1. Introduction
Giardia lamblia (G. lamblia) is the most common protozoan to infect the small intestine in humans, especially children [1]. Giardiasis is a major cause of enteric infections globally, with a prevalence of 10% to 50% of the population in developing countries [2,3]. It is estimated that approximately 280 million people worldwide have symptomatic giardiasis and around 500,000 new cases are reported annually [4]. G. lamblia is the only species that infects humans and other mammals [5], and it is classified into seven different genotypes/assemblages (A to G), each specific to a particular host. Assemblages A and B have been identified in humans, cattle, and various other mammals [6].
Giardia lamblia has two life cycle stages: trophozoite and cyst (Figure 1). Once ingested, the cysts undergo excystation in the proximal small intestine, which releases trophozoites. These trophozoites then attach to the walls of the small intestine and rapidly multiply, leading to clinical illness in humans [7]. Giardia cysts are the parasite’s environmentally stable stage and can survive for up to two months without being inactivated by common water disinfectants [6]. Contaminated food and water are the primary means of Giardia transmission. Other contributing factors include poor living conditions, overcrowded housing, inadequate environmental sanitation, and unclean personal hygiene practices.
G. lamblia can cause a range of clinical symptoms, from asymptomatic to acute or chronic diarrhea with malabsorption syndrome and weight loss [8]. Giardiasis often presents with diarrhea, lethargy, greasy feces, gas, abdominal cramping, bloating, and weight loss [9]. G. lamblia also significantly contributes to recurrent abdominal pain in children [10]. In addition, the prevalence of intestinal parasites, including Giardia, is influenced by various socioeconomic factors such as poverty, inadequate sanitation and water treatment systems, illiteracy, poor hygienic practices, and proximity to domestic and wild animals. These factors increase the risk of Giardia infection in different communities [11,12].
Few studies have investigated the prevalence and risk factors associated with Giardia infection in Pakistan in the past 20 years, with most studies focusing solely on children [7,13]. Reports indicate that between 9% and 10% of Pakistan’s population has G. lamblia, with malnourished children under 10 years of age particularly affected [14].
Although numerous studies have been conducted on the prevalence and distribution of giardiasis in Pakistan, there are still regions where epidemiological data are lacking, including Khyber Pakhtunkhwa. This study represents the first attempt to estimate the frequency of G. lamblia infection and identify contributing factors in this region. The study aims to determine the prevalence of G. lamblia infection in a healthy pediatric population across several Agro-ecological Zones (AEZs) of Khyber Pakhtunkhwa, Pakistan, and to identify any potential individual and community-level risk factors.
2. Materials and Methods
2.1. Sampling Technique and Sample Size Calculation
From March to December 2022, a cross-sectional study was conducted in the Khyber Pakhtunkhwa Province of Pakistan to determine the risk factors associated with giardiasis in children under five at both the individual and community levels. The province encompasses nine AEZs, including High Dry Mountains, Sub-Mountain Valleys, Sub-Humid Mountains, Wet Mountains, Valley Plains, Piedmont Plains, Semi-Arid Piedmont, Western Mountains, and Desert Plains. Each zone was treated as a stratum, and the stratified sampling technique was employed to select the study participants to collect an equal number of samples from each AEZ and ensure they were representative of their respective AEZs. Based on the previously reported prevalence of 8.0% [15], the sample size for each AEZ (stratum) was calculated to be 114, resulting in a total sample size of 1026 for all nine AEZs.
2.2. Stool Sample Collection and Giardia Detection
Random households were selected for both stool and data collection. If a household had more than one eligible child (under the age of five), one child was chosen using a lottery method. A total of 1026 stool samples were collected from the selected children and transported in an icebox to the Preventive Medicine and Public Health Laboratory at Abdul Wali Khan University Mardan for further processing. Giardia was detected in the stool samples using a commercial ELISA kit (IBL International GmbH, Hamburg, Germany) following the manufacturer’s instructions. Negative and positive controls were added to the first and second wells, respectively, while 50 μL of each sample was added to the remaining wells. Dilution buffer was then added to each sample well, and the mixture was incubated for 60 min at a temperature of 15–25 °C. After incubation, the wells were washed seven times with wash buffer, and enzyme conjugate was added to each well (including control wells) and incubated for 30 min at 15–25 °C. The wells were then washed seven times with wash buffer again. Chromogen was added to each well and incubated for 10 min at 15–25 °C, followed by the addition of a stop solution. Finally, an ELISA reader was used to take the reading.
2.3. Questionnaire and Observation Checklist for Assessing Giardiasis Risk Factors
In this study, we employed a comprehensive questionnaire and observation checklist to assess the risk factors associated with giardiasis at both the individual and community levels [Supplementary File S1]. The observation checklist was designed to gather data on various environmental factors, including domestic water storage vessels, the presence of rubbish heaps near homes, the condition of streets or pathways, latrine facilities, and the presence of companion animals. Simultaneously, the questionnaire focused on evaluating individual-level risk factors. It encompassed a range of factors, such as child gender, age, family size, mother’s and father’s educational level, attendance at daycare or kindergarten, handwashing behavior, and the potential entry of stray dogs and cats into the home. To ensure accuracy and reliability, face-to-face interviews were conducted with guardians or primary caregivers to gather data on these specific risk factors. Furthermore, community-level risk factors were also assessed as part of our investigation. These included the AEZs in the study area, drinking water sources, the usage of boiled or filtered drinking water, domestic water storage vessels, the presence of rubbish heaps near homes, the condition of streets or pathways, and the availability and quality of latrine facilities. By using this comprehensive questionnaire and observation checklist, we aimed to gather a detailed understanding of the risk factors associated with giardiasis at both the individual and community levels. This approach allowed us to capture a broad range of variables and factors that could potentially contribute to the prevalence of giardiasis in the studied population.
2.4. Data Processing and Statistical Analysis
The statistical software STATA version 16 was utilized to analyze the data with a significance level of 5% and a 95% confidence interval. Logistic regression models, including classical and multilevel methods, were employed to identify risk factors for giardiasis at the individual and community levels. The impact of potential risk factors on giardiasis occurrence was measured using multivariable logistic regression that considered individual and community-level factors. Four models were generated in this study to identify giardiasis risk factors in the study area. An initial model without any explanatory variables was employed to assess the variance of the outcome variable and served as a baseline for subsequent models. The model I and II were adjusted to include individual and community-level factors, respectively. The final full model included both individual and community-level factors. The relationship between the outcome variable (giardiasis) and explanatory variables (individual and community-level risk factors) was expressed using the adjusted odds ratio (AOR), and the significance level was set at p < 0.05 (two-tailed).
3. Results
3.1. Giardiasis Prevalences According to Individual-Level Factors in Children under Five
The research was conducted on 1026 stool samples collected from children under five to determine Giardia’s presence. Results showed that out of the samples tested, 34 tested positive, indicating a prevalence rate of 3.31%. The study also revealed that diarrhea was higher in male children (3.7%) than in female children. Moreover, the prevalence rate was 8% among children aged between 13 to 24 months and 3.4% among children from families with more than six members. The study further showed that the prevalence rate of giardiasis was 4.4% among children of illiterate mothers and 8.1% among children of illiterate fathers. Additionally, children who attended daycare institutions or kindergartens had an 8.8% prevalence rate of the disease. The study also found that 6.88% of giardiasis cases were reported among mothers who did not wash their hands during critical times, while 4.83% were observed among children from families with companion animals (Table 1).
3.2. Giardiasis Prevalences According to Community-Level Factors in Children under Five
The prevalence of giardiasis varies among regions, with the highest rates found in sub-mountain valleys (6.14%), high dry mountains (4.39%), and valley plains (4.39%). Lower rates were observed in sub-humid mountains (3.51%), wet mountains (3.51%), semi-arid piedmont (2.63%), western mountains (2.63%), piedmont plains (1.75%), and desert plains (0.88%). Among children who use un-piped water, 7.22% tested positive for giardiasis, while 3.47% of those who used un-boiled or unfiltered water had the infection. Children with inadequate domestic water storage vessels had a 9.27% prevalence of giardiasis, and those with a rubbish heap near their house had a prevalence estimated at 8.94%. Children with unpaved streets/pathways to their houses and those whose mothers used unimproved latrine facilities had a higher prevalence of giardiasis, at 4.08% and 8.41%, respectively (Table 2).
3.3. Significant Factors Associated with Giardiasis in Children under Five
The results of the multivariable analyses indicated that children aged 13–24 months had a 3.92 times higher risk of giardiasis (AOR 3.92; 95% CI 1.82–7.71) compared to those aged 49–60 months. Moreover, children of illiterate mothers had a 2.22 times higher risk of giardiasis (AOR 2.22; 95% CI 1.11–4.52) than those whose mothers had higher education. Similarly, children of illiterate fathers had a 4.82 times higher risk (AOR 4.82; 95% CI 2.33–9.61) than those whose fathers had higher education. Children who attended daycare institutions/kindergartens had a 3.12 times higher risk of giardiasis (AOR 3.12; 95% CI 1.61–6.42) than those who did not. Moreover, children whose mothers did not practice hand washing during critical times had a 3.61 times higher risk of giardiasis (AOR 3.61; 95% CI 1.91–6.94) compared to those whose mothers did practice hand washing. The risk of giardiasis was 5.72 times higher (AOR 5.72; 95% CI 2.81–11.78) among children with companion animals compared to those without. However, the risk was 4.62 times higher (AOR 4.62; 95% CI 2.23–8.92) among children in homes where stray dogs/cats entered compared to those where they did not. Lastly, residents of Sub-mountain valleys had a 7.23 times higher risk of giardiasis (AOR 7.23, 95% CI 3.51–13.74) than those in the Desert plains. According to a study, children from families that use un-piped water are 3.30 times more likely to contract giardiasis than those who use piped water. Furthermore, the likelihood of children getting giardiasis increases by 6.5 times when their families have inadequate domestic water storage vessels. Children who consume un-boiled or unfiltered water are 2.88 times more likely to contract giardiasis than those who drink boiled or filtered water. Living near rubbish heaps increases the risk of getting giardiasis by 5.2 times, while living near unpaved streets or pathways increases the risk by 2.19 times. Finally, families with unimproved Latrine facilities are 4.53 times more likely to have children with giardiasis than those with improved Latrine facilities (Table 3 and Table 4).
4. Discussion
G. lamblia is a common pathogenic protozoan that infects the small intestine and is a leading cause of death among children in developing countries [16]. The severity of G. lamblia infections is more prevalent in children than adults due to malnutrition, growth retardation, and inadequate care [17]. Poor personal hygiene, unhygienic toilet practices, consumption of unwashed fruits and vegetables, and the consumption of contaminated water and food contribute to the high morbidity rates among school children [18]. The study aims to determine the frequency of G. lamblia infection in children in various regions of Khyber Pakhtunkhwa, Pakistan. The research also explores potential individual and community-level risk factors associated with Giardia infection. The study employed direct microscopic examination or an immunochromatographic test (ICT) for epidemiological investigation, with ICT being more cost-effective. However, the ICT test’s low sensitivity could produce misleading information about the disease’s prevalence.
The results of our study indicate that the prevalence of G. lamblia infection among students in selected elementary schools is 3.31%. Other studies conducted in Pakistan have reported higher rates of G. lamblia infection, including 12.5% in the Khanewal district [13] and 6.5% in Faisalabad [13]. In Peshawar, the prevalence rate was even higher at 30.5% [19]. In comparison, Afghan refugees had a significantly higher prevalence rate of 37.7% [20], while Guatemala had the highest prevalence rate of 43.8% [21]. These variations in the prevalence rates of G. lamblia infection can be attributed to the socioeconomic differences between countries. For example, industrialized countries typically report lower prevalence rates of 2–7%, while developing countries have rates that can reach up to 40% [4].
The study found several risk factors associated with a higher risk of giardiasis infection at the individual level. The results indicated that children aged between 13–24 months were at a higher risk of contracting giardiasis (95% CI for AOR 3.92; 1.82–7.71). This finding is consistent with earlier studies [13,22,23]. The increased risk for young children could be due to their lack of acquired immunity and their higher exposure to the source of infection, which is often linked to inadequate personal hygiene and crowded living conditions. Furthermore, the study revealed that children attending daycare institutions or kindergartens (95% CI for AOR 3.12; 1.61–6.42) were also at a higher risk of giardiasis infection due to their poor hygiene habits and exposure to contaminated conditions. Daycare centers are places where children are highly vulnerable to parasites through interpersonal contact and unsanitary conditions. This finding is in line with earlier studies [13,24,25,26]. Overall, these findings suggest that young children and those attending daycare institutions/kindergartens are more susceptible to giardiasis infections due to their inadequate personal hygiene practices and exposure to contaminated environments.
The current study found no significant difference between males and females in terms of infection rate. Both genders had similar infection rates, with males at 3.7% and females at 3.1%. This finding is consistent with previous research [23,27,28]. The prevalence of intestinal parasites in children can be attributed to several factors, including food quality, water supply, personal and community hygiene, climate, sanitation conditions, proximity to domestic and wild animals, and socioeconomic status [29].
Our study found that parents’ educational level is a risk factor for giardiasis. Specifically, our results showed that children with illiterate mothers (95% CI for AOR 2.22; 1.11–4.52) and illiterate fathers (95% CI for AOR 4.82; 2.33–9.61) were more likely to be infected with G. lamblia. This finding is consistent with previous studies conducted in different regions of Pakistan [13,30], Malaysia [31], Tehran [32], and Mexico [24]. Moreover, other research has shown that a father’s educational level is also linked to a higher risk of G. lamblia infection, possibly due to its association with lower socioeconomic status and inadequate hygiene and sanitation practices [33]. Therefore, it is important to consider the influence of parents’ educational level and socioeconomic status when implementing prevention and control strategies for giardiasis.
Effective personal hygiene practices, such as handwashing, are crucial in preventing fecal-oral infections, including those caused by protozoa. Giardia cysts, for instance, can survive in the environment for an extended period, making handwashing a critical intervention to limit transmission via caregivers’ hands and contaminated food-common routes of infection [34]. The current study’s results support handwashing’s effectiveness in reducing the risk of giardiasis. Specifically, the study found that mothers who did not wash their hands during critical times had a higher risk of giardiasis (95% CI for AOR 3.61; 1.91–6.94). These findings are consistent with the study by [35], which reported a significant reduction in Giardia prevalence and infection intensity through handwashing promotion.
Our study revealed that owning companion animals (adjusted odds ratio [AOR] 5.72; 95% confidence interval [CI] 2.81–11.78) and living in homes with stray dogs/cats (AOR 4.62; 95% CI 2.23–8.92) were associated with a high incidence of giardiasis and were identified as risk factors for G. lamblia infection. It is widely recognized that G. lamblia is an intestinal parasite that primarily affects domestic animals, such as livestock, dogs, and cats, and has been isolated in varying prevalence from livestock and companion animals worldwide. For instance, dairy calves have been found to have the highest frequency of G. lamblia infection [36,37,38,39,40], while pigs [41], sheep [42], goats [43], elks and deer [44], dogs [45], and other ruminants [46] have also been found to carry the parasite.
The current study identified several risk factors at the community level. Our findings indicate that the prevalence of G. lamblia is significantly higher among children who consume un-piped water (95% CI for AOR 3.30; 1.5–6.8), use inadequate domestic water storage vessels (95% CI for AOR 6.5; 3.06–12.88), or drink un-boiled or unfiltered water (95% CI for AOR 2.88; 1.46–6.12). Contaminated drinking water is a well-known cause of many bacterial and parasitic diseases. Giardia and Cryptosporidium are recognized as the most common causes of waterborne outbreaks globally [47]. Our results are consistent with those of previous studies [13,48,49]. However, according to other studies [33,50], the risk of infection increases four-fold if untreated water is used.
Our research revealed that individuals living in houses without functioning toilets had higher chances of contracting Giardia infections (95% confidence interval [CI] for adjusted odds ratio [AOR] 4.53; 2.24–9.35). This finding is consistent with multiple earlier studies [48,49,51] that have emphasized the role of environmental contamination and transmission of giardiasis through the fecal-oral route. To combat this issue, interventions to improve sanitation and hygiene are essential. Previous studies have shown that latrine access, latrine use, and treating household drinking water can help reduce the odds of G. lamblia infection [52]. Furthermore, our research found that defecating in open areas like rivers and bushes was common in communities with inadequate toilet facilities [31]. Additionally, our study identified living in Sub-mountain valleys (95% CI for AOR 7.23; 3.51–13.74), residing near rubbish heaps (95% CI for AOR 5.52; 2.61–10.43), or living close to unpaved streets or pathways (95% CI for AOR 2.19; 1.04–4.41) as risk factors for giardiasis.
Notably, a study conducted in India reported the presence of Giardia cysts in 5% of vegetable samples [53]. Similarly, in Ethiopia, the prevalence of Giardia contamination was found in 6.9% of vegetable samples collected from local markets [54]. In Egypt, Giardia was found in 8.8% of vegetable samples [55]. Moreover, studies have demonstrated the viability of Giardia on lettuce leaves, thereby accentuating the augmented risk of contamination for consumers. Extensive research has focused on the transmission of Giardia through fecal-contaminated drinking water [56,57,58,59,60,61,62,63]. These findings underscore the heightened risk of Giardia transmission through practices such as irrigating vegetables with wastewater and fertilizing vegetable farms with manure [64,65,66]. These studies emphasize the potential for the transmission of Giardia to occur through these pathways, further highlighting the importance of addressing contamination risks in agricultural settings.
5. Conclusions
In conclusion, the prevalence of intestinal parasite infections in school-aged children due to their lower socioeconomic status is a significant public health concern, and our study conducted in Khyber Pakhtunkhwa, Pakistan, confirms this trend. Our findings demonstrate that various risk factors, such as cramped living conditions, consumption of tap water, unimproved latrine facilities, and low parental education and status, contribute significantly to the frequency of giardiasis. To combat this issue, integrated intervention strategies must target giardiasis prevention at both individual and community levels in Khyber Pakhtunkhwa, Pakistan. Therefore, it is essential to combine individual-level treatments, such as promoting hand washing and raising awareness about giardiasis prevention techniques, with interventions that encourage behavioral change and provide clean and appropriate water sources. Moreover, inter-sectoral cooperation between the health sector and other sectors is necessary to reduce the incidence of giardiasis in resource-poor communities effectively. Implementing these strategies will ensure a healthier future for school-aged children in Khyber Pakhtunkhwa and other regions with similar public health concerns.
Conceptualization, I.K. and N.N.; methodology, I.K., G.R. and K.K.; software, W.-L.Y., A.K. and M.B.S.; validation, C.-C.C., N.N. and G.R.; formal analysis, C.-C.C., A.K. and M.B.S.; investigation, N.N., T.U. and S.A.; resources, I.K., T.U. and S.A.; data curation, A.K. and C.-C.C.; writing—original draft preparation, I.K., W.-L.Y. and M.B.S.; writing—review and editing, I.K., W.-L.Y., N.N., K.K., M.B.S. and C.-C.C.; visualization, C.-C.C.; supervision, A.K. and C.-C.C.; project administration, A.K. and C.-C.C.; funding acquisition, C.-C.C. All authors have read and agreed to the published version of the manuscript.
All methods followed relevant guidelines and regulations. The Ethical Research Committee of the Abdul Wali Khan University, Madran, Pakistan approved all the experimental procedures and protocols in this study.
Written consent for interviews was obtained from all participants. All participants were provided with written information about the research and informed that their participation was voluntary and that they could withdraw from participation at any time.
The datasets generated and/or analyzed during the current study are not publicly available due to data transcripts, including personal participant information, not suitable for sharing but could be available from the corresponding authors at reasonable request.
The authors extend their appreciation to the Researchers Supporting Project number (RSPD2023R690), King Saud University, Riyadh, Saudi Arabia, for funding this research.
The authors declare no conflict of interest.
Footnotes
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Enlarge this image.Figure 1. The life cycle of Giardia lamblia. Infective cysts are typically spread through contaminated food or water, direct ingestion, or both. Following ingestion, these cysts excyst in the human small intestine, releasing pathogenic trophozoites. The breakdown of the intestinal epithelium is induced by the trophozoites, which aid in the pathophysiology of the illness. Both cysts and trophozoites can be identified in the feces, but the discharged trophozoites have a brief existence.
Prevalence and individual-level risk factors of giardiasis in Khyber Pakhtunkhwa, Pakistan.
| Individual-Level Risk Factors | Classes | Total | Positive (% ± C.I. 1) |
|---|---|---|---|
| Gender | Male | 428 | 16 (3.74 ± 1.80) |
| Female | 598 | 18 (3.01 ± 1.37) | |
| Age group | 0–6 | 79 | 1 (1.27 ± 2.47) |
| 7–12 | 86 | 1 (1.16 ± 2.27) | |
| 13–24 | 125 | 10 (8.0 ± 4.76) | |
| 25–36 | 288 | 10 (3.47 ± 2.11) | |
| 37–48 | 211 | 7 (3.32 ± 2.42) | |
| 49–60 | 237 | 5 (2.11 ± 1.83) | |
| Family size | <6 | 293 | 8 (2.73 ± 1.87) |
| ≥6 | 753 | 26 (3.45 ± 1.30) | |
| Mother’s educational level | Cannot read and write | 457 | 20 (4.38 ± 1.88) |
| Primary | 300 | 9 (3.0 ± 1.93) | |
| Secondary | 169 | 3 (1.78 ± 1.99) | |
| Higher education | 100 | 2 (2.0 ± 2.74) | |
| Father’s educational level | Cannot read and write | 99 | 8 (8.08 ± 5.37) |
| Primary | 210 | 11 (5.24 ± 3.01) | |
| Secondary | 414 | 10 (2.42 ± 1.48) | |
| Higher education | 303 | 5 (1.65 ± 1.43) | |
| Attend daycare | Yes | 125 | 11 (8.8 ± 4.97) |
| institution/Kindergarten | No | 901 | 23 (2.55 ± 1.03) |
| Handwashing behavior of | Washes at critical times | 750 | 15 (2.0 ± 0.1) |
| mothers | Does not wash at critical times | 276 | 19 (6.88 ± 2.99) |
| Companion animal | Yes | 642 | 31 (4.83 ± 1.66) |
| No | 384 | 3 (0.78 ± 0.88) | |
| Stray dogs/cats enter home | Yes | 275 | 21 (7.64 ± 3.14) |
| No | 751 | 13 (1.73 ± 0.93) |
Abbreviations: 1 C.I.: 95% confidence interval.
Prevalence and community-level risk factors of giardiasis in Khyber Pakhtunkhwa, Pakistan.
| Community-Level Factors | Classes | Total | Positive (% ± C.I. 1) |
|---|---|---|---|
| Agro-ecological zones | High dry mountains | 114 | 5 (4.39 ± 3.76) |
| Sub mountain valleys | 114 | 7 (6.14 ± 4.41) | |
| Sub humid mountains | 114 | 4 (3.51 ± 3.38) | |
| Wet mountains | 114 | 4 (3.51 ± 3.38) | |
| Valley plains | 114 | 5 (4.39 ± 3.76) | |
| Piedmont plain | 114 | 2 (1.75 ± 2.41) | |
| Semi-arid piedmont | 114 | 3 (2.63 ± 2.94) | |
| Western mountains | 114 | 3 (2.63 ± 2.94) | |
| Desert plains | 114 | 1 (0.88 ± 1.71) | |
| Drinking water sources | Piped | 846 | 21 (2.48 ± 1.05) |
| Un-piped | 180 | 13 (7.22 ± 3.78) | |
| Drinking water boiled or filtered | Yes | 75 | 1 (1.33 ± 2.60) |
| No | 951 | 33 (3.47 ± 1.16 | |
| Domestic water storage vessel | Adequate | 767 | 10 (1.30 ± 1.16) |
| Inadequate | 259 | 24 (9.27 ± 3.53) | |
| Presence of rubbish heap near the | Not present | 780 | 12 (1.54 ± 0.86) |
| house | Present | 246 | 22 (8.94 ± 3.57) |
| Condition of street or pathway | Paved | 711 | 13 (1.83 ± 0.98) |
| Unpaved | 515 | 21 (4.08 ± 1.71) | |
| Latrine facilities | Improved | 800 | 15 (1.88 ± 0.94) |
| Unimproved | 226 | 19 (8.41 ± 3.62) |
Abbreviations: 1 C.I.: 95% confidence interval.
Identified individual level risk factors of giardiasis in Khyber Pakhtunkhwa, Pakistan.
| Empty Model Factors | Classes | Models | ||
|---|---|---|---|---|
| Model I | Model II | Full Model | ||
| AOR (95 ± C.I.) | AOR (95 ± C.I.) | AOR (95 ± C.I.) | ||
| Age group | 0–6 | 0.60 (0.29–1.4) | - | 0.8 (0.29–1.4) * |
| (months) | 7–12 | 0.55 (0.26–1.3) | - | 0.61 (0.26–1.3) |
| 13–24 | 3.81 (1.82–7.71) | - | 3.92 (1.82–7.71) | |
| 25–36 | 1.65 (0.81–3.41) | - | 1.81 (0.81–3.41) | |
| 37–48 | 1.58 (0.81–3.22) | - | 1.62 (0.81–3.22) | |
| 49–60 | 1.00 | - | 1.00 | |
| Family size | <6 | 1.00 | - | 1.00 |
| ≥6 | 1.19 (0.584–2.41) | - | 1.0 (0.51–1.91) | |
| Mother’s | Cannot read and write | 2.19 (0.98–4.41) | - | 2.22 (1.11–4.52) * |
| educational | Primary | 1.50 (0.81–3.12) | - | 1.38 (0.66–3.18) |
| level | Secondary | 0.89 (0.56–1.82) | - | 0.89 (0.56–1.82) |
| Higher education | 1.00 | - | 1.00 | |
| Father’s | Cannot read and write | 4.75 (2.21–9.58) | - | 4.82 (2.33–9.61) * |
| educational | Primary | 3.08 (1.67–6.07) | - | 3.23 (1.69–6.14) |
| level | Secondary | 1.42 (0.65–2.92) | - | 1.38 (0.59–3.1) |
| Higher education | 1.00 | - | 1.00 | |
| Attend daycare | Yes | 3.38 (1.72–6.65) | - | 3.12 (1.61–6.42) * |
| institution/Kindergarten | No | 1.00 | - | 1.00 |
| Handwashing behavior | Washes at critical times | 1.00 | - | 1.00 |
| Does not wash at critical times | 3.44 (1.72–6.82) | - | 3.61 (1.91–6.94) * | |
| Companion animal | Yes | 6.04 (2.96–12.12) | - | 5.72 (2.81–11.78) * |
| No | 1.00 | - | 1.00 | |
| Stray dogs/cats | Yes | 4.49 (2.10–8.84) | - | 4.62 (2.23–8.92) * |
| enter home | No | 1.00 | - | 1.00 |
* Significant at p value < 0.05, C.I.; Confidence interval, AOR; Adjusted odds ratio.
Identified community-level risk factors of giardiasis in Khyber Pakhtunkhwa, Pakistan.
| Empty Model Factors | Classes | Models | ||
|---|---|---|---|---|
| Model I | Model II | Full Model | ||
| AOR (95 ± C.I.) | AOR (95 ± C.I.) | AOR (95 ± C.I.) | ||
| Agro-ecological zones | High dry mountains | - | 4.90 (2.43–9.81) | 5.11 (2.46–9.92) * |
| Sub mountain valleys | - | 6.97 (3.47–13.63) | 7.23 (3.51–13.74) | |
| Sub humid mountains | - | 4.12 (2.12–8.57) | 3.91 (2.03–8.41) | |
| Wet mountains | - | 4.12 (2.12–8.57) | 3.91 (2.03–8.41) | |
| Valley plains | - | 4.90 (2.43–9.81) | 5.11 (2.46–9.92) | |
| Piedmont plain | - | 2.13 (1.03–4.28) | 1.92 (0.98–4.02) | |
| Semi-arid piedmont | - | 2.94 (1.31–5.87) | 3.14 (1.37–5.99) | |
| Western mountains | - | 2.94 (1.31–5.87) | 3.14 (1.37–5.99) | |
| Desert plains | - | 1.00 | 1.00 | |
| Drinking water sources | Piped | - | 1.00 | 1.00 |
| Un-piped | - | 2.91 (1.42–5.98) | 3.30 (1.5–6.8) * | |
| Domestic water | Adequate | - | 1.00 | 1.00 |
| storage vessel | Inadequate | - | 7.13 (3.12–13.15) | 6.5 (3.06–12.88) * |
| Drinking water boiled | Yes | - | 1.00 | 1.00 |
| or filtered | No | - | 2.61 (1.21–5.41) | 2.88 (1.46–6.12) * |
| Presence of rubbish | Not present | - | 1.00 | 1.00 |
| heap near the house | Present | - | 5.81 (2.78–10.94) | 5.52 (2.61–10.43) * |
| Condition of street | Paved | - | 1.00 | 1.00 |
| or pathway | Unpaved | - | 2.23 (1.09–4.51) | 2.19 (1.04–4.41) * |
| Latrine facilities | Improved | - | 1.00 | 1.00 |
| Unimproved | - | 4.47 (2.18–9.21) | 4.53 (2.24–9.35) * | |
* Significant at p value < 0.05, C.I.; Confidence interval, AOR; Adjusted odds ratio.
Supplementary Materials
The following supporting information can be downloaded at:
References
1. Ali, S.A.; Hill, D.R. Giardia intestinalis. Curr. Opin. Infect. Dis.; 2003; 16, pp. 453-460. [DOI: https://dx.doi.org/10.1097/00001432-200310000-00012] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/14501998]
2. Savioli, L.; Smith, H.; Thompson, A. Giardia and Cryptosporidium join the ‘neglected diseases initiative’. Trends Parasitol.; 2006; 22, pp. 203-208. [DOI: https://dx.doi.org/10.1016/j.pt.2006.02.015] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16545611]
3. Daly, E.R.; Roy, S.J.; Blaney, D.D.; Manning, J.S.; Hill, V.R.; Xiao, L.; Stull, J.W. Outbreak of giardiasis associated with a community drinking-water source. Epidemiol. Infect.; 2010; 138, pp. 491-500. [DOI: https://dx.doi.org/10.1017/S0950268809990744]
4. Upcroft, P.; Upcroft, J.A. Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin. Microbiol. Rev.; 2001; 14, pp. 150-164. [DOI: https://dx.doi.org/10.1128/CMR.14.1.150-164.2001] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11148007]
5. Adam, R.D. Biology of Giardia lamblia. Clin. Microbiol. Rev.; 2001; 14, pp. 447-475. [DOI: https://dx.doi.org/10.1128/CMR.14.3.447-475.2001] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11432808]
6. Thompson, R.C. Giardiasis as a re-emerging infectious disease and its zoonotic potential. Int. J. Parasitol.; 2000; 30, pp. 1259-1267. [DOI: https://dx.doi.org/10.1016/S0020-7519(00)00127-2]
7. Tariq, M.T. Prevalence of Giardiasis in Afghan population. Pak. Pediatr. J.; 2013; 37, pp. 180-184.
8. Ensink, J.H.; van der Hoek, W.; Amerasinghe, F.P. Giardia duodenalis infection and wastewater irrigation in Pakistan. Trans. R. Soc. Trop. Med. Hyg.; 2006; 100, pp. 538-542. [DOI: https://dx.doi.org/10.1016/j.trstmh.2005.08.014]
9. Thompson, R.A. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol.; 2004; 126, pp. 15-35. [DOI: https://dx.doi.org/10.1016/j.vetpar.2004.09.008]
10. Buch, N.A.; Ahmad, S.M.; Ahmed, S.Z.; Ali, S.W.; Charoo, B.A.; Hassan, M.U. Recurrent abdominal pain in children. Indian Pediatr.; 2002; 39, pp. 830-834.
11. Faustini, A.; Marinacci, C.; Fabrizi, E.; Marangi, M.; Recchia, O.; Pica, R.; Giustini, F.; La Marca, A.; Nacci, A.; Panichi, G. et al. The impact of the Catholic Jubilee in 2000 on infectious diseases. A case-control study of giardiasis, Rome, Italy 2000–2001. Epidemiol Infect.; 2005; 134, pp. 649-658. [DOI: https://dx.doi.org/10.1017/S0950268805005327] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16255833]
12. Anuar, T.S.; Al-Mekhlafi, H.M.; Ghani, M.K.; Osman, E.; Yasin, A.M.; Nordin, A.; Azreen, S.N.; Salleh, F.M.; Ghazali, N.; Bernadus, M. et al. Giardiasis among different tribes of Orang Asli in Malaysia: Highlighting the presence of other family members infected with Giardia intestinalis as a main risk factor. Int. J. Parasitol.; 2012; 42, pp. 871-880. [DOI: https://dx.doi.org/10.1016/j.ijpara.2012.07.003] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22846786]
13. Naz, A.; Nawaz, Z.; Rasool, M.H.; Zahoor, M.A. Cross-sectional epidemiological investigations of Giardia lamblia in children in Pakistan. Sao Paulo Med. J.; 2018; 136, pp. 449-453.
14. Al-Mekhlafi, M.H.; Azlin, M.; Nor Aini, U.; Shaik, A.; Sa’iah, A.; Fatmah, M.S.; Ismail, M.G.; Ahmad Firdaus, M.S.; Aisah, M.Y.; Rozlida, A.R. et al. Giardiasis as a predictor of childhood malnutrition in Orang Asli children in Malaysia. Trans. R. Soc. Trop. Med. Hyg.; 2005; 99, pp. 686-691. [DOI: https://dx.doi.org/10.1016/j.trstmh.2005.02.006] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15992838]
15. Afridi, M.F.; Farhat, K.; Ali, S.; Qaisrani, M.N.; Ahmed, Z. Prevalence of intestinal parasitic infestations in relation to wasting among children under 5 years of age in Skardu, Pakistan: A cross sectional observational study. Isra Med. J.; 2021; 13, pp. 130-133.
16. Hailegebriel, T. Prevalence of intestinal parasitic infections and associated risk factors among students at Dona Berber primary school, Bahir Dar, Ethiopia. BMC Infect. Dis.; 2017; 17, 362. [DOI: https://dx.doi.org/10.1186/s12879-017-2466-x]
17. Hajare, S.T.; Chekol, Y.; Chauhan, N.M. Assessment of prevalence of Giardia lamblia infection and its associated factors among government elementary school children from Sidama zone, SNNPR, Ethiopia. PLoS ONE; 2022; 17, e0264812. [DOI: https://dx.doi.org/10.1371/journal.pone.0264812]
18. Haftu, D.; Deyessa, N.; Agedew, E. Prevalence and determinant factors of intestinal parasites among school children in Arba Minch town, Southern Ethiopia. Am. J. Health Res.; 2014; 2, pp. 247-254. [DOI: https://dx.doi.org/10.11648/j.ajhr.20140205.15]
19. Younas, M.; Shah, S.; Talaat, A. Frequency of Giardia lamblia infection in children with recurrent abdominal pain. J. Pak. Med. Assoc.; 2008; 58, 171.
20. Haq, K.U.; Gul, N.A.; Hammad, H.M.; Bibi, Y.; Bibi, A.; Mohsan, J. Prevalence of Giardia intestinalis and Hymenolepis nana in Afghan refugee population of Mianwali district, Pakistan. Afr. Health Sci.; 2015; 15, pp. 394-400. [DOI: https://dx.doi.org/10.4314/ahs.v15i2.12]
21. Duffy, T.L.; Montenegro-Bethancourt, G.; Solomons, N.W.; Belosevic, M.; Clandinin, M.T. Prevalence of giardiasis in children attending semi-urban daycare centres in Guatemala and comparison of 3 Giardia detection tests. J. Health Popul. Nutr.; 2013; 31, 290. [DOI: https://dx.doi.org/10.3329/jhpn.v31i2.16394] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23930348]
22. Kramar, L.V.; Reznikov, E.V.; Kramar, O.G. Prevalence if giardiasis in Volgograd city population. Meditsinskaia Parazitol. I Parazit. Bolezn.; 2003; 4, pp. 38-39.
23. Anim-Baidoo, I.; Narh, C.A.; Oddei, D.; Brown, C.A.; Enweronu-Laryea, C.; Bandoh, B.; Sampane-Donkor, E.; Armah, G.; Adjei, A.A.; Adjei, D.N. et al. Giardia lamblia infections in children in Ghana. Pan Afr. Med. J.; 2016; 24, 217. [DOI: https://dx.doi.org/10.11604/pamj.2016.24.217.8012] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27800072]
24. Quihui, L.; Valencia, M.E.; Crompton, D.W.; Phillips, S.; Hagan, P.; Morales, G.; Díaz-Camacho, S.P. 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, pp. 1-8. [DOI: https://dx.doi.org/10.1186/1471-2458-6-225]
25. Östan, İ.; Kilimcioğlu, A.A.; Girginkardeşler, N.; Özyurt, B.C.; Limoncu, M.E.; Ok, Ü.Z. Health inequities: Lower socio-economic conditions and higher incidences of intestinal parasites. BMC Public Health; 2007; 7, pp. 1-8. [DOI: https://dx.doi.org/10.1186/1471-2458-7-342]
26. Santos, C.K.; Grama, D.F.; Limongi, J.E.; Costa, F.C.; Couto, T.R.; Soares, R.M.; Mundim, M.J.; Cury, M.C. Epidemiological, parasitological and molecular aspects of Giardia duodenalis infection in children attending public daycare centers in southeastern Brazil. Trans. R. Soc. Trop. Med. Hyg.; 2012; 106, pp. 473-479. [DOI: https://dx.doi.org/10.1016/j.trstmh.2012.05.011]
27. Abbas, N.F.; El-Shaikh, K.A.; Almohammady, M.S. Prevalence of Giardia lamblia in diarrheic children in Almadinah Almunawarh, KSA. J. Taibah Univ. Sci.; 2011; 5, pp. 25-30. [DOI: https://dx.doi.org/10.1016/S1658-3655(12)60035-1]
28. Suman, M.S.; Alam, M.M.; Pun, S.B.; Khair, A.; Ahmed, S.; Uchida, R.Y. Prevalence of Giardia lamblia infection in children and calves in Bangladesh. Bangladesh J. Vet. Med.; 2011; 9, pp. 177-182. [DOI: https://dx.doi.org/10.3329/bjvm.v9i2.13474]
29. Reinthaler, F.F.; Feierl, G.; Stünzner, D.; Marth, E. Diarrhea in returning Austrian tourists: Epidemiology, etiology, and cost-analyses. J. Travel Med.; 1998; 5, pp. 65-72. [DOI: https://dx.doi.org/10.1111/j.1708-8305.1998.tb00466.x]
30. Chaudhry, Z.H.; Afzal, M.; Malik, M.A. Epidemiological factors affecting prevalence of intestinal parasites in children of Muzaffarabad district. Pak. J. Zool.; 2004; 36, pp. 267-271.
31. Choy, S.H.; Al-Mekhlafi, H.M.; Mahdy, M.A.; Nasr, N.N.; Sulaiman, M.; Lim, Y.A.; Surin, J. Prevalence and associated risk factors of Giardia infection among indigenous communities in rural Malaysia. Sci. Rep.; 2014; 4, 6909. [DOI: https://dx.doi.org/10.1038/srep06909] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25366301]
32. Nematian, J.; Nematian, E.; Gholamrezanezhad, A.; Asgari, A.A. Prevalence of intestinal parasitic infections and their relation with socio-economic factors and hygienic habits in Tehran primary school students. Acta Trop.; 2004; 92, pp. 179-186. [DOI: https://dx.doi.org/10.1016/j.actatropica.2004.06.010]
33. Júlio, C.; Vilares, A.; Oleastro, M.; Ferreira, I.; Gomes, S.; Monteiro, L.; Nunes, B.; Tenreiro, R.; Ângelo, H. Prevalence and risk factors for Giardia duodenalis infection among children: A case study in Portugal. Parasites Vectors; 2012; 5, pp. 22-28. [DOI: https://dx.doi.org/10.1186/1756-3305-5-22] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22284337]
34. Bartelt, L.A.; Sartor, R.B. Advances in understanding Giardia: Determinants and mechanisms of chronic sequelae. F1000prime Rep.; 2015; 7, 62. [DOI: https://dx.doi.org/10.12703/P7-62] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26097735]
35. Ashraf, S.; Nizame, F.A.; Islam, M.; Dutta, N.C.; Yeasmin, D.; Akhter, S.; Abedin, J.; Winch, P.J.; Ram, P.K.; Unicomb, L. et al. Nonrandomized trial of feasibility and acceptability of strategies for promotion of soapy water as a handwashing agent in rural Bangladesh. Am. J. Trop. Med. Hyg.; 2017; 96, 421. [DOI: https://dx.doi.org/10.4269/ajtmh.16-0304]
36. O’Handley, R.M.; Olson, M.E. Giardiasis and cryptosporidiosis in ruminants. Vet. Clin. Food Anim. Pract.; 2006; 22, pp. 623-643. [DOI: https://dx.doi.org/10.1016/j.cvfa.2006.07.002]
37. Geurden, T.; Berkvens, D.; Casaert, S.; Vercruysse, J.; Claerebout, E. A Bayesian evaluation of three diagnostic assays for the detection of Giardia duodenalis in symptomatic and asymptomatic dogs. Vet. Parasitol.; 2008; 157, pp. 14-20. [DOI: https://dx.doi.org/10.1016/j.vetpar.2008.07.002]
38. Lebbad, M.; Mattsson, J.G.; Christensson, B.; Ljungström, B.; Backhans, A.; Andersson, J.O.; Svärd, S.G. From mouse to moose: Multilocus genotyping of Giardia isolates from various animal species. Vet. Parasitol.; 2010; 168, pp. 231-239. [DOI: https://dx.doi.org/10.1016/j.vetpar.2009.11.003]
39. Mircean, V.; Györke, A.; Cozma, V. Prevalence and risk factors of Giardia duodenalis in dogs from Romania. Vet. Parasitol.; 2012; 184, pp. 325-329. [DOI: https://dx.doi.org/10.1016/j.vetpar.2011.08.022]
40. Minetti, C.; Taweenan, W.; Hogg, R.; Featherstone, C.; Randle, N.; Latham, S.M.; Wastling, J.M. Occurrence and diversity of Giardia duodenalis assemblages in livestock in the UK. Transbound. Emerg. Dis.; 2014; 61, pp. e60-e67. [DOI: https://dx.doi.org/10.1111/tbed.12075]
41. Armson, A.; Yang, R.; Thompson, J.; Johnson, J.; Reid, S.; Ryan, U.M. Giardia genotypes in pigs in Western Australia: Prevalence and association with diarrhea. Exp. Parasitol.; 2009; 121, pp. 381-383. [DOI: https://dx.doi.org/10.1016/j.exppara.2009.01.008] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19271283]
42. Yang, R.; Jacobson, C.; Gordon, C.; Ryan, U. Prevalence and molecular characterisation of Cryptosporidium and Giardia species in pre-weaned sheep in Australia. Vet. Parasitol.; 2009; 161, pp. 19-24. [DOI: https://dx.doi.org/10.1016/j.vetpar.2008.12.021] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19195787]
43. Bomfim, T.C.; Huber, F.; Gomes, R.S.; Alves, L.L. Natural infection by Giardia sp. and Cryptosporidium sp. in dairy goats, associated with possible risk factors of the studied properties. Vet. Parasitol.; 2005; 134, pp. 9-13. [DOI: https://dx.doi.org/10.1016/j.vetpar.2005.05.067] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16105719]
44. Paziewska, A.; Bednarska, M.; Nieweglowski, H.; Karbowiak, G.; Bajer, A. Distribution of Cryptosporidium and Giardia spp. in selected species of protected and game mammals from North-Eastern Poland. Ann. Agric. Environ. Med.; 2007; 14, pp. 265-270.
45. Feng, Y.; Xiao, L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin. Microbiol. Rev.; 2011; 24, pp. 110-140. [DOI: https://dx.doi.org/10.1128/CMR.00033-10]
46. O’handley, R.M.; Olson, M.E.; Fraser, D.; Adams, P.; Thompson, R.C. Prevalence and genotypic characterisation of Giardia in dairy calves from Western Australia and Western Canada. Vet. Parasitol.; 2000; 90, pp. 193-200. [DOI: https://dx.doi.org/10.1016/S0304-4017(00)00235-1] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10841999]
47. Baldursson, S.; Karanis, P. Waterborne transmission of protozoan parasites: Review of worldwide outbreaks—An update 2004–2010. Water Res.; 2011; 45, pp. 6603-6614. [DOI: https://dx.doi.org/10.1016/j.watres.2011.10.013]
48. Cifuentes, E.; Gomez, M.; Blumenthal, U.; Tellez-Rojo, M.M.; Romieu, I.S.; Ruiz-Palacios, G.; Ruiz-Velazco, S. Risk factors for Giardia intestinalis infection in agricultural villages practicing wastewater irrigation in Mexico. Am J. Trop. Med. Hyg.; 2000; 62, pp. 388-392. [DOI: https://dx.doi.org/10.4269/ajtmh.2000.62.388] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11037783]
49. Ngui, R.; Ishak, S.; Chuen, C.S.; Mahmud, R.; Lim, Y.A. Prevalence and risk factors of intestinal parasitism in rural and remote West Malaysia. PLoS Negl. Trop. Dis.; 2011; 5, e974. [DOI: https://dx.doi.org/10.1371/journal.pntd.0000974] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21390157]
50. Bello, J.; Núñez, F.A.; González, O.M.; Fernández, R.; Almirall, P.; Escobedo, A.A. Risk factors for Giardia infection among hospitalized children in Cuba. Ann. Trop. Med. Parasitol.; 2011; 105, pp. 57-64. [DOI: https://dx.doi.org/10.1179/136485911X12899838413385]
51. Ahmed, A.; Al-Mekhlafi, H.M.; Choy, S.H.; Ithoi, I.; Al-Adhroey, A.H.; Abdulsalam, A.M.; Surin, J. The burden of moderate-to-heavy soil-transmitted helminth infections among rural malaysian aborigines: An urgent need for an integrated control programme. Parasites Vectors; 2011; 4, 242. [DOI: https://dx.doi.org/10.1186/1756-3305-4-242] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22208559]
52. Speich, B.; Croll, D.; Fuerst, T.; Utzinger, J.; Keiser, J. Effect of sanitation and water treatment on intestinal protozoa infection: A systematic review and meta-analysis. Lancet Infect. Dis.; 2016; 16, pp. 87-99. [DOI: https://dx.doi.org/10.1016/S1473-3099(15)00349-7] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26404667]
53. Utaaker, K.S.; Kumar, A.; Joshi, H.; Chaudhary, S.; Robertson, L.J. Checking the detail in retail: Occurrence of Cryptosporidium and Giardia on vegetables sold across different counters in Chandigarh, India. Int. J. Food Microbiol.; 2017; 263, pp. 1-8. [DOI: https://dx.doi.org/10.1016/j.ijfoodmicro.2017.09.020]
54. Alemu, G.; Mama, M.; Misker, D.; Haftu, D. Parasitic contamination of vegetables marketed in Arba Minch town, southern Ethiopia. BMC Infect. Dis.; 2019; 19, 410. [DOI: https://dx.doi.org/10.1186/s12879-019-4020-5] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31088390]
55. Eraky, M.A.; Rashed, S.M.; Nasr Mel, S.; El-Hamshary, A.M.; Salah ElGhannam, A. Parasitic contamination of commonly consumed fresh leafy vegetables in benha, egypt. J. Parasitol. Res.; 2014; 2014, 613960. [DOI: https://dx.doi.org/10.1155/2014/613960] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25024845]
56. Swaffer, B.; Abbott, H.; King, B.; van der Linden, L.; Monis, P. Understanding human infectious Cryptosporidium risk in drinking water supply catchments. Water Res.; 2018; 138, pp. 282-292. [DOI: https://dx.doi.org/10.1016/j.watres.2018.03.063]
57. Benedict, K.M.; Reses, H.; Vigar, M.; Roth, D.M.; Roberts, V.A.; Mattioli, M.; Cooley, L.A.; Hilborn, E.D.; Wade, T.J.; Fullerton, K.E. et al. Surveillance for waterborne disease outbreaks associated with drinking water—United States, 2013–2014. MMWR Morb. Mortal. Wkly. Rep.; 2017; 66, pp. 1216-1221. [DOI: https://dx.doi.org/10.15585/mmwr.mm6644a3]
58. Alderisio, K.A.; Villegas, L.F.; Ware, M.W.; McDonald, L.A.; Xiao, L.; Villegas, E.N. Differences in staining intensities affect reported occurrences and concentrations of Giardia spp. in surface drinking water sources. J. Appl. Microbiol.; 2017; 123, pp. 1607-1613. [DOI: https://dx.doi.org/10.1111/jam.13585]
59. Dos Santos Toledo, R.; Martins, F.D.C.; Freire, R.L. Waterborne Giardia and Cryptosporidium: Contamination of human drinking water by sewage and cattle feces. Semina Ciências Agrárias; 2017; 38, pp. 3395-3415. [DOI: https://dx.doi.org/10.5433/1679-0359.2017v38n5p3395]
60. Efstratiou, A.; Ongerth, J.; Karanis, P. Evolution of monitoring for Giardia and Cryptosporidium in water. Water Res.; 2017; 123, pp. 96-112. [DOI: https://dx.doi.org/10.1016/j.watres.2017.06.042]
61. Gallas-Lindemann, C.; Sotiriadou, I.; Plutzer, J.; Karanis, P. Prevalence and distribution of Cryptosporidium and Giardia in wastewater and the surface, drinking and ground waters in the Lower Rhine, Germany. Epidemiol. Infect.; 2013; 141, pp. 9-21. [DOI: https://dx.doi.org/10.1017/S0950268812002026] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23010178]
62. Karanis, P.; Kourenti, C.; Smith, H. Waterborne transmission of protozoan parasites: A worldwide review of outbreaks and lessons learnt. J. Water Health; 2007; 5, pp. 1-38. [DOI: https://dx.doi.org/10.2166/wh.2006.002] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17402277]
63. Mahmoudi, M.R.; Ongerth, J.E.; Karanis, P. Cryptosporidium and cryptosporidiosis: The Asian perspective. Int. J. Hyg. Environ. Health; 2017; 220, pp. 1098-1109. [DOI: https://dx.doi.org/10.1016/j.ijheh.2017.07.005] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28760503]
64. Spanakos, G.; Biba, A.; Mavridou, A.; Karanis, P. Occurrence of Cryptosporidium and Giardia in recycled waters used for irrigation and first description of Cryptosporidium parvum and C. muris in Greece. Parasitol. Res.; 2015; 114, pp. 1803-1810. [DOI: https://dx.doi.org/10.1007/s00436-015-4366-6]
65. Domenech, E.; Amoros, I.; Moreno, Y.; Alonso, J.L. Cryptosporidium and Giardia safety margin increase in leafy green vegetables irrigated with treated wastewater. Int. J. Hyg. Environ. Health; 2018; 221, pp. 112-119. [DOI: https://dx.doi.org/10.1016/j.ijheh.2017.10.009]
66. Xiao, S.; Hu, S.; Zhang, Y.; Zhao, X.; Pan, W. Influence of sewage treatment plant effluent discharge into multipurpose river on its water quality: A quantitative health risk assessment of Cryptosporidium and Giardia. Environ. Pollut.; 2018; 233, pp. 797-805. [DOI: https://dx.doi.org/10.1016/j.envpol.2017.11.010]
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Details
; Khan, Khurshaid 3 ; Mourad Ben Said 6
; Chien-Chin, Chen 7
1 College of Veterinary and Animal Husbandry, Abdul Wali Khan University, Mardan 23200, Pakistan;
2 Department of Pediatrics, Ditmanson Medical Foundation Chia-Yi Christian Hospital, Chiayi 60002, Taiwan;
3 Department of Zoology, Abdul Wali Khan University, Mardan 23200, Pakistan;
4 Department of Zoology, Bacha Khan University, Charsadda 24540, Pakistan; Department of Biology, Mount Allison University, Sackville, NB E4L1E4, Canada
5 Department of Microbiology, Abdul Wali Khan University, Mardan 23200, Pakistan;
6 Laboratory of Microbiology, National School of Veterinary Medicine of Sidi Thabet, University of Manouba, Manouba 2010, Tunisia;
7 Department of Pathology, Ditmanson Medical Foundation Chia-Yi Christian Hospital, Chiayi 60002, Taiwan; Department of Cosmetic Science, Chia Nan University of Pharmacy and Science, Tainan 71710, Taiwan; Ph.D. Program in Translational Medicine, Rong Hsing Research Center for Translational Medicine, National Chung Hsing University, Taichung 40227, Taiwan; Department of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung University, Tainan 70101, Taiwan