females may According to Moravec (2001), Attia et al. produce free 1st stage larvae besides normal (2012): Male: Length 2.162-3.114µm, thick-walled unembryonated eggs. All Para- maximum width 30-36µm. Entire esophagus capillaria spp. are known to produce only 1.170-1.646 µm long (53-57% of body unembryonated thick-shelled eggs except length). Muscular esophagus measuring 138- Paracapillaria rhamdiae which is a stomach 177µm. Stichosome 1.029-1.484µm long parasite of catfishes in Mexico that may lay (15-19% of body length). Posterior end of eggs containing already formed larvae, but body rounded, provided with well-developed no hatched larvae were observed in uterus membranous bursa, supported by 2 rather (Moravec et al, 1995). Moravec (2001) in a wide digital lateral projections, not reaching key form divided the genus Paracapillaria to posterior margin of bursa, projections into three subgenera according to the directed posteriorly in lateral view and females being oviparous or larviparous and curved to median line in ventral view. One adults being in worm blooded vertebrates or pair of large round postanal papillae present cold blooded fishes, amphibians and reptiles. at base of caudal projections. Spicule 411- The first subgenus was Crossicapillaria 468um in length, 6-12; 4-5; 3-4um in width

162 at anterior end, middle part; posterior end larvae represent an important diagnostic respectively; its anterior end somewhat stage, laboratory staff should be aware of expanded; posterior end rounded; covered their structure. So, it is easy to differentiate with very long spineless sheath (about them from Strongyloides stercoralis larvae 400um). Female: Length 2.870-3.971µm, which have rhabditiform esophagus. maximum width at the posterior body part Eggs: Peanut-shaped with flattened bi- 36-48µm. Length of entire esophagus 1.224- polar plugs and striated shells (Zhigang et 1.659µm, representing 42-47% of body al, 2012). They contain either a single cell- length, muscular esophagus 120-180µ long, stage embryo or larvae. An inexperienced stichosome 1.104-1.515µm long. Sticho- laboratory worker may confuse them with cytes on the posterior portion appeared trichiura eggs which are barrel- somewhat larger than those on the anterior shaped and have prominent mucoid bipolar portion. Vulva located 24–36 µm posterior plugs (Saichua et al, 2008). According to to the esophagus. The uterus contained one Cross (1992), Anderson (2000), Moravec row of either thin- or thick-shelled eggs with (2001) and Attia et al. (2012), there are two defined or ill-defined embryos. Posterior types of C. philippinensis eggs: I- The thick- end rounded, and the anus subterminal. shelled eggs: peanut-shaped and had a Larvae: These stages were first satisfactorily yellowish-brown color, measuring40-48 x described (Chitwood et al,1968) as follows: 17-20 µm with inconspicuous flattened L1 is the smallest with a double row of bipolar plugs measuring 2-3.6 x 9-12 µm. stichocytes and esophagus about 4/5th the The wall thickness is 2-3 µm. Eggs usually body length; L2 is 417-550 um in length contain a single cell stage embryo that filled with double row of stichocytes in the most of the egg. Some eggs have a slipper or esophagus which is approximately 2/3rd the kidney shaped appearance (Khalifa et al, body length, genital column starts to appear; 2000). II- The thin-shelled eggs: peanut- L3 is 1.25 mm in length, most of the shaped measuring 38-45.6 x18-20 µm. They stichocytes are in one column and oral spear are translucent or yellowish in color having apparent, anterior genital column almost single cell-stage embryos or gradually complete and posterior one beginning to maturating larvae with two characteristically develop. L4 started the differentiation of the rounded mucoid plugs protruding from their future sex, but differ from adults in size and poles. III- Khalifa et al. (2000) added the body proportions and sclerotization of the abnormally swollen eggs: lacking one or spicule in males and vaginal development in both mucoid plugs which appeared un- females. No other detailed description of embryonated (unfertilized) and contained the larvae was given up till now, except that degenerated cells or refractile granules that reported by El-Dib et al. (1999a) who partially or completely filled the inner space described the 1st larval stage (130-150 u with of the egg. Swollen thin-shelled eggs with a esophagus more than three quarters of body smooth surface and non-apparent polar plugs length and formed of a double layer of at each end were also detected (Anderson, stichocytes) but found that the exact 2000; Moravec, 2001; Attia et al, 2012). demarcation between other different larval The size of both the thick and the thin- stages was not clear. Their description was shelled eggs detected by Attia et al. (2012) satisfactory and documented by clear was smaller than that found by Moravec pictures while Moravec (2001) described the (2001) but was slightly larger than those free larvae in uterus to be measuring 156- found by Cross (1992) and Khalifa et al. 183µm long and 6-9µm wide, with both (2000). In general, the thin-shelled eggs ends wide; giving no details of the larval were smaller than the thick-shelled eggs contents and stage of development. As (Moravec, 2001; Attia et al, 2012). Sukonta-

163 sonet al. (2006) using SEM described both (Black-crowned night heron), Bubulcus ibis thick- and thin-shelled eggs. Two distinct (Cattle Egret=Abo Kerdan), Ixobrychus morphological shapes of pea-nut-shaped sinensis (Yellow Bittern), Gallinula chloro- thick-shelled eggs were detected, and these pus (Common Moorhen=swamp chicken), consisted of the typical elongated egg and and Rostratula benghalensis (Greater the swollen egg. Moreover, an intermediate- painted Snipe), with larvae yielded mature shaped egg that appeared to have a partial adults (Saichua et al, 2008). beam-like network on its surface was There was failure to infect laboratory rats observed, but this shape was not observed in from embryonated eggs resulting from study the SEM study of Attia et al. (2012). No done by Cross (1990; 1992) and Khalifa et doubt, SEM added some ultrastructural al. (2000). An experimental infection of fish details to egg morphology, but these did not Oreochrois nilotica nilotica with eggs and/ seem to be of importance in the routine or larvae was attempted in Egypt by El-Dib laboratory egg identification. and Doss (2002) and Attia et al. (2012) Life cycle: The life cycle of C. philipp- without success. The local Egyptian fishes inensis was proposed (Cross, 1992) while its surveyed for nematode larvae recorded only complete cycle was given in experimental other capillarids (Capillaria yamaguti and studies, and may be either indirect C. fischi (Tadros and Mahmoud, 1986). (involving an intermediate host) or direct; According to Moravec (2001), fish-eating complete in one host (Saichua et al, 2008). birds may not be natural hosts for the Indirect life cycle: Fish-eating birds which parasite and in his opinion; the natural harbor adults in their intestines, shed definitive hosts of C. philippinensis remain embryonated eggs in their feces. When obscure. The present authors agree with that engulfed by uninfected fish, larvae are opinion and recommend future studies to be recovered from their intestines. When these done to explore the exact life cycle of the fishes are fed to uninfested birds, larvae parasite and to find out the final and develop into adults in their intestinal tract. intermediate hosts of the parasite in Egypt Larvae recovered from the fish also which are unknown up till now. developed into adults when experimentally Cross et al. (1978) succeeded in expe- fed to gerbils or monkeys (Bhaibulaya et al, rimental infection of Mongolian gerbil 1979). Naturally infested fish (Hypseleotris (Merionis unguicalatus) and short-lasting bipartita and Apagon sp.) and birds infection in a very small number of wild rats (Ixobrychus sp.) have also been found. (Rattus norvegicus and Rattu srattus) in Humans become infected when they eat raw which they never found natural infection. or undercooked whole small fish, which Thus, they recommended to use Mongolian have the infective larvae in their intestinal gerbils for keeping the laboratory infection tract. While the natural host range is not for parasitic studies by serial passages from known, experimental infections of several gerbil to another. Furthermore, El-Shazly et fishes, including Cyprinus carpio (Common al. (2008) in a cross-sectional survey of hel- Carp), Puntius gonionotus (Java Barb), minthes in 271 rodents of Rattus norvegicus, Rasbora borapetensis (Red-tailed Raspora), Rattus rattus frugivorous, Rattus r. alexan- Eleotris melanosoma (Broad-head Sleeper), drines and Mus musculus from Dakahlia and Ambassis commersoni and Apagon sp., with Menoufia Governorates, reported a total of C. philippinensis eggs yielded infective 24 species of helminthes; C. philippinensis larvae. Experimental infections of several was not among them. birds, including Amaurornis phoenicurus Direct life cycle: Researchers also found White breasted waterhen), Ardeola bacchus that feeding just a few dozen larvae from the (Chinese pond heron), Nycticorax nycticorax intestines of fish to Mongolian gerbils

164 (Meriones unguiculatus) or monkeys (Mac- and albumin in the blood of patients (Lu et aca sp.) led to infection with thousands of al, 2006; Saichua et al, 2008). adult worms through autoinfection. The According to Attia et al. (2012), in SEM; experimentally infested monkeys never the unexplained tight obscure membrane that developed any clinical symptoms, even covered nearly the entire surface of the adult during the prolonged active worms may have been the result of an (seeming to act as reservoir hosts). Of intense inflammatory reaction by the several rodents tested, only Mongolian immune system of the host. Bunches of gerbils developed severe symptoms due to intestinal villi that covered the cuticle and and died (Saichua et al, 2008). In plugged the mouth opening may be related the present author's opinion, autoinfection is to the mucosal penetration that is commonly different from direct life cycle which mean initiated by the worm and that manifests as the possibility of person to person infection; severe . In their study, each of the a condition which was never recorded in cases presented with various degrees of cases of human capillariasis. intestinal manifestations that included inter- Clinical manifestations and pathogenesis: mittent abdominal pain, borborygmi, chronic Intestinal capillariasis is a life-threatening (continuous or intermittent) diarrhea lasting disease in humans that causes severe entero- several weeks, and marked weight loss (up pathy (Cross, 1998). Intestinal capillariasis to 10 kg). In addition, these patients had patients usually present with watery various degrees of painless lower leg , diarrhea, weight loss, abdominal pain, bor- which is corresponding with the results of borygmi, muscle wasting, weakness, edema Ahmed et al. (1999) and Lu et al. (2006). and laboratory examination shows low El-Karaksyet al. (2004) reported two levels of potassium and albumin in blood, infected Egyptian sisters from El-Menia and malabsorption of fats and sugar. Those Governorate in which the previous clinical patterns may result from C. philippinensis pictures were detected in addition to the secretion of a proteolytic substance or direct presence of hyponatremia. Lu et al. (2006) penetration of the intestinal wall that causes found that when a diagnosis was finally cellular injury and dysfunction (Saichua et made, some cases already showed clinical al, 2008). Several studies showed intestinal symptoms of septic shock. If the infection pathological findings in C. philippinensis remains untreated, it leads to death. Attia et infection because the worms can be found in al. (2012) found many potential early cases the lumen, the mucosa, or in the crypts of of this infection needed to be differentiated Lieberkuhn in the human jejunum. The most from other diseases with identical clinical common pathological features are the thick- manifestations, such as Crohn’s disease, TB ening of the intestinal wall, the prominence enteritis, and various intestinal malignan- of the vessels, the atrophy of the crypts, and cies. As a result, these cases were evaluated flattening of the villi (Sangcha et al, 2007). using long list of sophisticated measures that Thus, the destruction of the intestinal cell were not diagnostic for intestinal capilla- membrane may interrupt nutrient absorption riasis but did reveal important features that that causes weight loss in intestinal improved knowledge of the pathogenicity of capillariasis patients. Moreover, the intes- this . These additional dia- tinal cells’ destruction may lead to fluids, gnostic measures included a full blood proteins and electrolytes loss because those panel, abdominal ultrasonography (revealing intestinal cells are dysfunctional and cannot pleural effusion and ascites in some pa- control body fluids and electrolytes balance tients), upper endoscopies (gastroduodeno- which results in a low level of potassium scopies that revealed malabsorption) and histopathological examinations of the

165 duodenal and jejunal biopsies (revealing the different Capillaria larval stages, as also atrophic and flattened villi, inflammatory juvenile and adults may be encountered in cell infiltration, and numerous sections of the same stool sample. the adult worm in the epithelial layer). It is 2- Detection of coproantigen may be used worth mentioning that up till now, the to overcome the false negative diagnosis of presence of mild or asymptomatic cases C. philippinesis at time of absence of eggs in (which is usually observed in almost all stool. El-Dib et al. (2004) designed C. phi- intestinal parasites) is absolutely unknown in lippinensis coproantigen to determine its cases of C. philippinensis infections. diagnostic value using two different ELISA Diagnosis: The diagnosis of intestinal techniques. This antigen was able to detect capillariasis is commonly delayed and anti-Capillaria antibodies in the sera of generally requires the experience of medical infected cases at the same OD level parasitologists and the physicians should be produced with Capillaria crude worm particularly sensitized to the consumption of antigen using indirect ELISA technique. C. raw fish which should be asked during philippenensis coproantigen did not cross- anamnesis and made aware of react with sera from patients with schisto- which are transmitted through raw or somiasis mansoni, fascioliasis or strongyloi- insufficiently cooked fish (Dronda et al, diasis at 1:100 serum dilutions. 1993; Zhigang et al, 2012). Reports of 3- Immunodiagnosis may be a supple- delayed diagnoses for more than few months mentary tool which helps to detect C. have been reported in Japan and India philippinensis infection which may be useful (Nawa et al, 1988), Korea (Lee et al, 1993; for screening persons who have intestinal Vasantha et al, 2012), Egypt (El-Dib and capillariasis-like symptoms before discover- Doss, 2002). The areas where C. philippi- ing Capillaria eggs or larvae in their stool. nensis has spread, the number of afflicted Thus, Banzon et al. (1975) used Capillaria countries and the infected cases may far obsignata in IHA test, Abdel-Rahman et al. exceed what one knows so far (Lu et al, (2005) used egg antigen and coproantigen in 2006). The majority of the patients had a diagnosis by immuoblot and Intapan et history of consuming raw or uncooked al.(2006, 2010) used spiralis fishes, and this is a crucial factor of soluble antigen in an immunoblot analysis intestinal capillariasis infection. and ELISA test respectively for diagnosis of The diagnosis depends mainly on: capillariasis cases where eggs and/or larvae 1- Stool examination for detection of eggs, are absent in stools. All cases showed larvae and/or adult worms. Unembryonated positive results. eggs are peanut-shaped with flattened 4- Small intestinal aspiration or biopsy may bipolar plugs and a striated shell. Multiple be necessary to confirm C. philippinensis stool samples may be needed for early infection (Cross, 199l; Lu et al, 2006). diagnosis in some cases as the eggs are shed Gastroduodenoscopy in a 13-year-old boy sporadically and irregularly in feces (Cross, from central Thailand showed the eggs in a 1992). The presence of Charcot-Leyden jejunal biopsy (Wongsawasdi et al, 2002). crystals in the stool samples of the patients Besides, jejunal mucosal biopsy and micro- supported the diagnosis, and number of scopic jejunal content examinations were these crystals is usually correlated with the successfully used to identify intestinal intensity of the the infection (Attia et al, capillariasis in a 27-year-old Thai man who 2012). Larvae may be found in the stools but had negative repeated stool tests (Sangcha et are difficultly diagnosed as those of C. al, 2007). El-Dib and Doss (2002) reported philippinensis (Cross, 1992).This needs one Egyptian case which was diagnosed by accurate and comprehensive description of abdominal laparoscopy. Kang et al. (1994),

166 Hong et al. (1994) and Wongsawasdi et al. Migratory fish-eating birds are considered (2002) had cases definitively diagnosed potential natural hosts, and their migratory based on histopathological findings on habits are considered responsible for disse- panendoscopic jejunal biopsy specimens. mination of the parasite to widely separated Histopathological examination of duodenal parts of the world (Austin et al, 1999). Bird biopsies indicated heavy cellular infiltration droppings along the flyways could easily around the sectioned adult worms and larvae disperse the eggs into water bodies, where (Lee et al, 1993; Abd-El-Salam et al, 2012). fish become infected. Birds and humans Transmission: The eating habits of people eating such fish would subsequently become are responsible for the transmission of infected (Zhigang et al, 2012). human intestinal capillariasis. Populations in The present Senior Author had supervised the Philippines where intestinal capillariasis several M.Sc and M.D Theses throughout is endemic have unique eating habits in that the last three decades on endoparasites of they prefer to eat a variety of sea foods fresh water fishes and wild birds from uncooked. In other countries, consumption Aswan, Qena, El-Minia and Assiut; amphi- of raw fish has been associated with most bians from Sohag and reptiles from Assiut infections (Cross, 1992). Since a number of and is now leading a team work for the study species of freshwater fish have been of endoparasites of Red Sea fishes without experimentally infected with C. philippi- reporting capillarid adults or larvae in all nensis and some fish in the Philippines were these hosts. Capillarid larvae were also not found naturally infected with larval forms of recorded in Ardeola goliath (El-Naffaret al, the parasite (Cross and Bhaibulaya, 1983), it 1980), Burhimus oedinemussahare (Khalifa is believed that the means of transmission of et al, 1989) and amphibians (Khalifa et al., the disease is by eating uncooked fish. Cross 1998). Thus, many unanswered questions (1992) reported that the parasite has not arise: what is the method of infection of C. been found in any area where populations do philippinensis in Egypt while its inter- not eat raw fish. Lu et al. (2006) believed mediate and final hosts are still unknown? that consuming raw or uncooked fishes is a How the parasite could initiate and com- crucial factor of intestinal Capillaria pleted its life cycle in our country? Why the infection. However, nearly all Egyptian parasite is more prevalent in some Middle patients denied having consumed any raw or Egyptian governorates? undercooked fishes. The present authors Intestinal capillariasis in Egypt: As many propose that the infection may occur when Egyptian authors usually publish their the ingested food is contaminated by the researches in unavailable local or university uncooked visceral contents of infested fish. periodicals, this review may be lacking some Therefore, whether patients have consumed of these studies. The incoming works are the raw or uncooked fish ought to be taken into available studies: It is noteworthy to men- consideration but should not be the basis for tion that infection has taken a serious ruling out the possibility of intestinal situation in Egypt with continuous detection capillariasis. Khalifa et al. (2000) stated that of new indigenous cases and it became the it would be very difficult to follow the country with the highest number of reported method of transmission, as infective larvae cases outside the endemic areas (El-Dib and are usually found in the intestine and not in Doss, 2002). The first Egyptian case was muscles of infected fish intermediate host, reported by Youssef et al. (1989) in a 41- meaning that infection only after swallowing year-old female from Cairo; the second case of intact fish (with intact intestine), which is was a 38-year-old female living in Lower not a habit in Egypt. Egypt (Mansour et al, 1990). Many sub- sequent cases have been reported from

167 different parts of Egypt including Cairo (El- the northern parts of Egypt should be more Dib et al, 1992; 1999) and Menouf City greatly affected than Upper Egypt (Ahmed (Mansour et al, 1998; Anis et al, 1998; et al, 1999). Additional hypotheses have Austin et al, 1999b). Ahmed et al. (1999) suggested that imported fish are the more reported four cases; three from Nagaa- likely source of this infection in Egypt, as Hammady City and one from Beni Suif. most of the frozen fish sold at Egyptian Khalifa et al. (2000) recovered the first case markets are imported from the Far East. from Assiut and El-Karkasyet al. (2004) However, because this fish is frozen at very detected two infected sisters in El-Minia low temperatures for a lengthy amount of City. time before consumption makes this theory It was demonstrated that the severity of difficult to accept. The study of Attia et al. intestinal capillariasis cases has grown in (2012) included 19 middle-aged females; Egypt and that the parasite still surprisingly most of them were housewives which may spreading more or less in most of the be related to their role in the preparation and Egyptian Governorates. Thus (El-Dib and cooking of the fish for the family, as they Doss, 2002) who reported 44 cases; 37 would have greater exposure to raw infested females and 7 males: 8 from Cairo, 2 from fish than would males. The actual pre- Menouf, 2 from Banha, 2 from El-Giza, 2 valence of this parasite is likely greater than from Al-Fayoum, 9 from Beni-Suif, 17 from was estimated, but physician incognizance El-Minia, 1 from both Assiut and Qena (30 and technician inexperience at clinical cases from Middle and Upper Egypt). laboratories as well as the availability of Moreover, in Assuit, Attia et al. (2012) over-the-counter anti-helminthic and the reported the first series of 21 patients with intestinal antiseptics have hindered its C. philippinensis infections outside the identification. Therefore, the present authors endemic area which suggests that the emphasized that clinicians should remain parasite has spread across Egypt and may highly alert to recognize the signs of this also indicate the presence of suitable natural treatable infection. Furthermore, the number intermediate and final hosts. Their data of cases of infection with this parasite may seems to answer the question posed by far exceed that estimated for Assuit Gover- Ahmed et al. (1999) as to whether C. norate and other Middle Egyptian governo- philippinensis infection will spread further rates. Actually, Parasitology research labora- across Egypt. tory, Assiut University Teaching Hospital It remains unclear how this disease, which added 2 newly discovered non notified cases is endemic in the Far East, began appearing within the last two months (personal com- in Egypt and other Middle East countries, munication). although it is possible that some of the Control: Strategy to fight the disease imported species of fresh water fish from the consists of not eating raw fish, promoting a Far East were infected. It has been suggested health education program and the early that some fish-eating migratory birds may diagnosisis necessary to minimize and/or acquire this infection by consuming infested eradicate C. philippinensis infection. The fish along migratory pathways and that the health education campaign aims to promote birds could then excrete eggs to infect fish in the consumption of cooked fish and to avoid other remote areas (El-Dib and Doss, 2002). defecation into a water resource in order to However, this theory is disproved because eliminate the infection. Early diagnosis is infected wild birds of the Far East migrate to necessary for treating patients, especially Europe, and it would be unlikely that they improving experience of laboratory techni- could have transmitted this parasite to cians and multiple stool examination Egypt. Furthermore, if this theory was true, (Saichua et al, 2008).The control measures

168 could be reasonable in Far East countries Anderson, RC, 2000:Nematode Parasites of where the parasite's life cycle is known and Vertebrates: Their Development and where populations used to consume raw fish Transmission. Second edition; Oxon, UK: CABI as a traditional habit, but in Egypt, control Publishing. measures could not be planned without Anis, MH, Shafik, H, Mansour, NS, Moo- dy, knowing how the parasite completed its life A, 1998: Intestinal capillariasis as a cause of cycle as well as its mode of transmission. chronic diarrhea in Egypt. J. Egypt. Soc. Parasitol. 28:143-7. Conclusion Attia, AH, Tolba, ME, Yones, DA, Bakir, HY, Capillaria philippinensis has been myste- et al, 2012: Capillaria philippinensis in Upper riously introduced to Egypt since 1989 and Egypt: Has it become endemic? Am. J. Trop. started to spread insidiously and gradually Med. Hyg. 86, 1:126-33. from one governorate to another; so as now Austin, DN, Mikhail, MG, Chiodini, PL, the parasite has been notified throughout Murray-Lyon, LM, 1999:Intestinal capi- almost the whole country. Since that time llariasis acquired in Egypt. Eur. J.Gastro-enterol. (about a quarter of a century); parasitologists Hepatol. 11:935-6. could not get answers to all the mysterious Bair, MJ, Hwang, KP, Wang, TE et al, 2004: questions concerning this parasite. In spite Clinical features of human intestinal capillariasis of the continuous efforts of research in Taiwan. Wld. J. Gastro-enerol. 15, 6:3391-3. workers, we did not found any convincing Banzon, TC, Lewert, RM, Yogore, MG, 1975: replies to how the parasite was introduced to Serology of Capillaria philippinensis: reactivity Egypt, its mode of transmission in absence of human sera to antigen prepared from Capillaria obsignataand other helmi-nthes. Am. of known intermediate and final hosts. J. Trop. Med. Hyg. 24, 2:256-63. Hence, it is highly recommended that a team Benjanuwattar, T, Morakote, N, Somb-oon, work of Biologists, Zoologists, Medical and P, Sivasomboon,B, 1990: Intestinal Veterinary Parasitologists should work capillariasis: indigenous cases from Chiang Mai together; hand in hand to try to explore the and Phayao provinces, Thailand. J. Med. Assoc. mysterious natural intermediate and final Thai. 73:414-7. hosts in which the parasite completes its life Bhaibulaya, MB, 1975: Studies on Ca-pillaria cycle in Egypt as a milestone to our philippinensis in Thailand. 1: Epidemiologic knowledge of its method of transmission and Survey. Report of Thailand Nat. Res. Council: future plans to its control. 11. Bhaibulaya, M, Indra-Ngarm, S, Anan- References thapruti, M, 1979: Freshwater fishes of Abdel-Rahman, SM, Moneib, ME, Sha-hin, Thailand as experimental intermediate host of MS, Abdel Aziz, LA, 2005: Immuno-diagnosis Capillaria philippinensis. Int. J. Parasitol. 9, of Capillaria philippinensis by western blot 2:79-157. using coproantigen and egg antigen. El-Minia Canlas, BC, Cabrera, BD, Davis,U, 1967: Med. Bull. 16, 2: 9-17. Human intestinal capillariasis. II. Patho-logical Abd-Elsalam, N, Hassany, SM, Medhat, M,et features. Acta Med. Philipp. 4:84-91. al, 2012: Capillaria philippinensis:A cause of Chen, CY, Hsieh, WC, Lin, JT, Lu, MC, chronic diarrhea in Upper Egypt. J. Arab. Soc. 1989: Intestrinal capillariasis: A report of a case. Med. Res. 7:10-3 J. Taiwan Med. Assoc. 88: 617-20. Ahmed, L,El-Dib, N, El-Borey, Y, Ibrah-im, Chichino, G, Bernuzzi, AM, Bruno, A,et al. M, 1999: Capillaria philippinensis: An 1992: Intestinal capillariasis acquired in emerging parasite causing severe diarrhea in Indonesia: a case report. Am. J. Trop. Med. Hyg. Egypt. J. Egypt. Soc. Parasitol. 29, 2:483-93. 47:10-12. Anderson, RC, 1992: Nematode Parasites of Chitwood, MB, Velasquez, C, Salazar, N G, Vertebrates: Their development and tran- 1964: Physiological changes in species of smission. CAB Internat.Willingford.UK.

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