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Confined vulnerability of HIV infection among pregnant women attending antenatal care clinics in Karnataka, India: Analysis of data from the HIV sentinel surveillance 2017
Corresponding author. Scientist-G, Division of Computing and Information Science, ICMR-National Institute of Epidemiology, R-127, 2nd Main Road, TNHB, Ayapakkam, Chennai, 600 077, Tamil Nadu, India.
Affiliations
ICMR-National Institute of Epidemiology, R-127, 2nd Main Road, TNHB, Ayapakkam, Chennai, 600 077, Tamil Nadu, India
HIV Sentinel Surveillance among pregnant women attending antenatal care clinics, ANC-HSS, is used to estimate HIV prevalence among the general population. Despite the declining trend, HIV prevalence among the general population in Karnataka is still higher than the national average (0.22%), with a recent, noticeable stabilization. Demographic analysis on concentrated HIV infection among pregnant women could be potential indicators for targeted HIV interventions among general population as well as and prevention of parent to child transmission (PPTCT).
Objectives
To analyse the demographics of HIV-positive pregnant mothers in Karnataka, thereby identifying the most-at-risk populations (MARP) within the general population.
Methods
In total, 24800 eligible pregnant women aged 15–49 attending the ANC clinic for the first time during the surveillance period (Jan–Mar, 2017) were enrolled. Demographic data and blood samples were collected, recorded and tested for HIV. Age-specific factors associated with HIV prevalence, besides the demographics of the HIV positive pregnant women, were analysed to identify the MARP for targeted HIV interventions.
Results
Comprehensively, none of the demographic factors was significantly associated with HIV prevalence. Nevertheless, analysis of demographics, HIV test history and ART status of HIV-positive pregnant women reveals prominent prevalence patterns. The epidemic was majorly confined within young, less educated, primigravida and rural mothers of low economic status.
Conclusion
ANC-HSS is designed to estimate the HIV prevalence among general population at national, state and district levels and is not reflective of the concentrated epidemic confined to MARP. Identifying the disease pattern specific to MARP is essential for effective targeted interventions and disease management.
HIV prevalence in India is periodically estimated through various national surveillance programs. HIV sentinel surveillance (HSS) initiated by the National AIDS control organization (NACO) in 1998 estimates the HIV prevalence among the general population as well as the HIV high-risk groups (FSW, MSM, IDU, TGs) biennially.
More specifically, male partners/clients of HRGs in sexual contact with their female partners (wife/girlfriend) are the main drivers of disease transmission to the general population, thus acting as the bridge population.
Hence, unprotected heterosexual act is identified as the main mode of HIV transmission to the general population and HIV prevalence among pregnant women (ANC-HSS) is, therefore, considered as a proxy indicator of HIV prevalence among the general population.
In Karnataka, the estimated adult HIV prevalence of 0.81% in 2006 has declined to 0.47% in 2017. Accordingly, the estimated HIV prevalence among ANC clinic attendees in Karnataka was 1.12% in 2006 and has declined to 0.38 in 2017.
and the levels of HIV prevalence vary within districts. In case of Karnataka, the northern districts have consistently recorded higher HIV prevalence among the ANC attendees.
Hence, an in-depth analysis of HSS data of the ANC attendees, might indicate potential association between any of the demographic variables with the infection risks.
The data from HSS among pregnant women has been considered as a key indicator of HIV prevalence among the general population.
Apart from estimation of HIV prevalence and deriving strategies for HIV intervention, analysis of ANC HSS data might provide valuable insights on the socio-demographics of the HIV positive pregnant women, which in turn might lead to indicators such as target groups for HIV interventions among the general populations, as well as measures to ensure complete prevention of mother to child transmission (PMTCT). Documentation of the socio-demographics of the HIV-positive cases has been done for better understanding of the disease profile in order to facilitate improved HIV prevention and management measures.
This paper, thus focuses on understanding the socio-demographics of the pregnant women with higher infection risks and expands into analysing the utilization of ANC and HIV testing services by the pregnant mothers in order to achieve complete PMTCT.
1.1 Surveillance methodology
Study Population: All pregnant women aged between 15 and 49 years who were attending the designated ANC sentinel sites in Karnataka for the first time during the surveillance period were included in the surveillance.
Study Setting: Data and samples were collected for 3 months between January, 2017 and March, 2017, or until the desired sample size was achieved, whichever was earlier. At least two sentinel sites per district; preferably one from urban and the other from rural were chosen.
Sample Size: The sample size was fixed at 400 for each site.
In total, 24775 respondents were included from 62 sites in Karnataka.
Study Design: HSS is a cross-sectional survey that follows consecutive sampling method, linked anonymous testing strategy and the standard two-test protocol. In the consecutive sampling method, all eligible pregnant women, were recruited in the same order in which they attend the ANC, so as to reduce the selection bias. In order to maintain the data-quality, data collection was limited to the first 20 eligible respondents in a sentinel site on a given day.
Variables: Information on socio-demographics as well as their HIV test/ART status, along with blood samples were collected from all eligible respondents Information collected from the respondents were i) Age, ii) Literacy status, iii) Gravida, iv) Duration of Pregnancy, v) Source of Referral vi) Current Residence vii) Duration of Stay at the Current Residence viii) Current Occupation of the Respondent ix) Current Occupation of the Respondent's Spouse x) Migration Status of the Spouse. Information related to respondents' HIV testing/ART status were also included, as follows; i) HIV Test History, ii) Time of the Last HIV Test, iii) Result of the Last HIV Test, iv) Management of HIV Infections v) ART Uptake Status. The variables were designed to analyse the basic socio-demographics and the level of HIV management among the pregnant women. It is believed that the trend observed among the pregnant women reflects the disease trends among the general population. The collected blood samples were tested for HIV biomarkers. The surveillance methodology is guide-lined andstandardized, wherein the data/sample collection and subsequent testing were done by trained personnel as described elsewhere.
Statistical Analysis: Descriptive statistics were used to describe the characteristics of the study samples. Chi-square and Fisher's exact tests were used to find the association between the age-specific variables and HIV prevalence. The logistic regression method was used to find the association between the demographic variables and the risk of HIV infection. All data were analysed using SPSS 26.0.
HIV prevalence among pregnant mothers is considered as proxy for estimation of HIV burden among general population aged between 15 and 49 years. With reference to general population, P ≥ 1% indicates high prevalence, P = 0.5–0.99 indicates moderate prevalence and P < 0.5 indicates low prevalence.
Socio-demographic profile of pregnant women attending ANC clinics in Karnataka:
Analysis of the factors influencing the HIV prevalence, gave insights on the perception and awareness levels of HIV among the pregnant women in Karnataka. The logistic regression found that none of the demographic factors was significantly associated with HIV prevalence, but certain trends were noted. The HIV prevalence was higher among ANC mothers aged between 25 and 49 years (0.47%) than those of 15–24 years (0.33%). HIV prevalence among women with tertiary education (0.47%) was comparable with those with no education (0.46%). HIV prevalence was higher in primi-gravids (0.43%) than multi-gravids (0.33%). Single (unmarried/widow/divorced) mothers (16%) were the most vulnerable to HIV infections than married women (0.36%). Based on the occupation of the respondents, significantly higher prevalence (0.31) of HIV infections was among labourers (agricultural/non-agricultural/skilled/semi-skilled) representing the low-income categories. Significantly higher prevalence (0.69%) of HIV infections was seen among the ANC mothers who indicated their spouse occupation as trucker/local transport worker/hotel staff or who were migrants (bridge population). The consolidated results categorized under the socio-demographical variables are presented in Table 1.
Table 1Category-wise Distribution and HIV Prevalence of pregnant women attending ANC services in Karnataka.
Socio-demographic profile of HIV positive pregnant women attending ANC clinics in Karnataka:
To probe further, the demographics of the HIV positive pregnant women alone were analysed in order to identify the vulnerable cohort and to understand their disease transmission patterns. However, an in-depth analysis of the demographics of the HIV-positive pregnant women reveals more confined disease patterns, strikingly different from that of the overall ANC-HIV pattern. Of the 24775 respondents, 94 were reported to be HIV positive in the current surveillance. In contrary to the overall HIV prevalence trends observed, this analysis revealed the confinement of the HIV infection among the young mothers (53.20%), with education up to secondary level or lesser (68.1%) and primigravids (48.90%). The infected women were majorly from the rural regions (61.3%) and were housewives (81.9%). The occupation of the spouses of the infected respondents majorly corresponded to low-income categories such as labourers/workers/small shop owners (60.6%) and transport workers (18.1%) (Table 2).
Table 2Category-wise Distribution of HIV Positive pregnant women, based on the result of their last HIV test, attending ANC services in Karnataka.
Variable
Group
Result of Last HIV Test (N = 94)
Total
%
Positive
Negative
NA#
94
Age (in years)
15–24
49.10%
64.70%
54.50%
50
53.20%
25–49
50.90%
35.30%
45.50%
44
46.80%
Education
Illiterate
14.50%
5.90%
13.60%
12
12.80%
Up to Std 5
10.90%
0.00%
9.10%
8
8.50%
Std 6 – Std 10
41.80%
58.80%
50.00%
44
46.80%
Std 11 to Undergraduate
30.90%
23.50%
27.30%
27
28.70%
Post Graduate
1.80%
11.80%
0.00%
3
3.20%
Gravida
First
45.50%
41.20%
63.60%
46
48.90%
Second
36.40%
41.20%
22.70%
32
34.00%
Third
14.50%
11.80%
9.10%
12
12.80%
Fourth/More
3.60%
5.90%
4.50%
4
4.30%
Trimester
First
23.60%
23.50%
36.40%
25
26.60%
Second
29.10%
47.10%
50.00%
35
37.20%
Third
47.30%
29.40%
13.60%
34
36.20%
Availed ANC Services
Yes
76.40%
82.40%
36.40%
64
68.10%
No
23.60%
17.60%
63.60%
30
31.90%
Source of Referral
Self-Referral
14.50%
6.30%
18.20%
13
14.00%
Family/Relatives/Neighbours/Friends
27.30%
25.00%
36.40%
27
29.00%
NGO
3.60%
0.00%
0.00%
2
2.20%
Private (Doctor/Nurses)
1.80%
12.50%
0.00%
3
3.20%
Govt. (including, ASHA/ANM)
49.10%
56.30%
40.90%
45
48.40%
ICTC/ART Centre
3.60%
0.00%
4.50%
3
3.20%
Residence
Urban
33.30%
47.10%
45.50%
36
38.70%
Rural
66.70%
52.90%
54.50%
57
61.30%
Resident Occupation
Agricultural Labourer
7.30%
5.90%
18.20%
9
9.60%
Non-Agricultural Labourer
5.50%
0.00%
4.50%
4
4.30%
Domestic Servant
1.80%
0.00%
0.00%
1
1.10%
Skilled/Semiskilled Worker
1.80%
5.90%
0.00%
2
2.10%
Petty Business/Small Shop
0.00%
0.00%
0.00%
0
0.00%
Large Business/Self Employed
0.00%
0.00%
0.00%
0
0.00%
Service (Govt./Pvt.)
0.00%
0.00%
4.50%
1
1.10%
Student
0.00%
0.00%
0.00%
0
0.00%
Hotel Staff
0.00%
0.00%
0.00%
0
0.00%
Truck Driver/Helper
0.00%
0.00%
0.00%
0
0.00%
Local Transport Worker
0.00%
0.00%
0.00%
0
0.00%
Agricultural Cultivator/Landholder
0.00%
0.00%
0.00%
0
0.00%
Housewife
83.60%
88.20%
72.70%
77
81.90%
Spouse Occupation
Agricultural Labourer
12.70%
17.60%
22.70%
15
16.00%
Non-Agricultural Labourer
34.50%
11.80%
27.30%
27
28.70%
Domestic Servant
0.00%
0.00%
0.00%
0
0.00%
Skilled/Semiskilled Worker
3.60%
11.80%
4.50%
5
5.30%
Petty Business/Small Shop
10.90%
23.50%
0.00%
10
10.60%
Large Business/Self Employed
1.80%
11.80%
4.50%
4
4.30%
Service (Govt./Pvt.)
7.30%
0.00%
4.50%
5
5.30%
Student
0.00%
0.00%
0.00%
0
0.00%
Hotel Staff
0.00%
11.80%
4.50%
3
3.20%
Truck Driver/Helper
1.80%
5.90%
9.10%
4
4.30%
Local Transport Worker
20.00%
5.90%
4.50%
13
13.80%
Agricultural Cultivator/Landholder
3.60%
0.00%
9.10%
4
4.30%
Unemployed
0.00%
0.00%
0.00%
0
0.00%
Not Applicable
3.60%
0.00%
9.10%
4
4.30%
Spouse Migration Status
No
94.50%
94.10%
86.40%
87
92.60%
Yes
1.80%
5.90%
4.50%
3
3.20%
NA*
3.60%
0.00%
9.10%
4
4.30%
Ever been tested for HIV
Yes
100.00%
100.00%
0.00%
72
76.60%
No
0.00%
0.00%
100.00%
22
23.40%
Time of Last HIV Test
Tested during current pregnancy
49.10%
70.60%
0.00%
39
41.50%
Tested before current pregnancy
50.90%
29.40%
0.00%
33
35.10%
NA
0.00%
0.00%
100.00%
22
23.40%
Result of Last HIV Test
Positive
100.00%
0.00%
0.00%
55
58.50%
Negative
0.00%
100.00%
0.00%
17
18.10%
NA
0.00%
0.00%
100.00%
22
23.40%
ART Status
Yes
92.60%
0.00%
0.00%
50
53.80%
No
7.40%
0.00%
0.00%
4
4.30%
NA (who were either never tested or not positive when last tested for HIV)
0.00%
100.00%
100.00%
39
41.90%
NA# Denotes the status/result of last HIV test – Never been tested or respondents who did not disclose/collect the result of the last HIV test, NA* Denotes respondents who were never married or with dissolved marriage (Separated/Divorced/Widowed) -Missing responses are included.
Age-specific analysis of the profile of pregnant women attending ANC clinics in Karnataka:
We categorized the respondents into 2 age-groups; 15–24 years and 25–49 years. Since, age is also an eligible criterion; data-sheets with improper age records were considered invalid. Among 15-24-years' group, the highest proportion (N = 54.4%) of respondents were primigravids whereas in 25–49 years’ group the highest proportion were secundigravids. As gravida represents the duration of HIV exposure risks, HIV prevalence among primi-gravida is also a proxy indicator for new infections. A significantly higher prevalence was observed among primi-gravid women aged between 25 and 49 years (0.9%, P = 0.001), attending the ANC centre during the first trimester (0.7%, P = 0.004) when compared to their respective counter-parts (Table 3).
Table 3Factors affecting age-specific HIV Prevalence of pregnant women, attending ANC services, in Karnataka.
Factors
HIV Prevalence (%)
P Value
Age
15-24 Yrs.
25-49 Yrs.
Karnataka
0.3
0.5
0.080
Gravida
First
0.3
0.9
<0.001***
Second
0.3
0.3
0.901
Third
0.4
0.3
0.585
Forth or More
0.0
0.5
0.368
Duration of Pregnancy
First
0.2
0.7
0.004**
Second
0.4
0.4
0.527
Third
0.3
0.4
0.271
History of HIV Testing
Previously Tested
0.4
0.5
0.322
Never Tested
0.2
0.3
0.190
Availed ANC Services during current pregnancy
Yes
0.3
0.4
0.605
No
0.3
0.7
0.015*
*Significantly differed at 5% level (P < 0.05); ** Significantly differed at 0.5% level (P < 0.005); *** Significantly differed at 0.1% level (P < 0.001)
2.1 Variation of HIV prevalence across the districts
At the state-level, ANC HIV prevalence was 0.38% with inter-district variations. It was higher than that of the state average in 9 districts and lesser than the state average in 21 districts which includes zero prevalence at 3 districts. Thirteen out of 30 districts in Karnataka recorded HIV prevalence higher than that of the national average of 0.28%
in which almost all of the North-Karnataka districts were included.
3. Discussion
3.1 State-level HIV prevalence
The HIV prevalence among pregnant mothers in Karnataka was 0.38% indicating a slight increase since 2015 (0.36%). Based on the analysis of the socio-demographic factors of the ANC attendees, none of the factors were significantly associated with the risk of HIV infection (Table 1). Age-specific analysis showed that HIV prevalence was significantly higher among pregnant women aged between 25 and 49 years, as compared to that of 15–24 years (Table 3). Lower HIV prevalence among young mothers is in line with the nation-wide declining trend of the adult HIV prevalence.
This may be attributed to increased awareness on HIV and considerable decrease in high-risk behavior among younger generation, particularly men, thereby reducing the risk of HIV transmission.
Education or economic status or place of residence did not have any significant effect on the overall HIV prevalence at the state-level.
However, focusing on the socio-demographics of the HIV positive-only respondents, higher proportion of the infected mothers were of young age, with literacy up to or below secondary level, of rural residence, being housewives, and with partners belonging to the bridge population/low-income occupational category (Table 2). With respect to the occupation (of both the respondents and their spouses), we could see the confinement of the epidemic within the agricultural and non-agricultural labourers. Concurrently, based on the report on the State epidemiological factsheets,
it is to be noted that about 45.9% of the female sex workers in Karnataka were agricultural or non-agricultural labourers, indicating a potential trend of disease transmission. Likewise, inter-district variations indicate concentration of high HIV prevalence in the northern districts of Karnataka. This could be attributed to the widely prevalent commercial sex practise and the seasonal out-migration of the labourers to the neighbouring districts and states.
In addition, while a major proportion of the infected mothers were house wives, the spouses of considerable proportion of the infected mothers were bridge populations (transport worker/hotel staffs). The declining trends in the HIV prevalence among pregnant women attending antenatal care clinics thus mask the confined vulnerability of HIV infection in Karnataka. The data emphasizes the need to channelize the HIV management programs towards poorly educated adults from rural areas and low economic background, with special focus on the house-wives, agricultural and non-agricultural labourers, transport workers and seasonal migrants.
Availing ANC Services, History of HIV Testing and ART Uptake Status:
The Prevention of Parent to Child Transmission of HIV/AIDS (PPTCT) programme commenced in 2002 has mandated HIV testing to every pregnant woman (universal coverage) in India, so as to cover all estimated HIV positive pregnant women and eliminate transmission of HIV from mother-to-child.
National AIDS Control Organisation, (NACO) Assessment of Prevention of Parent to Child Transmission of HIV (PPTCT) Services Implementation in the States of Andhra Pradesh, Telangana, Karnatka and Tamil Nadu.
NACO, Ministry of Health and Family Welfare, Government of India,
New Delhi2014
For this, all pregnant mothers must report to any of the ANC centres within the first trimester of the pregnancy to ensure risk-free pregnancy and management for high-risk infections such as HIV/TB.
Division, Department of AIDS Control Basic Services Updated Guidelines for Prevention of Parent to Child Transmission (PPTCT) of HIV Using Multi Drug Anti-retroviral Regimen in India.
Department of AIDS Control Basic Services Division, Ministry of Health & Family Welfare, Government of India,
New Delhi2013
At the state-level, about 27.6% of the pregnant mothers had not availed the ANC services previously and about 37.8% had not been tested for HIV. Possible reason could be first-order pregnancy/first trimester of the current pregnancy (Table 1). However, amongst the HIV infected respondents, 20.1% of them had not received any ANC services within the first trimester. About 58.5% of the positive cases were aware of their HIV positive status before their current ANC visit. About 23.4% of the HIV-positive mothers had never been tested for HIV earlier of which, 36.4% were multigravida women, thus posing a serious threat of horizontal and vertical HIV transmission. Among the known positives, 90.9% were on ART treatment. While 10% of the known-positives had not considered the ART treatment, indicating a concerning lack of awareness about HIV management among the pregnant mothers. Potential reasons for not taking or discontinuation of ART could be migration, accessibility of the ART owing to increased travel cost,
About 48% of the total HIV positive cases were primigravida, and a higher proportion of them (58.7%) were in 15–24 years’ group. About 45.4% of the primigravids were aware of their HIV status of which 72% had tested for HIV during their current (first) pregnancy indicating new infections, whereas 28% had acquired the infection before their first pregnancy. Another trend to be noted is HIV sero-conversion among pregnant mothers. 12.8% of the HIV positive mothers had been reported HIV negative in their last HIV test taken during the current pregnancy of which 83.3% were in the second or third trimester. This suggests the possibility of these mothers to be seroconverted during later pregnancy and emphasizes the need for HIV retesting during late pregnancy.
Towards achieving the 95-95-95 goal by 2030 and PPTCT, we suggest reaching out to the young mothers specifically from less educated and low-income backgrounds in Karnataka and disseminate HIV-related information by all possible means. Mandating RCH registration in PHCs for obtaining birth certificates as done in Tamilnadu,
would probably increase the proportion of those accessing the ANC services, which in turn would reflect on HIV testing and eventually ART uptake. Concurrently, although testing for HIV has been done by default in all ANC centres, question arises if the mother and her family members are aware of the information related to HIV testing and its follow-up. Hence it is important that all pregnant women undergoing the HIV test are well-informed about the test and its implications, through pre-test counselling for productive responses.
Appropriate pre-/post-test counselling and integrated state-level ART follow-ups, psychological support to the infected pregnant women and her family members are important for continued adherence to ART.
4. Conclusion
The accuracy of the estimates derived from ANC-HSS prevalence relies on the assumption that HIV prevalence trends among women attending ANC are representative of HIV trends among all adults aged 15–49 years. Data from HSS is a valuable resource to identify the missing HIV transmission links within the general and bridge populations. Here, in Karnataka, the disease was particularly confined within young and less educated, especially among the spouses of labourers. The proportion of pregnant women not availing ANC services corresponded with those not been tested for HIV. Measures to ensure that all pregnant mothers seek ANC services will therefore improve voluntary HIV testing and its management thereof. Likewise, counselling and psychological support to HIV-positive pregnant women will improvise the adherence to ART.
Funding
The Corresponding author received funding from the National AIDS Control Organization (NACO) (Government of India) for conducting the HIV Sentinel Surveillance (HSS) in state of Karnataka. NACO Grant No. T-11020/02/2015-NACO (Surveillance).
Authors contributions
AE, BG and AS conceptualised the frame work. NM and VMP performed the literature search. MM wrote the first draft of the manuscript and NJ done the required statistical analysis. AE and PK offered technical advice, intellectual contributions and revised the draft manuscript. BG performed the editing of the manuscript and revisions by all the authors. SR performed critical review of the manuscript. AS, BKK, CG and VR overseen the field activities. The decision of the final version of manuscript to be published was agreed upon by all the authors.
Declaration of competing interest
All the author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Acknowledgments
The authors wish to thank the Project Director of Karnataka State AIDS Prevention Society, Referral Laboratories, State Surveillance Team members and sentinel sites personnel for their support in completing the surveillance activities in a timely manner. The authors also express their special gratitude to Dr. Sanjay Madhav Mehendale, former Additional Director General, Indian Council of Medical Research, New Delhi; Prof. DCS Reddy, Former Professor and Head, Department of PSM, Banaras Hindu University, Varanasi; Dr. Arvind Pandey, Former Director, ICMR-National Institute of Medical Statistics, New Delhi; Prof. Shashi Kant, Professor and Head, Department of Community Medicine, AIIMS, New Delhi for their immense contribution and technical inputs towards establishing a robust HIV Sentinel Surveillance system in India. The authors also acknowledge the Institutional Human Ethics Committee and Scientific Advisory Committee of ICMR-National Institute of Epidemiology for granting approval of the study.
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