Intestinal coccidian parasites as an underestimated cause of travellers’ diarrhoea in Polish immunocompetent patients
-
Matylda Kłudkowska
,
Łukasz Pielok
Abstract
Intestinal coccidian parasites are intracellular protozoa most frequently transmitted during food-borne and water-borne infections. This group of parasites is responsible for acute diarrhoeal illnesses especially among immunocompromised patients. However, they are more frequently detected in immunocompetent individuals including travellers, and they should also be considered as important etiologic factors of travellers’ diarrhoea. We examined 221 immunocompetent patients hospitalized due to acute or chronic diarrhoea and other gastrointestinal symptoms after returning from international journeys to hot climates. A basic microscopical examination and acid – fast staining of stool samples was performed. Each patient was also a part of the epidemiological investigation to define potential risk factors of tropical gastrointestinal infections. Intestinal coccidiosis was confirmed in 12 out of 221 successively hospitalized patients (5.4%). The most common coccidian parasite was Cryptosporidium spp., detected in nine Polish travellers (4.1%). Cyclospora spp. was diagnosed in three cases (1.4%), including two mixed infections with Cryptosporidium spp., and Cystoisospora spp. in two other cases (0.9%). The study has revealed that intestinal coccidian parasites are a significant threat to immunocompetent travellers and should be always considered in the differential diagnosis of gastrointestinal disorders. Therefore, it is necessary to perform specialized diagnostic methods for the detection of Cryptosporidium spp., Cystoisospora spp., and Cyclospora spp. oocysts in reference parasitology laboratories. Clinical observations demonstrated simultaneously an insufficient level of knowledge in Polish tourists concerning the main risk factors of intestinal parasitic diseases during international travels, particularly to developing countries with lower economic and sanitary conditions.
References
Agnamey P., Djeddi D., Oukachbi Z., Totet A., Raccurt C.P. 2010. Cryptosporidium hominis and Isospora belli diarrhea in travelers returning from West Africa. Journal of Travel Medicine, 17, 141–142. 10.1111/j.1708-8305.2010.00393.xSuche in Google Scholar
Ashford R.W. 1979. Occurrence of an undescribed coccidian in man in Papua New Guinea. Annals of Tropical Medicine and Parasitology, 73, 497–500. 10.1080/00034983.1979.11687291Suche in Google Scholar
Bednarska M., Bajer A., Welc-Falęciak R., Pawełas A. 2015. Cyclospora cayetanensis infection in transplant traveller: a case report of outbreak. Parasites & Vectors, 8, 411. 10.1186/s13071-015-1026-8Suche in Google Scholar
Betancourt W.Q., Duarte D.C., Vásquez R.C., Gurian P.L. 2014. Cryptosporidium and Giardia in tropical recreational marine waters contaminated with domestic sewage: estimation of bathing-associated disease risks. Marine Pollution Bulletin, 85, 268–273. 10.1016/j.marpolbul.2014.05.059Suche in Google Scholar
Bohaychuk V.M., Bradbury R.W., Dimock R., Fehr M., Gensler G.E., King R.K., et al. 2009. A microbiological survey of selected Alberta-grown fresh produce from farmers’ markets in Alberta, Canada. Journal of Food Protection, 72, 415–420. http://dx.doi.org/10.4315/0362-028X-72.2.41510.4315/0362-028X-72.2.415Suche in Google Scholar
Briggs A.D., Boxall N.S., Van Santen D., Chalmers R.M., McCarthy N.D. 2014. Approaches to the detection of very small, common, and easily missed outbreaks that together contribute substantially to human Cryptosporidium infection. Epidemiology & Infection, 142, 1869–1876. 10.1017/S0950268814000673Suche in Google Scholar
Certad G., Arenas-Pinto A., Pocaterra L., Ferrara G., Castro J., Bello A., Núñez L. 2003. Isosporiasis in Venezuelan adults infected with human immunodeficiency virus: clinical characterization. American Journal of Tropical Medicine and Hygiene, 69, 217–222. https://doi.org/10.4269/ajtmh.2003.69.217Suche in Google Scholar
Chandra V., Torres M., Y.R. Ortega. 2014. Efficacy of wash solutions in recovering Cyclospora cayetanensis, Cryptosporidium parvum, and Toxoplasma gondii from basil. Journal of Food Protection, 77, 1348–1354. 10.4315/0362-028X.JFP-13-381Suche in Google Scholar
Checkley W., White Jr. A.C., Jaganath D., Arrowood M.J., Chalmers R.M., Chen X.M., et al. 2015. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for cryptosporidium. Lancet Infectious Diseases, 15, 85–94. 10.1016/S1473-3099(14)70772-8Suche in Google Scholar
Dash M., Padhi S., Panda P., Parida B. 2013. Intestinal Protozoans in Adults with Diarrhea. North American Journal of Medical Sciences, 5, 707–712. 10.4103/1947-2714.123261Suche in Google Scholar PubMed PubMed Central
Din N.U., Torka P., Hutchison R.E., Riddell S.W., Wright J., Gajra A. 2012. Severe Isospora (Cystoisospora) belli Diarrhea Preceding the Diagnosis of Human T-Cell-Leukemia-Virus-1-Associated T-Cell Lymphoma. Case Reports in Infectious Diseases, vol. 2012, Article ID 640104. 10.1155/2012/640104Suche in Google Scholar PubMed PubMed Central
DuPont HL. 2009. Systematic review: the epidemiology and clinical features of travellers’ diarrhoea. Alimentary Pharmacology & Therapeutics, 30, 187–196. 10.1111/j.1365-2036.2009.04028.xSuche in Google Scholar PubMed
Eraky M.A., El-Hamshary A.M.-S., Hamadto H.H., Abdallah K.F., Abdel-Hafed W.M., Abdel-Had S. 2014. Predominance of Cryptosporidium parvum genotype among diarrheic children from Egypt as an indicator for zoonotic transmission. Acta Parasitologica, 60, 26–34. 10.1515/ap-2015-0004Suche in Google Scholar PubMed
Godiwala T., Yaeger R. 1987. Isospora and traveler’s diarrhea. Annals of Internal Medicine, 106, 908–909. 10.7326/0003-4819-106-6-908_2Suche in Google Scholar PubMed
Gupta A.K. 2011. Intestinal coccidian parasitic infections in rural community in and around Loni, Maharashtra. Journal of Parasitic Diseases, 35, 54–56. 10.1007/s12639-011-0030-y.Suche in Google Scholar PubMed PubMed Central
Herwaldt B.L. 2000. Cyclospora cayetanensis: a review, focusing on the outbreaks of cyclosporiasis in the 1990s. Clinical Infectious Diseases, 31, 1040–1057. 10.1086/314051Suche in Google Scholar PubMed
Karanis P., Kourenti C., Smith H. 2007. Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. Journal of Water and Health, 5, 1–38. doi.org/10.2166/wh.2006.002Suche in Google Scholar
Kasper M.R., Lescano A.G., Lucas C., Gilles D., Biese B.J., Stolovitz G., Reaves E.J.. 2012. Diarrhea Outbreak during U.S. Military Training in El Salvador. PLoS One, 7, e40404. 10.1371/journal.pone.0040404Suche in Google Scholar PubMed PubMed Central
Kendall M.E., Crim S., Fullerton K., Han P.V., Cronquist A.B., Shiferaw B., et al. 2012. Travel-associated enteric infections diagnosed after return to the United States, Foodborne Diseases Active Surveillance Network (FoodNet), 2004-2009. Clinical Infectious Diseases, 54, 480–487. 10.1093/cid/cis052Suche in Google Scholar PubMed
Kim M.J., Kim W.H., Jung H.C., Chai J.W., Chai J.Y. 2013. Isospora belli Infection with Chronic Diarrhea in an Alcoholic Patient. Korean Journal of Parasitology, 51, 207–212. 10.3347/kjp.2013.51.2.207Suche in Google Scholar PubMed PubMed Central
Koru O., Araz E., Inci A., Tanyuksel M. 2006. Co-infection of Giardia intestinalis and Cyclospora cayetanensis in an immunocompetent patient with prolonged diarrhea: case report. Journal of Microbiology, 44, 360–362Suche in Google Scholar
Legua P., Seas C. 2013. Cystoisospora and cyclospora. Current Opinion in Infectious Diseases, 26, 479–483. 10.1097/01.qco.0000433320.90241.60Suche in Google Scholar PubMed
Malik A., Kulaar J., Shukla R., Dutta V. 2013. Triple protozoal enteropathy of the small intestine in an immunocompromised male: A rare histopathology report. Indian Journal of Sexually Transmitted Diseases, 34, 119–122. 10.4103/0253-7184.120548Suche in Google Scholar PubMed PubMed Central
Mallet V. 2015. The Ganges: holy, deadly river. Financial Times, http://www.ft.com/cms/s/2/dadfae24-b23e-11e4-b380-00144feab7de.html#slide.Suche in Google Scholar
Masucci L., Graffeo R., Siciliano M., Franceschelli A., Bugli F., Fadda G. 2008. First Italian case of cyclosporiasis in an immunocompetent woman: local acquired infection. New Microbiologica, 31, 281–284Suche in Google Scholar
McHardy I.H., Wu M., Shimizu-Cohen R., Couturier M.R., Humphries R.M.. 2014. Detection of intestinal protozoa in the clinical laboratory. Journal of Clinical Microbiology, 52, 712–720. 10.1128/JCM.02877-13Suche in Google Scholar PubMed PubMed Central
Milord F., Lampron-Goulet E., St-Amour M., Levac E., Ramsay D. 2012. Cyclospora cayetanensis: a description of clinical aspects of an outbreak in Quebec, Canada. Epidemiology & Infection, 140, 626-632. 10.1017/S095026881100121XSuche in Google Scholar PubMed
Miró J.M., Buira E., Mallolas J., Gallart T., Moreno A., Zamora L., et al. 1994. CD4+ lymphocytes and opportunistic infections and neoplasms in patients with human immunodeficiency virus infection (in Spanish). Medicina Clinica (Barc), 102, 566–570Suche in Google Scholar
Nair P., Mohamed J.A., DuPont H.L., Flores Figueroa J., Carlin L.G., Jiang Z.D., et al. 2008. Epidemiology of cryptosporidiosis in North American travelers to Mexico. American Journal of Tropical Medicine and Hygiene, 79, 210–214. https://doi.org/10.4269/ajtmh.2008.79.210Suche in Google Scholar
Navaneethan U., Venkatesh P.G., Downs-Kelly E., Shen B. 2012. Isospora belli superinfection in a patient with eosinophilic gastroenteritis – a diagnostic challenge. Journal of Crohn’s and Colitis, 6, 236–239. 10.1016/j.crohns.2011.08.010Suche in Google Scholar PubMed
Omoruyi B.E., Nwodo U.U., Udem C.S., Okonkwo F.O. 2014. Comparative diagnostic techniques for Cryptosporidium infection. Molecules, 19, 2674–2683. 10.3390/molecules19022674Suche in Google Scholar PubMed PubMed Central
Ortega Y.R., Sanchez R. 2010. Update on Cyclospora cayetanensis, a Food-Borne and Waterborne Parasite. Clinical Microbiology Reviews, 23, 218–234. 10.1128/CMR.00026-09Suche in Google Scholar PubMed PubMed Central
Pandey P., Bodhidatta L., Lewis M., Murphy H., Shlim D.R., Cave W., et al. 2011. Travelers’ diarrhea in Nepal: an update on the pathogens and antibiotic resistance. Journal of Travel Medicine, 18, 102–108. 10.1111/j.1708-8305.2010.00475.xSuche in Google Scholar PubMed
Paschke C., Apelt N., Fleischmann E., Perona P., Walentiny C., Löscher T., Herbinger K.H. 2011. Controlled study on enteropathogens in travellers returning from the tropics with and without diarrhoea. Clinical Microbiology & Infection, 17, 1194–1200. 10.1111/j.1469-0691.2010.03414.xSuche in Google Scholar PubMed
Pérez-Ayala A., Monge-Maíllo B., Díaz-Menéndez M., Norman F., Pérez-Molina J.A., López-Vélez R. 2011. Self-limited travelers’ diarrhea by Isospora belli in a patient with dengue infection. Journal of Travel Medicine, 18, 212–213. 10.1111/j.1708-8305.2010.00494.xSuche in Google Scholar
Porter C.K., Riddle M.S., Tribble D.R., Putnam S.D., Rockabrand D.M., Frenck R.W., et al. 2010. The epidemiology of travelers’ diarrhea in Incirlik, Turkey: a region with a predominance of heat-stabile toxin producing enterotoxigenic Escherichia coli. Diagnostic Microbiology and Infectious Diseases, 66, 241–247. 10.1016/j.diagmicrobio.2009.10.002Suche in Google Scholar
Putignani L., Menichella D. 2010. Global Distribution, Public Health and Clinical Impact of the Protozoan Pathogen Cryptosporidium. Interdisciplinary Perspectives on Infectious Diseases, vol. 2010, Article ID 753512. 10.1155/2010/753512Suche in Google Scholar
Quintero-Betancourt W., Peele E.R., Rose J.B. 2002. Cryptosporidium parvum and Cyclospora cayetanensis: a review of laboratory methods for detection of these waterborne parasites. Journal of Microbiology Methods, 49, 209–224. 10.1016/S0167-7012(02)00007-6Suche in Google Scholar
Rao A.C.K., Geetha V., Kudva R., Vidhyalakshmi S., Rupashree S. 2014. Histology as a diagnostic tool for intestinal isosporiasis in immunocompromised patients. Asian Pacific Journal of Tropical Disease, 2, 251–252. 10.1016/S2222-1808(12)60055-3Suche in Google Scholar
Ribes J.A., Seabolt J.P., Overman S.B. 2004. Point prevalence of Cryptosporidium, Cyclospora, and Isospora infections in patients being evaluated for diarrhea. American Journal of Clinical Pathology, 122, 28–32. 10.1309/AUJ5-WKE0-497X-KRUUSuche in Google Scholar PubMed
Riddle M.S., Rockabrand D.M., Schlett C., Monteville M.R., Frenck R.W, Romine M., et al. 2011. A prospective study of acute diarrhea in a cohort of United States military personnel on deployment to the Multinational Force and Observers, Sinai, Egypt. American Journal of Tropical Medicine and Hygiene, 84, 59–64. 10.4269/ajtmh.2011.10-0093Suche in Google Scholar PubMed PubMed Central
Romeu J., Miró J.M., Sirera G., Mallolas J., Arnal J., Valls M.E., et al. 1991. Efficacy of octreotide in the management of chronic diarrhoea in AIDS. AIDS, 5, 1495–149910.1097/00002030-199112000-00012Suche in Google Scholar PubMed
Rzezutka A., Nichols R.A., Connelly L., Kaupke A., Kozyra I., Cook N., et al. 2010. Cryptosporidium oocysts on fresh produce from areas of high livestock production in Poland. International Journal of Food Microbiology, 139, 96–101. 10.1016/j.ijfoodmicro.2010.01.027Suche in Google Scholar PubMed
Sancak B, Akyon Y., Ergüven S. 2006. Cyclospora infection in five immunocompetent patients in a Turkish university hospital. Journal of Medical Microbiology, 55, 459–462. 10.1099/jmm.0.46279-0Suche in Google Scholar PubMed
Vignesh R., Balakrishnan P., Shankar E.M., Murugavel K.G., Hanas S., Cecelia A.J., et al. 2007. High Proportion of Isosporiasis among HIV-Infected Patients with Diarrhea in Southern India. American Journal of Tropical Medicine and Hygiene, 77, 823–824. https://doi.org/10.4269/ajtmh.2007.77.823Suche in Google Scholar
Vuong T.A., Nguyen T.T., Klank L.T., Phung D.C., Dalsgaard A. 2007. Faecal and protozoan parasite contamination of water spinach (Ipomoea aquatica) cultivated in urban wastewater in Phnom Penh, Cambodia. Tropical Medicine and International Health, 12, 73–81. 10.1111/j.1365-3156.2007.01944.xSuche in Google Scholar PubMed
Widerström M., Schönning C., Lilja M., Lebbad M., Ljung T., Allestam G., et al. 2014. Large outbreak of Cryptosporidium hominis infection transmitted through the public water supply, Sweden. Emerging Infectious Diseases, 20, 581–589. 10.3201/eid2004.121415Suche in Google Scholar PubMed PubMed Central
Wilhelm C.L., Yarovinsky F. Apicomplexan infections in the gut. 2014. Parasite Immunology, 36, 409–420. 10.1111/pim.12115Suche in Google Scholar PubMed
© 2017 W. Stefański Institute of Parasitology, PAS
Artikel in diesem Heft
- Review
- Snail species diversity impacts the infection patterns of Echinostoma spp.: Examples from field collected data
- Molecular phylogeny of the Haplosplanchnata Olson, Cribb, Tkach, Bray and Littlewood, 2003, with a description of Schikhobalotrema huffmani n. sp.
- Structuraland antigenic analysis of a new Rhoptry Pseudokinase Gene (ROP54) in Toxoplasma gondii
- Ultrastructure of the spermatozoon of Macvicaria obovata (Digenea: Opecoelidae), a parasite of Sparus aurata(Pisces: Teleostei) from the Gulf of Gabès, Mediterranean Sea
- Epidemiology of Toxoplasma gondii infection in native Tibetans in Tibet, China
- A PCR survey of vector-borne pathogens in different dog populations from Turkey
- Diplectanids (Monogenea) parasitic on sciaenid fish from Peru with the proposal of Pseudorhamnocercoides n. gen., the description of Rhamnocercus dominguesi n. sp. and the redescription of Rhamnocercoides menticirrhi Luque and Iannacone, 1991
- Differentiation of Toxocara canis and Toxocara cati based on PCR-RFLP analyses of rDNA-ITS and mitochondrial cox1 and nad1 regions
- The Prevalence of Cyclospora cayetanensis and Cryptosporidium spp. in Turkish patients infected with HIV-1
- Molecular characterization and functional analysis of a glutathione peroxidase gene from Aphelenchoides besseyi (Nematoda: Aphelenchoididae)
- Durettenema guangdongense gen. et sp. nov. (Nematoda: Molineoidea) from Hipposideros larvatus (Horsfield) (Chiroptera: Rhinolophidae) with discussion of the taxonomic status of Macielia rhinolophi Yin, 1980
- In vitro effects of purine and pyrimidine analogues on Leishmania donovani and Leishmania infantum promastigotes and intracellular amastigotes
- Population structure of the monogenean, Paramazocraes thrissocles (Mazocraeidae) on the gills of clupeoid fish, Thryssa mystax of Visakhapatnam coast, Bay of Bengal
- Redescription of Eutarsopolipus elongatus Regenfuss, 1968 (Acari: Podapolipidae) parasitising carabid beetles, with first description of the male
- Seroprevalence and risk factors of Neospora spp. and Toxoplasma gondii infections among horses and donkeys in Nigeria, West Africa
- Spinicauda sumatrana sp. nov. (Nematoda: Heterakidae) from Ludeking’s Crested Dragon, Lophocalotes ludekingi (Agamidae), from the Bukit Barisan Range of Sumatra
- The systematic position and structure of the genus Leyogonimus Ginetsinskaya, 1948 (Platyhelminthes: Digenea) with comments on the taxonomy of the superfamily Microphalloidea Ward, 1901
- Leishmania infantum is present in vaginal secretions of naturally infected bitches at lower levels in oestrogenized bitches than in non-oestrogenized bitches
- Intestinal coccidian parasites as an underestimated cause of travellers’ diarrhoea in Polish immunocompetent patients
- Hymenolepididae (Cestoda, Cyclophyllidea) of ciconiiform and pelecaniform birds: the genera Oschmarinolepis Spassky and Spasskaja, 1954 and Paraoschmarinolepis gen. n.
- Redescription of two species of Thaparocleidus (Monogenea: Dactylogyridae), with the description of T. armillatus sp. n. from Wallago attu and a phylogenetic analysis based on 18S rDNA sequences
- In vitro and in vivo studies of nematophagous fungi Arthrobotrys musiformis and Arthrobotrys robusta against the larvae of the trichostrongylides
- Three monogeneans parasitic on marine sciaenid fish from Peru including description of Cynoscionicola veranoi n. sp. (Microcotylidae), and redescription of C. americanus Tantaleán, Martínez and Escalante, 1987 and Hargicotyle sciaenae Oliva and Luque, 1989 (Diclidophoridae)
- New and previously described dactylogyrid species (Monogenoidea: Polyonchoinea) and a gastrocotylinean pre-adult (Heteronchoinea) from pomacentrid and caesionid (Perciformes) fishes from Lizard Island, Great Barrier Reef, Australia
- Erratum to: 2017, 62(1) should be 2017, 62(2)
Artikel in diesem Heft
- Review
- Snail species diversity impacts the infection patterns of Echinostoma spp.: Examples from field collected data
- Molecular phylogeny of the Haplosplanchnata Olson, Cribb, Tkach, Bray and Littlewood, 2003, with a description of Schikhobalotrema huffmani n. sp.
- Structuraland antigenic analysis of a new Rhoptry Pseudokinase Gene (ROP54) in Toxoplasma gondii
- Ultrastructure of the spermatozoon of Macvicaria obovata (Digenea: Opecoelidae), a parasite of Sparus aurata(Pisces: Teleostei) from the Gulf of Gabès, Mediterranean Sea
- Epidemiology of Toxoplasma gondii infection in native Tibetans in Tibet, China
- A PCR survey of vector-borne pathogens in different dog populations from Turkey
- Diplectanids (Monogenea) parasitic on sciaenid fish from Peru with the proposal of Pseudorhamnocercoides n. gen., the description of Rhamnocercus dominguesi n. sp. and the redescription of Rhamnocercoides menticirrhi Luque and Iannacone, 1991
- Differentiation of Toxocara canis and Toxocara cati based on PCR-RFLP analyses of rDNA-ITS and mitochondrial cox1 and nad1 regions
- The Prevalence of Cyclospora cayetanensis and Cryptosporidium spp. in Turkish patients infected with HIV-1
- Molecular characterization and functional analysis of a glutathione peroxidase gene from Aphelenchoides besseyi (Nematoda: Aphelenchoididae)
- Durettenema guangdongense gen. et sp. nov. (Nematoda: Molineoidea) from Hipposideros larvatus (Horsfield) (Chiroptera: Rhinolophidae) with discussion of the taxonomic status of Macielia rhinolophi Yin, 1980
- In vitro effects of purine and pyrimidine analogues on Leishmania donovani and Leishmania infantum promastigotes and intracellular amastigotes
- Population structure of the monogenean, Paramazocraes thrissocles (Mazocraeidae) on the gills of clupeoid fish, Thryssa mystax of Visakhapatnam coast, Bay of Bengal
- Redescription of Eutarsopolipus elongatus Regenfuss, 1968 (Acari: Podapolipidae) parasitising carabid beetles, with first description of the male
- Seroprevalence and risk factors of Neospora spp. and Toxoplasma gondii infections among horses and donkeys in Nigeria, West Africa
- Spinicauda sumatrana sp. nov. (Nematoda: Heterakidae) from Ludeking’s Crested Dragon, Lophocalotes ludekingi (Agamidae), from the Bukit Barisan Range of Sumatra
- The systematic position and structure of the genus Leyogonimus Ginetsinskaya, 1948 (Platyhelminthes: Digenea) with comments on the taxonomy of the superfamily Microphalloidea Ward, 1901
- Leishmania infantum is present in vaginal secretions of naturally infected bitches at lower levels in oestrogenized bitches than in non-oestrogenized bitches
- Intestinal coccidian parasites as an underestimated cause of travellers’ diarrhoea in Polish immunocompetent patients
- Hymenolepididae (Cestoda, Cyclophyllidea) of ciconiiform and pelecaniform birds: the genera Oschmarinolepis Spassky and Spasskaja, 1954 and Paraoschmarinolepis gen. n.
- Redescription of two species of Thaparocleidus (Monogenea: Dactylogyridae), with the description of T. armillatus sp. n. from Wallago attu and a phylogenetic analysis based on 18S rDNA sequences
- In vitro and in vivo studies of nematophagous fungi Arthrobotrys musiformis and Arthrobotrys robusta against the larvae of the trichostrongylides
- Three monogeneans parasitic on marine sciaenid fish from Peru including description of Cynoscionicola veranoi n. sp. (Microcotylidae), and redescription of C. americanus Tantaleán, Martínez and Escalante, 1987 and Hargicotyle sciaenae Oliva and Luque, 1989 (Diclidophoridae)
- New and previously described dactylogyrid species (Monogenoidea: Polyonchoinea) and a gastrocotylinean pre-adult (Heteronchoinea) from pomacentrid and caesionid (Perciformes) fishes from Lizard Island, Great Barrier Reef, Australia
- Erratum to: 2017, 62(1) should be 2017, 62(2)
