Global status of intestinal parasitic infections among diabetic patients: A systematic review and meta-analysis
Abstract
Intestinal parasitic infections (IPIs) have been identified as a disease agent responsible for infections in immunocompromised patients such as diabetics. We searched six electronic databases and reviewed 38 related studies using the following keywords alone or in combination: “intestinal parasites,” “diabetes,” “immunocompromised,” “prevalence,” and “human.” The pooled prevalence of IPIs in diabetic patients was 24.4% worldwide. These patients with IPIs are advised to go to health centers and perform the relevant checkups with the advent of the first symptoms of the disease, such as diarrhea and abdominal pain. Moreover, early diagnosis and treatment of IPIs in diabetic patients are highly recommended to maintain quality of life.
References
Saki J., Khademvatan S., Foroutan-Rad M., Gharibzadeh M. 2017. Prevalence of intestinal parasitic infections in Haftkel County, southwest of Iran. International Journal of Infectious Diseases 4(4). https://doi.org/10.5812/iji.15593
Patwardhan V., Kumar D., Singh S. 2017. Parasitic infections in pediatric population of india: epidemiology, diagnosis, and strategies for prevention. Journal of Pediatric Infectious Diseases 12(04): 228–237.
Ukoh V., Ozurumba L. 2016. Comparative prevalence of intestinal parasitic infections (IPIs) in stool samples of patients attending UMTH Maiduguri between 2006 and 2007; its community health burden and proactive counter measures implications. Bioresearch Communications 2(2): 276–280.
Alemu M., Anley A., Tedla K. 2019. Magnitude of intestinal parasitosis and associated factors in rural school children, Northwest Ethiopia. Ethiopian Journal of Health Sciences 29(1). https://doi.org/10.4314/ejhs.v29i1.14
Khubchandani I.T., Bub D.S. 2019. Parasitic infections. Clinics in Colon and Rectal Surgery 32(05): 364–371.
Mendenhall E., Kohrt B.A., Norris S.A., Ndetei D., Prabhakaran D. 2017. Non-communicable disease syndemics: poverty, depression, and diabetes among low-income populations. Lancet 389(10072): 951–963. https://doi.org/10.1016/S0140-6736(17)30402-6
Dabelea D., Stafford J.M., Mayer-Davis E.J., D’Agostino R., Dolan L., Imperatore G., Linder B., Lawrence J.M., Marcovina S.M., Mottl A.K., Black M.H. 2017. Association of type 1 diabetes vs type 2 diabetes diagnosed during childhood and adolescence with complications during teenage years and young adulthood. JAMA Network Open 317(8): 825–835. https://doi.org/10.1001/jama.2017.0686
Mayer-Davis E.J., Lawrence J.M., Dabelea D., Divers J., Isom S., Dolan L., Imperatore G., Linder B., Marcovina S., Pettitt D.J., Pihoker C. 2017. Incidence trends of type 1 and type 2 diabetes among youths, 2002–2012. The New England Journal of Medicine 376: 1419–1429. https://doi.org/10.1056/NEJMc1706291
Saeedi P., Petersohn I., Salpea P., Malanda B., Karuranga S., Unwin N., Colagiuri S., Guariguata L., Motala A.A., Ogurtsova K., Shaw J.E. 2019. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas. Diabetes Research and Clinical Practice 157: 107843. https://doi.org/10.1016/j.diabres.2019.107843
Izadi S., Ghayour-Najafabadi Z., Yavari M., Mohaghegh M.A., Wannigama D.L., Moslemzadeh H-R., Azami M., Hejazi S.H. 2019. Intestinal parasites associated with opportunistic coccidial infections among immunocompromised individuals in central Iran: a cross sectional study. Archives of Clinical Infectious Diseases 14(2). https://doi.org/10.5812/archcid.79701
Horlocker T.T., Wedel D.J. 2006. Regional anesthesia in the immunocompromised patient. Regional Anesthesia and Pain Medicine 31(4): 334–345. https://doi.org/0.1016/j.rapm.2006.04.002
Al-Mousawi A., Neamah B. 2021. A study on intestinal parasites among diabetic patients in Najaf governorate of Iraq and its effect on some blood parameters. Iranian Journal of Ichthyology 8: 127–132.
Alemu G., Jemal A., Zerdo Z. 2018. Intestinal parasitosis and associated factors among diabetic patients attending Arba Minch Hospital, Southern Ethiopia. BMC Research Notes 11(1): 1–6. https://doi.org/10.1186/s13104-018-3791-x
Moher D., Liberati A., Tetzlaff J., Altman D.G., Group P. 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 6(7). https://doi.org/10.1136/bmj. b2535
PROSPERO. 2017. Global prevalence of intestinal parasites in diabetic patients: systematic review with meta-analysis, CRD42022297715.
Peterson J., Welch V., Losos M., Tugwell P. 2011. The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa: Ottawa Hospital Research Institute 2(1): 1–12.
Higgins J.P., Thompson S.G. 2002. Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21(11): 1539–1558. https://doi.org/10.1002/sim.1186
Shi X., Nie C., Shi S., Wang T., Yang H., Zhou Y., Song X. 2017. Effect comparison between Egger’s test and Begg’s test in publication bias diagnosis in meta-analyses: evidence from a pilot survey. International Journal of Research Studies in Bioscience 5(5): 14–20. https://doi.org/10.20431/2349-0365.0505003
Abaza S.M., Makhlouf L.M., El-Shewy K., El- Moamly A. 1995. Intestinal opportunistic parasites among different groups of immunocompromised hosts. Journal of the Egyptian Society of Parasitology 25(3): 713–727.
Lysy J., Israeli E., Goldin E. 1999. The prevalence of chronic diarrhea among diabetic patients. The American Journal of Gastroenterology 94(8): 2165–2170. https://doi.org/10.1016/S0002-9270(99)00345-7
Hunter P.R., Nichols G. 2002. Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clinical Microbiology Reviews 15(1): 145–154. https://doi.org/10.1128/CMR.15.1.145-154.2002
Akhlaghi L., Gharavi M., Faghihi A., Jabbari M. 2005. Survey on the prevalence rates of intestinal parasites in diabetic patients in Karaj and Savodjbolagh cities. Razi Journal of Medical Sciences 12(45): 23–29.
Baqai R., Anwar S., Kazmi S. 2005. Detection of Cryptosporidium in immunosuppressed patients. Journal of Ayub Medical College Abbottabad 17(3).
Mendonça S.C., Maria do Rosário F., Rodrigues R.M., Ferreira Jr A., Costa-Cruz J.M. 2006. Is there an association between positive Strongyloides stercoralis serology and diabetes mellitus? Acta Tropica 99(1): 102–105. https://doi.org/10.1016/j.actatropica.2006.06.006
Baiomy A.M.S., Mohamed K., Ghannam M.A.M., Al-Razek S. 2010. Opportunistic parasitic infections among immunocom-promised patients. Journal of the Egyptian Society of Parasitology 40(3): 797–807.
Hakim G.D., Kızıltas S., Ciftci H., Goktas S., Tuncer I. 2011. The prevalence of Giardia intestinalis in dyspeptic and diabetic patients. International Scholarly Research Notices 2011: 580793 https://doi.org/10.5402/2011/580793
Akinbo F.O., Olujobi S.O., Omoregie R., Egbe C. 2013. Intestinal parasitic infections among diabetes mellitus patients. Biomarkers and Genomic Medicine 5(1–2): 44–47. https://doi.org/10.1016/j.sciaf.2020.e00680 [28] Sabah A.A., Temsah A.G. 2015. Prevalence of some gastro-intestinal parasites in diabetic patients in tanta city, Gharbia Governorate, Egypt. Journal of the Egyptian Society of Parasitology 45(3): 681–684. https://doi.org/10.12816/0017936
Elnadi N.A., Hassanien H.A., Ahmad A.M., Abd Ellah A.K. 2015. Intestinal parasites in diabetic patients in Sohag University Hospitals, Egypt. Journal of the Egyptian Society of Parasitology 45(2): 443–449. https://doi.org/10.12816/0017597
Wiria A.E., Hamid F., Wammes L.J., Prasetyani M.A., Dekkers O.M., May L., Kaisar M.M., Verweij J.J., Guigas B., Partono F., Sartono E. 2015. Infection with soil-transmitted helminths is associated with increased insulin sensitivity. PloS One 10(6): e0127746.. https://doi.org/10.1371/journal.pone.0127746
Fattahi Bafghi A., Afkhami-Ardekani M., Dehghani Tafti A. 2015. Frequency distribution of intestinal parasitic infections in diabetic patients–Yazd 2013. Iranian Journal of Diabetes and Obesity 7(1): 33–37.
Cabral A.C., Iñiguez A.M., Moreno T., Bóia M.N., Carvalho-Costa F.A. 2015. Clinical conditions associated with intestinal strongyloidiasis in Rio de Janeiro, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 48: 321–325. https://doi.org/10.1590/0037-8682-0019-2015
Bora I., Dutta V., Lyngdoh W.V., Khyriem A.B., Durairaj E., Phukan A.C. 2016. Study of intestinal parasites among the immunosuppressed patients attending a tertiary-care center in Northeast India. International Journal of Medical Science and Public Health 5(5): 924–929. https://doi.org/10.5455/ijmsph.2016.08012016327
Tangi F.B., Fokam E.B., Longdoh N.A., Eteneneng E.J. 2016. Intestinal parasites in diabetes mellitus patients in the Limbe and Buea municipalities, Cameroon. Diabetes Research Open Journal 2(1): 1–7. https://doi.org/10.17140/DROJ-2-123
Siddiqua T., Sultana R., Khanum H. 2017. Prevalence of Entamoeba histolytica and Giardia lamblia infection among diabetic and non-diabetic patients of Bangladesh. Bioresearch Communication 3(2) :435–442.
McGuire E., Welch C., Melzer M. 2019. Is Strongyloides seropositivity associated with diabetes mellitus? A retrospective case-control study in an East London NHS Trust. Transactions of The Royal Society of Tropical Medicine and Hygiene 113(4): 189–194. https://doi.org/10.1093/trstmh/try132
Ali O.S., Mohammad S.A., Salman Y.J. 2018. Incidence of some intestinal parasites among diabetic patients suffering from gastroenteritis. International Journal of Current Microbiology and Applied Sciences 7(8): 3695–3708. https://doi.org/10.20546/ijcmas.2018.708.375
Machado E.R., Matos N.O., Rezende S.M., Carlos D., Silva T.C., Rodrigues L., Almeida M.J., de Oliveira M.R., Muniz-Junqueira M.I., Gurgel- Gonçalves R. 2018. Host-parasite interactions in individuals with type 1 and 2 diabetes result in higher frequency of Ascaris lumbricoides and Giardia lamblia in type 2 diabetic individuals. Journal of Diabetes Research 2018: 4238435. https://doi.org/10.1155/2018/4238435
Htun N.S.N., Odermatt P., Paboriboune P., Sayasone S., Vongsakid M., Phimolsarn-Nusith V., Tran X.D., Ounnavong P.S., Andriama-Hefasoa N., Senvanpan N.D., Homsana A. 2018. Association between helminth infections and diabetes mellitus in adults from the Lao People’s Democratic Republic: a cross- sectional study. Infectious Diseases of Poverty 7(1): 1–11. https://doi.org/10.1186/s40249-018-0488-2
Drawany Z., Saleh S., Etewa S., Ibrahim S. 2019. Prevalence of intestinal parasites among type 1 diabetic patients in pediatrics Zagazig university hospital. Endocrinology and Metabolism International Journal 7(6): 171–179. https://doi.org/10.15406/emij.2019.07.00265
Rady H.I., Elkazazz A., EL Saftawy E.A., Abdelrazek N.M. 2019. Parasites and Helicobacter pylori in Egyptian children with or without diabetes with gastrointestinal manifestations and high calprotectin level. Journal of the Egyptian Society of Parasitology 49(1): 243–248. https://doi.org/10.21608/jesp.2019.68310
Poorkhosravani Z., Agholi M., Sharifi-Sarasiabi K., Heydari-Hengami M., Shamseddin J. 2019. Frequency of intestinal parasites in patients with diabetes mellitus compared with healthy controls in Fasa, Fars Province, Iran, 2018. Hormozgan Medical Journal 23(2). https://doi.org/10.5812/hmj.91284
Ambachew S., Assefa M., Tegegne Y., Zeleke A.J. 2020. The prevalence of intestinal parasites and their associated factors among diabetes mellitus patients at the University of Gondar Referral Hospital, Northwest Ethiopia. Journal of Parasitology Research 2020: 8855965. https://doi.org/10.1155/2020/8855965
Chandi D.H., Lakhani S.J. 2020. Prevalence of parasitic infestation in diabetic patients in Tertiary Care Hospital. International Journal of Current Microbiology and Applied Sciences 9(2): 1434–1441. https://doi.org/10.20546/ijcmas.2020.902.166
Abdullahi I., Emeribe A., Umar K., Adekola H. 2020. Prevalence of cryptosporidiosis and associated risk factors among patients with acute diarrhoea attending Abuja Teaching Hospital, Nigeria. Brunei International Medical Journal 16. https://doi.org/10.4103/1596-3519.102852
Popruk N., Prasongwattana S., Mahittikorn A., Palasuwan A., Popruk S., Palasuwan D. 2020. Prevalence and subtype distribution of Blastocystis infection in patients with diabetes mellitus in Thailand. International Journal of Environmental Research and Public Health 17(23): 8877. https://doi.org/10.3390/ijerph17238877
Calderon de la Barca A.M., Castillo-Fimbres R.S., Mejía-Leon M.E., Quihui-Cota L., Ochoa-Leyva A., Aguayo-Patron S.V. 2020. Enteric parasitic infection disturbs bacterial structure in Mexican children with autoantibodies for type 1 diabetes and/or celiac disease. Gut Pathogens 12(1): 1–9. https://doi.org/10.1186/s13099-020-00376-3
Ibrahim S.S., Ismail M.A., Shaker M.A., Khlil D., Raafat A. 2020. Blastocystis hominis in diabetic and non-diabetic patients with irritable boewl syndrome in Beni-Suef city, Egypt. Journal of the Egyptian Society of Parasitology 50(3): 683–688. https://doi.org/10.21608/jesp.2020.131115
Kamki Y., Singh R.H., Singh N.T., Lungram P., Singh B.N. 2015. Intestinal protozoal and helminthic infections in immunocompromised patients attending RIMS Hospital, Imphal. Journal of Medical Society 29(2): 74. https://doi.org/10.4103/0972-4958.163192
Waly W.R., Ismail M., Abu-Sarea E.Y., Abd El Wahab W.M. 2021. Intestinal parasitic infections and associated risk factors in diabetic patients: a case- control study. Journal of Parasitic Diseases 45(4): 1106–1113. https://doi.org/10.1007/s12639-021-01402-0
Sisu A., Abugri J., Ephraim R.K., Dadzie I., Essien- Baidoo S., Kyei-Mensah J., Storph R.P., Toboh E. 2021. Intestinal parasite infections in diabetes mellitus patients: a cross-sectional study of the Bolgatanga municipality, Ghana. Scientific African 11: e00680. https://doi.org/10.1016/j.sciaf.2020.e00680
Sabaa T., Mohammad S.A. 2021. Comparison of some immunological parameters associated with Entamoeba histolytica and Giardia lamblia infections in people with diabetes mellitus. Annals of the Romanian Society for Cell Biology 25(7): 184–193.
Melo G.B., Mazzaro M.C., Gomes-Gouvêa M.S., Santos É.A., Souza L.V., Elias-Oliveira J., Gryschek R.C., Rodrigues R.M., Paula F.M. 2021. Blastocystis subtypes in patients with diabetes mellitus from the Midwest region of Brazil. Revista do Instituto de Medicina Tropical de São Paulo 63. https://doi.org/10.1590/S1678-9946202163032
Almugadam B.S., Ibrahim M.K., Liu Y., Chen S.M., Wang C.H., Shao C.Y., Ren B.W., Tang L. 2021. Association of urogenital and intestinal parasitic infections with type 2 diabetes individuals: a comparative study. BMC Infectious Diseases 21(1): 1–9. https://doi.org/10.1186/s12879-020-05629-9
Sitotaw B., Mekuriaw H., Damtie D. 2019. Prevalence of intestinal parasitic infections and associated risk factors among Jawi primary school children, Jawi town, north-west Ethiopia. BMC Infectious Diseases 19(1): 1–10. https://doi.org/10.1186/s12879-019-3971-x
Dunachie S., Chamnan P. 2019. The double burden of diabetes and global infection in low and middle- income countries. Transactions of the Royal Society of Tropical Medicine and Hygiene 113(2): 56–64. https://doi.org/10.1093/trstmh/try124
Periago M.V., García R., Astudillo O.G., Cabrera M., Abril M.C. 2018. Prevalence of intestinal parasites and the absence of soil-transmitted helminths in Añatuya, Santiago del Estero, Argentina. Parasites and Vectors 11(1): 1–13. https://doi.org/10.1186/s13071-018-3232-7
Qin Q., Yan S., Yang Y., Chen J., Li T., Gao X., Yan H., Wang Y., Wang J., Wang S., Ding S. 2021. A metagenome-wide association study of the gut microbiome and metabolic syndrome. Frontiers in Microbiology 12: 682721. https://doi.org/10.3389/fmicb.2021.682721
Beyhan Y.E., Cengiz Z.T. 2017. Comparison of microscopy, ELISA, and real-time PCR for detection of Giardia intestinalis in human stool specimens. Turkish Journal of Medical Sciences 47(4): 1295–1299. https://doi.org/10.3906/sag-1612-71
Anvari D., Sharif M., Sarvi S., Aghayan S.A., Gholami S., Pagheh A.S., Hosseini S.A., Saberi R., Chegeni T.N., Hosseininejad Z., Daryani A. 2019. Seroprevalence of Toxoplasma gondii infection in cancer patients: a systematic review and meta- analysis. Microbial Pathogenesis 129: 30–42. https://doi.org/10.1016/j.micpath.2019.01.040
Daryani A., Hosseini-Teshnizi S., Hosseini S.A., Ahmadpour E., Sarvi S., Amouei A., Mizani A., Gholami S., Sharif M. 2017. Intestinal parasitic infections in Iranian preschool and school children: a systematic review and meta-analysis. Acta Tropica 169: 69–83. https://doi.org/10.1016/j.actatropica.2017.01.019
Wondmieneh A., Gedefaw G., Alemnew B., Getie A., Bimerew M., Demis A. 2020. Intestinal parasitic infections and associated factors among people living with HIV/AIDS in Ethiopia: A systematic review and meta-analysis. PloS One 15(12). https://doi.org/10.1371/journal.pone.0244887
Behera B., Mirdha B.R., Makharia G.K., Bhatnagar S., Dattagupta S., Samantaray J.C. 2008. Parasites in patients with malabsorption syndrome: a clinical study in children and adults. Digestive Diseases and Sciences 53: 672–679. https://doi.org/10.1007/s10620-007-9927-9
Tracey E.F., McDermott R.A.. McDonald M.I., 2016. Do worms protect against the metabolic syndrome? A systematic review and meta-analysis. Diabetes Research and Clinical Practice 120: 209–220.
Yang Z., Grinchuk V., Smith A., Qin B., Bohl J.A., Sun R., Notari L., Zhang Z., Sesaki H., Urban Jr J.F., Shea-Donohue T. 2013. Parasitic nematode-induced modulation of body weight and associated metabolic dysfunction in mouse models of obesity. Infection and Immunity 81(6): 1905–1914.
Dash N., Al-Zarouni M., Anwar K., Panigrahi D. 2010. Prevalence of intestinal parasitic infections in Sharjah, United Arab Emirates. Human Parasitic Diseases 2: 21. https://doi.org/10.1016/j.ijid.2010.02.2129
Faria C.P., Zanini G.M., Dias G.S., da Silva S., de Freitas M.B., Almendra R., Santana P., Sousa M.D. 2017. Geospatial distribution of intestinal parasitic infections in Rio de Janeiro (Brazil) and its association with social determinants. PLoS Neglected Tropical Diseases 11(3). https://doi.org/10.1371/journal.pntd.0005445
