Kissin et al.

BMC Infectious Diseases 2011, 11:292

http://www.biomedcentral.com/1471-2334/11/292

RESEARCH ARTICLE Open Access

Five-year trends in epidemiology and prevention

of mother-to-child HIV transmission, St.
Petersburg, Russia: results from perinatal HIV
surveillance
Dmitry M Kissin1*, Michele G Mandel1, Natalia Akatova2, Nikolay A Belyakov2, Aza G Rakhmanova3,
Evgeny E Voronin4, Galina V Volkova2, Alexey A Yakovlev5, Denise J Jamieson1, Charles Vitek6, Joanna Robinson7,
William C Miller8 and Susan Hillis1

Abstract
Background: The HIV epidemic in Russia has increasingly involved reproductive-aged women, which may increase
perinatal HIV transmission.
Methods: Standard HIV case-reporting and enhanced perinatal HIV surveillance systems were used for prospective
assessment of HIV-infected women giving birth in St. Petersburg, Russia, during 2004-2008. Trends in social,
perinatal, and clinical factors influencing mother-to-child HIV transmission stratified by history of injection drug use,
and rates of perinatal HIV transmission were assessed using two-sided c2 or Cochran-Armitage tests.
Results: Among HIV-infected women who gave birth, the proportion of women who self-reported ever using
injection drugs (IDUs) decreased from 62% in 2004 to 41% in 2008 (P < 0.0001). Programmatic improvements led
to increased uptake of the following clinical services from 2004 to 2008 (all P < 0.01): initiation of antiretroviral
prophylaxis at ≤28 weeks gestation (IDUs 44%-54%, non-IDUs 45%-72%), monitoring of immunologic (IDUs 48%-
64%, non-IDUs 58%-80%) and virologic status (IDUs 8%-58%, non-IDUs 10%-75%), dual/triple antiretroviral
prophylaxis (IDUs 9%-44%, non-IDUs 14%-59%). After initial increase from 5.3% (95% confidence interval [CI] 3.5%-
7.8%) in 2004 to 8.5% (CI 6.1%-11.7%) in 2005 (P < 0.05), perinatal HIV transmission decreased to 5.3% (CI 3.4%-
8.3%) in 2006, and 3.2% (CI 1.7%-5.8%) in 2007 (P for trend <0.05). However, the proportion of women without
prenatal care and without HIV testing before labor and delivery remained unchanged.
Conclusions: Reduced proportion of IDUs and improved clinical services among HIV-infected women giving birth
were accompanied by decreased perinatal HIV transmission, which can be further reduced by increasing outreach
and HIV testing of women before and during pregnancy.

Background estimates HIV seroprevalence to be 37.2% among this

The HIV epidemic in Russia, historically concentrated group [2]. Although injection drug use remains the driv-
among male injection drug users, continues to grow [1]. ing force of the epidemic in Russia, there is growing evi-
Russia has one of the world’s highest prevalences of dence of its spread outside traditional risk groups to the
injection drug use and one of the world’s largest num- general population [3,4]. The bridging of HIV to indivi-
bers of injection drug users. The Reference Group to duals who never injected drugs primarily occurs through
the United Nations on HIV and Injecting Drug Use unprotected sexual contacts with HIV-infected injection
drug users, most of whom are young and sexually active
* Correspondence: [email protected]
[4,5]. The increase in sexual transmission of HIV dispro-
1
Centers for Disease Control and Prevention, 4770 Buford Highway NE, MS portionately affects women, whose proportion among
K-34, Atlanta, Georgia 30341, USA
Full list of author information is available at the end of the article

© 2011 Kissin et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
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newly registered HIV cases in Russia increased from Methods

13.0% in 1995 to 42.0% in 2008 [6]. Study population and data collection
In the absence of the full range of reproductive health The standard HIV case-reporting system collects annual
services for HIV-infected women, the growing presence data on all HIV cases, including age and gender. Inclu-
of women in the HIV epidemic may increase the num- sion in the standard HIV surveillance requires a thor-
ber of infants exposed to HIV. Although prevention of ough and lengthy clinical evaluation at the City AIDS
mother-to-child HIV transmission is among the highest Center, which provides state-subsidized services for
priorities in Russia, current transmission rates are still HIV-infected persons, including confirmatory testing,
higher than observed in high-income countries, where virologic infant diagnosis, antiretroviral treatment, care
elimination of perinatal HIV infection is a feasible goal and support. Therefore, the number of HIV cases in the
[7,8]. The widespread prophylactic use of highly active general population is severely underestimated [3]. At the
antiretroviral therapy throughout pregnancy, one of the same time, data on HIV among women giving birth are
mainstays of preventing perinatal HIV transmission in quite accurate because nearly all women in St. Peters-
North America and Western Europe, is underutilized in burg and Russia deliver in medical facilities, and there
Russia [9]. Many barriers to effective perinatal preven- has been high coverage with antenatal and natal HIV
tion relate to either behavioral characteristics of HIV- screening, although results were frequently not accessi-
infected women themselves (e.g., lack of family planning ble to guide prevention decisions. In April 2004, the
or prenatal care) or to the quantity and quality of clini- supplemental enhanced perinatal HIV surveillance was
cal services provided to these women and their infants established in maternity hospitals dedicated to providing
during pregnancy, labor and delivery, and the postpar- care for HIV-infected women or women with no or
tum period (e.g., late or inadequate antiretroviral pro- incomplete HIV testing during pregnancy [10]. Data
phylaxis, lack of HIV disease progression monitoring) were collected for all women who were HIV-infected at
[10]. It is unclear whether trends in these behavioral the time of delivery in these hospitals, including basic
and clinical barriers differ among those HIV-infected demographics, prenatal care, birth history, maternal HIV
women who used injection drugs, compared with those testing, antiretroviral therapy and/or prophylaxis, utiliza-
who did not. tion of HIV-related clinical services, substance use, and
St. Petersburg, the second largest Russian city, has the infant HIV serostatus. This enhanced surveillance cov-
highest number of people living with HIV and one of the ered >90% of HIV-infected women giving birth in St.
highest number of deliveries by HIV-infected women in Petersburg (<10% of HIV-infected women deliver at one
Russia [6]. Although the standard HIV case-reporting of the 14 low-risk maternity hospitals that provide deliv-
system is useful for measuring trends over time, it likely ery services primarily for women who have no serious
underestimates the true number of HIV-infected indivi- infectious diseases).
duals because of limited outreach to high-risk groups and
exclusion of HIV-infected inhabitants who are not official Variables and definitions
residents of the city. To supplement the standard HIV Data collected by using standard HIV surveillance
surveillance system with data that would inform preven- allowed calculation of the following: (a) HIV seropreva-
tion programs, an enhanced perinatal HIV surveillance lence among women giving birth based on the propor-
system was established in St. Petersburg to monitor tion of HIV-infected women among all women giving
uptake of prevention activities and rates of perinatal HIV birth in St. Petersburg (by using annual reporting to the
transmission [10]. The objectives of our analyses were to St. Petersburg City Health Committee), and (b) birth
explore five-year trends in factors influencing perinatal rate among HIV-infected women based on the propor-
HIV transmission. By using the standard HIV case- tion of HIV-infected women who gave birth in a given
reporting system, we assessed trends in HIV seropreva- year among all HIV-infected women registered at the
lence among all women giving birth and trends in birth City AIDS Center for that year.
rates among HIV-infected women. Furthermore, we used The enhanced perinatal HIV surveillance system used
enhanced perinatal HIV surveillance among HIV-infected medical record abstraction to provide further data about
women giving birth to explore overall trends in propor- a broader set of indicators for HIV-infected women giv-
tion of women with history of injection drug use before ing birth. Information on the history of injection drug
and during pregnancy; to evaluate trends in social, peri- use before and during pregnancy, maternal age, marital
natal, and clinical factors influencing mother-to-child status, city residence, previous livebirths, and intended-
HIV transmission among women with and without his- ness of pregnancy was self-reported either at admission
tory of injection drug use; and to assess whether these to the maternity hospital or during intrapartum hospita-
changes were accompanied by concurrent reductions in lization (information on maternal age and city residence
perinatal HIV transmission rates. is usually verified at admission, if identification is
Kissin et al. BMC Infectious Diseases 2011, 11:292 Page 3 of 11
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available). For the purposes of the study, injection drug women who received a dual or triple combination regi-
users (IDUs) were defined as women who reported men needed ARV treatment for their own health,
using injection drugs at any point in time, even if they whereas most women who received AZT monotherapy
were not current users. The gestational age was assessed for perinatal prophylaxis did not need ARV treatment
at admission to the hospital by the attending obstetri- for their own health. The infant’s HIV infection status
cian; preterm delivery was defined as delivery at <37 was determined by the case definition for surveillance
weeks gestation. Elective cesarean delivery was defined used by U.S. Centers for Disease Control and Prevention
as planned cesarean delivery performed on the basis of (CDC) for perinatally exposed non-breastfeeding infants
an obstetrical or medical indication before labor; emer- [15]: a) definitively HIV-infected (two or more positive
gency cesarean delivery was defined as cesarean delivery PCR tests using separate blood specimens); b) presump-
performed during labor. tively HIV-infected (one positive PCR and no subse-
The enhanced perinatal HIV surveillance also included quent negative HIV tests); c) definitively HIV-uninfected
information about laboratory tests for HIV-infected (two or more negative PCR tests from separate speci-
women. The Russian Ministry of Health recommends mens obtained at ≥1 month and ≥4 months of age and
HIV testing twice during pregnancy-at the first prenatal no other laboratory evidence of HIV infection); d) pre-
care visit, and again after 34 weeks of gestation [11]. All sumptively HIV-uninfected (two negative PCR tests,
women who were admitted for delivery and did not both at age ≥2 weeks and at least one test at age ≥4
have a negative HIV test after 34 weeks of gestation weeks and no subsequent positive PCR tests; one nega-
(except for women who already had documented HIV tive PCR test performed at ≥8 weeks of age and no sub-
infection) were tested with rapid HIV test (Determine, sequent positive PCR tests; or one positive PCR test
Abbott Laboratories, Abbott Park, IL) [10] and included followed by at least two negative PCR tests with one
in the current analysis if rapid test was positive (HIV test at age ≥8 weeks and no subsequent positive results).
diagnosis at labor and delivery). In addition, pregnant Perinatal HIV transmission was calculated as the pro-
women are tested routinely for hepatitis C virus (HCV) portion of infants who were definitively or presump-
by using anti-HCV enzyme immunoassay and Recom- tively HIV-infected among those who were born alive to
biBest anti-HCV polymerase chain reaction (PCR) test HIV-infected women and had determined HIV status as
(Vector-Best, Novosibirsk, Russia) or COBAS Amplicor of September 2008. Although information about breast-
HCV Monitor test (Roche-Diagnostics, Germany) [12]. feeding after the discharge from the hospital was not
Hepatitis C virus is primarily transmitted through expo- available, local experts believe that most HIV-exposed
sure to infected blood and has been used by some infants received replacement feeding. Therefore, HIV
researchers as a biomarker for injection drug use [13]. It infection in infants almost always represents perinatal
is recommended that all HIV-infected women have HIV transmission. A newborn infant was considered
immunologic and virologic monitoring during pregnancy, abandoned if the paperwork on relinquishment of par-
starting from the first prenatal care visit [11]. CD4 count ental rights was initiated by the mother before discharge
was assessed by using FACSCalibur (BD Biosciencies, from the maternity hospital or if the mother left the
San Jose, CA), and viral load was assessed by using hospital without the newborn.
Abbot RealTime HIV-1 (Abbott Laboratories, Abbott
Park, IL) tests. The values of the last available CD4 and Statistical analysis
viral load test during pregnancy were used in the cur- Data using standard HIV surveillance were calculated
rent analysis. for each calendar year from 2004 to 2008. Data from
In Russia, it is recommended that HIV-infected preg- the enhanced HIV surveillance were analyzed for each
nant women initiate antiretroviral prophylaxis at 22 of the five one-year data collection cycles starting from
weeks of gestation or continue antiretroviral treatment April 13, 2004. For the purposes of this manuscript, we
if they are already on therapy for their own HIV disease presented each year of data as the year when the data
[11,14]. Acceptable antenatal prophylactic regimens collection cycle began (e.g., the data collection cycle that
include AZT monotherapy, dual therapy typically with started on April 13, 2004 and ended on April 12, 2005
AZT and lamivudine (3TC), or triple combination ther- was labeled as 2004 and the data collection cycle that
apy typically with AZT, 3TC, and lopinavir/ritonavir started on April 13, 2005 and ended on April 12, 2006
(AZT monotherapy and AZT + 3TC dual therapy are was labeled as 2005. SAS version 9.2 (SAS Institute Inc.,
acceptable options for prophylaxis when maternal viral Cary, NC) was used for all analyses.
load <1,000 copies/mL). In addition, intravenous AZT The trend analyses of dichotomous variables were
administered to the mother at the onset of labor fol- conducted by using the two-sided c2 test; trend analyses
lowed by 4 weeks of AZT syrup for the infant are of polychotomous (three or higher level) variables were
recommended. During earlier years (2004-2006), most conducted by using the Cochran-Armitage two-sided
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test. The Kruskal-Wallis and the Wilcoxon rank-sum women coinfected with HCV decreased from 70.4% to
tests were used to compare median CD4-cell counts and 50.3% (both P < 0.0001). Although the decreasing pro-
median viral load values. portion of IDUs was accompanied by a smaller propor-
tion of women who reported injection drug use during
Ethical approvals pregnancy among all HIV-infected women (32.1%-
The project was reviewed for human subject concerns 25.5%, P < 0.005, Figure 2), the proportion of IDUs
by the CDC and the St. Petersburg City Health Commit- reporting injection drug use during pregnancy increased
tee and was determined to be public health practice, not (51.6%-62.3%, P < 0.05, Table 1).
research. Therefore, review was not needed by an insti- During the study period, we observed several signifi-
tutional review board. cant changes in the characteristics of HIV-infected
women giving birth. The proportion of women aged >30
Results years increased regardless of injection drug use history
Analyses of the standard HIV surveillance revealed that (2.9%-17.4% among non-IDUs, 2.9%-13.1% among
although the overall number of deliveries in St. Peters- IDUs); similarly and potentially related to this age trend,
burg during 2004-2009 increased, HIV seroprevalence of the proportion of women who had previous live births
women giving birth decreased as follows: 1.1% (466/ increased (20.6%-37.9% among non-IDUs, 26.7%-41.5%
42,846) in 2004; 1.0% (415/41,471) in 2005; 0.8% (346/ among IDUs) (all P < 0.001, Table 1). The majority of
41,815) in 2006; 0.8% (355/46,239) in 2007; 0.7% (357/ women giving birth were married or living in nonmarital
49,978) in 2008; and 0.7% (391/53,798) in 2009 (P < unions and were city residents, and thus eligible for
0.0001). Although the number of identified HIV-infected health-related and social services provided by the city
women in the city increased, the birth rate among HIV- (other HIV-infected women who live in the city but
infected women decreased: 6.9% (466/6,763) in 2004, don’t have official registration are usually eligible only
5.3% (415/7,849) in 2005, 3.9% (346/8,976) in 2006, 3.5% for emergency services, including delivery, but not for
(355/10,125) in 2007, 3.1% (357/11,405) in 2008, and routine HIV treatment, care and support). We observed
3.1% (391/12,695) in 2009 (P < 0.0001, Figure 1). a decreasing trend of unintended pregnancy (52.2%-
According to the enhanced perinatal HIV surveillance 30.2% among non-IDUs, 65.8%-46.0% among IDUs,
system, the number and proportion of IDUs among both P < 0.0001). The proportion of women without
HIV-infected women giving birth decreased from 62.3% prenatal care remained relatively stable, ranging from
in 2004 to 40.9% in 2008; similarly, the proportion of 9.8%-17.7% among non-IDUs, and from 29.5%-42.4%

8%
% HIV+ women giving birth
6.9% among all HIV+ women
7%
% HIV+ women among all
women giving birth
6%
5.3%

5%
3.9%
4% 3.5%
3.1% 3.1%
P<0.0001
3%

2%
1.1% 1.0%
0.8% 0.8% 0.7% P<0.0001
1% 0.7%

0%
2004 2005 2006 2007 2008 2009
Surveillance years
Figure 1 HIV seroprevalence among women giving birth and birth rate among HIV-infected women. Proportion of HIV-infected women
giving birth among all HIV-infected women and proportion of HIV-infected women among all women giving birth, St. Petersburg, Russia, 2004-
2009, standard HIV surveillance.
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Hepatitis C
injection drug use during pregnancy, hepatitis C
80%
Percent with history of injection drug use,

70.4%
70%
History of injection
65.9%
drug use
62.3%
59.4% 58.0%
60% Injection drug use
56.6%
during pregnancy
50.3%
50% 46.1% 45.2% P<0.0001
40.9%
40%
32.1% 33.7% P<0.0001
28.6%
30% 25.9% 25.5%

20%
P=0.0011

10%

0%
2004 2005 2006 2007 2008

Surveillance years
Figure 2 History of injection drug use and prevalence of hepatitis C among HIV-infected women giving birth. History of injection drug
use, history of injection drug use during pregnancy, and prevalence of hepatitis C among HIV-infected women giving birth, St. Petersburg,
Russia, 2004-2008, enhanced perinatal HIV surveillance.

among IDUs. Among women who did receive prenatal 64.9% and 11.0%-52.8%, respectively, both P < 0.0001,
care, we observed the tendency of its earlier initiation: e. Figure 4). Overall, infant follow-up was over 60% for the
g., the proportion of HIV-infected women who started first four years of surveillance (2004-2007) (Table 1). It
prenatal care ≤28 weeks of gestation increased from is important to note that since there is continuous work
60.9% to 66.7% (P < 0.05) among IDUs. Although the to increase follow-up of HIV-exposed infants who do
proportion of preterm deliveries was lower among non- not have determined HIV status, the rate of infant fol-
IDUs, it almost doubled in this group of women (10.7%- low-up for a given year represents outreach activities
19.7%, P < 0.05). The percentage of women with vaginal conducted during the subsequent years.
deliveries decreased (85.0%-76.8% among non-IDUs, The overall rate of perinatal HIV transmission during
86.6%-79.0% among IDUs, both P < 0.05). the 4-year surveillance period was 4.0% (CI 2.7%-5.8%)
Uptake of immunologic and virologic monitoring in and 7.0% (CI 5.5%-9.0%) among non-IDUs and IDUs,
both non-IDUs and IDUs also increased (Table 1). respectively. For all HIV-infected women giving birth in
Overall, in non-IDUs and IDUs combined, the propor- St. Petersburg, perinatal HIV transmission initially
tion of women who received CD4-cell count testing and increased from 5.3% (CI 3.5%-7.8%) in 2004 to 8.5% (CI
viral load testing increased significantly (51.4%-73.6% 6.1%-11.7%) in 2005 (P < 0.05), followed by a decline to
and 8.5%-68.2%, respectively, both P < 0.0001, Figure 3). 5.3% (CI 3.4%-8.3%) in 2006, and 3.2% (CI 1.7%-5.8%) in
Median CD4-cell count remained relatively stable at 565 2007 (P for trend <0.05, Figure 4). The rates of infant
cells/mL (IQR: 422-732 cells/mL), and median viral load abandonment decreased significantly from >15% during
(community viral load) decreased from 9,170 copies/mL the first three years of surveillance (2004-2006) to <10%
(IQR: 1,420-31,100 copies/mL) to 201 copies/mL (IQR: during 2007-2008 (P < 0.01) among IDUs, and remained
60-794 copies/mL) (P < 0.0001). unchanged at 3.0%-5.5% among non-IDUs (Table 1).
Significant changes in the timing and completeness of It is noteworthy that for most of the study years con-
antiretroviral prophylaxis during the five years of sur- sidered, IDUs were more likely than non-IDUs to be
veillance occurred among both non-IDUs and IDUs unmarried, to have unintended pregnancy, later initia-
(Table 1). For the two groups combined, both initiation tion of or no prenatal care, preterm delivery, to receive
of antiretroviral prophylaxis ≤28 weeks gestation and HIV diagnosis in labor and delivery, to have hepatitis C,
dual/triple antiretroviral prophylaxis increased (44.6%- no immunologic and virologic monitoring, lower CD4
 http://www.biomedcentral.com/1471-2334/11/292
Kissin et al. BMC Infectious Diseases 2011, 11:292
Table 1 Demographic, maternal and infant characteristics of HIV-infected women giving birth, by history of injection drug use and surveillance year, St.
Petersburg, Russia, 2004−2008, enhanced perinatal HIV surveillance.
No history of injection drug use History of injection drug use
2004 2005 2006 2007 2008 P- 2004 2005 2006 2007 2008 P-
N = 2091 N = 2331 N = 2461 N = 2691 N = 2641 value2 N = 3451 N = 3041 N = 2101 N = 2221 N = 1831 value2
% (n) % (n) % (n) % (n) % (n) % (n) % (n) % (n) % (n) % (n)
Maternal demographic characteristics and reproductive history
Age .0007
<21 years 34.0 (71) 27.2 (63) 20.7 (51) 13.8 (37) 9.5 (25) <.0001 13.0 (45) 11.5 (35) 6.2 (13) 6.8 (15) 6.0 (11)
21-30 years 63.2 (132) 66.4 (154) 69.1 (170) 75.1 (202) 73.1 (193) 0.0026 84.1 (290) 80.3 (244) 84.8 (178) 82.0 (182) 80.9 (148) 0.5529
>30 years 2.9 (6) 6.5 (15) 10.2 (25) 11.2 (30) 17.4 (46) <.0001 2.9 (10) 8.2 (25) 9.1 (19) 11.3 (25) 13.1 (24) <.0001
Married/Nonmarital union3 85.2 (178) 84.6 (197) 83.7 (206) 80.6 (214) 82.8 (212) 0.2695 77.1 (266) 66.4 (202) 60.0 (126) 65.8 (144) 56.9 (103) <.0001
City resident 62.2 (130) 68.2 (159) 64.5 (158) 64.3 (173) 72.0 (190) 0.1075 76.5 (264) 77.0 (234) 82.8 (173) 76.1 (169) 76.4 (139) 0.9424
Previous livebirth 20.6 (43) 26.3 (61) 26.4 (65) 30.9 (83) 37.9 (100) <.0001 26.7 (92) 42.8 (130) 43.3 (91) 42.8 (95) 41.5 (76) 0.0003
Perinatal characteristics
Unintended pregnancy 52.2 (109) 34.2 (79) 25.4 (62) 27.2 (67) 30.2 (70) <.0001 65.8 (225) 63.8 (192) 55.1 (109) 52.2 (105) 46.0 (63) <.0001
Start of prenatal care
≤28 weeks 77.5 (162) 82.8 (193) 85.4 (210) 84.8 (228) 83.7 (221) 0.0826 60.9 (210) 51.3 (156) 55.7 (117) 66.2 (147) 66.7 (122) 0.0214
>28 weeks 4.8 (10) 3.9 (9) 4.9 (12) 2.6 (7) 4.2 (11) 0.5403 6.4 (22) 6.3 (19) 4.3 (9) 3.2 (7) 3.8 (7) 0.0508
None 17.7 (37) 13.3 (31) 9.8 (24) 12.6 (34) 12.1 (32) 0.1136 32.8 (113) 42.4 (129) 40.0 (84) 30.6 (68) 29.5 (54) 0.1428
Injection drug use during N/A N/A N/A N/A N/A N/A 51.6 (178) 59.5 (181) 61.9 (130) 56.8 (126) 62.3 (114) 0.0387
pregnancy
Preterm delivery 10.7 (22) 15.7 (36) 14.4 (35) 15.2 (40) 19.7 (51) 0.0199 31.8 (108) 36.0 (108) 34.8 (72) 31.7 (70) 38.1 (69) 0.4036
Mode of delivery
Elective cesarean delivery 5.3 (11) 7.4 (17) 7.4 (18) 8.0 (21) 7.7 (20) 0.3419 2.3 (8) 4.0 (12) 3.9 (8) 4.5 (10) 5.5 (10) 0.0684
Emergency cesarean delivery 9.7 (20) 9.6 (22) 12.4 (30) 13.4 (35) 15.4 (40) 0.0233 11.1 (38) 6.3 (19) 4.8 (10) 9.1 (20) 15.5 (28) 0.2114
Vaginal 85.0 (175) 83.0 (190) 80.3 (195) 78.6 (206) 76.8 (199) 0.0124 86.6 (296) 89.7 (271) 91.3 (189) 86.4 (191) 79.0 (143) 0.0347
Maternal clinical characteristics
HIV Diagnosis at 12.5 (26) 11.2 (26) 6.9 (17) 8.2 (22) 9.9 (26) 0.2089 18.6 (64) 26.0 (79) 22.4 (47) 21.2 (47) 18.6 (34) 0.8095
Labor/Delivery
Hepatitis C 39.2 (82) 33.9 (79) 28.1 (69) 32.7 (88) 24.2 (64) 0.0013 89.3 (308) 90.5 (275) 96.2 (202) 88.7 (197) 88.0 (161) 0.7412
CD4 Test Performed 57.9 (121) 61.8 (144) 73.6 (181) 83.3 (224) 80.3 (212) <.0001 47.5 (164) 39.1 (119) 42.4 (89) 55.0 (122) 63.9 (117) <.0001
CD4 count
≤200 0.8 (1) 2.8 (4) 2.8 (5) 3.1 (7) 2.8 (6) 0.3366 3.1 (5) 5.0 (6) 6.7 (6) 9.0 (11) 8.6 (10) 0.0200
201-350 14.1 (17) 9.7 (14) 9.4 (17) 10.3 (23) 9.0 (19) 0.2599 12.8 (21) 8.4 (10) 13.5 (12) 8.2 (10) 12.8 (15) 0.8713
>350 85.1 (103) 87.5 (126) 87.9 (159) 86.6 (194) 88.2 (187) 0.5740 84.2 (138) 86.6 (103) 79.8 (71) 82.8 (101) 78.6 (92) 0.1771
Viral Load Test Performed 10.0 (21) 18.1 (42) 33.7 (83) 54.7 (147) 75.4 (199) <.0001 7.5 (26) 7.9 (24) 20.5 (43) 32.4 (72) 57.9 (106) <.0001
Viral load

Page 6 of 11
>10,000 42.9 (9) 23.8 (10) 22.9 (19) 18.4 (27) 8.5 (17) <.0001 42.3 (11) 54.2 (13) 23.3 (10) 22.2 (16) 12.3 (13) <.0001
1,001-10,000 38.1 (8) 42.9 (18) 36.1 (30) 26.5 (39) 10.1 (20) <.0001 34.6 (9) 29.2 (7) 32.6 (14) 34.7 (25) 16.7 (18) 0.0362
≤1,000 19.1 (4) 33.3 (14) 41.0 (34) 55.1 (81) 81.4 (162) <.0001 23.1 (6) 16.7 (4) 44.2 (19) 43.1 (31) 70.8 (75) <.0001
 http://www.biomedcentral.com/1471-2334/11/292
Kissin et al. BMC Infectious Diseases 2011, 11:292
Table 1 Demographic, maternal and infant characteristics of HIV-infected women giving birth, by history of injection drug use and surveillance year, St.
Petersburg, Russia, 2004?−?2008, enhanced perinatal HIV surveillance. (Continued)
Prevention of mother-to-child transmission and infant abandonment
Start of prenatal antiretroviral
therapy
≤28 weeks 44.9 (92) 56.1 (129) 67.1 (161) 72.6 (188) 72.3 (185) <.0001 44.4 (152) 35.9 (107) 40.3 (81) 50.7 (109) 54.2 (96) 0.0032
>28 weeks 34.2 (70) 24.4 (56) 18.8 (45) 10.8 (28) 9.8 (25) <.0001 19.0 (65) 17.5 (52) 12.4 (25) 7.9 (17) 7.9 (14) <.0001
None 21.0 (43) 19.6 (45) 14.2 (34) 16.6 (43) 18.0 (46) 0.2958 36.6 (125) 46.6 (139) 47.3 (95) 41.4 (89) 37.9 (67) 0.7900
Type of antiretroviral prophylaxis
Full course dual/triple ARV 13.9 (29) 15.0 (35) 18.7 (46) 55.8 (150) 59.1 (156) <.0001 9.3 (32) 5.3 (16) 17.6 (37) 41.9 (93) 43.7 (80) <.0001
prophylaxis4
Full course AZT prophylaxis5 61.2 (128) 59.7 (139) 64.2 (158) 22.7 (61) 20.5 (54) <.0001 50.4 (174) 45.1 (137) 33.3 (70) 16.2 (36) 16.9 (31) <.0001
Incomplete ARV prophylaxis6 24.9 (52) 25.3 (59) 17.1 (42) 21.6 (58) 20.5 (54) 0.1534 40.3 (139) 49.7 (151) 49.1 (103) 41.9 (93) 39.3 (72) 0.6076
Infant follow-up 75.5 (154/ 69.6 (156/ 71.7 (172/ 66.5 (173/ 41.8 (107/ <.0001 84.7 (282/ 78.9 (232/ 82.8 (168/ 66.1 (142/ 32.8 (58/ <.0001
204) 224) 240) 260) 256) 333) 294) 203) 215) 177)
Perinatal HIV transmission7 3.9 (6/154) 5.8 (9/156) 3.5 (6/172) 2.9 (5/173) NA 0.4250 6.0 (17/282) 10.3 (24/ 7.1 (12/168) 3.5 (5/142) NA 0.3851
232)
Infant abandonment 5.5 (11/202) 3.2 (7/221) 3.0 (7/237) 4.3 (11/257) 3.5 (9/255) 0.5531 15.6 (51/ 20.2 (55/ 18.8 (33/ 9.8 (20/205) 9.9 (17/ 0.0090
326) 273) 176) 172)
Petersburg, Russia, 2004-2008, enhanced perinatal HIV surveillance.
1
N varies due to missing data.
2
P-value from Cochran-Armitage two-sided test.
3
Compared with never married, widowed/divorced or unknown
4
Dual (typically AZT + 3TC) or triple (typically AZT+3TC+LPV/r) ARV prenatally, intravenous AZT intranatally and AZT syrup neonatally
5
AZT monotherapy prenatally, intravenous AZT intranatally and AZT syrup neonatally
6
Single-doze NVP intranatally and/or NVP syrup (or incomplete course of AZT syrup) neonatally
7
Delayed establishment of infant HIV status for many infants born in 2008 did not allow calculation of perinatal HIV transmission.

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Figure 3 CD4-cell count and viral load testing among HIV-infected women giving birth. CD4-cell counts and percentage covered by
immunologic monitoring, viral load and percentage covered by virologic monitoring, HIV-infected women giving birth, St. Petersburg, Russia,
2004-2008, enhanced perinatal HIV surveillance.

70%

60%

50%

40%

Start of prenatal ARV ”

30% weeks
Full course dual/triple
20% ARV prophylaxis
Perinatal HIV
8.5%
transmission
10% 5.3%
5.3%
3.2%

0%
2004 2005 2006 2007 2008
Surveillance years
Figure 4 Timing and completeness of antiretroviral prophylaxis and perinatal HIV transmission. Percentage of HIV-infected women who
started prenatal ARV ≤28 weeks gestation and received a full course dual/triple ARV prophylaxis, rate of perinatal HIV transmission, St.
Petersburg, Russia, 2004-2008, enhanced perinatal HIV surveillance.
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count, later or incomplete antiretroviral prophylaxis, prophylaxis were probably the main contributors [9].
higher rates of perinatal transmission and infant aban- Other factors that may have contributed to the decrease
donment (Table 1). in perinatal HIV transmission include a lower rate of
unintended pregnancies, earlier initiation of prenatal
Discussion care, and improved immunologic and virologic HIV
These analyses of five years of data from standard and monitoring. However, not all women had the benefits of
enhanced perinatal HIV surveillance provide important improved clinical services. The steady proportion of
information about trends in the epidemiology and pre- women who did not receive prenatal care and ARV pro-
vention of mother-to-child HIV transmission in St. phylaxis, and the increasing trend of injection drug use
Petersburg-one of the cities in Russia most affected by during pregnancy among IDUs, both indicate that out-
HIV. We observed a significant decrease in births reach programs are not reaching all women.
among all HIV-infected women, and a decrease in IDUs Standard HIV surveillance in pregnant women pro-
among HIV-infected women giving birth. Regardless of vides important data on trends of the epidemic and
injection drug use history, we noted impressive improve- overall effectiveness of preventive measures [17], yet
ments in the uptake of clinical services by HIV-infected contributes minimally to identifying specific areas for
women giving birth, such as earlier initiation of prenatal programmatic improvement. Enhanced perinatal surveil-
care, fewer unintended pregnancies, higher uptake of lance, on the other hand, provides supplementary
immunologic and virologic monitoring, earlier initiation detailed information on the mother-infant pair, includ-
and more complete antiretroviral prophylaxis. Most sig- ing risk factors, clinical services, and laboratory data,
nificantly, these improvements in clinical services were which assists timely evaluation of perinatal prevention
followed by a decrease in the rates of mother-to-child efforts [18,19]. It can be linked with other systems or
HIV transmission from 2005 to 2007. registries, such as, for example, maternal and infant
Our data show that in contrast to the increasing birth records at the City AIDS Center. The annual cost of
rate in the general population of women in St. Peters- enhanced perinatal surveillance in St. Petersburg was
burg, HIV-infected women are having fewer births. The approximately $20,000. If scaled up to a total of five
declining birth rate among HIV-infected women may be metropolitan areas with highest HIV seroprevalence (i.e.,
a result of increasing age of these women or indicate a Samara, Irkutsk, Yekaterinburg, Orenburg) [6], enhanced
decrease in their fertility desires, and/or improved family perinatal surveillance may provide valuable national data
planning because no increase of abortions was observed on the risk factors for perinatal HIV transmission for
in this population during the same time period (personal considerably less than one percent of the amount spent
communication with Dr. Nikolay Belyakov, Director, St. on HIV prevention in Russia [20]. In St. Petersburg,
Petersburg City AIDS Center, where 90% of abortions enhanced perinatal surveillance was critical in identify-
among HIV-infected women are performed). During the ing areas needing improvement, such as limited use of
last two years of assessment, many HIV-infected women effective family planning [21], low infant follow-up [10],
of reproductive age in St. Petersburg received free family and delayed and less effective antiretroviral prophylaxis
planning services, including the contraceptives of their [9]. Immediate, focused attention by the local public
choice [16]. These programmatic improvements likely health leadership made it possible to address each of
contributed to the decreases in the birth and unintended these issues in a timely fashion through program and
pregnancy rates among HIV-infected women. In addi- policy improvements. As a result, we observed fewer
tion, we observed a decreasing proportion of IDUs unintended pregnancies, improved infant follow-up, ear-
among HIV-infected women giving birth, which might lier and more effective antiretroviral prophylaxis, and,
be explained by ongoing heterosexual transmission of subsequently, fewer HIV-infected infants.
HIV from HIV-infected male IDUs and some heterosex- Our assessment supports the evidence from other
ual transmission outside of the traditional high-risk countries-improvement of clinical services for HIV-
groups. The improvements of clinical HIV services, infected women results in significant reductions in peri-
albeit more pronounced among women without a his- natal HIV transmission. The success of high-income
tory of injection drug use, were evident for both non- countries in reducing perinatal HIV transmission was
IDUs and IDUs. attributed to increased coverage of HIV-infected preg-
Perinatal HIV transmission during the first year of nant women by combination antiretroviral prophylaxis,
surveillance increased, coinciding with no improvements elective cesarean delivery, and avoidance of breastfeed-
in timing or completeness of antiretroviral prophylaxis. ing [22-24]. Despite a number of challenges in low- and
The subsequent decrease of perinatal transmission was middle-income countries [25,26], a few reports provide
most likely due to multiple factors, although earlier evidence that it is possible to reduce perinatal HIV
initiation and higher effectiveness of antiretroviral transmission with implementation of comparable
Kissin et al. BMC Infectious Diseases 2011, 11:292 Page 10 of 11
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preventive measures [27,28]. In Ukraine, which had a prevention measures are effective. In addition, this
healthcare system similar to the one in Russia, but had report demonstrates the vital role of enhanced perinatal
lower coverage by combination antiretroviral prophy- surveillance in driving programmatic improvements.
laxis at the time of assessment, perinatal HIV transmis- Scaling up enhanced perinatal surveillance in other key
sion was reduced in half in five years (from 15.2% in Russian regions will allow effective improvement in
2001 to 7.0% in 2006) by strengthening clinical services local perinatal HIV programs and provide useful data to
provided to HIV-infected women [27]. In Russia, where monitor trends in perinatal HIV transmission. Our data
the rate of perinatal HIV transmission has been rela- also suggest strategies to further reduce perinatal trans-
tively stable at 6%-8%, the St. Petersburg experience mission, which include widespread opt-out HIV testing
suggests that it is feasible to attain low rates of mother- of women before and during pregnancy and increased
to-child transmission similar to U.S. and Western Eur- outreach to high-risk HIV-infected women to avoid con-
opean rates. Since our observation of the impact of early sequences of drug use and facilitate their early contact
and effective antiretroviral prophylaxis on perinatal HIV with and retention in the healthcare system when they
transmission is consistent with findings from rando- become pregnant or are planning pregnancy. In addi-
mized controlled trials from various parts of the world tion, further reductions in perinatal HIV transmission
[29], the data described in this report may be generaliz- will require full access to effective and affordable family
able to other middle-income countries with a large pro- planning services for HIV-infected women. We believe
portion of hospital deliveries and replacement feeding that Russia has the tools to successfully prevent perina-
among HIV-infected women giving birth. tal HIV. The availability of effective antiretroviral regi-
The results of this assessment should be interpreted in mens, an adequate infrastructure for elective cesarean
light of its strengths and limitations. Strengths of the delivery, and the possibility to safely avoid breastfeeding,
study include almost universal coverage of HIV-infected should make it feasible to reduce and even eliminate
women giving birth by enhanced perinatal surveillance perinatal HIV transmission in Russia.
and standardized data collection methods that allow
trend analyses. Although ours is one of the few reports
Acknowledgements and Funding
to describe trends in critical indicators of perinatal HIV The enhanced perinatal surveillance system in St. Petersburg was established
transmission separately for non-IDUs and IDUs, it is and supported by the Elizabeth Glaser Pediatric AIDS Foundation, the St.
possible that due to social desirability, some women Petersburg City AIDS Center, USAID/Moscow, and CDC. The funding sources
had no role in the study design, data collection, data analysis, data
with a history of injection drug use were misclassified as interpretation, or writing of the report. We would like to thank the following
non-IDUs. In additional subgroup analysis (not shown), individuals for their invaluable support and important contributions to the
critical indicators of perinatal transmission among implementation of enhanced perinatal surveillance system and/or current
analyses: Bernard Branson, Galia Denisheva, Ken Dominguez, Kate Glynn,
women who reported no history of injection drug use Elena Gurvich, Gary Jeng, Natalia Khaldeeva, Elena Kuklina, Julie Lamb, Zoya
but had hepatitis C coinfection more closely resembled Lisitsina, Michael Mansour, Elizabeth Preble, Joanna Robinson, Robin Ryder,
non-IDUs, indicating that the effect of any misclassifica- Mida Samarskaya, Andrey Shved, Elena Stepanova, Olga Talantova, Elena
Vinogradova, Cathy Wilfert.
tion of self-reported injection drug use was likely to The findings and conclusions in this report are those of the authors and do
have been minimal. Another limitation of the study is a not necessarily represent the official position of the Centers for Disease
large proportion of HIV-exposed infants with undeter- Control and Prevention
mined HIV status (e.g., 33.7% during 2007). Previous Author details
analysis showed that characteristics of women whose 1
Centers for Disease Control and Prevention, 4770 Buford Highway NE, MS
infants had known HIV status were similar to that of K-34, Atlanta, Georgia 30341, USA. 2City AIDS Center, 12 Bumazgnaya Street,
St. Petersburg 198020, Russia. 3City Health Committee, 12 Bumazgnaya
the entire population of HIV-infected women. There Street, St. Petersburg 198020, Russia. 4Republican Hospital of Infectious
were, however, some differences: infant HIV status was Diseases Clinical AIDS Center, January 9th Prospect, Ust Izgora 196645, Russia.
5
more likely to be unknown for subgroups with both Botkin Hospital of Infectious Diseases, 3 Mirgorodskaya Street, St. Petersburg
191167, Russia. 6Centers for Disease Control and Prevention, 19 Nizhny Val,
increased (nonresidents and those with late initiation of Kiev 04071, Ukraine. 7Elizabeth Glaser Pediatric AIDS Foundation, 11150 Santa
antiretroviral prophylaxis) and decreased (those using Monica Boulevard, Suite 1050, Los Angeles, California 90025, USA. 8University
injection drugs during pregnancy) risk factors for trans- of North Carolina at Chapel Hill, 2105F McGavran-Greenberg Hall, Chapel Hill,
North Carolina 27599, USA.
mission [9]. Therefore, HIV transmission rates can be
either underestimated or overestimated. Authors’ contributions
All authors contributed to study conception and design; NA, NAB, AGR, EEV,
GVV, AAY contributed to local study implementation; MGM, DMK, SH, DJJ
Conclusion and CV contributed to data analysis and/or interpretation; DMK drafted the
To our knowledge, this report is the first to document a manuscript; all authors reviewed, critically revised, and approved the
successful reduction in perinatal HIV transmission in manuscript.

one of the most affected regions in Russia. Our report Competing interests
provides evidence that targeted and comprehensive HIV The authors declare that they have no competing interests.
Kissin et al. BMC Infectious Diseases 2011, 11:292 Page 11 of 11
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Received: 1 April 2011 Accepted: 27 October 2011 19. Centers for Disease Control and Prevention (CDC): Enhanced Perinatal
Published: 27 October 2011 Surveillance - Participating areas in the United States and dependent areas,
2000-2003. HIV/AIDS Surveillance Supplemental Report. Atlanta 2009.
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