Next Article in Journal
Assessment of Comorbidity in Patients with Drug-Resistant Tuberculosis
Next Article in Special Issue
Bacterial, Fungal, and Parasitic Zoonoses
Previous Article in Journal
Adherence to Anti-Malarial Treatment in Malaria Endemic Areas of Bangladesh
Previous Article in Special Issue
Cryptosporidium proventriculi in Captive Cockatiels (Nymphicus hollandicus)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 12
Issue 12
10.3390/pathogens12121393
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Evidence of the Zoonotic Transmission of Cryptosporidium among Children and Pets

by
Natalia Marinho Dourado Coelho
1,2,
Willian Marinho Dourado Coelho
2,
Jancarlo Ferreira Gomes
3,
Marcelo Vasconcelos Meireles
1,
Walter Bertequini Nagata
4,
Valéria Marçal Felix de Lima
1,
Thais Rabelo Santos-Doni
5,
Vitória Beatriz Silva
6,
Luiz da Silveira Neto
6,
Alex Akira Nakamura
1 and
Katia Denise Saraiva Bresciani
1,*
1
Faculdade de Medicina Veterinária, Universidade Estadual Paulista (Unesp), Araçatuba 16050-680, São Paulo, Brazil
2
Faculdade de Ciências Agrárias, Fundação Educacional de Andradina, Andradina 16901-160, São Paulo, Brazil
3
Faculdade de Ciências Médicas e Instituto de Computação, Universidade Estadual de Campinas (UNICAMP), Campinas 13083-887, São Paulo, Brazil
4
Escritório de Defesa Agropecuária, Coordenadoria de Defesa Agropecuária, Secretaria de Agricultura e Abastecimento do Estado de São Paulo, Lins 16400-050, São Paulo, Brazil
5
Instituto de Ciências Agrárias, Universidade Federal do Vale do Jequitinhonha e Mucuri (UFVJM), Unaí 38610-000, Minas Gerais, Brazil
6
Imunologia e Vacinologia, Curso de Engenharia de Bioprocessos e Biotecnologia, Universidade Federal do Tocantins (UFT), Gurupi 77410-530, Tocantins, Brazil
*
Author to whom correspondence should be addressed.
Pathogens 2023, 12(12), 1393; https://doi.org/10.3390/pathogens12121393
Submission received: 21 October 2023 / Revised: 20 November 2023 / Accepted: 23 November 2023 / Published: 27 November 2023
(This article belongs to the Special Issue Bacterial, Fungal and Parasitic Zoonoses)
Versions Notes

Abstract

:
We investigated the zoonotic transmission of Cryptosporidium among the children (n = 188), dogs (n = 133), and cats (n = 55) living in 188 households. Fecal samples were examined using ELISA and confirmed via nested PCR. Coproantigens oocysts were detected in 3.7% of children, 8.3% of dogs, and 5.5% of cats. We found strong evidence of two cases of the zoonotic transmission of Cryptosporidium canis between children and dogs. Furthermore, four children and their respective pets (one dog and three cats) were infected with Cryptosporidium parvum, but we cannot exclude the hypotheses that the oocysts were transmitted from children to animals or that both hosts were infected by a shared source, such as contaminated water or food. The presence of an infected animal elevated the risk of zoonotic transmission by 129.7-fold (95% CI: 13.92–1209.68). Furthermore, sharing a bed with pets was identified as a risk factor for infection in children (OR: 9.9, 95% CI: 1.37–71.2). In conclusion, the zoonotic transmission of Cryptosporidium among children and pets cohabiting in the same household may be quite common, especially when infected animals lie or sleep on children’s beds. These findings unequivocally highlight the public health concern surrounding C. canis.

1. Introduction

Cryptosporidium is a genus of protozoa known to cause gastroenteritis in both humans and animals. Infection typically occurs through the ingestion of oocysts found in the contaminated water and food sources in direct contact with infected individuals. The most prominent clinical symptom of cryptosporidiosis is diarrhea, which tends to be self-limiting in immunocompetent individuals but can become chronic and potentially life-threatening for immunosuppressed patients [1,2]. As a result, this pathogen garnered increased attention during the AIDS epidemic in the 1980s [3].
In regions such as Africa and Asia, Cryptosporidium is the second most important causative agent of diarrheic disease in children under 5 years and one of the major causes of mortality from infectious disease in toddlers aged 12–23 months in developing countries [4]. The primary symptoms observed in children include watery diarrhea, abdominal pain, fatigue, nausea, fever, vomiting, headache, and eye pain [5].
Currently, over 40 species and more than 120 genotypes of Cryptosporidium have been identified [6]. Cryptosporidium hominis and C. parvum are responsible for over 90% of human infections, while C. felis and C. canis, species typically associated with cats and dogs, have also been reported [7]. Conventional microscopy and immunodiagnostic assays cannot differentiate between Cryptosporidium oocysts due to their high morphological similarity and the presence of conserved antigens [8,9]. Therefore, the use of molecular characterization is crucial to provide new insights into the epidemiology of cryptosporidiosis, including the potential risk of transmission among humans and companion animals.
There are few reports on the zoonotic transmission of Cryptosporidium among children and dogs and cats in households [7,10,11,12], but it is unclear whether these pets play a minor role on the epidemiology of cryptosporidiosis or if this low occurrence is underestimated because it is still under-investigated. Hence, we investigated the zoonotic transmission of Cryptosporidium species among children and dogs and cats living in the same households, and analyzed the risk factors of infection.

2. Materials and Methods

2.1. Sampling

Stool samples were collected from 188 children, 133 dogs, and 55 cats residing in 188 households in the municipality of Andradina, São Paulo State, Brazil. The following inclusion criteria were applied for sample selection: each household contained only one child aged zero to 10 years and one dog or one cat, which was considered the sampling unit. Families with more than one child, children older than 10 years, or with more than one pet were excluded from the investigation.
Fecal samples were divided into three aliquots: 1 g was preserved in 10% formalin for direct ELISA, while two portions of 200 μg each were frozen at −20 °C in DNAse and RNAse-free microcentrifuge tubes for nested PCR (nPCR) analysis. Stool consistency was classified as diarrheic (liquid or pasty) or non-diarrheic (firm) according to the Bristol Stool Form Scale [13]. Additionally, parents completed a structured questionnaire to investigate potential risk factors.

2.2. Laboratory Techniques

All stool samples were tested for the presence of Cryptosporidium oocysts’ antigen using the Cryptosporidium II™ commercial kit (TechLab, Blacksburg, VA, USA) [14]. Briefly, 100 μL of diluent was added to each well of the microplate. Subsequently, 50 μL of each fecal sample preserved in 10% buffered formalin was transferred to individual wells. After incubation for one hour, the microplate was washed four times. Then, 50 μL of conjugated antibody was added to each well. Following a 30 min incubation, the plate was washed four times. A volume of 100 μL of substrate was added to each well. After a 10 min incubation, 50 μL per well of stop solution was added. Two minutes later, the reactions were read using an ELISA plate reader (Spectra Count, Packard Bio Science Company, Meriden, CT, USA) at 490 nm. Samples were considered positive if the optical density was ≥0.150 [15]. Only fecal samples from children that tested positive via the ELISA and from dogs or cats that had contact with an infected child in the same household were submitted to nPCR. Fecal samples from dogs or cats living with non-reactive children were not subjected to molecular analyses, because our objective was to investigate zoonotic transmission.
Genomic DNA was extracted from frozen fecal samples (−20 °C) from children, dogs, and cats, using the QIAamp® DNA Stool Mini Kit (Qiagen, Germantown, MD, USA). Subsequently, for the amplification of a fragment of the 18S rRNA gene, nPCR was performed with the primers 5′ TTC TAG AGC TAA TAC ATG CG 3′ and 5′ CCC ATT TCC TTC ACA GAA GGA 3′ for the primary reaction (amplicon size 1325 bp), and primers 5′ GGA AGG GTT GTA TTT ATT AGA TAA AG 3′ and 5′ AAG GAG TAA GGA ACA ACC TCC to 3′ for the secondary reaction (amplicon size 826–840 bp) [16]. All second-step PCR products were identified via electrophoresis on a 1.5% agarose gel, stained with GelRed® (Biotium, Fremont, CA, USA), and visualized with an ultraviolet light transilluminator. Ultrapure water was used as a negative control, and DNA from C. galli [EU543270] and C. parvum [GQ227477] served as positive controls for nPCR reactions.
Following the secondary PCR reaction, DNA fragments were purified using the QIAquick Gel Extraction kit (Qiagen) and sequenced using the ABI Prism Dye Terminator Cycling Sequencing kit (Applied Biosystems, Foster City, CA, USA) in an automated ABI 3730XL sequencer (Applied Biosystems, Foster City, CA, USA). Amplicons were sequenced in both directions using the nested primers. The consensus sequence was determined using Codoncode Aligner version 4.0.1 (CodonCode Corporation, Dedham, MA, USA). Consensus sequences were aligned to homologous sequences downloaded from Genbank using ClustalW [17] and the BioEdit sequence alignment editor [18].

2.3. Statistical Analyses

Statistical analyses were performed using the STATA/SE Software, Version 16.1 (Stata Corp LLC, College Station, TX, USA). The statistical significance level was set at ≤0.05.
For inferential statistics, the detection of Cryptosporidium coproantigens was considered the dependent variable, and the following variables were considered as explanatory or independent: age (children: ≤24, 25 > 59, ≥60 months of age; dog/cat: up to one year, two to seven years, over seven years), sex (male or female), consistency of feces (diarrheic or not diarrheic), animal (cat or dog), does your child wash their hands after playing with the pet? (yes or no), does the animal (dog and/or cat) usually lick the face and mouth of the child(ren)? (yes or no), do children play with sand at home or at school? (yes or no), does your child wash their hands after using the bathroom? (yes or no), do you have a water and sewage system? (yes or no), does the dog or cat usually lie down or sleep in bed with the child? (yes or no), where the child drinks water from (filtered or faucet), does the animal have street access? (yes or no), and is the animal dewormed? (yes or no).
Chi-square or Fisher’s exact tests were employed to assess the statistical significance of the association between the variables. To explore the independent risk factors for each explanatory variable, all variables demonstrating a p-value of ≤0.25 in univariate analysis were subjected to multivariate logistic regression [19]. Utilizing an initial screening p-value cut-off point of 0.25 is recommended, as the conventional probability of 0.05 might overlook variables that are known to be significant. The probability ratio (odds ratio, OR) and the corresponding 95% confidence intervals (95% CI) were calculated using both univariate and multiple logistic regression models [20].

3. Results

Cryptosporidium coproantigens were detected in 3.7% (7/188) of children, in 5.7% (3/55) of cats, and 8.3% (11/133) of dogs (Table 1). In children, cats, and dogs that exhibited the symptom of diarrhea, the prevalence rates were 16.3% (7/43), 27.3% (3/11), and 25.0% (8/32), respectively.
The results of the univariable and multivariable regression models exploring the risk factors in children are presented in Table 2. A multivariable logistic regression model of the predictors of Cryptosporidium was performed on all variables (the age group of 25 to 59 months, diarrhea, the lack of an installed water and sewage system in the household, and sleeping or lying with the animal) that showed a p value ≤ 0.25 in the univariate analysis.
Overall, the predictor that remained independently associated with Cryptosporidium in the multivariate logistic regression model was sleeping or lying with the animal (adjusted odds ratio [aOR]: 9.9, 95% CI: 1.37–71.2).
There was no association with other variables investigated. Regarding hygiene habits, most children did not wash their hands after using the toilet or playing with their animals and allowed animals to lick their mouth and face. Almost half of the children drank tap water and lived in homes without access to water and sewage systems.
The prevalence of Cryptosporidium in dogs was 8.3% (11/133; 95% CI: 3.6–13.0). Applying the multivariate logistic regression model, tests of the association between the Cryptosporidium infection in dogs and potential predictors showed that diarrhea was a significant (p < 0.001) independent predictor for the infection. Among the 11 positive animals, eight (72.7%) presented with diarrhea. Associations between the infection and the age range of 2 to 7 years (p = 0.208) and access to streets (p = 0.0037) were found in the univariate analysis (Table 3).
In cats, Cryptosporidium coproantigens were detected in 5.5% (3/55; 95% CI: 0–11.5) of samples. The infection appears to have contributed to the occurrence of diarrhea in the feline host (p = 0.006). No evidence of other infection risk factors in dogs and cats was found (Table 3).
Among the seven infected children, six (85.7%) lived with an animal that was also positive. Of the 11 infected dogs, only three (27.3%) lived with infected children. Samples from the eight dogs living with non-reactive children were not subjected to molecular analysis, because our objective was to investigate the zoonotic transmission of the parasite. C. parvum was identified in five children, one dog, and three cats, while two children and their respective dogs were infected with C. canis (Table 4). These species shared 100% similarity to MF589922 and EU754833, respectively.
In the present study, children living with a pet (cat or dog) were 129.75 times more likely to have a Cryptosporidium infection (Table 5).

4. Discussion

Our main objective was to investigate the zoonotic transmission and risk factors of Cryptosporidium between children under 10 years old and dogs/cats in the same household. Coproantigens’ oocysts detection and nPCR were used as the screening and confirmatory techniques, respectively. Molecular characterization was performed through the sequencing of amplified 18S rRNA gene fragments.
We found strong evidence of the zoonotic transmission of C. canis in two children and their dogs, given that dogs serve as the primary host for this protozoan species [21]. Furthermore, four children and their respective pets (one dog and three cats) were infected with C. parvum. This species includes over 20 gp60 subtype families. Typically, human infections are associated with zoonotic subtype families IIa and IId, whereas subtype IIc is exclusively linked to anthropogenic transmission [21]. Although the gp60 gene sequences were not analyzed in our study, it is improbable that the four children and their pets were infected with different gp60 subtype families simultaneously within the same household. However, we did not exclude the possibility that C. parvum oocysts were transmitted from children to animals, or that both hosts were infected through a shared source, such as contaminated water or food.
Although C. felis and C. canis are the fourth and fifth most common Cryptosporidium species in humans, few studies have investigated the infection of humans and pets living in the same household [21]. Zoonotic transmissions of C. canis and C. parvum between children and dogs have been reported in Peru [10] and Egypt [11], respectively. In adults, cats have served as a source of C. parvum infection in Chile [22], and C. felis in Sweden [23]. These two cases of zoonotic transmission with C. canis and C. felis have been recently confirmed by subtype analyses, with identical subtypes being found in both humans and their pets [24,25]. In these studies, the patients involved included children and immunocompetent adults, suggesting that these pet pathogens are threats to both immunocompromised and immunocompetent persons. Curiously, the C. felis species was not found in our study.
In the univariate analysis, the presence of Cryptosporidium coproantigens was associated with the occurrence of diarrhea in children (p < 0.001), but this relationship was not confirmed via the multivariate analysis, which suggests the influence of multiple risk factors. It is important to note that, in the major cases of the zoonotic transmission of Cryptosporidium confirmed within households, both interacting hosts were asymptomatic [11,22] or only the humans presented with diarrhea [10]. The clinical manifestation of cryptosporidiosis in humans and pets living together and at the same time is rare [23]. Of the seven children infected by the parasite, six (85.7%) did not wash their hands after using the bathroom, five (71.4%) did not have a water and sewage system installed in their residence, and three (42.9%) drank water from the tap. All of these variables can serve as confounding predictors for the occurrence of diarrhea, as they favor the occurrence of gastrointestinal disorders caused by other pathogens frequently transmitted by contaminated water and food, such as Blastocystis hominis [26,27], Giardia duodenalis [26,28,29], Escherichia coli enteropathogenic [29,30], Shigella spp. [30], Salmonella spp. [30], Yersinia spp. [30], Astrovirus [29], and Rotavírus [31].
Most published epidemiological surveys typically focus on examining fecal samples from a single host species within a household. Frequently, these studies do not investigate the occurrence of the parasite in other interacting host species, particularly when they are asymptomatic. Indeed, the source of infection is often attributed to contaminated water and food, because cryptosporidiosis is traditionally classified as a foodborne and waterborne disease [26,32,33,34,35,36,37,38]. This leads us to believe that the transmission of Cryptosporidium among humans and their pets is underestimated, because the earlier conclusion might hide the real problem: a zoonotic transmission.
Some investigations suggest that contact with animals increases the likelihood of Cryptosporidium infection in humans [39,40,41,42,43], but it remains controversial [26,32,33,44,45]. It is important to note that fecal samples from humans, dogs, and cats living in the same household are rarely analyzed in cross-sectional studies [40,45]. Typically, previous conclusions have been based on comparing the results obtained via diagnostic techniques to structured questionnaire data [26,32,39,43] and/or considered the presence of C. canis and C. felis as an indicator of low zoonotic transmission risk [34,46]. These extrapolations from earlier findings might have biased previous conclusions. This context highlights a crucial question: are children and pets in the same household sufficient to represent a risk factor? What is the chance of zoonotic transmission occurring when children cohabitate with an infected pet, and under what circumstances?
While children and pets cohabiting in the same household alone did not contribute significantly to Cryptosporidium infection (p = 0.419), the presence of an infected animal increased the risk of zoonotic transmission by 129.7 times (p < 0.00001). These results underscore the likelihood of zoonotic transmission. We believe that the animals might have carried the oocysts to the children’s beds, considering that this habit was the only risk factor confirmed via multivariate analysis.
It is important to highlight a similar study conducted in the province of Álava, Northern Spain, where 63 families with children, dogs, and cats living together provided individual fecal samples from each member of the household, including pets. Cryptosporidium spp. oocysts were found in a single household in which a cat and its owner were infected, but zoonotic transmission was not confirmed molecularly. Unfortunately, the risk factor analysis was limited due to the low number of positive samples [45]. Some methodological differences may explain the divergence in our results. All human fecal samples examined in our study were collected from children under 10 years of age, who are more susceptible to Cryptosporidium infection. Environmental, infrastructural, and behavioral factors can also influence the occurrence of the disease [47].
The occurrence of Cryptosporidium to the order of the 3.7% that was found in the fecal samples from children was expected for an upper middle-income country, where the prevalence varies from 5.0 to 16.2% [47]. However, the results found in this research are below those of most epidemiological surveys conducted in Brazil [26,28,29,32,33,35,36,37,38,44]. This divergence may be related to differences in the sampling methodologies and diagnostic techniques used in these studies.
In Brazil, most epidemiological surveys of Cryptosporidium in children use non-probability sampling methods, in addition to adopting acute/persistent diarrhea [27,38,44,48], children attending daycare centers [26,32,36], or communities with precarious basic sanitation [33,35], as inclusion criteria.
In dogs, Cryptosporidium oocyst antigens were detected in 8.3% of fecal samples, similar to other epidemiological surveys conducted in Brazil [49,50,51], where the occurrence of the parasite in this host ranged from below 3.0% [52,53,54,55] to above 25% [31,56,57]. Worldwide, the expected prevalence of Cryptosporidium in dogs is approximately 10% [58]. The presence of oocysts in feces contributed to the occurrence of diarrhea (p = 0.004), confirming the clinical importance of Cryptosporidium infection for the canine host.
In Brazil, the occurrence of Cryptosporidium in cats varies from 0.5% [59] to 30% [60]. The results of this study are in line with most epidemiological surveys in Brazil [31,57,61,62,63,64,65,66,67,68]. The clinical relevance of Cryptosporidium in the feline host remains uncertain [69,70]. We found an association between the presence of Cryptosporidium oocysts and the occurrence of diarrhea (p = 0.006), but the low number of positive samples reduced the reliability of the results of the uni- and multivariate analyses.
The sensitivity and specificity values of the diagnostic techniques used in this study were not calculated because the samples were not examined in a paired manner. Coproantigens’ oocyst detection and nPCR were employed as screening and confirmatory techniques, respectively. However, all positive results via direct ELISA were confirmed via nPCR, followed by genetic sequencing.
In conclusion, our research suggests that the zoonotic transmission of Cryptosporidium among children under 10 years old and the dogs and cats living in the same household may be quite common, especially when infected animals lie or sleep on children’s beds. These findings unequivocally highlight the public health concern surrounding C. canis. Under conducive circumstances, transmission from dogs to humans is possible. As a result, we recommend that children do not share their beds with pets, particularly under immunosuppression conditions.

Author Contributions

Conceptualization N.M.D.C., W.M.D.C., J.F.G., M.V.M. and K.D.S.B.; methodology, N.M.D.C., W.M.D.C., M.V.M. and K.D.S.B.; validation, N.M.D.C., W.M.D.C., M.V.M., V.M.F.d.L., J.F.G., A.A.N. and K.D.S.B.; formal analysis, N.M.D.C., W.B.N., M.V.M., V.M.F.d.L., K.D.S.B., L.d.S.N., A.A.N. and T.R.S.-D.; investigation, N.M.D.C., W.M.D.C., M.V.M., V.M.F.d.L. and K.D.S.B.; resources, N.M.D.C., M.V.M., V.M.F.d.L. and K.D.S.B.; data curation, N.M.D.C., W.B.N., M.V.M., V.M.F.d.L., L.d.S.N., V.B.S., T.R.S.-D. and K.D.S.B.; writing—original draft preparation, N.M.D.C., L.d.S.N., V.B.S., T.R.S.-D., A.A.N. and K.D.S.B.; writing—review and editing, L.d.S.N., T.R.S.-D., J.F.G., K.D.S.B., V.B.S. and K.D.S.B.; visualization, N.M.D.C., M.V.M., V.M.F.d.L., A.A.N. and K.D.S.B.; supervision, M.V.M., V.M.F.d.L. and K.D.S.B.; project administration, K.D.S.B.; funding acquisition K.D.S.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), grant number 2010525423.

Institutional Review Board Statement

This study was approved by the Ethics and Research Committee of the School of Dentistry-FOA/UNESP (protocol n. º 2670/08), and the Animal Use Ethics Committee (CEUA) of São Paulo State University (UNESP), School of Veterinary Medicine, Araçatuba (protocol n. º 2008-0007756).

Informed Consent Statement

Informed consent was obtained from all parents/owners involved in this study.

Data Availability Statement

The data presented in this study are available within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ryan, U.; Zahedi, A.; Paparini, A. Cryptosporidium in Humans and Animals—A One Health Approach to Prophylaxis. Parasite Immunol. 2016, 38, 535–547. [Google Scholar] [CrossRef] [PubMed]
  2. Dărăbuș, G.; Lupu, M.A.; Mederle, N.; Dărăbuș, R.G.; Imre, K.; Mederle, O.; Imre, M.; Paduraru, A.A.; Morariu, S.; Olariu, T.R. Epidemiology of Cryptosporidium Infection in Romania: A Review. Microorganisms 2023, 11, 1793. [Google Scholar] [CrossRef] [PubMed]
  3. Navin, T.R.; Juranek, D.D. Cryptosporidiosis: Clinical, Epidemiologic, and Parasitologic Review. Clin. Infect. Dis. 1984, 6, 313–327. [Google Scholar] [CrossRef]
  4. Kotloff, K.L.; Nataro, J.P.; Blackwelder, W.C.; Nasrin, D.; Farag, T.H.; Panchalingam, S.; Wu, Y.; Sow, S.O.; Sur, D.; Breiman, R.F.; et al. Burden and Aetiology of Diarrhoeal Disease in Infants and Young Children in Developing Countries (the Global Enteric Multicenter Study, GEMS): A Prospective, Case-Control Study. Lancet 2013, 382, 209–222. [Google Scholar] [CrossRef] [PubMed]
  5. Adler, S.; Widerström, M.; Lindh, J.; Lilja, M. Symptoms and Risk Factors of Cryptosporidium hominis Infection in Children: Data from a Large Waterborne Outbreak in Sweden. Parasitol. Res. 2017, 116, 2613–2618. [Google Scholar] [CrossRef] [PubMed]
  6. Ryan, U.M.; Feng, Y.; Fayer, R.; Xiao, L. Taxonomy and Molecular Epidemiology of Cryptosporidium and Giardia—A 50 Year Perspective (1971–2021). Int. J. Parasitol. 2021, 51, 1099–1119. [Google Scholar] [CrossRef] [PubMed]
  7. Feng, Y.; Ryan, U.M.; Xiao, L. Genetic Diversity and Population Structure of Cryptosporidium. Trends Parasitol. 2018, 34, 997–1011. [Google Scholar] [CrossRef] [PubMed]
  8. Chalmers, R.M.; Katzer, F. Looking for Cryptosporidium: The Application of Advances in Detection and Diagnosis. Trends Parasitol. 2013, 29, 237–251. [Google Scholar] [CrossRef]
  9. Xiao, L.; Fayer, R.; Ryan, U.M.; Upton, S.J. Cryptosporidium Taxonomy: Recent Advances and Implications for Public Health. Clin. Microbiol. Rev. 2004, 17, 72–97. [Google Scholar] [CrossRef]
  10. Xiao, L.; Cama, V.A.; Cabrera, L.; Ortega, Y.; Pearson, J.; Gilman, R.H. Possible Transmission of Cryptosporidium canis among Children and a Dog in a Household. J. Clin. Microbiol. 2007, 45, 2014–2016. [Google Scholar] [CrossRef]
  11. Gharieb, R.M.A.; Merwad, A.M.A.; Saleh, A.A.; Abd El-Ghany, A.M. Molecular Screening and Genotyping of Cryptosporidium Species in Household Dogs and In-Contact Children in Egypt: Risk Factor Analysis and Zoonotic Importance. Vector-Borne Zoonotic Dis. 2018, 18, 424–432. [Google Scholar] [CrossRef] [PubMed]
  12. Jiang, W.; Roellig, D.M.; Guo, Y.; Li, N.; Feng, Y.; Xiao, L. Development of a Subtyping Tool for Zoonotic Pathogen Cryptosporidium canis. J. Clin. Microbiol. 2021, 59, 1–8. [Google Scholar] [CrossRef] [PubMed]
  13. Martinez, A.P.; Azevedo, G.R.d. The Bristol Stool Form Scale: Its Translation to Portuguese, Cultural Adaptation and Validation. Rev. Lat. Am. Enfermagem 2012, 20, 583–589. [Google Scholar] [CrossRef]
  14. TechLab. Cryptosporidium II. Available online: https://www.techlab.com/wp-content/uploads/2023/08/CRYPTOSPORIDIUM-II-PI-91-406-02-TL_3_2023.pdf (accessed on 20 November 2023).
  15. Ali, F.M.; Ali, S.A.K. Cryptosporidiosis in Sulaimani Pediatric Teaching Hospital and Comparison of Different Diagnostic Methods for Its Detection. Eur. Sci. J. 2013, 9, 1857–7881. [Google Scholar]
  16. Xiao, L.; Escalante, L.; Yang, C.; Sulaiman, I.; Escalante, A.A.; Montali, R.J.; Fayer, R.; Lal, A.A. Phylogenetic Analysis of Cryptosporidium Parasites Based on the Small- Subunit RRNA Gene Locus. Appl. Environ. Microbiol. 1999, 65, 1578–1583. [Google Scholar] [CrossRef] [PubMed]
  17. Thompson, J. The CLUSTAL_X Windows Interface: Flexible Strategies for Multiple Sequence Alignment Aided by Quality Analysis Tools. Nucleic Acids Res. 1997, 25, 4876–4882. [Google Scholar] [CrossRef] [PubMed]
  18. Hall, T.A. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41, 95–98. [Google Scholar]
  19. Bendel, R.B.; Afifi, A.A. Comparison of Stopping Rules in Forward “Stepwise” Regression. J. Am. Stat. Assoc. 1977, 72, 46–53. [Google Scholar] [CrossRef]
  20. Panegossi, M.F.d.C.; Widmer, G.; Nagata, W.B.; Oliveira, B.C.M.; Ferrari, E.D.; Gomes, J.F.; Meireles, M.V.; Nakamura, A.A.; do Santos-Doni, T.R.; da Silveira Neto, L.; et al. Cryptosporidium proventriculi in Captive Cockatiels (Nymphicus hollandicus). Pathogens 2023, 12, 710. [Google Scholar] [CrossRef]
  21. Ryan, U.; Zahedi, A.; Feng, Y.; Xiao, L. An Update on Zoonotic Cryptosporidium Species and Genotypes in Humans. Animals 2021, 11, 3307. [Google Scholar] [CrossRef]
  22. Neira, P.; Muñoz, S.N.; Rosales, L.M.J. Infección Por Cryptosporidium parvum En Una Mujer Embarazada, Inmunocompetente, Con Riesgo Ocupacional. Rev. Chil. Infectología 2010, 27, 345–349. [Google Scholar] [CrossRef] [PubMed]
  23. Beser, J.; Toresson, L.; Eitrem, R.; Troell, K.; Winiecka-Krusnell, J.; Lebbad, M. Possible Zoonotic Transmission of Cryptosporidium felis in a Household. Infect. Ecol. Epidemiol. 2015, 5, 28463. [Google Scholar] [CrossRef] [PubMed]
  24. Yang, R.; Ying, J.L.J.; Monis, P.; Ryan, U. Molecular Characterisation of Cryptosporidium and Giardia in Cats (Felis catus) in Western Australia. Exp. Parasitol. 2015, 155, 13–18. [Google Scholar] [CrossRef] [PubMed]
  25. Rojas-Lopez, L.; Elwin, K.; Chalmers, R.M.; Enemark, H.L.; Beser, J.; Troell, K. Development of a Gp60-Subtyping Method for Cryptosporidium felis. Parasit. Vectors 2020, 13, 39. [Google Scholar] [CrossRef]
  26. de Carvalho, T.B.; de Carvalho, L.R.; Mascarini, L.M. Occurrence of Enteroparasites in Day Care Centers in Botucatu (São Paulo State, Brazil) with Emphasis on Cryptosporidium sp., Giardia duodenalis and Enterobius vermicularis. Rev. Inst. Med. Trop. Sao Paulo 2006, 48, 269–273. [Google Scholar] [CrossRef]
  27. Carvalho-Costa, F.A.; Gonçalves, A.Q.; Lassance, S.L.; Albuquerque, C.P.d.; Leite, J.P.G.; Bóia, M.N. Detection of Cryptosporidium spp. and Other Intestinal Parasites in Children with Acute Diarrhea and Severe Dehydration in Rio de Janeiro. Rev. Soc. Bras. Med. Trop. 2007, 40, 346–348. [Google Scholar] [CrossRef] [PubMed]
  28. Loureiro, E.C.B.; Linhares, A.C.; Mata, L. Criptosporidiose Em Crianças de 1 a 2 Anos de Idade, Com Diarréia Aguda Em Belém, Pará, Brasil. Mem. Inst. Oswaldo Cruz 1989, 84, 117–122. [Google Scholar] [CrossRef] [PubMed]
  29. Rossit, A.R.B.; de Almeida, M.T.G.; Nogueira, C.A.M.; da Costa Oliveira, J.G.; Barbosa, D.M.U.; Moscardini, A.C.; Mascarenhas, J.D.A.P.; Gabbay, Y.B.; Marques, F.R.; Cardoso, L.V.; et al. Bacterial, Yeast, Parasitic, and Viral Enteropathogens in HIV-Infected Children from São Paulo State, Southeastern Brazil. Diagn. Microbiol. Infect. Dis. 2007, 57, 59–66. [Google Scholar] [CrossRef]
  30. Medeiros, M.I.C.; Neme, S.N.; Silva, P.D.; Capuano, D.M.; Errera, M.C.; Fernandes, S.A.; Valle, G.R.D.; De Avila, F.A. Etiology of Acute Diarrhea among Children in Ribeirão Preto-SP, Brazil. Rev. Inst. Med. Trop. Sao Paulo 2001, 43, 21–24. [Google Scholar] [CrossRef]
  31. Santos, V.S.; Nóbrega, F.A.; Soares, M.W.S.; Moreira, R.D.; Cuevas, L.E.; Gurgel, R.Q. Rotavirus Genotypes Circulating in Brazil before and after the National Rotavirus Vaccine Program: A Review. Pediatr. Infect. Dis. J. 2018, 37, e63–e65. [Google Scholar] [CrossRef]
  32. Mascarini, L.M.; Donalísio, M.R. Giardiasis and Cryptosporidiosis in Children Institutionalized at Daycare Centers in the State of São Paulo. Rev. Soc. Bras. Med. Trop. 2006, 39, 577–579. [Google Scholar] [CrossRef] [PubMed]
  33. Newman, R.D.; Sears, C.L.; Moore, S.R.; Nataro, J.P.; Wuhib, T.; Agnew, D.A.; Guerrant, R.L.; Lima, A.A.M. Longitudinal Study of Cryptosporidium Infection in Children in Northeastern Brazil. J. Infect. Dis. 1999, 180, 167–175. [Google Scholar] [CrossRef] [PubMed]
  34. Pacheco, F.T.F.; Freitas, H.F.D.; Silva, R.K.N.R.; Carvalho, S.S.D.; Martins, A.S.; Menezes, J.F.; Ribeiro, T.C.M.; Mattos, Â.P.D.; Costa-Ribeiro Júnior, H.D.; Pedreira, J.N.R.; et al. Cryptosporidium Diagnosis in Different Groups of Children and Characterization of Parasite Species. Rev. Soc. Bras. Med. Trop. 2022, 55, e00412022. [Google Scholar] [CrossRef] [PubMed]
  35. Bushen, O.Y.; Kohli, A.; Pinkerton, R.C.; Dupnik, K.; Newman, R.D.; Sears, C.L.; Fayer, R.; Lima, A.A.M.; Guerrant, R.L. Heavy Cryptosporidial Infections in Children in Northeast Brazil: Comparison of Cryptosporidium hominis and Cryptosporidium parvum. Trans. R. Soc. Trop. Med. Hyg. 2007, 101, 378–384. [Google Scholar] [CrossRef] [PubMed]
  36. Carvalho-Almeida, T.T.; Pinto, P.L.S.; Quadros, C.M.S.; Torres, D.M.A.G.V.; Kanamura, H.Y.; Casimiro, A.M. Detection of Cryptosporidium sp. in Non Diarrheal Faeces from Children, in a Day Care Center in the City of São Paulo, Brazil. Rev. Inst. Med. Trop. Sao Paulo 2006, 48, 27–32. [Google Scholar] [CrossRef]
  37. Gennari-Cardoso, M.L.; Costa-Cruz, J.M.; De Castro, E.; Lima, L.M.F.S.; Prudente, D.V. Cryptosporidium sp. in Children Suffering from Acute Diarrhea at Uberlândia City, State of Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz 1996, 91, 551–554. [Google Scholar] [CrossRef] [PubMed]
  38. Mangini, A.C.S.; Dias, R.M.D.S.; Grisi, S.J.F.E.; Escobar, A.M.U.; Torres, D.M.A.G.V.; Zuba, I.P.R.; Quadros, C.M.S.; Chieffi, P.P. Parasitismo Por Cryptosporidium sp. Em Crianças Com Diarreia Aguda. Rev. Inst. Med. Trop. Sao Paulo 1992, 34, 341–345. [Google Scholar] [CrossRef]
  39. Oshiro, E.T.; Dorval, M.E.; Nunes, V.L.; Silva, M.A.; Said, L.A. Prevalência Do Cryptosporidium parvum Em Crianças Abaixo de 5 Anos, Residentes Na Zona Urbana de Campo Grande, MS, Brasil, 1996. Rev. Soc. Bras. Med. Trop. 2000, 33, 277–280. [Google Scholar] [CrossRef]
  40. Pereira, C.R.A.; Ferreira, A.P. Ocorrência e Fatores de Risco Da Criptosporidiose Em Felinos de Companhia de Idosos. Rev. Bras. Geriatr. Gerontol. 2012, 15, 681–691. [Google Scholar] [CrossRef]
  41. Bouzid, M.; Kintz, E.; Hunter, P.R. Risk Factors for Cryptosporidium Infection in Low and Middle Income Countries: A Systematic Review and Meta-Analysis. PLoS Negl. Trop. Dis. 2018, 12, e0006553. [Google Scholar] [CrossRef]
  42. Liu, A.; Gong, B.; Liu, X.; Shen, Y.; Wu, Y.; Zhang, W.; Cao, J. A Retrospective Epidemiological Analysis of Human Cryptosporidium Infection in China during the Past Three Decades (1987–2018). PLoS Negl. Trop. Dis. 2020, 14, e0008146. [Google Scholar] [CrossRef] [PubMed]
  43. Mohammad, S.M.; Ali, M.S.; Abdel-Rahman, S.A.; Moustafa, R.A.; Sarhan, M.H. Genotyping of Cryptosporidium Species in Children Suffering from Diarrhea in Sharkyia Governorate, Egypt. J. Infect. Dev. Ctries. 2021, 15, 1539–1546. [Google Scholar] [CrossRef] [PubMed]
  44. Pereira, M.D.G.C.; Atwill, E.R.; Barbosa, A.P.; Silva, S.A.E.; García-Zapata, M.T.A. Intra-Familial and Extra-Familial Risk Factors Associated with Cryptosporidium parvum Infection among Children Hospitalized for Diarrhea in Goiânia, Goiás, Brazil. Am. J. Trop. Med. Hyg. 2002, 66, 787–793. [Google Scholar] [CrossRef] [PubMed]
  45. de Lucio, A.; Bailo, B.; Aguilera, M.; Cardona, G.A.; Fernández-Crespo, J.C.; Carmena, D. No Molecular Epidemiological Evidence Supporting Household Transmission of Zoonotic Giardia duodenalis and Cryptosporidium spp. from Pet Dogs and Cats in the Province of Álava, Northern Spain. Acta Trop. 2017, 170, 48–56. [Google Scholar] [CrossRef] [PubMed]
  46. Lucio-Forster, A.; Griffiths, J.K.; Cama, V.A.; Xiao, L.; Bowman, D.D. Minimal Zoonotic Risk of Cryptosporidiosis from Pet Dogs and Cats. Trends Parasitol. 2010, 26, 174–179. [Google Scholar] [CrossRef] [PubMed]
  47. Dong, S.; Yang, Y.; Wang, Y.; Yang, D.; Yang, Y.; Shi, Y.; Li, C.; Li, L.; Chen, Y.; Jiang, Q.; et al. Prevalence of Cryptosporidium Infection in the Global Population: A Systematic Review and Meta-Analysis. Acta Parasitol. 2020, 65, 882–889. [Google Scholar] [CrossRef] [PubMed]
  48. Lima, A.A.M.; Fang, G.; Schorling, J.B.; Albuquerque, L.D.; Mcauliffe, J.F.; Mota, S.; Leite, R.; Guerrant, R.L. Persistent Diarrhea in Northeast Brazil; Etiologies and Interactions with Malnutrition. Acta Paediatr. 1992, 381, 39–44. [Google Scholar] [CrossRef]
  49. Lallo, M.A.; Bondan, E.F. Prevalência de Cryptosporidium Sp. Em Cães de Instituições Da Cidade de São Paulo. Rev. Saude Publica 2006, 40, 120–125. [Google Scholar] [CrossRef]
  50. Grecca, M.; Thomaz-Soccol, V.; Ribeiro, M.C.C.; Truppel, J.H.; Pereira, J.T.; Osaki, S.C. Occurrence of Cryptosporidium sp. in Dogs and Cats from Curitiba and Its Metropolitan Area. Arch. Vet. Sci. 2013, 18, 1–6. [Google Scholar] [CrossRef]
  51. de Oliveira, A.G.L.; Sudré, A.P.; Bomfim, T.C.B.; Santos, H.L.C. Molecular Characterization of Cryptosporidium spp. in Dogs and Cats in the City of Rio de Janeiro, Brazil, Reveals Potentially Zoonotic Species and Genotype. PLoS ONE 2021, 16, e0255087. [Google Scholar] [CrossRef]
  52. Huber, F.; Bomfim, T.C.B.; Gomes, R.S. Comparison between Natural Infection by Cryptosporidium sp., Giardia sp. in Dogs in Two Living Situations in the West Zone of the Municipality of Rio de Janeiro. Vet. Parasitol. 2005, 130, 69–72. [Google Scholar] [CrossRef] [PubMed]
  53. Mundim, M.J.S.; Rosa, L.A.G.; Hortêncio, S.M.; Faria, E.S.M.; Rodrigues, R.M.; Cury, M.C. Prevalence of Giardia duodenalis and Cryptosporidium spp. in Dogs from Different Living Conditions in Uberlândia, Brazil. Vet. Parasitol. 2007, 144, 356–359. [Google Scholar] [CrossRef] [PubMed]
  54. Bresciani, K.D.S.; Amarante, A.F.T.; Lima, V.M.F.; Marcondes, M.; Feitosa, F.L.F.; Táparo, C.V.; Serrano, A.C.M.; Ishizaki, M.N.; Tome, R.O.; Perri, S.H.V.; et al. Infecções Por Cryptosporidium spp. Em Cães de Araçatuba, Brasil. Veterinária Zootec. 2008, 15, 466–468. [Google Scholar]
  55. Lemus, S.d.N.; Mourão, L.P.B.; Ferrari, E.D.; Bresciani, K.D.S.; Silveira Neto, L.d.; Pimenta, R.S. Low Occurrence of Cryptosporidium canis in Feces of Dogs Seroreactive for Leishmania spp. Semin. Ciências Agrárias 2022, 43, 1823–1834. [Google Scholar] [CrossRef]
  56. Balassiano, B.C.C.; Campos, M.R.; Menezes, R.d.C.A.A.; Pereira, M.J.S. Factors Associated with Gastrointestinal Parasite Infection in Dogs in Rio de Janeiro, Brazil. Prev. Vet. Med. 2009, 91, 234–240. [Google Scholar] [CrossRef] [PubMed]
  57. Alves, M.E.M.; Martins, F.D.C.; Bräunig, P.; Pivoto, F.L.; Sangioni, L.A.; Vogel, F.S.F. Molecular Detection of Cryptosporidium spp. and the Occurrence of Intestinal Parasites in Fecal Samples of Naturally Infected Dogs and Cats. Parasitol. Res. 2018, 117, 3033–3038. [Google Scholar] [CrossRef] [PubMed]
  58. Taghipour, A.; Olfatifar, M.; Bahadory, S.; Godfrey, S.S.; Abdoli, A.; Khatami, A.; Javanmard, E.; Shahrivar, F. The Global Prevalence of Cryptosporidium Infection in Dogs: A Systematic Review and Meta-Analysis. Vet. Parasitol. 2020, 281, 109093. [Google Scholar] [CrossRef] [PubMed]
  59. Torrico, K.J.; Santos, N.J.R.d.; Abate, H.L.; Martins, F.D.C.; Barros, L.D.d.; Seixas, M.; Martins, T.A.; Garcia, J.L.; Vidotto, O. Occurrence of Gastrointestinal Protozoans in Cats from Londrina, Paraná, Brazil. Semin. Ciências Agrárias 2020, 41, 213. [Google Scholar] [CrossRef]
  60. Huber, F.; da Silva, S.; Bomfim, T.C.B.; Teixeira, K.R.S.; Bello, A.R. Genotypic Characterization and Phylogenetic Analysis of Cryptosporidium sp. from Domestic Animals in Brazil. Vet. Parasitol. 2007, 150, 65–74. [Google Scholar] [CrossRef]
  61. Coelho, W.M.D.; do Amarante, A.F.T.; de Soutello, R.V.G.; Meireles, M.V.; Bresciani, K.D.S. Ocorrência de Parasitos Gastrintestinais Em Amostras Fecais de Felinos No Município de Andradina, São Paulo. Rev. Bras. Parasitol. Vet. 2009, 18, 46–49. [Google Scholar] [CrossRef]
  62. da Silveira Neto, L.; Widmer, G.; Lima, V.M.F.d.; Meireles, M.V.; Inácio, S.V.; Marques, M.G.; Marques, A.E.G.W.; Matos, L.V.S.d.; Panegossi, M.F.d.C.; Bresciani, K.D.S. Prevalence of Cryptosporidium Infection in Domestic Cats from an Urban Area in Brazil. Semin. Ciências Agrárias 2020, 41, 2677–2686. [Google Scholar] [CrossRef]
  63. Funada, M.R.; Pena, H.F.J.; Soares, R.M.; Amaku, M.; Gennari, S.M. Freqüencia de Parasitos Gastrointestinais Em Cães e Gatos Atendidos Em Hospital-Escola Veterinário Da Cidade de São Paulo. Arq. Bras. Med. Veterinária Zootec. 2007, 59, 1338–1340. [Google Scholar] [CrossRef]
  64. Gennari, S.M.; Ferreira, J.I.G.d.S.; Pena, H.F.d.J.; Labruna, M.B.; Azevedo, S.d.S. Frequency of Gastrointestinal Parasites in Cats Seen at the University of São Paulo Veterinary Hospital, Brazil. Rev. Bras. Parasitol. Veterinária 2016, 25, 423–428. [Google Scholar] [CrossRef] [PubMed]
  65. Huber, F.; Bomfim, T.C.B.; Gomes, R. Comparação Entre Infecção Por Cryptosporidium sp. e Por Giardia sp. Em Gatos Sob Dois Sistemas de Criação. Rev. Bras. Parasitol. Vet. 2002, 11, 7–12. [Google Scholar]
  66. de Oliveira Lemos, F.; Almosny, N.P.; Soares, A.M.B.; Alencar, N.X. Cryptosporidium Species Screening Using Kinyoun Technique in Domestic Cats with Diarrhea. J. Feline Med. Surg. 2012, 14, 113–117. [Google Scholar] [CrossRef]
  67. Mósena, A.C.S.; Cruz, D.L.; Canal, C.W.; Marques, S.M.T.; Valle, S.F.; Soares, J.F.; Mattos, M.J.T.; Costa, F.V.A. Detection of Enteric Agents into a Cats’ Shelter with Cases of Chronic Diarrhea in Southern Brazil. Pesqui. Veterinária Bras. 2019, 39, 630–634. [Google Scholar] [CrossRef]
  68. Ragozo, A.M.A.; Muradian, V.; Silva, J.C.R.e.; Caravieri, R.; Amajoner, V.R.; Magnabosco, C.; Gennari, S.M. Ocorrência de Parasitos Gastrintestinais Em Fezes de Gatos Das Cidades de São Paulo e Guarulhos. Brazilian J. Vet. Res. Anim. Sci. 2002, 39, 244–246. [Google Scholar] [CrossRef]
  69. Taghipour, A.; Khazaei, S.; Ghodsian, S.; Shajarizadeh, M.; Olfatifar, M.; Foroutan, M.; Eslahi, A.V.; Tsiami, A.; Badri, M.; Karanis, P. Global Prevalence of Cryptosporidium spp. in Cats: A Systematic Review and Meta-Analysis. Res. Vet. Sci. 2021, 137, 77–85. [Google Scholar] [CrossRef]
  70. Meng, X.-Z.; Li, M.-Y.; Lyu, C.; Qin, Y.-F.; Zhao, Z.-Y.; Yang, X.-B.; Ma, N.; Zhang, Y.; Zhao, Q. The Global Prevalence and Risk Factors of Cryptosporidium Infection among Cats during 1988–2021: A Systematic Review and Meta-Analysis. Microb. Pathog. 2021, 158, 105096. [Google Scholar] [CrossRef]
Table 1. Detection of Cryptosporidium sp., via ELISA, in children and their respective pets (cat/dogs).
Table 1. Detection of Cryptosporidium sp., via ELISA, in children and their respective pets (cat/dogs).
Species/SexELISATotal
Negative n (%)Positive n (%)
Dogs
Female39 (90.7)4 (9.3)43
Male83 (92.2)7 (7.8)90
TOTAL122 (92.2)11 (8.3)133
Cats
Female24 (96.0)1 (4.0)25
Male28 (93.3)2 (6.7)30
TOTAL52 (94.6)3 (5.5)55
Children
Female85 (97.7)2 (2.3)87
Male96 (95.1)5 (4.9)101
TOTAL181 (96.3)7 (3.7)188
Table 2. Univariable analysis and multivariable logistic regression model of the presence of Cryptosporidium coproantigens in children.
Table 2. Univariable analysis and multivariable logistic regression model of the presence of Cryptosporidium coproantigens in children.
Risk FactorsCryptosporidium Coproantigens (ELISA)Univariable AnalysisMultivariable Logistic
Regression
Negative n (%)Positive n (%)TotalOR (95% CI) 1p 2AOR (95% CI) 3p 2
Sex
Female85 (97.7)2 (2.3)87 (46.3) 0.454
Male96 (95.1)5 (4.9)101 (53.7)2.21 (0.42 < OR < 11.71)
Age (months)
≤2453 (96.4)2 (3.6)55 (29.3)1.03 (0.20 < OR < 5.50)0.968
25 > 5981 (94.2)5 (5.8)86 (45.7)3.08 (0.58 < OR < 16.32)0.185 *0.96 (0.13 < OR < 7.12)0.973
≥6047 (100)0 (0)47 (25.0)NC0.992
Fecal consistency
Not Diarrhea145 (100)0 (0)145 (77.1)NC<0.001 *10.997
Diarrhea36 (83.7)7 (16.3)43 (22.9)
Living with animal
Cat52 (94.6)3 (5.4)55 (29.3) 1.86 (0.40 < OR < 8.60)0.419
Dog129 (96.3)4 (3.0)133 (70.7)
Washing hands after playing with the pet
No172 (96.1)7 (3.9)179 (95.2)NC1.00
Yes9 (100)0 (0)9 (4.8)
Does the animal (dog and/or cat) usually lick the face and mouth of the child(ren)?
No28 (93.3)2 (6.7)30 (16.0)2.18 (0.40 < OR < 11.83)0.364
Yes153 (96.8)5 (3.2)158 (84.0)
Playing with sand at home or at school
No25 (92.6)2 (7.4)27 (14.4)2.50 (0.46 < OR < 13.57)0.290
Yes156 (96.9)5 (3.1)161 (85.6)
Washing hands after using the toilet
No146 (96.1)6 (3.9)152 (80.9)1.44 (0.17 < OR < 12.14)0.740
Yes35 (97.2)1 (2.8)36 (19.1)
Access to a water and sewage system
No80 (94.1)5 (5.8)85 (45.2)3.16 (0.60 < OR < 16.70)0.176 *5.09 (0.69 < OR < 37.16)0.109
Yes101 (98.1)2 (1.9)103 (54.8)
Lying down or sleeping in bed with the pet
No142 (98.6)2 (1.4)144 (76.0)
Yes39 (88.6)5 (11.4)44 (24.0)9.10 (1.70 < OR < 48.73)0.006 *9.88 (1.37 < OR < 71.20)0.023
Source of water
Filtered or boiled90 (96.8)3 (3.2)93 (49.5)
Tap91 (95.8)4 (4.2)95 (50.5)1.32 (0.29 < OR < 6.06)0.722
1 OR: odds ratio; reference group marked as OR = 1; CI: confidence interval; 2 Pearson’s chi-square; 3 AOR: adjusted odds ratio; NC: not calculated; * significant association (p < 0.25).
Table 3. Univariable analysis and multivariable logistic regression model of the presence of Cryptosporidium coproantigens in pets (cat/dogs).
Table 3. Univariable analysis and multivariable logistic regression model of the presence of Cryptosporidium coproantigens in pets (cat/dogs).
PetRisk FactorsCryptosporidium Coproantigens (ELISA)Univariable Analysis *Multivariable Logistic Regression
Negative n (%)Positive n (%)TotalOR (95% CI) 1p 2AOR (95% CI ) 3p 2
CatSex
Female24 (96.0)4 (4.0)25 (45.5) 0.668
Male28 (93.3)2 (6.7)30 (54.5)1.71 (0.15 < OR < 20.10)
Age (year)
≤133 (91.7)3 (8.3)36 (65.5)NC0.544
2 ≥ 719 (100)0 (0)19 (34.5)NC0.544
>70 (0)0 (0)0 (0)NC
Fecal consistency
Not Diarrhea44 (100)0 (0)44 (80)NC0.006
Diarrhea8 (72.7)3 (27.3)11 (20)
Access to street
No2 (100)0 (0)2 (3.6)NCNC
Yes50 (94.3)3 (5.7)53 (96.4)
Dewormed
No36 (92.3)3 (7.7)39 (70.9)NC0.996
Yes16 (100)0 (0)16 (29.1)
DogSex
Female39 (90.7)4 (9.3)43 (32.3)1.21 (0.34 < OR < 4.40)0.766
Male83 (92.2)7 (7.8)90 (67.7)
Age (year)
≤158 (89.2)7 (10.8)65 (48.9)1.93 (0.54 < OR < 6.93)0.358
2 ≥ 758 (95.1)3 (4.9)61 (45.9)0.41 (0.11 < OR < 1.63)0.2080.23 (0.05 < OR < 1.10)0.065
>76 (85.7)1 (14.3)7 (5.2)1.93 (0.21 < OR < 17.68)0.559
Fecal consistency
Not Diarrhea98 (97.0)3 (3.0)101 (75.9) 0.001 0.004
Diarrhea24 (75.0)8 (25.0)32 (24.1)10.89 (2.69 < OR < 44.16)11.76 (2.22 < OR < 62.41)
Access to street
No51 (100)0 (0)51 (38.4)NC0.007 0.989
Yes71 (86.7)11 (13.3)82 (61.6)
Dewormed
No73 (89.0)9 (11.0)82 (61.6)3.02 (0.63 < OR < 14.58)0.169 1.00 (0.15 < OR < 6.67)0.990
Yes49 (96.1)2 (3.9)51 (38.4)
1 OR: odds ratio. Reference group marked as OR = 1; CI: confidence interval. 2 Pearson’s chi-square. 3 NC: not calculated. * Significant association (p < 0.25).
Table 4. Molecular characterization of Cryptosporidium in feces from children and their respective pets (cat/dogs).
Table 4. Molecular characterization of Cryptosporidium in feces from children and their respective pets (cat/dogs).
Household ChildrenAnimal
Molecular Characterization DiarrheaPetMolecular CharacterizationDiarrhea
1C. canisYesDogC. canisYes
2C. canisYesDogC. canisYes
3C. parvumYesDogC. parvumYes
4C. parvumYesDogNot amplifiedNo
5C. parvumYesCatC. parvumYes
6C. parvumYesCatC. parvumYes
7C. parvumYesCatC. parvumYes
Table 5. Univariable analysis model of the presence of Cryptosporidium sp. in children and their respective pets (cat/dogs).
Table 5. Univariable analysis model of the presence of Cryptosporidium sp. in children and their respective pets (cat/dogs).
PetsNegative n (%)Positive n (%)TotalOR (CI 95%) 1p 2
Children
Negative173 (95.6)8 (4.4)181 (96.3)129.75 (13.92 < OR < 1209.68)< 0.00001
Positive1 (14.3)6 (85.7)7 (3.7)
1 OR: odds ratio. Reference group marked as OR = 1; CI: confidence interval. 2 Pearson’s chi-square (p < 0.05).
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.

Share and Cite

MDPI and ACS Style

Coelho, N.M.D.; Coelho, W.M.D.; Gomes, J.F.; Meireles, M.V.; Nagata, W.B.; de Lima, V.M.F.; Santos-Doni, T.R.; Silva, V.B.; da Silveira Neto, L.; Nakamura, A.A.; et al. Evidence of the Zoonotic Transmission of Cryptosporidium among Children and Pets. Pathogens 2023, 12, 1393. https://doi.org/10.3390/pathogens12121393

AMA Style

Coelho NMD, Coelho WMD, Gomes JF, Meireles MV, Nagata WB, de Lima VMF, Santos-Doni TR, Silva VB, da Silveira Neto L, Nakamura AA, et al. Evidence of the Zoonotic Transmission of Cryptosporidium among Children and Pets. Pathogens. 2023; 12(12):1393. https://doi.org/10.3390/pathogens12121393

Chicago/Turabian Style

Coelho, Natalia Marinho Dourado, Willian Marinho Dourado Coelho, Jancarlo Ferreira Gomes, Marcelo Vasconcelos Meireles, Walter Bertequini Nagata, Valéria Marçal Felix de Lima, Thais Rabelo Santos-Doni, Vitória Beatriz Silva, Luiz da Silveira Neto, Alex Akira Nakamura, and et al. 2023. "Evidence of the Zoonotic Transmission of Cryptosporidium among Children and Pets" Pathogens 12, no. 12: 1393. https://doi.org/10.3390/pathogens12121393

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop