https://orcid.org/0000-0001-8597-4645
Abstract
Objective
Listeriosis is a foodborne disease that occurs in immunocompromised patients. Pregnant women are a high-risk group for the disease. Listeria infection during pregnancy is uncommon in China because of dietary habits, with little clinician attention and minimal therapeutic options due to its population-specific nature.This article studies the clinical characteristics of Listeria infection in pregnant women and the improvement of treatment methods.
Subjects
This study collected clinical data from 16 cases of pregnant patients with laboratory-confirmed Listeria monocytogenes infections at the Women and Children's Hospital of Jiaxing University. These data were combined with 77 cases that were reported in the literature for a total of 93 cases of Listeria monocytogenes infection in pregnancy that occurred in China over a 15-year interval.
Methods
We collected the clinical data of 16 pregnant patients with listeriosis diagnosed in the laboratory of the Women and Children's Hospital of Jiaxing University from May 2013 to December 2020, and combined it with 77 cases of Listeria monocytogenes during pregnancy in China obtained from a literature search. We summarized the clinical features of listeriosis in pregnancy infection and investigated its treatment methods and prevention.
Results
Ninety-three cases of Listeria monocytogenes infection in pregnancy occurred in early, middle and late pregnancy in 31, 27, and 35 patients, respectively. The initial clinical presentation was fever in 90 patients, intermittent lower abdominal pain in 50 patients, and abnormal fetal movement and/or abnormal fetal heartbeat in 27 cases. Specimens with a positive bacterial culture included the following: 6 amniotic fluid cultures, 35 blood cultures, 37 maternal placenta and uterine secretion cultures, and 15 neonatal blood cultures. Fifty-seven cases of placental pathology, all showing of neutrophil infiltration, were 100% consistent with acute chorioamnionitis. Fifty-eight patients were initially treated with cephalosporin antibiotics, and only 24 cases were initially treated with broad-spectrum penicillins to cover the pathogenic bacteria. Drug sensitivity tests revealed resistant strains, 15 penicillin G-resistant, 14 oxacillin-resistant, and 13 ampicillin-resistant strains. After penicillin failure, vancomycin or meropenem was given. Maternal outcomes included the following: 20 cases of sepsis, 3 cases of pneumonia, 6 cases of acute pyelonephritis, 28 cases of intrauterine infection, 2 cases of multiple organ dysfunction syndromes, and 1 case of septic shock. The fetal and neonatal outcomes were as follows: 16 cases of abortion, 16 cases of intrauterine fetal death, 22 cases of death after birth, and 39 cases of cure.
Conclusion
In our study and reported cases, Listeria monocytogenes in pregnancy is associated with fever as the primary manifestation, a high incidence of adverse pregnancy outcomes, and a significant increase in fetal and neonatal mortality. The low coverage of practical use of antimicrobial drugs and the emergence of drug-resistant strains in recent years have increased the difficulty of treatment, suggesting the need for clinicians to raise awareness of the disease and strengthen healthy diet promotion for women in pregnancy.
1. Background
Listeriosis is a foodborne zoonotic infection caused by Listeria monocytogenes (LM). Although the incidence of invasive disease caused by LM is relatively low, the morbidity and mortality rates are as high as 20–30% [Citation1]. Groups that are susceptible to LM mainly include the elderly, immunocompromised individuals, pregnant women, and newborns. The risk of infection with L. monocytogenes during pregnancy is 13–100 times higher than that of the average population [Citation2]. The incidence of miscarriage and premature birth in women with LM infection during pregnancy varies from 2.4 cases per 1,000 pregnancies to 5.5 cases per 1,000 pregnancies, and the incidence of LM in newborns is nearly 0.52 per 1,000 births [Citation3]. It can be transmitted directly from mother to child through the placenta, leading to adverse pregnancy outcomes. Concentrated outbreaks or disseminated cases of listeriosis are often reported in European and American countries, but the disease is rare in China due to different dietary habits. Unlike European and American countries, traditional Chinese people are accustomed to eating cooked food rather than raw food. In this study, we collected clinical data of 16 laboratory-confirmed cases of listeriosis during pregnancy at the Women and Children's Hospital of Jiaxing University in the past eight years. We searched for cases of listeriosis during pregnancy in China and published in Chinese journals in the past 15 years, and analyzed their clinical data in addition to our cases, for a total of 93 laboratory-confirmed cases.
2 Materials and methods
2.1. Research objective
We collected date from 16 pregnant patients with laboratory-confirmed L. monocytogenes infection that were hospitalized at the Women and Children's Hospital of Jiaxing University from May 2013 to December 2020. Diagnostic criteria included the following: clinical manifestations such as fever, flu-like symptoms, abdominal pain and diarrhea, abnormal fetal movement or fetal heart monitoring in women during pregnancy, and at least one of the following conditions were met [Citation4]: (1) Listeria monocytogenes was isolated from bacterial cultures at sterile sites (usually blood, cerebrospinal fluid, deep pus or tissue obtained from sterile procedures) in patients during pregnancy, and (2) Acute Listeria monocytogenes septicemia (early-onset) in newborns, immediately after birth.
2.2. Research methods
We conducted a retrospective analysis of data from 16 pregnant patients with listeriosis including clinical presentation, weeks of gestation of at disease onset, the season of onset, laboratory tests and drug sensitivity test results, imaging changes (lung X-ray, or lung ultrasound), placental pathology, antibiotic use, pregnancy outcome, and regression.
2.3. Statistical methods
Categorical variables are presented as frequencies (percentage) and were compared using the Pearson χ2 test or Fisher's exact test. Statistical analysis was performed using SPSS version 25 (IBM Corp., Armonk, NY, USA). A two-tailed p < .05 was considered statistically significant.
2.4. Literature search
Search: China Knowledge Network internet (CNKI), Wanfang Medical Network and Wanfang Data, and other domestic databases. We used “pregnancy,” “listeria,” and “infection” as search terms and searched 75 articles from January 2006 to December 2020. After reviewing the abstracts, we chose to read the full text of 30 papers, 16 of which met the inclusion criteria, with 100 cases reported. We excluded 23 cases for which bacterial culture results were not clearly reported and selected 77 laboratory-confirmed cases for study. Combined with the 16 cases that occurred in our hospital, the total number of cases was 93. Inclusion criteria: presentation of nonspecific influenza-like illness during pregnancy, blood culture or amniotic fluid culture or placental culture, or detection of Listeria monocytogenes in the newborn. Case exclusion criteria included the following: (1) The literature was only in the form of a review and did not contain case reports. (2) Repeatedly published or reported cases from the same unit were excluded. (3) Cases with an unknown history of diagnosis and treatment and incomplete basic information.
3. Results
3.1. General information
All sixteen pregnant women in our center were singleton pregnant, and their ages were 20–36 years of age, with an average of 28 ± 5 years. The gestational weeks were as follows: one case in the first trimester (<12 weeks), seven patients in the second trimester (12–28 weeks), and eight cases in the third trimester (>28 weeks). The distribution by season included four cases in spring, nine in summer, two in autumn, and one in winter. All sixteen patients were healthy women and denied a history of immune system diseases and other chronic diseases.
3.2. Clinical manifestations
Fifteen of the sixteen patients presented with fever, twelve with high fever (>39 °C); seven with headache; four with respiratory symptoms, manifested as paroxysmal cough and sputum; five with lower abdominal pain; four with urinary tract irritation such as lumbago, urinary frequency, and urgency; two with reduced faetal movement; two with premature rupture of membranes; and one with vaginal bleeding. None of the pregnant women had digestive symptoms, such as diarrhea, nausea, or vomiting.
3.3. Laboratory tests
The mean blood leukocyte count was 19.9 ± 6.9 × 109 /L on day one of admission (7.4–30.1 × 109 /L,), with thirteen cases above the upper limit of normal; ultrasensitive C-reactive protein ranged from 5.5 to 208.3 mg/L, mean (74.8 ± 43.4) mg/L, with fifteen patients above the upper limit of normal (>5 mg/L). LM-confirmed clinical specimen sources included the following: blood in twelve cases, amniotic fluid in three cases, placental tissue culture in one case, and neonatal blood cultures in two cases. We tested the specimens for drug sensitivity and found the following resistant strains: five penicillin G resistant strains, four oxacillin-resistant strains, three ampicillin-resistant strains, three ciprofloxacin-resistant strains, and three clindamycin resistant strains were found.
3.4. Imaging examination
Lung imaging (lung computed tomography or lung ultrasound) was performed in eight of the patients, two had pulmonary infections () and one had a left pleural effusion. Two patients with pulmonary infection had a temperature >39 °C and respiratory symptoms such as paroxysmal cough and phlegm. We performed a pulmonary CT examination in five of the following cases: two patients with early-term pregnancy who were stillborn on admission; two patients with mid-term pregnancy after delivery of the neonates or offspring to stillborn fetus; and one patient with late pregnancy admitted to the hospital who had preterm labor who underwent CT pulmonary examination after delivery. Ultrasound of the lungs was performed in three patients.
Figure 1. CT scan of the chest of a pregnant woman infected with Listeria monocytogenes in the second trimester.
Figure 2. Thoracic ultrasound scan of a pregnant woman infected with Listeria monocytogenes in the second trimester.
3.5. Placental pathology
Six patients underwent pathological examination of the placenta, which showed chorioamnionitis ranging from stage II grade III to stage III grade III (): varying degrees of dilated and congested interstitial vasculature chorionic villi, inflammatory cell infiltration, local hemorrhage, necrosis, and calcification.
Figure 3. Pathology of the placenta of a pregnant woman infected with Listeria monocytogenes in the third trimester of pregnancy. At 37w of pregnancy, placental pathological chorionic vasodilatation, hyperemia, with local bleeding, chorioamnionitis: stage II, grade III.
3.6. Treatment and outcome
Initial treatment: Piperacillin/tazobactam in five patients, including one case in combination with metronidazole, and cephalosporins in ten patients, including two cases with also azithromycin; and azithromycin in combination with amineptine in one case. After checking the pathogenic and drug sensitivity tests, we changed two cases to ampicillin or ampicillin sodium/sulbactam sodium, two to amoxicillin-clavulanic acid potassium injection, and three to meropenem, and five patients continued with piperacillin/tazobactam. One patient was only positive for L. monocytogenes in the neonatal blood cultures, and we discontinued the drug after three days of cefoxitin. All patients recovered well after their treatment, and two of them had pulmonary infections that were found by imaging which were subsequently treated, and then the infections resolved.
3.7. Pregnancy outcome
There was one case of intrauterine fetal death in early pregnancy. There were seven patients with mid-pregnancy infections, four who were induced due to intrauterine death, and three who improved after aggressive antibiotic treatment and were able to continue the pregnancy until full-term delivery. There were eight patients with late pregnancy infections, one who improved after treatment and continued the pregnancy to 40 weeks until their cesarean section; the other seven patients were delivered immediately after the onset, four of who were delivered by cesarean section and three by vaginal delivery. There were two neonatal deaths, three cases of neonatal septicemia, one case of neonatal bacterial meningitis, and six cases of neonatal pneumonia. Details of treatment and pregnancy outcome and regression are shown in .
Table 1. Treatment and pregnancy outcome in 16 cases of Listeria monocytogenes（LM） infection during pregnancy.
3.8. Ninety-three cases of listeriosis in China
We found 77 cases of pregnancy complicated with LM infection reported in the literature, and 16 cases in our center ().
Table 2. Summary of 93 cases of Listeria infection during pregnancy in China from 2006 to 2020.
The timeframes of patient listeriosis onset during pregnancy included the following: 31 cases in early pregnancy, 27 cases in middle pregnancy, and 35 cases in late pregnancy.
The clinical manifestations of listeriosis included the following: 90 cases of fever; 50 cases of irregular lower abdominal pain, and 27 cases of abnormal fetal movement and/or the abnormal fetal heartbeat.
The laboratory evidence for listeriosis included the following: 33 cases with elevated white blood cells (>15 × 109/L): Culture results of various specimens including the following: 6 patients with positive amniotic fluid cultures that were LM (+), 35 cases with maternal blood cultures that were LM (+), 37 cases with maternal placenta and uterine secretion cultures that were LM (+), and 15 patients with neonatal blood cultures that were LM (+).
Amniotic fluid and placenta: there was no amniotic fluid in 1 case, clear amniotic fluid in 10 patients, grade I meconium in 3 cases, grade II meconium in 5 cases, grade III meconium in 23 cases, patina-coloured amniotic fluid in 1 patient and unreported amniotic fluid in 73 cases. The placenta was sent for pathological examination in 57 patients, and the results were all suggestive of high neutrophil infiltration that was 100% consistent with the presentation of acute chorioamnionitis. The 59 remaining cases did not report pathological placental findings.
Antibiotic treatment: fifty-eight cases were initially treated with cephalosporin antibiotics, and the antibiotics changed after the laboratory results were confirmed. Twenty-four subjects were initially treated with broad-spectrum penicillin to cover the pathogenic bacteria, and eleven patients were treated with other antibiotics. Drug sensitivity tests revealed the following resistant strains：15 penicillin G-resistant, 14 oxacillin-resistant, and 13 ampicillin-resistant strains. Patients were switched to vancomycin or meropenem after penicillin treatment was ineffective.
Complications and outcomes of the pregnant women were as follows: 20 cases of sepsis, 3 cases of pneumonia, 6 cases of acute pyelonephritis, 28 cases of intrauterine infection, 2 cases of multiorgan dysfunction syndrome, and 1 case of septic shock. All 93 pregnant women recovered and were discharged after treatment.
Fetal and neonatal outcomes were as follows: 16 cases of miscarriage, 16 cases of intrauterine death, 22 cases of death after birth, and 39 cases were discharged after treatment.
4. Discussion
Listeria monocytogenes is a gram-positive, non-spore forming intracellular anaerobic bacterium, that produces a hemolytic exotoxin but not endotoxins. T lymphocytes play an essential role in eliminating the bacteria, but humoral immunity has no protective effect on L. monocytogenes infection. Therefore, the most susceptible people are newborns, pregnant women, adults over 40 years of age, and others with impaired cellular immune functions [Citation5]. Bacteria have excellent plasticity in their living environment and can tolerate low temperatures. It is a typical cold-tolerant pathogen that can grow and reproduce for a long time in the refrigerator. The growth temperature is 1.5 ∼ 45.0 °C, and it can tolerate pasteurization [Citation6]. It is one of the deadliest foodborne pathogens. As reported in the literature, most of our cases were transmitted by mouth, and the months with the highest incidence were July and August. Pregnant women are at higher risk of contracting listeriosis than the general population due to elevated progesterone in the body, which leads to decreased cellular immunity [Citation7]. According to the data analysis of the American Foodborne Disease Active Surveillance Network system, the risk of listeriosis in pregnant women aged 15–44 is 114.6 times higher than that of non-pregnant women [Citation8]. Listeria monocytogenes infection can penetrate the placental endothelial cell layer and infect the fetus [Citation9], resulting in a high incidence of intrauterine infections. The newborn condition and the prognosis of the fetus is poor, and the case fatality rate is as high as 25–30% [Citation10]. According to the statistics of the patients in our center, there were five cases of fetal death in the early and second trimester of pregnancy, and two cases of newborn babies delivered in the third trimester of pregnancy died, with a mortality rate of 43.75%. The results are consistent with previous studies [Citation4,Citation10]. In this study, ninety -three pregnant women returned to normal and were discharged after treatment. Nevertheless, the fetus and newborn had a poor outcome, with a mortality rate of 58.06% and a poor prognosis. The results showed that the mortality rate was higher than that of previous studies
Listeria monocytogenes is severely invasive and can cross the intestinal barrier, the blood-brain barrier, and the placental barrier. It can lead to severe complications such as febrile gastroenteritis, bacteremia, central nervous system infections, miscarriage, stillbirth, neonatal sepsis, and neonatal meningitis [Citation11]. Wolfe et al. [Citation12] found in a gestational primate model of listeriosis that L. monocytogenes aggregated in the highest concentrations in the meconium, placenta, and fetal tissues. Pathology showed vasculitis, fibrinoid necrosis, and metaplastic spiral artery thrombosis, with changes such as acute chorioamnionitis and chorioretinitis, indicating that the organism crosses the placenta [Citation11]. Listeria monocytogenes infection can occur in all stages of pregnancy. It has been reported that most of the damages are in the third trimester (>28 weeks), but an animal model [Citation12] shows that the risk of fetal death caused by L. monocytogenes infection in the early stage of pregnancy is much higher than that in the third trimester. Among the eight cases of early and second-trimester pregnancy, five cases were intrauterine fetal deaths, and the other eight cases were in the third trimester of pregnancy, including two cases of neonatal deaths. The probability of fetal loss in the first and second trimesters was higher than that in the third trimester (5/8 vs. 2/8, p = .315). The clinical analysis of our center found that all sixteen cases of LM infection during pregnancy were acute, and the onset time was short. The main clinical manifestations were high fever, headache, a significant increase in white blood cells and CRP, and a decrease or disappearance of fetal movement. There were two patients with pulmonary infection, and we found no apparent digestive tract symptoms in any of the cases. Listeria pneumonia is rare; only one case was reported in China, and it was confirmed by percutaneous tissue culture [Citation13].
In this study, there were two patients with pulmonary infection; the infection area was small, and no traumatic diagnosis was performed because of pregnancy. Sixteen pregnant women turned out well after active treatment, but there was a high incidence of adverse pregnancy outcomes. Early and mid-pregnancy resulted in a significantly higher proportion of intrauterine infections and intrauterine death, while those with late gestational onset tended to have contaminated amniotic fluid, premature rupture of membranes, preterm delivery, and neonatal sepsis. After the pathogenic diagnosis, four of our cases were confirmed, and the patient was treated with an effective antibiotic based on a drug sensitivity test and was in remission until full-term delivery. Because the clinical symptoms are not typical and the positive rate of microbial culture is not high, it is easy to miss the diagnosis of L. monocytogenes infection during pregnancy. In particular, the missed diagnosis rate in the early stage of pregnancy is twice as high as that in the third trimester. It has been reported [Citation14] that 30% of pregnant women infected with LM are asymptomatic, and the positive rate of blood culture in infected pregnant women with clinical symptoms was only 36%. Therefore, the actual number of cases of listeriosis during pregnancy far exceeds the number of clinically confirmed cases. There are no internationally agreed criteria for the diagnosis of listeriosis. The diagnosis of listeriosis in pregnancy depends on the presence of L. monocytogenes in a culture from a sterile site (blood, cerebrospinal fluid, amniotic fluid, deep pus, or tissue obtained by aseptic manipulation, etc.) If the newborn had an infection at birth or within 72 h of birth, then the mother had a history of listeriosis during pregnancy [Citation15]. The condition caused by mother-to-child transmission and intrauterine infection is most often seen in preterm infants. All five cases of Listeria septicemia in newborns in our center were of early-onset. Therefore, if there is unexplained fever, significantly elevated haemogram, digestive tract symptoms, changes in fetal heart rate or fetal movement, and other symptoms during pregnancy, doctors should actively performs microbial cultures to prevent missed diagnoses and delayed treatment. LM is naturally resistant to cephalosporins [Citation16]; amoxicillin or ampicillin is the first choice. The regimen recommended first-line is ampicillin ≥6 g/d and second-line erythromycin four g/d intravenously for 14 d [Citation4].
Because L. monocytogenes is rare, clinicians lack knowledge of the disease, and antibiotics coverage for LM is not taken into account, so cephalosporins are commonly chosen due to their broader antibacterial spectrum. We should pay attention to recent drug sensitivity tests which found that L. monocytogenes could be resistant to penicillin and ampicillin [Citation17]. The selection of antibiotics that are safe during pregnancy are relatively limited, which made planning patient treatment challenging. Some strains are resistant to ampicillin, penicillin, oxacillin, ciprofloxacin, clindamycin, and other antibiotics. Although the number of cases in our center was relatively small, it also suggests that the resistance rate of L. monocytogenes to multiple drugs may change. In this study, all the three patients who received meropenem therapy recovered after treatment. According to Hou et al. [Citation18], the results of the resistance analysis of L. monocytogenes showed 100% carbapenem susceptibility, which may provide alternative drug options for penicillin allergy or penicillin resistant listeriosis during pregnancy. Clinically, although there are drug-resistant strains, penicillin or ampicillin is recommended for patients who are highly suspected of having a L. monocytogenes infection before drug sensitivity tests return. However, it is necessary to dynamically monitor the infection index and general condition of the patient, adjust antibiotics in time according to the efficacy and drug sensitivity results, and consider the safety of the fetus during pregnancy. Macrolides or carbapenems can be selected for severe cases or when patients have drug allergies.
5. Conclusion
Listeriosis during pregnancy primarily presents as a fever and is characterized by low coverage broad-spectrum antibiotics. It results in a high incidence of adverse pregnancy outcomes and a significant increase in fetal and neonatal mortality. Prevention of listeriosis during pregnancy begins with dietary education. Pregnancy healthcare professionals can tell pregnant women to avoid eating raw and cold foods, such as cheese, fresh milk, meat, and vegetables stored in the refrigerator for a long time. To improve clinicians' understanding of the disease, L. monocytogenes infections should be suspected in patients with a fever of unknown origin (FUO) during pregnancy, and a relevant dietary history. To ensure early treatment, early diagnosis should be performed to improve the outcome of pregnancy.
Ethical approval
The research plan was approved by the Ethics Committee of Women's and Children's Hospital of Jiaxing University. Informed consent was obtained from all subjects involved in the study.
Author contributions
Li Xu, acquired, analyzed, and interpreted the data, drafted the initial manuscript, and reviewed and revised it. Yuhai Du and Yan Wu contributed to the analysis and interpretation of the data, contributed to drafting the manuscript, and reviewed and revised the manuscript. All authors approved the final manuscript as it is submitted and agree to be accountable for all aspects of the work. All authors have read and agreed to the published version of the manuscript.
Acknowledgment
No funding was secured for this study.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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