By mid-April 2020, the Coronavirus disease-2019 (COVID-19) had spread across all continents with two million cases and 120,000 deaths reported worldwide [1
]. Risk factors for adverse outcomes had already been established [2
] with healthy women of childbearing age, newborn babies and infants generally considered to be less severely affected by the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) than other age groups [4
]. However, as the pandemic has progressed, the associated disruption of public services has caused significant collateral damage with particular implications for maternal and child health [6
There are now growing concerns over the severe impact of COVID-19 on the provision of vital immunization services [8
], although the consequences are yet to be systematically evaluated. Finding the balance between guarding against the spread of COVID-19 versus controlling well known preventable diseases has proven to be delicate and difficult. For instance, recent modelling has predicted that not maintaining routine childhood immunization in Africa will lead to more deaths than possible COVID-19 deaths associated with visits to vaccination clinics [10
]. The World Health Organisation (WHO), in conjunction with UNICEF, GAVI and the Sabin Vaccine Institute, has undertaken two online immunization “pulse” surveys. The first of over 800 national and subnational immunization experts, completed in April 2020, focused on understanding the disruption caused by COVID-19 to routine delivery of the expanded programme on immunization and mass vaccination campaigns [11
]. The second, published in June 2020, after our own survey was completed, also aimed to understand the extent of disruption, although it had fewer respondents [13
]. Based on their first survey, the WHO warned that COVID-19 was beginning to disrupt life-saving immunization services around the world, putting millions of children—in rich and poor countries alike—at risk of diseases such as diphtheria, measles and polio [11
]. By the end of May, mass vaccination campaigns against measles were beginning to be cancelled in some countries for fear of contracting COVID-19 when visiting health services [14
]. The ability to deliver routine vaccines will also have been affected by redeployment of healthcare workers to tackle COVID-19.
To gather a swift snapshot of the global picture and to explore the changes in immunization services experienced by local frontline staff, we initiated an online survey of the members of the IMmunising PRegnant women and Infants NeTwork (IMPRINT) in mid-April 2020. IMPRINT is a UK-funded global network of stakeholders working within basic science, immunology, vaccinology, social sciences, industry, public health and national and international policy, who are investigating the biological and implementation challenges to the use of vaccines in pregnancy and the early postnatal period [16
]. Given the special interests of IMPRINT, our survey had a specific focus on immunization services for pregnant women and newborns, but also included questions on routine infant and toddler vaccination schedules. With its 290 members based in 51 countries worldwide, this network provided a unique forum to collate personal insights into the “collateral damage” caused by COVID-19, specifically related to the delivery of local and national immunizations, allowing us to further compare the situation in high income (HICs) versus low and middle income countries (LMICs).
The IMPRINT survey has provided a snapshot and “big picture” impression of the impact of COVID-19 on maternal and infant immunization services at the grassroots level, within a global context. At the time of our survey, the epidemic was in full swing in HICs and precautionary measures were being taken across LMICs. Our findings support the concerns of healthcare professionals and organisations worldwide about the significant indirect or “collateral” implications of the global COVID-19 pandemic on the provision of services for pregnant women and children. This is predicted to have enormous consequences to maternal and child health outcomes in both the short- and long-term [7
Whilst there is public concern about immunization services in times of COVID-19, accurate country-specific data remain poorly available, most notably from LMICs [8
]. Our stakeholder survey included both HICs and LMICs and found that more than half of respondents reported disruption in routine maternal and childhood vaccination programmes. This is consistent with the World Health Organisation’s (WHO) first online immunization survey of over 800 immunization experts, including representatives of Health Ministries and global health organizations from over 100 countries, which reported that over 50% of the expanded programme on immunization programmes had been disrupted [11
]. The repeat WHO survey conducted in June 2020 found that immunization programme disruption remained an issue for the majority of respondents [13
]. Similarly, in recent correspondence from Pakistan, one of the only published reports providing this level of detailed data in a LMIC, the average number of daily immunization visits (accounting for all antigens) are reported to have decreased by more than half during the lockdown compared with baseline, with the steepest decline at the start of the pandemic in Pakistan in April 2020 [39
]. There is also growing evidence from England, Scotland and the United States that the COVID-19 pandemic response has caused vaccination rates to decline even within HICs [40
Our survey explores issues as perceived not only by experts but also healthcare providers and researchers, at the grass roots level of vaccine delivery. This grassroots perspective complements the WHO immunization surveys whose respondents worked at national or subnational levels [13
]. Moreover, it conveys the concerns of stakeholders from LMICs, specifically Sub-Saharan African, representing 75% and 65% of the total participants, respectively. This has enabled us to explore potential differences between HICs and LMICs. Although several studies have emerged modelling the trajectory of the outbreak in African countries [43
], the voice of health care providers and governing bodies in these settings has been less audible and there is a distinct lack of large-scale data or more granular evidence from national immunization programmes. This may be because, to date, the epicentre of the pandemic has primarily been within Asia, Europe and the Americas, with lower case numbers within Sub-Saharan African countries, with the exception of South Africa. As the epidemiology shows, however, the pandemic is still evolving and cases in sub-Saharan Africa are increasing daily [1
]. Finally, our survey is unique in reporting issues not only around delivery of the infant expanded programme on immunization vaccines but also extending to immunization services for pregnant women, providing insights into the provision of antenatal care where these vaccines might be administered. Pregnant women represent a vulnerable group, often overlooked during epidemics, as recently seen during the Ebola outbreak [44
Whilst the overarching sentiment expressed by the respondents was uncertainty, we identified three key vaccine delivery issues relating to (i) access, (ii) provider and (iii) user concerns, each with different associated subthemes. These are largely consistent with the main reasons attributed by experts, to date, to the disruption of global immunization services, primarily highlighting a combination of vaccine demand and supply factors [45
]. More specifically, the WHO survey outlined the contribution of: (1) parental reluctance to leave home due to restrictions on movement, a lack of information or fear of COVID-19, (2) poor availability of health workers due to travel restrictions, lack of PPE and redeployment to pandemic response duties and (3) transport delays and problems getting vaccine supplies to clinics [11
]. These themes are entirely in keeping with our results.
Although similar issues were broadly reported by all respondents, irrespective of immunization and location, there appeared to be some differences between HICs and LMICs, implying that tailored strategies are needed. “Parental concern” was more frequently reported from HICs respondents, particularly fear of contracting COVID-19 by attending healthcare settings. In comparison, respondents from LMICs more commonly reported “access” and “provider” issues; indeed, difficulties secondary to “vaccine shortages” and “logistics” were primarily described within LMICs and were only rarely mentioned by HIC respondents. Our finding is supported by reports from UNICEF, stating that the pandemic response to COVID-19 has caused logistical delays to vaccine shipments worldwide, namely in LMICs [45
The consequences of interruptions to routine immunization programmes has the potential to be widespread and catastrophic [7
]. At least 80 million children under the age of one are estimated to be at risk from vaccine preventable diseases due to missing out of routine immunizations [11
] with measles a particular concern [15
]. Previous infectious disease outbreaks (including Ebola) were also associated with increased cases of vaccine-preventable diseases such as measles [46
]. In the recent outbreak in the Democratic Republic of Congo, three times as many people died from measles than from Ebola [47
]. Moreover, lockdown has exposed and exacerbated existing immunization inequities and uptake barriers, both within and between different countries [9
]. A recent detailed benefit–risk analysis, modelling the impact of missed childhood vaccinations in Africa, found that the benefit of averting vaccine-preventable infections far outweighed any possible COVID-19 morbidity and mortality associated with immunization clinic visits [10
Our study has some clear limitations. Although our geographical reach was very wide, the number of respondents per location is small and represents only a convenience sample. In particular there were a small number of respondents (n
= 12) from HICs. More detail on disruption issues was given from the United Kingdom (UK) respondents, which is then reflected with more comments in Figure 2
B being from the UK. A further limitation is that the overall response rate from the IMPRINT network was quite low (17%), although this is likely due to the limited time period given to respond, in order to primarily capture the initial concerns and attitudes towards vaccine delivery, as a “snapshot” at the start of the pandemic. Further surveys would benefit from involving more grass-roots participants based in different locations, including a comparison of rural versus urban settings. Nevertheless, our survey represented 18 nationalities worldwide, across 5 continents, and included a range of stakeholders, based in clinical, public health or research departments. Non-response bias could also have occurred in this study; important responses by participants from particular demographic groups, occupations or countries, or those too busy to respond, could be missing and therefore their views are not accounted for within the results. It is also possible that those who responded were biased towards having noticed changes, whilst others who felt that all had remained the same were possibly less likely to engage in the questionnaire. Further research is also needed to quantify the impact of the COVID-19 pandemic on the delivery of routine immunizations worldwide to enable catch up programmes to be planned. However, the ability to assess this rapidly will vary by location based on the routine immunization data collection systems available.
Repeating this survey in the future would be informative and is already planned. This would primarily assess any changes in the key issues identified, particularly as the first wave of the pandemic evolves [1
]. This repeat survey will aim to increase the response rate, particularly from countries now at the epicentre of the pandemic, and to explore further how to manage the challenges of immunization disruption. The epicentre has currently shifted to South America (Brazil) and, therefore, it would have been too early to capture the key issues, concerns and experiences of these countries with this initial survey [1
]. Moreover, some areas in Sub-Saharan African are now seeing a significant increase in COVID-19 cases [43
], which might lead to further changes in routine immunization services; on the other hand, other countries may have established effective mitigation strategies, after initially responding by downgrading services for fear of a rising epidemic, which, to date, has not materialised. Finally, it would be important to assess if lessons have been learned, further recommendations or guidelines have been published at the national or local level (or alterations to the existing ones) and the implementation of novel strategies has helped to overcome identified barriers.
As the COVID-19 pandemic continues, ongoing studies are needed to monitor routine immunization disruption and to further understand the reasons for disruptions to inform local vaccination catch-up programmes. Similarly, further work, beyond the modelling undertaken so far [10
], is needed to understand the benefits of attending immunization appointments versus COVID-19 transmission risk. To address the current uncertainty reflected by this short study and experienced by healthcare providers, clearer and more tailored communication is urgently needed [8
], particularly for LMICs. Improved efforts in communicating policies and conveying key messages should be targeted at pregnant women and parents, emphasizing the importance of attending routine vaccination services, despite the COVID-19 pandemic response. This is imperative for all settings, although our findings suggest there has been less official information provided for parents based in LMICs. Potential strategies in these settings may also need to focus on more community engagement to improve immunization uptake [48
]. Accurate and up-to-date advice can be delivered using more user-friendly approaches, for example via social media, given the importance of accurate online messaging during the pandemic [49
]. Effective communication strategies would serve to tackle misinformation, which has, unfortunately, been a worldwide concern during the pandemic [49
]. Within our survey, “vaccine acceptance/conspiracy theories/anti-vaxx sentiments” were brought up more frequently by LMICs, specifically Sub-Saharan African countries (although not uniformly across settings). This may be consistent with the wave of vaccine hesitancy [47
] and broader mistrust currently spreading across this region, with regards to both COVID-19 illness and potential COVID-19 vaccine trials to be undertaken in the future [51
]. To date, the pandemic has largely been interpreted as an imported problem. This perception has in some places hampered acceptance of preventative measures [52
] and might impact on future immunization campaigns, if a vaccine is tested and finally introduced.
Given the provider issues voiced by respondents in this questionnaire, increased efforts are needed to optimize logistics, both at a local and national level. This primarily includes supporting vaccine supply chains, reinforcing transport or infrastructure networks (for both vaccine delivery and user access/travel) and providing access to hand-washing facilities and PPE.
Prioritization of vaccination services is needed at local, regional and national levels, and recommendations have been provided by agencies such as the Joint Committee on Vaccination and Immunization in the United Kingdom and in Canada (both referenced by respondents in this survey) [32
]. Midway during the pandemic, WHO also published a framework for governments to guide the conduct of vaccination campaigns [27
]. This includes the importance of risk assessing the likelihood of outbreaks of vaccine-preventable diseases alongside the current transmission of COVID-19. General efforts explaining the safety measures implemented need to be communicated, in combination with the message that vaccination matters and saves lives, pandemic or not.
Beyond blanket recommendations, however, we may also need to focus on developing alternative, innovative and, in some cases, context-specific strategies to overcome or circumvent disruptions to service provision. Local measures should, therefore, ensure safety and practicality, but still be sufficiently flexible to rapidly adapt to the evolving situation, thereby avoiding suspension of key immunization programmes or services. Simple solutions such as aligning vaccination with other maternal and child health reviews, as well as robust infection control procedures, can enable the safe provision of key vaccines during the pandemic [37
]. Alternative vaccination delivery mechanisms such as utilising pharmacies may also need to be considered [55
]. More innovative examples include the development of drive-by or mobile clinics [56
]; reassigning existing locations to facilitate vaccine delivery e.g., maternal antenatal clinics moved to the local football stadium, as described by one respondent, thereby overcoming issues with overcrowding and enabling social distancing; and a trial of “trace and immunise” systems (particularly using a digital interface) [39
Based on our findings, the WHO framework and also the outcomes of the recent GAVI summit [57
], we developed an “at-a-glance” visual summary of important recommendations for key stakeholders (Figure 3