Abstract
Infection with intestinal parasites is widespread worldwide, especially in developing countries. Intestinal parasites are a major cause of diarrhea in both immunocompetent and immunocompromised people, but cancer patients are more prone to infection. This study aimed to investigate the prevalence and risk factors of intestinal parasitic infections (IPIs) among cancer patients undergoing chemotherapy at Nepal Cancer Hospital and Research Center (NCHRC) in Nepal. One hundred individuals were selected with a convenience sampling strategy. The stool samples were examined by direct wet mount, sedimentation, flotation, and acid-fast methods to determine the prevalence and intensity of IPIs in this population. The overall prevalence of IPIs was 8% (4% protozoan and 4% helminths). Altogether, three species of intestinal parasites were detected. Cryptosporidium (4%) was predominant followed by Trichuris trichiura (2%) and Ancylostoma duodenale (2%). Multivariable regression analysis revealed that “not using soap for handwashing” was significantly associated with the prevalence of overall IPIs. None of the other evaluated risk factors indicated an association with IPIs infection. In this study, the IPIs were attributable to individual hygiene behaviors, but not to nutritional status or socio-demographic characteristics. Yet, significant numbers of males reported anemia and undernutrition in this study population.
Keywords: Cancer patients, Intestinal parasitic infections, Immunocompromised people, Nepal, Prevalence, Risk factors
Introduction
Intestinal parasitosis is one of the major causes of public health problems worldwide, particularly in developing nations such as Nepal. Intestinal parasitosis affects around 1.5 billion people worldwide, 260 million preschool-age children, 654 million school-age children (WHO 2018). Intestinal parasites are one of the leading causes of diarrhea in both immunocompetent and immunocompromised people, but cancer patients are especially vulnerable to contamination (Salehi Kahyesh et al. 2020). In patients with a suppressed immune system, opportunistic parasitic infections are the most common cause of secondary infection (Uysal et al. 2017). Cancer patients receiving chemotherapy and other immunosuppressive medications are always vulnerable to infections, including opportunistic parasites (Salehi et al. 2018). If not diagnosed and treated early, intestinal parasite infections can lead to major consequences in immunocompromised patients. Due to the high rate of the high rate of enteroparasitosis in cancer patients, which is most likely due to their immunocompromised status, these people are more susceptible to becoming infected by a variety of parasite species (Jeske et al. 2017). Opportunistic parasites are usually associated with immunocompromised individuals due to immune system deficiencies. Lymphocytes are impaired in their ability to fight opportunistic infections due to alterations in their cellular and humoral responses. As a result, immunocompromised persons are more vulnerable to microorganisms such as viruses, bacteria, fungi, and parasites (Hassanein and Fanaky 2021). Immunocompromised individuals are more susceptible to opportunistic parasite infection when CD4+ T lymphocyte number drop below 200 cells/L.
In underdeveloped countries, intestinal helminth infections are becoming more common due to poor environmental sanitation, personal cleanliness habits, limited resources, and inadequate hygiene standards. There is a large overlap between chronic diseases including HIV, TB, cancer, and intestinal helminthic infections (Sitotaw et al. 2022). In developing countries like Nepal, intestinal parasite infections are a major cause of morbidity. Ascaris lumbricoides, Hymenolepis nana, hookworm, Trichuris trichiura, Giardia lamblia, and Entamoeba histolytica are the most prevalent intestinal parasites found in Nepal (Dahal et al. 2022). The high occurrence of these intestinal parasitic infestations is closely associated with overall poverty, poor environmental hygiene, and inadequate healthcare (Chandrashekhar et al. 2009).
Earlier studies have suggested that many socioeconomic and behavioral factors are associated with gastrointestinal parasites such as hygiene behaviors (Parajuli et al. 2009), eating raw or unwashed fruits and vegetables (Isazadeh et al. 2020), drinking water quality (Maharjan et al. 2013), parent's occupation and education (Shrestha et al. 2019), family income (Quihuiet al. 2006), children's hygiene and food habits (Maharjan et al. 2013) and malnutrition (Buzigi 2015; Unachukwu and Nwakanma 2018).
Intestinal parasite infections (IPIs) prevalence have been decreasing since the adoption of the national deworming program initiated in 2004. Some earlier studies among ethnic groups still reported a high prevalence (Parajuli et al. 2009; Adhikari et al. 2021). People with cancer may have suppressed immunity to opportunistic intestinal parasites. Hence, this study aims to evaluate such IPIs and associated factors. Further, this design will also allow witnessing the prevalence and intensity of parasitic infection in association with suggested socioeconomic status (SES), and socio-demographic and behavioral factors which may help to formulate relevant policies to support a vulnerable population of society.
Materials and methods
Study area
This study was carried out among cancer patients visiting the Nepal Cancer Hospital and Research Center (NCHRC) located in the Lalitpur metropolitan city in the Lalitpur District of Bagmati Province in central Nepal. Lalitpur metropolitan city lies in the hilly region and extends within 27° 40′ N 85° 19′ E (with an area of 396.92 km2). NCHRC is a privately owned hospital to provide a wide range of care to cancer patients and their families from all over the country. NCHRC provides individual, family, and group counseling sessions for both inpatient and outpatient.
Ethical approval
Hospital authorities were approached with study proposals with the explicit objectives, procedures, and schedules with minimum hinderance in their regular schedules. The ethical approval for this study was obtained from the institutional review board (IRB) of the Institute of Science and Technology (IOST), Tribhuvan University (Approval No. 22–0058) and the IRB of NCHRC.
Study population and sample collection
Each participant was explained about the study protocol and asked if they and/or their parents (in the case of non-adult participants) agreed to participate in the study. As the study was focused on a group of people with a special medical condition, a purposive sampling method was adopted with a sample size of 100. The study was conducted between October 2022 to February 2023. Nutritional status of the participants was accessed by taking anthropometric measurements (height, weight). BMI was evaluated with measured height and weight by using the formula BMI = Weight (kg)/Height (m2). At the same time, the questionnaire survey was conducted among the participants separately and individually in different isolated place within the hospital premises to obtain socio-economic, and socio-demographic data. Participants in the study site were recruited on a first come first served basis, i.e., a purposive sampling technique was followed. Patients diagnosed with cancer and undergoing the treatment were included, and the cases who reported recent (≤1 month or less) intake of anthelmintics were excluded in the study.
The participants were instructed to use a clean stick to scoop a small portion of their faeces from the first, middle, and last parts in the morning and to transfer it into the already provided sterile collection vial. Care was taken not to contaminate the sample with urine or soil. The collected samples were preserved in 2.5% of potassium dichromate solution and stored at 4 °C until laboratory analysis. The data regarding the blood parameters of the subjects under investigation was obtained from the hospital records (i.e., secondary data). The definition of World Health Organization (WHO) was used to define anaemia wherein haemoglobin less than 13 g/dl in men and less than 12 g/dl in non-pregnant women was considered anaemic as suggested by Bhandari et al. (2021).
Lab examination of fecal samples
All the fecal samples were macroscopically examined for their consistency and to find if any adult worms were present. The intestinal parasites were identified on the basis of morphometric characteristics (cysts, oocysts, eggs and larvae) using an Olympus compound microscope. Wet mounts (physiological saline and 1% Lugols iodine solution), floatation technique, sedimentation technique and acid-fast stainingwere adopted to ensure the detection of intestinal parasites (Dhakal et al. 2023). The photographs of the diagnostic stages of parasites were taken at 400 × magnification and identified based on the morphometric characters (shape, size, color, cyst wall, shell structure, internal content of the cyst or oocyst or eggs or larvae). The parasite intensity was categorized according to Erdman (1981) where ‘0’was assigned for the absence of any IPIs egg/oocyst, ‘1’for few eggs/oocysts (1–5 eggs/oocysts) per high power field (HPF), ‘2’ for moderate eggs/oocysts (6–20 eggs per HPF), and ‘3’for many eggs (> 20 eggs/oocysts) per HPF (400x) field of microscope.
Data analysis
All behavioral, demographic, and socioeconomic questions were coded, and the distributions of all variables were examined. For multiple group comparisons (Table 1), independent t-test was used for continuous data while a Chi-square/ Fisher’s Exact test was used for analyzing categorical data (Fig. 1). Multivariable logistic regression was used to investigate the association between the prevalence of overall IPIs and possible risk factors, (hygiene behaviors, nutritional status, socio-demographic characteristics, and community). The level of significance was set at p < 0.05. All the statistical analyses were performed using using IBM SPSS statistic v25.
Table 1.
Characteristic features of the studied cancer patients in Nepal
| Parameter | Male (n = 50) | Female (n = 50) | p value | Total |
|---|---|---|---|---|
| Mean ± SD/n(%) | Mean ± SD/n (%) | Mean ± SD/n(%) | ||
| Demographic parameter | ||||
| Age (years) | 40.40 ± 25.99 | 54.34 ± 12.49 | 0.001a | 47.37 ± 21.47 |
| Weight (kg) | 50.32 ± 19.50 | 59.18 ± 11.28 | 0.007a | 54.75 ± 16.46 |
| Height (Metre) | 1.51 ± 0.25 | 1.54 ± 0.06 | NSa | 1.53 ± 0.18 |
| BMI (kg/m2) | 20.93 ± 4.93 | 24.86 ± 4.17 | 0.000a | 22.9 ± 4.95 |
| Blood parameter | ||||
| Hemoglobin gram/decilitre (g/dl) | 12.00 ± 1.64 | 11.73 ± 1.65 | NSa | 11.86 ± 1.64 |
| Total leucocyte count (TLC) | 7762 ± 4821 | 6820 ± 3592 | NSa | 7290.61 ± 4256.21 |
| Differential leucocyte count (DLC) | ||||
| Neutrophils | 61.23 (11.05) | 61.90 (10.74) | NSa | 61.56 (10.7) |
| Lymphocytes | 34.88 (10.74) | 33.68 (11.60) | NSa | 34.28 (11.14) |
| Monocytes | 2.94 (2.56) | 2.56 (2.04) | NSa | 2.75 (2.31) |
| Eosinophils | 1.57 (1.60) | 1.70 (2.26) | NSa | 1.63 (1.95) |
| Socioeconomic parameter | ||||
| Household (HH) crowding | ||||
| Yes (> 5 member in HH) | 37(74) | 36(72) | NS* | 73(73) |
| No (< 5 member in HH) | 13(26) | 14(28) | 27(27) | |
| Can read and write | ||||
| Yes (Literate) | 44(88) | 45(90) | NS* | 89(89) |
| No (Illiterate) | 6(12) | 5(10) | 11(11) | |
| Reported SES | ||||
| Normal | 34(68) | 35(70) | NS* | 69(69) |
| Good | 16(32) | 15(30) | 31(31) | |
| Rear poultry and/or pets in house | ||||
| Yes | 4 (8) | 3 (6) | NS* | 7 (7) |
| No | 46(92) | 47(94) | 93(93) | |
| Do you exercise regularly? | ||||
| Yes | 8(16) | 12(24) | NS* | 20(20) |
| No | 42(84) | 38(76) | 80(80) | |
| Do you consume meat? | ||||
| Rarely | 21(42) | 14(28) | NS* | 35(35) |
| Frequently | 29(58) | 36(72) | 65(65) | |
| Do you consume fruits? | ||||
| Rarely | 9(18) | 2 (4) | 0.051 | 11(11) |
| Frequently | 41(84) | 48(96) | 89(89) | |
aIndependent T-test
*Chi square test
Fig. 1.
Behavioral, lifestyle and health status characteristics of studied cancer patients in Nepal
Results
Table 1 illustrates that the study participants mostly were middle-aged with a mean age of 47.37 years, with more older females compared to male participants (p < 0.001) in the study. Women participants were heavier and with higher BMI compared to male participants. Yet, height and blood parameters including haemoglobin (Hb), total leucocyte count (TLC), differential leucotyte count (DLC—neutrophil, eosinophil, and monocytes) were comparable between males and females. Similarly, none of the socio-economic factors differed between male and female participants except fruit consuming habits. More frequent fruit consumption was reported by female participants compared to males (p ~ 0.05). Most of the participants reported households with more than 5 members in households, can read and write with normal (SES) and frequent consumption of meat. However, the majority of them did not exercise and did not have pets or poultry at home.
Figure 1 represents the behavioral and lifestyle characteristics of the study participants, with healthier behavioral and lifestyle characteristics (i.e., handwashing before eating and wearingfootwear while outdoors) among females compared to male participants (p < 0.05) in the study. Yet, males reported frequent recent consumption of anthelminthic drugs than females (p < 0.05). There was no significant difference between male and female participants in nail trimming habits. Most of the participants reported knowledge of IPIs, and covering food. However, more than one-third of the participants were found not trimming their nails regularly (data not shown). Two third of participants were anemic while males dominated the prevalence of anemia compared to females. Similarly, one-third of the participants were overweight and among them more than half were women. While males reported significantly high prevalence of underweight compared to women participants (p < 0.001).
Characteristics and behaviours differed significantly between male and female participants *: at p < 0.05 and ** p < 0.01.
Of the 100 fecal samples evaluated, only 8 samples (8%) were found shedding one or more species of IPIs (Table 2) including Cryptosporidium (4%), T. trichiura (2%), and hookworms (2%). The male participants had significantly high IPIs prevalence (Chi square p < 0.030) (Table3) and egg density (t-test, p = 0.06) but statistically not significant.
Table 2.
Prevalence of intestinal parasites in the studied cancer patients in Nepal (n = 100)
| Parasite species | Male (%) | Female (%) | Fisher’s Exact test p value | Total |
|---|---|---|---|---|
| Cryptosporidium | 3 (6) | 1 (2) | NA | 4 (4) |
| Trichuris trichiura | 2 (4) | 0 (0) | NA | 2 (2) |
| Hookworms | 2 (4) | 0 (0) | NA | 2 (2) |
| Infection density | 0.20 (0.54) | 0.04 (0.28) | 0.065a | |
| Total infection | 7(14) | 1 (2) | 0.03* | 8 (8) |
| Protozoa | 3 (6) | 1 (2) | NA | 4 (4) |
| Helminth | 4 (8) | 0 (0) | NA | 4 (4) |
aIndependent T-test
*Fisher’s Exact test
Table 3.
Prevalence and odds ratio of IPIs with of the studied cancer patients in Nepal with respect to behavioral and individual characteristics (n = 100)
| Any IPIs (n = 100) | |||
|---|---|---|---|
| % | Univariate | Multivariate* | |
| OR (95%CI) | AOR (95%CI) | ||
| Socioeconomic (SES) Parameter | |||
| Household (HH) Crowding | |||
| No (< 5 member in HH) | 11.11 | ref | |
| Yes (> 5 member in HH) | 6.84 | 0.59 (0.13 to 2.65) | |
| Can read and write | |||
| Yes (Literate) | 7.87 | ref | |
| No (Illiterate) | 9.09 | 1.17 (0.13 to 10.52) | |
| Reported SES | |||
| Middle High | 3.2 | ref | |
| Low | 10.14 | 3.39 (0.40 to 28.79) | |
| Do you exercise regularly? | |||
| Yes | 20 | ref | ref |
| No | 5 | 0.21 (0.05 to 0.93) | 0.08 (0.01 to 0.52) |
| Use of soap for handwashing | |||
| Yes | 6.38 | ref | ref |
| No | 33.33 | 7.33 (1.11 to 48.45) | 9.55 (1.03 to 88.46) |
| Walk barefoot while outdoor | |||
| Yes | 16.67 | ref | |
| No | 6.81 | 2.73 (0.49 to 15.41) | |
| BMI category | |||
| Underweight | 18.18 | 3.11 (0.63 to 15.34) | |
| Normal | 6.67 | ref | |
| Overweight | 3.03 | 0.44 (0.04 to 4.41) | |
| Anemia | |||
| No | 2.77 | ref | |
| Yes | 10.94 | 4.30 (0.51 to 36.43) | |
| Did you trim nails regularly? | |||
| Rarely | 7.93 | ref | |
| Frequently | 8.10 | 1.02 (0.23 to 4.55) | |
| Did you consume anthelminthic within 6 months? | |||
| Yes | 18.75 | ref | |
| No | 5.95 | 0.27 (0.06 to 1.29) | |
*Model adjusted for gender
OR Odds ratio, AOR Adjusted odds ratio, CI Confidence interval, % Percentage, ref Reference
Table 3 shows the association between parasite infections and associated factors. The presence of any parasite infection was higher among participants doing frequent exercise compared to participants who exercise rarely. This study also indicates that the prevalence of IPIs was significantly high among participants who did not use soap to wash hands before eating (p < 0.001) in both univariate as well as adjusted multivariate model. However, the prevalence of IPIs was not associated with any demographic, SES, lifestyle, or other behavioral characteristics evaluated.
Discussion
Intestinal parasites are considered as major health problems particularly in resource poor countries where overcrowding, inadequate environmental sanitation, and poor personal hygiene behavior are common (WHO 2018). Soil-transmitted helminth diseases caused by Ascaris, Trichuris, and hookworms are the most common, with more than 1.5 billion people believed to be infected (WHO 2018). Coccidian protozoa and microsporidia are opportunistic pathogens with their common occurrence in immunocompromised individuals. In most cases, these parasites invade the intestinal epithelium, leading to secretory diarrhea and malabsorption. Immunocompromised individuals have a larger illness burden and a longer disease timeline (Einhorn et al. 2023).
This study investigated the prevalence of IPIs among cancer patients with suppressed immunity. The prevalence of IPIs in this study (i.e., 8%) is comparable with the prevalence of IPIs reported from different studies such as 10% (10/100) among cancer patients in Ardabil Province, Northwest Iran (Mohammadi-Ghalehbin et al. 2017), 9.9% (9/91) among leukemic patient in Turkey (Uysal et al. 2017) and 8.5% (8/94) in Turkey (Karabey et al. 2021). A lower prevalence of IPIs compared to this study has also been reported among cancer patients like 4.8% (12/250) in Shahrekord, Central Southwest Iran (Banihashemi et al. 2020). In contrast, quite a high prevalence of IPIs have also been reported by many previous studies. For instance, in Ahvaz, Southwest Iran, 38.38% (19/52) individuals were infected with intestinal parasites (Salehi Kahyesh et al. 2020). Similarly, in a study of intestinal parasites in cancer patients in 15 municipalities in southern Brazil 61.65% (45/73) samples were found positive for parasites (Jeske et al. 2017). Another study at King Khalid University Hospital in Saudi Arabia reported an overall prevalence of 88.9% (48/54) among cancer patients. Patients with lymphoma had a higher incidence of Cryptosporidium (100%) and Cyclospora (66.6%), respectively (Sanad et al. 2014). Such a discrepancy in the prevalence of IPIs mightbe due to the difference in climatic conditions and different levels of awareness (Adhikari et al. 2021). The lower prevalence of IPIs in this study participants may be partially explained by ongoing routine deworming programs. In addition, most of the participants reported healthier behavioral and lifestyle characteristics, knowledge of IPIs, and covering food.
The prevalence of overall IPIs was higher among males compared to females. Yet males indicated higher egg density compared to females but could not achieve statistical significance. A few earlier studies reported similar findings with elevated IPIs prevalence among males compared to females (Dersoet al. 2021; Sharma et al. 2021; Ifeoma et al. 2022; Ulhaq et al. 2022). Yet, a few studies reported similar risks of IPIs between males and females among cancer patients (Al-Qobati et al. 2012). In this study, majority of females reported healthier behavioral and lifestyle characteristics compared to male participants (p < 0.05), which may explain the discrepancy in IPIs infection by gender. Further, males had a higher prevalence of anemia and undernutrition with low BMI which may lead to weak nutritional as well as immunity for elevated IPIs infections. Yet, further study needs to be conducted to confirm this association.
The prevalance of IPIs was higher among participants involved in frequent exercise. None of the previous studies evaluated such an association in Nepal. However, it can be assumed that regular exercise may enhance the chance of contamination of the hand with the surface and may also contribute to infestation by hookworm or Strongyloides, if the participants walked barefoot. About 24% of the males reported barefoot walking while outdoors indicated higher IPIs compared to females. In addition, hand washing habits are consistently associated with IPIs prevalence in univariate and multivariate models after adjustment with gender and exercise. Yet, the small sample size limits for generalization and further studies are warranted to confirm this association.
This study also indicates that the prevalence of IPIs was significantly high among participants who did not use soap to wash their hands before eating (p < 0.001) in both univariate as well as adjusted multivariate models. However, the prevalence of IPIs was not associated with any demographic, SES, lifestyle, or other behavioral characteristics evaluated. The findings agree with previous studies (Olsen et al. 2001) that reported a significant association between “not using soap for hand washing” after defecation with round worm infection among 2 to 12 year old children in Egypt. A faecal-oral route of transmission is the established route of transmission of IPIs (Parajuli et al. 2009, 2014). This is probably because the sevariables were proxy measures of poor hygiene in general. However, the odds ratios were always consistently greater for both univariate and multivariate models after adjustment. Since the participants are cancer-diagnosed patients with compromised immunity, hand hygiene might be crucial among current vulnerable populations.
Conclusion
IPIs among vulnerable (i.e., immunocompromised because of ongoing chemotherapy) populations may pose a serious health problem. Multivariate logistic regression analysis showed that the IPIs were attributable to individual differences in behavior like “not using soap for handwashing”. High malnutrition (reported under, overnutrition, and high anaemia) that stemmed from their dietary patterns, medication, and morbidity might worsen the situation of cancer patients together with IPIs. Yet, the small sample size and cross-sectional design limit us for generalization. Health education on hygiene habits should be given to cancer patients to minimize the risk of IPIs.
Acknowledgements
The authors want to thank Dr. Anjali Pandit and Dr. Pravin Jaiswal for their co-operation and support throughout the study. Further, thanks to Mrs. Urina Shrestha and the rest of the staff at the Nepal Cancer Hospital and Research Center for their kind support during the study. Authors are very thankful to the participants and their parents for their participation in this study, support, and cooperation for the sample and questionnaire survey.
Author Contributions
BS: Conceptualization, Methodology, Investigation, and Original draft preparation. PD: Conceptualization, Methodology, Writing-Reviewing. RPP: Supervision, Investigation, Writing-Reviewing and Resources.
Funding
The author would like to thank the university grant commission (UGC; Grant #MRS-78-79-S and T-140) for providing research funding for this study. This work received support from the "Higher Education Reform Project (HERP) DLI-7B Research Grant, Nepal. The funders played no role in the study's design, data collection, analysis and interpretation, manuscript composition, or the determination to publish.
Data availability
Data sets generated during the study are available from the corresponding author on reasonable request.
Declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- Adhikari RB, Parajuli RP, Maharjan M, Ghimire TR. Prevalence and risk factors of gastrointestinal parasites in the Chepangs in Nepal. Ann Parasitol. 2021;67(3):387–405. doi: 10.17420/ap6703.353. [DOI] [PubMed] [Google Scholar]
- Al-Qobati SA, Al-Maktari MT, Al-Zoa AMB, Derhim M. Intestinal parasitosis among Yemeni patients with cancer, Sana’a, Yemen. J Egypt Soc Parasitol. 2012;42(3):727–734. doi: 10.12816/0006356. [DOI] [PubMed] [Google Scholar]
- Banihashemi SM, Soleymani E, Abdizadeh R, Motavalli Haghi M, Khalili B. Intestinal protozoan infections in cancer patients undergoing chemotherapy in shahrekord the central southwest of Iran in 2018. Int J Epidemiol Res. 2020;7(4):144–151. doi: 10.34172/ijer.2020.26. [DOI] [Google Scholar]
- Bhandari A, Shah P, Pandey NK, Nepal R, Sherchand O. Anaemia among patients of heart failure in a tertiary care centre of Nepal: a descriptive cross-sectional study. JNMA J Nepal Med Assoc. 2021;59(241):833–838. doi: 10.31729/jnma.6486. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buzigi E. Prevalence of intestinal parasites, and its association with severe acute malnutrition related diarrhoea. J Biol Agric Healthcare. 2015;5(2):81–92. [Google Scholar]
- Chandrashekhar T, Joshi H, Gurung M, Subba S, Shivananda RMP. Prevalence and distribution of intestinal parasitic infestations among school children in Kaski District. Western Nepal J Biomed Res. 2009;4(1):78–82. doi: 10.4314/jmbr.v4i1.10672. [DOI] [Google Scholar]
- Dahal A, Roka DB, Prasad SM, Shrestha S. Prevalence of intestinal parasitic infection among school children in Kirtipur Municipality. Kathmandu Nepal Med Coll J. 2022;24(2):121–126. doi: 10.3126/nmcj.v24i2.46027. [DOI] [Google Scholar]
- Derso A, Yenealem G, Addisu A. A five-year trend of intestinal parasite prevalence among students attending clinic at University of Gondar, Northwest Ethiopia. J Parasitol Res. 2021;10:1–5. doi: 10.1155/2021/8897935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dhakal P, Sharma HP, Shah R, Thapa PJ, Pokheral CP. Copromicroscopic study of gastrointestinal parasites in captive mammals at Central Zoo, Lalitpur. Nepal Vet Med Sci. 2023;9(1):457–464. doi: 10.1002/vms3.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Einhorn N, Lamphier I, Klinkova O, Baluch A, Pasikhova Y, Greene J, Einhorn N, Lamphier I, Klinkova O, Baluch A, Pasikhova Y, Greene J. Intestinal coccidian infections in cancer patients: a case series. Cureus. 2023 doi: 10.7759/cureus.38256. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Erdman DD. Clinical comparisonof ethyl acetate and diethyl ether inthe formalin-ether sedimentation technique. J Clin Microbiol. 1981 doi: 10.1128/jcm.14.5.483-485.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hassanein F, Fanaky N. Systematic review of opportunistic parasites among Egyptian immunocompromised individuals from 2010 to 2020. Parasitol United J. 2021;14(2):122–132. doi: 10.21608/PUJ.2021.70785.1115. [DOI] [Google Scholar]
- Ifeoma A, Apalata T, Aviwe B, Oladimeji O, Abaver DT. Prevalence of intestinal parasites in HIV/AIDS-infected patients attending clinics in selected areas of the eastern cape. Microbiol Res. 2022;13(3):574–583. doi: 10.3390/microbiolres13030040. [DOI] [Google Scholar]
- Isazadeh M, Mirzaii-Dizgah I, Shaddel M, Homayouni MM. The prevalence of parasitic contamination of fresh vegetables in Tehran. Iran Turk Parazitolojii Derg. 2020;44(3):143–148. doi: 10.4274/tpd.galenos.2020.6469. [DOI] [PubMed] [Google Scholar]
- Jeske S, Bianchi TF, Moura MQ, Baccega B, Pinto NB, Berne MEA, Villela MM. Intestinal parasites in cancer patients in the South of Brazil. Braz J Biol. 2017;78(3):574–578. doi: 10.1590/1519-6984.175364. [DOI] [PubMed] [Google Scholar]
- Karabey M, Can H, Öner TÖ, Döşkaya M, Alak SE, Döşkaya AD, Karakavuk M, Köseoğlu AE, Ün C, Gürüz AY, Alacacıoğlu A, Pektaş B, Gül A, Kaya S, Gökmen AA. Cryptosporidium spp. during chemotherapy: a cross-sectional study of 94 patients with malignant solid tumor. Ann Saudi Med. 2021;41(5):293–298. doi: 10.5144/0256-4947.2021.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maharjan R, Timilshina M, Shakya R, Bhattarai S, Bhattarai S, Gurung P. Prevalence of intestinal parasitic infection of kindergarten children. Int J Infect Microbiol. 2013;2(3):111–113. doi: 10.3126/ijim.v2i3.8205. [DOI] [Google Scholar]
- Mohammadi-Ghalehbin B, Pezeshki A, Kohansal MH, Esmaeilnezhad G. Frequency of intestinal parasites in patients with malignancy in Ardabil Prov-ince, Northwest Iran. J Hum Environ Health Promot. 2017;2(2):118–124. doi: 10.29252/jhehp.2.2.118. [DOI] [Google Scholar]
- Parajuli RP, Umezaki M, Watanabe C. Behavioral and nutritional factors and geohelminth infection among two ethnic groups in the Terai region. Nepal Am J Hum Biol. 2009;21(1):98–104. doi: 10.1002/ajhb.20825. [DOI] [PubMed] [Google Scholar]
- Parajuli RP, Fujiwara T, Umezaki M, Konishi S, Takane E, Maharjan M, Tachibana K, Jiang HW, Pahari K, Watanabe C. Prevalence and risk factors of soil-transmitted helminth infection in Nepal. Trans R Soc Trop Med Hyg T Roy Soc Trop Med H. 2014;108(4):228–236. doi: 10.1093/trstmh/tru013. [DOI] [PubMed] [Google Scholar]
- Olsen A, Samuelsen H, Onyango-Ouma W. A study of risk factors for intestinal helminth infections using epidemiological and anthropological approaches. J Biosoc Sci. 2001;33(4):569–584. doi: 10.1017/s0021932001005697. [DOI] [PubMed] [Google Scholar]
- Quihui L, Valencia ME, Crompton DWT, Phillips S, Hagan P, Morales G, Díaz-Camacho SP. Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in Mexican rural schoolchildren. BMC Public Health. 2006;6(1):1–8. doi: 10.1186/1471-2458-6-225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salehi S, Elmi T, Meamar AR, Basi A, Mirhosseini A, Najm M, Namdari H, Ranjbar M. Investigating the prevalence of enteric opportunistic parasitic infections among cancer patients of a teaching hospital. Int J Hosp Res. 2018;7(1):12–22. doi: 10.15171/ijhr.2018.xx. [DOI] [Google Scholar]
- Salehi Kahyesh R, Algasi A, Haddadi S, Sharhani A. Intestinal parasites infection in children with cancer in Ahvaz, Southwest Iran. Interdiscip Perspect Infect Dis. 2020 doi: 10.1155/2020/8839740. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanad MM, Thagfan FA, Al Olayan EM, Almogren A, Al Hammaad A, Al- Mawash A, Mohamed AA. Opportunistic coccidian parasites among saudi cancer patients presenting with diarrhea: Prevalence and immune status. J Parasitol. 2014;9(2):55–63. doi: 10.3923/jp.2014.55.63. [DOI] [Google Scholar]
- Sharma MR, Jha S, Jha P, Dahal P. Prevalence of intestinal parasites among the patients visiting sub-regional hospital, Dadeldhura. Nepal Hijost. 2021;5(01):15–19. doi: 10.3126/hijost.v5i01.42145. [DOI] [Google Scholar]
- Shrestha J, Bhattachan B, Rai G, Park EY, Rai SK. Intestinal parasitic infections among public and private schoolchildren of Kathmandu, Nepal: prevalence and associated risk factors. BMC Res Notes. 2019;12(1):1–7. doi: 10.1186/s13104-019-4225-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sitotaw E, Sitotaw A, Aleka Y, Lemma M. Research article prevalence of intestinal helminths among cancer patients who are under chemotherapy at the University of Gondar Comprehensive Specialized Hospital Oncology Clinic. J Cancer Epidemiol. 2022 doi: 10.1155/2022/4484183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ulhaq Z, Khan W, Khan MF, Kabir M, Ujjan AA, Ullah W, Masood Z, Khan S, De P, Escalante R. Prevalence of intestinal parasitic diseases in school children of rural areas of district Lower Dir. Pakistan Int J Parasitol. 2022;4(1):19–24. doi: 10.1590/1519-6984.243150. [DOI] [PubMed] [Google Scholar]
- Unachukwu MN, Nwakanma C. Prevalence of intestinal parasitic infection and malnutrition in Enugu Urban and Suburban Area. Int J Med Res. 2018;2(6):565–572. doi: 10.17511/ijmrr.2014.i06.10. [DOI] [Google Scholar]
- Uysal S, Öztürk EA, Tunalı V, Uysal A, Ünver A, Saydam G, Taşbakan MI, Pullukçu H, Turgay N, Arda B. Intestinal parasitic infections in leukemic patients with diarrhea. J Microbiol Infect Dis. 2017;7(2):63–66. doi: 10.5799/ahinjs.02.2017.02.0256. [DOI] [Google Scholar]
- WHO (2018) Soil-transmitted helminth infections: Key facts. World Health Organization. https://apps.who.int/iris/handle/10665/42281, Accessed 24 October 2023
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Data sets generated during the study are available from the corresponding author on reasonable request.