Keywords
University of Mbujimayi/Intestinal Parasitosis/Season/ Association/Protozoa/Helminths
Intestinal parasitoses are one of the main causes of morbidity and mortality in Africa, with a prevalence of 42.18%. The tropical climate in the D.R. Congo provides parasites with an environment conducive to their proliferation. The prevalence rates of intestinal parasitoses remain poorly understood in the D.R. Congo.
This study aims to estimate the overall and specific prevalence of intestinal parasitosis and to determine an association between intestinal parasitosis and the season.
From January 1, 2020, to December 31, 2021, patients for whom a direct stool examination was requested at the Notre Dame de l’Espérance University Hospital Center were included in this study. Stool samples were collected and examined under an optical microscope.
During the period of the study, we recorded 187 patients aged 2 to 77 years. The prevalence of intestinal parasitosis was 75.40%. The specific prevalence rates for parasites were as follows: Entamoeba H., the most common, with a prevalence of 55.08%, followed by Trichomonas I. and Giardia L. with respective prevalence rates of 9.09% and 6.24%. Ascaris L. had a prevalence of 27.81%, followed by Schistosoma M., Ankylostoma D., and Enterobius V. with respective prevalence rates of 3.74%, 1.60%, and 1.07%. There was no association between the season and the overall prevalence of intestinal parasitosis.
The prevalence of intestinal parasitosis was higher during the dry season. There is no statistically valid association between the season and the prevalence of intestinal parasitosis.
University of Mbujimayi/Intestinal Parasitosis/Season/ Association/Protozoa/Helminths
Intestinal parasitic infections are serious diseases worldwide. However, doctors working in these regions tend to give them little attention due to the commonality of their occurrence. As a result, they are rarely a reason for regular consultation.1,2 Although they attract little interest today compared to diseases such as AIDS, tuberculosis, malaria, and onchocerciasis, they remain a public health issue in tropical and impoverished areas.3
Climatic conditions are one of the main factors that contribute greatly to the spread of intestinal parasitic infections, by increasing their transmission and perpetuating the parasitic cycles.4
According to World Health Organization (WHO) estimates, more than three billion people are affected, with 450 million severely ill; of these, over 50% are school-aged children.5 The global prevalence is 35.8% in the world population.6 These diseases have disastrous health, social, and economic consequences for more than one billion people (WHO, 2023).
In Africa, a study conducted in Morocco in 2019 among migrants from sub-Saharan Africa (Equatorial Guinea “30.6%”, Côte d’Ivoire “16.6%”, Senegal “9.29%”, Cameroon “8.01%”, with the remaining patients coming from Niger, Togo, Congo, Burkina Faso, Mali, Gabon, and Benin “35.5%”) showed a prevalence of 43.18% for intestinal parasitic infections. Among these individuals, 63.15% were infested with various digestive parasites simultaneously.7 A study conducted at the University Hospital of Tlemcen, ABOU BEKR BELKAID University in Algeria in 2016 showed that among the identified protozoa, Blastocystis Hominis was the most common (76.6%), followed by Endolimax Nanus and Giardia Intestinalis, with 10.6% each.8 In Senegal, a study conducted in 2010 by Diallo on the prevalence of helminths revealed the following frequencies: Ascaris Lumbricoides (1.9%), Strongyloides Stercoralis (0.8%), Trichuris Trichiura (0.4%), Enterobius vermicularis (0.1%), and Taenia Saginata (0.04%).9
In the DRC, parasitic infections pose a public health problem due to multiple crises that have led to displacement and a lack of potable water, food hygiene, and sanitary facilities.10 A study conducted in Bukavu in 2016 on the impact of seasons on intestinal parasitic infections showed a prevalence of 94%. The identified helminths, in decreasing order of frequency, were: Schistosoma M. (30.6%), Strongyloides S. (21.3%), Ankylostoma D. (13.6%), Ascaris L. (12.6%), Trichuris T. (9.0%), and Taenia S. (6.6%). Identified protozoa included Trichomonas I. (13.69%), Entamoeba H. (6.75%), and Giardia L. (4.76%).11 According to a 2019 study conducted in Kinshasa by Dr. Mulumba, Ntumpa, and Muhido on geo-helminth prevalence, Ascaris lumbricoides had the highest prevalence (27%), followed by T. trichiura (10.3%), S. stercoralis (2.9%), and Ankylostoma sp. (2.8%). All these nematodes showed a decline during the study period, except for A. lumbricoides, which increased at a rate 3.2 times faster in children than in adults.12
The East Kasai region is dominated by a humid tropical climate. The population living in the eastern part of its capital, Mbujimayi, and the surrounding villages, served by CHUNDE, is poor and lives in very poor hygienic conditions. We have not identified any study that could inform us about the prevalence of intestinal parasitic infections here.
The prevalence of intestinal parasitic infections is likely very high at CHUNDE and may be associated with the season.
This study included patients who consulted at the Notre Dame de l’Espérance University Hospital Center (CHUNDE) and were requested to have a direct stool examination. This center serves the East Kasai province, particularly the rural-urban areas to the east of Mbujimayi city in the DRC. These areas are characterized by poor sanitary and economic conditions. The study period was from January 1, 2020, to December 31, 2021.
The study included all patients who consulted at CHUNDE during the study period and were requested by physicians to have a direct stool examination. Patients who did not provide a sample for this examination were excluded.
Fresh stool samples of approximately 10-20 grams (5-6 milliliters if liquid) were collected by the patient. For this collection, the laboratory provided each patient with a clean container and rod.
The direct stool examination was conducted within 30 minutes of sample collection. Approximately 2 grams of stool were mixed with 1 milliliter of saline solution (0.9%) on a slide. After homogenization, this preparation was covered with a slide and observed under an optical microscope at 10x and 40x objectives. The results were recorded in the laboratory register and entered into an Excel database as follows: Parasitic infection (yes, no), type of parasite (helminths, protozoa), multiple infestation (yes, no), types of combined parasites, Entamoeba Histolytica (yes, no), Giardia Lamblia (yes, no), Trichomonas Intestinalis (yes, no), Ascaris Lumbricoides (yes, no), Schistosoma mansoni (yes, no), Ankylostoma Duodenalis (yes, no), Enterobius Vermicularis (yes, no). Cases of Entamoeba Histolytica also included those of Entamoeba Dispar due to the difficulty in distinguishing them microscopically.
The prevalence of intestinal parasitic infections was calculated by dividing the number of patients with at least one identified parasite in a direct stool examination by the total number of patients who underwent this examination. The prevalence in a given population group was calculated by dividing the number of patients in that group with at least one identified parasite by the total number of patients in that group who underwent this examination. The prevalence of a specific intestinal parasitic infection was calculated by dividing the number of patients with a specific parasite by the total number of patients who underwent the examination. The confidence interval (CI) for each prevalence rate is 95%. Statistical analyses were performed using EPI INFO 7.2.6.0 and R version 4.3.3.
This study received approval from the ethics committee of the University of Mbujimayi on N52/CEUM1209 of 11th December 2019. It was conducted in accordance with the requirements of good clinical practices and the principles of the Helsinki Declaration of the World Medical Association, along with any subsequent relevant amendments.
All patients who have participated in this study have provided their consent by signing a written Document, the consent form.
From January 1, 2020, to December 31, 2021, 187 patients were included in our study.
Table 1 and Figure 1 summarize their demographic characteristics: Among the 187 patients included in our study, 94 were female and 93 were male. The sex ratio was one woman for one man. A total of 158 patients were adults [≥18 years <70], 20 were children [<18 years], and 9 were elderly [≥70 years]. The mean age was 41.68 ± 17.95 years. The youngest patient was 2 years old, and the oldest was 77 years.
Frequencies (N=187) | % | |
---|---|---|
Sex | ||
Women | 93 | 49.73 |
Men | 94 | 50.27 |
Ratio | 1F/1H | |
Age groups | ||
childreen (<18 years old) | 20 | 10.69 |
Adults (18-70 years old) | 158 | 84.49 |
Senior adults (˃70 years old) | 9 | 4.81 |
Mean age | 41.68±17.95 | |
Median age | 46 |
As shown in Table 2, a total of 141 patients, or 75.40%, had at least one intestinal parasitic infection. Forty-seven patients (24.13%) had multiple infestations, of which 37 (19.79%) combined at least one helminth and one protozoan, and 10 (5.35%) combined at least two protozoa. The most frequent combination was Entamoeba histolytica and Ascaris lumbricoides, with 27 cases (14.44%). Intestinal parasitic infections were more frequent among children (95.00%) and elderly adults (88.89%). They were also more common in women (78.49%) than in men (72.34%). A total of 114 patients (60.96%) had at least one intestinal protozoan, and 66 patients (35.29%) had an intestinal helminth infection.
Figure 2 shows that Entamoeba histolytica was the most frequent protozoan, with 103 cases (55.08%), followed by Schistosoma M., Ankylostoma D., and Enterobius V. with respective prevalence rates of 3.74%, 1.60%, and 1.07%.
As shown in Figure 3, Ascaris lumbricoides was the most frequent helminth, with 52 cases (27.81%), followed by Schistosoma mansoni, with 7 cases (3.74%), Ancylostoma duodenale, with 3 cases (1.60%), and Enterobius vermicularis, with 2 cases (1.07%).
Figure 4 shows the evolution of frequency of intestinal parasitoses by year (2020 and 2021). It allows to analyse this evolution in the relation with the season(dry season: from 15/5 to 15/8 and rainy season: from 1/1 to 14/5 and from 16/8 to 31/12).
In 2020, the frequency of intestinal parasitic infections was high, with peak values during the dry season (83-100% in May, June, and July) and in October. In 2021, the frequency also remained high, particularly with peak values observed during the dry season (87-90% in May and June) and in September.
Table 3 shows that the frequency of intestinal parasitic infections was higher during the dry season (83.33%) compared to the rainy season (72.66%). When considered by year, the frequency was higher during the dry season (87.50%) than during the rainy season (62.69%) in 2020, whereas in 2021, the rainy season recorded a slightly higher frequency than the dry season, with 81.94% and 79.17%, respectively. But the chi-square test showed that there was no association between intestinal parasitic infections and the season.
Figure 5 shows that the frequency of intestinal protozoa was high in both 2020 and 2021. In 2020, two peaks of this frequency were observed during the dry season (100% in May and July). In 2021, two high values of this frequency, 80% and 85%, were observed in May and September, respectively.
As shown in Table 4 the dry season recorded a higher frequency of intestinal protozoa (64.58%) compared to the rainy season (59.71%). This superiority remained stable in both 2020 and 2021. There is no association between the frequency of intestinal protozoa and the season. The frequencies of Entamoeba H., Trichomonas I., and Giardia L. are not associated with the season.
The frequency of intestinal helminthiasis was higher in 2021 than in 2020. In 2020, three high frequencies were recorded during the dry season (66% and 40% in May and July) and in October (74%). In 2021, three other high frequencies (72%, 56%, and 60%) were recorded in February, June, and October, respectively (Figure 6).
The frequency of intestinal helminthiasis (37.50%) was higher during the dry season than during the rainy season (34.53%). In 2020, the dry season recorded a frequency of 25.00%, higher than that of the rainy season (17.91%). In 2021, both seasons recorded the same frequency (50.00%).
There is no association between the frequency of intestinal helminthiasis and the season. The frequencies of Ascaris L., Schistosoma M., Ankylostoma D., and Enterobius V. are not associated with the season (Table 5).
In this study, we estimated the prevalence of intestinal parasitoses in general, as well as the prevalence of different types of intestinal parasitoses, among patients who underwent direct stool examination at CHUNDE in 2020 and 2021. These patients were aged between 2 years and 77 years, with an odds ratio of one woman for every man. The strength of this study lies in providing prevalence data for different types of intestinal parasitoses in Kasai Oriental, where such data had not been published until now.
1. Prevalence of intestinal parasitoses: The overall prevalence of intestinal parasitoses was 75.40%. The prevalence of intestinal protozoa and helminths was 60.69% and 35.29%, respectively. The most prevalent intestinal protozoa were Entamoeba histolytica (55.08%), followed by Trichomonas intestinalis (9.09%) and Giardia lamblia (6.24%). The most prevalent intestinal helminths were Ascaris lumbricoides (27.81%), followed by Schistosoma mansoni (3.74%), Ankylostoma duodenale (1.60%), and Enterobius vermicularis (1.07%). Worldwide, a study in Brazil estimated the prevalence at 10.8% (95% CI: 8.6–13.4). Endolimax nana was the most frequent parasite (4.8%), followed by Entamoeba histolytica/dispar (1.7%). In Africa, the prevalence of intestinal parasitoses remains high in many studies. Studies in Algeria and Morocco on sub-Saharan migrants showed high frequencies of intestinal parasitoses but lower than ours, with prevalences of 34.45% (protozoa 78.75%, helminths 21.25%) and 43.18%, respectively.7,13,14
In Tunisia, F. Cheikhrouhou et al. (2009) in a retrospective study from 1997 to 2006 in the Sfax region found an overall prevalence of intestinal parasitoses of 26.6%, one-third of which were children. Protozoa accounted for 96.5% of isolated parasites, with flagellates (54.3%) dominated by Dientamoeba fragilis (30.3%) and Giardia lamblia (17%). Amoebas represented 41.9%, with E. histolytica/E. dispar making up 2.2%. Helminths (3.5%) included Enterobius vermicularis (49%), Hymenolepis nana (31.4%), Strongyloides stercoralis (0.3%), Taenia saginata (0.3%), and Ankylostoma duodenale (one case).15
In the DRC, Serge Nimo Ngbabo (2008) found a global prevalence of intestinal parasitoses at C.S. Boyoma in Kisangani of 62%. In his study, Ankylostoma was the most frequently encountered parasite (32.4%), followed by Entamoeba histolytica (18.4%), Ascaris lumbricoides (10.7%), Strongyloides stercoralis (8.2%), Trichuris trichiura (7.5%), Trichomonas intestinalis (1.1%), and Enterobius vermicularis (0.2%).6
In all these studies, the prevalence of intestinal parasitoses remains high, with intestinal protozoa being more frequent than helminths. We note some differences, which we attribute to the fact that these studies were conducted in different regions with varying hygienic conditions. Specifically, studies in Tunisia provide percentages of intestinal helminths and protozoa relative to the total number of people affected by intestinal parasitoses, while our study shows the actual prevalence of each specific parasite type within the total population studied.
2. Polyparasitism: 45 patients (24.13%) were infested by multiple intestinal parasites simultaneously, with 19.79% combining at least one helminth and one protozoan. The most frequent combination was Entamoeba histolytica and Ascaris lumbricoides, with 27 cases (14.44%). Other studies have noted cases of polyparasitism. A study conducted in Benin between 2005 and 2013 by Sissinto et al. showed a polyparasitism rate of 17.4% (3.09% of the total study population). The most common associations were Blastocystis hominis + Entamoeba histolytica/dispar (20.1%), Entamoeba coli + Entamoeba histolytica/dispar (17.2%), and Blastocystis hominis + Endolimax nana (11.7%). In Morocco, Zouitni reported a polyparasitism rate of 63.15% (27.2% of their study population). In the DRC, Woolf K. et al. reported a polyparasitism prevalence of 23.41%. We note similarities between our polyparasitism rate and those found in the last two studies mentioned.7,10,16
3. Age and gender prevalence: Intestinal parasitoses were more frequent among children (95.00%) and elderly adults (88.89%). They were also more frequent among women (78.49%) than men (72.34%). In their study among children under 5 years old in Kivu, DRC, Woolf K. et al. recorded a prevalence of intestinal parasitoses of 94%, very close to the rate recorded in our study for children. In Tunisia, F. Cheikhrouhou et al. showed a predominance of intestinal parasitoses among children under 12 years (50.2% of cases). A study in Bangui by Lango Y. et al. showed a higher prevalence of intestinal parasitoses in women (35.10%) compared to men (32.89%).3,10,15,17
4. Seasonal variation: Intestinal parasitoses were more prevalent during the dry season than during the rainy season. However, there was no statistically significant association between season and the prevalence of intestinal parasitoses in general, nor with intestinal helminthiasis or protozoan infections. In the DRC, a study conducted in Sake (Kivu) among 504 children under 5 years old showed no association between season and the prevalence of intestinal parasitoses.10 This result underscores the need to study the behaviors adopted by the population during different seasons to identify factors that directly affect the prevalence of parasitoses. As highlighted in the introduction, this region is known for its poor hygiene conditions, with frequent shortages of drinking water and poor waste management, especially for fecal matter.
• Conception and implementation: All authors
• Financial support: All authors
• Administrative support: Lufuluabu M. Alphonse and Tshishimbi Jean Hubert
• Provision of study material or patients: All authors
• Data collection and assembly: Lufuluabu M. Alphonse and Tshodi B. Arsène
• Data analysis and interpretation: All authors
• Manuscript writing: All authors
• Final manuscript approval: All authors
• Responsible for all aspects of the work: All authors
The authors are employees of the University of Mbujimayi, all in training at its medical faculty and assigned to its University Hospital Center Notre-Dame de l’Espérance.
This study received approval from the ethics committee of the University of Mbujimayi on N52/CEUM1209 of 11th December 2019. It was conducted in accordance with the requirements of good clinical practices and the principles of the Helsinki Declaration of the World Medical Association, along with any subsequent relevant amendments. All patients who have participated in this study have provided their written informed consent by signing a written document, the consent form.
• Intestinal parasitoses are a major global public health problem.
• Intestinal amebiasis, in particular, should be considered part of the Neglected Tropical Diseases (NTDs).
• In relation to SDG 6, there is a need to raise awareness and educate the population on hygiene.
• Funding longitudinal data collection is necessary to better understand the factors influencing the prevalence of intestinal parasitoses across seasons.
Figshare: Impact of the season and prevalence of intestinal parasitosis at the Notre Dame de l’Espérance University Hospital Center. [Dataset]. figshare. 2023. https://doi.org/10.6084/m9.figshare.28050665.v1.18
This study contains the following underlying data: Data.xls (anonymised results of microscopic examination of stools, yes=positive, no=negative, na=not attributable, p=rainy season, s=dry season, pro=protozoa, hel=helminth, adu=adult, enf=child, vieu=elder, eh=entamoeba, h giar=giardia, tric=trichomonas, al=ascaris l, sm=schistosoma mansoni, ank=ankylostoma, ox=entérobius v).
Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).
We would like to thank the University of Mbujimayi for allowing us to conduct our study at its University Hospital Center Notre-Dame de l’Espérance.
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Is the work clearly and accurately presented and does it cite the current literature?
Partly
Is the study design appropriate and is the work technically sound?
No
Are sufficient details of methods and analysis provided to allow replication by others?
No
If applicable, is the statistical analysis and its interpretation appropriate?
I cannot comment. A qualified statistician is required.
Are all the source data underlying the results available to ensure full reproducibility?
Partly
Are the conclusions drawn adequately supported by the results?
Partly
Competing Interests: No competing interests were disclosed.
Reviewer Expertise: Neglected Tropical Diseases, Parasitology, Infectious Diseases Epidemiology, Laboratory Medicine
Is the work clearly and accurately presented and does it cite the current literature?
Partly
Is the study design appropriate and is the work technically sound?
No
Are sufficient details of methods and analysis provided to allow replication by others?
No
If applicable, is the statistical analysis and its interpretation appropriate?
Partly
Are all the source data underlying the results available to ensure full reproducibility?
Partly
Are the conclusions drawn adequately supported by the results?
Partly
References
1. Al-Refai M, Wakid M: Prevalence of intestinal parasites and comparison of detection techniques for soil-transmitted helminths among newly arrived expatriate labors in Jeddah, Saudi Arabia. PeerJ. 2024; 12. Publisher Full TextCompeting Interests: No competing interests were disclosed.
Reviewer Expertise: Professor and Consultant in Diagnostic Medical Parasitology.
Is the work clearly and accurately presented and does it cite the current literature?
Partly
Is the study design appropriate and is the work technically sound?
Partly
Are sufficient details of methods and analysis provided to allow replication by others?
Partly
If applicable, is the statistical analysis and its interpretation appropriate?
Partly
Are all the source data underlying the results available to ensure full reproducibility?
Yes
Are the conclusions drawn adequately supported by the results?
Partly
Competing Interests: No competing interests were disclosed.
Reviewer Expertise: Microbiology
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