Genetic Diversity of Strongyloides stercoralis with Attention to Clinical Features in Patients Originated from Three Endemic Provinces in the North and South of Iran
Abstract
Background: Strongyloides stercoralis is one of the neglected tropical diseases. We aimed to verify the genetic diversity of S. stercoralis with attention to clinical features of the infection in patients using the Cox1 gene and DNA sequencing.
Methods: Using parasitological methods, S. stercoralis was isolated from stool samples of patients who had been referred to Tehran University of Medical Sciences, Tehran, Iran. The patients originated from three endemic provinces of Iran including Guilan and Mazandaran in the north and Khouzestan in the south of Iran. After recording the clinical symptoms of the patients, DNA extraction of the isolates, PCR, and sequencing of the Cox1 gene region were performed. The gene sequences were analyzed by Chromas, Bio edit, and Dna SP 6.0, and phylogenetic analysis using MEGA 7.
Results: Overall 10 isolates of S. stercoralis were collected from patients 55 to 73 years old. Among the patients, gastrointestinal, respiratory, and cutaneous clinical symptoms were the most common, respectively. Ten isolates were classified into 4 haplotypes, 2 of which were specific to this study. Haplotypes 2 and 3 were placed in a subclade with haplotypes including isolates from dogs in Cambodia. Haplotype 4 which is hereby introduced in the world for the first time included an isolate from a patient with hyper-infection syndrome and disseminated strongyloidiasis.
Conclusion: The Cox1 gene showed genetic diversity for S. stercoralis isolates. Accordingly, no significant genetic difference was observed between the sequences from patients with hyper-infection and non-hyper-infection. The only isolate from a patient with disseminated and hyper-infection strongyloidiasis was genetically different from all other isolates in the present study.
1. Olsen A, van Lieshout L, Marti H, et al. Strongyloidiasis–the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg, 2009;103(10):967-72.
2. Schär F, Trostdorf U, Giardina F, et al. Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis. 2013; 7(7):e2288.
3. Buonfrate D, Bisanzio D, Giorli G, et al. The global prevalence of Strongyloides stercoralis infection. Pathogens. 2020; 9(6):468.
4. Montresor A, Mupfasoni D, Mikhailov A, et al. The global progress of soil-transmitted helminthiases control in 2020 and World Health Organization targets for 2030. PLoS Negl Trop Dis. 2020; 14(8):e0008505.
5. Muller R, Wakelin D. Worms and human disease. CABi; 2002.
6. Grove DI. Human strongyloidiasis. Adv Parasitol. 1996; 38:251–309.
7. Paniker CJ, Ghosh S. Paniker’s textbook of medical parasitology. JP Medical Ltd; 2017.
8. Gillespie SH, Pearson RD, editors. Principles and Practice of Clinical Parasitology. 1st ed. Wiley; 2001.
9. Mejia R, Nutman TB. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Curr Opin Infect Dis. 2012; 25(4):458-63.
10. Sharifdini M, Mirhendi H, Ashrafi K, et al. Comparison of nested polymerase chain reaction and real-time polymerase chain reaction with parasitological methods for detection of Strongyloides stercoralis in human fecal samples. Am J Trop Med Hyg. 2015; 93(6):1285-91.
11. Sudarshi S, Stümpfle R, Armstrong M, et al. Clinical presentation and diagnostic sensitivity of laboratory tests for Strongyloides stercoralis in travelers compared with immigrants in a non‐endemic country. Trop Med Int Health. 2003; 8(8):728–32.
12. Dacal E, Saugar JM, Soler T, et al. Parasitological versus molecular diagnosis of strongyloidiasis in serial stool samples: how many? J Helminthol. 2018; 92(1):12–6.
13. Sultana Y, Jeoffreys N, Watts MR, Gilbert GL, Lee R. Real-time polymerase chain reaction for detection of Strongyloides stercoralis in stool. Am J Trop Med Hyg. 2013; 88(6):1048-51.
14. Fakhrieh-Kashan Z, Zahabiun F, Sharifdini M, Fotouhi-Ardakani R, Kia EB. Critical diagnosis of complicated strongyloidosis with nestedPCR and High Resolution Melting analysis (HRM). Ann Parasitol. 2019; 65(4): 333–339.
15. Viney ME, Lok JB. Strongyloides spp. WormBook. 2007; 1-15.
16. Hays R, Esterman A, McDermott R. Control of chronic Strongyloides stercoralis infection in an endemic community may be possible by pharmacological means alone: Results of a three-year cohort study. PLoS Negl Trop Dis. 2017; 11(7):e0005825.
17. Hasegawa H, Kalousova B, McLennan MR, et al. Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. Parasitol Int. 2016; 65(5 Pt A):367-70.
18. Jaleta TG, Zhou S, Bemm FM, et al. Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis. PLoS Negl Trop Dis. 2017; 11(8):e0005752.
19. Nagayasu E, Aung MPPTHH, Hortiwakul T, et al. A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Sci Rep. 2017; 7 (1):4844.
20. Thanchomnang T, Intapan PM, Sanpool O, et al. First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand. Parasitol Res. 2017; 116(7):1917–23.
21. Laymanivong S, Hangvanthong B, Insisiengmay B, et al. First molecular identification and report of genetic diversity of Strongyloides stercoralis, a current major soil-transmitted helminth in humans from Lao People’s Democratic Republic. Parasitol Res. 2016; 115(8):2973–80.
22. Pumidonming W, Salman D, Gronsang D, et al. Prevalence of gastrointestinal helminth parasites of zoonotic significance in dogs and cats in lower Northern Thailand. J Vet Med Sci. 2017; 78(12):1779–84.
23. Najjari M, Ebrahimipour M, Kaheh A, Karimazar M. Disseminated strongyloidiasis in an immunodeficient patient (pemphigus vulgaris) due to corticosteroid therapy: a case report. Iran J Parasitol. 2016; 11(3):411-416.
24. Moghadam KG, Khashayar P, Hashemi M. Gastrointestinal strongyloidiasis in immunocompromised patients: a case report. Acta Med Indones. 2011; 43(3):191–4.
25. Sharifdini M, Kia EB, Ashrafi K, et al. An analysis of clinical characteristics of Strongyloides stercoralis in 70 indigenous patients in Iran. Iran J Parasitol. 2014; 9(2):155–62.
26. Arakaki T, Iwanaga M, Kinjo F, Saito A, Asato R, Ikeshiro T. Efficacy of agar-plate culture in detection of Strongyloides stercoralis infection. J Parasitol. 1990; 76(3):425-8.
27. Nilforoushan MR, Mirhendi H, Rezaie S, Rezaian M, Meamar AR, Kia EB. A DNA-based identification of Strongyloides stercoralis isolates from Iran. Iran J Public Health. 2007; 36(3):16–20.
28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731–9.
29. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003; 19(18):2496–7.
30. Barratt JL, Lane M, Talundzic E, et al. A global genotyping survey of Strongyloides stercoralis and Strongyloides fuelleborni using deep amplicon sequencing. PLoS Negl Trop Dis. 2019; 13(9):e0007609.
31. Fadaei Tehrani M, Sharifdini M, Zahabiun F, Latifi R, Kia EB. Molecular characterization of human isolates of Strongyloides stercoralis and Rhabditis spp. based on mitochondrial cytochrome c oxidase subunit 1 (cox1). BMC Infect Dis. 2019 Dec; 19(1):776.
32. Iamrod K, Chaidee A, Rucksaken R, et al. Development and efficacy of droplet digital PCR for detection of Strongyloides stercoralis in stool. Am J Trop Med Hyg. 2021; 106(1):312-319.
33. Hasegawa H, Hayashida S, Ikeda Y, Sato H. Hyper-variable regions in 18S rDNA of Strongyloides spp. as markers for species-specific diagnosis. Parasitol Res. 2009; 104(4):869–74.
34. Fakhrie KZ. Isolation of Strongyloides stercoralis from humans in endemic areas of Iran and determination of their intraspecific diversity based on Cox1 and 18S rDNA by DNA sequencing and HRM (High Resolution Melting) analysis, a thesis presented for the Doctor of Philosophy Degree (Ph.D.) Medical Parasitology, School of Public Health: Teheran University of Medical Sciences.
35. Blouin MS. Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol. 2002; 32(5):527–31.
36. Hasegawa H, Sato H, Fujita S, et al. Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: Dispersal and diversity of Strongyloides spp. and their hosts. Parasitol Int. 2010; 59(3):407–13.
2. Schär F, Trostdorf U, Giardina F, et al. Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis. 2013; 7(7):e2288.
3. Buonfrate D, Bisanzio D, Giorli G, et al. The global prevalence of Strongyloides stercoralis infection. Pathogens. 2020; 9(6):468.
4. Montresor A, Mupfasoni D, Mikhailov A, et al. The global progress of soil-transmitted helminthiases control in 2020 and World Health Organization targets for 2030. PLoS Negl Trop Dis. 2020; 14(8):e0008505.
5. Muller R, Wakelin D. Worms and human disease. CABi; 2002.
6. Grove DI. Human strongyloidiasis. Adv Parasitol. 1996; 38:251–309.
7. Paniker CJ, Ghosh S. Paniker’s textbook of medical parasitology. JP Medical Ltd; 2017.
8. Gillespie SH, Pearson RD, editors. Principles and Practice of Clinical Parasitology. 1st ed. Wiley; 2001.
9. Mejia R, Nutman TB. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Curr Opin Infect Dis. 2012; 25(4):458-63.
10. Sharifdini M, Mirhendi H, Ashrafi K, et al. Comparison of nested polymerase chain reaction and real-time polymerase chain reaction with parasitological methods for detection of Strongyloides stercoralis in human fecal samples. Am J Trop Med Hyg. 2015; 93(6):1285-91.
11. Sudarshi S, Stümpfle R, Armstrong M, et al. Clinical presentation and diagnostic sensitivity of laboratory tests for Strongyloides stercoralis in travelers compared with immigrants in a non‐endemic country. Trop Med Int Health. 2003; 8(8):728–32.
12. Dacal E, Saugar JM, Soler T, et al. Parasitological versus molecular diagnosis of strongyloidiasis in serial stool samples: how many? J Helminthol. 2018; 92(1):12–6.
13. Sultana Y, Jeoffreys N, Watts MR, Gilbert GL, Lee R. Real-time polymerase chain reaction for detection of Strongyloides stercoralis in stool. Am J Trop Med Hyg. 2013; 88(6):1048-51.
14. Fakhrieh-Kashan Z, Zahabiun F, Sharifdini M, Fotouhi-Ardakani R, Kia EB. Critical diagnosis of complicated strongyloidosis with nestedPCR and High Resolution Melting analysis (HRM). Ann Parasitol. 2019; 65(4): 333–339.
15. Viney ME, Lok JB. Strongyloides spp. WormBook. 2007; 1-15.
16. Hays R, Esterman A, McDermott R. Control of chronic Strongyloides stercoralis infection in an endemic community may be possible by pharmacological means alone: Results of a three-year cohort study. PLoS Negl Trop Dis. 2017; 11(7):e0005825.
17. Hasegawa H, Kalousova B, McLennan MR, et al. Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. Parasitol Int. 2016; 65(5 Pt A):367-70.
18. Jaleta TG, Zhou S, Bemm FM, et al. Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis. PLoS Negl Trop Dis. 2017; 11(8):e0005752.
19. Nagayasu E, Aung MPPTHH, Hortiwakul T, et al. A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Sci Rep. 2017; 7 (1):4844.
20. Thanchomnang T, Intapan PM, Sanpool O, et al. First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand. Parasitol Res. 2017; 116(7):1917–23.
21. Laymanivong S, Hangvanthong B, Insisiengmay B, et al. First molecular identification and report of genetic diversity of Strongyloides stercoralis, a current major soil-transmitted helminth in humans from Lao People’s Democratic Republic. Parasitol Res. 2016; 115(8):2973–80.
22. Pumidonming W, Salman D, Gronsang D, et al. Prevalence of gastrointestinal helminth parasites of zoonotic significance in dogs and cats in lower Northern Thailand. J Vet Med Sci. 2017; 78(12):1779–84.
23. Najjari M, Ebrahimipour M, Kaheh A, Karimazar M. Disseminated strongyloidiasis in an immunodeficient patient (pemphigus vulgaris) due to corticosteroid therapy: a case report. Iran J Parasitol. 2016; 11(3):411-416.
24. Moghadam KG, Khashayar P, Hashemi M. Gastrointestinal strongyloidiasis in immunocompromised patients: a case report. Acta Med Indones. 2011; 43(3):191–4.
25. Sharifdini M, Kia EB, Ashrafi K, et al. An analysis of clinical characteristics of Strongyloides stercoralis in 70 indigenous patients in Iran. Iran J Parasitol. 2014; 9(2):155–62.
26. Arakaki T, Iwanaga M, Kinjo F, Saito A, Asato R, Ikeshiro T. Efficacy of agar-plate culture in detection of Strongyloides stercoralis infection. J Parasitol. 1990; 76(3):425-8.
27. Nilforoushan MR, Mirhendi H, Rezaie S, Rezaian M, Meamar AR, Kia EB. A DNA-based identification of Strongyloides stercoralis isolates from Iran. Iran J Public Health. 2007; 36(3):16–20.
28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731–9.
29. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003; 19(18):2496–7.
30. Barratt JL, Lane M, Talundzic E, et al. A global genotyping survey of Strongyloides stercoralis and Strongyloides fuelleborni using deep amplicon sequencing. PLoS Negl Trop Dis. 2019; 13(9):e0007609.
31. Fadaei Tehrani M, Sharifdini M, Zahabiun F, Latifi R, Kia EB. Molecular characterization of human isolates of Strongyloides stercoralis and Rhabditis spp. based on mitochondrial cytochrome c oxidase subunit 1 (cox1). BMC Infect Dis. 2019 Dec; 19(1):776.
32. Iamrod K, Chaidee A, Rucksaken R, et al. Development and efficacy of droplet digital PCR for detection of Strongyloides stercoralis in stool. Am J Trop Med Hyg. 2021; 106(1):312-319.
33. Hasegawa H, Hayashida S, Ikeda Y, Sato H. Hyper-variable regions in 18S rDNA of Strongyloides spp. as markers for species-specific diagnosis. Parasitol Res. 2009; 104(4):869–74.
34. Fakhrie KZ. Isolation of Strongyloides stercoralis from humans in endemic areas of Iran and determination of their intraspecific diversity based on Cox1 and 18S rDNA by DNA sequencing and HRM (High Resolution Melting) analysis, a thesis presented for the Doctor of Philosophy Degree (Ph.D.) Medical Parasitology, School of Public Health: Teheran University of Medical Sciences.
35. Blouin MS. Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol. 2002; 32(5):527–31.
36. Hasegawa H, Sato H, Fujita S, et al. Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: Dispersal and diversity of Strongyloides spp. and their hosts. Parasitol Int. 2010; 59(3):407–13.
| Files | ||
| Issue | Vol 19 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i4.17167 | |
| Keywords | ||
| Iran Strongyloides stercoralis DNA sequencing Cytochrome c oxidase 1 Hyper-infection syndrome Haplotype | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Semnan S, Kia EB, Sharifdini M, Darabi E, Fakhrieh Kashan Z. Genetic Diversity of Strongyloides stercoralis with Attention to Clinical Features in Patients Originated from Three Endemic Provinces in the North and South of Iran. Iran J Parasitol. 2024;19(4):465-474.
