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PEDIATRICS Vol. 111 No. 6 June 2003, pp. 1442-1446

EXPERIENCE AND REASON

Transmission of Salmonella enterica Serotype Typhimurium DT104 to Infants Through Mother’s Breast Milk

Salah S. Qutaishat, PhD, Mary E. Stemper, MS, Susan K. Spencer, BS, Mark A. Borchardt, PhD, James C. Opitz, MD, Timothy A. Monson, MS, Jennifer L. Anderson, BS and Jay L. E. Ellingson, PhD

Saint Joseph’s Hospital, Marshfield, WI 54449
Marshfield Laboratories, Marshfield Clinic, Marshfield, WI 54449
Marshfield Medical Research Foundation, Marshfield, WI 54449
Department of Pediatrics, Marshfield Clinic, Marshfield, WI 54449
Communicable Disease Division, Wisconsin State Laboratory of Hygiene, Madison, WI 53706
Food Safety Services, Marshfield Clinic, Marshfield, WI 54449


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 CASE REPORT AND LABORATORY...
 DISCUSSION
 REFERENCES
 
This study documents the first reported transmission of Salmonella enterica serotype Typhimurium definitive type 104 (DT104) to premature fraternal twins via their mother’s breast milk. When premature twin neonates developed severe enteritis in the neonatal intensive care unit (NICU), stool samples and the mother’s breast milk were cultured for the presence of Salmonella. Antibacterial susceptibility patterns were determined. Semiquantitative organism abundance data were retrospectively gathered on 54 stored breast milk samples collected on 34 different days using a rapid, real-time polymerase chain reaction (PCR) methodology (LightCycler PCR). Fecal samples from other infants in the NICU at that time were also tested. Pulsed-field gel electrophoresis (PFGE) was used to assess the genetic composition of the isolated organisms. The twins’ neonatal stools and mother’s breast milk cultures revealed a resistance pattern (R-type) to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline. LightCycler PCR analysis of sequential breast milk samples confirmed this to be the likely source of transmission. In the subsequent outbreak investigation, none of the NICU surveillance fecal samples proved positive for this organism. The genetic composition of organisms isolated from the maternal breast milk was indistinguishable from those isolated from neonatal specimens as determined by PFGE. Antibiotic susceptibility tests coupled with PFGE patterns suggested that these Salmonella isolates were DT104. Because the prevalence of DT104 infections is rising in the United States, neonatologists should be aware of breast milk as a potential mode of transmission.

Key Words: Salmonella enterica serotype Typhimurium DT104 • breast milk • neonatal infection • antibacterial susceptibility • real-time PCR • LightCycler • pulsed-field gel electrophoresis • outbreak

Abbreviations: NICU, neonatal intensive care unit • DT104, definitive type 104 • PCR, polymerase chain reaction • ACSSuT, ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline • PFGE, pulsed-field gel electrophoresis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
CASE REPORT AND LABORATORY...
 DISCUSSION
 REFERENCES
 
Serious human neonatal viral and bacterial infections can occasionally be acquired through breast milk.1–3 Documented cases of tuberculosis,4 hepatitis B,4 cytomegalovirus,5 human immunodeficiency virus,4,6 herpes simplex,7 Epstein-Barr virus,8 West Nile virus,9 Listeria,10 Leptospirosis,11 brucellosis,12 and group B Streptococcus13 have been demonstrated to be transmitted by this mechanism. In addition, human breast milk has been responsible for several Salmonella outbreaks in neonatal intensive care units (NICUs).3,14–18 Salmonella kottbus has been reported in association with banked donor breast milk.14,18 Salmonella senftenberg15 and Salmonella enterica serotype Typhimurium16,17 are both transmissible through breast milk.

We present the case of fraternal twin infants who developed serious sepsis involving multidrug-resistant Salmonella enterica serotype Typhimurium definitive type 104 (DT104). The etiology of this infection was traced through standard laboratory culture methods and the use of a rapid, semiquantitative polymerase chain reaction (PCR) method for the detection of infectious Salmonella species. Although several outbreaks of the DT104 serotype have been linked to consumption of dairy products,19,20 to our knowledge this is the first report in the literature to describe the transmission of Salmonella enterica serotype Typhimurium DT104 via human breast milk.


   CASE REPORT AND LABORATORY INVESTIGATIONS
TOP
 ABSTRACT
 INTRODUCTION
 CASE REPORT AND LABORATORY...
DISCUSSION
 REFERENCES
 
Fraternal twins were delivered by cesarean section at 29 weeks’ gestation with birth weights of 680 g (male) and 685 g (female). On day 3 postpartum, the mother developed fever secondary to endometritis and was treated with ampicillin and gentamicin. On day 16 postdelivery the female twin developed lethargy and hemorrhagic enteritis. Blood and urine specimens tested positive for Gram-negative bacilli, which were confirmed to be Salmonella enterica serotype Typhimurium. The male twin became symptomatic on day 19, and fecal and blood cultures subsequently revealed the same organism. Fecal samples obtained from the mother were negative; however, Salmonella enterica serotype Typhimurium was isolated from her breast milk.

Breast milk samples were cultured for Salmonella using the method described for liquid milk in the Bacteriologic Analytical Manual for the US Food and Drug Administration.21 Antimicrobial susceptibility testing of isolates from the 2 infants and the mother’s breast milk were resistant (R-type) to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (ACSSuT).

The mother remained asymptomatic throughout the entire observation period. Antimicrobial therapy was initiated in both the infants (rifampin, cefotaxime, and tobramycin) and the mother (ciprofloxacin). The infants were critically septic and required ventilator support, but did respond to antimicrobial therapy. Both infants survived. Although the twins were asymptomatic after hospital discharge, they continued to shed the organisms for up to 6 months after birth. No follow-up data were available thereafter.

To confirm the source of this neonatal infection, a full laboratory investigation was initiated. As with all premature deliveries, the mother was encouraged to continue to collect and store breast milk to maintain lactation for later feeding of the infants. The mother complied, and milk specimens were collected daily from the time of birth and throughout the course of the study. Breast milk was collected by the mother using 2 separate mechanical pumps and stored frozen. Breast milk was collected either at the hospital or in the mother’s home. Specimens received no special handling or treatment and were selected randomly from either collection site for analysis. Fifty-four breast milk samples collected on 34 different days were tested for Salmonella in this study. Daily samples were selected randomly from those collected and stored at the hospital or at the mother’s home.

Bacterial DNA was extracted from human breast milk samples and positive control Salmonella preparations using the Qiagen QIAamp DNA mini kit (Qiagen, Inc, Valencia, CA) according to the manufacturer’s instructions. Positive control DNA samples were prepared by adding 105 Salmonella organisms to known negative human breast milk samples. Series of dilutions of the extracted DNA (102, 103, 104) were prepared for testing. DNA samples were amplified and quantitated using a Roche LightCycler-DNA master hybridization probes kit (Roche Molecular Biochemicals, Mannheim, Germany). The LightCycler obtains semiquantitative data by comparing the fluorescence values of a PCR product of unknown concentration in the log-linear phase of amplification, to the fluorescence of positive control standards included in each experiment. In this assay fluorescence occurs only when the probe binds to Salmonella DNA in the sample. To confirm that the amplified product was the targeted amplicon sequence, Salmonella-specific hybridization probes were used that demonstrated no cross-reactivity with any other species tested. The 54 samples were simultaneously analyzed by standard culture techniques. Presence/absence results were concordant between the 2 methods.

The relative number of Salmonella enterica serotype Typhimurium genomic copies detected in the mother’s breast milk samples (days 11–18 postdelivery) is shown in Fig 1. Milk samples collected outside this period were negative for the presence of Salmonella. The female twin became symptomatic on day 16 postdelivery and the male twin became symptomatic 3 days later.


Figure 1
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  		Fig 1. Number of Salmonella enterica serotype Typhimurium genomic copies in daily breast milk samples.

 
Bacterial DNA was prepared and analyzed by pulsed-field gel electrophoresis (PFGE) using a modification of the method previously described by the Centers for Disease Control and Prevention.22 The genetic profiles of the organisms isolated from maternal and neonatal specimens were indistinguishable by PFGE and were consistent with the unique genotype seen among multidrug-resistant Salmonella enterica serotype Typhimurium (Fig 2).


Figure 2
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  		Fig 2. Patterns of pulsed-field gel electrophoresis of isolates of Salmonella enterica serotype Typhimurium from stool and blood samples of twin neonates and breast milk from the mother. Lanes 1, 7, 14, 20: Salmonella enterica serotype Newport am01144 markers (M); lane 2: twin A blood; lane 3: twin A feces; lane 4: twin B blood; lane 5: twin B feces; Lanes 6, 8 to 13, 15 to 17: mother’s breast milk; lane 18: Salmonella enterica Typhimurium ATCC 14028; lane 19: Salmonella enterica Typhimurium (R-type ACSSuT from the Minnesota Department of Health—MDH designation TM5b).

 
To rule out nosocomial transmission from other infants in the NICU, stool samples of all 16 neonates present in the NICU were tested for the presence of Salmonella by culture 1 week after the organism was isolated from the index cases. Only stool samples obtained from the twins described in this report were positive for Salmonella.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 CASE REPORT AND LABORATORY...
 DISCUSSION
REFERENCES
 
This study presents evidence that human breast milk served as the source of transmission of Salmonella enterica serotype Typhimurium from a mother to her premature fraternal twin neonates. Salmonella was first detected in blood and urine samples of the female twin 16 days after birth. This triggered an epidemiologic investigation to identify the source of transmission. The investigation involved performing surveillance cultures of stool and blood samples on the index patient (female twin), the male twin, and stool and breast milk samples from the mother. In addition, a point prevalence study was performed on all patients in the NICU. This included testing stool samples from all patients in the NICU 1 week after identification of the infection in the index case. We further expanded the investigation to include the semiquantitative testing of a large number of stored breast milk samples by real-time LightCycler PCR to confirm the transmission source.

The organism that was cultured from the neonatal blood and urine samples and mother’s breast milk exhibited multidrug resistance (ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline), identifying it as an R-type ACSSuT strain. The DT104 designation was based on 2 criteria: the susceptibility pattern and the PFGE pattern. In a recent study of 270 isolates with R-type ACSSuT, phage typing determined that 80.4% were DT104, 6.7% were DT12, 4.1% were DT120, and the remainder were other or unknown phage types.23 Recent studies24,25 have shown that certain unique PFGE patterns are associated with DT104. In our study, the breast milk isolate was indistinguishable by PFGE from a Salmonella enterica Typhimurium isolate from an epidemiologically unrelated source (Fig 2, lane 19). This isolate’s PFGE type (Minnesota Department of Health designation: TM5b) is always DT104 (Dave Boxrud, personal communication, August 2002). This evidence suggests that the breast milk isolate is DT104.24–27

The evidence strongly suggests that the presence of Salmonella enterica serotype Typhimurium in the mother’s breast milk originated from a maternal systemic infection as opposed to an environmental contamination source. Poor maternal hygiene was not likely to be a factor in that culture-positive samples had been collected both in the hospital and at home. Although lax maternal hygiene may be a suspected source of contamination in the home environment, hygienic contamination was far less likely in a monitored hospital setting.

The same argument holds for unclean breast pumps. Culture-positive breast milk samples were collected from both hospital pumps and the home pump, as were culture-negative samples. Finally, if maternal hygiene and home pump contamination were at play, one would have expected recurrence of the infection in the infants after release from the hospital, which did not occur. The fact that only the twins and none of the other neonates in the NICU tested positive for Salmonella further suggests a direct transmission route to the twins, rather than by contaminated hospital equipment.

The most compelling argument against external contamination, however, is the temporal pattern of the Salmonella concentration in the milk shown by the quantitative PCR data. The same Salmonella enterica Typhimurium genotype was isolated only from milk samples collected over 8 consecutive days out of a total of 34 consecutive days sampled. The pattern of organism contamination suggests a continuous rise and fall only over a week’s time, as illustrated in Fig 1. On day 11 postpartum, the milk tested positive for Salmonella, but quantitation was low. Thereafter, the milk concentration increased, peaking from days 13 through 17 and then dropped to undetectable levels after 19 days. This pattern is consistent with an infection course of colonization, pathogen growth, and immune response, and is a hallmark of a systemic bacterial bloom, rather than sporadic contamination. If there had been external contamination, one would have expected an intermittent pattern of Salmonella isolation in the breast milk with at least some overlap with antibiotic treatment. This was not the case, however. The bacteria were present in milk samples only after the woman had completed a course of antibiotics.

This is not the first report of Salmonella enterica serotype Typhimurium being passed through human breast milk.3–18 The most compelling case was reported by Fleishrocker et al17 in which a very similar instance of transmission was recorded from maternal breast milk to an infant. This is, however, the first reported case of an apparent transmission of the DT104 strain being transmitted through breast milk.

There is a biologically feasible mechanism of transport of Salmonella from the gastrointestinal tract to breast milk. Salmonella are resistant to the acidic environment of the stomach and usually invade or are phagocytosed by cells lining Peyer’s patches in the small intestine.28 Specialized epithelial M cells overlying the lymphoid follicles of Peyer’s patches provide a portal of entry for Salmonella enterica Typhimurium. Penetration of these intestinal M and epithelial cells by Salmonella enterica Typhimurium requires an invasion gene: Salmonella Pathogenicity Island 1. Salmonella enterica Typhimurium is transported from the gastrointestinal tract to the bloodstream by CD18-expressing phagocytic leukocytes, and may use macrophages and dendritic cells as a conduit to deeper tissue.29 Salmonella enterica Typhimurium replicates within macrophages. A specific regulatory system that controls the synthesis of many Salmonella proteins required for virulence and survival within macrophages is one mechanism that this particular intracellular pathogen has evolved to resist host clearance.30,31 The colonization of the mammary gland during lactation by the immune system cells is the result of a selective homing process regulated by lactogenic hormones.32,33 Immune cells are abundant in human colostrum and milk. Most cells are phagocytic neutrophils and macrophages. Macrophages make up some 40% of all leukocytes in colostrums.34 Counts for macrophages, neutrophils, and lymphocytes are significantly higher in preterm colostrum and milk, as compared with full-term colostrum and milk.35 In our patient, after the birth of the twin infants, the abundance of DT104 peaked 13 to 15 days after the delivery of the preterm infants, who then became ill on days 16 and 19, coinciding with the characteristic 2- to 3-day incubation period for this organism. Again, this pattern is consistent with an infection course of colonization, pathogen growth, and immune response.

The question arises as to why the mother was an apparent asymptomatic carrier of DT104. She exhibited no signs of either gastroenteritis or mastitis. It has been shown that this form of Salmonella behaves in humans more like it does in cattle than it does in mice.28 If so, there may be an explanation. Cattle exhibit a subacute form of the disease, where there may be few symptoms at the time of infection. However, under stress (such as during calving or with the development of another disease) the activity of the bacteria is triggered, resulting in an acute case.35 Milk from infected cattle can then transmit the organism.19,20

This case is of particular interest because the mother had been employed at a local dairy farm and reported contact with calves infected with Salmonella on that farm. She chose not to disclose her employer’s identity. Thus, it was not possible to investigate further this potential source of exposure. It remains possible that this woman may have become infected with DT104 while working with these cattle.36 Although DT104 infections can be severe in the elderly and very young, in most healthy individuals DT104 infections are mild and self-limited.37 She may, therefore, have been harboring a latent or occult infection.

What, then, may have been the stressor? Endometriosis itself is rarely associated with a Salmonella infection;38 however, it may be that the stress of surgery and subsequent endometriosis may have been enough to trigger an acute episode of an otherwise latent infection. On activation, it appears evident in this case that, as in dairy cattle, the breast milk served as a portal for transmission of the organism.

In analyzing the samples for this study, we found that the real time PCR (Roche LightCycler) technique was useful in rapidly and efficiently obtaining semiquantitative estimates of the DT104 levels in these samples. This technique has advantages over traditional culturing and standard PCR techniques, and should find wider application in the future. The application of PFGE to this case demonstrated that the organisms isolated from the maternal breast milk and those isolated from different biological specimens obtained from the neonates were genetically indistinguishable.

Salmonella in general causes an estimated 800 000 to 4 million human infections each year in the United States, and ~25% of these are serotype Typhimurium.20 The multidrug-resistant DT104 strain first appeared in this country in the 1990s and has been on the rise ever since. In 1990, DT104 accounted for <1% of isolates, and by 1996 it accounted for 34% of isolates.20 By 1999, DT104 was the second most prevalent type of Salmonella isolated from humans in England, and the prevalence rate in the United States appears to be lagging 5 to 10 years behind that in the United Kingdom.20 Its occurrence as a foodborne pathogen, its multiple-drug resistance, and its enhanced virulence in the very young and very old make it a particularly worrisome emerging infectious disease. Our study should alert infection control personnel to potential cases of breast milk transmission, such that more complete proof of this mechanism can be gathered through more timely direct collection of breast milk expressed under sterile conditions. Our demonstration of the likely transmission of DT104 to neonates through breast milk should also serve to alert neonatologists to this as a potential source of neonatal Salmonella infections.


   ACKNOWLEDGMENTS
 
We wish to thank Marshfield Medical Research Foundation for its support through the assistance of Alice Stargardt, Doreen Luepke, and Graig Eldred in the preparation of this manuscript. We also thank Dirk Vevea and Mary Vevea for technical assistance.


   FOOTNOTES
 
Received for publication Sep 9, 2002; Accepted Dec 12, 2002.

Reprint requests to (S.S.Q.) Saint Joseph’s Hospital, 611 Saint Joseph Ave, Marshfield, WI 54449. Email: qutaishs{at}stjosephs-marshfield.org


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 DISCUSSION
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PEDIATRICS (ISSN 1098-4275). ©2003 by the American Academy of Pediatrics

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