Measles outbreak: knowledge, vaccine hesitancy, health-seeking practices among caregivers of children with measles and factors associated with measles transmission in Sanyati District, Zimbabwe, 2022

¹Department of Global Public Health and Family Medicine, Faculty of Medicine and Health Sciences, University of Zimbabwe, Harare, Zimbabwe, ²Department of Health and Environmental Services, Kadoma City, Kadoma, Zimbabwe, ³Zimbabwe Field Epidemiology Training Program, Harare, Zimbabwe, ⁴African Field Epidemiology Network, Harare, Zimbabwe

^&Corresponding author
Tendai Munetsi, Department of Global Public Health and Family Medicine, Faculty of Medicine and Health Sciences, University of Zimbabwe, Harare, Zimbabwe

Introduction    

Measles is a vaccine-preventable disease and still causes mortality and morbidity in developing countries. The disease is caused by a morbillivirus and humans are the only reservoirs. The mode of transmission is through aerosolized droplets, direct contact with the nasal and throat secretions of infected persons [1]. Infected individuals are infectious four days before and four days after the onset of rash [2]. The case fatality ratio is between 3%-5% in developing countries; however, it may increase in times of crisis [1]. The complications of measles are severe in malnourished children and children with weakened immune systems due to HIV/AIDS and other diseases [2].

Globally in 2018, there were 9.7 million cases reported and 14 000 deaths because of measles, and the majority of the cases were children under the age of five years. In the World Health Organization (WHO) African region, there were 43 950 confirmed measles cases from the case-based surveillance system [2]. The African region incidence was 38.4 cases per million inhabitants, and 12 countries in the region had an incidence less than one per million inhabitants. In the first quarter of 2022, 17 500 cases were reported, and it was a 400% increase when compared to the same period in 2021. Twenty outbreaks were also reported during the first quarter of 2022 and it was an increase in eight countries when comparing to the same period in 2021 [3]. In 2013, measles caused 40 000 deaths in the African region and it remains the major cause of death among children under five in many African countries [1]. In Zimbabwe 2008, eight percent of under-five mortality was as a result of measles [4].

In 2011, the WHO African Region adopted goals for measles elimination by 2022; however, despite all efforts being made to increase vaccination coverage, pockets of unvaccinated children still exist in societies for philosophical, religious, and cultural reasons. Outbreaks usually occur among those groups of people with low vaccination coverage [5]. Vaccine hesitancy is one of the major factors contributing to low vaccination coverage, hence outbreaks [6]. Sanyati District identified three cases of suspected measles and three suspected measles deaths on the 4^th of August 2022 at Chakari 40 km from Kadoma City. On the 11^th of August 2022, the cases increased by 1400% to 42 suspected cases, and the deaths increased to four. Four specimens were taken to the laboratory for testing, and they were all immunoglobulin M (IgM) positive. A single laboratory confirmed measles case indicates an outbreak and Sanyati District was therefore in an outbreak of measles since 4 August 2022 [7].

Measles is a highly infectious disease that can spread rapidly among susceptible individuals if there are no appropriate containment measures. The disease has been targeted for elimination, hence the need for prompt investigation. We therefore investigated the measles outbreak in terms of time, person, and place, knowledge, vaccine hesitancy, and health-seeking practices of caregivers. We also determined the factors associated with measles transmission in Sanyati District, 2022.

Methods     

Study setting: the study setting was Sanyati District with 18 rural wards and 17 urban wards and a population of 256 613 people [8]. The district is in Mashonaland West Province, Zimbabwe. It has a total of 18 rural health facilities, six council clinics, one mission hospital, and Kadoma General Hospital, all but one provide vaccination services. The estimated population of children under 15 years was 135 674 in Sanyati District [8].

Study design and study population: we used a 1:1 unmatched case-control study to determine vaccine hesitancy, knowledge, health-seeking practices and factors associated with measles transmission. A case was defined as any person who developed fever and maculopapular rash and cough or coryza or conjunctivitis or any laboratory-confirmed measles IgM during the period 4th of August 2022 to 30th of September 2022, below the age of 15 years, whose residency was in Sanyati District and appeared on the district line list. A control was defined as any person who did not develop signs and symptoms consistent with measles and resided in the same locality as a case in Sanyati District from August 4, 2022, to September 30, 2022, and was under 15 years of age. The study population was any resident of Sanyati District under the age of 15 years and their caregiver. The study unit was any child who was under the age of 15 years and their caregiver who resided in Sanyati District and met the inclusion criteria. Any child under the age of 15 years and their caregiver who met the case definition, gave consent, and lived in Sanyati District during the period from August 4, 2022, to September 30, 2022, were included. Any child who was under the age of 15 years whose sibling or caregiver had already been interviewed in this study was excluded. We used the under 15 years´ population as measles predominantly affects children under 15 years, especially in regions with suboptimal vaccination coverage. This age group often accounts for the majority of cases during outbreaks.

Sample size calculation: we calculated sample size using Pococks´ formula for sample size calculation at 95% confidence interval and 80% power. Sensitivity analysis was done for the risk factors: being unvaccinated (83.6%), vitamin A supplementation (66.5%) and belonging to the apostolic sect (63.65%) [9]. Expecting a 75% response rate the minimum calculated sample size was 123 caregivers of cases and 123 caregivers of controls.

Sampling: all cases were recorded in the district line list on Microsoft Excel 10^TM. To select cases, we conducted simple random sampling using Microsoft Excel 10^TM RAND function with the measles line list as the sampling frame. Inclusion criteria were applied before sampling. We selected neighbors of cases who had children under fifteen years who had not developed signs and symptoms consistent with measles as our controls.

Measurement of variables: we calculated the case fatality ratio (CFR) using the total number of cases on the line list as the denominator. Age-specific attack rates (AR) for children under 15 years were calculated for the whole district and also for the wards with the under-15 years´ population for the whole district and each specific ward as the denominator, respectively. Vaccine hesitancy was measured by a validated Parent Attitudes about Childhood Vaccines (PACV) survey using a five-point, bipolar Likert scale [10]. Vaccine hesitancy responses were grouped together and non-hesitant responses were grouped to become yes and no responses to hesitancy. The responses were also scored by assigning a numeric score of two for items answered with a hesitancy response, a score of one to items answered with don´t know/ not sure and a score of zero to non-hesitant responses. Item scores were summed up to a raw score in an unweighted fashion and converted to a scale ranging from 0-100 using simple linear transformation [10]. A score of 50 and above indicated vaccine hesitancy [10]. Good knowledge on measles was measured by four correct answers out of the five questions asked.

Data collection tools and procedure: a pretested interviewer-administered questionnaire with ‘adapted parental attitudes´ on childhood vaccinations was used to collect data. Records were reviewed to gather information from patient records, Road to Health Cards and the measles line list.

Data analysis: we used Microsoft Excel 10^TM to calculate CFR and AR for the whole district and also for each ward in the district. An epidemiological curve was created using Microsoft Excel 10^TM and a spot map was created using Q-GIS version 3.26.1™. The software CDC Epi Info version 7.2.5™ was used to generate frequencies, medians and proportions for the demographic characteristics, knowledge on measles, health-seeking practices, and vaccine hesitancy of caregivers and compared them between cases and controls. Backward logistic regression was used to identify independent factors associated with measles transmission. The variables that had p < 0.25 during bivariate analysis were included in the multivariate analysis.

Data availability statement: the dataset for the interviewer-administered questionnaires is available upon request.

Ethical considerations: approval was obtained from the Health Studies Office (HSO) and permission to conduct the study from the District Health Executive (DHE) Sanyati District. Ethical approval was sought from the local institution review board in Sanyati District and Kadoma City Health. Written informed consent was obtained from caregivers and assent from children/minors. The questionnaires and consent forms were stored under lock and key.

Results     

We analyzed the Sanyati District line list for the period 30 April 2022 to 27 August 2022. A total of 281 cases, including 27 deaths were recorded on the line list between 30 April 2022 and 27 August 2022. All deaths were among children under the age of 15 years. The median age of the cases was 60 months (Q1=26; Q3=108). The median delay in health seeking was 3 days (Q1=2; Q3=5). The case fatality rate (CFR) was 9.6 per 100 cases for Sanyati District. The attack rate was 1.08 per 1000 population for the whole district. There were 131 (47%) females with an attack rate of 0.97 per 1000 population and 150 (53%) males with an attack rate of 1.10 per 1000 population. The attack rates and deaths by ward in Sanyati District are presented in Figure 1.

Time attributes (Epi Curve)

The primary case was on 30 April 2022, several other cases were reported in May, June and July 2022. The first deaths were recorded on 8 May 2022 and were recorded on the line list in retrospect. The index cases were reported on 4 August 2022 at Chakari Clinic from New Begin Village. The first peak was reached on 11 August and the second on 20 August 2022. There were 70 cases on the line list that did not have a date of onset. The outbreak was still ongoing after 25 August 2022. The time attributes for the Sanyati District outbreak are presented in Figure 2.

Case - Control study

Demographic characteristics

A total of 123 cases and 123 controls were interviewed. Fifty cases (40.7%) were below the age of five years and for controls 94 (76.4%) were below the age of five years. There were 71 (58%) males among cases and 72 (59%) males among controls. Seventy-four cases (60.2%) were not vaccinated for measles with the measles rubella vaccine whereas 16 (13%) of controls were not vaccinated with the measles rubella vaccine. Vitamin A supplementation among cases was 56 (45.5%) and among controls it was 110 (89.4%). There were 122 (99.2%) Christians among cases and 121 (98.4%) among controls, with 59 (48.0%) of cases and 113 (91.9%) of controls belonging to denominations that allow health seeking. The cases and controls were comparable on most demographic variables (Table 1).

Clinical Signs, Symptoms and Complications of Measles in Sanyati District, 2022

The most common signs and symptoms of measles were maculopapular rash 121 (98.4%), fever 112 (91.1%), cough 103 (83.7%) and conjunctivitis 100 (81.3%). General body malaise 2 (1.6%) was the least common symptom. Of the eleven measles cases that did not present with fever, seven had received measles vaccination. Eighty-seven cases (70.7%) presented with at least one measles complication. These were: pneumonia 17 (13.8%), ear infection 32 (26.0%), mouth ulcers 36 (29.2%), diarrhoea 68 (55.3%), and vomiting 12 (9.8%).

Health seeking practices and management of measles cases in Sanyati District, 2022

Sixty-one (48.8%) cases indicated that they sought treatment for measles and 64 (51.2%) indicated not seeking treatment for measles. Treatment for measles was based on the presenting symptoms. Among those that sought treatment for measles at health facilities, Paracetamol 28 (22.7%), Tetracycline Eye Ointment (TEO) 19 (15.4%) and Amoxicillin 31 (25.2%) were the most prescribed medications at health facilities. The cases also used home remedies to manage measles 69 (56.1%) and the home remedies included okra (Dicerocaryum senecioides), Coca-Cola, not bathing, parents´ celibacy and confession in cases of infidelity. About 62 (50.4%) of cases were satisfied with the use of home remedies and 69 (56.1%) cases preferred home treatment to hospital treatment.

Caregiver knowledge on measles in Sanyati District, 2022

Forty-seven (38.2%) caregivers of cases knew the cause of measles, whereas 82 (66.7%) caregivers of controls knew the causes of measles. One hundred and eighteen (95.9%) caregivers of cases knew at least one symptom and 119 (96.8%) caregivers of controls knew at least one symptom of measles. Sixty-two (50.4%) of caregivers of cases knew how measles is prevented and 107 (87.0%) caregivers of controls knew how measles is prevented. On knowledge of precautions to take when there is a measles case at home 91 (74.0%) caregivers of cases were knowledgeable and 110 (89.4%) caregivers of controls were knowledgeable. Approximately 85 (69.1%) of the cases knew home remedies for treatment of measles and 30 (24.4%) of controls knew home remedies for measles treatment.

Vaccine hesitancy and parental attitudes about childhood vaccines in Sanyati District, 2022

Among the respondents, 74 (60.2%) cases and 20 (16.3%) controls delayed having a child get the measles vaccine for reasons other than illness or allergy. Sixty-five (52.99%) cases and 10 (8.1%) controls decided that children should not get the measles vaccine for reasons other than illness or allergy. After total scoring there were 47 (38.2%) cases with vaccine hesitancy and 6 (4.9%) controls with vaccine hesitancy scores (Table 2).

Factors associated with measles transmission in Sanyati District, 2022

The factors that were included in multivariate analysis that had a p<0.25 were being unvaccinated (OR=10.10 95%CI: 5.34-19.10), age more than five years old (OR=4.73 95%CI: 2.73-8.20), being apostolic (OR=3.33 95%CI: 1.90-5.86), being male (OR=0.97 95%CI: 0.58-1.61), distance to health facility less than five kilometers (OR=0.90 95%CI: 0.53-1.52), vitamin A supplementation (OR=0.10 95%CI: 0.05-0.19), attending a gathering (OR=3.09 95%CI: 1.82-5.23), knowledge on measles cause (OR=0.31 95%CI: 0.18-0.52), knowledge on measles precautions (OR=0.34 95%CI: 0.17-0.68), knowledge on measles prevention (OR=0.15 95%CI: 0.08-0.29) and knowledge on measles spread (OR=0.62. 95%CI: 0.31-1.23). The independent factors associated with measles transmission were not being vaccinated (aOR=3.26 95%CI: 1.27-8.34) (p=0.01), being over the age of five years (aOR=3.38 95%CI: 1.81-6.31 (p<0.001) and having received vitamin A supplementation (aOR=0.31 95%CI: 0.11-0.83) (p=0.02) (Table 3).

Discussion     

The major findings in our study were that the cases had poor health-seeking practices and they preferred use of home remedies to hospital treatment. The majority of cases were not vaccinated against measles, most cases were above the age of five years, and most caregivers of cases belonged to an apostolic sect that does not allow health seeking. Factors associated with measles transmission included not being vaccinated against measles, being over the age of five years and vitamin A supplementation.

Children who were not vaccinated were at a higher risk of contracting measles compared to those who were vaccinated. This is consistent with the results from a measles outbreak investigation in Zaka, Masvingo, where those not vaccinated were at risk for contracting measles [9]. It is also consistent with the results from an outbreak investigation in Nigeria in which the risk of having measles was lower with at least one dose of measles vaccination compared to those who were not vaccinated [11]. In another study on measles outbreak in Uganda, low vaccination coverage was identified as a factor associated with measles transmission together with single-dose measles immunisation [12]. The majority of caregivers of controls knew the causes of measles, how it is prevented and the precautions to take when there was a measles case at home, when compared to caregivers of cases. These different levels of knowledge of measles may explain why the majority of controls were vaccinated.

In our study, the main reason for not vaccinating children was belonging to apostolic sects that do not allow health-seeking. The overall vaccination coverage in Sanyati District at the time of the outbreak was at 90% which was close to the WHO-recommended 95% coverage; however, pockets of unvaccinated children existed in areas that were dominated by religious objectors [13]. An analysis of measles vaccine hesitancy in Sanyati District in this study revealed that children were not being vaccinated for reasons other than vaccine availability, illness, or allergy. The majority of caregivers were not concerned about potential side effects or that the vaccine would not work; however, the main reason for not vaccinating their children was due to religious reasons. Parental exposure to measles anti-vaccination material and perceptions on the effectiveness of the measles vaccine were some of the reasons for vaccine hesitancy in a study on measles vaccine hesitancy in Sudan [14]. On the other hand, a study on the religious barriers to measles vaccination in United States indicated that they were centred on the use of aborted human foetus in the vaccine; however, the barriers were not only based on faith reasons [15]. The same was reported in a study on religion and measles vaccination in Indonesia, where Muslims did not vaccinate their children from measles as the measles vaccine contains haram materials [16]. Other barriers to measles vaccination among religious objectors were related to the safety and efficacy of the vaccines and these reasons are different from what we found in Sanyati District [16].

Being older than five years old was found to be a substantial risk factor for measles infection, which may be due to a combination of immunological, behavioral, and programmatic characteristics. Following the first measles vaccination, children in this age range may have had declining immunity, particularly if they missed the second dose, which is normally given at 18 months. Unvaccinated or just partially protected older children may result from inadequate follow-up and poor coverage of the second dose vaccination. Additionally, their exposure risk in high-transmission environments is exacerbated by greater social mixing brought about by community involvement and school attendance.

We recommended including the Apostolic Women Empowerment Trust (AWET) in the childhood vaccination activities. We also recommended health education targeting the catchment areas of the facilities with high attack rates. Another recommendation was that children should be vaccinated against measles and receive vitamin A supplementation. Outreaches for vaccinations and health education on measles should be done every quarter in hard-to-reach areas. Consultations with local religious leaders should be done.

Strengths and limitations: our study strengths included a representative sample size, which improves the generalizability of our results and the use of advanced statistical analyses to strengthen interpretations. One of the study's limitations was poor data quality on the measles line list, as there were cases that did not have a date of onset indicated and cases that were entered in retrospect on the line list, which were identified during active case searches and contact tracing. To address this, we excluded cases that did not have complete vital information from analysis.

Conclusion     

The main findings of this study were, the majority of cases were not vaccinated, most caregivers of cases belonged to an apostolic sect that does not allow health seeking. Factors associated with measles transmission were measles vaccination, Vitamin A supplementation and being over five years. The majority of cases preferred home treatment of measles to hospital treatment. As part of the public health actions, health education was given to caregivers on the signs and symptoms of measles and the importance of reporting to health care facilities for management. Awareness campaigns and active case searching were done. Supplementary activities for immunization were done for the six-month to 59-month age group and Vitamin A supplementation. Consultations with community and church leaders were conducted in the hard-to-reach areas.

Competing interests     

The authors declare no competing interests.

Authors' contributions     

Tendai Munetsi, Daniel Chirundu, and Addmore Chadambuka: conception, design, data collection, analysis and interpretation of data. The first draft of the manuscript was written by Tendai Munetsi and Daniel Chirundu. Addmore Chadambuka, Tsitsi Patience Juru, Gerald Shambira, Notion Tafara Gombe, Mufuta Tshimanga and Richard Makurumidze critically revised the manuscript for intellectual content. All authors read and approved the final manuscript.

Acknowledgments     

We would like to acknowledge Kadoma City, Health Studies Office, and Sanyati District.

Tables and figures     

Table 1: demographic information of the cases and controls in Sanyati District, Zimbabwe, 2022

Table 2: vaccine hesitancy using the parental attitudes on childhood vaccines in Sanyati District, Zimbabwe, 2022

Table 3: factors associated with measles transmission in Sanyati District Zimbabwe, 2022

Figure 1: measles attack rates by ward and spatial distribution of measles deaths in Sanyati District, Zimbabwe, 2022

Figure 2: epi curve for Sanyati District, Zimbabwe measles outbreak 2022

References