Parvovirus B19 Infection in Pregnancy

MEDICINE
This text is a
translation from
the original
German which
should be used
for referencing.
The German
version is
authoritative.
REVIEW ARTICLE
Parvovirus B19 Infection
in Pregnancy
Susanne Modrow, Barbara Gärtner
SUMMARY
Introduction: Parvovirus B19 is the causative agent of erythema infectiosum (fifth disease),
a predominantly benign and self-limiting disease manifesting as rash with associated anemia.
Occasionally, arthritis and arthalgia, hepatitis, encephalitis, meningitis and myocarditis can
develop as complications. Acute infection in non-immune pregnant women can lead to fetal
hydrops. Methods: The data are based on a selective search of the literature and on the authors'
clinical experience. Results: In seronegative pregnant women acute parvovirus B19 infections
can result in fetal death and/or hydrops fetalis. Since the majority of infections occur during
childhood, the risk of complications is high in seronegative pregnant women working in
contact with children, particularly in nursery and primary school teachers and in child health.
Discussion: This article reviews current scientific knowledge and presents incidence data for
fetal complications in Germany, to inform antenatal care and public health.
Dtsch Arztebl 2006; 103(43): A 2869–76.
Key words: Parvovirus B19, erythema infectiosum, fetal hydrops, pregnancy, childcare
P
arvovirus B19 causes "slapped cheek syndrome" or fifth disease, one of the
5 common childhood exanthems (measles, chicken pox, rubella, scarlet fever and
fifth disease). The virus infects and destroys red blood cell precursors, causing inevitable
anemia. Acute B19 infection in seronegative pregnant women can cause fetal death or
hydrops (1). According to § 4 Section 2 No. 6 of the Antenatal Care Act, a pregnant
women is not allowed to carry out any work "which puts her, by virtue of the pregnancy,
at increased risk of occupational disease, or in which the risk of an occupational
disease might endanger either mother or fetus". This legal requirement has led to an
increasing tendency in recent years in Germany to declare seronegative pregnant
women who work with children medically unfit to work for the duration of pregnancy.
If the employer is unable to offer alternative work, the pregnant woman is relieved of
her duties until the birth of the baby. This practice has unleashed heated debate. Against
this background, it is essential to present the current state of knowledge in relation to
the epidemiology and clinical course of Parvovirus B19 infection, based on personal
experience and international publications, together with an evaluation of the current
situation on Germany.
Transmission
Parvovirus B19 is transmitted via droplet infection, or via contact with saliva, blood or
other body fluids. Acutely infected individuals have extremely high viral concentrations
(1011 to 1013 particles/ml) in blood and other body fluids such as saliva or urine. Since
parvoviruses have no lipid capsule, their infectivity is unaffected by solvents and
detergents. A strong emphasis on hygiene is essential in pediatric practices, where a high
level of infection is to be expected, but also in nursery schools, if viral transmission via
contaminated objects is to be prevented. Since viremia precedes symptoms and can be
persistent, one in every 1000 to 2000 blood donations is affected by the virus,
sometimes in high concentrations. The virus is stable in blood products (clotting factors
VIII and IX, albumin, mmunoglobulins) and remains infectious.
Institut für Medizinische Mikrobiologie und Hygiene, Universität Regensburg (Prof. Dr. Modrow);
Institut für Virologie, Universitätsklinikum Homburg/Saar (Prof. Dr. Gärtner)
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
1
MEDICINE
DIAGRAM 1
a) Antibody production and blood virus concentration during acute infection
b) Antibody production and blood virus concentration during infection with a prolonged viremic phase. A prolonged
viremic phase is common in pregnant women with acute parvovirus B19 infection.
Diagnosis
The virus is detected directly via polymerase chain reaction (PCR). B19 specific antibodies
can be assayed using ELISA or immunoblot tests. The viremia begins around 4 to 5 days
following exposure. 2 to 3 days later the blood viral load will have reached the level of 1011
to 1013 particles/ml. IgM antibodies, predominantly against VP2 capsid proteins, are detectable
after around 10 days post contact, at around the same time as the onset of rash. At this phase
of the illness and in the days following, blood and saliva levels of 104 to 108 genome
equivalents of virus DNA/ml can be found. B19 specific IgM is frequently undetectable
from 3 weeks following initial contact, although the patient is still viremic at this stage.
Rising titers of anti VP1 and VP2 capsid protein IgG are measurable around 2 weeks after
initial contact, and remain elevated for life (diagram 1a). IgM and IgG are partially
neutralizing, and lower the viral load (diagram 2). In children, the pathogen has usually
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
2
MEDICINE
been eliminated by 3 to 4 weeks following infection, and undetectable in blood or saliva
even with sensitive PCR methods. In adults, the viremic phase with blood levels of between
103 and 107 genome equivalents/ml of blood can last longer, sometimes several years. In
addition to IgG antibodies against structural proteins, these patients also form immunoglobulins
against the non structural protein NS1 (diagram 1b). Even after elimination from the blood,
B19 DNA can persist in skin, synovial, bone marrow, myocardial and liver cells. This latent
presence of viral genome occasionally poses a diagnostic problem in poorly defined
illnesses with a possible B19 association.
Acutely infected pregnant women are often viremic for months, often beyond delivery,
despite IgG production (between 103 and 104 genome equivalents/ml). Similar viral loads are
detectable in umbilical cord blood. Because IgM levels often fall rapidly in the
presence of persistent viremia, pregnant women with questionable parvovirus B19
serology should undergo PCR to look for possible viral DNA, in addition to antibody assay,
wherever there has been contact with fifth disease infected individually, and regardless of
symptoms. The presence of B19 specific IgG antibodies in the absence of DNA and IgM
assays is suggestive of old B19 infection with successful elimination of virus from the blood.
These individuals can be treated as immune, and are protected against reinfection with B19.
Clinical course
The clinical picture associated with parvovirus B19 infection is variable (box) (2). Around
30% of infections are sub clinical in children, whereas adults tend to be more unwell. B19
commonly begins as erythema infectiosum, following with a non specific prodromal phase
and flu like symptoms such as fever, headache, nausea and diarrhea. After 2 to 5 days, at
around the same time as the first virus specific IgM antibody, the characteristic rash appears
as a fiery red eruption on the cheeks (slapped cheek syndrome) (figure 1), extending over
the following one to four days into a characteristic ring-shaped erythematous,
maculopapular rash on the arms and legs (figure 2). All B19 infections, whether or not
symptomatic, are accompanied by a transient fall in reticulocyte count and hemoglobin,
marking viral destruction of erythrocyte precursors. Occasionally the acute symptoms are
followed by severe arthralgia and arthritis. In addition to anemia, severe and occasionally
persistent thrombocytopenia and neutropenia can occur, which can be life threatening (2).
DIAGRAM 2
Acute Infection: Viral load (genome equivalents per ml) measurable in the blood and sputum of acutely infected
patients. The values given are those which were the first measurable sign of infection on the relevant day after the
onset of fever. The viral contact can be assumed to have taken place four to six days previously.
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
3
MEDICINE
BOX
Illness patterns associated
with parvovirus B19 infections
Immunocompetent individuals
Common
Non specific malaise
Erythema infectiosum
Transient anemia
Transient mono or polyarthritis
Transient arthralgia
Rare
Thrombocytopenia
Granulocytopenia
Henoch-Schönlein Purpura
Chronic arthritis
Scleroderma
Idiopathic thrombocytopenic purpura
"papular purpuric gloves and socks syndrome" (PPGSS)
Pancytopenia
Virus associated hemophagocytic syndrome (VAHS)
Acute liver failure/hepatitis
Pseudoappendicitis/mesenteric lymphadenitis
Myositis
Myocarditis
Glomerulonephritis
Meningitis
Encephalitis
Gullian-Barré syndrome
Cerebellar Ataxia
Individuals with underlying hematologic disease
Severe anemia
Aplastic crisis
Fetuses
Miscarriage
Fetal hydrops
Intrauterine death
Immunosuppressed individuals
Chronic anemia
Erythroblastopenia ("pure red cell aplasia")
Chronic thrombocytopenia
Chronic granulocytopenia
Chronic pancytopenia
Myocarditis/pericarditis/acute heart failure
Acute liver failure/hepatitis
Meningitis/encephalitis
Infection before the 20th week of pregnancy can have severe consequences for the fetus,
where fetal mortality rates of around five percent greater than in the background population
are quoted. The cause of death is probably infection related platelet damage in the placenta.
Infectable fetal erythrocyte precursors are formed from the 10th to 12th week of
pregnancy. From this point on, the virus no longer reproduces within the fetus, even if it
transferred across the placenta. This type of viral transmission was found in 16% to 33% of
acutely infected pregnant women. The fatality rate is however markedly lower, at 0% to 15%
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
4
MEDICINE
(3, 5–9). From the tenth to twelfth week of pregnancy the virus infects and reproduces
within the pronormoblasts in the fetal liver. The destruction of erythrocyte precursors
disrupts the formation of red blood cells, leading to severe anemia, edema, ascites,
hydrothorax, and hydropericardium. This non immunological fetal hydrops develops
between weeks 14 and 28 of pregnancy. It is estimated that parvovirus infection accounts
for around 10% of these in total (4).
The onset of symptoms in the fetus are delayed, usually to around 3 to 6 weeks after the
acute maternal infection, but occasionally up to 18 weeks later. Sometimes viral genome is
found in the fetal lung and myocardium. Myocarditis can develop, accompanied by heart
failure which exacerbates the hydropic symptoms. It is unclear whether other factors such
as level and duration of viremia, maternal health and coinfection affect fetal illness. A twin
pregnancy has been reported in which only one fetus developed hydrops.
Since B19 infection has been an established cause of fetal hydrops, fetal mortality has
fallen markedly. Early studies quoted fetal demise in 9% of B19 infected pregnant women
(5). A recent German study in 1 018 women with acute B19 infection showed that of 40
fetuses, (3.9%) with fetal hydrops, 12 died, corresponding to a mortality rate of 1.2%. The
marked decrease in deaths is probably attributable to increased awareness and early
diagnosis of fetal anemia using Doppler ultrasound. Swedish studies of intrauterine deaths
in late pregnancy without hydrops suggested that 7.5% were associated with parvovirus
B19 (10). Again, fetal symptoms can arise more than five months after the acute maternal
infection. Possible causes include virally induced vasculitides in the placental lobes, or fetal
myocarditis. There are no indications to date of fetal anomalies resulting from parvovirus
B19 infection (8, 9). Occasionally, B19 induced fetal myocarditis can persist postnatally and
require heart transplantation due to terminal heart failure.
Prevention and treatment
There is currently no vaccination against parvovirus B19. High dose immunoglobulin
treatment may be used to treat persistent infection, particularly in immune suppressed
patients. Single case reports suggest that this may also be used to treat fetal hydrops, but no
studies have been carried out.
Immunoglobulin prophylaxis to prevent transplacental transmission in pregnant women
is not indicated. However, close monitoring using Doppler sonography should be instituted,
with a view to early detection of fetal anemia. Since fetal symptoms are delayed relative to
the maternal infection, women must be followed up into late pregnancy. In the case of
severe hydrops (Hb < 6–8 g/dl), intrauterine blood transfusion via the umbilical vein saves
the lives of 80% of fetuses (3). Around two thirds die without treatment. In the remainder,
hydrops is so mild as to be spontaneously resorbed.
Epidemiology
Most parvovirus B19 infections occur in childhood: 40% to 50% of children and adolescents
between 10 and 15 years old have B19 specific IgG antibody as a sign of old B19 infection.
Since adults are also infected, the rate of infection in the population rises to around 60 to 70% in
20 to 30 year olds, and 80% in 60 to 70 year olds. Studies in several countries have investigated
how many women of reproductive age are immune to parvovirus B19 (table). Values of
between 28% in the USA and 81% in Sweden were quoted (8, 11–21). Some studies explicitly
report large fluctuations when groups are studied from different regions or at different times
(15). No large scale serological studies of this type have been carried out in Germany. One study
in healthy blood donors (average age 35 years) showed B19 specific IgG antibody in 68%.
Annual seroconversion rates in susceptible adults differ between endemic and epidemic
periods. In endemic phases an incidence of between 0.65% and 1.5% in non immune
individuals would be expected (11–14, 17, 20). Regionally circumscribed epidemics with
incidence rates of 10% to 15%, and up to 30% at the height of the outbreak are observed
between February and June (8, 12, 13, 22).
During an epidemic, the infection risk is independent of whether susceptible individuals
are occupationally exposed to B19 infected or potentially infected patients – such as
doctors, hospital staff, teachers, nursery nurses – or work in unrelated areas. A study from
the USA compared hospital staff in contact with acutely infected patients suffering from
aplastic anemia with unexposed staff: 3,1% of susceptible individuals in the groups with
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
5
MEDICINE
Figure 1
Seven year old boy with acute parvovirus
B 19 infection and erythema infectiosum
("slapped cheek syndrome")
Figure 2
Characteristic ring-shaped rash on the arm
of a child infected with parvovirus B19
patient contact became infected, whereas in the unexposed group 8,1% seroconverted (23).
During a B19 outbreak on the delivery unit of an American maternity hospital staff working
on the unit were examined, as well as staff from other areas of the hospital, staff from
another hospital, and registered blood donors in the same area. In all groups, independently
of exposure, new infection rates of 23% to 30% were found (24). In Mexico, clinical
medical students exposed to infected patients during a parvovirus B19 outbreak were
compared with preclinical students (22). The potentially exposed group showed a
seroconversion rate of 33.6%, the other group 42.6%. These examples show that during an
epidemic, the extremely stable parvoviruses are ubiquitous, leaving all susceptible
individuals with a similar exposure risk to affected individuals or contaminated objects.
A number of studies have attempted to clarify whether the risk of parvovirus B19
infection in non immune pregnant women is dependent on contact with children, as in the
case of teachers and nursery nurses. The largest of these studies examined more than 30 000
Danish pregnant women in respect of B19 specific IgM and IgG. Data were collected on
occupation, family circumstances and age (13). Women working with children under six
had a threefold increased risk of becoming infected with parvovirus B19 during pregnancy,
relative to other occupational groups (Odds-Ratio [OR] 3.97). Women with a child of their
own at home showed a similar risk (OR 3.17), whereas with two or three children at home
the odds ratio increased to 5.47 und 7.54. In teachers teaching 7 to 16 year olds, the risk of
infection was not significantly increased.
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
6
MEDICINE
That children in the home environment pose the greatest parvovirus B19 risk during
pregnancy is confirmed by other authors: Harger studied 618 pregnant women in contact
with B19 infected individuals and found no significantly increased risk in teachers, nursery
nurses or in women employed in the health system (8). Children in the home represented
the greatest infection risk (factor 2.8). A Canadian study suggested that 50% of acute
infections in pregnant women are attributable to contact with infected children and only
20% to 30% to occupational exposure. Similar data have been reported from Japan, where
contact with own children was responsible for 60% of new infections in pregnant women,
and only 20% due to occupational exposure. In a review article Mead et al. calculated a
6.3% increased risk of B19 associated complications of pregnancy arising in domestic
contact with children, while the occupational risk was estimated to be 1.7% (25). A Canadian
study examined seroprevalence rates in women employed in a variety of pre-school child
care settings (17). The highest infection rate was found among individuals who had contact
with children under 18 months. The seroprevalence increased with length of employment.
Employees with five years' employment experience had an increased odds ratio of 1.7 (at
age 20) and 1.4 (at age 30) relative to new employees of equivalent age. These results
suggest that the greatest risk of an acute B19 infection in pregnant women arises from contact
with a woman's own children.
Estimation of annual numbers of cases in Germany
The population of adult women in Germany is around 42 161 000. Of these, around
19 000 000 are of reproductive age. According to current trends, reproductive age is
between the ages of 15 and 50. 700 000 live births occur annually. Based on an estimated
seroprevalence of 65% in the population at large, around 300 000 children annually are born
to B19 seronegative women. An annual new infection rate of 1.5% gives an expected rate
of acute parvovirus B19 infection in pregnant women of 3 000 to 4 000 (13). This figure
would yield an expected 70 to 80 fetal deaths due to miscarriage and fatal hydrops, and
TABLE
Daten zur Seroprävalenz von IgG-Antikörpern gegen Parvovirus B19 bei
jungen Erwachsenen
Land
Untersuchte
Bevölkerungsgruppe
Seroprävalenz
(%)
Autor/Veröffentlichung
Finland
pregnant women
58.6
Alanen et al., 2005 (14)
Mexico
medical students
45.9
Noyola et al., 2004 (22)
Canada
child carers
69.8
Gilbert et al., 2005 (17)
Iran
women
66.5
Ziyaeyan et al., 2005 (20)
Italy
blood donors
79.5
Manaresi et al., 2004 (e1)
Ireland
pregnant women
64.0
Knowles et al., 2004 (15)
Russia
pregnant women
75.3
Odland et al., 2001 (e2)
Australia
pregnant women
64.0
Karunajeewa et al., 2001 (16)
Denmark
pregnant women
66.0
Jensen et al., 2000 (12)
Denmark
pregnant women
65.0
Valeur-Jensen et al., 1999 (13)
USA
pregnant women
49.7
Harger et al., 1998 (8)
Sweden
pregnant women
81,0
Skjoldebrand-Sparre et al.,
1996 (11)
USA
child carers
58.0
Gillespie et al., 1990 (18)
USA
women
28.0
Koch and Adler, 1989 (21)
e1. Manaresi E, Gallinella G, Morselli Labate AM, Zucchelli P, Zaccarelli D, Ambretti S,
Delbarba S, Zerbini M, Musiani M: Seroprevalence of IgG against conformational and linear capsid
antigens of parvovirus B19 in Italian blood donors. Epidemiol Infect 2004; 132: 857–62.
e2. Odland IO, Sergejeva IV, Ivaneer MD, Jensen IP, Stray-Pedersen B: Seropositivity of cytomegalovirus,
parvovirus and rubella in pregnant women and recurrent aborters in Leningrad County, Russia.
Acta Obstet Gynecol Scan 2001; 80: 1025–29.
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
7
MEDICINE
110 to 120 cases of fetal hydrops. The detailed figures will be published by the authors
elsewhere along with an economic evaluation. No such data exist for other infectious
diseases in pregnancy which are not preventable by immunization. Rubella, which is
preventable by vaccination, causes embryopathies, where the infection is contracted before
the 20th week of pregnancy. One to two cases are seen in Germany, annually.
Conclusion
Parvovirus B19 infection in a pregnant woman represents a risk to the unborn child. It
therefore makes sense to establish a woman's immunological status early in pregnancy.
5% of infections in the first twenty weeks of pregnancy will result in fetal death. These are
often early miscarriages. 4% of infections contracted during the whole of pregnancy will
result in fetal hydrops following transplacental transmission. Early diagnosis of fetal anemia
via close sonographic monitoring allows treatment with intrauterine blood transfusion,
which is usually successful.
In endemic periods, it is women who have contact with children at home who have the
highest risk of a new infection during pregnancy. Pregnant women who are occupationally
exposed to children under six have a slightly raised infection risk, especially in the first
years of their career. During epidemics, the infection risk for all population and occupational
groups is similar, and not dependent on direct exposure to infected individuals. Current
evidence does not therefore support a general prohibition on working for seronegative
pregnant women who have occupational contact with children.
Acknowledgment
The authors would like to thank Prof. Dr. Peter Wutzler, Institute for Virology and Antiviral Therapy at Jena University, German
Society for the Control of Viral Illnesses e.V. (DVV e.V.), for his support, and the members of the expert committee "Parvoviruses"
of DVV e.V. for numerous helpful discussions.
Conflict of Interest Statement
The authors declare that no conflict of interest exists according to the Guidelines of the International Committee of Medical Journal
Editors.
Manuscript received on 8 November 2005, final version accepted on 13 March 2006.
Translated from the original German by Dr. Sandra Goldbeck-Wood.
REFERENCES
For e-references please refer to the additional references listed below.
1. Brown T, Anand A, Ritchie LD, Clewley JP, Reid TM: Intrauterine parvovirus infection associated with hydrops fetalis.
Lancet 1984; ii: 1033–4.
2. Kerr JR, Modrow S: Human and primate parvovirus infections and associated disease. In: Berns K et al., eds:
Parvoviruses. London: Edward Arnold (Publishers) Ltd. 2006; 385–416.
3. Enders M, Weidner A, Zoellner I, Searle K, Enders G: Fetal morbidity and mortality after acute human parvovirus
B19 infection in pregnancy: prospective evaluation of 1018 cases. Prenat Diagn 2004; 24: 513–8.
4. Yaegashi N, Okamura K, Yajima A, Murai C, Sugamura K: The frequency of human parvovirus B19 infection in
nonimmune hydrops fetalis. J Perinat Med 1994; 22: 159–63.
5. Public health laboratory service working party on fifth disease. Prospective study of human parvovirus (B19) infection
in pregnancy. Br Med J 1990; 300: 1166–70.
6. Gratacos E, Torres PJ, Vidal J et al.: The incidence of human parvovirus B19 infection during pregnancy and its impact
on perinatal outcome. J Infect Dis 1995; 171: 1360–3.
7. Koch WC, Harger JH, Barnstein B, Adler SP: Serologic and virologic evidence for frequent intrauterine transmission of
human parvovirus B19 with a primary maternal infection during pregnancy. Pediatr Infect Dis J 1998; 17: 489–94.
8. Harger JH, Adler SP, Koch WC, Harger GF: Prospective evaluation of 618 pregnant women exposed to parvovirus B19:
risks and symtoms. Obstet Gynecol 1998; 91: 413–20.
9. Miller E, Fairley C, Cohen BJ, Seng C: Immediate and long term outcome of human parvovirus B19 infection in
pregnancy. Br J Obstet Gynecol 1998; 105: 174–8.
10. Skjoldebrand-Sparre L, Tolfvenstam T, Papadogiannakis N, Wahren B, Broliden K, Nyman M: Parvovirus B19 infection:
association with third-trimester intrauterine fetal death. BJOG 2000; 107: 476–80.
11. Skjoldebrand-Sparre L, Fridell E, Nyman M, Wahren B: A prospective study of antibodies against parvovirus B19 in
pregnancy. Acta Obstet Gynecol Scand 1996; 75: 336–9.
12. Jensen IP, Thorsen P, Jeune B, Moller BR, Vestergaard BF: An epidemic of parvovirus B19 in a population of 3,596
pregnant women: a study of sociodemographic and medical risk factors. BJOG 2000; 107: 637–43.
13. Valeur-Jensen AK, Pedersen CB, Westergaard T et al.: Risk factors for parvovirus B19 infection in pregnancy. JAMA
1999; 281: 1099–105.
14. Alanen A, Kahala K, Vahlberg T, Koskela P, Vainionpaa R: Seroprevalence, incidence of prenatal infections and reliability
of maternal history of varicella zoster virus, cytomegalovirus, herpes simplex virus and parvovirus B19 infection in
South-Western Finland. BJOG 2005; 112: 50–6.
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
8
MEDICINE
15. Knowles SJ, Grundy K, Cahill I, Cafferkey MT: Susceptibility to infectious rash illness in pregnant women from diverse
geographical regions. Commun Dis Public Health 2004; 7: 344–8.
16. Karunajeewa H, Siebert D, Hammond R, Garland S, Kelly H: Seroprevalence of varicella zoster virus, parvovirus B19
and Toxoplasma gondii in a Melbourne obstetric population: implications for management. Aust N Z J Obstet Gynaecol
2001; 41: 23–8.
17. Gilbert NL, Gyorkos TW, Beliveau C, Rahme E, Muecke C, Soto JC: Seroprevalence of parvovirus B19 infection in
daycare educators. Epidemiol Infect 2005; 133: 299–304.
18. Gillespie SM, Cartter ML, Asch S et al: Occupational risk of human parvovirus B19 infection for school and day-care
personnel during an outbreak of erythema infectiosum. JAMA 1990; 263: 2061–5.
19. Cartter ML, Farley TA, Rosengren S et al.: Occupational risk factors for infection with parvovirus B19 among pregnant
women. J Infect Dis 1991; 163: 282–5.
20. Ziyaeyan M, Rasouli M, Alborzi A: The seroprevalence of parvovirus B19 infection among to-be-married girls, pregnant
women, and their neonates in Shiraz, Iran. Jpn J Infect Dis 2005; 58: 95–7.
21. Koch WC, Adler SP: Human parvovirus B19 infections in women of childbearing age and within families. Pediatr Infect
Dis J 1989; 8: 83–7.
22. Noyola DE, Padilla-Ruiz ML, Obregon-Ramos MG, Zayas P, Perez-Romano B: Parvovirus B19 infection in medical
students during a hospital outbreak. J Med Microbiol 2004; 53: 141–6.
23. Ray SM, Erdman DD, Berschling JD, Cooper JE, Torok TJ, Blumberg HM: Nosocomial exposure to parvovirus B19: low
risk of transmission to healthcare workers. Infect Control Hosp Epidemiol 1997; 18: 109–14.
24. Dowell SF, Török TJ, Thorp JA et al.: Parvovirus B19 infection in hospital workers: community or hospital acquisition?
J Infect Dis 1995; 172: 1076–9.
25. Mead PB et al., eds: Protocols for infectious diseases in obstretic. (Protocols in obstretic and gynecology). Oxford:
Blackwell Science Ltd. 2000; 171–80.
ADDITIONAL REFERENCES
This text is a
translation from
the original
German which
should be used
for referencing.
The German
version is
authoritative.
e1. Manaresi E, Gallinella G, Morselli Labate AM et al.: Seroprevalence of IgG against conformational and linear
capsid antigens of parvovirus B19 in italian blood donors. Epidemiol Infect 2004; 132: 857–62.
e2. Odland IO, Sergejeva IV, Ivaneer MD et al.: Seropositivity of cytomegalovirus, parvovirus and rubella in pregnant
women and recurrent aborters in Leningrad County, Russia. Acta Obstet Gynecol Scand 2001; 80: 1025–9.
Corresponding author
Prof. Dr. rer. nat. Susanne Modrow
Institut für Medizinische Mikrobiologie und Hygiene
Universität Regensburg, Franz-Josef-Strauß-Allee 11
93053 Regensburg, Germany
Dtsch Arztebl 2006; 103(43): A 2869–76 ⏐ www.aerzteblatt.de
9