Invasive Enterobacter sakazakii disease in infants.Enterobacter sakazakii kills 40%-80% of infected infants and has been associated with powdered formula. We analyzed 46 cases of invasive infant E. sakazakii infection to define risk factors and guide prevention and treatment. Twelve infants had bacteremia bacteremia: see septicemia. bacteremia Presence of bacteria in the blood. Short-term bacteremia follows dental or surgical procedures, especially if local infection or very high-risk surgery releases bacteria from isolated sites. , 33 had meningitis, and 1 had a urinary tract infection urinary tract infection (UTI), n infection in one or more of the structures that make up the urinary system. Occurs more often in women and is most commonly caused by bacteria. . Compared with infants with isolated bacteremia, infants with meningitis had greater birthweight (2,454 g vs. 850 g, p = 0.002) and gestational age ges·ta·tion·al age n. See estimated gestational age. Gestational age The estimated age of a fetus expressed in weeks, calculated from the first day of the last normal menstrual period. (37 weeks vs. 27.8 weeks, p = 0.02), and infection developed at a younger age (6 days vs. 35 days, p<0.001). Among meningitis patients, 11 (33%) had seizures, 7 (21%) had brain abscess Brain Abscess Definition Brain abscess is a bacterial infection within the brain. Description The brain is usually well insulated from infection by bacteria, protected by the skull, the meninges (tissue layers surrounding the brain), , and 14 (42%) died. Twenty-four (92%) of 26 infants with feeding patterns specified were fed powdered formula. Formula samples associated with 15 (68%) of 22 cases yielded E. sakazakii; in 13 cases, clinical and formula strains were indistinguishable. Further clarification of clinical risk factors and improved powdered formula safety is needed. ********** Enterobacter sakazakii, a gram-negative bacillus bacillus (bəsĭl`əs), any rod-shaped bacterium or, more particularly, a rod-shaped bacterium of the genus Bacillus. Some bacterium in the genus cause disease, for example B. , is a re cause of bloodstream and central nervous system infections (1-8). The organism has also been associated with necrotizing enterocolitis Necrotizing Enterocolitis Definition Necrotizing enterocolitis is a serious bacterial infection in the intestine, primarily of sick or premature newborn infants. ; however, it has not been firmly established as a causative agent (8-10). Reported outcomes are often severe: seizures; brain abscess; hydrocephalus hydrocephalus (hī'drəsĕf`ələs), also known as water on the brain, developmental (congenital) or acquired condition in which there is an abnormal accumulation of body fluids within the skull. ; developmental delay developmental delay n. A chronological delay in the appearance of normal developmental milestones achieved during infancy and early childhood, caused by organic, psychological, or environmental factors. ; and death in as many as 40%-80% of cases (11). Premature infants are thought to be at greater risk than more mature infants, other children, or adults, and outbreaks of disease have occurred in hospital units for newborns (1,2, 4, 6, 8-10,12). Infant infections with E. sakazakii have been associated with contaminated powdered formula products, but other environmental sources of contamination are possible (1, 3, 9,10,13). In this analysis, we attempt to more clearly define the host risk factors and disease course to refine prevention and treatment efforts. Methods We reviewed the literature for reports of E. sakazakii disease in infants. Using medical subject heading terms "E. sakazakii" or "Enterobacter" in combination with "new-born," "infant," or "meningitis," we searched PubMed and examined the bibliographies of resulting articles. Finally, we reviewed E. sakazakii case consultations conducted by the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. (CDC See Control Data, century date change and Back Orifice. CDC - Control Data Corporation ) from 1998 to 2005 and reviewed results of a French outbreak reported to CDC in 2005 (14). We defined a case as an infant (<12 months of age) with E. sakazakii cultured from an area of the body that is normally sterile: tissue, blood, cerebrospinal fluid cerebrospinal fluid (CSF) Clear, colourless liquid that surrounds the brain and spinal cord and fills the spaces in them. It helps support the brain, acts as a lubricant, maintains pressure in the skull, and cushions shocks. , or urine aspirated through the bladder wall. Infants with cultures of cerebrospinal fluid or brain abscesses yielding E. sakazakii were considered to have meningitis. Because bacteremia is usually an intermediate step during the process of developing meningitis, patients with both bacteremia and meningitis were included in the meningitis group. Bacteremia was defined as E. sakazakii grown from the blood of a case-patient without evidence of meningitis. Infants with gestational ages <37 weeks, or those reported to be premature, were considered premature. A gestational age of 40 weeks was assigned to 3 (27%) of 11 infants with bacteremia and 4 (14%) of 28 infants with meningitis who were reported as born following term gestation without a specific gestational age mentioned. We defined birthweight <2,500 g as low birthweight (LBW LBW Low birth weight, see there ), <1,500 g as very low birthweight (VLBW VLBW Very low birth weight, see there ), and <1,000 g as extremely low birthweight (ELBW ELBW Extremely low birth weight infant, see there ). Descriptive analysis was performed by using SAS (1) (SAS Institute Inc., Cary, NC, www.sas.com) A software company that specializes in data warehousing and decision support software based on the SAS System. Founded in 1976, SAS is one of the world's largest privately held software companies. See SAS System. software (SAS Institute, Cary, NC, USA). Groups were compared by using 2-tailed Fisher exact test. Results Forty-six infants met the case definition (Table 1). Reported onset years ranged from 1958 to 2005; 32 (70%) cases were reported during the second half of this period. Cases were reported in 7 countries in North America, Europe, and the Middle East. Thirty-three (72%) infants had meningitis, 12 (26%) had bacteremia, and 1 (2%) had a urinary tract infection. Clinical characteristics were available for a subset of cases (Table 2). Eight (40%) of 20 infants for whom data were available were delivered by cesarean section cesarean section (sĭzâr`ēən), delivery of an infant by surgical removal from the uterus through an abdominal incision. The operation is of ancient origin: indeed, the name derives from the legend that Julius Caesar was born in this . Twenty-nine (69%) of 42 infants experienced disease onset within a hospital. Gestational duration was available for 38 infants; 21 (55%) were born prematurely, and the median gestational age overall was 36 weeks (range 23.5-40 weeks). The median birthweight was 2,063 g (range 540-3,401); 18 (56%) of 32 infants had LBW; 9 (28%) of these met the definition for VLBW, and 7 (22%) met the definition for ELBW. Median age at the time of infection onset was 8.5 days (range 2-300). Although the proportion of infants who experienced nosocomial nosocomial /noso·co·mi·al/ (nos?o-ko´me-il) pertaining to or originating in a hospital. nos·o·co·mi·al adj. 1. Of or relating to a hospital. 2. disease onset was not significantly different between the meningitis and bacteremia groups, other infant characteristics differed by site of infection (Figure). The median gestational ages of infants with meningitis and bacteremia were 37 and 27.8 weeks, respectively (p = 0.02). Median birthweights were 2,454 g and 850 g, respectively (p = 0.002). However, median age at infection onset was 6 days in the group with meningitis and 35 days in the group with bacteremia (p < 0.0001). Thirty (94%) of 32 infants with meningitis, but only 2 (18%) of 11 infants with bacteremia, were <28 days old when infection was detected. One infant (8%) with bacteremia died; this infant also had necrotizing enterocolitis. The single infant with a urinary tract infection recovered without complication. In contrast, 14 (42%) of 33 infants with meningitis died. Of 19 surviving infants, only those with meningitis suffered adverse outcomes, including brain abscess (21%, p = 0.2), developmental delays (53%, p = 0.004), motor impairment (21%, p = 0.3), and ventricular shunt Ventricular Shunt Definition Ventricular shunt is a surgical procedure in which a tube is placed in one of the fluid-filled chambers inside the brain (ventricles). The fluid around the brain and the spinal column is called the cerebrospinal fluid. placement (42%, p = 0.01); 74% experienced at least one of these outcomes. [FIGURE OMITTED] Feeding practices were described for 26 infants. Twenty-four (92%) received a powdered formula product, including an infant who received powdered breast milk fortifier but no powdered infant formula; 1 additional infant received formula of an unspecified type. E. sakazakii was cultured from formula associated with 15 (68%) of 22 cases investigated. Isolates were obtained from prepared formula, opened formula tins, and previously unopened formula tins associated with 2, 6, and 7 cases, respectively. Thirteen (87%) of the 15 formula isolates were indistinguishable from the corresponding clinical strain by biotype biotype /bio·type/ (bi´o-tip) 1. a group of individuals having the same genotype. 2. any of a number of strains of a species of microorganisms having differentiable physiologic characteristics. or genotype; multiple formula manufacturers were implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. . In one of the remaining cases, multiple E. sakazakii strains were recovered from powdered formula, but none matched the clinical isolate by pulsed-field gel electrophoresis (CDC, unpub, data). In the other case, 2 E. sakazakii strains were isolated from blood and from rectal swabs; a third strain, as determined by arbitrarily primed PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) , was recovered from the powdered infant formula (9). Discussion Although numerous reports include infants with E. sakazakii isolated from nonsterile sites, such as respiratory secretions or stool, 46 infants identified from the literature and CDC sources met the case definition for this analysis (1,9,10,12). Of the infants with sterile-site infection, 72% had meningitis. Contrary to previous characterizations of E. sakazakii disease, we found that infants with meningitis and bacteremia alone fell into 2 distinct groups. Those in whom meningitis developed tended to be of greater gestational age and birthweight than those with bacteremia alone. In fact, infants in whom meningitis developed tended to attain near-term gestational age and birthweight. In contrast, infants in whom bacteremia alone developed tended to be born very prematurely and have ELBW. A second major difference between the group with meningitis and the group with bacteremia was the infants' chronological ages. Infants with meningitis were generally <1 week of age at the onset of infection with E. sakazakii, whereas infants with bacteremia had generally surpassed the neonatal period at the onset of their disease. Rates of adverse outcome also differed between the 2 groups, although this was not unexpected. Most infants with E. sakazakii bacteremia fared better than those with meningitis. Among those in whom meningitis developed, rates of adverse outcome were similar to those reported in the literature: In this case series, 74% of meningitis survivors experienced an adverse neurologic outcome, while other studies cite adverse outcome in 20%-78% of neonatal or infant meningitis survivors (21-23). The division of the infant population into 2 distinct groups occurred for unclear reasons. That infants < 1 week of age comprised the meningitis group was not surprising; the disparities in other infant characteristics, however, are not intuitive. Since infants in the 2 groups experienced similar rates of nosocomial disease onset, the infants with bacteremia were unlikely to have simply received treatment earlier in the disease course than the infants with meningitis. Other risk factors are probable. One likely set of risk factors is infant formula-feeding practices. Powdered infant formula is a demonstrated source of E. sakazakii infection. A microbiologic survey of powdered infant formulas published in 1988 found E. sakazakii in 20 (14%) of 141 samples tested (24). However, a survey of 82 powdered infant formula samples in 2003 yielded E. sakazakii in 2 (2.4%), which suggests that recent rates of powdered formula contamination may be lower (25). Powdered formula has also been implicated both epidemiologically and microbiologically as a vehicle in several cases of E. sakazakii disease in infants (1,3,9,10,13). Although we could not explore feeding exposures fully with the data available in this series, infant feeding practices may relate to the differences we describe in chronological age of infants at onset of meningitis and bacteremia. Infants with nearly normal gestational ages and birthweights are likely to be tended in normal newborn nurseries during the first 24-72 hours of life. In such nurseries, powdered formula is frequently given to babies who are not breast-fed breast·feed or breast-feed v. breast-fed , breast-feed·ing, breast-feeds v.tr. To feed (a baby) mother's milk from the breast; suckle. v.intr. To breastfeed a baby. , and it may also be used as a supplement by mothers who have chosen to breast-feed breast-feed v. To feed a baby mother's milk from the breast; suckle. . Since infants are at highest risk for meningitis during the first several weeks of life, possibly because of immaturity of the blood-brain barrier blood-brain barrier n. Abbr. BBB A physiological mechanism that alters the permeability of brain capillaries so that some substances, such as certain drugs, are prevented from entering brain tissue, while other substances are allowed to , exposures to E. sakazakii in powdered formula or other sources during this time may quickly lead to central nervous system disease (26,27). Conversely, in the intensive care settings where immature and low birthweight infants are tended, babies are not often fed powdered formula in the first few weeks of life. They may be given parenteral nutrition Parenteral nutrition Nutrition supplied intravenously, thus bypassing the patient's digestive tract entirely. Mentioned in: Electrolyte Supplements, Necrotizing Enterocolitis parenteral nutrition initially and may be fed breast milk from their own mothers or from a banked source when they do begin enteral enteral /en·ter·al/ (en´ter'l) enteric. en·ter·al adj. 1. Within or by way of the intestine, as distinguished from parenteral. 2. Enteric. feeds. If breast milk is not available, they are more likely to be given sterile, premixed infant formula than powdered formula, since standard preterm infant preterm infant n. An infant born before the 37th week of gestation. preterm infant Premature infant, see there formula is only available in this form (28). Powdered breast milk fortifiers are not introduced until premature infants tolerate full-volume feeds, which may not occur for days or weeks after birth. Thus, infants in intensive care settings may not be exposed to nonsterile formula until they are more mature, which would lead to a greater proportion of E. sakazakii bacteremia than meningitis in this group if powdered formula is a source of infection. In this series, we were unable to explore the roles of indwelling indwelling /in·dwell·ing/ (in´dwel-ing) pertaining to a catheter or other tube left within an organ or body passage for drainage, to maintain patency, or for the administration of drugs or nutrients. enteric enteric /en·ter·ic/ (en-ter´ik) within or pertaining to the small intestine. en·ter·ic adj. 1. Of, relating to, or within the intestine. 2. tubes, prior gastrointestinal surgery, and antecedent antacid antacid, any one of several basic substances that counteract stomach acidity (see stomach). Antacids are used by physicians to treat hyperchlorhydria, i.e., the excessive production of hydrochloric acid by the parietal cells lining the stomach. or antimicrobial drug use as risk factors for infection. While the reservoir for E. sakazakii is unknown, several environmental sources have been reported. E. sakazakii has been isolated from factories used to produce milk powder, chocolate, cereal, potato flour, spices, and pasta (29). It also has been isolated from household vacuum cleaner bags and from the guts of the stable fly, Stomoxys calcitrans Stomoxys calcitrans the ubiquitous stable fly, about house fly size, and a pest wherever horses are. It is a blood-sucker and transmits a number of trypanosomes including Trypanosoma evansi (Surra), T. equinum (Mal de Caderas), T. brucei and T. , and the Mexican fruit fly, Anastrpha ludens (29-31). The relationship between these potential environmental sources and infant disease remains unclear. Although a human vaginal tract culture yielding E. sakazakii has been reported, vertical transmission is unlikely because nearly half of infants with E. sakazakii disease in this review were delivered by cesarean section, and symptoms developed in only 1 infant earlier than 3 days of age (32). Our analyses were constrained by the use of retrospective and often incomplete data. Although cases with more severe outcomes might have been investigated and published more frequently than uncomplicated cases, this possible bias would not likely affect the representativeness of baseline infant characteristics. Assigning a gestational age of 40 weeks to term infants without a reported gestational age may have falsely elevated the median gestational ages we report, since most term infants are born at <40 weeks' gestation (33). However, a greater proportion of bacteremic bac·te·re·mi·a n. The presence of bacteria in the blood. bac  te·re infants than meningitic infants
received this assignment, and therefore the significance of the
differences in gestational age between the groups may be even greater
than we report. We were unable to explore the effects of concomitant
medical problems, treatments, and other environmental factors, and we
relied on existing reports of feeding practices and formula testing.
Clearly, additional study is needed to elucidate the lingering questions
about E. sakazakii reservoirs, disease risk factors, and disease course.Other gram-negative organisms, including Escherichia coli Escherichia coli (ĕsh'ərĭk`ēə kō`lī), common bacterium that normally inhabits the intestinal tracts of humans and animals, but can cause infection in other parts of the body, especially the urinary tract. Enterobacter agglomerans, E. cloacae, Klebsiella pneumoniae Klebsiella pneu·mo·ni·ae n. Friedlander's bacillus. , K. oxytoca, and Citrobacter freundii Citrobacter freundii Microbiology A Citrobacter opportunistic pathogen Management Cephalothin, aminoglycosides , can be found in powdered infant formula (24,25). Powdered infant formula also has been associated with outbreaks of illness due to Citrobacter and multiple Salmonella serotypes (13,34-38). The degree to which E. sakazakii is a marker for a range of neonatal infections possibly related to powdered infant formula remains to be defined. Certain steps can be taken immediately, however, to prevent or mitigate E. sakazakii disease. In a joint conference on infant formula safety in February, 2004, the World Health Organization and Food and Agriculture Organization of the United Nations Noun 1. Food and Agriculture Organization of the United Nations - the United Nations agency concerned with the international organization of food and agriculture FAO, Food and Agriculture Organization made the following recommendations: 1) encourage industry partners to develop a range of affordable sterile formula options; 2) consider setting an industry standard for Enterobacteriaecae and E. sakazakii in infant formula; 3) inform infant caregivers of the risks associated with nonsterile, powdered formula; and 4) consider feeding high-risk infants sterile formula if they cannot breast-feed (39). The findings of our case review suggest that all neonates as well as premature infants should be included in this high-risk infant category. The American Dietetic Association The American Dietetic Association (ADA) is the United States' largest organization of food and nutrition professionals, with nearly 65,000 members. Approximately 75 % of ADA's members are registered dietitians and about 4 % are dietetic technicians, registered. has issued guidelines for infant formula preparation, storage, and administration; these should be followed by infant caregivers in hospitals and private homes (40). Rapid reporting of cases by clinicians could streamline data collection by local health departments and more rapidly resolve remaining questions about this illness. Manufacturer warning labels on powdered infant formula packages should stress that powdered infant formula is nonsterile and requires proper preparation, handling, and storage, and that sterile, liquid formula alternatives are available. These actions, adopted in whole or in part, may decrease the infectious risks associated with powdered formula and prevent this rare but potentially devastating dev·as·tate tr.v. dev·as·tat·ed, dev·as·tat·ing, dev·as·tates 1. To lay waste; destroy. 2. To overwhelm; confound; stun: was devastated by the rude remark. disease. Acknowledgments Thanks to L. Clifford McDonald, Matthew Kuehnert, and R. Mike Hoekstra for their unflagging technical support and to Matthew Arduino, Terri Forster, and Bette Jensen for sharing their laboratory expertise. All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is required. Use of trade names is for identification only and does not imply endorsement by the Public Health Service or by the U.S. Department of Health and Human Services Noun 1. Department of Health and Human Services - the United States federal department that administers all federal programs dealing with health and welfare; created in 1979 Health and Human Services, HHS . References (1.) Centers for Disease Control and Prevention. Enterobacter sakazakii infections associated with the use of powdered infant formula--Tennessee, 2001. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg, Morb Mortal Wkly Rep. 2002;51: 297-300. (2.) Bar-Oz B, Peleg O, Block C, Arad I. Enterobacter sakazakii infection in the newborn. Acta Paediatr. 2001;90:356-8. (3.) Biering G, Karlsson S, Clark N, Jonsdottir K, Ludvigsson P, Steingrimsson O. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. J Clin Microbiol. 1989;27:205445. (4.) Block C, Peleg O, Minster N, Bar-Oz B, Simhon A, Arad I, et al. Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Eur J Clin Microbiol Infect Dis. 2002;21:613-56. (5.) Joker RN, Norholm T, Siboni KF. A case of neonatal meningitis caused by a yellow Enterobacter. Dan Med Bull. 1965;12:128-30. (6.) Lai KK. Enterobacter sakazakii infections among neonates, children, and adults. Medicine. 2001;80:113-22. (7.) Monroe PW, Tift WL. Bacteremia associated with Enterobacter sakazakii (yellow pigmented Enterobacter cloacae). J Clin Microbiol. 1979;10:850-1. (8.) Muytjens HL, Zanen H, Sonderkamp H, Kollee L, Wachsmuth I, Farmer J. Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J Clin Microbiol. 1983; 18:115-20. (9.) Van Acker J, de Smet F, Muyldermans G, Bougatef A, Naessens A, Lauwers S. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. 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Infections severes a Enterobacter sakazakii chez chez prep. At the home of; at or by. [French, from Old French, from Latin casa, cottage, hut.] chez prep at the home of [French] des nouveau-nes ayant consomme une preparation en poudre pour nourrissons, France, octobre-decembre 2004. Available from: http://www.invs.sante.fr/BEh/2006/02_03/beh_02_03_2006.pdf. (15.) Urmenyi AM, Franklin AW. Neonatal death from pigmented coliform coliform /col·i·form/ (kol´i-form) pertaining to fermentative gram-negative enteric bacilli, sometimes restricted to those fermenting lactose, e.g., Escherichia, Klebsiella, or Enterobacter. infection. Lancet. 1961;1:313-5. (16.) Kleiman MB, Allen SD, Neal P, Reynolds J. Meningoencephalitis meningoencephalitis /me·nin·go·en·ceph·a·li·tis/ (me-ning?go-en-sef?ah-li´tis) inflammation of the brain and meninges. toxoplasmic meningoencephalitis and compartmentalization of the cerebral ventricles caused by Enterobacter sakazakii. J Clin Microbiol. 1981;14:352-4. (17.) Naqvi SH, Maxwell MA, Dunkle LM. Cefotaxime therapy of neonatal gram-negative bacillary bacillary /bac·il·la·ry/ (bas´i-lar?e) pertaining to bacilli or to rodlike structures. bac·il·lar·y or ba·cil·lar adj. 1. Shaped like a rod. 2. meningitis. Pediatr Infect Dis. 1985;4:499-502. (18.) Lecour H, Seara J, Miranda M. Treatment of childhood bacterial meningitis. Infection. 1989; 17:343-6. (19.) Noriega FR, Kotloff KL, Martin MA, Schwalbe RS. Nosocomial bacteremia caused by Enterobacter sakazakii and Leuconostoc mesenteroides resulting from extrinsic EVIDENCE, EXTRINSIC. External evidence, or that which is not contained in the body of an agreement, contract, and the like. 2. It is a general rule that extrinsic evidence cannot be admitted to contradict, explain, vary or change the terms of a contract or of a contamination of infant formula. Pediatr Infect Dis J. 1990;9:447-9. (20.) Gallagher PG, Ball WS. Cerebral infarctions due to CNS See Continuous net settlement. CNS See continuous net settlement (CNS). infection with Enterobacter sakazakii. Pediatr Radiol. 1991;21:135-6. (21.) Stevens JP, Eames M, Kent A, Halket S, Holt D, Harvey D. Long term outcome of neonatal meningitis. Arch Dis Child Fetal Neonatal Ed. 2003;88:F179-84. (22.) Bedford H, de Louvais J, Halket S, Peckham C, Hurley R, Harvey D. Meningitis in infancy in England and Wales England and Wales are both constituent countries of the United Kingdom, that together share a single legal system: English law. Legislatively, England and Wales are treated as a single unit (see State (law)) for the conflict of laws. : follow up at age 5 years. BMJ BMJ n abbr (= British Medical Journal) → vom BMA herausgegebene Zeitschrift . 2001;323:533-6. (23.) Harvey D, Holt D, Bedford H. Bacterial meningitis in the newborn: a prospective study of morbidity and mortality Morbidity and Mortality can refer to:
(24.) Muytjens HL, Roelofs-Willemse H, Jaspar GH. Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. J Clin Microbiol. 1988;26:743-6. (25.) Iversen C, Forsythe S. Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant formula milk and related products. Food Microbiol. 2004;21:771-7. (26.) Schuchat A, Robinson K, Wenger J, Harrison L, Farley M, Reingold A, et al. Bacterial meningitis in the United States in 1995. N Engl J Med. 1997;337:970-6. (27.) Wenger JD, Hightower AW, Facklam RR, Gaventa S, Broome CV. Bacterial meningitis in the United States, 1986: report of a multistate surveillance study. J Infect Dis. 1990;162:1316-23. (28.) Current marketing and use of powdered infant formula in the United States, 2003, US Food and Drug Administration. Available from http://www.fda.gov/ohrms/dockets/ac/03/briefing/3939b1_tab4c_cov ersheet.pdf (29.) Kandhai MC, Reij MW, Gorris LG, Guillaume-Gentil O, van Schothorst M. Occurrence of Enterobacter sakazakii in food production environments and households. Lancet. 2004;363:39-40. (30.) Hamilton JV, Lehane MD, Braig HR. Isolation of Enterobacter sakazakii from midgut midgut /mid·gut/ (mid´gut) the region of the embryonic digestive tube into which the yolk sac opens and which gives rise to most of the intestines; ahead of it is the foregut and caudal to it is the hindgut. of Stomoxys calcitrans. Emerg Infect Dis. 2003;9:1355-6. (31.) Kuzina LV, Peloquin J J, Vacek DC, Miller TA. Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens. Curr Microbiol. 2001;42:290-4. (32.) Ongradi J. Vaginal infection by Enterobacter sakazakii. Sex Transm Infect. 2002;78:467-8. (33.) Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2002. Natl Vital Star Rep. 2003;52:1-113. PMID PMID PubMed-Indexed for MEDLINE PMID Portable Multispectral Imaging Device PMID Process Management Improvement & Deployment PMID Physical Media Id PMID Performance Metric Identifier : 14717305 (34.) Collins RN, Treger MD, Goldsby JB, Boring JR, Coohon DB, Barr RN. Interstate outbreak of Salmonella newbrunswick infection traced to powdered milk. JAMA JAMA abbr. Journal of the American Medical Association . 1968;203:838-44. (35.) Thurm V, Gericke B. Identification of infant food as a vehicle in a nosocomial outbreak of Citrobacter freundii: epidemiological sub-typing by allozyme, whole-cell protein and antibiotic resistance. J Appl Bacteriol. 1994;76:553-8. (36.) Usera MA, Echeita A, Aladuena A, Blanco MC. Reymundo R, Prieto MI, et al. Interregional in·ter·re·gion·al adj. Of, involving, or connecting two or more regions: interregional migration; interregional banking. foodborne salmonellosis salmonellosis (săl'mənĕlō`sĭs), any of a group of infectious diseases caused by intestinal bacteria of the genus Salmonella, outbreak due to powdered infant formula contaminated with lactose-fermenting Salmonella virchow. Enr J Epidemiol. 1996;12:377-81. (37.) Threlfall EJ, Ward LR, Hampton MD, Ridley AM, Rowe B, Roberts D, et al. Molecular fingerprinting defines a strain of Salmonella enterica serotype anatum responsible for an international outbreak associated with formula-dried milk. Epidemiol Infect. 1998;121:289-93. (38.) Rowe B, Begg N, Hutchinson D, Dawkins H, Gilbert R, Jacob M, et al. Salmonella Ealing infections associated with consumption of infant dried milk. Lancet. 1987;2:900-3. (39.) Enterobacter sakazakii and other microorganisms in powdered infant formula: meeting report. In: Microbiological risk assessment series, no. 6. Geneva Geneva, canton and city, Switzerland Geneva (jənē`və), Fr. Genève, canton (1990 pop. 373,019), 109 sq mi (282 sq km), SW Switzerland, surrounding the southwest tip of the Lake of Geneva. : World Health Organization; 2004. (40.) American Dietetic Association. Infant feedings: guidelines for preparation of formula and breast milk in health care facilities, 2003, Washington: American Dietetic Association; 2004. Anna B. Bowen * and Christopher R. Braden * * Centers for Disease Control and Prevention, Atlanta, Georgia, USA Dr Bowen is a medical epidemiologist in the Foodborne and Diarrheal Diseases Branch at CDC. Her primary research interests include global infant feeding safety, hygiene, sanitation, and diarrheal diseases in the developing world. Dr Braden is a medical epidemiologist in the Foodborne and Diarrheal Diseases Branch at CDC. His main areas of interest are the surveillance and epidemiology of foodborne diseases. Address for correspondence: Anna B. Bowen, Foodborne and Diarrheal Diseases Branch, Centers for Disease Control and Prevention, 1600 Clifton Rd, Mailstop A38, Atlanta, GA 30333, USA. email: abowen@ edc.gov
Table 1. Cases of invasive Enterobacter sakazakii disease
among infants
Year of Location No. Reference
report cases
1961 England 2 (15)
1965 Denmark 1 (5)
1979 Georgia, USA 1 (7)
1981 Indiana, USA 1 (16)
Oklahoma, USA 1
1983 Netherlands 8 (8)
1985 Missouri, USA 1 (17)
1988 USA 2
1989 Portugal 1 (18)
Iceland 3 (3)
Tennessee, USA 3 (10)
1990 Maryland, USA 1 (19)
1991 Ohio, USA 1 (20)
2000 North Carolina, USA 1
2001 Israel 2 (2,4)
Belgium 1 (9)
2002 Israel 2 (4)
Tennessee, USA 1 (1)
Wisconsin, USA 1 CDC, unpub. data
2003 USA 6 CDC, unpub. data
2004 France 2 (14)
USA 2 CDC, unpub. data
2005 USA 2 CDC, unpub. data
Table 2. Characteristics of infants in the Enterobacter sakazakii
case series
Characteristic Published Unpublished
cases, n/N cases, n/N Overall %
Male 15/30 6/9 54
Cesarean delivery 6/13 2/7 40
Nosocomial onset 24/31 5/11 69
Premature birth 17/29 4/9 55
Birthweight *
LBW 16/27 2/5 56
VLBW 8/27 1/5 28
ELBW 6/27 1/5 22
* LBW, low birth weight; VLBW, very low birth weight; ELBW, extremely
low birth weight.
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