SMFM Papers www. AJOG.

org

Obstetric management of hepatitis C-positive mothers:

analysis of vertical transmission in 559 mother-infant pairs
Moya B. McMenamin, MRCPI; Abigail D. Jackson, PhD; John Lambert, MD; William Hall, MD;
Karina Butler, MRCPI; Sam Coulter-Smith, MD; Fionnuala M. McAuliffe, MD

OBJECTIVE: The objective of the study was to determine vertical trans- vaginal delivery or emergency cesarean in labor was no different when
mission rates of hepatitis C in 2 tertiary level maternity units. compared with those delivered by planned cesarean (4.2% vs 3.0%, P
⫽ NS). Among women in whom hepatitis C RNA was detected antena-
STUDY DESIGN: This was a retrospective review of all hepatitis C-
tally, this finding remained (7.2% vs 5.3%, P ⫽ NS). No case of ver-
positive mothers and their pregnancy outcomes.
tical transmission was noted among hepatitis C RNA-negative
RESULTS: Of 74,629 deliveries, 559 liveborn infants were born to 545 mothers.
hepatitis C mothers; the rate of antenatal hepatitis C infection was
CONCLUSION: This study reports a vertical transmission rate for hep-
0.7%. In the neonatal period, 423 infants tested negative for hepatitis C
atitis C of 4.1%. These results do not support a recommendation of
ribonucleic acid (RNA) (75.7%), 18 were positive (3.2%), and 118
planned cesarean to reduce vertical transmission of hepatitis C
infants were not tested or were lost to follow-up (21.1%). The overall
infection.
vertical transmission rate is 18 of 441 (4.1%, 95% confidence interval
2.3% to 5.9%). The vertical transmission rate for infants following Key words: hepatitis C infection, vertical transmission

Cite this article as: McMenamin MB, Jackson AD, Lambert J, et al. Obstetric management of hepatitis C-positive mothers: analysis of vertical transmission in 559
mother-infant pairs. Am J Obstet Gynecol 2008;199:315.e1-315.e5.

H epatitis C (HCV) is an important

clinical infection, affecting an esti-
mated 170 million people worldwide or for infants and children. Following the
and risk factors antenatally for vertical
transmission. Vertical transmission rates
for hepatitis C viral infection range from
3% of the global population.1 It is a ma- introduction of blood product screen- 5% to 10% in reported studies5-15 and
jor worldwide public health issue and is ing, vertical transmission has emerged as are higher in infants born to mothers
documented as a significant cause of the primary route of infection in infancy. coinfected with HIV.7,8,16-18
acute and chronic hepatitis, liver cirrho- Antenatal hepatitis C infection rates vary Selective antenatal HCV screening is
sis, and hepatocellular carcinoma. worldwide, from 1% to 2.5% in Europe used on the basis of risk factors for expo-
The primary transmission route in to more than 10% in some sub-Saharan sure to the virus, such as a history of in-
adults is through needle sharing during countries.1-6 Studies have shown the travenous drug abuse. Routine universal
intravenous drug injection. Before blood prevalence to be as high as 40% in some antenatal screening for hepatitis C infec-
product screening for hepatitis C was in- parts of Egypt.7 tion has been found not to fulfill all cri-
troduced, transfusion represented an Infant infection rates are now depen- teria required of a screening program3
important route of HCV transmission dent on numbers of mothers infected and has not been shown to be cost
effective.19
From the Department of Obstetrics and Gynaecology, National Maternity Hospital, In the case of HIV and hepatitis B ante-
University College Dublin School of Medicine and Medical Science (Drs McMenamin and natal infection, vertical transmission can
Prof McAuliffe); University College Dublin School of Public Health and Population Science be reduced with the use of antiretrovirals
(Dr Jackson) and the National Virus Reference Laboratory University College Dublin (Dr or postnatal administration of immuno-
Hall); Rotunda Hospital (Drs Jackson, Lambert, and Coulter-Smith); and Our Lady’s globulin and vaccination. Cesarean deliv-
Children’s Hospital, Crumlin (Dr Butler), Dublin, Ireland. ery has been recommended for HCV-pos-
Presented at the 28th Annual Meeting of the Society for Maternal-Fetal Medicine, Dallas, TX, Jan. itive women coinfected with HIV;
28-Feb. 2, 2008. however, to date, there are no proven strat-
Received Feb. 27, 2007; revised April 19, 2008; accepted May 27, 2008. egies to reduce vertical HCV transmis-
Reprints: Prof Fionnuala M. McAuliffe, MD, FRCPI, MRCOG, DCH, University College Dublin sion.20 The available therapies are contra-
School of Medicine and Medical Science, Obstetrics and Gynaecology, University College Dublin,
indicated in pregnancy: ribavirin for its
National Maternity Hospital, Holles St, Dublin 2, Ireland.
teratogenic effects and interferon for its
0002-9378/$34.00 • © 2008 Mosby, Inc. All rights reserved. • doi: 10.1016/j.ajog.2008.05.021
possible effects on fetal growth.21
The aim of this study was to review
For Editors’ Commentary, see Table of Contents obstetric management and determine
the vertical transmission rate of hepatitis

SEPTEMBER 2008 American Journal of Obstetrics & Gynecology 315.e1

SMFM Papers www.AJOG.org

Amplicor HCV assay (Roche, New Jersey).

TABLE 1 An in-house reverse transcriptase-PCR as-
Patient demographic details and obstetric data on hepatitis say, which detects more than 100 copies/
C-positive mothers and infants (n ⴝ 559) mL, was the test used for PCR positivity,
Total group n (%) and a threshold of 100 copies/mL was used
Mother HIV positive 18 (3.2%) to constitute positivity in this study. Viral
..............................................................................................................................................................................................................................................
Mother HBV positive 3 (0.5%) load was measured by branched deoxyri-
..............................................................................................................................................................................................................................................
bonucleic acid signal amplification
Mother hepatitis C RNA positive 295 (52.8%)
.............................................................................................................................................................................................................................................. (Chiron, Novartis Vaccines and Diagnos-
Mother hepatitis C RNA negative 166 (29.7%) tics, Emeryville, CA), and HCV genotype
..............................................................................................................................................................................................................................................
Vaginal delivery/emergency cesarean 515 (92.1%) was identified by restriction fragment
..............................................................................................................................................................................................................................................
Planned prelabor cesarean 44 (7.9%) length polymorphism.
..............................................................................................................................................................................................................................................
Once the cohort was identified, demo-
Gestation (wks), median (range) 39 (28-42 wks)
.............................................................................................................................................................................................................................................. graphic details and antenatal and deliv-
Birthweight (kg), mean (SD) 3.06 (0.591) ery data were obtained from the hospital
..............................................................................................................................................................................................................................................
Maternal age (y), median (range) 26 (16-44) computerized systems and analyzed. A
..............................................................................................................................................................................................................................................
Nationality, Irish 458 (81.9%) ␹2 analysis was used to assess differences
..............................................................................................................................................................................................................................................
between groups, with P ⬍ .05 considered
Intrapartum procedures FSE and FBS 24 (4.3%)
.............................................................................................................................................................................................................................................. statistically significant.
FBS, fetal scalp sampling intrapartum; FSE, fetal scalp electrode; HBV, hepatitis B positive. The hospital ethical committee deter-
McMenamin. Obstetric management of hepatitis C-positive mothers. Am J Obstet Gynecol 2008.
mined that specific ethical approval was
not required for this retrospective audit
C virus in 2 tertiary level maternity units electrode, fetal scalp blood sampling, of outcome of HCV-exposed children.
over a 5-year period. mid- to high-cavity instrumental deliv-
ery. Immediate cord clamping and bath- R ESULTS
M ATERIALS AND M ETHODS ing at birth is also performed. Infants are Between Jan. 1, 2001, and Dec. 31, 2005,
This is a retrospective, 2-center analysis routinely tested for HCV RNA at 6 weeks there were 74,629 deliveries (greater
of 74,629 deliveries during a 5 year pe- of age at the maternity hospital and then than 500 g birthweight) at the 2 mater-
riod in Dublin, Ireland. The National referred to the national pediatric infec- nity hospitals. A total of 26,390 tests were
Maternity Hospital and the Rotunda tious diseases clinic at which HCV RNA performed for HCV antibody: 35% of
Hospital are 2 tertiary level stand-alone testing is repeated at 6 months and RNA the antenatal population (26,390 of
maternity units in Dublin, Ireland, each and antibody testing at 18 months of age. 74,629). Of these, 2.1% of pregnant
with 7000-8000 deliveries annually. Hepatitis C-positive mothers were women (545 of 26,390) tested positive
Antenatal HIV screening is offered to all identified by determining those with for hepatitis C. This represents a mini-
mothers, with an uptake of 98%. Selective positive samples in the National Virus mum antenatal hepatitis C infection rate
HCV screening based on risk factors for Reference Laboratory where the sample of 0.7% (545 of 74,629).
hepatitis C infection (mother’s or partner’s originated in either of the 2 maternity Of 545 mothers testing positive for
history of intravenous drug abuse, partner hospitals studied. Their infants’ serology hepatitis C, 66 had a miscarriage (12%).
known to be hepatitis C positive, possible was followed up. A positive neonatal re- There were 5 stillbirths and 1 neonatal
transmission via infected blood products, sult was defined as positive neonatal hep- death (6 of 565, 1%), all born to Irish
tattoos, multiple body piercing) is offered atitis C RNA after 1 month of age, and a mothers. The neonatal death occurred in
to antenatal patients. Those who were hep- negative result was defined as negative an infant born at 37 weeks with a birth-
atitis C positive antibody were recalled for HCV RNA after 1 month of age.22 weight of 1.725 kg, and the stillbirths oc-
ribonucleic acid (RNA) assessment and All serological testing and molecular curred at 25 weeks (660 g), 33 weeks
liver function tests and referred to the local testing for HCV was performed at the Na- (1.956 kg), 35 weeks (2.42 kg), 25 weeks
hepatology clinic. tional Virus Reference Laboratory, Uni- (820 g), and 27 weeks (700 g). Perinatal
Polymerase chain reaction (PCR) as- versity College, Dublin. Hepatitis C anti- mortality rate was thus 6 of 545 (11 of
sessment was performed once during body is detected using 1 or more 1000), consistent with general hospital
pregnancy. Cesareans were performed commercial third-generation enzyme im- rates. Including only those deliveries in
only for usual obstetric indications in munoassays (Ortho-Clinical Diagnostics, which the outcome was a liveborn infant,
hepatitis C-positive, human immunode- Chicago, IL; Abbott Laboratories, Chi- the number of deliveries was 559 born to
ficiency virus (HIV)-negative women. cago, IL; Axysm, Abbott Diagnostics, Chi- 473 mothers.
Standard labor management is to avoid cago, IL). Confirmation of antibody status
the following, regardless of maternal was determined using the RIBA-3 assay Demographics
RNA status: prolonged rupture of mem- (Ortho Diagnostic Systems, Chicago, IL). Patient demography is shown in Table 1.
branes, the application of a fetal scalp Hepatitis C RNA was detected using the Nationality of the patients included 458

315.e2 American Journal of Obstetrics & Gynecology SEPTEMBER 2008

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Irish (82%), 30 European Union nation-

als (5.4%, including 25 Eastern Euro- TABLE 2
pean), 54 non-European Union nation- Factors affecting vertical transmission of hepatitis C infection
als (9.7%, including 17 Nigerian, 11 Estimated vertical P
Asians, and 12 from Ukraine and Rus- Factor n transmission ratea value
sia), and 17 (3%) of unknown/unre- Babies whose mothers were hepatitis C positive 559
..............................................................................................................................................................................................................................................
corded nationality. Baby follow-up available, n 441 4.1% (18/441)
..............................................................................................................................................................................................................................................
Patient demographics were similar to Maternal hepatitis C RNA status
that of our general antenatal population .....................................................................................................................................................................................................................................

with similar numbers of Irish and non- Positive 295 7.1% (18/255) b
⬍.05 b
.....................................................................................................................................................................................................................................
b
national mothers studied. However, of Negative 155 0% (0/117)
.....................................................................................................................................................................................................................................
note there was a 2-fold increased rate of Not known 98 0% (0/69)
..............................................................................................................................................................................................................................................
preterm delivery in the group studied HIV status
(11% less than 37 weeks and 4% less than .....................................................................................................................................................................................................................................
b b
34 weeks of gestation). The preterm de- Positive 18 5.9% (1/17) NS
.....................................................................................................................................................................................................................................
b
livery rate for the general antenatal pop- Negative 534 4.1% (17/418)
.....................................................................................................................................................................................................................................
ulation in the time period studied was Not known 7 0% (0/6)
..............................................................................................................................................................................................................................................
5.7% less than 37 weeks.4,5
Mode of delivery
.....................................................................................................................................................................................................................................

Mode of delivery Vaginal delivery/emergency cesarean 515 4.2% (17/408) NS

.....................................................................................................................................................................................................................................
Overall, the cesarean rate was 20.7%. Planned cesarean 44 3.0% (1/33)
..............................................................................................................................................................................................................................................
Forty-four planned cesareans were per- a
Denominator is the numbers of babies in which neonatal follow-up was available in each group.
formed (44 of 559, 7.9%), and 72 emer- b
P value refers to comparison of these 2 values.
gency cesareans were carried out (72 of McMenamin. Obstetric management of hepatitis C-positive mothers. Am J Obstet Gynecol 2008.
559, 12.9%). The instrumental delivery
rate was 9.5% (10 forceps deliveries were
performed, 41 infants were delivered by negative, and 118 of 559 infants (21.1%) (95% CI, 6.6% to 11%). To assess the
ventouse, and 2 infants were delivered by did not get tested or were lost to follow- effect of labor on vertical transmission,
ventouse/forceps). up. Including those neonates in which vaginal delivery was combined with
follow-up data are available, the vertical those delivered by emergency cesarean in
Intrapartum procedures transmission rate is thus 18 of 441 (4.1%, labor and compared with those for
A total of 4.3% of infants had intrapartum 95% confidence interval [CI] 2.3 to whom a prelabor planned cesarean was
procedures performed. One intrapartum 5.9%). Infant HCV RNA samples were performed (Table 2). No significant dif-
fetal blood sample was performed (mater- tested at a median 6 weeks after delivery, ference in vertical transmission was
nal HCV RNA status unknown, baby HCV mean 12.5 weeks (range 4-166 weeks). noted between these 2 groups (4.2%,
RNA negative), and 23 babies had fetal Six infants were tested only at birth and 4 95% CI, 2.3% to 6.2%, 17/408 vs 3%
scalp electrode applied. Where the fetal infants only before 4 weeks of age and 95% CI, 0% to 8.8%, 1/33, p⫽NS).
scalp electrode was applied, the mother thus were deemed to be of indeterminate Further analysis of effect of mode of
had HCV RNA detected in 4 cases and not status and included in the unknown delivery on transmission rate was con-
detected in 11 cases, and the maternal group. Five infants were tested for HCV fined to those infants delivered to moth-
HCV RNA status was unknown in 8 cases. RNA between 4 and 6 weeks old, with the ers with PCR positivity antenatally, and
None of these infants subsequently was majority of samples taken at 6-week fol- again the difference was not significant
identified as HCV RNA positive (11 tested low-up (274 infants). Twenty-two were (vaginal delivery/emergency cesarean,
negative, and 12 did not have infant HCV tested between 7 and 12 weeks, 33 tested 7.2% [95% CI, 3.9% to 10.5%], 17 of 236
RNA checked). between 13 and 24 weeks, 48 at 24 weeks, vs planned cesarean, 5.3%, 1/19 [95%
and 49 infants were tested for PCR status CI, 0% to 15.3%, P ⫽ NS]).
Detection of maternal at older than 24 weeks old.
hepatitis C RNA Vertical transmission of infants
Of the 559 liveborn infants, maternal Vertical transmission according born to mothers HCV RNA positive
hepatitis C RNA was detected in 295 to mode of delivery In cases in which the maternal HCV
pregnancies (52.8%), undetected in 166 Based on 441 infants with available data, RNA was positive, there was a vertical
(29.7%), and not tested in 98 (17.5%). the vertical transmission rate for infants transmission rate of 7.1% (95% CI, 6.3 to
delivered vaginally (12 of 352) was 3.4% 7.9%) (18 infants positive, 237 infants
Detection of infant hepatitis C RNA (95% CI, 1.6% to 5.2%); for planned ce- negative, 40 not tested, 18 of 255). In
In the postnatal period, 18 of 559 infants sarean (1 of 33), 3% (95% CI, 0% to cases in which the maternal HCV RNA
(3.2%) tested positive for hepatitis C 8.8%); and for those delivered by emer- was negative, the vertical transmission
RNA, 423 of 559 infants (75.7%) tested gency cesarean in labor (5 of 56), 8.9% rate was 0% (0 infant positive, 117 in-

SEPTEMBER 2008 American Journal of Obstetrics & Gynecology 315.e3

SMFM Papers www.AJOG.org

fants negative, 49 not tested, 0 of 117, P RNA, 1 had maternal HIV positive serol- bined with the metaanalysis of Thomas et
⬍ .05). In cases in which maternal HCV ogy antenatally. Seventeen of the 18 in- al,10 then together we report circa 850
RNA status was unknown or not tested fected infants testing positive were born HCV RNA negative mothers who deliv-
for, the vertical transmission rate was 0% to Irish mothers. ered hepatitis C negative infants.
(0 infant positive, 69 infants negative, 29 Vertical transmission in the group of
not tested, 0 of 69). infants in which the mother was HIV
Two hundred thirty-three infants C OMMENT coinfected antenatally was 5.9%. This is
born to mothers HCV RNA positive The antenatal hepatitis C infection rate in lower than published studies, perhaps
(79%) delivered vaginally, 23 (7.8%) by our study was 0.7%, which is comparable because of the high cesarean delivery rate
planned cesarean, and 39 (13.2%) by with that found in other studies in similar in this group, and thus supports the cur-
emergency cesarean in labor. populations. Our vertical transmission rent recommendations for cesarean de-
rate at 4.1% was similar to that in the pub- livery in HIV and HCV coinfected moth-
HIV coinfection lished literature.8-15 This is 1 of the largest ers.20 Other studies have reported 2- to
Eighteen of 559 infants were born to series in the literature.8-10,25-27 3.8-fold higher rates of vertical transmis-
mothers coinfected with HIV, and 3 in- A significant proportion of infants sion in which the mother is coinfected
fants were born to mothers coinfected (21%, n ⫽ 118) were lost to follow-up. with HIV.7,8,16,17
with hepatitis B. All HIV-positive moth- Inclusion of these babies could alter the It has been suggested that the immu-
ers were treated antenatally with highly rates we calculated for vertical transmis- nosuppressive effect of HIV results in a
active antiretroviral therapy (HAART). sion. This reflects some of the difficulties higher HCV viral load. We noted no dif-
One infant tested positive for hepatitis C encountered in the management of this ference in hepatitis C vertical transmis-
RNA in which the mother was coinfected group of patients. Despite the input of sion between those coinfected with HIV
with HIV, and 1 infant did not attend for drug liaison nurses and social workers, and those not coinfected with HIV. This
testing. The infected infant of the mother this group of mothers tend to be poor suggests that antenatal treatment with
coinfected with HIV delivered by emer- hospital attenders. Similar noncompli- HAART, which, by restoring immune
gency cesarean at 35 weeks to an Irish ance with neonatal follow-up has been function, may reduce degree of HCV
mother with a birthweight of 2.28 kg. In found in other studies, with a default rate viremia, resulting in a lower risk of hep-
the cases in which the mother was coin- for neonatal sampling ranging from 8% atitis C transmission, as noted in other
fected with hepatitis B, 1 infant tested to 50%.11,12,28 This is certainly an area studies.32 The numbers of our study did
negative for hepatitis C RNA and 2 were that requires improvement. not allow us to make any significant con-
not tested. Vertical transmission rate in The main risk factor identified for verti- clusions about hepatitis C vertical trans-
which the mother was hepatitis C/HIV cal transmission was maternal hepatitis C mission rates among women both hepa-
coinfected, compared with HCV-posi- viremia. Mode of delivery did not influ- titis C and HIV positive.
tive/HIV-negative was 5.9% (95% CI, ence vertical transmission rate of hepatitis More controversial is the effect of
0% to 17.2% [1 of 17] vs 4.1%, 95% CI, C. For mothers who tested positive for mode of delivery on vertical transmis-
2.2% to 6.0% [17 of 418], P ⫽ NS). hepatitis C RNA, vertical transmission was sion. In our study vertical transmission
In these 2 hospitals, planned cesarean significantly higher at 7.1% when com- was similar when the infants were ex-
is routinely recommended for HIV/ pared with 0% transmission for those who posed to labor, compared with those
HCV coinfected women. In the study tested HCV RNA negative antenatally. born by planned prelabor cesarean in
group of 18 HIV coinfected women, 9 This has been reported previously in the HIV-negative, HCV-positive mothers
had planned cesarean (50%), 5 emer- literature and reflects that viremia holds a (4.2% vs 3.0%). When the analysis was
gency cesarean in labor (27.8%), and 4 higher risk of vertical transmission.13,14,16 confined to mothers who were hepatitis
(22.2%) vaginal delivery. Total cesarean Although there are a few reports of vertical C RNA positive, it again showed no sig-
delivery rate in this group was 77.8% (14 transmission in which the mother did not nificant difference in rates of vertical
of 18). have viremia detected antenatally, this transmission (7.2% vs 5.3%). It is possi-
would seem to be a rare occurrence.29,30 ble that to demonstrate the protective ef-
Infants testing hepatitis C Maternal HCV RNA status can be of ben- fect of cesarean delivery with such low
RNA positive efit in the counseling of patients, and if rates of vertical transmission that a larger
Maternal HCV RNA tests were positive hepatitis C RNA is not detected antena- number of cases controlled for viral load
in all 18 infected infants. Of these 10 de- tally, then the patient can be reassured and would be required to minimize the risk
livered by normal vaginal delivery, 2 de- advised that the risk of vertical transmis- of a type 2 error. Whereas some studies
livered by ventouse, and 6 delivered by sion is minimal. have shown a protective benefit from
cesarean (5 emergency cesarean in labor, Seroconversion in pregnancy has been cesarean delivery,26,33 many have
1 planned cesarean). None had a fetal recognized, however,31 and, therefore, a not.9,25,34,35 Thus, the majority of the
scalp electrode attached or a fetal blood third-trimester negative HCV RNA result published literature would suggest that
sampling performed in labor. Of the in- would be required prior to planning labor mode of delivery is not a key factor influ-
fants testing positive for hepatitis C management. If our numbers are com- encing hepatitis C vertical transmission.

315.e4 American Journal of Obstetrics & Gynecology SEPTEMBER 2008

www.AJOG.org SMFM Papers

A number of areas for improvement 4. Louis FJ, Maubert B, Le Hesran J-Y, Kem- 20. Newell M-L. Pregnancy and HIV infection: A
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fection with parenteral schistosomiasis treat- report for the year 2001-2005. Dublin: Rotunda
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