Over the past two decades, the world has encountered the emergence of three coronaviruses, including SARS-CoV, with mortality rate of 9.5% in September 2003, the new MERS-CoV, which causes respiratory diseases, and first appeared in the Middle East 9 years later, and also a group of patients with pneumonia of un-known cause was observed in Wuhan, China on December 30, 2019. A week later, on January 7, 2020, a novel coronavirus (SARS-CoV-2) was discovered in these patients in Wuhan, China. The virus was formerly known as the novel coronavirus 2019 (2019-nCoV), but on February 11, 2020, the disease was officially renamed to COVID-19 by the World Health Organization (WHO). The COVID-19 was more contagious compared to the previous two generations and infected more people with much more fatalities (1). Examining the laboratory parameters in order to determine the severe or less severe cases of COVID-19, identifying patients who are at higher risk of mortality, and increasing awareness for the appropriate action in improving the clinical situation will be useful (2).
The intestinal parasitic infections (IPIs) are major public health problems with disproportionately high prevalence rates in low- and middle-income countries (LMICs) (3.5 billion people suffering) (3). Four hundred fifty million people develop symptomatic clinical forms, and more than 200,000 deaths are annually reported (4). The IPIs comprise both pathogenic and non-pathogenic protozoa and helminths, which produce a variety of symptoms, including malnutrition, weight loss, growth retardation, malabsorption, anemia, stomach ache, nausea, and vomiting (5). About half of the COVID-19 patients experienced gastrointestinal symptoms, including nausea, diarrhea, vomiting, and abdominal pain, which often precede respiratory symptoms, all of which are signs of the intestinal parasites (6). The concomitant parasitic infections in COVID-19 patients may not have any significant association (7). However, concurrent parasite infections with COVID-19 in the patients may alter the host's immune response to the SARS-CoV-2 with either advantageous or deleterious consequences, like a double-edged sword (8, 9). Indeed, parasite-induced immunomodulatory responses may mute the hyper-inflammation associated with the severe COVID-19 and, in contrast, co-infections may suppress an efficient immune response against SARS-CoV-2 early stage of the infection and increase the complications caused by COVID-19 (10). Since SARS-CoV-2 infection can contribute to the spread (11) or reactivation of infectious diseases and given that many patients with COVID-19 will have some degrees of immunosuppression, it is expected to be at risk of reactivation of dormant/latent parasitic infections, especially in endemic areas (12). Therefore, the present study aimed to evaluate the parasitic infections in the patients hospitalized with COVID-19 in Bandar Abbas city, Iran, in 2020-2021.
The current cross-sectional study was done with the informed consent of the patients tested positive with COVID-19 by polymerase chain reaction (PCR) who were hospitalized at Shahid Mohammadi Hospital in Bandar Abbas County, Hormozgan Province, Iran, between December 2020 and July 2021. The study was approved by the Ethics Committee of the Deputy of Research and Technology of the Hormozgan University of Medical Sciences-Iran with an ethical code (IR.HUMS.REC.1399.428).
The following data were extracted from each patient's medical record by the trained research team of Hormozgan University of Medical Sciences: social demographic, clinical data, laboratory data, underlying diseases, treatment regimens, duration of treatment, and disease outcome.
Fresh fecal samples were collected from the COVID-19 patients to evaluate IPIs. First, the macroscopic and then the microscopic examinations of the samples were conducted through wet mount (WM) (direct wet method with Lugol and physiological saline), and formalin ethyl-acetate concentration technique (FECT). Modified Ziehl-Neelsen and trichrome staining methods were used to increase the sensitivity of the parasite detection (13).
Data analysis
Data were analyzed by the SPSS 26 software using descriptive statistical techniques, including tables of frequency distribution and percentages, sketching qualitative variables, and utilizing statistical indices like mean and standard deviation of quantitative variables. The Chi-square test and Fisher's exact test were utilized to examine the qualitative variables. The non-parametric Mann-Whitney test (two groups) and Kruskal-Wallis test (three groups and more) were used to compare the quantitative variables of age and length of hospitalization among the groups in terms of the abnormal distribution of these two variables in the groups.
P-value | With parasite N=18 | Without parasite N=132 |
All patients N=150 |
Characteristic | Socio-demographic features |
0.462 | 6 (33.3) | 56 (42.4) | 62 (41.3) | Female | Sex, N (%) |
12 (66.7) | 76 (57.6) | 88 (58.7) | Male | ||
0.806 | 52 (21.8) | 49 (23.8) | 49 (23.3) | Age in years [median (IQR)] | |
0.737 | 8 (44.4) | 54 (40.9) | 62 (41.3) | <44 | Age group [years, N (%)] |
3 (16.7) | 33 (25.0) | 36 (24.0) | 45-59 | ||
7 (38.9) | 45 (34.1) | 52 (34.7) | 60≤ | ||
0.573 | 3 (16.7) | 30 (22.7) | 33 (22.0) | Employee | Occupation |
6 (33.3) | 41 (31.1) | 47 (31.3) | Self-Employment | ||
5 (27.8) | 46 (34.8) | 51 (34.0) | Housewife | ||
4 (22.2) | 15 (11.4) | 19 (12.7) | Retired | ||
0.054* | 0 (0.0) | 25 (18.9) | 25 (16.7) | Illiterate | Education level |
15 (83.3) | 74 (56.1) | 89 (59.3) | Diploma and lower | ||
3 (16.7) | 33 (25.0) | 36 (24.0) | college education |
Staining methods | Concentration Techniques | Wet mount | Combined Method | ||||
Modified Ziehl-Neelsen staining Pos (%) |
Trichrome staining Pos (%) |
Formalin-Ethyl acetate Concentration Technique (FECT) Pos (%) | LUGOL'S IODINE STAIN Pos (%) |
Direct fecal smear Pos (%) |
|||
0 (0) | 18 (12.0) | 14 (9.3) | 11 (7.3) | 11 (7.3) | 18 (12.0) | Yes | any Parasite |
150 (100) | 132 (88.0) | 136 (90.7) | 139 (92.7) | 139 (92.7) | 132 (88.0) | No | |
- | 15 (10.0) | 11 (7.3) | 9 (6.0) | 9 (6.0) | 15 (10.0) | Blastocystis spp. | Parasite Species |
- | 2 (1.3) | 2 (1.3) | 1 (0.7) | 1 (0.7) | 2 (1.3) | Giardia lamblia | |
- | 1 (0.7) | 1 (0.7) | 1 (0.7) | 1 (0.7) | 1 (0.7) | Trichomonas hominis |
P-value | With parasite | Without parasite | All patients | Characteristic | |
0.949 | 12 (66.7) | 89 (67.4) | 101 (67.3) | fever | Clinical symptoms and signs |
0.685 | 7 (38.9) | 58 (43.9) | 65 (43.3) | Chills | |
0.015 | 15 (83.3) | 70 (53.0) | 85 (56.7) | decreased appetite | |
0.002 | 8 (44.4) | 19 (24.4) | 27 (18.0) | Stomach ache | |
0.802 | 4(22.2) | 26 (19.7) | 30 (20.0) | Diarrhea | |
0.002 | 4 (22.2) | 5 (3.8) | 9 (6.0) | Flatulence | |
0.264 | 9 (50.0) | 84 (63.6) | 93 (62.0) | Respiratory symptoms | |
1.000* | 0 (0.0) | 3 (2.3) | 3 (2.0) | Loss of smell and/or taste | |
0.212 | 5 (27.8) | 21 (15.9) | 26 (17.3) | Head ache | |
0.330 | 2 (11.1) | 7 (5.3) | 9 (6.0) | Dizziness | |
0.594 | 7 (38.9) | 43 (32.6) | 50 (33.3) | Cough (any type) | |
0.596* | 0 (0.0) | 8 (6.1) | 8 (5.3) | Dry cough | |
1.000* | 0 (0.0) | 1 (0.8) | 1 (0.7) | Haemoptysis | |
0.596* | 0 (0.0) | 8 (6.1) | 8 (5.3) | Vomiting | |
0.101 | 2 (11.1) | 4 (3.0) | 6 (4.0) | Chest pain | |
0.356 | 0 (0.0) | 6 (4.5) | 6 (4.0) | Sore throat | |
0.835 | 7 (38.9) | 48 (36.4) | 55 (36.7) | Dyspnea | |
0.439 | 13 (72.2) | 83 (62.9) | 96 (64.0) | Other symptoms | |
0.444 | 11 (61.1) | 68 (51.5) | 79 (52.7) | Comorbidity (at least 1) | Comorbidities |
0.315 | 2 (11.1) | 28 (21.2) | 30 (20.0) | Hypertension | |
0.559 | 4 (22.2) | 22 (16.7) | 26 (17.3) | Diabetes | |
0.948 | 2 (11.1) | 14 (10.6) | 16 (10.7) | Cardio-vascular diseases | |
1.000* | 0 (0.0) | 5 (3.8) | 5 (3.3) | Chronic liver disease | |
1.000* | 0 (0.0) | 4 (3.0) | 4 (2.7) | Chronic obstructive lung diseases and asthma | |
0.447* | 1 (5.6) | 4 (3.0) | 5 (3.3) | Chronic kidney disease | |
0.447* | 1 (5.6) | 4 (3.0) | 5 (3.3) | Autoimmune diseases | |
1.000* | 0 (0.0) | 2 (1.5) | 2 (1.3) | Tumor | |
1.000* | 0 (0.0) | 1 (0.8) | 1 (0.7) | Hepatitis c | |
1.00 | 18 (100.0) | 130 (97.5) | 148 (98.7) | Hospitalized in COVID-19 ward | Patient condition |
0 (0.0) | 2 (1.5) | 2 (1.3) | Hospitalized in ICU ward | ||
0.879 | 4.0 (2.0) | 4.0 (2.0) | 4.0 (2.0) | Length of stay (LOS)(Days) | |
0.00 | 00 (00) | 00 (00) | 00 (00) | Death |
P-value | With parasite | Without parasite | All patients | Laboratories findings, (median, IQR) |
0.694 | 6.0 (2.9) | 5.8 (4.0) | 5.8 (4.0) | WBC, ×103/uL |
0.784 | 4.5 (1.2) | 4.5 (0.9) | 4.5 (0.9) | RBC, ×106/uL |
0.726 | 13.4 (3.8) | 12.4 (2.8) | 12.4 (2.8) | Hb, g/dL |
0.713 | 37.8 (9.6) | 37.1 (6.7) | 37.4 (6.6) | HCT, % |
0.611 | 203.0 (122.5) | 197.0 (101.0) | 200.0 (106.0) | Plt, ×103/uL |
0.991 | 73.2 (13.5) | 75.0 (16.7) | 75.0 (16.0) | NEUT, % |
0.724 | 19.1 (12.0) | 18.8 (13.5) | 18.8 (13.3) | Lym, % |
0.184 | 4.7 (4.4) | 5.5 (5.0) | 5.0 (5.0) | Mixed, % |
0.694 | 32.5 (14.5) | 33.0 (15.0) | 33.0 (15.0) | Urea, mg/dL |
0.286 | 1.1 (0.4) | 1.0 (0.3) | 1.0 (0.3) | Cr, mg/dL |
0.756 | 137.5 (4.0) | 138.0 (5.0) | 138.0 (5.0) | Na, mEq/L |
0.643 | 4.6 (0.8) | 4.3 (0.8) | 4.4 (0.8) | K, mEq/L |
0.701 | 618.5 (311.8) | 580.0 (345.0) | 580.0 (340.0) | LDH, mg/dL |
0.995 | 599.5 (892.8) | 483.0 (763.0) | 487.0 (766.0) | Ferritin, μg/mL |
0.931 | 36.6 (55.8) | 30.0 (48.0) | 31.0 (48.5) | CRP, mg/Lit |
0.970 | 44.5 (46.5) | 41.0 (30.0) | 42.0 (34.0) | ESR, mm/h |
0.405 | 115.0 (49.0) | 118.0 (55.0) | 118.0 (53.0) | BS, mg/dL |
0.890 | 36.0 (9.5) | 38.0 (17.0) | 37.0 (17.0) | SGOT, U/L |
0.970 | 36.5 (26.3) | 37.0 (26.0) | 37.0 (25.0) | SGPT, U/L |
0.268 | 180.5 (110.5) | 172.0 (80.0) | 172.0 (83.0) | ALP, U/L |
The relatively low prevalence of IPIs was observed in Bandar Abbas, where Blastocystis spp. was the most common intestinal parasite, followed by Giardia lamblia and Trichomonas hominis, respectively. Considering the high prevalence of Strongyloides stercoralis and other opportunistic parasitic infections in Bandar Abbas in the past, the conventional diagnostic methods alone are not sufficient to diagnose the parasitic infections; hence, the specialized methods to diagnose these infections, such as FEC and helminths culture, should be combined with WM as a routine diagnostic method in the medical diagnostic laboratories, as well as collecting several samples on different days before starting chemotherapy, especially for the COVID-19 patients who are taking immunosuppressive drugs.
The authors would like to thank the Hormozgan University of Medical Sciences and Shahid Mohammadi Hospital in Bandar Abbas, Hormozgan Province, Iran, as well as all the staff of this hospital, especially the nurses and doctors working in the COVID-19 wards, for their kind service to the patients.
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Ethical Considerations
The study protocol was approved by the Ethics Committee of the Deputy of Research and Technology of the Hormozgan University of Medical Sciences, Iran (ethical code IR.HUMS.REC.1399.428).
Authors’ Contributions
KS and JS conceived and designed the study. SAM and MN participated in collecting and evaluating the samples. Analysis was performed by SMM, ER and MF. The first draft of the manuscript was written by KS, JS, and SMM and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
The Hormozgan University of Medical Sciences funded this study. There was no influence regarding the study design, collection, analysis, and interpretation, and in the writing of the manuscript by the funding body.
Conflicts of Interest
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