maternal listeriosis in pregnancy without fetal or neonatal infection

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Journal of Infection (I99I) zz, 53-57 CASE REPORT Maternal listeriosis in pregnancy without fetal or neonatal infection A. P. MacGowan,* P. H. T. Cartlidge,t F. MacLeod~ and J. McLaughlin~ * Department of Microbiology, t Department of Neonatal Medicine and ~ Department of Obstetrics and Gynaecology, Southmead Hospital, Westbury-on-Trym, Bristol, and ~ Central Public Health Laboratory, 6I Colindale Avenue, London, U.K. Accepted for publication 23 May I99O Summary Maternal infection with Listeria monocytogenes without fetal or neonatal involvement is relatively rare. Eleven cases arising in England and Wales between I967 and I988 are presented. Introduction Listeriosis is an increasingly common human disease with an estimated incidence of at least 0"43 case per Io 5 population per year in England and Wales. 1 The increase in human beings has been mirrored by an increased prevalence in farm animals, the organism circulating readily among human beings, animals and the environment where it lives freely on vegetation. 2 Recently, it has been suggested that food is a major means of transmission to human beings, but such a means of transmission has only rarely been proved for individual sporadic cases. 3 A study of 722 British patients with listeriosis, reported between I967 and I985, showed that 34 % cases were associated with pregnancy and, of those, about half were neonatal infections, the overall neonatal mortality being about 500/0. 4 Pregnancy-associated infection is usually recognised in the last half of pregnancy. The illness presents with influenza-like symptoms of fever, sore throat, myalgia, malaise, lower abdominal pain and back pain. Occasionally, vaginal discharge, diarrhoea or urinary symptoms are noted. The peripheral blood white cell count may be raised with neutrophilia, and L. monocytogenes may be isolated from the blood. Fetal survival is partly determined by the length of gestation, abortion taking place early in pregnancy and neonatal infection later. Maternal infection alone, however, may occur without infection of the infant. In Sweden, 8 % (4/46) cases of maternal bacteraemia did not result in fetal or neonatal infection5 and in the U.S.A. io % maternal infections in a food-borne outbreak did not cause fetal infection. 6 Several other cases have also been reported from North America. 7-11 Here we record a case of Listeria bacteraemia in a penicillin- allergic woman which was successfully treated with erythromycin and gentamicin. Also, we review Io other cases of maternal infection with fetal oi63-4453/9I/oioo53 +05 803.00/0 © I99I The British Society for the Study of Infection

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Page 1: Maternal listeriosis in pregnancy without fetal or neonatal infection

Journal of Infection (I99I) zz, 53-57

CASE REPORT

M a t e r n a l l i s t er io s i s in p r e g n a n c y w i t h o u t f e ta l or n e o n a t a l i n f e c t i o n

A. P. MacGowan,* P. H. T. Cartl idge,t F. MacLeod~ and J. McLaughlin~

* Department of Microbiology, t Department of Neonatal Medicine and ~ Department of Obstetrics and Gynaecology, Southmead Hospital, Westbury-on-Trym, Bristol, and ~ Central Public Health Laboratory,

6I Colindale Avenue, London, U.K.

Accepted for publication 23 May I99O

Summary

Maternal infection with Listeria monocytogenes without fetal or neonatal involvement is relatively rare. Eleven cases arising in England and Wales between I967 and I988 are presented.

Introduction

Listeriosis is an increasingly common human disease with an estimated incidence of at least 0"43 case per Io 5 population per year in England and Wales. 1 The increase in human beings has been mirrored by an increased prevalence in farm animals, the organism circulating readily among human beings, animals and the environment where it lives freely on vegetation. 2 Recently, it has been suggested that food is a major means of transmission to human beings, but such a means of transmission has only rarely been proved for individual sporadic cases. 3 A study of 722 British patients with listeriosis, reported between I967 and I985, showed that 34 % cases were associated with pregnancy and, of those, about half were neonatal infections, the overall neonatal mortality being about 500/0. 4 Pregnancy-associated infection is usually recognised in the last half of pregnancy. The illness presents with influenza-like symptoms of fever, sore throat, myalgia, malaise, lower abdominal pain and back pain. Occasionally, vaginal discharge, diarrhoea or urinary symptoms are noted. The peripheral blood white cell count may be raised with neutrophilia, and L. monocytogenes may be isolated from the blood. Fetal survival is partly determined by the length of gestation, abortion taking place early in pregnancy and neonatal infection later. Maternal infection alone, however, may occur without infection of the infant. In Sweden, 8 % (4/46) cases of maternal bacteraemia did not result in fetal or neonatal infection 5 and in the U.S.A. io % maternal infections in a food-borne outbreak did not cause fetal infection. 6 Several other cases have also been reported from North America. 7-11 Here we record a case of Listeria bacteraemia in a penicillin- allergic woman which was successfully treated with erythromycin and gentamicin. Also, we review Io other cases of maternal infection with fetal

oi63-4453/9I/oioo53 +05 803.00/0 © I99I The British Society for the Study of Infection

Page 2: Maternal listeriosis in pregnancy without fetal or neonatal infection

54 A . P . M A c G O W A N E T A L .

sparing, strains from which had been referred to the Central Public Health Laboratory, Colindale, London, for serotyping.

Case report

A 37-year-old operator of a word processor, married to a 33-year-old engineer, became pregnant in February I988 (patient i I , Table I). She had had a previous termination of pregnancy in I977. The pregnancy was uneventful until July I988 when the patient was admitted to hospital with a 2 days' history of shivers, backache, malaise and headache. She was febrile (38"5 °C). There was no photophobia, neck stiffness, sore throat or diarrhoea. She had recently eaten some soft Danish cheese. Examination was unremarkable and consistent with her dates. The WBC was 9"5 × IO9/1 with a 69 % neutrophilia. After I day's incubation, blood cultures grew a small Gram-positive bacillus later identified as L. rnonocytogenes. Since the patient was allergic to penicillin, treatment began with intravenous (IV) crythromycin plus gentamicin. An ultrasound scan revealed a viable fetus without any placental abnormalities. After 5 days' Iv therapy, the patient was discharged well, with instructions to take erythromycin orally for g weeks. The rest of her pregnancy was normal. Listeria sp. was not grown from a remnant of the Danish cheese.

At 42 weeks' gestation, the patient went into spontaneous labour and a healthy female infant of 3460 g was delivered by means of Kielland's forceps. The placenta, however, was retained in utero and required manual removal. The puerperium was uneventful. The baby was clinically normal and cerebral, hepatic, splenic and renal ultrasound scans did not show any abnormalities. Histological examination of the placenta revealed four old abscess cavities about I cm in diameter containing sterile pus. The mother and infant remained well 8 weeks after delivery.

Listeriosis in Bristol has been monitored from I983, since when I3 cases of pregnancy-associated infection have been recorded. Of these, I2 resulted in fetal or neonatal infection. This indicates that 7"7 % (I/13) maternal infections in this area did not result in fetal infection.

Other s imi lar cases reported f rom England and Wales since x967

Pregnancy-associated infections with L. monocytogenes from which strains were referred to the Division of Microbiological Reagents and Quality Control, Central Public Health Laboratory, Colindale, London, for serotyping since I967 were reviewed. In I7 cases the fetus was uninfected or its fate was not known. Photocopies of the patients' notes were therefore requested from the hospitals to which the patients had been admitted. When these became available, seven cases were excluded since two were cases of neonatal infection and five were untraceable, so leaving IO cases of proven maternal infection with fetal or neonatal sparing. This means that at least 2"7% (IO/37o) pregnancy-associated cases did not result in fetal or infant infection between I967 and I987. Our case, which arose in I988, was excluded from the calculation. Details of the patients are shown in Table I.

Serovars of L. monocytogenes were equally divided between serovars I/2 and 4, while the average maternal age was 29"6 (range 23-38) years. All the

Page 3: Maternal listeriosis in pregnancy without fetal or neonatal infection

Maternal listeriosis with fetal sparing 55

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Page 4: Maternal listeriosis in pregnancy without fetal or neonatal infection

56 h . P . M A c G O W A N E T A L .

infections took place in the final trimester of pregnancy, most (6 / I I) after the 35th week. Many patients presented with influenza-like symptoms and, with one exception, L. monocytogenes was isolated from blood cultures, usually within x days of their starting incubation. The time from onset of symptoms to initiation of suitable antibiotic therapy varied from I to I I days. Trea tment of patients not allergic to penicillin was with ampiciUin combined, in three cases, with gentamicin. Six infants also received antibiotics in spite of not having any clinical or microbiological evidence of infection. Delivery was within 4 days of Listeria being isolated in seven pregnancies. In only three cases (I, 5 and II) , did pregnancy continue after cessation of maternal treatment with antibiotics. Interestingly, all these pregnancies were at less than 30 weeks gestation when the diagnosis was made. The mode of delivery was unknown in two cases; of the others, three had Caesarian sections and six vaginal deliveries.

Discuss ion

About 3 % maternal infections with L. monocytogenes in England and Wales have not resulted in fetal infection, a figure which agrees with that of others. 5' * Most cases of maternal infection alone presented with typical histories for maternal listeriosis, some infections being so mild as to produce only fever, all being in the second half of pregnancy as has been previously reported. 5 Blood cultures are essential in pregnant women with influenza-like symptoms in order to help with confirmation or exclusion of listeriosis. When these are positive, the organism is usually isolated within 2 days. The length of t ime before patients presented to medical services varied. One patient did not receive appropriate antibiotics for I I days. It has been suggested that early presentation with rapid diagnosis by blood culture may help to prevent some cases of septic abortion, while early maternal antibiotic therapy has been shown to reduce mortality and morbidi ty in infected neonates, y' 11

Ampicillin is the treatment of choice in listeriosis and was effective in many of these cases. Alternatives include co-trimoxazole or erythromycin. ~ Treat- ment with co-trimoxazole is not recommended in pregnancy but erythromycin is safe and was effective in our patient. The treatment of infants with ampicillin was common in the absence of clinical or microbiological evidence of infection, and is perhaps understandable when the mother delivers a short t ime after the infection is diagnosed. It is not necessary, however, in all cases since several authors have reported successful t reatment of maternal bacteraemia with full courses of antibiotics. These patients were bacteraemic at 19 and 20 weeks' or 8 months ' gestation, which is similar to cases I, 5 and I I . 7-10 The reason why the fetuses were not infected in unclear but various factors may be important.

Variation in the pathogenicity of L. rnonocytogenes for experimental mice is well recorded. 12 This may relate to strain variation in the product ion of listeriolysin o or monocytosis-producing agent (MPA). 1~ Alternatively, serial passage of Listeria through experimental animals increases pathogenicity, and it may be that strains that have recently infected animals are more pathogenic to human beings than those derived from vegetable matter. Similarly, cold storage of Listeria may increase their pathogenicity. This

Page 5: Maternal listeriosis in pregnancy without fetal or neonatal infection

M a t e r n a l listeriosis wi th f e t a l sparing 57

m a y be r e l eva n t i f i n f ec t i on is c o n t r a c t e d f r o m r e f r i g e r a t e d foods . H o s t gene t i c f ac to r s are k n o w n to affect r e s i s t ance in mice , 1~ h a v i n g effects o n n o n - s p e c i f i c i m m u n i t y as wel l as o n the f u n c t i o n o f T - l y m p h o c y t e s . T - h e l p e r a n d cy to tox i c cells are i m p o r t a n t in m a c r o p h a g e ac t iva t ion a n d c lea rance o f in t r ace l lu l a r i n f ec t i on in m i c e bu t , in h u m a n be ings , n o n - s p e c i f i c i m m u n i t y to l is ter iosis m a y also be i m p o r t a n t . 1~

I n conc lus ion , b l o o d cu l tu r e s are vi ta l in the d iagnos i s o f l is ter iosis whi le amp ic i l l i n w i t h or w i t h o u t an a m i n o g l y c o s i d e m a y p r o v i d e a d e q u a t e t h e r a p y , t h e r e b y p r o v i d i n g a chance to de l ive r an u n i n f e c t e d infant . A n t i m i c r o b i a l t h e r a p y o f the in fan t is p r o b a b l y i n d i c a t e d a f te r cl inical a n d m i c r o b i o l o g i c a l a s s e s s m e n t s in those in fan t s b o r n a sho r t t i m e a f te r m a t e r n a l b a c t e r a e m i a , b u t no t i f t he m o t h e r has c o m p l e t e d a full c o u r s e o f an t ib io t ics . F ina l ly , t hese cases s h o w tha t an t ib io t i c t h e r a p y m a y resu l t in fe ta l su rv iva l to t e r m a f te r m a t e r n a l a n d p l acen t a l Lis ter ia in fec t ion , a l t h o u g h the r easons fo r th is are unc lea r .

(We thank those clinicians who provided information for the cases reported, D r T . L. Chambers for allowing us to report case I I and D r D. S. Reeves for helpful comments on her antimicrobial therapy.)

R e f e r e n c e s

I. McLauchlin J, Saunders NA, Ridley AM, Taylor AG. Listeriosis and food borne transmission. Lancet I988 ; ii: 177-8.

2. Lamont RJ, Postlethwaite R, MacGowan AP. Listeria monocytogenes and its role in human infection..7 Infect I988 ; I7 : 7-28.

3. Bannister BA, Listeria monoeytogenes meningitis associated with eating soft cheese..7 Infect I987; I5: I65-168.

4. McLauchlin J. Listeria monoeytogenes, recent advances in the taxonomy and epidemiology of listeriosis in humans..7 Appl Bacteriol i987; 63: I-I1.

5. Larsson S, Cronberg S, Winblad S. Listeriosis during pregnancy and neonatal period in Sweden i958-i974. Acta Paediatr I979; 68: 485-93.

6. Linnan MJ, Mascola L, Dorg Laux et al. Epidemic listeriosis associated with Mexican- style cheese. N Engl.7 Med 1988; 312: 4o4-4o7.

7. Hood M. Listeriosis as an infection of pregnancy manifested in the newborn. Paediatrics 196I; 27: 39o-396.

8. Hume OS. Maternal Listeria monocytogenes septicaemia with sparing of the fetus. Obstet Gyneeol I976; 48: 33s-34s.

9. Zerroudaks I, Cederquist. Effect of Listeria monocytogenes septicaemia during pregnancy on the offspring. Am .70bstet Gynaecol I977 ; xz9 : 465-467 •

to. Holhouser CA, Ansbacher R, McNutt T, Steele R. Bacterial endocarditis due to Listeria monocytogenes in a pregnant diabetic. Obstet Gynaecol 1977; 51: 9--IOS.

IL Boucher M, Youkera L. Perinatal listeriosis (early-onset): correlation of antenatal manifestations and neonatal outcome. Obstet Gynaecol I986; 68: 593-597.

12. Mainou Fowler T, MacGowan AP, Postlethwaite R. Virulence of Listeria spp. x course of infection in resistant and susceptible mice. -7 Clin Microbiol I988 ; z7: I3I-I4o.

13. Goebel W, Karhariou S, Kuhn M, Sokolovic Z, Kreft J, Kohler S, Funke D, Chakraborty T, Leimeister-Wachter M. Hamneolysin from Lis te r ia - biochemistry, genetics, and function in pathogenesis. Infection I988; 16 (Suppl 2): i49-I56.

14. Cheers C, Mackenzie IFC, Paulto M, Ward C, York K. Resistance and susceptibility of mice to bacterial infection: course of listeriosis in resistant or susceptible mice. Infect Immune 1978 ; 19: 763-770.

15. MacGowan AP, Peterson PK, Keane W, Quie PG. Human peritoneal macrophages. Phagocytic, killing and chemiluminescent responses to opsonized Listeria monocytogenes. Infect Immune I983 ; 4 ° : 44o-443 .