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Published in: European Journal of Clinical Microbiology & Infectious Diseases 11/2020

Open Access 01-11-2020 | Diarrhea | Original Article

Protozoan infections are under-recognized in Swedish patients with gastrointestinal symptoms

Authors: Jessica Ögren, Olaf Dienus, Jessica Beser, Anna J. Henningsson, Andreas Matussek

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 11/2020

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Abstract

In acute gastroenteritis (GE), identification of the infectious agent is important for patient management and surveillance. The prevalence of GE caused by protozoa may be underestimated in Swedish patients. The purpose was to compare the prevalence of E. histolytica, Cryptosporidium spp., G. intestinalis, and C. cayetanensis in samples from patients where the clinician had requested testing for gastrointestinal parasites only (n = 758) to where testing for bacterial GE only (n = 803) or where both parasite and bacterial testing (n = 1259) was requested and a healthy control group (n = 197). This prospective cohort study was conducted in Region Jönköping County, Sweden (October 2018–March 2019). Fecal samples were analyzed with microscopy and real-time PCR. Cryptosporidium spp. was detected in 16 patients in the bacterial GE group and in 13 in the both bacterial and parasite group; no cases were detected in the group were only parasite infection was suspected. C. cayetanensis was detected in two patients in the bacterial GE group. One case of E. histolytica was detected in the bacterial group and one in the both bacterial and parasite group. G. intestinalis was detected in 14 patients in the parasite only group, 12 in the both parasite and bacterial group, three in the bacterial GE group, and one in the control group. Diarrhea caused by protozoa, especially Cryptosporidium was under–recognized by clinicians and is likely more common than hitherto estimated in Sweden. A more symptom-based diagnostic algorithm may increase detection and knowledge about protozoan infections.
Literature
1.
go back to reference Fletcher SM, Stark D, Harkness J, Ellis J (2012) Enteric Protozoa in the developed world: a public health perspective. Clin Microbiol Rev 25:420–449CrossRef Fletcher SM, Stark D, Harkness J, Ellis J (2012) Enteric Protozoa in the developed world: a public health perspective. Clin Microbiol Rev 25:420–449CrossRef
2.
go back to reference Cacciò SM, Chalmers RM (2016) Human cryptosporidiosis in Europe. Clin Microbiol Infect 22:471–480CrossRef Cacciò SM, Chalmers RM (2016) Human cryptosporidiosis in Europe. Clin Microbiol Infect 22:471–480CrossRef
3.
go back to reference Skovgaards DM, Hartmeyer GN, Skov MN, Hoegh SV, Kemp M (2018) Cryptosporidium species are frequently present but rarely detected in clinical samples from children with diarrhea in a developed country. Pediatr Infect Dis J 37:e138–e140CrossRef Skovgaards DM, Hartmeyer GN, Skov MN, Hoegh SV, Kemp M (2018) Cryptosporidium species are frequently present but rarely detected in clinical samples from children with diarrhea in a developed country. Pediatr Infect Dis J 37:e138–e140CrossRef
4.
go back to reference Harvala H, Ogren J, Boman P, Riedel HM, Nilsson P, Winiecka-Krusnell J, Beser J (2016) Cryptosporidium infections in Sweden-understanding the regional differences in reported incidence. Clin Microbiol Infect 22:1012–1013CrossRef Harvala H, Ogren J, Boman P, Riedel HM, Nilsson P, Winiecka-Krusnell J, Beser J (2016) Cryptosporidium infections in Sweden-understanding the regional differences in reported incidence. Clin Microbiol Infect 22:1012–1013CrossRef
5.
go back to reference Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80–89CrossRef Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80–89CrossRef
6.
go back to reference Lilja M, Widerstrom M, Lindh J (2018) Persisting post-infection symptoms 2 years after a large waterborne outbreak of Cryptosporidium hominis in northern Sweden. BMC Res Notes 11:625CrossRef Lilja M, Widerstrom M, Lindh J (2018) Persisting post-infection symptoms 2 years after a large waterborne outbreak of Cryptosporidium hominis in northern Sweden. BMC Res Notes 11:625CrossRef
7.
go back to reference Rehn M, Wallensten A, Widerstrom M, Lilja M, Grunewald M, Stenmark S, Kark M, Lindh J (2015) Post-infection symptoms following two large waterborne outbreaks of Cryptosporidium hominis in Northern Sweden, 2010-2011. BMC Public Health 15:529CrossRef Rehn M, Wallensten A, Widerstrom M, Lilja M, Grunewald M, Stenmark S, Kark M, Lindh J (2015) Post-infection symptoms following two large waterborne outbreaks of Cryptosporidium hominis in Northern Sweden, 2010-2011. BMC Public Health 15:529CrossRef
8.
go back to reference Robertson LJ, Chalmers RM (2013) Foodborne cryptosporidiosis: is there really more in Nordic countries? Trends Parasitol 29:3–9CrossRef Robertson LJ, Chalmers RM (2013) Foodborne cryptosporidiosis: is there really more in Nordic countries? Trends Parasitol 29:3–9CrossRef
10.
go back to reference Fournet N, Deege MP, Urbanus AT, Nichols G, Rosner B, Chalmers RM, Gorton R, Pollock KGJ, Giessen JWV, Wever PC, Dorigo-Zetsma JW, Mulder B, Mank TG, Overdevest I, Kusters JG, Wv P, Kortbeek LM (2013) Simultaneous increase of Cryptosporidium infections in the Netherlands, the United Kingdom and Germany in late summer season, 2012. https://doi.org/10.25646/1347 Robert Koch-Institut, Infektionsepidemiologie Fournet N, Deege MP, Urbanus AT, Nichols G, Rosner B, Chalmers RM, Gorton R, Pollock KGJ, Giessen JWV, Wever PC, Dorigo-Zetsma JW, Mulder B, Mank TG, Overdevest I, Kusters JG, Wv P, Kortbeek LM (2013) Simultaneous increase of Cryptosporidium infections in the Netherlands, the United Kingdom and Germany in late summer season, 2012. https://​doi.​org/​10.​25646/​1347 Robert Koch-Institut, Infektionsepidemiologie
11.
go back to reference Minetti C, Chalmers RM, Beeching NJ, Probert C, Lamden K (2016) Giardiasis. BMJ 355:i5369CrossRef Minetti C, Chalmers RM, Beeching NJ, Probert C, Lamden K (2016) Giardiasis. BMJ 355:i5369CrossRef
12.
go back to reference Mmbaga BT, Houpt ER (2017) Cryptosporidium and Giardia infections in children: a review. Pediatr Clin N Am 64:837–850CrossRef Mmbaga BT, Houpt ER (2017) Cryptosporidium and Giardia infections in children: a review. Pediatr Clin N Am 64:837–850CrossRef
13.
go back to reference Fotedar R, Stark D, Beebe N, Marriott D, Ellis J, Harkness J (2007) Laboratory diagnostic techniques for Entamoeba species. Clin Microbiol Rev 20:511–532CrossRef Fotedar R, Stark D, Beebe N, Marriott D, Ellis J, Harkness J (2007) Laboratory diagnostic techniques for Entamoeba species. Clin Microbiol Rev 20:511–532CrossRef
14.
go back to reference Shirley D-AT, Farr L, Watanabe K, Moonah S (2018) A review of the global burden, new diagnostics, and current therapeutics for amebiasis. Open Forum Infect Dis 5:ofy161–ofy161CrossRef Shirley D-AT, Farr L, Watanabe K, Moonah S (2018) A review of the global burden, new diagnostics, and current therapeutics for amebiasis. Open Forum Infect Dis 5:ofy161–ofy161CrossRef
15.
go back to reference Lebbad M, Svard SG (2005) PCR differentiation of Entamoeba histolytica and Entamoeba dispar from patients with amoeba infection initially diagnosed by microscopy. Scand J Infect Dis 37:680–685CrossRef Lebbad M, Svard SG (2005) PCR differentiation of Entamoeba histolytica and Entamoeba dispar from patients with amoeba infection initially diagnosed by microscopy. Scand J Infect Dis 37:680–685CrossRef
16.
go back to reference Marques DFP, Alexander CL, Chalmers RM, Elson R, Freedman J, Hawkins G, Lo J, Robinson G, Russell K, Smith-Palmer A, Kirkbride H, Chiodini P, Godbole G (2017) Cyclosporiasis in travellers returning to the United Kingdom from Mexico in summer 2017: lessons from the recent past to inform the future. Euro Surveill 22:30592CrossRef Marques DFP, Alexander CL, Chalmers RM, Elson R, Freedman J, Hawkins G, Lo J, Robinson G, Russell K, Smith-Palmer A, Kirkbride H, Chiodini P, Godbole G (2017) Cyclosporiasis in travellers returning to the United Kingdom from Mexico in summer 2017: lessons from the recent past to inform the future. Euro Surveill 22:30592CrossRef
17.
go back to reference Legua P, Seas C (2013) Cystoisospora and cyclospora. Curr Opin Infect Dis 26:479–483CrossRef Legua P, Seas C (2013) Cystoisospora and cyclospora. Curr Opin Infect Dis 26:479–483CrossRef
18.
go back to reference Chalmers RM, Atchison C, Barlow K, Young Y, Roche A, Manuel R (2015) An audit of the laboratory diagnosis of cryptosporidiosis in England and Wales. J Med Microbiol 64:688–693CrossRef Chalmers RM, Atchison C, Barlow K, Young Y, Roche A, Manuel R (2015) An audit of the laboratory diagnosis of cryptosporidiosis in England and Wales. J Med Microbiol 64:688–693CrossRef
19.
go back to reference Munoz FM, Attias E, Czinn SJ, Black J (2016) Paediatrician and caregiver awareness of cryptosporidiosis and giardiasis in children: US survey responses. Zoonoses Public Health 63:410–419CrossRef Munoz FM, Attias E, Czinn SJ, Black J (2016) Paediatrician and caregiver awareness of cryptosporidiosis and giardiasis in children: US survey responses. Zoonoses Public Health 63:410–419CrossRef
20.
go back to reference Ogren J, Dienus O, Matussek A (2020) Optimization of routine microscopic and molecular detection of parasitic protozoa in SAF-fixed faecal samples in Sweden. Infect Dis (Lond) 52:87–96CrossRef Ogren J, Dienus O, Matussek A (2020) Optimization of routine microscopic and molecular detection of parasitic protozoa in SAF-fixed faecal samples in Sweden. Infect Dis (Lond) 52:87–96CrossRef
21.
go back to reference Verweij JJ, Laeijendecker D, Brienen EA, van Lieshout L, Polderman AM (2003) Detection of Cyclospora cayetanensis in travellers returning from the tropics and subtropics using microscopy and real-time PCR. Int J Med Microbiol 293:199–202CrossRef Verweij JJ, Laeijendecker D, Brienen EA, van Lieshout L, Polderman AM (2003) Detection of Cyclospora cayetanensis in travellers returning from the tropics and subtropics using microscopy and real-time PCR. Int J Med Microbiol 293:199–202CrossRef
22.
go back to reference Qvarnstrom Y, Benedict T, Marcet PL, Wiegand RE, Herwaldt BL, da Silva AJ (2018) Molecular detection of Cyclospora cayetanensis in human stool specimens using UNEX-based DNA extraction and real-time PCR. Parasitology 145:865–870CrossRef Qvarnstrom Y, Benedict T, Marcet PL, Wiegand RE, Herwaldt BL, da Silva AJ (2018) Molecular detection of Cyclospora cayetanensis in human stool specimens using UNEX-based DNA extraction and real-time PCR. Parasitology 145:865–870CrossRef
23.
go back to reference Xiao L, Bern C, Limor J, Sulaiman I, Roberts J, Checkley W, Cabrera L, Gilman RH, Lal AA (2001) Identification of 5 types of Cryptosporidium parasites in children in Lima, Peru. J Infect Dis 183:492–497CrossRef Xiao L, Bern C, Limor J, Sulaiman I, Roberts J, Checkley W, Cabrera L, Gilman RH, Lal AA (2001) Identification of 5 types of Cryptosporidium parasites in children in Lima, Peru. J Infect Dis 183:492–497CrossRef
24.
go back to reference Xiao L, Escalante L, Yang C, Sulaiman I, Escalante AA, Montali RJ, Fayer R, Lal AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65:1578–1583CrossRef Xiao L, Escalante L, Yang C, Sulaiman I, Escalante AA, Montali RJ, Fayer R, Lal AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65:1578–1583CrossRef
25.
go back to reference Alves M, Xiao L, Sulaiman I, Lal AA, Matos O, Antunes F (2003) Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. J Clin Microbiol 41:2744–2747CrossRef Alves M, Xiao L, Sulaiman I, Lal AA, Matos O, Antunes F (2003) Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. J Clin Microbiol 41:2744–2747CrossRef
26.
go back to reference Insulander M, SilverlÅS C, Lebbad M, Karlsson L, Mattsson JG, Svenungsson B (2013) Molecular epidemiology and clinical manifestations of human cryptosporidiosis in Sweden. Epidemiol Infect 141:1009–1020CrossRef Insulander M, SilverlÅS C, Lebbad M, Karlsson L, Mattsson JG, Svenungsson B (2013) Molecular epidemiology and clinical manifestations of human cryptosporidiosis in Sweden. Epidemiol Infect 141:1009–1020CrossRef
27.
go back to reference Chalmers RM, Robinson G, Elwin K, Elson R (2019) Analysis of the Cryptosporidium spp. and gp60 subtypes linked to human outbreaks of cryptosporidiosis in England and Wales, 2009 to 2017. Parasites Vectors 12:95CrossRef Chalmers RM, Robinson G, Elwin K, Elson R (2019) Analysis of the Cryptosporidium spp. and gp60 subtypes linked to human outbreaks of cryptosporidiosis in England and Wales, 2009 to 2017. Parasites Vectors 12:95CrossRef
28.
go back to reference Chalmers RM, Katzer F (2013) Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends Parasitol 29:237–251CrossRef Chalmers RM, Katzer F (2013) Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends Parasitol 29:237–251CrossRef
29.
go back to reference Beser J, Bujila I, Wittesjö B, Lebbad M (2020) From mice to men: three cases of human infection with Cryptosporidium ditrichi. Infect Genet Evol 78:104120CrossRef Beser J, Bujila I, Wittesjö B, Lebbad M (2020) From mice to men: three cases of human infection with Cryptosporidium ditrichi. Infect Genet Evol 78:104120CrossRef
30.
go back to reference Lebbad M, Beser J, Insulander M, Karlsson L, Mattsson JG, Svenungsson B, Axén C (2013) Unusual cryptosporidiosis cases in Swedish patients: extended molecular characterization of Cryptosporidium viatorum and Cryptosporidium chipmunk genotype I. Parasitology 140:1735–1740CrossRef Lebbad M, Beser J, Insulander M, Karlsson L, Mattsson JG, Svenungsson B, Axén C (2013) Unusual cryptosporidiosis cases in Swedish patients: extended molecular characterization of Cryptosporidium viatorum and Cryptosporidium chipmunk genotype I. Parasitology 140:1735–1740CrossRef
31.
go back to reference Beser J, Toresson L, Eitrem R, Troell K, Winiecka-Krusnell J, Lebbad M (2015) Possible zoonotic transmission of Cryptosporidium felis in a household. Infect Ecol Epidemiol 5:28463PubMed Beser J, Toresson L, Eitrem R, Troell K, Winiecka-Krusnell J, Lebbad M (2015) Possible zoonotic transmission of Cryptosporidium felis in a household. Infect Ecol Epidemiol 5:28463PubMed
32.
go back to reference Golan Shaposhnik E, Abozaid S, Grossman T, Marva E, On A, Azrad M, Peretz A (2019) The prevalence of Cryptosporidium among children hospitalized because of gastrointestinal symptoms and the efficiency of diagnostic methods for Cryptosporidium. Am J Trop Med Hyg 101:160–163CrossRef Golan Shaposhnik E, Abozaid S, Grossman T, Marva E, On A, Azrad M, Peretz A (2019) The prevalence of Cryptosporidium among children hospitalized because of gastrointestinal symptoms and the efficiency of diagnostic methods for Cryptosporidium. Am J Trop Med Hyg 101:160–163CrossRef
33.
go back to reference Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EAT, van Rooyen MAA, van Lieshout L, Polderman AM (2004) Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvumin fecal samples by using multiplex real-time PCR. J Clin Microbiol 42:1220–1223CrossRef Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EAT, van Rooyen MAA, van Lieshout L, Polderman AM (2004) Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvumin fecal samples by using multiplex real-time PCR. J Clin Microbiol 42:1220–1223CrossRef
34.
go back to reference Stensvold CR, Nielsen HV (2012) Comparison of microscopy and PCR for detection of intestinal parasites in Danish patients supports an incentive for molecular screening platforms. J Clin Microbiol 50:540–541CrossRef Stensvold CR, Nielsen HV (2012) Comparison of microscopy and PCR for detection of intestinal parasites in Danish patients supports an incentive for molecular screening platforms. J Clin Microbiol 50:540–541CrossRef
35.
go back to reference Forsell J, Granlund M, Samuelsson L, Koskiniemi S, Edebro H, Evengård B (2016) High occurrence of Blastocystis sp. subtypes 1–3 and Giardia intestinalis assemblage B among patients in Zanzibar, Tanzania. Parasites Vectors 9:370CrossRef Forsell J, Granlund M, Samuelsson L, Koskiniemi S, Edebro H, Evengård B (2016) High occurrence of Blastocystis sp. subtypes 1–3 and Giardia intestinalis assemblage B among patients in Zanzibar, Tanzania. Parasites Vectors 9:370CrossRef
36.
go back to reference Muhsen K, Levine MM (2012) A systematic review and meta-analysis of the association between Giardia lamblia and endemic pediatric diarrhea in developing countries. Clin Infect Dis 55(Suppl 4):S271–S293CrossRef Muhsen K, Levine MM (2012) A systematic review and meta-analysis of the association between Giardia lamblia and endemic pediatric diarrhea in developing countries. Clin Infect Dis 55(Suppl 4):S271–S293CrossRef
Metadata
Title
Protozoan infections are under-recognized in Swedish patients with gastrointestinal symptoms
Authors
Jessica Ögren
Olaf Dienus
Jessica Beser
Anna J. Henningsson
Andreas Matussek
Publication date
01-11-2020
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 11/2020
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-020-03974-w

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