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Review

Progress and barriers towards maternal and neonatal


tetanus elimination in the remaining 12 countries:
a systematic review
Nasir Yusuf, Azhar A Raza, Diana Chang-Blanc, Bilal Ahmed, Tedbabe Hailegebriel, Richard R Luce, Patricia Tanifum, Balcha Masresha,
Mehoundo Faton, Mohamed D Omer, Saadia Farrukh, Khin D Aung, Heather M Scobie, Rania A Tohme

This systematic review assessed the progress and barriers towards maternal and neonatal tetanus elimination in the Lancet Glob Health 2021;
12 countries that are yet to achieve elimination, globally. Coverage of at least 80% (the coverage level required for 9: e1610–17

elimination) was assessed among women of reproductive age for five factors: (1) at least two doses of tetanus toxoid- Department of Immunization,
Vaccines, and Biologicals,
containing vaccine, (2) protection at birth, (3) skilled birth attendance, (4) antenatal care visits, and (5) health facility
World Health Organization,
delivery. A scoping review of the literature and data from Demographic and Health Surveys and Multiple Indicator Geneva, Switzerland
Cluster Surveys provided insights into the barriers to attaining maternal and neonatal tetanus elimination. Findings (N Yusuf MD,
showed that none of the 12 countries attained at least 80% coverage for women of reproductive age receiving at least D Chang-Blanc MPH);
Programme Division, United
two doses of tetanus toxoid-containing vaccine or protection at birth according to the data from Demographic and
Nations Children Fund
Health Surveys or Multiple Indicator Cluster Surveys. Barriers to maternal and neonatal tetanus elimination were (UNICEF), New York, NY, USA
mostly related to health systems and socioeconomic factors. Modification to existing maternal and neonatal tetanus (A A Raza MD, B Ahmed MBBS,
elimination strategies, including innovations, will be required to accelerate maternal and neonatal tetanus elimination T Hailegebriel MD); Department
of Immunization and Vaccine
in these countries.
Development, World Health
Organization Regional Office
Introduction As of December, 2020, 12 (20%) of the 59 high-risk for Africa, Brazzaville, Republic
In 1989, the World Health Assembly endorsed the global countries had yet to achieve MNTE: Afghanistan, Angola, of the Congo (R R Luce MD,
P Tanifum MD, B Masresha MD);
initiative to eliminate neonatal tetanus by 1995. In 1999, Central African Republic, Guinea, Mali, Nigeria, Pakistan, Health Section, UNICEF
the initiative was relaunched as maternal and neonatal Papua New Guinea, Somalia, South Sudan, Sudan, and Regional Office for West and
tetanus elimination (MNTE) because tetanus also affects Yemen. The slow pace of MNTE implementation Central Africa, Dakar, Senegal
mothers, targeting 59 high-risk countries and setting a indicates the complexities in these countries, which have (M Faton MD); Health Section,
UNICEF Regional Office for
target date for 2020 after the initial target dates of 2005 made it impossible to meet the global deadline of Eastern and Southern Africa,
and 2015 were missed. Neonatal tetanus elimination, elimination by 2020. This systematic review highlights Nairobi, Kenya
defined as having less than one neonatal tetanus case per the progress towards the global goal to eliminate maternal (M D Omer MBBS); Health
1000 livebirths in every district each year, is also used as a and neonatal tetanus in the remaining 12 countries and Section, UNICEF Regional
Office for South Asia,
proxy for maternal tetanus elimination.1 Strategies to the barriers that have delayed elimination. Kathmandu, Nepal
achieve MNTE include several approaches: vaccinating at (S Farrukh MBBS); Health
least 80% of pregnant women with at least two doses of Methods Section, UNICEF Regional
tetanus toxoid-containing vaccines (TTCV2+) during Search strategy and selection criteria Office for East Asia and the
Pacific, Bangkok, Thailand
antenatal care and outreach sessions; doing at least three We assessed the progress and barriers towards MNTE in (K D Aung MD); Global
rounds of tetanus toxoid-containing vaccine (TTCV) each of the 12 countries through compilation of MNTE Immunization Division,
supple­mentary immunisation activities, targeting women programmatic performance indicators using different Centers for Disease Control and
Prevention, Atlanta, GA, USA
of reproductive age in high-risk areas and aiming for at data sources. We assessed the protection of women
(H M Scobie PhD, R A Tohme MD)
least 80% TTCV2+ coverage; promoting clean births and infants against tetanus through immunisation
Correspondence to:
and umbilical cord care by strengthening skilled birth via several approaches: compiling the percentage of Dr Nasir Yusuf, Department of
attendance (SBA); and strengthening neonatal tetanus pregnant women receiving TTCV2+, from official Immunization, Vaccines, and
surveillance, including case investigation and response.2 country estimates reported to the WHO/UNICEF Joint Biologicals, World Health
Despite several missed deadlines to achieve MNTE, Reporting Form between 2015 and 2019,6 and from the Organization, Geneva 1211,
Switzerland
47 (80%) of the originally targeted 59 high-risk countries most recent Demographic and Health Surveys7 or yusufn@who.int
had achieved MNTE as of December, 2020 (figure 1), Multiple Indicator Cluster Surveys8 based on data among
resulting in an 88% decrease in the annually reported women aged 15–49 years who reported a livebirth during
neonatal tetanus deaths from an estimated 200  000 the last 5 years preceding the survey; compiling the
in 2000, to 25 000 in 2018.4 Additionally, partial elimination percentage of infants with protection at birth (PAB)
has been achieved in Nigeria (southeast and southwest against tetanus, which was assessed on the basis of
geopolitical zones), Pakistan (Punjab province), and Mali the timing since the last dose and number of doses of
(central and southern regions).5 Between 2010 and 2017, TTCV received by the mother, from WHO estimates
the number of targeted countries validated for MNTE between 2015 and 2019,9 and from the most recent
increased from 19 to 44, with an average of three countries Demographic and Health Surveys7 or Multiple Indicator
validated each year, but the number declined to one or Cluster Surveys;8 and compiling the total number of
two during 2018 and 2020 (figure 2). women of reproductive age who were targeted and

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Eliminated between January, 2000 and December, 2020 Not eliminated Eliminated before 2000 NA
women aged 15–49 years who reported a livebirth during
the last 5 years preceding the survey. Data was compiled
on three MNTE indicators: the percentage of deliveries
assisted by skilled birth attendants (eg, doctors, nurses,
and midwives), the percentage of deliveries that occurred
in health facilities, and the percentage of pregnancies
that had at least one antenatal care (ANC1) visit.
To assess barriers to achievement of MNTE in the
12 countries, we analysed data from the most recent
Demographic and Health Surveys7 or Multiple Indicator
Cluster Surveys8 to assess the predictors of the last birth
being protected against tetanus in each country and the
Figure 1: Global progress with maternal and neonatal tetanus elimination, 2000–20
barriers to accessing health care among women aged
Reproduced with permission from the World Health Organization.3 Progress towards the global goal of eliminating 15–49 years. A scoping review of the literature provided
maternal and neonatal tetanus in 59 high-burden countries, with 47 (80%) of 59 countries achieving elimination. an insight into health and other systems-wide barriers
Eight (67%) of 12 countries that are yet to eliminate maternal and neonatal tetanus are in the African continent, to achieving MNTE. The impact of the COVID-19
whereas the remaining four (33%) are in southeast Asia, and in eastern Mediterranean and western Pacific regions.
World Health Organization disclaimer: the boundaries and names shown and the designations used on this map do
pandemic on the implementation of vaccination and
not imply the expression of any opinion whatsoever of the World Health Organization concerning the legal status of TTCV supplementary immunisation activities was
any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. compiled from data available in the WHO repository.10
Dotted and dashed lines on maps represent approximate border lines for which there may not yet be full
agreement. World Health Organization, WHO. 2020. All rights reserved. NA=not applicable.
Data analysis
We compared the percentage coverage of TTCV2+
50 with the percentage PAB coverage to elucidate the
47 47 discrepancies in coverage that usually exist between
45
45 43
44 these two methods of computing tetanus protection
41 coverage.2 Although coverage of TTCV2+ considers only
40 vaccination coverage during the last pregnancy, PAB
35 coverage considers the total number of TTCV doses
35 34
received by the pregnant woman in her lifetime and the
date of the last dose to assess if the birth was protected.2
Number of countries

30 29
For South Sudan, the coverage of TTCV2+ from the
25 23
2010 Demographic and Health Survey was compared
with the coverage from the 2013 WHO/UNICEF Joint
20 19 Reporting Form, the first year WHO/UNICEF Joint
16 Reporting Form data were available for that country.
15
12 Additionally, the cumulative coverage of TTCV2+ from
11
10 9 9 supplementary immunisation activity rounds targeting
6 women of reproductive age was also analysed with data
5
5 4 from the global calendar of TTCV supplementary
2 immunisation activities.10
1
0 Although the WHO/UNICEF Joint Reporting Form
data allowed for national-level analyses, Demo­ graphic
00

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03
04

05
06

07
08
09

10

11
12
13
14

15
16

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18
19
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20
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20

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20
20
20
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20
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20

20

20
20

Year and Health Surveys or Multiple Indicator Cluster Surveys


also provided data for first subnational level (ie, regions,
Figure 2: Cumulative number of countries validated for maternal and neonatal tetanus elimination between
2000 and 2020 states, or provinces) and by demographic and socio­
Number of countries validated out of the total 59 countries targeted for maternal and neonatal tetanus economic factors. For all indicators, we assessed
elimination. Although progress has been made towards attaining the global goal, the different global deadlines countries’ performances towards attaining at least
(2005, 2015, and 2020) set for elimination have been missed.
80% coverage, the threshold for achieving MNTE.

received TTCV2+ during TTCV supplementary Results


immunisation activities from the most recent Demographics and income status of the 12 countries
(April, 2021) list of TTCV supplementary immunisation In 2019, the 12 countries that had yet to eliminate MNTE
activities available on the WHO website.10 had a total combined population of 149 million women of
To assess the protection against tetanus through clean reproductive age, with 98 million (66%) of these women
delivery in each of the 12 countries, we used estimates living in Nigeria and Pakistan (table 1). Eight (67%;
reported by the most recent Demographic and Health Afghanistan, Central African Republic, Guinea, Mali,
Surveys7 or Multiple Indicator Cluster Surveys8 among Somalia, South Sudan, Sudan, and Yemen) of the

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Population Year TTCV2+ coverage from SIAs among WRA10


of WRA
in 2019
(× 1000)11
2015 2016 2017 2018 2019 WRA WRA WRA with Date of last SIA10
targeted vaccinated TTCV2+
(× 1000) with TTCV2+ coverage
10

(× 1000)10

TTCV2+6 PAB9 TTCV2+6 PAB9 TTCV2+6 PAB9 TTCV2+6 PAB9 TTCV2+6 PAB9
Afghanistan 8778 91% 70% 58% 70% 86% 70% 85% 68% 85% 68% 11 472 5212 45% February, 2019
Angola 7327 71% 78% 70% 78% 67% 78% 66% 78% 54% 70% 8452 7097 84% December, 2014
Central African 1150 52% 60% 54% 60% 62% 60% 89% 60% 64% 60% 1033 804 78% September, 2011
Republic
Guinea 3161 54% 80% 60% 80% 60% 80% 70% 80% 80% 80% 5643 4773 85% March, 2020
Mali 4391 63% 85% 75% 85% 75% 85% 60% 85% 46% 85% 8462 4158 49% June, 2020
Nigeria 46 238 40% 55% 47% 55% 60% 55% 62% 60% 40% 60% 14 256 9365 65% March, 2020
Pakistan 51 374 68% 75% 78% 80% 62% 85% 60% 85% 62% 85% 30 235 25 405 84% March, 2020
Papua New 2159 46% 70% 44% 70% 40% 70% 25% 70% 31% 70% 1725 450 26% November, 2016
Guinea
Somalia 3544 67% 67% 62% 67% 61% 67% 59% 67% 58% 67% 1852 497 27% October, 2009
South Sudan 3190 28% 68% 38% 68% 49% 68% 44% 68% 40% 68% 9399 6002 64% January, 2020
Sudan 10 347 53% 77% 52% 77% 54% 80% 51% 80% 52% 80% 8491 7294 86% December, 2019
Yemen 7497 16% 70% 19% 70% 21% 70% 22% 70% 25% 70% 6650 3533 53% March, 2020
Total 149 156 ·· ·· ·· ·· ·· ·· ·· ·· ·· ·· 107 670 74 590 69% ··
PAB=protection at birth. SIA=supplementary immunisation activity. TTCV2+=at least two doses of tetanus toxoid-containing vaccine. WRA=women of reproductive age.

Table 1: Trend of coverage with TTCV2+ and PAB from 2015 to 2019 and TTCV2+ in SIAs in the 12 countries that have not yet achieved maternal and neonatal tetanus elimination

12 countries were classified by the World Bank Group as 80% in all 12 countries; however, PAB coverage
low-income countries in 2019, whereas the remaining was higher than TTCV2+ coverage in all countries.7,8
four (33%; Angola, Nigeria, Pakistan, and Papua New Pakistan (57%) and Yemen (9%) had the highest
Guinea) were classified as lower-middle-income and lowest TTCV2+ coverage, respectively, whereas
countries.12 Angola (66%) and Somalia (27%) had the highest and
lowest PAB coverage, respectively (table 2).
Protection against tetanus through immunisation As of 2020, 74·5 million (69%) of the estimated
In 2019, only two (17%; Afghanistan and Guinea) cumulative 107·6 million women of reproductive age
of the 12 countries reported the target of at least in the 12 countries that were targeted for TTCV
80% TTCV2+ coverage according to their official supplementary immunisation activities had received
estimated coverage through the WHO/UNICEF Joint TTCV2+, with coverage varying from as high as 86% in
Reporting Form,6 whereas four (33%; Guinea, Mali, Sudan to as low as 26% in Papua New Guinea (table 1).
Pakistan, and Sudan) countries achieved at least Many of the 12 countries have done at least one or
80% PAB coverage (WHO estimates).9 Yemen reported two rounds of supplementary immunisation activities in
the lowest coverage of TTCV2+ by the WHO/UNICEF a phased manner spread over 1 year or 2 years, but
Joint Reporting Form (25%), whereas Central African Angola, Papua New Guinea, and Somalia have not done
Republic and Nigeria had the lowest percentage of any rounds of supplementary immunisation activities
infants with PAB (60% each). The PAB coverage since 2014, 2016, and 2009, respectively. Mali, Guinea,
estimate, a more reliable indicator of the level of tetanus and Sudan have completed their three rounds of
protection than coverage of TTCV2+, maintained a supplementary immunisation activities in all high-risk
steadier trend and was higher than TTCV2+ coverage in districts and could be ready for MNTE validation in 2021.
all countries except in Afghanistan and in the Central However, the escalation of the COVID-19 pandemic in
African Republic. Between 2015 and 2019, there was no the African region might hinder validation in these
or limited improvement in TTCV2+ or PAB coverage in countries in 2021.
the 12 countries (table 1).
Based on the most recent Demographic and Health Protection against tetanus through clean delivery
Surveys or Multiple Indicator Cluster Surveys data, Data from the most recent Demographic and Health
TTCV2+ and PAB coverage among women that had a Surveys or Multiple Indicator Cluster Surveys showed
livebirth in the 5 years preceding the survey was less than that only four (33%; Angola, Guinea, Mali, and Pakistan)

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TTCV2+ coverage from the WHO/UNICEF MNTE indicators from most recent DHS7 or MICS8
Joint Reporting Form6
TTCV2+ coverage TTCV2+ coverage during Year of most TTCV2+ PAB Health facility SBA ANC1
in 2019 the year of most recent recent DHS or delivery
DHS or MICS MICS
Afghanistan 85% 93% 2015 34% 53% 48% 51% 59%
Angola 54% 70% 2016 56% 66% 46% 50% 82%
Central African 86% 76% 2010 ND ND 53% ND 68%
Republic
Guinea 94% 91% 2018 48% 59% 53% 55% 81%
Mali 72% 75% 2018 36% 50% 67% 67% 80%
Nigeria 40% 50% 2018 53% 62% 39% 43% 67%
Pakistan 62% 60% 2018 57% 64% 62% 64% 80%
Papua New Guinea 31% 25% 2018 27% 38% 55% 55% 76%
Somalia 58% 58% 2020 17% 27% 21% 32% 31%
South Sudan 38% 46% 2010 28% 37% 12% 19% 62%
Sudan 53% 53% 2014 32% 58% 28% 78% 79%
Yemen 25% 18% 2013 9% 28% 30% 45% 60%
ANC1=first antenatal care visit. DHS=Demographic Health Survey. MICS=Multiple Indicator Cluster Survey. MNTE=maternal and neonatal tetanus elimination. ND=no data
available. PAB=protection at birth. SBA=skilled birth attendance. TTCV2+=at least two doses of tetanus toxoid-containing vaccine.

Table 2: MNTE performance indicators in the 12 countries that have not achieved MNTE

Type and date of survey7,8 Subnational level Residence Education Wealth quintile
(province, region,
state, or governorate)
Lowest Highest Rural Urban No At least Lowest Highest
coverage coverage education secondary
education
Afghanistan DHS 2015 3% 79% 53% 55% 49% 76% 53% 59%
Angola DHS 2015 and 2016 39% 86% 46% 77% 45% 83% 42% 88%
Central African Republic DHS 2010 ND ND ND ND ND ND ND ND
Guinea DHS 2018 48% 73% 53% 73% 55% 76% 43% 75%
Mali DHS 2018 14% 67% 45% 65% 45% 67% 41% 68%
Nigeria DHS 2018 22% 97% 51% 77% 40% 90% 38% 87%
Pakistan DHS 2017 and 2018 27% 81% 63% 80% 52% 91% 44% 90%
Papua New Guinea DHS 2016 and 2018 15% 62% 36% 50% 21% 61% 25% 53%
Somalia DHS 2020 ND ND 32% 43% 23% 60% 10% 44%
South Sudan HHS 2010 ND ND ND ND ND ND ND ND
Sudan MICS 2014 42% 73% 55% 68% 47% 79% 44% 74%
Yemen DHS 2013 5% 53% 24% 38% 21% 56% 20% 40%
DHS=Demographic Health Survey. HHS=Household Health Survey. MICS=Multiple Indicator Cluster Survey. ND=no data available.

Table 3: Proportion of women aged 15–49 years whose last livebirth was protected against tetanus according to their background characteristics based
on the most recent DHS7 or MICS8 in the 12 countries that are yet to eliminate maternal and neonatal tetanus

of the 12 countries achieved at least 80% ANC1 coverage, Barriers to achieving MNTE in the 12 remaining countries
and none of the 12 countries had at least 80% coverage Analysis of the most recent Demographic and Health
for health facility delivery or SBA.7,8 ANC1 coverage was Surveys and Multiple Indicator Cluster Surveys data
highest in Angola (82%) and lowest in Somalia (31%), showed that children born to educated mothers, residing
SBA coverage was highest in Sudan (78%) and lowest in in urban areas, and from wealthy households were more
South Sudan (19%), and coverage for health facility likely to be protected at birth against tetanus versus
delivery was highest in Mali (67%) and lowest in South infants whose mothers were less educated, whose
Sudan (12%). In all countries, ANC1 coverage was higher families lived in rural areas, or whose families were
than coverage for health facility delivery and SBA, except poorer (table 3).7,8 For example, in Nigeria, infants born to
in Somalia. ANC1 coverage was also higher than TTCV2+ mothers in the highest wealth quintile households (87%)
and PAB coverage (table 2). were 2·3 times more likely to be protected at birth

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compared with infants whose mothers were in the lowest


Getting Getting Distance to Not wanting At least one
quintile households (38%). Nigerian infants born to permission money for health to go alone problem
mothers from Imo State in the southeast zone (97%) to go for treatment facility accessing
were 4·4 times more likely to be protected at birth treatment health care
compared with infants born in Zamfara State in the Afghanistan 51% 67% 67% 70% 89%
northwest zone (22%). Angola 31% 63% 52% 32% 70%
The most commonly reported barriers to accessing Central African Republic ND ND ND ND ND
health care by women living in eight of the 12 countries Guinea 30% 60% 46% 32% 68%
according to Demographic and Health Surveys or Mali 27% 41% 29% 20% 47%
Multiple Indicator Cluster Surveys were “getting money Nigeria 11% 46% 26% 16% 52%
for treatment” and “distance to health facility” (highest Pakistan 21% 30% 42% 58% 67%
in Afghanistan at 67% each).7,8 Other barriers reported Papua New Guinea 32% 63% 56% 44% 74%
included “not wanting to go alone” and “getting Somalia 50% 65% 62% 47% 73%
permission to go for treatment”, which in most cases South Sudan ND ND ND ND ND
could mean “getting permission from their husbands” Sudan ND ND ND ND ND
(table 4).7,8 Affordability, availability, and accessibility of Yemen ND ND ND ND ND
antenatal care providers were cited as hurdles to antenatal
ND=no data available.
care use in Nigeria,13 whereas in rural Mali, scarcity of
health facilities, limited availabilty of transportation, and Table 4: Proportion of women aged 15–49 years who reported that they have serious problems in
a long distance to health facilities were identified as some accessing health care for themselves when they are sick, by type of problem in the 12 countries yet to
eliminate maternal and neonatal tetanus7,8
of the barriers to antenatal care attendance, and access to
SBA and health facility delivery.14
MNTE implementation, especially TTCV supple­ were completely or partially destroyed.21 In Yemen, an
mentary immunisation activities, in the 12 remaining estimated 14·8 million people (>50% of the country’s
countries has been hampered by other competing population) had little to no access to basic health care,
priorities, scarce funding, and poor focused attention on including 8·8 million living in severely underserved
MNTE. Response to frequent disease outbreaks was the areas. Medical materials were reported to be in
key impediment to implementation of planned MNTE chronically short supply, with only 45% of health facilities
activities and might remain so in the foreseeable future, functioning.22 The United Nations Office for the
given the susceptibility of these countries to frequent Coordination of Humanitarian Affairs estimates that
disease outbreaks.15 Of top priority to most of the 1·2 million people (81% of whom are in Borno State)
12 countries is the response to ongoing wild poliovirus remain inaccessible to humanitarian agencies in
transmissions in Afghanistan and Pakistan, and the northeast Nigeria as a result of a humanitarian crisis
outbreaks of circulating vaccine-derived polioviruses lasting over a decade.23
in 23 countries, including Angola, Central African The COVID-19 pandemic has led to the postponement
Republic, Guinea, Mali, Nigeria, Somalia, Sudan, and of TTCV supplementary immunisation activities planned
Yemen, as well as measles outbreaks in Angola, for the first half of 2020 in seven countries (Central
Cameroon, Chad, Nigeria, South Sudan, and Sudan.16,17 African Republic, Guinea, Mali, Nigeria, Pakistan, South
Additionally, prolonged outbreaks of yellow fever in Sudan and Yemen) until the second half of the year and
Angola and Lassa fever in Nigeria have been reported.18,19 into 2021, and TTCV supplementary immunisation
In the face of frequent and prolonged diseases outbreaks activities were cancelled in three countries (Afghanistan,
in these countries, the implementation of MNTE Papua New Guinea, and Sudan). These rounds of
becomes of a lower priority as resources (time, financial, supplementary immuni­ sation activities were targeting
and human) become less available.15 an estimated 18 million women of reproductive age in
Protracted humanitarian crises, including armed the ten countries.10
conflicts, in parts of Afghanistan, Central African
Republic, Mali, Nigeria, Somalia, South Sudan, Sudan, Discussion
and Yemen have resulted in the destruction of health Despite the discrepancies in coverage between the
facilities, displacement of populations, including health different data sources, analyses show that, except for a
workers, have reduced access to health services by few countries, the performance indicators for MNTE in
populations, and have substantially delayed the imple­ the remaining 12 countries are generally suboptimal,
mentation of MNTE. A 2018 UN humanitarian crisis indicating poor implementation of MNTE strategies in
report noted that ongoing conflict in Afghanistan these countries. The WHO-recommended approach of
continued to hamper maternal and child health, targeting women of reproductive age in high-risk districts
particularly in rural areas where 75% of women live.20 In with three rounds of TTCV supplementary immunisation
the Central African Republic, of the total 1010 health activities enables a rapid build-up of immunity against
facilities, 236 (23%) were not functional because they tetanus and is the leading MNTE strategy, especially in

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the countries that have suboptimal routine immunisation Sustainable Development Goals and Immunization
programmes.24 This strategy, facilitated by country Agenda 2030, which has the goal to ensure that everyone
ownership, technical support from partners (WHO and has access to immunisation services,28,29 the 5·0 equity
UNICEF), and funding from donors, has helped to goal from Gavi, the Vaccine Alliance of reducing the
accelerate elimination. number of children that have never been vaccinated in
Due mostly to poor technical capacity, health workers in the past (zero dose),30 and the WHO Director-General’s
many countries suboptimally adhere to the recommended report on the Global Strategy for Women’s, Children’s
practice of adequately screening and administering and Adolescents’ Health (2016–2030).31 Using MNTE as a
appropriate doses of TTCV to pregnant women during tracer to promote health equity could help to address the
antenatal care visits. These health workers also do not scarce financial and human resources to support MNTE
have the skills to adequately and comprehensively record activities in those countries, and would ensure a system-
all TTCV doses administered to pregnant women, strengthening approach that would be sustainable to
including those doses provided during previous preg­ maintain MNTE.
nancies, which leads to an underestimation of livebirths The 12 countries that have not achieved MNTE are also
that were protected at birth.2 The WHO recom­mendation facing common barriers to attaining global eradication
of at least eight antenatal care contacts during each or elimination goals for polio, measles, rubella, and
pregnancy increases the opportunity to administer TTCV other diseases preventable by vaccination. Compared
to pregnant women, but implemen­ tation remains a with tetanus, countries usually prioritise the control of
challenge in countries with weak health systems.25 The polio or measles over MNTE implementation, due to
Maternal Immunization and Antenatal Care Situation their high transmissibility and potential for outbreaks,
Analysis (MIACSA) project noted that countries that including spread across borders.15 Given the common
recom­mended at least four antenatal care contacts were challenges across several disease initiatives, MNTE
more likely to have high PAB coverage (>90%).26 In most implementation in the remaining countries needs to tap
of the remaining 12 countries, TTCV2+, PAB, health into the experiences of the Global Polio Eradication
facility delivery, and SBA coverages were lower than Initiative and the other interventions delivered in
ANC1 coverage, suggesting missed opportunities to humanitarian settings to reach displaced, nomadic, and
administer TTCV and to educate pregnant women about conflict-affected populations with strong engagement of
the importance of health facility delivery and SBA. In civil society and key community stakeholders. Addition­
Angola, despite 82% ANC1 coverage in 2019, TTCV2+, ally, those 12 countries could accelerate the implemen­
PAB, health facility delivery and SBA coverages were tation of TTCV supplementary immunisation activities
56%, 66%, 46%, and 50%, respectively—an indication by integrating the activities with polio, measles, cholera,
of missed opportunities. A study in Lubumbashi, yellow fever, and other supplementary immunisation
Democratic Republic of the Congo, showed that despite activities for vaccine-preventable diseases.
93% of women having attended at least one ANC visit, The remaining 12 countries face multiple challenges
only 61% received at least one dose of TTCV.27 This to achieving MNTE, including poor political will,
discrepancy between antenatal care and TTCV2+ coverage scarce technical and financial resources, humanitarian
can be easily addressed by educating pregnant women crises, and competing priorities.15 Hence, achieving, and
and health-care providers, and ensuring availability of documenting, MNTE in those countries would require
TTCV at antenatal care sites. new tools and methods. In addition to the previously
As reported through Demographic and Health Surveys highlighted potential of linking MNTE to health equity,
or Multiple Indicator Cluster Surveys, the socioeconomic engagement of civil society and communities, and
barriers to seeking health care could also lower clinic integration of TTCV supplementary immunisation
attendance of maternal and newborn services. Barriers to activities with other vaccine-preventable diseases,
access to essential health services might be particularly countries might need to use new methods for delivery of
worse in the remaining 12 countries, especially among TTCV, such as the easy-to-use, compact, prefilled auto-
marginalised communities and populations and in rural disable devices, in remote and unsafe areas where low
areas. Given that tetanus affects the poorest and most numbers of sufficiently trained health-care workforces
marginalised populations, deprioritising MNTE might might hinder the provision of injectable vaccines.15,32
worsen existing health inequities, which could constrain Disruptions of essential health services (including
the achievement of the equity goal of universal health immunisation and reproductive, maternal, newborn, and
coverage. Ensuring that all pregnant women have child health) due to the COVID-19 pandemic were
access to clean deliveries and TTCV could be a path to reported by many countries and TTCV supplementary
strengthening the primary health care platform for the immunisation activities were postponed or cancelled in
integrated delivery of essential maternal, newborn, seven (Central African Republic, Guinea, Mali, Nigeria,
child, and adolescent health services. Hence, supporting Pakistan, South Sudan, and Yemen) of the 12 countries.33,34
those 12 countries to achieve MNTE would facilitate A modelling study to estimate the indirect effects of the
the implementation of the equity agenda of the COVID-19 pandemic on maternal and child mortality in

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low-income and middle-income countries showed an Declaration of interests


8–39% increase in maternal deaths per month, across We declare no competing interests.
118 countries, and reduced coverage of four childbirth Data sharing
interventions, including clean delivery, would account for All data used in this paper are publicly available and can be shared by the
corresponding author. The findings and conclusions in this report are
approximately 60% of the additional maternal deaths.35 those of the authors and do not necessarily represent the official position
The MNTE initiative needs to leverage on the ongoing of WHO, UNICEF, and the Centers for Disease Control and Prevention.
global efforts to sustain essential health services, to
Editorial note: the Lancet Group takes a neutral position with respect to
ensure the continued delivery of maternal and neonatal territorial claims in published maps and institutional affiliations.
services while countries are responding to the COVID-19
References
pandemic. 1 WHO. Maternal and neonatal tetanus elimination: the strategies.
Some limitations were apparent in the current 2020. https://www.who.int/initiatives/maternal-and-neonatal-
tetanus-elimination-(mnte)/the-strategies (accessed June 7, 2021).
systematic review. Our study data emanate from sources
2 WHO. Protecting all against tetanus: guide to sustaining maternal
that have known quality issues. With no access to the and neonatal tetanus elimination (MNTE) and broadening tetanus
raw data from the various sources, we were unable to protection for all populations. Geneva: World Health Organization,
2019.
calculate summary statistics, including 95% CI, as
3 WHO. Maternal and neonatal tetanus elimination: progress
the study relied on already calculated percentages for towards global MNT elimination. 2020. https://www.who.int/
the various indicators. The WHO/UNICEF Joint initiatives/maternal-and-neonatal-tetanus-elimination-(mnte)/
progress-towards-global-mnt-elimination (accessed June 7, 2021).
Reporting Form-reported TTCV2+ underestimates the
4 WHO. Maternal and neonatal tetanus elimination. 2020.
true tetanus protection among women of reproductive https://www.who.int/initiatives/maternal-and-neonatal-tetanus-
age. Low retention of home-based records by women elimination-(mnte) (accessed June 7, 2021).
of reproductive age results in recall biases during 5 WHO. Maternal and neonatal tetanus elimination: the partnership.
2020. https://www.who.int/initiatives/maternal-and-neonatal-
Demographic and Health Surveys or Multiple Indicator tetanus-elimination-(mnte)/the-partnership (accessed June 7, 2021).
Cluster Surveys for TTCV2+ and PAB estimates. We 6 WHO. Protection at birth (PAB) against neonatal tetanus and
were unable to assess the coverage of umbilical cord tetanus toxoid-containing vaccine (TT2+/Td2+) vaccination
coverage. 2020. https://immunizationdata.who.int/pages/coverage/
care practices, given that only two (Nigeria and Pakistan) tt2plus.html?GROUP=Countries&YEAR=&CODE= (accessed
of the 12 countries had this information in their June 7, 2021).
Demographic and Health Survey or Multiple Indicator 7 The DHS Program. Demographic and Health Surveys.
https://www.dhsprogram.com/Countries/ (accessed June 7, 2021).
Cluster Survey reports. Additionally, because of the
8 UNICEF. Multiple Indicator Cluster Surveys (MICS). https://mics.
known under-reporting of neonatal tetanus cases by unicef.org/surveys (accessed June 7, 2021).
surveillance systems that are mostly suboptimal in these 9 WHO. WHO–UNICEF coverage estimates data for protection at
countries, our analyses did not include neonatal tetanus birth (PAB) time series. 2020. https://www.who.int/entity/
immunization/monitoring_surveillance/data/PAB_estimates.xls
incidence. Strengthening neonatal tetanus surveillance (accessed June 7, 2021).
and using tetanus seroprevalence data for triangulation 10 WHO. Maternal and neonatal tetanus elimination: programmatic
of data sources could be used to improve on data quality update. 2021. https://www.who.int/initiatives/maternal-and-
neonatal-tetanus-elimination-(mnte)/programmatic-update
for the purpose of validation of MNTE.15,36 (accessed June 7, 2021).
11 WHO. Vaccine-preventable diseases: monitoring system.
Conclusions 2020 global summary. 2020. https://apps.who.int/immunization_
monitoring/globalsummary/countries (accessed June 7, 2021).
Despite the substantial progress towards MNTE, weak
12 World Bank. World Bank Country and Lending Group—country
health systems, humanitarian and socio­ economic classification. 2019. https://datahelpdesk.worldbank.org/
challenges, and more recently the COVID-19 pandemic, knowledgebase/articles/906519-world-bank-country-and-lending-
groups (accessed June 7, 2021).
are hampering the achievement of MNTE in the
13 Fagbamigbe AF, Idemudia ES. Barriers to antenatal care use in
remaining 12 countries. To overcome those challenges, Nigeria: evidences from non-users and implications for maternal
countries need to implement innovative approaches, health programming. BMC Pregnancy Childbirth 2015; 15: 95.
such as integrating MNTE activities with other health 14 Gage AJ. Barriers to the utilization of maternal health care in rural
Mali. Soc Sci Med 2007; 65: 1666–82.
activities, using MNTE to promote health equity access, 15 WHO. Report of the SAGE Working Group on Maternal and
sensitising health-care workers on the vaccination of Neonatal Tetanus Elimination and Broader Tetanus Prevention.
pregnant women during antenatal care, creating demand 2016. https://www.who.int/immunization/sage/meetings/2016/
october/1_Report_of_the_SAGE_Working_Group_on_Maternal_
for immunisation and clean deliveries from pregnant and_Neonatal_Tetanus_27Sep2016.pdf (accessed June 9, 2021).
women, and enabling non-traditional health workers to 16 WHO. Circulating vaccine-derived poliovirus type 2—global update.
administer TTCV using simple devices, especially in 2021. https://www.who.int/emergencies/disease-outbreak-news/
item/circulating-vaccine-derived-poliovirus-type-2-global-update
remote and rural areas. (accessed June 7, 2021).
Contributors 17 I VACCINATE. New measles surveillance data from WHO. 2019.
NY conceptualised the idea for this study, collected and analysed the data, https://ivaccinate.org/new-measles-surveillance-data-from-who/
and wrote the manuscript. HMS and RAT contributed to data abstraction (accessed Aug 26, 2021).
and the write up and review of the manuscript. All other authors 18 Relief Web. The yellow fever outbreak in Angola and Democratic
participated in the writing, reviewing, and editing of the manuscript, and Republic of the Congo ends. 2017. https://reliefweb.int/report/
have read and agreed to the published version of the manuscript. NY and democratic-republic-congo/yellow-fever-outbreak-angola-and-
RAT accessed and verified the data underlying the study. democratic-republic-congo-ends (accessed June 7, 2021).

www.thelancet.com/lancetgh Vol 9 November 2021 e1616


Review

19 WHO. Emergencies, preparedness, response. Lassa fever—Nigeria 29 Immunization Agenda 2030: a global strategy to leave no one
disease outbreak news. 2020. https://www.who.int/emergencies/ behind. 2021. http://www.immunizationagenda2030.org/ (accessed
disease-outbreak-news/item/2020-DON245 (accessed June 7, 2021).
June 7, 2021). 30 Gavi, the Vaccine Alliance. Gavi 5·0 strategy: phase V (2021–2025).
20 Relief Web. 2019 Afghanistan humanitarian needs overview. 2018. 2019. https://www.gavi.org/our-alliance/strategy/phase-5-2021-2025
https://reliefweb.int/report/afghanistan/2019-afghanistan- (accessed June 7, 2021).
humanitarian-needs-overview (accessed June 7, 2021). 31 WHO. Global Strategy for Women’s, Children’s and Adolescents
21 Equipe Humanitaire Pays et Partenaires. Plan de Réponse Health (2016–2030). https://www.who.int/life-course/partners/
Humanitaire, Janvier–Décembre 2019. Republique Centrafricaine. global-strategy/globalstrategyreport2016-2030-lowres.pdf (accessed
Humanitarian Relief Plan—Central African Republic. 2019. June 7, 2021).
https://reliefweb.int/sites/reliefweb.int/files/resources/2018_hrp_ 32 Quiroga R, Halkyer P, Gil F, Nelson C, Kristensen D. A prefilled
CAR_french-final.pdf (accessed June 7, 2021). injection device for outreach tetanus immunization by Bolivian
22 WHO. Yemen humanitarian response plan 2017. 2017. https://www. traditional birth attendants. Rev Panam Salud Publica 1998; 4: 20–25.
who.int/emergencies/response-plans/2017/yemen/en/ (accessed 33 WHO. WHO and UNICEF warn of a decline in vaccinations during
June 7, 2021). COVID-19. 2020. https://www.who.int/news/item/15-07-2020-who-
23 United Nations Office for the Coordination of Humanitarian and-unicef-warn-of-a-decline-in-vaccinations-during-covid-19
Affairs. About OCHA Nigeria. https://www.unocha.org/nigeria/ (accessed June 7, 2021).
about-ocha-nigeria (accessed June 7, 2021). 34 UNICEF. Maternal and newborn health and COVID-19. 2020.
24 WHO. The “high-risk” approach: the WHO-recommended strategy https://data.unicef.org/topic/maternal-health/covid-19/ (accessed
to accelerate elimination of neonatal tetanus. Wkly Epidemiol Rec June 7, 2021).
1996; 71: 33–36. 35 Roberton T, Carter ED, Chou VB, et al. Early estimates of the
25 WHO. WHO recommendations on antenatal care for a positive indirect effects of the COVID-19 pandemic on maternal and child
pregnancy experience. 2017. https://www.who.int/publications/i/ mortality in low-income and middle-income countries: a modelling
item/9789241549912 (accessed June 7, 2021). study. Lancet Glob Health 2020; 8: e901–08.
26 Giles ML, Mason E, Muñoz FM, et al. Antenatal care service 36 WHO. Vaccine preventable diseases surveillance standards. Annex 2:
delivery and factors affecting effective tetanus vaccine coverage in tetanus serosurveys. 2018. https://www.who.int/immunization/
low- and middle-income countries: results of the Maternal monitoring_surveillance/burden/vpd/WHO_SurveillanceVaccine
Immunisation and Antenatal Care Situational Analysis (MIACSA) Preventable_25_Annex2_R2.pdf?ua=1 (accessed June 7, 2021).
project. Vaccine 2020; 38: 5278–85.
27 Abel Ntambue ML, Françoise Malonga K, Dramaix-Wilmet M, This is an Open Access article published under the CC BY-NC-ND 3.0
Donnen P. Determinants of maternal health services utilization in IGO license which permits unrestricted use, distribution, and
urban settings of the Democratic Republic of Congo—a case study reproduction in any medium, provided the original work is properly
of Lubumbashi City. BMC Pregnancy Childbirth 2012; 12: 66. cited. In any use of this article, there should be no suggestion that WHO
28 UN. The Sustainable Development Goals Report 2016: leaving no endorses any specific organisation, products or services. The use of the
one behind. 2016. https://unstats.un.org/sdgs/report/2016/leaving- WHO logo is not permitted. This notice should be preserved along with
no-one-behind (accessed June 7, 2021). the article’s original URL.

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