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Predictors of optional immunization uptake in an urban south Indian population
Vaccine 32 (2014) 3417–3423
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Predictors of optional immunization uptake in an urban south Indian population Kalpana Manthiram a,∗ , Emily A. Blood b,c , Vasanthan Kuppuswamy d , Yolanda Martins e , Athi Narayan f , Kelly Burmeister e , K. Parvathy g , Areej Hassan b a
Division of Pediatric Infectious Disease, Vanderbilt University Medical Center, Nashville, TN, United States Division of Adolescent Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA, United States c Clinical Research Center, Boston Children’s Hospital, Harvard Medical School, Boston, MA, United States d Medical University of South Carolina, Charleston, SC, United States e Center for Population Sciences, Dana-Farber Cancer Institute, Boston, MA, United States f Department of Neonatalogy, Emory Johns Creek Hospital, Johns Creek, GA, United States g Pallavaram Children’s Medical Centre, Pallavaram, Tamil Nadu, India b
a r t i c l e
i n f o
Article history: Received 25 November 2013 Received in revised form 24 February 2014 Accepted 2 April 2014 Available online 13 April 2014 Keywords: Immunization coverage Optional immunizations Parental attitudes
a b s t r a c t Background: In Tamil Nadu, India, bacille Calmette–Guérin, diphtheria–tetanus–pertussis, oral poliomyelitis, hepatitis B, and measles vaccines are part of the routine immunization schedule and are available free from government health centers. All other vaccines are optional and available in the private sector at a cost to families. This study assesses immunization rates of routine and optional vaccines and examines parental attitudes toward vaccines in Pallavapuram, Tamil Nadu. Methods: The cluster sampling method was used to estimate immunization coverage. Seven children 18 to 36 months old were selected from 30 clusters for a total sample of 210 children. Demographics and vaccination data were collected from interviews and immunization records. Predictors of vaccination status were identified with logistic regression models. In addition, 21 parents participated in semi-structured interviews regarding their attitudes toward vaccination. Interviews were analyzed qualitatively for themes. Results: Eighty one percent of children were fully immunized with routine vaccines. However, only 21% received all “major” optional vaccines, defined as 3 doses of Haemophilus influenzae type b vaccine, one dose of measles, mumps, rubella vaccine, and one dose of varicella zoster virus vaccine. Birth in a private hospital (OR 5.6, 95% CI 1.3 to 22.9, P < 0.01), higher income (P = 0.03), and maternal completion of high school (OR 6.4, 95% CI 1.5 to 27.6, P < 0.01) were significant predictors of receiving all major optional vaccines. Elucidated themes from interviews included (1) strong parental support for immunizations, (2) low concern for side effects, and (3) low uptake of optional vaccines due to high cost and lack of awareness. Conclusions: Coverage of optional vaccines is low despite positive attitudes toward immunizations. Efforts to reduce cost and increase awareness of these vaccines particularly among low-income families or to include these vaccines in the routine schedule may increase uptake and reduce morbidity and mortality from vaccine-preventable diseases. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Immunizations are widely considered to be the most important public health intervention of the last century and are estimated to prevent 6 million deaths annually [1]. At its initiation in 1974, the World Health Organization’s expanded
∗ Corresponding author. Tel.: +1 5124972541. E-mail address: [email protected] (K. Manthiram). http://dx.doi.org/10.1016/j.vaccine.2014.04.012 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
programme on immunization (EPI) recommended inclusion of bacille Calmette–Guérin (BCG), diphtheria–tetanus–pertussis (DTP), oral poliomyelitis (OPV), and measles vaccines in routine immunization schedules. Although several additional vaccines, such as Haemophilus influenzae type b (Hib); hepatitis B (HBV); pneumococcal conjugate (PCV); measles, mumps, rubella (MMR); varicella zoster virus (VZV); and rotavirus vaccines have since become available, they are not all part of routine immunization schedules which vary among low- and middle-income countries.
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In the south Indian state of Tamil Nadu, the routine immunization schedule for infants less than one year of age includes 1 dose of BCG, 4 doses of OPV, 3 doses of DTP, 3 doses of HBV, and 1 dose of measles vaccine. Routine vaccines are provided free at government health centers. Through door-to-door surveys, the 2005–2006 National Family Health Survey and 2009 UNICEF Coverage Evaluation Survey reported that 78 to 81% of children under one year of age in Tamil Nadu were fully immunized with routine vaccines [2–4]. In comparison, in all of India, 61% of children were fully immunized by one year of age. Although Tamil Nadu has one of the highest rates of vaccine coverage in India, it has not yet achieved the target vaccination rate of 90% set forth by the WHO and UNICEF’s Global Immunization Vision and Strategy framework [5]. Although many of the newly developed vaccines are not included in the routine immunization schedule, the Indian Academy of Pediatrics recommends that infants receive 3 doses of Hib, 3 doses of PCV, 3 doses of rotavirus vaccine, 1 dose of MMR, and 1 dose of VZV before 18 months of age in addition to those on the routine schedule. These additional vaccines, called “optional vaccines,” are not subsidized by the government and are only available at privately owned clinics for families to purchase. Immunizations on the routine schedule can also be purchased in the private sector if so desired by the child’s family. In late 2011, after this study was conducted, Hib vaccine was added to the routine schedule in Tamil Nadu; in this study, it is reported as an optional vaccine. Unlike the routine vaccines, little is known about coverage of optional vaccines, factors affecting their uptake, and parental attitudes toward these immunizations in Tamil Nadu. The objectives of this study were to (1) measure coverage of both routine and optional vaccines in children 18 to 36 months of age in Pallavapuram, India, (2) determine whether particular sociodemographic factors are associated with vaccine uptake, and (3) examine parental attitudes toward immunizations in this population. 2. Methods This is a mixed-methods study with two parts: (1) quantitative design to measure immunization rates and (2) qualitative design to assess parental attitudes. Data were collected from July to August 2011. 2.1. Study area The study was conducted in Pallavapuram municipality, an urban area located in Kanchipuram district in the state of Tamil Nadu, India. It is about 15 km from Chennai, which is the largest city in Tamil Nadu. The population of Pallavapuram is 213,800. Urban areas in Kanchipuram district have an infant mortality rate of 19 per 1000 live births and literacy rate of 79% [6]. The mean per capita monthly income in Tamil Nadu is Rs. 6083 ($134), and the urban poverty line is defined as a per capita monthly income of less than Rs. 937 ($20) [7,8]. Two government primary health centers in the municipality provide the routine immunizations (BCG, OPV, DTP, HBV, and measles vaccines) and the state government also distributes OPV during pulse polio vaccination campaigns. Numerous private clinics throughout the municipality provide optional immunizations (Hib, PCV, rotavirus, MMR, VZV, and influenza vaccines) at a cost to families. 2.2. Quantitative study design We utilized the EPI’s validated ‘30 × 7’ cluster sampling method, which rapidly estimates immunization coverage with a precision of approximately ±10% [9,10]. Pallavapuram was separated into 30
clusters based on ward divisions and population; 7 children were sampled in each cluster for a total sample size of 210 children. Immunization data for children between 18 and 36 months of age were collected. If multiple children were present in a household, only the youngest child in that age range was included. Although the EPI recommends sampling children between 12 and 23 months of age, we sampled a slightly modified age range in order to calculate the rate of uptake of MMR and VZV. The starting street in each cluster was randomly selected from a ward street list, and the starting house was the lowest number house on this street. Subsequent houses were sampled based on closest proximity to the prior house until seven participants who met inclusion criteria were interviewed in each cluster. Demographic information was collected with a verbal survey, and immunization records were reviewed. If written records were not available, parental recall was used. The interviewer asked the parent which vaccines by name and how many injected and oral doses the child received at each recommended age similar to the procedure used in Demographic and Health Surveys [11]. If the child was missing any routine vaccines or did not receive any optional vaccines, parents were asked why the child was incompletely immunized. Answers were recorded verbatim. 2.3. Vaccine outcomes Validity of each immunization dose was determined for each participant. The dose was considered valid if the vaccination record or parental recall indicated that the child received the vaccine at the appropriate time. For BCG vaccine, the presence of a scar on the arm consistent with vaccination was considered evidence of a valid dose. Vaccine doses were considered invalid if (1) no record of receipt was available and parents were unable to recall receipt or (2) if the vaccine was given at an inappropriate age or time interval from the prior dose. In addition to describing the rates of immunization for each routine and optional vaccine, we defined two outcome measures: (1) complete vaccination with all routine vaccines which includes 1 valid dose of BCG, 4 valid doses of OPV, 3 valid doses of DTP, 3 valid doses of HBV, and 1 valid dose of measles vaccine and (2) complete vaccination with all “major” optional vaccines which we defined as 3 valid doses of Hib, one valid dose of MMR, and one valid dose of VZV. These vaccines were chosen as the “major” optional vaccines because they were the most widely available. 2.4. Statistical analyses To assess the association between socio-demographic characteristics and outcome measures, logistic regression models were fit via generalized estimating equations (GEE) to account for sampling cluster. Odds ratios and 95% confidence intervals were determined. For each vaccination outcome, characteristics that were found to be significant predictors in the univariate model were entered into a multivariate GEE model. All analyses were performed using SAS version 9.3. 2.5. Qualitative study design We recruited a convenience sample of parents with children between 18 and 36 months of age from the waiting room of Pallavaram Children’s Medical Centre, a private clinic in Pallavapuram, and from their homes in Pallavapuram. Ten to twenty minute interviews were conducted in Tamil by the principal investigator. Interviews followed a semi-structured guide exploring parents’ knowledge and attitudes toward vaccines. Recruitment continued until thematic saturation was attained.
K. Manthiram et al. / Vaccine 32 (2014) 3417–3423 Table 1 Demographic characteristics of participants.
Age (year) 1.5–2 2–2.5 2.5–3
N (%) Average = 27 months 81 (38.6%) 72 (34.3%) 57 (27.1%)
Gender Male Female
113 (53.8%) 97 (46.2%)
Number of children 1 Child 2 Or more children
Average = 1.6 children 90 (43.1%) 119 (56.9%)
Birthplace Government hospital or home Private hospital
112 (53.6%) 97 (46.4%)
Monthly income (Rs.) 0–4999 5000–14,999 >15,000
Average = Rs. 12,080 ($260) Median = Rs. 6000 ($130) 59 (29.6%) 95 (47.7%) 45 (22.6%)
Maternal education Did not complete high school Completed high school
117 (56.0%) 92 (44.0%)
Paternal education Did not complete high school Completed high school
111 (53.1%) 98 (46.9%)
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due. Fifty four percent of children received over half of their routine vaccines at a government health center; the remainder received the majority at private clinics. The most commonly obtained optional vaccines were Hib, MMR, and VZV. Uptake of rotavirus vaccine and PCV was very low, and no children received all three recommended doses of either of these vaccines. Although 21% (95% CI 13.6 to 29.2%) were completely vaccinated with all major optional vaccines, 54% (95% CI 44.7 to 63.8%) did not receive a single optional vaccine. Of those who did not receive any optional vaccines, lack of awareness of the availability of these vaccines (59%) and high cost (19%) were the most commonly cited reasons for not purchasing these vaccines. Other reasons included concerns about side effects (4%), advice from doctors that they were not necessary (4%), and delay of doses due to illness (2%). 3.3. Predictors of vaccination status Univariate predictors of complete vaccination with routine vaccines were birth in a private hospital, higher income, and maternal and paternal completion of high school (Table 3). Only birth in a private hospital was predictive in the multivariate analysis. In addition to birth in a private hospital, higher family income, and maternal and paternal completion of high school, we found that children with no siblings were also more likely to receive all major optional vaccines in the univariate analysis (Table 4). In the multivariate analysis, birth at a private hospital, family income, and maternal completion of high school remained significant.
2.6. Qualitative analysis
3.4. Qualitative interviews
Interviews were tape-recorded, transcribed and translated by the principal investigator. Two researchers read all transcripts and identified preliminary themes that were then discussed with the larger research group to determine final themes. Using a grounded, inductive technique, a coding scheme was developed and data were classified using these codes. A second coder, independent to this study, coded a randomly selected 25% of interviews. Inter-coder agreement was = 0.79. The coders discussed all data that were coded discrepantly until they reached agreement in their classification. We received approval from the Boston Children’s Hospital Institutional Review Board in the United States and YRG-CARE Institutional Review Board in Chennai, India.
The parents of 21 children were interviewed. Two were fathers, and for one child, both a mother and father were interviewed together. Seven parents were recruited at Pallavaram Children’s Medical Center, and 14 were recruited in the community. Parents had an average of 1.5 children and a monthly income of Rs. 22,000 ($485). Forty-eight percent of children had mothers and 29% had fathers who did not complete high school. Forty-two percent of the children were born in a private hospital. The vast majority (95%) of the children had received all routine vaccines, while 38% received all major optional vaccines. Themes and illustrative quotes are shown in Table 5. All parents understood that vaccines were given to prevent illness and overwhelmingly felt that vaccines achieved this purpose. Most parents identified disability as a consequence of polio, but very few could identify the symptoms of measles, varicella, or influenza infection. Although parents perceived vaccine-preventable diseases, particularly polio, to be very severe, direct experience with most of these diseases was minimal. Most parents reported that their children experienced fever or pain after vaccination. However, all participants felt that the benefits of vaccination outweighed the risks, and several believed fever was a sign of vaccine efficacy. In 2011, a two-year-old boy died two hours after receiving the oral polio vaccine during a pulse vaccination campaign in Chennai, India [12,13]. Many parents mentioned this incident. Despite initial apprehension, all parents stated that the death did not ultimately affect their desire to vaccinate their child. Finally, many parents wanted to obtain additional vaccines for their children. About half of parents felt that optional vaccines were too expensive, but despite the cost, the majority was eager to obtain these vaccines because of the protection they afforded. In particular, a doctor’s recommendation to obtain optional vaccines weighed heavily in parents’ decision-making.
3. Results 3.1. Demographics The demographic characteristics for the 210 participants are shown in Table 1. Fourteen families (7%) with eligible children refused to participate. Immunization data were retrieved fully from written records for 51% of participants. No written records were available for 23% of participants, and parental recall was substituted. The remainder (26%) had incomplete written records, which were supplemented with parental recall. 3.2. Immunization rates Immunization rates for routine and optional vaccines are shown in Table 2. Eighty-one percent of children received all routine vaccines. Major reasons for incomplete vaccination were lack of awareness that vaccination was incomplete and delay of immunization due to illness in the child at the time the immunization was
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Table 2 Vaccination coverage of children 18–36 months old. Immunization
Percentage of children who received vaccine, N = 210 N (%) Birth
Routine immunizations BCG OPVa DTPb Hepatitis B Measles Optional immunizations Hib PCV Rotavirus MMR VZV Influenza
Received all routine vaccines Received all major optional vaccines (3 Hib, one MMR, one VZV) a b
210 (100%) 210 (100%)
6 weeks
10 weeks
14 weeks
209 (99.5%) 209 (99.5%) 199 (94.7%)
210 (100%) 209 (99.5%) 197 (93.8%)
204 (97.1%) 203 (96.7%) 188 (89.5%)
9 months
12–15 months
186 (88.6%) 91 (43.3%) 7 (3.3%) 8 (3.8%)
81 (38.6%) 1 (0.5%) 7 (3.3%)
77 (36.7%) 0 (0%) 0 (0%) 68 (32.3%) 57 (27.1%) 1 dose: 7 (3.3%) 2 doses: 2 (1.0%)
169 (80.5%, 95% CI 72.9 to 88.1%) 45 (21.4%, 95% CI 13.6 to 29.2%)
IPV doses included as OPV in table and analysis. DTaP doses included as DTP in table and analysis.
4. Discussion This study is among the first to assess optional vaccine coverage in Tamil Nadu, India. Only 21% of children received all major optional vaccines. Birth at a private hospital, higher income, and higher maternal education were predictors of receiving the major optional vaccines. We found strong support for vaccination in Pallavapuram.
Previous studies in India primarily focused on routine vaccines. The rates and predictors of routine immunization we found are similar to other studies [2–4,14–17]. Optional vaccine coverage is often estimated from vaccine sales data and birth rates; population surveys are rarely done. In India, door-to-door surveys to estimate optional vaccine uptake were conducted in Chandigarh and Amritsar in northern India [18,19]. In these cities, 20–28% of children received 3 doses of Hib, and 6% received VZV. Higher parental
Table 3 Univariate and multivariate logistic regression analysis of factors associated with receipt of all routine vaccines (1 BCG, 3 DTP, 3 HBV, 4 OPV, 1 measles vaccine). Percent who received all routine vaccines (%)
Odds ratio by univariate analysis (95% CI)
Age (year) 1.5–2 2–2.5 2.5–3
77.8 81.9 82.5
0.74 (0.31–1.77) 0.97 (0.39–2.44) Ref P = 0.66
Gender Female Male
78.4 82.3
Ref 1.28 (0.64–2.58) P = 0.50
Number of children 1 Child 2 Or more children
85.6 76.5
1.86 (0.69–5.00) Ref P = 0.21
71.4
Ref
Ref
90.7
3.97 (1.90–8.29) P < 0.01
2.96 (1.14–7.72) P = 0.02
Monthly income (Rs.) 0–4999 5000–14,999 >15,000
72.9 79.0 95.6
Ref 1.38 (0.65–2.94) 8.20 (1.66–40.40) P = 0.02
Ref 0.96 (0.39–2.34) 2.32 (0.25–21.20) P = 0.65
Maternal education Did not complete high school Completed high school
74.4 88.0
Ref 2.73 (1.22–6.12) P = 0.02
Ref 1.07 (0.34–3.39) P = 0.92
Paternal education Did not complete high school Completed high school
72.1 89.8
Ref 3.39 (1.62-7.07) P < 0.01
Ref 1.48 (0.61–3.57) P = 0.38
Birthplace Government hospital or home Private hospital
Odds ratio by multivariate analysis (95% CI)
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Table 4 Univariate and multivariate logistic regression analysis of factors associated with receipt of major optional vaccines (3 Hib, one VZV, and one MMR vaccine doses). Percent who received major optional vaccines (%)
Odds ratio by univariate analysis (95% CI)
Odds ratio by multivariate analysis (95% CI)
Age (year) 1.5–2 2–2.5 2.5–3
18.5 26.4 19.3
1.05 (0.55–1.99) 1.40 (0.61–3.20) Ref P = 0.74
Gender Female Male
20.6 22.1
Ref 1.18 (0.70–1.99) P = 0.54
Number of children 1 Child 2 Or more children
30.0 15.1
2.04 (1.13–3.68) Ref P = 0.03
1.26 (0.48–3.32) Ref P = 0.64
Ref
Ref
Birthplace Government hospital or home Private hospital
43.3
27.17 (7.76–95.08) P < 0.01
5.55 (1.34–22.86) P = 0.01
Monthly income (Rs.) 0–4999 5000–14,999 >15,000
1.7 10.5 66.7
Ref 6.93 (0.83–57.86) 119.36 (15.41–924.60) P < 0.01
Ref 2.17 (0.22–21.62) 8.12 (0.72–92.09) P = 0.03
Maternal education Did not complete high school Completed high school
2.6 45.7
Ref 33.64 (9.37-120.74) P < 0.01
Ref 6.41 (1.48–27.64) P < 0.01
Paternal education Did not complete high school Completed high school
2.7 42.9
Ref 27.20 (8.08-91.54) P < 0.01
Ref 1.94 (0.40–9.39) P = 0.40
2.7
education and birth at a hospital were predictors of receiving optional vaccines. In Istanbul, Turkey, receipt of optional vaccines was associated with higher socioeconomic status, and in Shandong province, China, uptake of VZV was associated with proximity to immunization facilities and the socioeconomic status of the county in which the child resided [20,21]. In all of these studies, optional vaccine uptake lagged behind that of routine vaccines. The predictors of optional vaccine uptake (birthplace, income, and maternal education) corresponded to the impediments we identified in the qualitative part of the study, namely high cost and lack of awareness of these vaccines. Optional vaccines range in cost from Rs. 500 to 2000 ($11 to 44) per vaccine per dose. With 30% of the population in Pallavapuram having a monthly income of
less than Rs. 5000 ($110), it is not surprising that higher income is strongly associated with the receipt of optional vaccines. In addition, knowledge about the availability of these vaccines is strongly linked to the child’s birthplace where initial vaccination occurs. Children born in government facilities are more likely to receive immunizations in the public sector so their parents are less likely to be exposed to the concept of optional vaccines. The positive association between maternal education and vaccination status has been reported in other studies in India and is thought to arise from heightened knowledge about health and enhanced communication skills stemming from education [22]. We found considerable differences in the uptake rates of the various optional vaccines. This variation may be a consequence
Table 5 Themes and illustrative participant quotes from semi-structured interviews. Theme and subtheme
Illustrative quotes
Knowledge about immunization need and vaccine preventable diseases “I get immunizations to keep my children from getting diseases. . .so my child does not Immunizations prevent disease in children have problems in the future.” Polio leads to disability and is a severe disease “It’s [the consequences are] great. If the child has a handicap in their body, if they don’t have an arm or leg, their life is lost. . .so we have to be careful and get the immunizations.” Perceptions about vaccine side effects “We will not miss any immunizations. Even if she has pain, she will cry for a little bit, Side effects are temporary and then it will go away.” “There will be a light fever because they got the shot. The fever shows that the Fever is a sign of vaccine efficacy medicine is working correctly. We are happy that it is working correctly.” “That child [who died after receiving polio drops] must have had a sickness already. Possible vaccine-related adverse events do not affect behavior We should not give polio drops to that child. If we do, he will get vomiting and diarrhea, right? Only healthy children should get it.” Receipt of optional vaccines “We couldn’t afford the cost, so we didn’t get it. His [my husband’s] salary is 4000 Cost is a limiting factor rupees. If we had to spend 2500 monthly and cut out everything else for the child’s immunizations, it would be hard” “If it’s for the child, we have to spend it. No matter how much it costs, if it’s for the Will obtain immunizations at any cost child, we have to spend money and buy it.”
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of fewer private providers offering PCV and rotavirus vaccines compared to Hib, MMR, and VZV. A recent survey of Indian pediatricians indicated that while most offered Hib routinely, most only selectively offered PCV and rotavirus vaccine to particular patients [23]. Reasons for this bias in offering of immunizations may be related to the higher cost and more recent licensure of PCV and rotavirus vaccine resulting in decreased provider familiarity. In our interviews, many parents expressed interest in purchasing additional optional vaccines but were limited by which ones their providers offered. Enhancing provider knowledge about and access to PCV, rotavirus, and influenza vaccines may increase their use. Strong parental support for vaccines was a major motivating factor in Pallavapuram as was found in another study on vaccine acceptability in India [24]. Barriers often noted in other studies like anxiety about vaccine side effects or perception that vaccines are unnecessary were rare in Pallavapuram [4,25–30]. In the literature, lack of concern about vaccine-preventable diseases is thought to be associated with decreasing experience with these diseases [25–28]. In our population, we did not find this relationship. Awareness of poliomyelitis was high and parents greatly feared the consequences of polio, but very few had direct experience with the disease. Knowledge of and reported experience with other vaccinepreventable diseases were even lower. General apprehension about infectious diseases and faith in immunizations boosted parental support of vaccination. Our study has several strengths. The area we studied encompasses the diverse socioeconomic statuses present in urban areas of south India, and door-to-door coverage studies are more accurate appraisals of immunization delivery than utilizing manufacturers’ sales data [10]. The coverage rates we measured for routine vaccines were comparable to published studies. Lastly, because vaccination rates in Tamil Nadu are among the highest in India secondary to a robust vaccine delivery system and outreach efforts, the state offers a good environment to study optional vaccine uptake. Limitations of our study include small sample size and area of sampling, which may limit generalizability. In our population, no central vaccination records existed so individual families maintained records. If no written vaccine record was available, we relied on parental recall to determine immunization status, which is subject to recall bias. However, studies in diverse communities demonstrate that parental recall has fairly good accuracy when compared to written records and that relying on card alone results in underestimation of immunization rates [31–34]. Parental recall has been used effectively in other recent coverage surveys in India [2,3]. We found that cost and lack of awareness were the greatest barriers to optional vaccine uptake. Adding these vaccines to the routine immunization schedule could address these barriers. Future analysis of vaccination rates of Hib in Tamil Nadu after its recent incorporation into the routine vaccination schedule may provide compelling data to support this argument. Concerns about disease burden, vaccine efficacy, availability of an affordable vaccine supply, and expense have hindered introduction of new vaccines in low- and middle-income countries [35,36]. In India, there is evidence to suggest that these obstacles can be overcome. Indian companies produce many of the optional vaccines [37]. Several studies indicate that introduction of rotavirus vaccine and PCV in the national immunization schedule would be cost effective [38,39]. The majority of childhood mortality in India is from diarrhea and pneumonia, and introduction of PCV and rotavirus vaccine in other countries resulted in significant reductions in rates of these diseases [40–47]. Increasing uptake of these vaccines has the potential to substantially decrease morbidity and mortality from vaccine-preventable disease.
5. Conclusions Uptake of routine immunizations was high in Pallavapuram but still fell below the goals espoused by the WHO and UNICEF. Coverage of optional vaccines was considerably lower and was deterred by high cost and low parental awareness. However, parental desire to obtain these vaccines was high. We believe Tamil Nadu is an ideal location in which to introduce additional vaccines into the routine schedule because there is strong support for vaccination and uptake of routine vaccines is already high. Competing interests The authors declare that they have no competing interests. Authors’ contributions AN initiated the concept for this study. KM and AH reviewed the literature, designed the study, and were responsible for writing the paper. KM, VK, and KP coordinated data collection in India. EB, YM, KB aided with statistical analysis for the cluster and qualitative study. All authors read and approved the final manuscript. Acknowledgments The authors would like to thank the Pallavapuram community for participating in this study. Funding was provided from the Leadership Education in Adolescent Health training grant #T71MC00009 from the Maternal and Child Health Bureau at the Health Resources and Services Administration and the Schiesman Traveling Fellowship from Boston Children’s Hospital. Dr. S. Swarnalakshmi, PhD, Ms. Geetha, and Dr. Suniti Solomon, MD, at YRG-CARE kindly reviewed the ethical aspects of the project in India. Mr. and Mrs. Kuppuswamy, Ms. Mary, Ms. Anjali, Ms. Dhanam, Ms. Pilomina, Mr. Vignesh, Mr. Rajendran Venkattareddy, Mr. Ravikumar, Ms. Uma Ganapathi, Mr. Shankar Kumar, Mr. Kolandavel Ramasamy, and Ms. Rajeswari Manthiram were graciously helpful in data collection and translation. Drs. Kathryn Edwards, MD, Elizabeth Woods, MD, Heather Corliss, PhD, Atsuko Koyama, MD, and Kathryn Brigham, MD provided helpful input on study design and/or manuscript review. References [1] Ehreth J. The global value of vaccination. Vaccine 2003;21(7):596–600. [2] International Institute for Population Sciences and Macro International. National family health survey (NFHD-3) India, 2005–06. Tamil Nadu, Mumbai, India: International Institute for Population Sciences and Macro International; 2008. [3] The United Nations Children’s Fund. Coverage evaluation survey: all India report. New Delhi, India: The United Nations Children’s Fund; 2009. [4] Kumar D, Aggarwal A, Gomber S. Immunization status of children admitted to a tertiary-care hospital of north India: reasons for partial immunization or non-immunization. J Health Popul Nutr 2010;28(3):300–4. [5] World Health Organization Department of Immunization, Vaccines, and Biologicals and UNICEF Programme Division, Health Section. Global immunization vision and strategy 2006–2015. Geneva, Switzerland: World Health Organization Department of Immunization, Vaccines, and Biologicals and UNICEF Programme Division, Health Section; 2005. [6] District Profile of Kanchipuram District. 2001; Available from: http://www. kanchi.nic.in/district profile pro.html. [7] Government of India Planning Commission. Press Note on Poverty Estimates, 2011–2012. Available from: http://planningcommission.nic.in/news/ pre pov2307.pdf. [8] Government of Tamil Nadu. Department of Economics and Statistics, Statistical handbook 2012, Available from: http://www.tn.gov.in/deptst/ Ecoindicator.htm. [9] Sundaresan T, Henderson RH. Cluster sampling to assess immunization coverage: a review of experience with a simplified sampling method. Bull World Health Organ 1982;60(2):253–60. [10] World Health Organization Department of Immunization, Vaccines and Biologicals. Immunization coverage cluster survey—reference manual. Geneva,
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Predictors of optional immunization uptake in an urban south Indian population Kalpana Manthiram a,∗ , Emily A. Blood b,c , Vasanthan Kuppuswamy d , Yolanda Martins e , Athi Narayan f , Kelly Burmeister e , K. Parvathy g , Areej Hassan b a
Division of Pediatric Infectious Disease, Vanderbilt University Medical Center, Nashville, TN, United States Division of Adolescent Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA, United States c Clinical Research Center, Boston Children’s Hospital, Harvard Medical School, Boston, MA, United States d Medical University of South Carolina, Charleston, SC, United States e Center for Population Sciences, Dana-Farber Cancer Institute, Boston, MA, United States f Department of Neonatalogy, Emory Johns Creek Hospital, Johns Creek, GA, United States g Pallavaram Children’s Medical Centre, Pallavaram, Tamil Nadu, India b
a r t i c l e
i n f o
Article history: Received 25 November 2013 Received in revised form 24 February 2014 Accepted 2 April 2014 Available online 13 April 2014 Keywords: Immunization coverage Optional immunizations Parental attitudes
a b s t r a c t Background: In Tamil Nadu, India, bacille Calmette–Guérin, diphtheria–tetanus–pertussis, oral poliomyelitis, hepatitis B, and measles vaccines are part of the routine immunization schedule and are available free from government health centers. All other vaccines are optional and available in the private sector at a cost to families. This study assesses immunization rates of routine and optional vaccines and examines parental attitudes toward vaccines in Pallavapuram, Tamil Nadu. Methods: The cluster sampling method was used to estimate immunization coverage. Seven children 18 to 36 months old were selected from 30 clusters for a total sample of 210 children. Demographics and vaccination data were collected from interviews and immunization records. Predictors of vaccination status were identified with logistic regression models. In addition, 21 parents participated in semi-structured interviews regarding their attitudes toward vaccination. Interviews were analyzed qualitatively for themes. Results: Eighty one percent of children were fully immunized with routine vaccines. However, only 21% received all “major” optional vaccines, defined as 3 doses of Haemophilus influenzae type b vaccine, one dose of measles, mumps, rubella vaccine, and one dose of varicella zoster virus vaccine. Birth in a private hospital (OR 5.6, 95% CI 1.3 to 22.9, P < 0.01), higher income (P = 0.03), and maternal completion of high school (OR 6.4, 95% CI 1.5 to 27.6, P < 0.01) were significant predictors of receiving all major optional vaccines. Elucidated themes from interviews included (1) strong parental support for immunizations, (2) low concern for side effects, and (3) low uptake of optional vaccines due to high cost and lack of awareness. Conclusions: Coverage of optional vaccines is low despite positive attitudes toward immunizations. Efforts to reduce cost and increase awareness of these vaccines particularly among low-income families or to include these vaccines in the routine schedule may increase uptake and reduce morbidity and mortality from vaccine-preventable diseases. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Immunizations are widely considered to be the most important public health intervention of the last century and are estimated to prevent 6 million deaths annually [1]. At its initiation in 1974, the World Health Organization’s expanded
∗ Corresponding author. Tel.: +1 5124972541. E-mail address: [email protected] (K. Manthiram). http://dx.doi.org/10.1016/j.vaccine.2014.04.012 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
programme on immunization (EPI) recommended inclusion of bacille Calmette–Guérin (BCG), diphtheria–tetanus–pertussis (DTP), oral poliomyelitis (OPV), and measles vaccines in routine immunization schedules. Although several additional vaccines, such as Haemophilus influenzae type b (Hib); hepatitis B (HBV); pneumococcal conjugate (PCV); measles, mumps, rubella (MMR); varicella zoster virus (VZV); and rotavirus vaccines have since become available, they are not all part of routine immunization schedules which vary among low- and middle-income countries.
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In the south Indian state of Tamil Nadu, the routine immunization schedule for infants less than one year of age includes 1 dose of BCG, 4 doses of OPV, 3 doses of DTP, 3 doses of HBV, and 1 dose of measles vaccine. Routine vaccines are provided free at government health centers. Through door-to-door surveys, the 2005–2006 National Family Health Survey and 2009 UNICEF Coverage Evaluation Survey reported that 78 to 81% of children under one year of age in Tamil Nadu were fully immunized with routine vaccines [2–4]. In comparison, in all of India, 61% of children were fully immunized by one year of age. Although Tamil Nadu has one of the highest rates of vaccine coverage in India, it has not yet achieved the target vaccination rate of 90% set forth by the WHO and UNICEF’s Global Immunization Vision and Strategy framework [5]. Although many of the newly developed vaccines are not included in the routine immunization schedule, the Indian Academy of Pediatrics recommends that infants receive 3 doses of Hib, 3 doses of PCV, 3 doses of rotavirus vaccine, 1 dose of MMR, and 1 dose of VZV before 18 months of age in addition to those on the routine schedule. These additional vaccines, called “optional vaccines,” are not subsidized by the government and are only available at privately owned clinics for families to purchase. Immunizations on the routine schedule can also be purchased in the private sector if so desired by the child’s family. In late 2011, after this study was conducted, Hib vaccine was added to the routine schedule in Tamil Nadu; in this study, it is reported as an optional vaccine. Unlike the routine vaccines, little is known about coverage of optional vaccines, factors affecting their uptake, and parental attitudes toward these immunizations in Tamil Nadu. The objectives of this study were to (1) measure coverage of both routine and optional vaccines in children 18 to 36 months of age in Pallavapuram, India, (2) determine whether particular sociodemographic factors are associated with vaccine uptake, and (3) examine parental attitudes toward immunizations in this population. 2. Methods This is a mixed-methods study with two parts: (1) quantitative design to measure immunization rates and (2) qualitative design to assess parental attitudes. Data were collected from July to August 2011. 2.1. Study area The study was conducted in Pallavapuram municipality, an urban area located in Kanchipuram district in the state of Tamil Nadu, India. It is about 15 km from Chennai, which is the largest city in Tamil Nadu. The population of Pallavapuram is 213,800. Urban areas in Kanchipuram district have an infant mortality rate of 19 per 1000 live births and literacy rate of 79% [6]. The mean per capita monthly income in Tamil Nadu is Rs. 6083 ($134), and the urban poverty line is defined as a per capita monthly income of less than Rs. 937 ($20) [7,8]. Two government primary health centers in the municipality provide the routine immunizations (BCG, OPV, DTP, HBV, and measles vaccines) and the state government also distributes OPV during pulse polio vaccination campaigns. Numerous private clinics throughout the municipality provide optional immunizations (Hib, PCV, rotavirus, MMR, VZV, and influenza vaccines) at a cost to families. 2.2. Quantitative study design We utilized the EPI’s validated ‘30 × 7’ cluster sampling method, which rapidly estimates immunization coverage with a precision of approximately ±10% [9,10]. Pallavapuram was separated into 30
clusters based on ward divisions and population; 7 children were sampled in each cluster for a total sample size of 210 children. Immunization data for children between 18 and 36 months of age were collected. If multiple children were present in a household, only the youngest child in that age range was included. Although the EPI recommends sampling children between 12 and 23 months of age, we sampled a slightly modified age range in order to calculate the rate of uptake of MMR and VZV. The starting street in each cluster was randomly selected from a ward street list, and the starting house was the lowest number house on this street. Subsequent houses were sampled based on closest proximity to the prior house until seven participants who met inclusion criteria were interviewed in each cluster. Demographic information was collected with a verbal survey, and immunization records were reviewed. If written records were not available, parental recall was used. The interviewer asked the parent which vaccines by name and how many injected and oral doses the child received at each recommended age similar to the procedure used in Demographic and Health Surveys [11]. If the child was missing any routine vaccines or did not receive any optional vaccines, parents were asked why the child was incompletely immunized. Answers were recorded verbatim. 2.3. Vaccine outcomes Validity of each immunization dose was determined for each participant. The dose was considered valid if the vaccination record or parental recall indicated that the child received the vaccine at the appropriate time. For BCG vaccine, the presence of a scar on the arm consistent with vaccination was considered evidence of a valid dose. Vaccine doses were considered invalid if (1) no record of receipt was available and parents were unable to recall receipt or (2) if the vaccine was given at an inappropriate age or time interval from the prior dose. In addition to describing the rates of immunization for each routine and optional vaccine, we defined two outcome measures: (1) complete vaccination with all routine vaccines which includes 1 valid dose of BCG, 4 valid doses of OPV, 3 valid doses of DTP, 3 valid doses of HBV, and 1 valid dose of measles vaccine and (2) complete vaccination with all “major” optional vaccines which we defined as 3 valid doses of Hib, one valid dose of MMR, and one valid dose of VZV. These vaccines were chosen as the “major” optional vaccines because they were the most widely available. 2.4. Statistical analyses To assess the association between socio-demographic characteristics and outcome measures, logistic regression models were fit via generalized estimating equations (GEE) to account for sampling cluster. Odds ratios and 95% confidence intervals were determined. For each vaccination outcome, characteristics that were found to be significant predictors in the univariate model were entered into a multivariate GEE model. All analyses were performed using SAS version 9.3. 2.5. Qualitative study design We recruited a convenience sample of parents with children between 18 and 36 months of age from the waiting room of Pallavaram Children’s Medical Centre, a private clinic in Pallavapuram, and from their homes in Pallavapuram. Ten to twenty minute interviews were conducted in Tamil by the principal investigator. Interviews followed a semi-structured guide exploring parents’ knowledge and attitudes toward vaccines. Recruitment continued until thematic saturation was attained.
K. Manthiram et al. / Vaccine 32 (2014) 3417–3423 Table 1 Demographic characteristics of participants.
Age (year) 1.5–2 2–2.5 2.5–3
N (%) Average = 27 months 81 (38.6%) 72 (34.3%) 57 (27.1%)
Gender Male Female
113 (53.8%) 97 (46.2%)
Number of children 1 Child 2 Or more children
Average = 1.6 children 90 (43.1%) 119 (56.9%)
Birthplace Government hospital or home Private hospital
112 (53.6%) 97 (46.4%)
Monthly income (Rs.) 0–4999 5000–14,999 >15,000
Average = Rs. 12,080 ($260) Median = Rs. 6000 ($130) 59 (29.6%) 95 (47.7%) 45 (22.6%)
Maternal education Did not complete high school Completed high school
117 (56.0%) 92 (44.0%)
Paternal education Did not complete high school Completed high school
111 (53.1%) 98 (46.9%)
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due. Fifty four percent of children received over half of their routine vaccines at a government health center; the remainder received the majority at private clinics. The most commonly obtained optional vaccines were Hib, MMR, and VZV. Uptake of rotavirus vaccine and PCV was very low, and no children received all three recommended doses of either of these vaccines. Although 21% (95% CI 13.6 to 29.2%) were completely vaccinated with all major optional vaccines, 54% (95% CI 44.7 to 63.8%) did not receive a single optional vaccine. Of those who did not receive any optional vaccines, lack of awareness of the availability of these vaccines (59%) and high cost (19%) were the most commonly cited reasons for not purchasing these vaccines. Other reasons included concerns about side effects (4%), advice from doctors that they were not necessary (4%), and delay of doses due to illness (2%). 3.3. Predictors of vaccination status Univariate predictors of complete vaccination with routine vaccines were birth in a private hospital, higher income, and maternal and paternal completion of high school (Table 3). Only birth in a private hospital was predictive in the multivariate analysis. In addition to birth in a private hospital, higher family income, and maternal and paternal completion of high school, we found that children with no siblings were also more likely to receive all major optional vaccines in the univariate analysis (Table 4). In the multivariate analysis, birth at a private hospital, family income, and maternal completion of high school remained significant.
2.6. Qualitative analysis
3.4. Qualitative interviews
Interviews were tape-recorded, transcribed and translated by the principal investigator. Two researchers read all transcripts and identified preliminary themes that were then discussed with the larger research group to determine final themes. Using a grounded, inductive technique, a coding scheme was developed and data were classified using these codes. A second coder, independent to this study, coded a randomly selected 25% of interviews. Inter-coder agreement was = 0.79. The coders discussed all data that were coded discrepantly until they reached agreement in their classification. We received approval from the Boston Children’s Hospital Institutional Review Board in the United States and YRG-CARE Institutional Review Board in Chennai, India.
The parents of 21 children were interviewed. Two were fathers, and for one child, both a mother and father were interviewed together. Seven parents were recruited at Pallavaram Children’s Medical Center, and 14 were recruited in the community. Parents had an average of 1.5 children and a monthly income of Rs. 22,000 ($485). Forty-eight percent of children had mothers and 29% had fathers who did not complete high school. Forty-two percent of the children were born in a private hospital. The vast majority (95%) of the children had received all routine vaccines, while 38% received all major optional vaccines. Themes and illustrative quotes are shown in Table 5. All parents understood that vaccines were given to prevent illness and overwhelmingly felt that vaccines achieved this purpose. Most parents identified disability as a consequence of polio, but very few could identify the symptoms of measles, varicella, or influenza infection. Although parents perceived vaccine-preventable diseases, particularly polio, to be very severe, direct experience with most of these diseases was minimal. Most parents reported that their children experienced fever or pain after vaccination. However, all participants felt that the benefits of vaccination outweighed the risks, and several believed fever was a sign of vaccine efficacy. In 2011, a two-year-old boy died two hours after receiving the oral polio vaccine during a pulse vaccination campaign in Chennai, India [12,13]. Many parents mentioned this incident. Despite initial apprehension, all parents stated that the death did not ultimately affect their desire to vaccinate their child. Finally, many parents wanted to obtain additional vaccines for their children. About half of parents felt that optional vaccines were too expensive, but despite the cost, the majority was eager to obtain these vaccines because of the protection they afforded. In particular, a doctor’s recommendation to obtain optional vaccines weighed heavily in parents’ decision-making.
3. Results 3.1. Demographics The demographic characteristics for the 210 participants are shown in Table 1. Fourteen families (7%) with eligible children refused to participate. Immunization data were retrieved fully from written records for 51% of participants. No written records were available for 23% of participants, and parental recall was substituted. The remainder (26%) had incomplete written records, which were supplemented with parental recall. 3.2. Immunization rates Immunization rates for routine and optional vaccines are shown in Table 2. Eighty-one percent of children received all routine vaccines. Major reasons for incomplete vaccination were lack of awareness that vaccination was incomplete and delay of immunization due to illness in the child at the time the immunization was
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Table 2 Vaccination coverage of children 18–36 months old. Immunization
Percentage of children who received vaccine, N = 210 N (%) Birth
Routine immunizations BCG OPVa DTPb Hepatitis B Measles Optional immunizations Hib PCV Rotavirus MMR VZV Influenza
Received all routine vaccines Received all major optional vaccines (3 Hib, one MMR, one VZV) a b
210 (100%) 210 (100%)
6 weeks
10 weeks
14 weeks
209 (99.5%) 209 (99.5%) 199 (94.7%)
210 (100%) 209 (99.5%) 197 (93.8%)
204 (97.1%) 203 (96.7%) 188 (89.5%)
9 months
12–15 months
186 (88.6%) 91 (43.3%) 7 (3.3%) 8 (3.8%)
81 (38.6%) 1 (0.5%) 7 (3.3%)
77 (36.7%) 0 (0%) 0 (0%) 68 (32.3%) 57 (27.1%) 1 dose: 7 (3.3%) 2 doses: 2 (1.0%)
169 (80.5%, 95% CI 72.9 to 88.1%) 45 (21.4%, 95% CI 13.6 to 29.2%)
IPV doses included as OPV in table and analysis. DTaP doses included as DTP in table and analysis.
4. Discussion This study is among the first to assess optional vaccine coverage in Tamil Nadu, India. Only 21% of children received all major optional vaccines. Birth at a private hospital, higher income, and higher maternal education were predictors of receiving the major optional vaccines. We found strong support for vaccination in Pallavapuram.
Previous studies in India primarily focused on routine vaccines. The rates and predictors of routine immunization we found are similar to other studies [2–4,14–17]. Optional vaccine coverage is often estimated from vaccine sales data and birth rates; population surveys are rarely done. In India, door-to-door surveys to estimate optional vaccine uptake were conducted in Chandigarh and Amritsar in northern India [18,19]. In these cities, 20–28% of children received 3 doses of Hib, and 6% received VZV. Higher parental
Table 3 Univariate and multivariate logistic regression analysis of factors associated with receipt of all routine vaccines (1 BCG, 3 DTP, 3 HBV, 4 OPV, 1 measles vaccine). Percent who received all routine vaccines (%)
Odds ratio by univariate analysis (95% CI)
Age (year) 1.5–2 2–2.5 2.5–3
77.8 81.9 82.5
0.74 (0.31–1.77) 0.97 (0.39–2.44) Ref P = 0.66
Gender Female Male
78.4 82.3
Ref 1.28 (0.64–2.58) P = 0.50
Number of children 1 Child 2 Or more children
85.6 76.5
1.86 (0.69–5.00) Ref P = 0.21
71.4
Ref
Ref
90.7
3.97 (1.90–8.29) P < 0.01
2.96 (1.14–7.72) P = 0.02
Monthly income (Rs.) 0–4999 5000–14,999 >15,000
72.9 79.0 95.6
Ref 1.38 (0.65–2.94) 8.20 (1.66–40.40) P = 0.02
Ref 0.96 (0.39–2.34) 2.32 (0.25–21.20) P = 0.65
Maternal education Did not complete high school Completed high school
74.4 88.0
Ref 2.73 (1.22–6.12) P = 0.02
Ref 1.07 (0.34–3.39) P = 0.92
Paternal education Did not complete high school Completed high school
72.1 89.8
Ref 3.39 (1.62-7.07) P < 0.01
Ref 1.48 (0.61–3.57) P = 0.38
Birthplace Government hospital or home Private hospital
Odds ratio by multivariate analysis (95% CI)
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Table 4 Univariate and multivariate logistic regression analysis of factors associated with receipt of major optional vaccines (3 Hib, one VZV, and one MMR vaccine doses). Percent who received major optional vaccines (%)
Odds ratio by univariate analysis (95% CI)
Odds ratio by multivariate analysis (95% CI)
Age (year) 1.5–2 2–2.5 2.5–3
18.5 26.4 19.3
1.05 (0.55–1.99) 1.40 (0.61–3.20) Ref P = 0.74
Gender Female Male
20.6 22.1
Ref 1.18 (0.70–1.99) P = 0.54
Number of children 1 Child 2 Or more children
30.0 15.1
2.04 (1.13–3.68) Ref P = 0.03
1.26 (0.48–3.32) Ref P = 0.64
Ref
Ref
Birthplace Government hospital or home Private hospital
43.3
27.17 (7.76–95.08) P < 0.01
5.55 (1.34–22.86) P = 0.01
Monthly income (Rs.) 0–4999 5000–14,999 >15,000
1.7 10.5 66.7
Ref 6.93 (0.83–57.86) 119.36 (15.41–924.60) P < 0.01
Ref 2.17 (0.22–21.62) 8.12 (0.72–92.09) P = 0.03
Maternal education Did not complete high school Completed high school
2.6 45.7
Ref 33.64 (9.37-120.74) P < 0.01
Ref 6.41 (1.48–27.64) P < 0.01
Paternal education Did not complete high school Completed high school
2.7 42.9
Ref 27.20 (8.08-91.54) P < 0.01
Ref 1.94 (0.40–9.39) P = 0.40
2.7
education and birth at a hospital were predictors of receiving optional vaccines. In Istanbul, Turkey, receipt of optional vaccines was associated with higher socioeconomic status, and in Shandong province, China, uptake of VZV was associated with proximity to immunization facilities and the socioeconomic status of the county in which the child resided [20,21]. In all of these studies, optional vaccine uptake lagged behind that of routine vaccines. The predictors of optional vaccine uptake (birthplace, income, and maternal education) corresponded to the impediments we identified in the qualitative part of the study, namely high cost and lack of awareness of these vaccines. Optional vaccines range in cost from Rs. 500 to 2000 ($11 to 44) per vaccine per dose. With 30% of the population in Pallavapuram having a monthly income of
less than Rs. 5000 ($110), it is not surprising that higher income is strongly associated with the receipt of optional vaccines. In addition, knowledge about the availability of these vaccines is strongly linked to the child’s birthplace where initial vaccination occurs. Children born in government facilities are more likely to receive immunizations in the public sector so their parents are less likely to be exposed to the concept of optional vaccines. The positive association between maternal education and vaccination status has been reported in other studies in India and is thought to arise from heightened knowledge about health and enhanced communication skills stemming from education [22]. We found considerable differences in the uptake rates of the various optional vaccines. This variation may be a consequence
Table 5 Themes and illustrative participant quotes from semi-structured interviews. Theme and subtheme
Illustrative quotes
Knowledge about immunization need and vaccine preventable diseases “I get immunizations to keep my children from getting diseases. . .so my child does not Immunizations prevent disease in children have problems in the future.” Polio leads to disability and is a severe disease “It’s [the consequences are] great. If the child has a handicap in their body, if they don’t have an arm or leg, their life is lost. . .so we have to be careful and get the immunizations.” Perceptions about vaccine side effects “We will not miss any immunizations. Even if she has pain, she will cry for a little bit, Side effects are temporary and then it will go away.” “There will be a light fever because they got the shot. The fever shows that the Fever is a sign of vaccine efficacy medicine is working correctly. We are happy that it is working correctly.” “That child [who died after receiving polio drops] must have had a sickness already. Possible vaccine-related adverse events do not affect behavior We should not give polio drops to that child. If we do, he will get vomiting and diarrhea, right? Only healthy children should get it.” Receipt of optional vaccines “We couldn’t afford the cost, so we didn’t get it. His [my husband’s] salary is 4000 Cost is a limiting factor rupees. If we had to spend 2500 monthly and cut out everything else for the child’s immunizations, it would be hard” “If it’s for the child, we have to spend it. No matter how much it costs, if it’s for the Will obtain immunizations at any cost child, we have to spend money and buy it.”
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of fewer private providers offering PCV and rotavirus vaccines compared to Hib, MMR, and VZV. A recent survey of Indian pediatricians indicated that while most offered Hib routinely, most only selectively offered PCV and rotavirus vaccine to particular patients [23]. Reasons for this bias in offering of immunizations may be related to the higher cost and more recent licensure of PCV and rotavirus vaccine resulting in decreased provider familiarity. In our interviews, many parents expressed interest in purchasing additional optional vaccines but were limited by which ones their providers offered. Enhancing provider knowledge about and access to PCV, rotavirus, and influenza vaccines may increase their use. Strong parental support for vaccines was a major motivating factor in Pallavapuram as was found in another study on vaccine acceptability in India [24]. Barriers often noted in other studies like anxiety about vaccine side effects or perception that vaccines are unnecessary were rare in Pallavapuram [4,25–30]. In the literature, lack of concern about vaccine-preventable diseases is thought to be associated with decreasing experience with these diseases [25–28]. In our population, we did not find this relationship. Awareness of poliomyelitis was high and parents greatly feared the consequences of polio, but very few had direct experience with the disease. Knowledge of and reported experience with other vaccinepreventable diseases were even lower. General apprehension about infectious diseases and faith in immunizations boosted parental support of vaccination. Our study has several strengths. The area we studied encompasses the diverse socioeconomic statuses present in urban areas of south India, and door-to-door coverage studies are more accurate appraisals of immunization delivery than utilizing manufacturers’ sales data [10]. The coverage rates we measured for routine vaccines were comparable to published studies. Lastly, because vaccination rates in Tamil Nadu are among the highest in India secondary to a robust vaccine delivery system and outreach efforts, the state offers a good environment to study optional vaccine uptake. Limitations of our study include small sample size and area of sampling, which may limit generalizability. In our population, no central vaccination records existed so individual families maintained records. If no written vaccine record was available, we relied on parental recall to determine immunization status, which is subject to recall bias. However, studies in diverse communities demonstrate that parental recall has fairly good accuracy when compared to written records and that relying on card alone results in underestimation of immunization rates [31–34]. Parental recall has been used effectively in other recent coverage surveys in India [2,3]. We found that cost and lack of awareness were the greatest barriers to optional vaccine uptake. Adding these vaccines to the routine immunization schedule could address these barriers. Future analysis of vaccination rates of Hib in Tamil Nadu after its recent incorporation into the routine vaccination schedule may provide compelling data to support this argument. Concerns about disease burden, vaccine efficacy, availability of an affordable vaccine supply, and expense have hindered introduction of new vaccines in low- and middle-income countries [35,36]. In India, there is evidence to suggest that these obstacles can be overcome. Indian companies produce many of the optional vaccines [37]. Several studies indicate that introduction of rotavirus vaccine and PCV in the national immunization schedule would be cost effective [38,39]. The majority of childhood mortality in India is from diarrhea and pneumonia, and introduction of PCV and rotavirus vaccine in other countries resulted in significant reductions in rates of these diseases [40–47]. Increasing uptake of these vaccines has the potential to substantially decrease morbidity and mortality from vaccine-preventable disease.
5. Conclusions Uptake of routine immunizations was high in Pallavapuram but still fell below the goals espoused by the WHO and UNICEF. Coverage of optional vaccines was considerably lower and was deterred by high cost and low parental awareness. However, parental desire to obtain these vaccines was high. We believe Tamil Nadu is an ideal location in which to introduce additional vaccines into the routine schedule because there is strong support for vaccination and uptake of routine vaccines is already high. Competing interests The authors declare that they have no competing interests. Authors’ contributions AN initiated the concept for this study. KM and AH reviewed the literature, designed the study, and were responsible for writing the paper. KM, VK, and KP coordinated data collection in India. EB, YM, KB aided with statistical analysis for the cluster and qualitative study. All authors read and approved the final manuscript. Acknowledgments The authors would like to thank the Pallavapuram community for participating in this study. Funding was provided from the Leadership Education in Adolescent Health training grant #T71MC00009 from the Maternal and Child Health Bureau at the Health Resources and Services Administration and the Schiesman Traveling Fellowship from Boston Children’s Hospital. Dr. S. Swarnalakshmi, PhD, Ms. Geetha, and Dr. Suniti Solomon, MD, at YRG-CARE kindly reviewed the ethical aspects of the project in India. Mr. and Mrs. Kuppuswamy, Ms. Mary, Ms. Anjali, Ms. Dhanam, Ms. Pilomina, Mr. Vignesh, Mr. Rajendran Venkattareddy, Mr. Ravikumar, Ms. Uma Ganapathi, Mr. Shankar Kumar, Mr. Kolandavel Ramasamy, and Ms. Rajeswari Manthiram were graciously helpful in data collection and translation. Drs. Kathryn Edwards, MD, Elizabeth Woods, MD, Heather Corliss, PhD, Atsuko Koyama, MD, and Kathryn Brigham, MD provided helpful input on study design and/or manuscript review. References [1] Ehreth J. The global value of vaccination. Vaccine 2003;21(7):596–600. [2] International Institute for Population Sciences and Macro International. National family health survey (NFHD-3) India, 2005–06. Tamil Nadu, Mumbai, India: International Institute for Population Sciences and Macro International; 2008. [3] The United Nations Children’s Fund. Coverage evaluation survey: all India report. New Delhi, India: The United Nations Children’s Fund; 2009. [4] Kumar D, Aggarwal A, Gomber S. Immunization status of children admitted to a tertiary-care hospital of north India: reasons for partial immunization or non-immunization. J Health Popul Nutr 2010;28(3):300–4. [5] World Health Organization Department of Immunization, Vaccines, and Biologicals and UNICEF Programme Division, Health Section. Global immunization vision and strategy 2006–2015. Geneva, Switzerland: World Health Organization Department of Immunization, Vaccines, and Biologicals and UNICEF Programme Division, Health Section; 2005. [6] District Profile of Kanchipuram District. 2001; Available from: http://www. kanchi.nic.in/district profile pro.html. [7] Government of India Planning Commission. Press Note on Poverty Estimates, 2011–2012. Available from: http://planningcommission.nic.in/news/ pre pov2307.pdf. [8] Government of Tamil Nadu. Department of Economics and Statistics, Statistical handbook 2012, Available from: http://www.tn.gov.in/deptst/ Ecoindicator.htm. [9] Sundaresan T, Henderson RH. Cluster sampling to assess immunization coverage: a review of experience with a simplified sampling method. Bull World Health Organ 1982;60(2):253–60. [10] World Health Organization Department of Immunization, Vaccines and Biologicals. Immunization coverage cluster survey—reference manual. Geneva,
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