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, Elham Rezaee2 , Majid Najafi-Asl1 , Jebreil Shamseddin3 , Masoud Fotouhizadeh4 , Khojasteh Sharifi-Sarasiabi5 , Seyed Mahmoud Mousavi6
2- Department of Medical Parasitology and Mycology, Faculty of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
3- Infectious and Tropical Diseases Research Center, Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
4- Department Food Hygiene, College of Veterinary Medicine Branch, Islamic Azad University Kazeroon, Iran
5- Infectious and Tropical Diseases Research Center, Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran ,
6- Department of Parasitology and Mycology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran
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.
The present descriptive and cross-sectional study evaluated 150 fecal samples of the COVID-19 patients who were confirmed by PCR and admitted to the Shahid Mohammadi Hospital in Bandar Abbas in 2020-2021. The stool specimens of these patients were examined. Eighty-eight participants (58.7%) were female, and the education level of most participants (59.3%) was high school diploma and lower. The demographic characteristics are shown in Table 1. There was no significant difference between individual demographic variables and parasite prevalence in the stool samples.
The macroscopic examination of the stool samples indicated that the highest frequency of color and consistency of feces were formed (72.0%) and brown (87.3%), respectively. The overall prevalence of IPIs was estimated to be 12% (Table 2). According to the similar studies before the COVID-19 epidemic in Bandar Abbas, Turki et al. (14) reported the prevalence of IPIs to be 6.5% among primary school children in Bandar Abbas. Mohammadi-Meskin et al. (15) reported 55.2% IPI prevalence in intellectually disabled individuals and rehabilitation personnel in Bandar Abbas. Heydari-Hengami et al. (16) reported their prevalence at about 34.9% in food operators in Bandar Abbas. Their findings differed from ours in terms of the frequency of the intestinal parasites owing to the varied demographics. Also among the causes of this decrease in the frequency of intestinal parasites, it could be the general hygiene rules that were observed much more in the period of COVID-19 and decreased interpersonal contact (17). Furthermore, in other parts of the world, Wolday et al. (9) reported a prevalence of 37.8% for IPI in the study of COVID-19 patients in Ethiopia. Al-Khaliq et al. (18) in Baghdad, the capital city of Iraq, reported the prevalence of 1.1% for the intestinal parasites in COVID-19 patients, which were different from our study.
The prevalence of Blastocystis was 10% (Table 2), which was inconsistent with microscopic studies obtained by Turki et al. (14), Heydari-Hengami et al. (16), and Mohammadi-Meskin et al. (15) all in Bandar Abbas with the prevalence of Blastocystis at 2.1%, 24.3% and 30.2%, respectively. Furthermore, in comparison with other studies from other parts of the world; Aydemir et al. (17) in Turkey reported the prevalence of Blastocystis in the period of COVID-19 as 11.86%, which was relatively similar to our study.
Regarding giardiasis, the microscopic examination of our study indicated its prevalence at 1.3% (Table 2), which was similar to the previous studies in Iran before the COVID-19 pandemic conducted by Turki et al. (14) with the prevalence of 2.9%. Our result was inconsistent with the results of studies conducted by Heydari-Hengami et al. (15) and Mohammadi-Meskin et al., (15) in Bandar Abbas that reached the prevalence of 6.8% and 5.6%, respectively. Compared to the other parts of the world; Aydemir et al. (17) in Turkey reported the prevalence of giardiasis in the period of COVID-19 as 1.60%, which was similar to our study. The prevalence of Trichomonas hominis was obtained 0.7% (Table 2).
Even though the parasitic diseases are on the way to decline in Iran compared to the earlier decades, intestinal parasites, particularly protozoa, still remain a difficult public health concern in the areas where there are few healthcare measures (19). Regarding the intestinal helminths infections in our study, no infection was detected among people with COVID-19, but previous studies by Mohammadi-Meskin et al. (15) reported the prevalence of Strongyloides stercoralis at 16.6% in intellectually disabled patients in Bandar Abbas. Since dexamethasone (a corticosteroid) was in use to treat some COVID-19 patients, there was a risk for increased incidence of severe Strongyloides infections by increasing dexamethasone usage (20). Hence, specific parasite detection methods should be examined that was not in the line with our study.
Clinical symptoms were evaluated in individuals with and without parasites (Table 3). Decreased appetite (83.3%), stomach ache (44.4%), and flatulence (22.2%) were significantly higher in individuals with parasites infection compared to those without parasites (P<0.05). There was no significant difference between the presence of the parasite and the other symptoms such as fever and chills (Table 3). Furthermore, no correlation was found between the existence of comorbidities and the patient's condition with the presence or absence of the parasite. Wolday et al. (9) found that concomitant parasitic infections (protozoa and helminths) might protect against progression to the severe COVID-19 in terms of parasitic immune system modulatory responses. Al-Khaliq et al. (18) also showed in their 2021 study an inverse relationship between parasitic infection and COVID-19 infections, however, the possible relationship cannot be reliably speculated and it requires extensive future studies.
So far, the laboratory parameters have been less used for the definitive diagnosis of COVID-19 due to their low sensitivity and specificity, but they have been considered as valuable prognostic indicators and provide useful information regarding the severity of the disease, the course of the disease, and the response to treatment (21). Our laboratory findings of the participants indicated no significant difference in the laboratory results between parasite and non-parasitic groups, however, Tao et al. (22) discovered that various coagulation, cardiac, renal, and hepatic functions such as PT, LDH, Total bilirubin, CRP, and ESR increased in the parasite group. In our study, no significant difference was found between COVID-19 patients with any concomitant parasitic infection compared to the patients without parasitic infection during hospitalization, and no death was reported among the participants (Table 4).
It was the first study on the prevalence of IPIs among the patients with COVID-19 in Bandar Abbas. Microscopic examination of fecal samples of the patients was performed with WM (direct wet method with Lugol and physiological saline) and FECT. Furthermore, modified Ziehl-Neelsen and trichrome staining methods were used for the accurate confirmation to increase the validity of measuring the dependent variable. In this study, no statistically significant difference was shown between different methods in terms of detecting parasites (Table 2), but considering that molecular methods have higher sensitivity than microscopic methods in detecting intestinal parasites (23), one of the limitations of this study could be not applying this technique and since we examined only one replication of stool sample for each patient, we might underestimate the true prevalence of parasitic infections; hence, it is recommended that at least three consecutive samples should be examined from each patient for three consecutive days. Undoubtedly, studies with larger sample sizes as well as further studies to confirm the association of concomitant parasitic infection in the patients with COVID-19 are needed.
Table 1. Socio-demographic characteristics among COVID-19 patients with or without parasitic co-infection
| 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 |
Table 2. Prevalence of intestinal parasite species identified by the wet mount, concentration techniques, and staining methods among COVID-19 patients
| 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 | |
Table 3. Clinical features among COVID-19 patients with or without parasitic co-infection
| 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 |
Table 4. Laboratories findings among COVID-19 patients with or without parasitic co-infection
| 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
Received: 2024/06/16 | Accepted: 2024/09/3 | ePublished: 2024/09/29
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