Poliomyelitis outbreak investigation in Kayanza Health District, Burundi, 2023

Munekayi Padingani^1,2,3,&, Ezéchiel Nimbona^1,4, Bernadin Nyabenda^1,4, Doris Nindagira⁴, Grace Mbila⁵, Désiré Nolna⁶, Joseph Nyandwi^1,3

 

¹Field Epidemiology Training Program, Bujumbura, Burundi, ²African Field Epidemiology Network, Bujumbura, Burundi, ³National Institute of Public Health, Bujumbura, Burundi, ⁴Ministry of Public Health and fight against HIV and AIDS, Kayanza District, Burundi, ⁵Ministry of Public Health and fight against HIV and AIDS, Extend Program of Immunization, Burundi, ⁶World Health Organization Afro, Regional Office, Brazzaville, Congo

 

 

^&Corresponding author
Munekayi Padingani, Field Epidemiology Training Program, Buyezi, Bujumbura, Burundi.

 

 

 

 

Poliomyelitis is an infectious disease of viral origin that manifests clinically by the acute onset of flaccid paralysis. Poliovirus (PV) infection is transmitted either via the intestinal mucosa or the oropharyngeal mucosa. PV replicate within these mucous membranes, spread locally via the lymphatic system then systemically via the blood stream. Through blood PV can be disseminated in the body, subsequently infecting the central nervous system (CNS), causing aseptic meningitis or potentially irreversible acute paralysis. Paralysis can particularly affect the legs, arms and muscles responsible for breathing or swallowing, depending on the areas of the CNS that are affected by the infection. Paralysis of the respiratory muscles and/or swallowing can be fatal. This is observed in less than 1% of poliovirus infections in children under 5 years old [1, 2].

 

The common incubation period is 7 to 14 days, with a range of 3 to 35 days [1]. Infected people are most infectious 7 to 10 days before or after the onset of symptoms [1].

 

PV infection remains asymptomatic in approximately 90% of cases. Systemic symptoms such as fever, general malaise, headache, nausea and vomiting are present in approximately 10% of cases. Less than 1% of cases of PV infection cause severe disease (acute flaccid paralysis or aseptic meningitis); among which 5 to 10% die [1, 3].

 

Polioviruses (PV) are excreted in the stools and in the oropharyngeal secretions of the patient. PV transmission is done person to person through ingestion of water, food or other particles contaminated by stools containing PV (fecal-oral route) or by inhalation of pharyngeal secretions containing poliovirus (oral-oral route) [1,3]. The poliovirus is highly contagious, with sero conversion rates among household contact of children close to 100% [1].

 

In 1988, the World Health Assembly resolved to eradicate polio, leading to the establishment of the Global Polio Eradication Initiative (GPEI). As a result, partners are working together to ensure that every child gets several doses of polio vaccines [2]. Since the GPEI was launched, the number of polio cases has fallen worldwide by over 99%. More than 18 million affected people are able to walk today, who would otherwise have been paralyzed. Four out of five people in the world now live in certified polio-free regions [3]. Vaccines have stopped the spread of wild poliovirus in all countries, only Afghanistan and Pakistan remain endemic to Polio and experiencing an epidemic of wild poliovirus type I [4]. However, in recent years Africa has been facing epidemics linked to poliovirus derived from the vaccine strain with a predominance of type 2. This situation does not spare the sub-region of Central Africa including Burundi [5].

 

Burundi has been implementing an integrated surveillance system including the surveillance of cases of AFP and other vaccine-preventable diseases since May 1999 in all its health districts including Kayanza district. Through the surveillance system, the country was able to meet the certification criteria and virological classification of cases in June 2000. The quality of this system enabled the rapid detection in 2009 of a case of imported wild poliovirus. Following this detection, interventions were implemented to stop this transmission in 2011.

 

Circulating vaccine-derived poliovirus type 2 (cVDPV2) is the most prevalent form of polio in Africa and outbreaks of this type of poliovirus are the highest reported in the region, with more than 400 cases reported in 14 countries in 2022 [6]. Burundi shares a border with the DRC, which has experienced epidemics of cVDPV2 since 2017 and measles in 2022. The South Kivu Province, DRC has recorded VDPV2 cases. The movement of populations and goods between the two countries increases the risk of importing these epidemics between these countries.

 

The country is currently facing a series of health emergencies, including the polio epidemic due to cVDPV2, declared on March 17, 2023, following the isolation of a 4-year-old child with acute flaccid paralysis (AFP). In addition to the AFP case, 21 other VDPV2 were isolated from environmental wastewater samples [7]. Internal population movements put everyone at risk of contracting polio.

 

The Republic of Burundi is a landlocked country in Central Africa within the Great Lakes region; made of eighteen (18) provinces and forty-nine (49) districts [8]. It has a population of 12.5 million people (2021), high proportion of young people under 15, a very low proportion of elderly people, a sex ratio of 97 men for 100 women, a mainly rural population [9]. Burundi is one of the most densely populated countries in the world, estimated at a ratio of 442 people per square kilometer (2020 population projection). With a gross domestic product of 3.07 billion USD in 2022, Burundi is considered as a low-income country [10]. The country has a poor life expectancy of 62 years largely driven by deaths due to preventable diseases [11].

 

The lack of adequate infrastructure and human resources to meet urgent community health needs makes Burundi's health system unstable. People of Burundi are highly susceptible to the wide variety of diseases that are ravaging the country. A case of AFP was notified on June 18 2023 from Kayanza district, samples were collected and positive results to cVDPV2 were received on 8 August 2023. An investigation was initiated to determine cases´ characteristics, identify possible sources of infection, determine the extent of the outbreak and make recommendations.

 

 

Study Setting

 

The study was conducted in Kayanza district of Kayanza province, in the northern part of Burundi with a population of 843.799 in 2011 [9]. The district had twenty-five health facilities, seventeen performed daily vaccine-preventable diseases surveillance while eight did not do diseases surveillance, all were private health facilities.

 

Poliomyelitis is one of the notifiable diseases under surveillance. Health structures send reports at the end of each week to district, provincial and national level through DHIS2. Districts also send monthly reports to provincial and national levels. All cases of acute flaccid paralysis (AFP) are notified within 24 hours to the next level.

 

Kayanza clinic catchment area has both rural and urban zones. Our study was conducted in the urban zone because that is where the confirmed case resided.

 

Concerning routine vaccination, Kayanza Health District had not reached the threshold of 90% coverage in OPV3 and IPV over the last 3 years. 2023 data shows coverage of less than 50% of target children. Kayanza health center reported vaccination coverage of around 50% in the first half of 2023.

 

Burundi-EPI

 

The country has an expanded programme on Immunization (EPI), whose mission is to protect children against vaccine-preventable diseases such as diphtheria, tuberculosis, pertussis, measles, poliomyelitis, tetanus, hepatitis B virus and haemophilus influenza type b. It has officers at central level in Bujumbura, provincial level, district level, primary health level and community level with daily vaccine-preventable routine vaccination and diseases surveillance. Concerning poliomyelitis, Burundi´s routine vaccination offers 5 doses of polio vaccines. First dose bivalent oral polio vaccine (bOPV) is given at birth, second dose bOPV given at six weeks, third dose bOPV given at ten weeks and fourth (bOPV) and fifth inactivated polio vaccine (IPV) doses are given at 14 weeks [12].

 

Acute Flaccid Paralysis (AFP) case finding is done clinically using the World Health Organization (WHO) case definition ie. an acute onset of weakness or paralysis, characterized by reduced tone without obvious causes[13]. After AFP detection, the case must be notified then investigated. Two stool samples are collected 24 hours apart from an AFP case and from contacts during investigation based on date of symptoms onset[14]. An AFP contact is any child with frequent contact such as touching, sharing toys and sharing food with an AFP case. The surveillance data flows from community level to central level passing through district level and provincial level using phone calls, notification forms and District Health Information Software (DHIS2). The notification form is available at all health facilities. The stool specimens are collected by laboratory staff or clinicians from the identified AFP case and transported to the regional laboratory in Kampala Uganda by WHO country office for testing through the national EPI office. The turnaround time from sample collection to results is 2 weeks. The results of the tests are documented at National EPI office and shared back to the referring district and health facility.

 

Burundi is using nVPO2 vaccine to respond to cVDPV2 outbreak. In case there is an AFP case confirmed with polio after test, an investigation of the confirmed case will follow. For each confirmed case twelve community contacts matched by age to that case are investigated. The vaccination history of these contacts will be recorded and a stool sample for each contact obtained. Data and findings from detailed investigation will be sent to the national EPI office. This procedure must be completed within forty eight hours following confirmation of a case of cVDPV2[15]. All investigations are provided free of charge to all contacts.

 

Study design and population

 

This was a cross-sectional study design involving all children under 15 years of age and residents of Kayanza district from June to August 2023 .

 

Sample

 

This was a convenience sampling. Polio confirmed case and 12 contacts of less than 5 year´s old living in urban zone of Kayanza clinic catchment area in Kayanza health district, Burundi from June to August 2023 were included in the study. According to nVPO2 surveillance guidelines.

 

Data collection and analysis

 

Data were collected using a Polio investigation form extracted from nVPO2 surveillance guidelines. Patient´s notes review and confirmed case household visit were conducted to fill the form. We used an interviewer-administered questionnaire to collect data from family members of confirmed case and parents or guardians of contacts aged less than 5 years old who lived in the case´s area at the time of paralysis onset. The selection of contact was done according to nVPO2 surveillance guidelines, where a total of 12 households were visited with 12 community controls interviewed; one control per household. Four (4) households were selected from each of three (3) randomly selected directions of the VDPV2 case. In each direction, every fourth household was sampled. When a household did not have children meeting the inclusion criteria or the child and primary caregiver were not present at two attempted visits, the next adjacent households was visited until a suitable household was reached. Information relating to vaccination status, the presence or absence of signs of AFP was sought from contacts.

 

Stool samples were collected from contacts by laboratory staff, transported in a cooler to EPI office in Bujumbura for transmission to the regional laboratory in Kampala for testing, where the Poliovirus case diagnosis was made. The environmental assessment was performed in the confirmed case household, its surroundings and the mother´s workplace. We checked for data quality using completeness of patient notes, completeness of the investigation form and completeness of vaccination cards. Data were analyzed using Excel to calculate frequencies, proportions and median.

 

Ethical considerations

 

Permission was sought from the provincial medical Director, District head Doctor and from National EPI office. Since this was a response activity to an outbreak, no formal ethical clearance was sought. Written consents were obtained from parents or caregivers of children and medical staff. Confidentiality was assured and maintained throughout the study and no names were used in the questionnaire. We kept the data safe and confidential in an office and computer only accessible by authors.

 

 

Clinical description

 

This was a confirmed case of circulating vaccine-derived poliovirus type 2 (cVDPV2) notified as AFP in June 2023 by Kayanza clinic. The case was a male child, aged 18 months, from a family of 2 children of which he is the second and from the Province and health district of Kayanza. The patient was living with his parents in the urban center of the Kayanza clinic catchment area. The child´s father was unemployed and the mother run a small business selling avocados near Kayanza market, always with the child.

 

He presented to the clinic on 18 June, 2023 with paralysis which began suddenly on his right leg on June 15, 2023. Samples were collected according to guidelines but positive results came after 52 days. In the history of the illness, his mother said that the child had fever at the beginning and the paralysis progressed gradually and on examination the paralyzed limb was sensitive and the paralysis was asymmetrical. In the past medical history, the child was on plumpy Nut which is a specific formulated product for the nutritional rehabilitation of children from six months of age and adults suffering from severe acute malnutrition. Concerning vaccination, the child received 4 doses of bivalent oral polio vaccine (bOPV) and one dose of inactivated polio vaccine (IPV) according to his vaccination card and this was in line with the country´s polio routine vaccination schedule. He also received a dose of novel oral polio vaccine type 2 (nOPV2) during the first round of the national immunization response campaign on June 13, 2023 at the market where his mother sold goods, according to the mother.

 

During the household visit, the case still had paralysis of the right lower limb but no more pain nor fever. However, he was able to crawl and stand upright by leaning on an immovable object. The mother declared that she had lived in different places with her son, one of them is Bujumbura Mairie nord district where many polio environmental cases were detected[16] before returning in October 2022 to Kayanza where she is now based. There was no history of travelling outside Burundi.

 

Environmental assessment

 

The case family lived in an unhygienic environment and the household did not meet the conditions of a healthy habitat. Drinking water in the house was stored in uncovered containers which highly predisposed it to contamination. The neighbourhood was an unsanitary area. The case family´s latrine had a door but was stained with stool . The daily activity of the child's mother was selling avocados along the Kayanza market alongside other people selling food in the open and she was always with her son. We observed an open drain with wastewater all along Kayanza Market. One market septic tank was filled and its contents flowed into the same drain.

 

Contacts tracing

 

Twelve contact cases were found based on nOVP2 surveillance guidelines. 67% (8) of contacts were male and 33% (4) female. All contacts were fully vaccinated and had received one dose of nOPV2 during the June 2023 immunization campaign, 75% (9/12) had vaccination card, 25% (3/12) did not have and 100% (12/12) of contacts did not present any signs or symptoms related to polio. Their median age was 23.4 months with An interquartile range of 20.25 to 34.5 months (Table 1).

 

 

Our study revealed that the confirmed poliomyelitis case received 4 doses of bOPV, one dose of IPV and one dose of nOPV2 on 13 June and developed paralysis on 15 June. All contacts were vaccinated and had no clinical signs pointing to polio. We postulate that the case probably fell ill due to inability to mount sufficient immune response because he was malnourished. The case child was taking plumpy Nut before getting sick implying that he had malnutrition. This is supported by Dr Michel de Lorgeril, who underlined that fragile subjects whose immune system is not capable of neutralizing the toxin can become ill despite vaccination and vaccination itself can weaken the immune system[17]. His thoughts are supported by Anthony R Mawson et al in a study done in the United States of America where they found that vaccinated children had a higher rate of allergies and neurodevelopmental disorders (NDD) compared to unvaccinated children, vaccination was significantly associated with NDD after controlling for other factors[18]. Our case received only one dose of IPV. The Centers for Disease Control and Prevention (CDC) of the United States of America considered fully vaccinated a person who received four doses of any combination of IPV and trivalent oral polio vaccine (tOPV), or a primary series of at least three doses of IPV or tOPV. Two doses of inactivated polio vaccine (IPV) are 90% effective or more against paralytic polio but three doses are 99% to 100% effective[19]. Based on the above this case child was not fully vaccinated nor protected against polio. This maybe a contributing factor to the paralysis.

 

However, it is possible that immunodeficient patients could excrete polio virus for a prolonged time after receiving oral polio vaccine according to Madhu Chhanda Mohanty et al in study done in India[20]. Considering that both the case and the contacts in our study received five doses of oral polio vaccine, the above explanation could explain the presence of polio virus in the case stool specimen, since the latter was malnourished/immunodeficient.

 

Our finding was contrary to the 2022 Israel polio outbreak where the first confirmed case was an unvaccinated case[21].

 

The switch from trivalent oral polio vaccine (tOPV) to bivalent oral polio vaccine (bOPV) came with some disadvantages. The cessation of tOPV facilitates the spread of undictated or newly emergent cVDPV2 among persons without immunity to serotype 2 polioviruses after switch[22], this could be the case with the polio case in our study.

 

Our study noted crowding and exposure to an inadequate hygienic environment to the child, with the possibility of contamination of drinking water inside the house and poor maintenance of latrine in the home of the case and its surroundings could all have contributed to the child getting ill considering that a circulating variant poliovirus was identified in many environmental surveillance sites in Burundi[7]. All these factors were probably linked to poverty. By improving standard of living, we can control and/or eliminate polio in Burundi. This is similar to findings by Michel Georget who said the rise in the standard of living and improvement in hygiene have been the essential factors in improving health, far ahead of vaccinations[23].

 

Our study was not without limitations. We conducted our investigation 2 months after onset of paralysis because of the long turnaround time of results. This could have impacted negatively on the investigation´s outcomes. Such as reduction of chances to find active or positive cases among contacts, change of environment and any other areas of investigation.

 

 

Our study shows that there was only one confirmed polio case in Kayanza district during the investigation period. We noted factors that can facilitate poliovirus transmission from confirmed case's household setting and behaviors of the community at large. The case child lived in an unhygienic environment which may have exposed him to polio virus in the environment either from circulating polio virus or virus which he shed due to his poor immunity. The child got only one dose of IVP and was malnourished which could have contributed to his failure to mount an adequate immune response to polio making him vulnerable to get poliomyelitis. It is necessary to continue investigation of all AFP cases, initiate environmental surveillance of polio in the area. There is need to introduce one or two more inactivated polio vaccine doses in the Burundi's routine vaccination schedule and sensitize the community on personal and environmental hygiene.

 

 

The authors declare no competing interests.

 

Funding

 

The study was made possible by AFENET and WHO Burundi.

 

 

Conception of the study: Munekayi Padingani, Ezéchiel Nimbona, Bernadin Nyabenda, Doris Nindagira, Grace Mbila, Désiré Nolna, Joseph Nyandwi; data collection: Munekayi Padingani, Ezéchiel Nimbona, Bernadin Nyabenda, Doris Nindagira, Grace Mbila; data Analysis: Munekayi Padingani, Ezéchiel Nimbona, Grace Mbila, Désiré Nolna; writing the paper: Munekayi Padingani, Ezéchiel Nimbona; critical Review of the paper and final approval for submission: Munekayi Padingani, Ezéchiel Nimbona, Bernadin Nyabenda, Doris Nindagira, Grace Mbila, Désiré Nolna, Joseph Nyandwi. All the authors have read and agreed to the final manuscript.

 

 

This research was conducted through the structured Field Epidemiology Training Program supported by African Field Epidemiology Network and Centers for Disease Control and Prevention of United States through the Ministry of Public Health and fight against HIV/AIDS. We would like to acknowledge the support of Kayanza district health staff and the community for data collection. Consent for publication was obtained from the study population.

 

 

Table 1: Demographic and clinical characteristics and vaccination status of polio case contacts in Kayanza clinic catchment area, August 2023

 

 

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