Diarrhoeagenic Escherichia coli and Salmonella spp. Contamination of Food and Water Consumed by Children with Diarrhoea in Maputo, Mozambique
1
Department of Consumer and Food Sciences, Faculty of Natural and Agricultural Sciences, University of Pretoria, Private Bag X20, Pretoria 0028, South Africa
2
Department of Hygiene and Public Health, Veterinary Faculty, Eduardo Mondlane University, Maputo P.O. Box 257, Mozambique
3
National Food Institute, Technical University of Denmark, Private Bag 201, 2800 Kongens Lyngby, Denmark
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2024, 21(9), 1122; https://doi.org/10.3390/ijerph21091122
Submission received: 19 July 2024
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Revised: 19 August 2024
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Accepted: 23 August 2024
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Published: 26 August 2024
Abstract
:In Mozambique, about 500,000 cases of diarrhoea were caused by foodborne pathogens in 2018. A review of the epidemiology of diarrhoea in children under five showed a high disease burden. This study aimed to identify Diarrhoeagenic Escherichia coli (DEC) and Salmonella spp. contamination of food and water in urban and rural areas of Maputo consumed by children under five with diarrhoea. One hundred and eighty-six children with diarrhoea were selected from Primeiro de Maio and Marracuene Health Care Centres from the Kamaxakeni and Marracuene districts, respectively. Food (n = 167) and water (n = 100) samples were collected in children’s households for diarrhoeagenic bacterial identification. Interviews were conducted using a semi-structured questionnaire to collect data about demographics and foods consumed a week before the children’s diarrhoea episodes. The prevalence of both DEC and Salmonella spp. was 9.8% in food and 5.4% in water samples. DEC was most prevalent in cereals (urban = 2.8%; rural = 2.4%) and water samples (urban = 1.4%; rural = 3.3%). Salmonella spp. was mainly detected in cereals (urban = 0.7%; rural = 0.8%). Diarrhoeagenic pathogens were associated with the type of food frequently consumed by children under five years with diarrhoea (infant formula, fruit puree, ready-to-eat meals, and bottled water), while the association with demographics was absent. We found that the infant foods consumed by children with diarrhoea are associated with DEC and Salmonella spp., and the prevalence of these contaminants is higher in the rural (8.9%) than in the urban area (6.3%), showing the need for caregiver education on food handling practices.
1. Introduction
Foodborne illnesses constitute a public health concern, leading to 420,000 deaths yearly worldwide, where low and middle-income countries have the highest burden, accounting for 53% of all foodborne illnesses and 70% of related deaths [1]. Children under five years are at higher risk, and almost 40% of foodborne diseases and 30% of associated deaths occur in this group age [2].
The high foodborne illness rates in low and middle-income countries can be attributed to several factors. These include the lack of clean water for washing utensils and food, unsafe water supply systems, poor sanitation, inadequate hygiene, and the use of human sewage or animal waste for irrigation [3]. Contaminants in food may be due to food preparation and storage, hygiene practices, children feeding themselves, and exposure to infected animals [4,5]. In Mozambique, about 500,000 cases of diarrhoea were caused by foodborne pathogens in 2018 [6]. A review of the epidemiology of diarrhoea in children under five years showed a high disease burden and an associated case fatality rate of 10% [7]. From 2015 to 2019, 9041 cases of diarrhoea were reported in children under five years old in Maputo, of which 25.2% were in rural areas and 74.8% were in urban areas [8].
The majority of the current literature available for Mozambique identified diarrheagenic pathogens in humans. These included Rotavirus, Adenovirus, Shigella spp., Escherichia coli, Vibrio cholera, and Cryptosporidium spp. [7,9]. Limited existing data showed an association between caregiver hygiene practices during food preparation and storage and infant food contamination [4]. This study aimed to ascertain the prevalence of diarrhoeagenic pathogens, such as E. coli and Salmonella spp., in food and water consumed by children under five years of age with diarrhoea.
2. Materials and Methods
2.1. Target Population
Children under five were selected from the Primeiro de Maio Health Care Centre in the Kamaxakeni district (urban area) and the Marracuene Health Care Centre in the Marracuene district (rural area) in Maputo (Mozambique). These health care centres offer primary health care services.
A total of 186 children were selected based on convenience sampling methods where they were included because they appeared in the health care centre and if they fulfilled the following inclusion criteria: (i) children were under five years old with diarrhoea, (ii) their caregiver consented to complete the questionnaire, and (iii) consented to provide food and water samples from their respective households for laboratory analyses.
2.2. Interviews with Caregivers
We conducted face-to-face interviews based on a semi-structured questionnaire to collect demographic data and information on the possible source/vehicle of infection as perceived by the caregivers. We also gathered data on the food consumed in the household a week before the children experienced diarrhoea episodes and the water supply. The questionnaire was designed to obtain information about the food consumed by children under five, especially those younger than two years old.
2.3. Food and Water Samples Collected from Households
A total of 267 samples, comprising 167 food and 100 tap water specimens, were collected from selected households. About 100 g of food that was available during sampling collection and 1L of water were collected with sterile containers, kept chilled and transported to the laboratory at Eduardo Mondlane University, Mozambique.
The breakdown of food samples included cereal (urban = 57; rural = 26), combined foods (urban = 30; rural = 24), pasteurised cow’s milk and milk products (urban = 8; rural = 3), cooked vegetables (urban = 5; rural = 2), and other miscellaneous foods (urban = 2) (Table 1). It is important to note that “combined food” typically entailed a blend of pap or rice with curry, or a meat or vegetable stew. This type of meal is prevalent in Mozambican communities as a complementary food for children transitioning to solid foods. Regarding the water samples, 42 were sourced from urban locations, while the remaining 58 were collected from rural settings.
2.4. Bacteriological Analysis of Food and Water Samples
2.4.1. Detection of Salmonella spp., Shigella spp., and E. coli
Table 2 summarises Salmonella spp., Shigella spp., and E. coli methodology used. Salmonella spp. and Shigella spp. detection was conducted using the standard operating procedure created based on the Food and Drug Administration-Bacteriological Analytical Manual (FDA BAM) and ISO 6579-1:2017, while E. coli identification was conducted following the FDA-BAM and National Authority official methods [10,11,12,13]. From these analyses, 104 food and 37 water samples were found to have Salmonella spp./Shigella spp. isolates, while 49 food and 38 water samples harboured E. coli strains. A single colony of each isolate was further analysed using biochemical tests, confirming the identification of the strains obtained in the culture method.
2.4.2. MALDI-TOF MS Confirmation of Bacterial Isolates
For confirmation, 228 isolates were submitted to the matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF MS) [14]. Single colonies from overnight-grown bacteria isolated from food and water samples were analysed on MALDI Biotyper® sirius RUO (Bruker Daltonics GmbH & Co. KG, 2021; Bremen, Germany) using Bruker Daltonics MALDI-TOF biotyper flex control 3.4 software. A representative spectrum was obtained by collecting 40 shots on six different positions of the sample (240 laser shots in total) in about 15 s per sample, and the results were displayed in real time. The results were obtained by comparing the Bruker Daltonics MALDI-TOF biotyper compass RTC 4.1.100 database strains.
2.4.3. DNA Extraction and Diarrhoeagenic Escherichia coli PCR
DNA was extracted from confirmed 16 h E. coli cultures using the Quick-DNA Fungal/Bacterial Miniprep kit (Zymo Research, Tustin, CA, USA).
Polymerase Chain Reaction (PCR) amplification of Diarrhoeagenic Escherichia coli (DEC) genes was performed using SSI Diagnostic protocol (Hillerød, Denmark), which detects Enterohemorrhagic Escherichia coli (EHEC), Enteroinvasive Escherichia coli (EIEC), Enteropathogenic Escherichia coli (EPEC), and Enterotoxigenic Escherichia coli (ETEC) pathotypes.
The PCR was carried out in a T100TM Thermal cycler (Bio-Rad, Hercules, CA, USA) in a total volume of 20 μL, containing 10 μL PCR ReadyMix, 6 μL Primer Mix, and 4 µL of extracted DNA. The amplification cycle included denaturation for 2 min at 95 °C, which was performed in one cycle, followed by 35 cycles of denaturation at 94 °C for 50 s, annealing for 40 s at 62 °C, extension at 72 °C for 50 s, and one cycle of the final annealing at 72 °C for 3 min.
The 18 µL of each completed PCR reaction were visualised in 2% agarose gel for 40 min at 70 V, stained with SYBR green, and detected by Gel doc TM EZ system (Bio-Rad, Hercules, CA, USA).
2.5. Data Analysis
Preliminary screening of the demographic characteristics and the caregiver’s perception of the cause of diarrhoea in the children was conducted using univariate analyses on Epi info (version 7.2.5.0) [15]. The univariate analysis screened the variables for inclusion in the binomial logistic regression model using X2 with the threshold set at p ≤ 0.2 with an odd ratio (OR > 1), based on the Fischer test and considering the one-tailed hypothesis. The binomial regression model was performed in the R environment for Windows (version 4.3.1) using the package MASS (Version 7.3-60) [16]. For the binomial regression analysis, the presence or absence of DEC/Salmonella in food samples was considered an outcome variable, while the explanatory variables included child age, caregiver age, child gender, caregiver gender, marital status, source of thinking, sampling site, baby bottle, bottled water, fruit puree, infant formula, milk breastfeeding, ready-to-eat meals, goat, cassava leaves, water source, water treatment, monthly income, and toilet system. The X2 test was conducted to detect differences between the urban and rural areas.
3. Results
3.1. The Sociodemographic Characteristics of the Caregivers and Children under Five Years Old
The study included 186 children, most of whom were from the urban area (54.8%) and mostly male (58.8%). In the rural area, most children were female (51.2%). The majority of the children (53.2%) were between 7 and 24 months old, and their caregivers were mainly female (94.1%), with over half of them being between 18 and 25 years old. The majority of the caregivers were single but living with a partner (76.8%) (Table 3). The X2 test indicated a significant difference (p < 0.05) in child age in the urban and rural areas.
In terms of monthly income, most caregivers in the urban area (33.3%) and the rural area (28.6%) were unaware of the primary breadwinner’s income. Among those who did provide information, the majority reported it to be between $71.00 and $140.00 (8.8% urban; 9.5% rural) (Table 3).
Concerning water supply, 99.0% of the participants used potable municipal water in the urban area, while in the rural area, they used municipal water and community wells. For water treatment, boiling was the most used method (10.8% urban; 8.3% rural). Flush or pour toilets with septic tanks, including squat toilets, were the most common toilet systems: 56.9% in urban areas and 32.1% in rural areas. The X2 test indicated a significant difference (p < 0.05) in the water source and toilet system used in both sampling areas (Table 3).
3.2. The Caregiver’s Perception of the Cause of Diarrhoea in Children under Five Years Old
Table 4 shows the cause of diarrhoea as perceived by the caregivers, where the majority of respondents in both urban, 52.0% (53/102), and rural, 25% (23/84), areas could not identify a probable cause for episodes of diarrhoea in the children included in the study. However, some caregivers attributed the cause of diarrhoea to factors such as vegetables, cereals, cookies/cakes/popcorn, weaning/infant formula, teething, and fruits/juice. Interestingly, only a small percentage of respondents in the urban area (2.9%) and the rural area (2.4%) considered water a probable cause of diarrhoea. The X2 indicated that there was a significant difference (p < 0.05) in caregivers’ perception of the cause of diarrhoea between the urban and rural areas.
3.3. One-Week Food Consumption Recall for Children under Five with Diarrhoea
Table 5 details the food consumed by children with diarrhoea the week before their visit to the health care centre. Based on the one-week food recall, the children had consumed animal protein, vegetables, and fruits (only rural). Chickens were the most commonly consumed source of animal protein, accounting for 36.3% of cases in the urban area and 90.5% in the rural area. Among dairy products, milk was reported as the most commonly consumed in the urban area, accounting for 12.7% of cases, while in the rural area, yoghurt was the most commonly consumed, accounting for 29.8% of cases. Cheese was only reported to be consumed by the children included in the study in the urban area, 2.9% of cases. Most children consumed green cabbage a week before the in 37.3% of the episodes of diarrhoea in the urban area and 19.0% in the rural area. Fruits were only consumed in the rural area, in 7.1% of cases.
Regarding food consumption by children under two years old, biscuits/rusks/cookies were the most commonly consumed item in the urban area, accounting for 33.3% of consumption. In the rural area, fermented cereals were the most consumed, representing 33.3% of consumption. Children under two years old were also fed liquid foods using feeding bottles, with 21.6% in urban areas and 29.8% in rural areas (Table 5).
The p-value of the X2 test indicated a significant difference (p < 0.05) in the consumption of certain foods before the occurrence of diarrhoeal episodes in children in both sampling areas. These foods include animal proteins (such as beef, pork, goat, chicken, eggs, fish, and yoghurt) and vegetables like cacana (Momordica balsamina), which is used as a food in south Mozambique and as medicine in other parts of the country (Table 5).
3.4. Prevalence of Foodborne Pathogens in Food and Water Samples
Table 6 shows the prevalence of foodborne pathogens in samples collected from the children’s households. In both rural and urban areas, contamination with Diarrhoeagenic E. coli (DEC) and Salmonella spp. was found in the food and water collected from the children’s homes. The overall prevalence of bacterial contamination was 15.2%, with a higher prevalence in the rural area (8.9%), and water and cereal samples contributed 12.1%. The most prevalent pathogen was DEC, primarily found in cereal and water samples, with a prevalence of 9.9% in both areas. Salmonella spp. was only identified in the water samples (0.7%) collected in the urban area and cereal samples (1.5%) from both areas. DEC was the only pathogen detected in combined food (2.4%) and yoghurt (0.7%) from rural and urban areas, respectively.
3.5. Prevalence of Diarrhoeagenic E. coli in Food and Water Samples
Table 7 represents the prevalence of DEC pathotypes among food and water samples collected in households and the sampling sites. The overall frequency of the DEC pathotypes is 13.0% and ETEC was the most prevalent, contributing 11.5% in both rural and urban areas. The other pathotypes consisted of EIEC detected in cereal food from rural areas and EPEC identified in water samples from urban areas.
3.6. Associated Factors
Table 8 presents the results of a binomial logistic regression analysis that aimed to assess the relationship between the prevalence of DEC isolated from the food and water samples and the demographics and food consumed by children participating in the study. However, this analysis was not conducted for Salmonella spp. because only three samples were found to be contaminated with this pathogen, which falls below the threshold for conducting binomial logistic regression.
The results of the analysis demonstrated a significant association between DEC contamination and the consumption of fruit puree [(B = 1.50); 95% CI (1.31–14.70), (p < 0.05)] and infant formula [(B = 1.34); 95% CI (0.91–13.90), (p < 0.05)] in children under two years of age. Additionally, the binomial logistic regression analysis conducted on the urban area data revealed associations between the consumption of certain foods by children under two years, such as associations of infant formula [(B = 2.24); 95% CI (0.04–83.40), (p < 0.05)] and ready-to-eat meals [(B = 2.03); 95% (0.84–60.7), (p < 0.05)] with DEC contamination. Conversely, in the rural area, the consumption of fruit puree [(B = 2.17); 95% CI (1.65–56.2), (p < 0.05)] and bottled water [(B = 3.04); 95% CI (2.79–>100), (p < 0.05)] by children under five years of age was associated with DEC contamination. Notably, no association was found between demographic characteristics and DEC contamination in this study.
4. Discussion
This study assessed the prevalence of diarrhoeagenic bacteria in food and water consumed by children with diarrhoea in urban and rural areas of Maputo and factors associated with children’s food contamination.
Most of the selected children were below two years old in urban and rural areas, showing that children of this age group were the most affected by diarrhoea [17].
The source of water in urban and rural households was different. In the urban area, only tap water was used, while in rural households, tap water and community wells were used as sources of water. This difference may be related to the coverage of municipal water distribution, which is high in the urban area [18]. The type of toilet facility used in the urban and rural areas is also different; more than half of households in the urban area use flush or pour toilets with septic tanks, including squat toilets. This may be related to lower socioeconomic status, as this type of facility is more costly than others.
Although caregivers from urban and rural areas indicated several factors as responsible for the cause of diarrhoea in children under five, most of them did not know the cause. Similar to a study carried out in Ethiopia [19], in this study, the percentage of respondents without knowledge of the cause of diarrhoea was higher in the urban area than in the rural area, contradicting the expected association with education level in this area. Chicken consumption in Maputo was lower than reported in other areas of Africa, which may be a protective factor, as poultry may carry pathogenic agents, including E. coli, Listeria monocytogenes, Campylobacter, Salmonella, and Staphylococcus aureus that can cause diseases, especially in children with weak immune systems [20,21,22].
Yoghurt consumption was higher in the rural area compared to a study conducted in Nigeria [23]. The consumption of yoghurt benefits for gastrointestinal conditions such as diarrhoeal disease [24]. The consumption of lettuce and banana was different in urban and rural areas; this fresh produce may constitute a vehicle for diarrhoeagenic pathogens when good hygiene is not appropriately followed [25].
DEC was the most frequent pathogen isolated in water collected from households in urban and rural areas (5.4%), which was lower than the prevalence reported in another study from Mozambique [26]. The presence of DEC in drinking water may be due to faecal contamination. Salmonella spp. was only detected in water samples collected in the urban area of Maputo, while in South Africa, this pathogen was identified in rural areas [27]. The presence of Salmonella spp. in water samples may be related to the dissemination of these bacteria through the faecal–oral route. Cereal-based foods were the most consumed by children in urban and rural areas, and DEC and Salmonella spp. were contaminants of this food group, similar to findings reported in South Africa. The contamination by DEC might have occurred during food preparation and the preservation of leftovers. Salmonella spp. contamination may be related to sanitation and poor operational practices during food processing [28,29]. The prevalence of diarrhoeagenic contaminants was higher in the rural area than in the urban area, which may be due to the ability of people in urban areas to purchase and access better quality and safe foods [30]. Additionally, the urban area (Kamaxakeni) has benefited from several educational sessions related to food handling practices, as this has been the focus of many studies that include health promotion activities to prevent illness. Contamination of combined food collected in households was observed, similar to a study in Bangladesh that reported contamination of complementary food with E. coli [31]. The presence of DEC in tested food samples indicates faecal contamination and poor hygiene conditions during food preparation and conservation, which can cause gastroenteritis in children [32].
The present study evaluated the association between diverse types of food and water with DEC contamination. Infant formula and fruit puree were associated with DEC contamination. Infant formula contamination by E. coli may occur during preparation, storage, and feeding, making this infant food unacceptable for consumption, so following hygiene practices is essential [33].
Unpasteurised fruit products can contribute to foodborne illness as they can act as vehicles for foodborne pathogens. For example, berry juices and purees have been shown to support pathogens like E. coli O157:H7 [25]. In the urban area, factors associated with the presence of contaminants were infant formula and ready-to-eat meals, which is concerning as improper practices during their preparation can introduce diarrhoeagenic pathogens to children.
In the rural area, food contamination was associated with fruit puree and bottled water. The use of bottled water was associated with DEC contamination, which may be related to water counterfeiting. Other studies have also found DEC in bottled water, showing that water that people believe to be safe for consumption can be a risk factor for foodborne illness [34].
The present study did not address aspects related to how the caretaker prepares the food and how this is conserved, especially the leftover food, which are crucial points where contamination can occur; that is why a study should be carried out to ascertain when and where the contamination takes place in Maputo households.
5. Conclusions
Diarrhoeagenic E. coli and Salmonella spp. are present in food and water consumed by children under five years with diarrhoea in Kamaxakeni, an urban area, and Marracuene, a rural area of Maputo. The prevalence of these diarrhoeagenic pathogens is higher in rural areas.
Significant disparities are noted between the two study areas in caregivers’ perceptions of the causes of diarrhoea, the types of water sources and toilet systems utilized, and the dietary habits of children in the week preceding diarrheal episodes.
These findings underscore the necessity for educating caregivers on proper food handling practices and enhancing water sources, given the evidence of diarrhoeagenic pathogens.
Author Contributions
Conceptualization, S.F., E.B., C.M. and J.G.; Data curation, S.F.; Funding acquisition, T.H.; Investigation, S.F.; Methodology, T.H.; Project administration, E.B.; Resources, T.H.; Supervision, E.B., C.M. and J.G.; Validation, E.B.; Visualization, S.F.; Writing—original draft, S.F. and Writing—review & editing, E.B., C.M., J.G. and T.H. All authors have read and agreed to the published version of the manuscript.
Funding
This study was co-funded by the Bill & Melinda Gates Foundation and the Foreign, Commonwealth & Development, Office (FCDO) of the United Kingdom Government [Grant Agreement Investment ID OPP1195617].
Institutional Review Board Statement
The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board Faculty of Medicine/Hospital Central de Maputo (CIBS FM&HCM) (protocol code: CIBS FM&HCM/092/2019; date of approval:12/12/2019).
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
The data presented in this study are available on request from the corresponding author as the data was stored electronically and transferred to a password-protected database to ensure privacy and confidentiality.
Acknowledgments
The authors acknowledge the Bill and Melinda Gates Foundation and the United Kingdom’s Department of International Development, Office (FCDO) of the United Kingdom Government [Grant Agreement Investment ID OPP1195617]. Under the grant conditions of the Foundation, a Creative Commons Attribution 4.0 Generic License has already been assigned to the Author Accepted Manuscript version that might arise from this submission.
Conflicts of Interest
The authors declare no conflicts of interest.
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Table 1.
Food and water samples collected from households of children with diarrhoea in urban and rural areas of Maputo.
Table 1.
Food and water samples collected from households of children with diarrhoea in urban and rural areas of Maputo.
| Collected Samples | Sampling Site | |
|---|---|---|
| Urban Area No (%) | Rural Area No (%) | |
| Cereal | 57 (21.3) | 36 (13.5) |
| Combined food | 30 (11.2) | 24 (9.0) |
| Milk and milk product | 8 (3.0) | 3 (1.1) |
| Vegetable (cooked) | 5 (1.9) | 2 (0.7) |
| Other food (fish and fruit puree) | 2 (0.7) | 0 |
| Water | 42 (15.7) | 58 (21.7) |
Table 2.
Diarrhoeagenic bacteria’s identification in food and water samples collected from households of children with diarrhoea.
Table 2.
Diarrhoeagenic bacteria’s identification in food and water samples collected from households of children with diarrhoea.
| Diarrheagenic Pathogen | Steps for Strain Identification | Media | References |
|---|---|---|---|
| Salmonella spp./Shigella spp. | Pre-enrichment | BPW and mTSB broth | [10,11] |
| Enrichment | |||
| Strain identification | XLD agar, HE agar, MAC agar, TSI agar, and MIO | ||
| Escherichia coli | Enrichment | BPW | [12,13] |
| Strins identification | MAC agar, TSI agar, and MIO |
BPW (Buffer Peptone Water, Liofilchem Diagnostici-2360611014, Roseto degli Abruzzi, Italy); mTSB (Modified Tryptic Soy Broth, Liofilchem Diagnostici-2360610352, Roseto degli Abruzzi, Italy); RVS (Rappaport-Vassiliadis with Soya, Liofilchem Diagnostici-610175, Roseto degli Abruzzi, Italy); MKTTn (Muller-Kauffman Tetrathionate-novobiocin Broth, Liofilchem Diagnostici-2360610239, Roseto degli Abruzzi, Italy); XLD (Xylose Lysine Deoxycholate agar, Neogen-NCM0021A, Lansing, MI, USA); HE (Hektoen enteric agar, HIMEDIA M377-500G, Kennett Square, PA, USA); MAC (MacConkey agar, Liofilchem Diagnostici-610028, Italy); TSI (Triple Sugar Iron agar, Liofilchem Diagnostici-360620055, Italy); MIO (Motility Indole Ornithine Medium, HIMEDIA–M378-500G, Square, PA, USA).
Table 3.
Sociodemographic characteristics of the caregivers and children under five years with diarrhoea (n = 186).
Table 3.
Sociodemographic characteristics of the caregivers and children under five years with diarrhoea (n = 186).
| Variable | Category | Urban Area (n = 102) | Rural Area (n = 84) | p-Value for X2 |
|---|---|---|---|---|
| n (%) | n (%) | |||
| Child gender | Female | 42 (41.2) | 43 (51.2) | 0.22 |
| Male | 60 (58.8) | 41 (48.8) | ||
| Caregiver gender | Female | 97 (95.1) | 78 (92.9) | 0.74 |
| Male | 5 (4.9) | 6 (7.1) | ||
| Child age (months) | ≤6 months | 11 (10.8) | 22 (26.2) | 0.02 |
| 7 to 24 months | 60 (58.8) | 39 (46.4) | ||
| >24 months | 31 (30.4) | 22 (26.2) | ||
| Not disclosed | 0 | 1 (1.2) | ||
| Caregiver (age years) | 18 to 25 years | 50 (49.0) | 42 (50) | 0.94 |
| 26 to 35 years | 33 (32.4) | 31 (36.9) | ||
| >35 years | 10 (9.8) | 9 (10.7) | ||
| Not disclosed | 9 (8.8) | 2 (2.4) | ||
| Marital status | Single but lives with someone | 75 (73.5) | 67 (79.8) | 0.26 |
| Single and living alone | 10 (9.8) | 3 (3.5) | ||
| Married | 17 (16.7) | 13 (15.5) | ||
| Widow | 0 | 1 (1.2) | ||
| Relation to the child | Mother | 91 (89.2) | 76 (90.5) | 0.42 |
| Father | 5 (4.9) | 6 (7.1) | ||
| Grandmother/Parents | 6 (5.9) | 2 (2.4) | ||
| Monthly income (USA Dollar) | 0 to 70.00 $ | 6 (5.9) | 7 (8.3) | 0.85 |
| 71.00–140.00$ | 9 (8.8) | 8 (9.5) | ||
| >140.00$ | 2 (2.0) | 2 (2.4) | ||
| Don’t know the income | 34 (33.3) | 24 (28.6) | ||
| Not disclosed | 51 (50.0) | 43 (51.2) | ||
| Water source | Home pipe water | 101 (99.0) | 68 (81.0) | <0.05 |
| Public/community wells | 0 | 12 (14.3) | ||
| Not disclosed | 1 (0.5) | 4 (4.8) | ||
| Water treatment | Boiling | 11 (10.8) | 7 (8.3) | 0.37 |
| Other treatment methods | 1 (1.0) | 1 (1.2) | ||
| Not disclosed | 90 (88.2) | 76 (90.5) | ||
| Toilet system | Pit latrine with covering slab | 28 (27.5) | 12 (14.3) | <0.05 |
| Pit latrine without covering slab | 3 (2.9) | 13 (15.5) | ||
| Flush or pour toilet with septic tank, including squat toilet | 58 (56.9) | 27 (32.1) | ||
| Flush or pour toilet connected to sewer pipe | 1 (1.0) | 19 (22.6) | ||
| Other toilet system | 0 | 3 (3.6) | ||
| Not disclosed | 12 (11.8) | 10 (11.9) |
Table 4.
Perception of the cause of diarrhoea by the caregivers of the children (n = 186).
| Variable | Categories | Urban Area (102) | Rural Area (84) | p-Value for X2 |
|---|---|---|---|---|
| n (%) | n (%) | |||
| Cause of diarrhoea in children under five years old | Vegetables | 2 (2.0) | 5 (6.0) | <0.05 |
| Cereals | 2 (2.0) | 3 (3.6) | ||
| Cookies/cake/popcorn | 3 (2.9) | 5 (6.0) | ||
| Fruit/Juice | 3 (2.9) | 9 (10.7) | ||
| Other food (peanut and fish) | 1 (1.0) | 1 (1.2) | ||
| Food not specified | 4 (4.0) | 2 (2.4) | ||
| Dentition | 6 (5.9) | 14 (16.7) | ||
| Weaning/Infant formula | 5 (4.9) | 15 (17.9) | ||
| Water | 2 (2.9) | 2 (2.4) | ||
| Other causes | 2 (2.0) | 3 (3.5) | ||
| Don’t know the reason | 53 (52.0) | 21 (25.0) | ||
| Not disclosed | 19 (18.6) | 4 (4.8) |
Table 5.
Food consumed by children under five a week before attending the health care centres.
| Variables | Categories | Urban Area (n = 102) | Rural Area (n = 84) | p-Value for X2 | ||
|---|---|---|---|---|---|---|
| Consumed n (%) | Not Consumed n (%) | Consumed n (%) | Not Consumed n (%) | |||
| Source of animal protein | Beef | 23 (22.5) | 78 (76.5) | 64 (76.2) | 19 (22.6) | <0.05 |
| Pork | 11 (10.8) | 90 (88.2) | 45 (53.6) | 38 (45.2) | <0.05 | |
| Lamb | 1 (1.0) | 100 (98.0) | 3 (3.6) | 80 (95.2) | 0.48 | |
| Goat | 3 (2.9) | 98 (96.1) | 27 (32.1) | 56 (66.7) | <0.05 | |
| Chicken | 37 (36.3) | 64 (62.7) | 76 (90.5) | 7 (8.3) | <0.05 | |
| Egg | 23 (22.5) | 78 (76.5) | 64 (76.2) | 19 (22.6) | <0.05 | |
| Not disclosed | 1 (1.0) | 1 (1.2) | N/A | |||
| Fish | 30 (29.4) | 72 (70.6) | 69 (82.1) | 15 (17.9) | <0.05 | |
| Other sources of animal protein | Milk (pasteurised) | 13 (12.7) | 88 (86.3) | 11 (13.1) | 72 (85.7) | 1.00 |
| Yoghurt | 6 (5.9) | 95 (93.1) | 25 (29.8) | 58 (6.9.0) | <0.05 | |
| Cheese | 3 (2.9) | 98 (96.1) | 0 | 83 (98.8) | 0.32 | |
| Not disclosed | 1 (1.0) | 1 (1.2) | N/A | |||
| Vegetables | Lettuce | 6 (5.9) | 40 (39.2) | 9 (10.7) | 13 (15.5) | <0.05 |
| Cassava leaves | 12 (11.8) | 34 (33.3) | 10 (11.9) | 12 (14.3) | 0.19 | |
| Pumpkin leaves | 8 (7.8) | 38 (37.2) | 7 (8.3) | 15 (17.9) | 0.30 | |
| Cowpea leaves | 13 (12.7) | 33 (32.4) | 12 (14.3) | 10 (11.9) | 0.10 | |
| Green cabbage | 38 (37.3) | 8 (7.8) | 16 (19.0) | 6 (7.1) | 0.53 | |
| Sweet potato leaves | 6 (5.9) | 40 (39.2) | 3 (3.6) | 19 (22.6) | 1.00 | |
| Cacana | 0 | 46 (45.1) | 7 (8.3) | 15 (17.9) | <0.05 | |
| Other vegetables | 8 (7.8) | 38 (37.3) | 5 (6.0) | 17 (20.2) | 0.85 | |
| Not disclosed | 56 (54.9) | 62 (73.8) | N/A | |||
| Fruits | Fruits | 0 | 0 | 6 (7.1) | 0 | N/A |
| Not disclosed | 102 (100.0) | 78 (92.9) | ||||
| Food consumed by children <2 years | Milk breastfeeding | 25 (24.5) | 77 (75.4) | 19 (22.6) | 65 (77.4) | 0.90 |
| Infant formula | 15 (14.7) | 87 (85.3) | 6 (7.1) | 78 (92.9) | 0.16 | |
| Fermented cereals | 22 (21.6) | 80 (78.4) | 28 (33.3) | 56 (66.7) | 0.10 | |
| Ready-to-eat meals | 7 (6.9) | 95 (93.1) | 8 (9.5) | 76 (90.5) | 0.69 | |
| Fruit puree | 12 (11.8) | 90 (88.2) | 11 (13.1) | 73 (87.0) | 0.96 | |
| Biscuits/rusks/cookies | 34 (33.3) | 68 (66.7) | 20 (23.8) | 64 (76.2) | 0.21 | |
| Fruit/vegetable/juices | 28 (27.5) | 69 (67.6) | 20 (23.8) | 63 (75.0) | 0.58 | |
| Not disclosed | 5 (4.9) | 1 (1.2) | N/A | |||
| Baby bottle | 22 (21.6) | 53 (52.0) | 25 (29.8) | 50 (59.5) | 0.72 | |
| Not disclosed | 27 (26.5) | 9 (10.7) | N/A | |||
| Bottled water | 22 (21.6) | 79 (77.5) | 23 (27.4) | 61 (72.6) | 0.48 | |
| Not disclosed | 1 (1.0) | 0 | N/A | |||
| Boiled water | 1 (1.0) | 91 (89.2) | 5 (6.0) | 71 (84.5) | 0.14 | |
| Not disclosed | 10 (9.8) | 8 (9.5) | N/A | |||
| Water not boiled | 31 (30.4) | 61 (59.8) | 26 (31.0) | 50 (59.5) | 1.00 | |
| Not disclosed | 10 (9.8) | 8 (9.5) | N/A | |||
N/A: Not Applicable.
Table 6.
Pathogens distribution among food (n = 167) and water (n = 100) samples collected in under five children’s households.
Table 6.
Pathogens distribution among food (n = 167) and water (n = 100) samples collected in under five children’s households.
| Samples | Total number of isolates No (%) | Urban Area (n = 144) | Rural Area (n = 123) | ||
|---|---|---|---|---|---|
| DEC | Salmonella spp. | DEC | Salmonella spp. | ||
| No (%) | No (%) | No (%) | No (%) | ||
| Cereal | 9 (6.7) | 4 (2.8) | 1 (0.7) | 3 (2.4) | 1 (0.8) |
| Combined food | 3 (2.4) | ND | ND | 3 (2.4) | ND |
| Milk and Milk Products | 1 (0.7) | 1 (0.7) | ND | ND | ND |
| Vegetable (cooked) | ND | ND | ND | ND | ND |
| Other food (fish and fruit puree) | ND | ND | ND | ND | ND |
| Water | 7 (5.4) | 2 (1.4) | 1 (0.7) | 4 (3.3) | ND |
| Total | 20 (15.2) | 7 (4.9) | 2 (1.4) | 10 (8.1) | 1 (0.8) |
ND: Not detected; DEC: Diarrhoeagenic E. coli.
Table 7.
Diarrhoeagenic E. coli pathotypes prevalent in food and water samples collected in rural and urban households from children under five with diarrhoea.
Table 7.
Diarrhoeagenic E. coli pathotypes prevalent in food and water samples collected in rural and urban households from children under five with diarrhoea.
| Samples | Number of Isolates No (%) | Urban Area (n = 144) | Rural Area (n = 123) | ||||
|---|---|---|---|---|---|---|---|
| ETEC No (%) | EPEC No (%) | EIEC No (%) | ETEC No (%) | EPEC No (%) | EIEC No (%) | ||
| Cereal | 7 (5.2) | 4 (2.8) | ND | ND | 2 (1.6) | ND | 1 (0.8) |
| Combined food | 3 (2.4) | ND | ND | ND | 3 (2.4) | ND | ND |
| Yoghurt | 1 (0.7) | 1 (0.7) | ND | ND | ND | ND | ND |
| Vegetable (cooked) | ND | ND | ND | ND | ND | ND | ND |
| Other food (fish and fruit puree) | ND | ND | ND | ND | ND | ND | ND |
| Water | 6 (4.7) | 1 (0.7) | 1 (0.7) | ND | 4 (3.3) | ND | ND |
| Total | 17 (13.0) | 6 (4.2) | 1 (0.7) | 0 | 9 (7.3) | 0 | 1 (0.8) |
EIEC—Enteroinvasive Escherichia coli; EPEC—Enteropathogenic Escherichia coli; ETEC—Enterotoxigenic Escherichia coli; ND—Not detected.
Table 8.
Binomial logistic regression of Diarrhoeagenic E. coli presence on food and water in urban and rural areas of Maputo.
Table 8.
Binomial logistic regression of Diarrhoeagenic E. coli presence on food and water in urban and rural areas of Maputo.
| Variable Group | Category | B (SE) | 95% CI for Odds Ratio | ||
|---|---|---|---|---|---|
| Lower | Odds Ratio | Upper | |||
| Diarrheagenic E. coli | |||||
| 18 to 25 years | −3.15 (0.45) | ||||
| Caregiver age | 26 to 35 years | −0.51 (0.67) | 0.14 | 0.60 | 2.07 |
| >35 years | −0.42 (0.90) | 0.83 | 0.66 | 3.28 | |
| Food consumed by children < 2 years | Fruit puree | 1.50 (0.61) * | 1.31 | 4.50 | 14.70 |
| Infant formula | 1.33 (0.68) * | 0.91 | 3.81 | 13.90 | |
| Milk breastfeeding | −1.44 (0.08) | 0.01 | 0.24 | 1.32 | |
| Ready-to-eat meal | 1.17 (0.68) | 0.77 | 3.24 | 11.80 | |
| Salmonella spp. | |||||
| Intercept | −4.60 (1.16) *** | ||||
| Caregiver age | 26 to 35 years | −17.9 (>100) | N/A | <0.01 | >100 |
| Source of animal protein | Pork | −0.77 (1.43) | 0.02 | 0.46 | 7.01 |
| Food consumed by children < 2 years | Baby bottle | −0.03 (1.40) | 0.13 | 0.97 | 14.5 |
| Bottled water | 0.02 (1.32) | 0.04 | 1.02 | 12.6 | |
| Ready-to-eat meal | 3.20 (1.31) * | 2.03 | 24.6 | >100 | |
| Kamakeni (Urban area) | |||||
| Caregiver age | 18 to 25 years | −3.32 (0.69) *** | |||
| 26 to 35 years | −1.04 (1.36) | 0.01 | 0.3 | 3.71 | |
| >35 years | 0.09 (1.31) | 0.04 | 1.09 | 11.5 | |
| Food consumed by children < 2 years | Bottled water | −18.67 (>100) | NA | <0.01 | >100 |
| Infant formula | 2.24 (1.08) * | 0.04 | 9.38 | 83.4 | |
| Ready-to-eat meal | 2.03 (1.04) * | 0.84 | 7.64 | 60.7 | |
| Marracuene (Rural area) | |||||
| Male | −3.84 (1.41) ** | ||||
| Caregiver gender | Female | −1.16 (1.33) | 0.02 | 0.31 | 7.58 |
| Food consumed by children < 2 years | Bottled water | 3.04 (1.22) * | 2.79 | 20.80 | >100 |
| Baby bottle | −0.45 (1.21) | 0.03 | 0.64 | 5.78 | |
| Fruit puree | 2.18 (0.87)* | 1.65 | 0.80 | 56.20 | |
Significance level: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.0; B: Estimated coefficient; E: Standard error; CI: Confidence interval; N/A: Not applicable
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MDPI and ACS Style
Faife, S.; Macuamule, C.; Gichure, J.; Hald, T.; Buys, E. Diarrhoeagenic Escherichia coli and Salmonella spp. Contamination of Food and Water Consumed by Children with Diarrhoea in Maputo, Mozambique. Int. J. Environ. Res. Public Health 2024, 21, 1122. https://doi.org/10.3390/ijerph21091122
AMA Style
Faife S, Macuamule C, Gichure J, Hald T, Buys E. Diarrhoeagenic Escherichia coli and Salmonella spp. Contamination of Food and Water Consumed by Children with Diarrhoea in Maputo, Mozambique. International Journal of Environmental Research and Public Health. 2024; 21(9):1122. https://doi.org/10.3390/ijerph21091122
Chicago/Turabian StyleFaife, Sara, Custódia Macuamule, Josphat Gichure, Tine Hald, and Elna Buys. 2024. "Diarrhoeagenic Escherichia coli and Salmonella spp. Contamination of Food and Water Consumed by Children with Diarrhoea in Maputo, Mozambique" International Journal of Environmental Research and Public Health 21, no. 9: 1122. https://doi.org/10.3390/ijerph21091122
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