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Outbreak-Associated Cases of

In 2007, outbreak-associated infectie accounted for 86 (15.8%) of STEC 0157 cas and 364 (5.4%) of Salmonella cases ascertain:similar to proportions in previous years. For large multistate outbreaks of Salmonella inte tions that included FoodNet sites were invest gated in 2007: an outbreak of S. Tennesse infections caused by contaminated peanut but ter (4), an outbreak of S. I 4,[5],12:1:- infectie caused by contaminated frozen pot pies, an cu break of S. Wandsworth and S. Typhimurinn infections attributed to a puffed vegetable snack and an outbreak of S. Paratyphi B var. Java as ciated with exposure to turtles (5). Reported by: D Vugia, MD, California Dept of Pris Health. A Cronquist, MPH, Colorado Dept of Public Hos and Environment. J Hadler, MD, Connecticut Dept of Health. M Tobin-D'Angelo, MD, Div of Public Heale Georgia Dept of Human Resources. D Blythe, MD, Mark Dept of Health and Mental Hygiene. K Smith, DV! Minnesota Dept of Health. S Lathrop, PhD, New Ma. Dept of Health. D Morse, MD, New York State Dept of Heave P Cieslak, MD, Oregon Public Health Div. ) Dunn, DII Tennessee Dept of Health. PL White, DVM, Food Safery. Inspection Suc, US Dept of Agriculture. JJ Guzewich, MPH Center for Food Safety and Applied Nutrition, Food as Drug Admin. Ol Henao, PhD, RM Hoekstra, PA E Scallan, PhD, FJ Angulo, DVM, PM Griffin, MDR Tauxe, MD, Div of Foodborne, Bacterial and Mycotic Disca". National Center for Zoonotic, Vector-Borne and Ente Diseases; C Barton Behravesh, DVM, EIS Officer, CDC. Editorial Note: Although significant declines ir the incidence of certain foodborne pathogers have occurred since 1996, these declines 2" occurred before 2004. Comparing 2007 with 2004-2006, the estimated incidence of infec tions caused by Campylobacter, Listeria, Salmenella, Shigella, STEC 0157, Vibrio, and Yersin. did not decline significantly, and the incidence of Cryptosporidium infections increased. Ths incidence of Salmonella infections in 2009 (14.92 cases per 100,000) was the furthest from


Relative rate (log scale)

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Shiga toxin-producing Escherichia coli. + The position of each line indicates the relative change in the incidence of that pathogen compared with 1996–1998. The actual incidences of these infections can differ.

e national target for 2010 (6.80 cases), and only infecons caused by Salmonella serotypes Typhimurium and eidelberg declined significantly. Salmonella organisms live in the intestines of most food imals. Transmission of Salmonella to humans can occur

many routes, including consumption of food animal oducts or raw produce contaminated with animal waste, antact with animals and their environment, and contami

ted water. Outbreaks caused by contaminated peanut .tter, frozen pot pies, and a puffed vegetable snack in 2007 derscore the need to prevent contamination of commerally produced products. The outbreak associated with rtle exposure highlights the importance of animals as a infood source of human infections. To reduce the incince of Salmonella infections, concerted efforts are needed roughout the food supply chain, from farm to processg plant to kitchen. Recognizing the need to prevent Imonella contamination of poultry products and other eats, the U.S. Department of Agriculture's Food Safety d Inspection Service (USDA FSIS) launched a Imonella initiative in 2006, with enhancements in 2008 :). A USDA FSIS testing program reported recent declines

the percentage of broiler chicken carcasses that yielded Imonella, from 16.3% in 2005 to 11.4% in 2006 and 5% in 2007 (7). Declines in the incidence of STEC 0157 infections in 103 and 2004 have not been maintained. Although the SDA FSIS and the beef processing industry have impleented interventions to reduce ground beef contaminaon, 21 beef product recalls for possible contamination ith STEC 0157 were issued in 2007, of which 10 were ness associated, an increase compared with previous years. SDA FSIS launched an STEC 0157 initiative in fall 2007 ad hosted a public meeting in spring 2008 to explore olutions to the challenges this pathogen presents. Addional efforts are needed to control STEC 0157 in cattle ad to prevent its spread to other food animals and food roducts, such as produce. The increase in reported Cryptosporidium infections comared with 2004-2006 might reflect an increase in diagostic testing stimulated by licensing of a new treatment nitazoxanide). The incidence of Campylobacter, Salmonella, :higella, and STEC O157 infections remains highest among

nildren aged <5 years, highlighting the need for targeted iterventions. Identified risk factors for bacterial enteric illess in young children include riding in a shopping cart ext to raw meat or poultry, attendance at day care,

visiting or living on a farm, and living in a home with a reptile (8,9). Recent Salmonella outbreaks associated with exposure to small turtles (carapace lengths of <4 inches) highlight the importance of enforcing a 1975 prohibition on their sale and distribution in the United States (5).

The findings in this report are subject to at least four limitations. First, FoodNet relies on laboratory diagnoses, and changing laboratory practices might affect the reported incidence for some pathogens, especially STEC. Second, many foodborne illnesses (e.g., norovirus) are not reported to Food Net. Third, differences in health-care seeking behaviors might contribute to a higher incidence of reported illnesses in certain age groups (e.g., young children). Finally, although the FoodNet population is similar to the U.S. population, the findings might not be generalizable (1).

Enhanced measures are needed to understand the complex ecologies that link pathogens to animals and plants; to control or eliminate pathogens in food sources; to reduce or prevent contamination during food growing, harvesting, and processing; and to educate restaurant workers and consumers about infection risks and prevention measures. Such measures can be more focused when the sources of human infections are known. More outbreaks can be recognized through more rapid and complete subtyping of pathogens and interviewing of ill persons and controls when clusters of illness are recognized.

Consumers can reduce their risk for foodborne illness by following safe food-handling and preparation recommendations and avoiding unsafe foods. Information on food safety practices is available at,, and pets. References 1. Scallan E. Activities, achievements, and lessons learned during the first

10 years of the Foodborne Diseases Active Surveillance Network: 1996–

2005. Clin Infect Dis 2007;44:718–25. 2. US Department of Health and Human Services. Healthy people 2010.

Washington, DC: US Department of Health and Human Services;

2000. Available at 3. CDC. Laboratory-confirmed non-0157 Shiga toxin-producing

Escherichia coliConnecticut, 2000–2005. MMWR 2007;56:29–31. 4. CDC. Multistate outbreak of Salmonella serotype Tennessee infections

associated with peanut butter-United States, 2006–2007. MMWR

2007;57:521-4. 5. CDC. Multistate outbreak of human Salmonella infections associated

with exposure to turtles—United States, 2007–2008. MMWR 2008;

57:69–72. 6. US Department of Agriculture, Food Safety and Inspection Service.

FSIS seeks comments on Salmonella sampling programs and activities. Washington, DC: US Department of Agriculture; 2008. Available at

Additional information about USDA FSIS and the STEC 0157 initiative and - neeting is available at

7. US Department of Agriculture, Food Safety and Inspection Service.

Progress report on Salmonella testing of raw meat and poultry products, 1998–2007. Washington, DC: US Department of Agriculture; 2008. Available at

testing/index.asp. 8. Fullerton KE, Ingram LA, Jones TF, et al. Sporadic Campylobacter infec

tion in infants a population-based surveillance case-control study. Pediatr

Infec Dis J 2007;26:19–24. 9. Jones TF, Ingram LA, Fullerton KE, et al. A case-control study of the

epidemiology of sporadic Salmonella infection in infants. Pediatrics 2006;118:2380–7.

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In 1991, approximately 100,000 Bhutanese mostly of Nepali origin began fleeing ethnic persecution in Bhutan and now live in seven refugee camps in southeastern Nepal. This refugee population has been stable since 1993 but remains dependent on food assistance. During January 28– February 6, 2007, a cross-sectional survey was conducted in the Bhutanese refugee camps. The number of households selected in each camp was proportional to the size of the camp;

individual households were selected using a systematic random sampling method. Information was collected regarding all children aged 6–59 months in each household by interviewing their mothers. Questions were asked regarding foods eaten by their children within the preceding 24 hours, incidence of diarrhea (i.e., three or more episodes within the preceding 24 hours) or ARI (i.e., fever plus either cough or difficulty breathing) in children within the preceding 14 days, and beliefs regarding their practices for feeding their children. In addition, the children's weight and height measurements, hemoglobin levels, and presence of clinical signs of angular stomatitis were assessed.

Weight was measured using digital scales, and height (or recumbent length for children aged <2 years) was measured using a Shorr Infant-Child Height Board (4). Acute malnutrition was defined as a weight-for-height 2-score <-2

presence of edema; severe acute malnutrition was defined as a weight-for-height 2-score <-3 or edema (5). Chronic malnutrition was defined as a height-for-age Z-score <-2; severe chronic malnutrition was defined as a height-for-age z-score <-3. Underweight was defined as a weight-for-age z-score <-2; severe underweight was defined as a weight-for-age Z-score <-3. Hemoglobin was measured using a Hemocue B-Hemoglobin Photometer (6). Anemia was defined as hemoglobin s11.0 g/dL for children and pregnant women and <12.0 g/dL for nonpregnant women.

The survey sample included 497 children and their 413 mothers. Twenty-one (4.2%) of the children aged 6–59 months had acute malnutrition, and one (0.2%) had severe acute malnutrition (Table). The prevalence of acute malnutrition was greatest (6.0%) among children aged 12-23 months. Chronic malnutrition was identified in 134 (26.9%) children, and severe chronic malnutrition was identified in 21 (4.2%) children. A total of 125 (25.1%) children were underweight, and 24 (4.8%) were severely underweight. Both chronic malnutrition and underweight increased with age (chi square for both trends: p = 0.001).

Among the children, 215 (43.3%) had anemia; prevalence of anemia decreased with age (Figure), from 78.8% among infants aged 6-11 months to 20.1% among children aged 48–59 months (chi square for trend: p<0.001).

Malnutrition and Micronutrient

Deficiencies Among Bhutanese Refugee Children Nepal, 2007

Acute and chronic malnutrition and micronutrient deficiencies have been found in refugee camp populations (1). In southeastern Nepal, despite consistent access by refugees to general rations,* certain micronutrient deficiencies have posed a substantial health burden to the approximately 100,000 Bhutanese residing in seven refugee camps (2). Limited food diversity, frequent illness, and poor feeding practices have been cited as underlying causes of poor nutritional status in this population. Annual surveys to assess levels of acute malnutrition (i.e., wasting) and chronic malnutrition (i.e., stunting) have been conducted in these camps by the Association of Medical Doctors of Asia (AMDA) and United Nations High Commissioner for Refugees (UNHCR); however, the capacity to reliably evaluate micronutrient deficiencies has not existed locally in the camps (3). In January 2007, AMDA and CDC, at the request of UNHCR and the World Food Programme (WFP), conducted a nutritional survey of children aged 6–59 months, assessing 1) the prevalence of acute malnutrition, chronic malnutrition, underweight, anemia, and angular stomatitis (i.e., riboflavin deficiency); 2) the cumulative incidence of diarrhea and acute respiratory illness (ARI); and 3) the feeding practices of the children's mothers. This report describes the results of that survey, which indicated that, although acute malnutrition was found in only 4.2% of the children, chronic malnutrition was found in 26.9% and anemia in 43.3%. These findings underscore the importance of monitoring both malnutrition and micronutrient deficiencies and addressing the underlying causes of nutritional deficits.

or the

* A daily general ration in Bhutanese refugee camps in Nepal consists of parboiled rice, 400 whole grain, 20 g; lentils, 40 g; vegetable oil, 25 g; sugar, 20 g wheat soya blend, 35 g; salt, 7,5 g; fresh vegetables, 260 g (rotated each month and including cauliflower, potato, pumpkin, squash, and radish).


ABLE. Number and percentage of Bhutanese refugee children aged 6–59 months with malnutrition or micronutrient deficiencies, age group-Nepal, 2007

Age group (mos)

No. (%)
No. (%)
No. (%)


(%) alnutrition/Deficiency

(n = 52)
(n = 117)
(n = 328)

(N = 497)

(95% CI) ute malnutrition wt for ht z-score)

1 (1.9)
7 (6.0)
13 (3.9)

21 (4.2)

(2.8-6.4) everes

0 (0)
0 (0)
1 (0.3)

1 (0.2)

(0.0-1.1) ronic malnutrition nt for age z-score)

5 (9.6)
(23.1) 102 (31.1)

134 (26.9) (23.2-31.0) Severe**

0 (0)
5 (4.3)
16 (4.9)

21 (4.2)

(2.8-6.4) nderweight (wt for age z-score) 4 (7.7)

25 (21.4)
96 (29.3)

125 (25.1) (21.5-29.1) Severe**

3 (5.8)
3 (2.6)
18 (5.5)

24 (4.8)

(3.3-7.1) nemia

41 (78.8)
80 (68.4)
94 (28.7)

215 (43.3) (39.0-47.7) ngular stomatitis

1 (1.0)
4 (3.4)
51 (15.5)

56 (11.3) (8.8–14.3) arrhea

27 (51.9)
54 (46.2)
68 (20.7)

149 (30.0) (26.2–34.2) cute respiratory illness 23 (44.2) 45 (38.5)

75 (22.9)

143 (28.8) (25.0–32.9) Confidence interval. Defined as a z-score <-2.0 standard deviations from the reference median or presence of edema. (World Health Organization Expert Committee on Physical Status. Physical status: the use and interpretation of anthropometry. World Health Organ Tech Rep Ser 1995;854). Defined as a z-score <-3.0 standard deviations from the reference median or presence of edema. Defined as a z-score <-2.0 standard deviations from the reference median. Defined as a z-score <-3.0 standard deviations from the reference median.

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and 314 (76.1%) reported introducing liquids other than breast milk to their children aged <3 months.

Cumulative incidence of diarrhea and ARI, frequency of foods consumed within the preceding 24 hours, and presence of anemia in mothers were not associated with anemia among the children. However, given the high prevalence of anemia, iron supplementation was recommended for all children aged <2 years, in accordance with World Health Organization guidelines (7). Other recommendations included investigation of the causes of high incidence of diarrhea and ARI in the children and expanded education of mothers regarding recommended feeding practices, particularly exclusive breastfeeding of children aged <6 months and age-appropriate introduction of complementary foods. Reported by: F Abdalla, J Mutharia, MD, United Nations High Commissioner for Refugees, Geneva, Switzerland. N Rimal, MD, Assoc of Medical Doctors of Asia, Bhadrapur, Nepal

. O Bilukha, MD, PhD, L Talley

, MPH, T Handzel, PhD, National Center for Environmental Health; S Bamrah, MD, EIS Officer, CDC. Editorial Note: The nutritional status of refugees is determined by the prevalence of conditions related to both malnutrition and micronutrient deficiencies. However, historically, much attention has been paid to acute malnutrition and little attention to chronic malnutrition and micronutrient deficiencies. In the Bhutanese camps in Nepal, a stable population of refugees has been receiving a general ration that includes some fresh vegetables and fortified blended flour but does not meet requirements for key micronutrients such as iron, riboflavin, and vitamin C. Food often is brought to refugee camps from a distance

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and requires storage and distribution. Perishable foods, such as vegetables (particularly green vegetables), fruits, and meats often are too costly and logistically difficult to be purchased in large quantities, stored, transported, likely stored again, and then distributed to refugees.

Restriction of refugee movement to participate in agriculture, forage for supplemental foods, or earn wages to buy commodities, further diminishes their ability to obtain micronutrient-rich foods not included in the

general ration. Refugees in this setting have access to food markets; however, most do not have resources to afford foods rich in vitamins and minerals.

Micronutrient deficiencies are not clinically identifiable until late stages, and serologic testing is logistically difficult and costly. Given their diagnostic difficulty and impact on growth and development, micronutrient deficiencies should be addressed in children at an early age. This survey found that the prevalence of anemia was high in children, particularly those aged 6–11 months. Anemia is a common clinical manifestation of micronutrient deficiency, particularly iron deficiency. The prevalence of anemia was much higher in the children than in their mothers, despite access to similar foods. Potential reasons for this include 1) inadequate numbers of iron-rich foods, 2) poor feeding practices, and 3) frequent episodes of common diseases, such as those causing diarrhea and respiratory infections, which can increase loss of micronutrients.

Because options for diversification of the general ration are limited, diet supplementation and/or food fortification are the most likely methods to prevent micronutrient deficiencies. However, both fortification and supplementation are costly, and the addition of some fortificants reduces the shelf-life of commodities (8). Implementing supplementation and fortification programs will require changes in policies and practices of food aid agencies and increased donor participation, although fortification often is a cost-effective strategy for addressing micronutrient problems.

Educating mothers regarding appropriate breastfeeding and complementary feeding practices also is critical to preventing anemia and malnutrition in young children. Appropriate feeding practices include both exclusive breastfeeding until age 6 months and introduction of complementary foods rich in vitamins and minerals at appropriate ages. Exclusive breastfeeding until age 6 months is nutritionally adequate, protects children against infection, and prevents introduction of liquids, such as tea, that can inhibit iron absorption (9).

The high incidence of illness, particularly diarrheal disease, in these children can decrease absorption and increase

loss of micronutrients while also increasing metabolic (and consequently micronutrient) requirements. Determining the causes of frequent illnesses in the Bhutanese refugee children and implementing appropriate interventions to address these causes can decrease the effects of morbidity on micronutrient deficiencies and overall nutritional status (10).

The findings in this report are subject to at least ons limitation. Although anemia was evaluated as a marker fo: iron deficiency, levels of iron deficiency (e.g., ferritin or transferrin receptors) were not measured directly. In addition, other clinically relevant micronutrients, such as thiamine, vitamin A, or zinc, were not measured because of cost and logistical constraints.

Additional priority given to chronic malnutrition and micronutrient deficiencies in refugee camps might reduce the incidence of anemia and other potential sequelae of these conditions, including slowed growth and development. One strategy that has been shown to reduce anemia in children and is currently being evaluated in refugee camp settings i the use of Sprinkles®,t packets of dry powder, containing iron and other micronutrients intended for home fortification of foods. As lengths of stay in refugee camps increase agencies should consider this and other new strategies to address all possible negative nutritional outcomes o: prolonged dependence on food aid.

Acknowledgment This report is based, in part, on contributions by S Mukherjec. World Food Programme, Damak, Nepal. References 1. World Food Programme. Food and nutrition handbook. Rome, Itali

World Food Programme; 2002. 2. Blanck HM, Bowman BA, Serdula MK, Khan LK, Kohn W, Woodruff

BA; Bhutanese Refugee Investigation Group. Angular stomatitis and riboflavin status among adolescent Bhutanese refugees living in south

eastern Nepal. Am J Clin Nutr 2002;76:430–5. 3. UNHCR/WFP Joint Assessment Mission. Assistance to Bhutanes

refugees in Nepal. World Food Programme and United Nations High Commissioner for Refugees; 2006. Available at

publ/PUBL/45f81e6a2.pdf. 4. United Nations. How to weigh and measure children. Assessing th:

nutritional status on young children in household surveys. New York

NY: United Nations; 1986. 5. WHO Expert Committee on Physical Status. Physical status: the us

and interpretation of anthropometry. World Health Organ Tech Rep

Ser 1995;854. 6. Cohen AR, Seidl-Friedman J. HemoCue system for hemoglobin mea

surement: evaluation in anemic and nonanemic children. Am J Clip Pathol 1988;90:302-5.

Additional information available at

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