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Fecal contamination of food, water, hands, and kitchen utensils at the household level in rural areas of Peru.


Diarrheal diseases are among the leading causes of childhood illness and death in developing countries, killing an estimated 1.3 million children less than five years of age annually (Black et al., 2010).

The World Health Organization outlines several aspects critical to the prevention of diarrhea. They include improved drinking water systems and sanitation facilities, improved nutrition (through breast-feeding and better weaning practices), and good personal and domestic hygiene, among others (United Nations Children's Fund/World Health Organization [WHO], 2009). Several studies have demonstrated a high prevalence of bacterial contamination of water and foods within households (Black et al., 1989; Lanata, 2003; Wright et al., 2004), which is likely associated with incidence of infections in susceptible individuals, especially children.

A need exists for effective interventions in developing countries that can minimize food and water contamination at the household level and therefore reduce the rate of diarrhea in these environments (Hunter, 2009; Lanata, 2003). By measuring risky practices and behaviors and identifying kitchen sites, niches, and surfaces that harbor pathogenic microorganisms, we can provide a basis from which to develop effective interventions. The aim of our study was to identify those potential exposures at the household level, specifically those associated with contamination of food, drinking water, kitchen utensils and surfaces, and caregivers' and children's hands. Our study was conducted to inform a subsequent randomized trial that evaluated the health effects of an integrated home-based intervention package in a rural area of Peru. In addition, we tested for the presence of diarrheagenic E. coli (Nataro & Kaper, 1998) as an indicator of pathogenic E. coli in this setting.

Materials and Methods

Study Site

Our study was conducted in rural communities of San Marcos Province, Cajamarca, situated at 2,200 to 3,900 m above sea level in the highlands of Peru. Daily temperatures ranged from 7.6[degrees]C-25.0[degrees]C during the study period and relative humidity was between 59% and 73%. Agriculture and subsistence farming are the major economic activities in this area. Houses are mud brick structures with clay tile roofs supported by tree rods, earthen floors, and few open windows. A typical house consists of three rooms: a kitchen and dining room, a living and sleeping room, and a storage area. Water supply for about 61% of rural homes in San Marcos comes from a piped gravity system that transports untreated water captured from springs through individual or small-scale collective plastic piping to a tap in the courtyard. Only 9% of households have electricity, 2% have a closed sewage system, and 75% have access to a pit latrine (Instituto Nacional de Estadistica e Informatica, 2007).

Meals are based mainly on potatoes and other tubers and legumes, eaten with rice or boiled in a soup or a stew. Red meat and chicken are seldom consumed due to their high cost. Animals like dogs, guinea pigs, and chickens roam free in kitchens and households. The latter two are bred at home for sale or reserved for festive meals. Meals are prepared three to four times a day and eaten by adults and children alike. Leftover food is not consumed but discarded or fed to the animals. No time is set at which to start cooking the midday meal. Mothers start cooking anywhere from 8:00 a.m. to 12:00 p.m. and keep the food on the fire until lunch. Meals are served directly from pots to plates using wooden ladles. Kitchen utensils are washed with water brought from an outside faucet in a plastic basin, and a malla, a local kitchen cloth, also is used to clean dirty surfaces and caregivers' hands while cooking. The malla is kept wet after rinsing in the same washing up water, which is not changed very often.

Most households have access to tap water from a faucet installed in the yard. The gravity-based piped water supply system provides spring water to each household. The water is unfiltered, untreated, and chlorination is uncommon. Drinking water is either consumed directly from the faucet or boiled with herbs for children's consumption only. Hygiene practices include hand washing with water only; soap and detergent are rarely used.

Study Design

Households were identified in 32 communities based on home visits and enrolled by a trained field worker between April and September 2008 if they had a child aged 6 to 35 months. Field workers visited each participating household (N = 64) once, mostly at noon, to sample food, water, and kitchen environments.

Sample Collection

In each household approximately 20 g of each food served to the child was collected. If the child had already eaten, samples were taken from the pot. Between 50 and 100 mL of the child's drinking water and one sample from each of the available kitchen utensils (i.e., dish, cup, pot, cutlery, cutting board, and kitchen cloth) were also collected. For both the child and the caregiver, one hand was rinsed in buffer solution for microbiological testing. Samples were collected following standard procedures (Swanson, Busta, Peterson, & Johnson, 1992; WHO, 1997).

For kitchen surfaces, a 10 x 10 cm area of the cutting board or table and the surface of the utensil that was in contact with the child's food or drink was wiped using a cotton swab moistened with Butterfield's phosphate buffer (BPB) and then placed into a tube containing 10 mL of BPB. Kitchen cloths were collected in a new resealable plastic bag and a 10-[cm.sup.2] portion was cut and placed in a sterile plastic bag filled with 100 mL of BPB. To obtain samples from hands, caregivers and children placed one hand into a sterile plastic bag filled with 100 mL of BPB. The hand was massaged for 60 seconds, with emphasis on rubbing between fingers, around the fingernails, and the palm of the hand. All samples were kept in a Styrofoam box with cold packs for transport to the project laboratory in San Marcos City and stored at 8[degrees]C until processing the same day

Sample Analyses

Food, utensils, and hand samples were analyzed for total coliforms and E. coli using Petrifilm E. coli/coliform count plates, following standard procedures (Association of Analytical Communities [AOAC], 2000). A 1-mL aliquot of 10-fold dilutions was plated onto a Petrifilm EC plate. The plates were incubated at 35[degrees]C [+ or -] 1[degrees]C for 24 hours [+ or -] 2 hours to enumerate total coliforms and 48 hours [+ or -] 2 hours to enumerate E. coli. Water samples were analyzed for thermotolerant (fecal) coliforms using a membrane-filtration method, i.e., the Oxfam DelAgua water testing kit, and results were recorded as E. coli (CFU/100mL of water), an indicator for thermotolerant coliforms.

Colony counts were recorded by the onduty lab microbiologist. Cultures were reread by a second microbiologist. Digital pictures taken from each sample were read by a third microbiologist to decide on a final result in case of discrepancies (more than 10% difference) between the first two counts.

For the detection of diarrheagenic E. coli, five colonies per sample were saved in peptone media vials for further characterization. From the Petrifilm EC plate, priority was given to typical E. coli-like colonies (blue colonies with gas) (AOAC, 2000); however, other coliforms were saved if less than five typical E. coli-like colonies were present. The peptone media vials were transported to the Enteric Diseases and Nutrition Laboratory at the Tropical Medicine Institute, Cayetano Heredia University, Lima, for analysis using a real-time polymerase chain reaction (PCR) multiplex system (Guion, Ochoa, Walker, Barletta, & Cleary, 2008), which detects virulence genes of enterotoxigenic E. coli (ETEC), enteroinvasive E. coli (EIEC), enteropathogenic E. coli (EPEC), Shiga-toxin-producing E. coli (STEC), enteroaggregative E. coli (EAEC) and diffuse-adherent E. coli (DAEC). The multiplex PCR was done in a five-colony pool per sample (Barletta et al., 2009).

Data Analysis

Geometric means of the colony counts (total coliforms and E. coli) for each type of sample were calculated. A value of 0.5 was assigned to all samples with zero colony counts to allow for calculations. Proportional differences were analyzed by Chisquare tests with Yates's correction or by two-tailed Fisher's exact test using Epi Info version 6 statistical package.


A total of 275 samples (134 from kitchen utensils, 77 from children's meals, 43 from hands, and 21 from children's drinking water) from 64 households were analyzed. The frequency of contamination with total coliforms and E. coli by type of sample is presented in Table 1. Total coliforms were significantly more present on hands (65%) and on kitchen utensils (58%) than in children's meals (19%); p < .01. Kitchen cloths (89%, 17/19) and caregivers' hands (76%, 17/19) were the individual samples most frequently contaminated with total coliforms. The frequency of E. coli in drinking water (48%) was significantly higher than that of kitchen utensils (16%, p = .002) and children's meals (4%, p < .0001). No statistical difference was observed, however, when comparing drinking water and all hands (p = .09). Kitchen cloths were most frequently contaminated with E. coli (42%), with a geometric mean of 1.2 x [10.sup.4] CFU/100 [cm.sup.2].

A total of 108 samples were tested for diarrheagenic E. coli. DAEC was the most frequent type identified (9/108), followed by ETEC (8/108), EIEC (4/108), STEC (3/108), and EAEC (1/108). Overall, at least one type of diarrheagenic E coli was detected in 20% of all tested samples, including in 33% (2/6) of children's drinking water, 27% (3/11) of children's meals, 23% (14/60) of kitchen utensils, and 10% (3/31) of hands.


Our study describes the high frequency of microbiological contamination of water and food consumed by children in parts of rural Peru, and indicates an important potential cause of diarrhea. A high percentage (48%) of the water consumed by children was often boiled with herbs and subsequently kept in jars or pots, but contained thermotolerant coliforms. Dairy products and boiled soups also had remarkably high E. coli counts (up to [10.sup.7] CFU/mL in dairy). The source of these contaminants likely originates from contaminated kitchen utensils including plates, spoons, pots, or jars, as well as mallas, the local kitchen cloths. Children's and caregivers' hands were also contaminated with E. coli due to poor hygiene practices.

Our study had some limitations. Sampling was conducted during the dry season (April to September), and not during the rainy season (December through March). Hence, seasonal variations in water and food contamination were not captured. Study conditions allowed for only a small number of convenience samples from each type of food or kitchen utensil, which is sufficient for descriptive purposes, but limited for giving precise estimates. Sampling centered on the midday meal for logistical reasons. It is possible that meals prepared in the early morning or in the evening may have had different levels of contamination, influenced by cooler temperatures at those times. Future studies would need to sample children's meals over a 24-hour period and ideally, repeatedly, in order to fully describe the level and variability of food contamination in these households. Study conditions did not allow for serial sample collection before and after food preparation and at the time of serving to children, which would have allowed us to identify the critical control points to minimize or eliminate the risk of contamination in a hazard analysis and critical control point system (Bryan, 1981).

Few studies (Adachi, Mathewson, Jiang, Ericsson, & DuPont, 2002; Vigil et al., 2009) have attempted to identify diarrheagenic E. coli--the strains of E. coli--in environmental samples (food, water, and utensils), using molecular and specific PCR methods. We tested for these groups of pathogens by PCR, based on a presumptive identification of E. coli-like colonies and coliforms. We found only a small number of colonies with diarrheagenic E. coli strains. It is unclear whether the lower isolation rates found are real or are due to low sensitivity in our selection of E. coli-like colonies. These results suggest that risk estimates based on total coliform or E. coli counts overestimated the true risk of diarrheal diseases from food and water due to pathogenic E. coli.

Despite these limitations, the results of our study are comparable to others from developing country settings, where weaning food and water in households were frequently found to be contaminated with fecal matter (Clasen et al., 2003; Kung'u et al., 2009; Rufener, Mausezahl, Mosler, & Weingartner, 2010). In a study conducted in peri-urban Lima, Peru (Black et al., 1989), weaning food was found to be contaminated with Salmonella spp., Vibrio cholerae non-O1, and ETEC originating from secondary contamination of kitchen utensils after food preparation. Foodborne illnesses are associated with food preparation too far in advance of consumption (allowing growth of pathogens present in the food to levels exceeding the minimal infectious dose), improper cooling, and inadequate reheating (Lanata, 2003). In our study communities, food stuffs and leftovers were not stored for second servings, since cooking was done three to four times per day; however, food samples collected at eating time directly after cooking were found to be contaminated. This could be explained by the high frequency of contamination found on kitchen surfaces and utensils, most likely due to the washing up process: washing up in a plastic basin with untreated and unchanged water leaves food residuals behind as a source for bacterial growth. Other studies have shown how common cross contamination is in the kitchen through contaminated water used to clean dishes (Beumer & Kusumaningrum, 2003).

Our study indicates that kitchen cloths may present a significant yet underrecognized source of contamination of kitchen utensils, since cloths are used all over the kitchen to wipe dirty surfaces as well as hands and remain wet after rinsing in the same washing-up water. In other settings, kitchen cloths were identified as vehicles for pathogens that were able to survive for extended periods of time (Kusumaningrum, van Putten, Rombouts, & Beumer, 2002; Mattick et al., 2003). Food safety interventions in these communities should focus on kitchen hygiene practices, hand washing, safe food preparation, and safe handling of cooked food.


The prevalence of fecal contamination of food and drinking water given to children highlights the need for improving domestic hygienic practices, like hand washing and cleaning kitchen utensils, to prevent diarrheal diseases transmitted through the fecal-oral route. Effective interventions to reduce contamination of the kitchen environment should be developed. Further studies are needed on the correlation between diarrheagenic E coli identification as detected by PCR and the traditional culture method for detecting fecal coliforms in food and water. In a related study, we will evaluate the impact on the rate of diarrheal diseases in young children of an intervention designed to improve water availability in the kitchen environment through kitchen sink installation, using point-of-use water disinfection by solar exposure. Further effects of promoting hand washing with soap or detergent and improving hygiene practices in the kitchen will also be studied. Hf|

Acknowledgements: We would like to extend our thanks to the families who participated in the study for their contributions; to the field workers for their dedication to obtaining the samples; to Mrs. Selenne Flores, the study field supervisor, for her care and diligence in getting this study done; to Dr. Jan Hattendorf, for his help revising the manuscript; and to Amena Briet for language editing. We would also like to express our appreciation to the local authorities and the Cajamarca Health Region for their support throughout the study. A grant from UBS Optimus Foundation, Zurich, Switzerland, supported this work. The ethical review boards of the Instituto de Investigacion Nutricional, Lima, Peru, and the cantonal ethical review board of Basel, Switzerland, approved the study.

Corresponding Author: Ana I. Gil, Instituto de Investigacion Nutricional, Av. La Molina 1885, Lima 12, Peru. E-mail:


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Ana I. Gil, MSc

Instituto de Investigation Nutricional, Lima

Claudio F. Lanata, MPH, MD

Instituto de Investigacion Nutricional Escuela de Medicina, Universidad Peruana de Ciencias Aplicadas, Lima

Stella M. Hartinger, MSc

Instituto de Investigacion Nutricional, Lima

Swiss Tropical and Public Health Institute University of Basel

Daniel Mausezahl, PhD

Swiss Tropical and Public Health Institute University of Basel

Beatriz Padilla, MSc

Wageningen University Wageningen, Netherlands

Theresa J. Ochoa, MD

Universidad Peruana Cayetano Heredia, Lima

University of Texas School of Public Health

Michelle Lozada

Ines Pineda

Hector Verastegui

Instituto de Investigacion Nutricional, Lima

Total Coliforms and E. coli in Food, Water, Utensils, and
Hands From Rural Households of Peru

Sample Type                       Total Coliforms

                            % (n/N)       Geometric Mean

    Child meals                                CFU/g

    Salad                   67 (2/3)         4.4 x 10
    Dairy                   44 (4/9)         8.1 x 10
    Tuber cooked/fried     21 (3/14)            1.6
    Rice                   18 (2/11)            1.2
    Soup                   17 (2/12)            1.7
    Toasted bread           11 (1/9)            0.8
    Oat                     9 (1/11)            1.4
    Stew                     0(0/8)
    All child meals        19 (15/77)
  Drinking water              N/A               N/A

Kitchen utensils                            CFU/utensil

    Kitchen cloth          89 (17/19)    1.2 x [10.sup.4]
                                          ([double dagger])
    Washing basin          70 (7/10)         2.1 x 10
    Water jar              69 (9/13)     1.3 x [10.sup.2]
    Pot                    64 (7/11)     6.3 x [10.sup.2]
    Spoon                  64 (9/14)         2.9 x 10
    Dish                   58 (7/12)     1.2 x [10.sup.2]
    Cup                    50 (6/12)         2.5 x 10
    Bottle's nipple        45 (5/11)         2.4 x 10
    Cutting board          43 (6/14)         2.0 x 10
                                          ([double dagger])
    Ladle                  28 (5/18)            2.2
    All kitchen utensils   58 (78/13)

Hands                                        CFU/hands

    Caregiver              76 (16/21)    2.8 x [10.sup.2]
    Child                  55 (12/22)        2.2 x 10
    All hands              65 (28/43)

Sample Type                   Total Coliforms         E. coli

                                   Ranges             % (n/N)

    Child meals                    CFU/g

    Salad                        [10.sup.2]           0 (0/3)
    Dairy                  [10.sup.2]-[10.sup.9]     22 (2/9)
    Tuber cooked/fried     [10.sup.1]-[10.sup.2]     0 (0/14)
    Rice                   [10.sup.1]-[10.sup.2]     0 (0/11)
    Soup                   [10.sup.2]-[10.sup.3]     8 (1/12)
    Toasted bread                [10.sup.1]           0 (0/9)
    Oat                          [10.sup.4]          0 (0/11)
    Stew                             0                0 (0/8)
    All child meals             0-[10.sup.9]         4 (3/77)
  Drinking water                    N/A             48 (10/21)

Kitchen utensils           CFU/utensil ([dagger])

    Kitchen cloth          [10.sup.0]-[10.sup.7]     42 (8/19)
                             ([double dagger])
    Washing basin          [10.sup.1]-[10.sup.3]     10 (1/10)
    Water jar              [10.sup.1]-[10.sup.9]     15 (2/13)
    Pot                    [10.sup.1]-[10.sup.9]     18 (2/11)
    Spoon                  [10.sup.1]-[10.sup.3]     21 (3/14)
    Dish                   [10.sup.1]-[10.sup.9]     8 (1/12)
    Cup                    [10.sup.0]-[10.sup.7]     8 (1/12)
    Bottle's nipple        [10.sup.1]-[10.sup.9]     9 (1/11)
    Cutting board          [10.sup.0]-[10.sup.5]     14 (2/14)

    Ladle                  [10.sup.1]-[10.sup.3]     6 (1/18)
    All kitchen utensils   [10.sup.0]-[10.sup.9]    16 (22/134)

Hands                            CFU/hands

    Caregiver              [10.sup.1]-[10.sup.5]     29 (6/21)
    Child                  [10.sup.1]-[10.sup.4]     18 (4/22)
    All hands              [10.sup.1]-[10.sup.5]    23 (10/43)

Sample Type                           E. coli

                            Geometric Mean             Ranges

    Child meals                  CFU/g                 CFU/g

    Salad                                                0
    Dairy                         4.2          [10.sup.0]-[10.sup.7]
    Tuber cooked/fried                                   0
    Rice                                                 0
    Soup                          1.0                [10.sup.3]
    Toasted bread                                        0
    Oat                                                  0
    Stew                                                 0
    All child meals                                 0-[10.sup.7]
  Drinking water                 2.6 *              [10.sup.0]-
                                                    [10.sup.2] *

Kitchen utensils              CFU/utensil      CFU/utensil ([dagger])

    Kitchen cloth              1.2 x 10        [10.sup.0]-[10.sup.5]
                           ([double dagger])     ([double dagger])
    Washing basin                 1.0                [10.sup.2]
    Water jar                     1.2          [10.sup.1]-[10.sup.2]
    Pot                           1.4          [10.sup.0]-[10.sup.3]
    Spoon                         1.3          [10.sup.1]-[10.sup.2]
    Dish                          0.6                [10.sup.1]
    Cup                           0.5                [10.sup.0]
    Bottle's nipple               1.1                [10.sup.3]
    Cutting board                 0.8                [10.sup.0]
                           ([double dagger])     ([double dagger])
    Ladle                         0.6                [10.sup.1]
    All kitchen utensils                       [10.sup.0]-[10.sup.5]

Hands                          CFU/hands             CFU/hands

    Caregiver                     4.8          [10.sup.1]-[10.sup.4]
    Child                         1.4          [10.sup.1]-[10.sup.3]
    All hands                                  [10.sup.1]-[10.sup.4]

* Thermotolerant (fecal) coliform CFU/[10.sup.0] mL.

([dagger]) Area of utensil in contact with food/drink.

([double dagger]) CFU/[10.sup.0] [cm.sup.2].
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Article Details
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Author:Gil, Ana I.; Lanata, Claudio F.; Hartinger, Stella M.; Mausezahl, Daniel; Padilla, Beatriz; Ochoa, T
Publication:Journal of Environmental Health
Article Type:Report
Geographic Code:3PERU
Date:Jan 1, 2014
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