OBJECTIVES:

In Zambia, a significant number of infants die in the community. It is hypothesized that delays in care contribute to many of these so-called “brought in dead” infants.

METHODS:

We analyzed free-text narratives from verbal autopsies, in which families narrate the final series of events leading to each infant’s death. Using the 3-delays model framework and working iteratively to achieve consensus, we coded each narrative using NVivo software to identify, characterize, and quantify the contribution of delays and other factors to the fatal outcome.

RESULTS:

Verbal autopsies were collected from 230 families of brought in dead infants younger than 6 months of age. As many as 82.8% of infants had 1 or more delays in care. The most-common delay was in the family’s decision to seek care (54.8%), even as severe symptoms were frequently described. Similarly, 27.8% of infants died en route to a health care facility. Delays in receiving adequate care, including infants dying while waiting in line at a clinic or during referral from a clinic to a hospital, occurred in 24.7% of infants. A third of infants had been previously evaluated by a clinician in the days before their death.

CONCLUSIONS:

Delays in care were the rule rather than the exception in this population of Zambian infants. Accessing care requires families to navigate significant logistic barriers, and balance complex forces in deciding to seek care. Strategies to avoid such delays could save many infants lives.

What’s Known on This Subject:

The 3 delay model addresses delays in seeking, reaching, and receiving care in low-middle-income countries. It is commonly used in studies of pregnant women and their newborns. Little is known about delays in care of infants beyond the immediate newborn period.

What This Study Adds:

Stories of infants who were brought dead revealed nonbiological circumstances contributing to infant deaths as perceived by the family. Through their voices we describe delays in care of these infants and identify factors that could be targeted for preventive measures.

Under-5 mortality rates in sub-Saharan Africa are the highest in the world, estimated at 78 per 1000 live births. Many deaths are not recorded by the health system, and official cause of death is lacking. In Zambia, under-5 mortality rates are high, estimated at 40 to 75 per 1000 births.1  A significant number of infants die in the community and are referred to as “brought in dead” (BID). There is an extreme paucity of data around the problem of infant community deaths, and identifying the circumstances surrounding them is critical to reduce infant mortality rates.

Since 2017, we have been conducting a prospective postmortem study; the Zambia Pertussis Respiratory Syncytial Virus Infant Mortality Estimation (ZPRIME) study. In ZPRIME, we use a modified verbal autopsy (VA) to try to categorize causes of death among BID infants. VAs are used to estimate the probable cause of death in cases in which an official cause is not available and involve an interview of a caregiver about signs and symptoms of the deceased.2,3  The modified VA in ZPRIME includes an open-ended narrative, in which the infants’ caregivers describe in their own words the events that led to the infant’s death. As our team reviewed the reports, it became increasingly apparent that the narratives represented a potentially valuable source of qualitative data describing the social circumstances surrounding each death.

Accordingly, we conducted an analysis of these narratives to try and better identify common patterns of health-seeking behaviors that contributed to these deaths. We organized our analysis around the “3 delay model,” described by Thaddeus and Maine.4  The model, originally used to explore delays in care surrounding obstetrical deaths, has since been adopted to describe delays in care for neonates in low-middle-income countries (LMICs).57  The 3 delays are (1) delays in decision to seek care, (2) delays reaching the health care facility, and (3) delays receiving adequate care at the health care facility.

Applying this model, we aimed to better identify common patterns of health-seeking behaviors that might have contributed to infant deaths in the community and identify potential opportunities to prevent such deaths in the future.

ZPRIME is an ongoing postmortem study funded by the Bill & Melinda Gates Foundation. ZPRIME seeks to enroll all deceased infants, hospitalized and BID, aged 4 days to 6 months in Lusaka, Zambia, an age group at high risk of dying from respiratory syncytial virus and pertussis. Lusaka is a large city of >2 million.8  The majority (>90%) live in large, dense peri-urban slums. There are approximately a dozen primary health care facilities serving these populations; all are referrals to University Teaching Hospital (UTH). UTH morgue serves as the source for enrolling all of the infants included in the current analysis.

Ethical oversight for ZPRIME was provided by the institutional review boards at the University of Zambia and Boston University. All caregivers of enrolled infants provided written informed consent.

Data collection was completed by a team trained in grief counseling, interviewing families of deceased infants and nasopharyngeal swab collection. In Lusaka, the majority of BID infants are referred from outside clinics to the UTH morgue, where an official death certificate is issued. Fifty-two percent of deaths in our study were BID. The research counselors located at UTH were notified about each BID infant. Because of resource constraints, we were only able to collect VAs among ∼90% of BID infants. After adjusting for our 89% consent rate, approximately two-thirds of all Lusaka’s BID infants were enrolled in ZPRIME and provided VA data during the time period of this analysis.

Between August 2017 and October 2018, we conducted 230 VAs among BID infants. For each infant, counselors collected demographic and medical information, a nasopharyngeal swab sample for pathogen testing, and a VA from the caretakers. The VA was conducted in English, which is nearly universally spoken in Zambia. We defined BID infants as infants who died without having been admitted to a hospital. This included deaths occurring during the delivery of outpatient care at clinics and during referral to a higher level of care.

Our VA is an abbreviated version of the validated Institute for Health Metrics and Evaluation tool.3  The modified VA contains close-ended questions about symptoms preceding the death, followed by a free-text narrative prompted by the following phrase: “Now, using your own words, please describe the events leading up to your child’s death. Please take as much time as you need and be as detailed as you can.”

The current analysis is focused solely on the VA narratives. Our 5-person coding team included a qualitative researcher, an epidemiologist, a pediatrician, and 2 medical students. All data were coded and analyzed by using NVivo software. Demographic data for each infant were included as attributes. To estimate severity of medical status, we developed a modified list of danger signs based on the Integrated Management of Childhood Illness guidelines, as detailed in Fig 1.9,10  The process of identifying common themes related to infant deaths was iterative. First, each team member read all the narratives independently to build a list of nonbiological themes (codes) identified as contributing to the death. Next, we harmonized our lists into a single comprehensive list, assigning clear definitions to all codes (Fig 2).

FIGURE 1

Final listing of codes for the free-text narrative analysis. With the exception of the 3 delays, which were included a priori as the primary framework for analysis of these data, the list of codes and attributes was developed through an iterative process by the coding team. Final codes were determined by consensus, and quality control was ensured by having the coding team individually code a set of 20 narratives to ensure consistent interpretation and application of these codes.

FIGURE 1

Final listing of codes for the free-text narrative analysis. With the exception of the 3 delays, which were included a priori as the primary framework for analysis of these data, the list of codes and attributes was developed through an iterative process by the coding team. Final codes were determined by consensus, and quality control was ensured by having the coding team individually code a set of 20 narratives to ensure consistent interpretation and application of these codes.

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FIGURE 2

Danger signs suggesting severe disease in an infant. This list was created by the World Health Organization and is used, in part, to render clinical decisions within the Integrated Management of Childhood Illness algorithm.

FIGURE 2

Danger signs suggesting severe disease in an infant. This list was created by the World Health Organization and is used, in part, to render clinical decisions within the Integrated Management of Childhood Illness algorithm.

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Each narrative could be assigned to >1 code. To confirm coding consistency, 20 random narratives were coded by each of the researchers independently, then decisions were compared and discussed. The process was repeated until there was uniform consistency in coding. We then divided up all narratives and coded them individually, each narrative coded by at least 2 researchers. If there were disagreements, coding was discussed by the team to achieve consensus.

Demographic data were included in each infant’s NVivo file as attributes. For each code, we reported the number and percentage of narratives that were linked. We then completed a mixed-methods analysis (ie, quantitative analysis of the qualitative data, comparing and matching different codes and attribute values; eg, delay in reaching care and parental education).

We report results in percentage and relative risk and provide confidence intervals. Statistical analysis was performed by using Microsoft Excel version 16.16.25.

A complete verbatim list of all narratives is provided as Supplemental Table 6. We include this to describe the coding decisions made and also wished to give voice to the families who had suffered a loss. Demographic characteristics of these infants are presented in Table 1. Slightly more infants were boys (54%), and most lived in households with other siblings (82%). All lived with their biological mother; a quarter of fathers did not live in the home. Educational attainment for both parents was low and rarely extended beyond secondary school. Although the median age at infant death was 60 days, deaths were heavily concentrated among infants aged 28 days or younger.

TABLE 1

Demographic Characteristics of Infants and Their Caregivers

CharacteristicN = 230
Age at death, d, median 60 
 <1 mo, % 33.3 
 1–2 mo, % 16.7 
 2–3 mo, % 14.0 
 3–4 mo, % 13.2 
 4–5 mo, % 10.1 
 5–6 mo, % 11.4 
 >6 mo,a1.3 
Infant sex, %  
 Male 54.8 
 Female 45.2 
Domestic composition, n (%)  
 Has siblings 187 (81.3) 
 Father lives in home 171 (74.3) 
 Mother lives in home 230 (100) 
Father’s education, n (%)  
 None 5 (2.2) 
 Some primary or completed primary 42 (18.3) 
 Some secondary or completed secondary 128 (55.7) 
 Some postsecondary or completed postsecondary 11 (4.8) 
 Unknown 44 (19.1) 
Mother’s education, n (%)  
 None 10 (4.3) 
 Some primary or completed primary 94 (40.9) 
 Some secondary or completed secondary 111 (48.3) 
 Some postsecondary or completed postsecondary 5 (2.2) 
 Unknown 10 (4.3) 
CharacteristicN = 230
Age at death, d, median 60 
 <1 mo, % 33.3 
 1–2 mo, % 16.7 
 2–3 mo, % 14.0 
 3–4 mo, % 13.2 
 4–5 mo, % 10.1 
 5–6 mo, % 11.4 
 >6 mo,a1.3 
Infant sex, %  
 Male 54.8 
 Female 45.2 
Domestic composition, n (%)  
 Has siblings 187 (81.3) 
 Father lives in home 171 (74.3) 
 Mother lives in home 230 (100) 
Father’s education, n (%)  
 None 5 (2.2) 
 Some primary or completed primary 42 (18.3) 
 Some secondary or completed secondary 128 (55.7) 
 Some postsecondary or completed postsecondary 11 (4.8) 
 Unknown 44 (19.1) 
Mother’s education, n (%)  
 None 10 (4.3) 
 Some primary or completed primary 94 (40.9) 
 Some secondary or completed secondary 111 (48.3) 
 Some postsecondary or completed postsecondary 5 (2.2) 
 Unknown 10 (4.3) 
a

A few infants were enrolled whose ages exceeded the 6-mo limit by several days.

Overall, some form of delay in care was noted for 82.8% of deceased infants. The proportions of each of the 3 delays identified are shown in Table 2, together with other themes identified in the narratives. By contrast, delays in care were not identified for the remaining 18.2%. Among this latter group, most appeared to be cases of sudden unexplained infant death (SUID). By extension, the majority of deaths (88.7%) were among infants whose parents had noted the onset of symptoms.

TABLE 2

Number of Narratives Assigned to Each Code

Characteristics and Delays in Pathway to CareInfants n (%)
Comorbidities and/or history of birth complication 48 (20.8) 
Symptomatic death 204 (88.7) 
Asymptomatic death, apparent SUID 26 (11.3) 
3 delays  
 Delay 1: decision to seek care 126 (54.8) 
 Delay 2: reaching care 5 (2.2) 
 Delay 3: receiving adequate care 57 (24.7) 
No delay, includes SUIDs and cases in which no delay was identified 42 (18.2) 
Location of death  
 At home 112 (48.2) 
 En route 64 (32.2) 
 At the clinic, in line 16 (6.9) 
 At the clinic, under care 20 (8.7) 
 Referred to UTH and died en route or before receiving care 14 (6) 
 Location unspecified 4 (1.7) 
Danger signs mentioned in narratives  
 Fever 108 (47) 
 Convulsions, fits, seizures 9 (3.9) 
 Excessive crying, irritability 47 (20.4) 
 Respiratory distress 91 (39.6) 
 Diarrhea 19 (8.3) 
 Vomiting 17 (7.4) 
 Difficulty feeding or refusing feeding 65 (28.3) 
Infant seen by a provider shortly before death 85 (37) 
Family expresses uncertainty regarding cause of death 13 (5.6) 
Characteristics and Delays in Pathway to CareInfants n (%)
Comorbidities and/or history of birth complication 48 (20.8) 
Symptomatic death 204 (88.7) 
Asymptomatic death, apparent SUID 26 (11.3) 
3 delays  
 Delay 1: decision to seek care 126 (54.8) 
 Delay 2: reaching care 5 (2.2) 
 Delay 3: receiving adequate care 57 (24.7) 
No delay, includes SUIDs and cases in which no delay was identified 42 (18.2) 
Location of death  
 At home 112 (48.2) 
 En route 64 (32.2) 
 At the clinic, in line 16 (6.9) 
 At the clinic, under care 20 (8.7) 
 Referred to UTH and died en route or before receiving care 14 (6) 
 Location unspecified 4 (1.7) 
Danger signs mentioned in narratives  
 Fever 108 (47) 
 Convulsions, fits, seizures 9 (3.9) 
 Excessive crying, irritability 47 (20.4) 
 Respiratory distress 91 (39.6) 
 Diarrhea 19 (8.3) 
 Vomiting 17 (7.4) 
 Difficulty feeding or refusing feeding 65 (28.3) 
Infant seen by a provider shortly before death 85 (37) 
Family expresses uncertainty regarding cause of death 13 (5.6) 

SUID is defined here as death occurring in absence of any previous disease symptoms.

The location of the infant’s death was noted for 218 of 230 deaths (92%). Deaths occurred at home in 112 (48.7%) cases, en route or on arrival to a health care facility in 64 (27.8%), and at a health care facility in 36 (15.6%).

The most-common delay in this cohort was in the decision to seek care. This was identified in 126 (54.8%) deaths. Of these, 115 (91.3%) infants had exhibited danger signs (Fig 1), such as excessive crying, high fevers, and refusal to feed. In 24.6% (31 of 126) of cases in which there was a delay in seeking care, the symptoms reportedly worsened during the night, and the family waited until morning to take the infant to clinic. Delays in the family’s decision to seek care were more common in neonates (64%, 48 of 75) compared with older infants (50.3%, 78 of 155), relative risk = 1.3, (95% confidence interval: 1.0–1.6). Among neonates, 51 (66.2%) displayed danger signs, and 38 (49.4%) had fever, with or without other symptoms. The delay had no apparent relationship with infant’s sex or parental education. A representative summary of narratives with delays in seeking care is shown in Table 3.

TABLE 3

Representative Narratives Documenting Delays in Seeking Care

NarrativeAge at Death, d
1. According to the father, "as from yesterday the baby was just fine, active and feeding well, until today around 10:00 h, the baby started crying nonstop until it became very weak. We went to consult the elders to come and help us.a When they arrived, they looked at the baby and said the baby was already dead; we didn’t even have the time to go to the clinic."a 
2. Informant: the grandmother. "This baby was born with a swelling at the back. This was in Katete [a neighborhood clinic in Lusaka], so they were referred to UTH for further management. Arrived on Wednesday at UTH; after the doctor’s assessment, the baby was discharged and scheduled to come back on Monday for surgical intervention. Then just yesterday, the baby’s condition changed; started having difficulties in breathing, grunting-like breathing, and the temperature was high.a So, this morning we decided to bring back the baby to UTH. Unfortunately, the baby died on the way, so we just went straight to the police."a 
3. "The baby was just ok except for some fever, which was not serious.a After midnigh,t we only observed some white stuff coming through the nose and the baby was not breathing. Took her to the clinic only to be told the child was dead, go to the police." 11 
4. Informant: the father. "The baby was only sick for 2 days and only suffered from flu, it was sneezing, coughing, and a bit of fever. Now in the morning of 4/3/1, the baby started having difficulty in breathing.a It sounded like there was a blockage and eventually stopped breathing at the time we rushed to the clinic. The doctor only confirmed that the baby was dead." 12 
5. Informant: the grandmother. "According to the mother, the baby has been sick for 1 week but not very sure of the problem, just said abdominal discomfort.a I [the grandmother] always visited them and did not notice any problem, but this morning when I went to visit, I asked the mother to give me the baby. When she brought the baby, I noticed the baby was motionless not making any movements. When I checked the chest, the baby was not breathing. We rushed to the clinic. When the doctor looked at the baby, he just said this baby died a long time ago. So, we went to the police." 16 
6. Informant: the grandfather. "The child was with mother in Lusaka West [a health center in Lusaka]. She told us that the baby started coughing 6 days ago; it was taken to the clinic where they were given a prescription to buy the medicine. But then 2 days ago, the cough got worse. The baby was even failing to breastfeed; that was when they rushed to our place so that we could help with the money to buy medicine.a As we were planning to go to the clinic, the baby died and we went to the police." 50 
7. "The baby got sick 3 days ago; it was just coughing but the coughing was not that bad.a Yesterday, we observed the baby was not feeding that much.a In the night, it stopped feeding completely, so this morning, we thought of taking the baby to the clinic. Unfortunately, it died on the way." 60 
8. "The baby has been suffering from chest pains and coughing for 2 weeks now. Earlier we took the baby to Kanyama Clinic [a level 1 hospital in Lusaka] and was admitted for 2 days. Then we were discharged, stayed home for few days. Just yesterday the baby started breathing fast again and the coughing worsened; today we decided to take the baby to the clinic.a Just upon arrival, we were told the baby is dead." 93 
9. "The baby developed a cough yesterday in the morning but it wasn’t that serious.a In the evening, it just became dull [the baby’s behavior], not as active as usual. In the evening, it started crying nonstop and it cried all night. In the morning today, the mother decided to take the baby to the clinic, but she passed through her mother’s place who first decided to start with going for prayers then proceeded to the clinic.a At the clinic while the baby was being attended to, it passed on. We were told that we had brought the baby late to the clinic. So, we went to the police to report." 162 
10. "The baby was sick for 7 days; it was coughing nonstop but the problem was that the mother also got very sick so there was no one to take care of the baby properly.a Then, 2 days ago, the baby’s condition worsened, started having difficulties in breathing, so were planning to take the baby to the clinic with the mother, but the baby died in the night. The mother’s condition is not very well." 175 
NarrativeAge at Death, d
1. According to the father, "as from yesterday the baby was just fine, active and feeding well, until today around 10:00 h, the baby started crying nonstop until it became very weak. We went to consult the elders to come and help us.a When they arrived, they looked at the baby and said the baby was already dead; we didn’t even have the time to go to the clinic."a 
2. Informant: the grandmother. "This baby was born with a swelling at the back. This was in Katete [a neighborhood clinic in Lusaka], so they were referred to UTH for further management. Arrived on Wednesday at UTH; after the doctor’s assessment, the baby was discharged and scheduled to come back on Monday for surgical intervention. Then just yesterday, the baby’s condition changed; started having difficulties in breathing, grunting-like breathing, and the temperature was high.a So, this morning we decided to bring back the baby to UTH. Unfortunately, the baby died on the way, so we just went straight to the police."a 
3. "The baby was just ok except for some fever, which was not serious.a After midnigh,t we only observed some white stuff coming through the nose and the baby was not breathing. Took her to the clinic only to be told the child was dead, go to the police." 11 
4. Informant: the father. "The baby was only sick for 2 days and only suffered from flu, it was sneezing, coughing, and a bit of fever. Now in the morning of 4/3/1, the baby started having difficulty in breathing.a It sounded like there was a blockage and eventually stopped breathing at the time we rushed to the clinic. The doctor only confirmed that the baby was dead." 12 
5. Informant: the grandmother. "According to the mother, the baby has been sick for 1 week but not very sure of the problem, just said abdominal discomfort.a I [the grandmother] always visited them and did not notice any problem, but this morning when I went to visit, I asked the mother to give me the baby. When she brought the baby, I noticed the baby was motionless not making any movements. When I checked the chest, the baby was not breathing. We rushed to the clinic. When the doctor looked at the baby, he just said this baby died a long time ago. So, we went to the police." 16 
6. Informant: the grandfather. "The child was with mother in Lusaka West [a health center in Lusaka]. She told us that the baby started coughing 6 days ago; it was taken to the clinic where they were given a prescription to buy the medicine. But then 2 days ago, the cough got worse. The baby was even failing to breastfeed; that was when they rushed to our place so that we could help with the money to buy medicine.a As we were planning to go to the clinic, the baby died and we went to the police." 50 
7. "The baby got sick 3 days ago; it was just coughing but the coughing was not that bad.a Yesterday, we observed the baby was not feeding that much.a In the night, it stopped feeding completely, so this morning, we thought of taking the baby to the clinic. Unfortunately, it died on the way." 60 
8. "The baby has been suffering from chest pains and coughing for 2 weeks now. Earlier we took the baby to Kanyama Clinic [a level 1 hospital in Lusaka] and was admitted for 2 days. Then we were discharged, stayed home for few days. Just yesterday the baby started breathing fast again and the coughing worsened; today we decided to take the baby to the clinic.a Just upon arrival, we were told the baby is dead." 93 
9. "The baby developed a cough yesterday in the morning but it wasn’t that serious.a In the evening, it just became dull [the baby’s behavior], not as active as usual. In the evening, it started crying nonstop and it cried all night. In the morning today, the mother decided to take the baby to the clinic, but she passed through her mother’s place who first decided to start with going for prayers then proceeded to the clinic.a At the clinic while the baby was being attended to, it passed on. We were told that we had brought the baby late to the clinic. So, we went to the police to report." 162 
10. "The baby was sick for 7 days; it was coughing nonstop but the problem was that the mother also got very sick so there was no one to take care of the baby properly.a Then, 2 days ago, the baby’s condition worsened, started having difficulties in breathing, so were planning to take the baby to the clinic with the mother, but the baby died in the night. The mother’s condition is not very well." 175 

Narratives have been slightly edited to insert punctuation and correct spelling, with clarifying comments added in brackets as needed. UTH is Lusaka’s tertiary referral center.

a

Passages linked to the delay in question.

Delays in reaching care, defined as the family specifically mentioning difficulty finding transportation, was the least common of the 3 delays, occurring in only 5 (2.2%) cases. A summary of these narratives is provided in Table 4.

TABLE 4

Representative Narratives Suggesting Transport-Related Delays in Reaching Care

NarrativeAge at Death, d
1. The father to the deceased stated that, “the baby fell ill on Saturday 14-04-18. The baby developed fever and dry cough, was taken to Chipata Clinic where was treated as an outpatient. The father does not know the medicines they were given at the clinic. The fever and dry cough persisted despite taking medication. Early hours of Tuesday 17-04-18, the baby started coughing a lot, such that became weak and developed fast difficult breathing. While we were arranging for transporta to take the baby to the clinic, the condition deteriorated and passed on.” 47 
2. "The baby fell ill on Monday 06-08-18, developed a dry cough and poor breastfeeding. The mother continued breastfeeding with difficulties. Vomited each time she coughed for 2 days. Tuesday 07-08-18 in the night, the baby developed severe cough, fast difficult breathing. Early hours of today [Wednesday], the baby became very weak with shallow respiration. The father went to look for transport to take the baby to the clinic,a by the time he came back home with transport, he was informed that the baby collapsed around 07:00 h. We took the baby to Kanyama Clinic where we were told the baby was already dead and went to obtain a police report at Los Angeles Police Post then proceeded here to the UTH morgue." 83 
3. "The uncle to the deceased stated that the baby fell sick 3 days ago. Developed fever and cough. Was taken to George Clinic was treated as an outpatient. Does not know the names of medicines given to them. Wednesday 30/05/18, late in the evening, the cough became severe such that [the baby] developed fast grunting breathing and very hot body. We gave the medicines we were given at the clinic but the breathing became difficulty. Early hours of 31/05/18, we decided to take the baby back to the clinic, however as we were arranging for transport,a the baby stopped breathing. We took the body to George Police who told us that the baby was already dead at 03:00 h of 31/05/18. We took the baby to UTH morgue." 92 
4. "The baby has been unwell for close to almost a month. We have been taking the baby to George Clinic. Baby has been having diarrhea on and off and coughing. The last time we took the baby to the clinic, we were given amoxicillin and Panadol [acetaminophen], so yesterday we observed the baby was having difficulties in breathing, it was grunting-like. We took the baby back to the clinic. We were told to go back home and complete the course of medicines we were given earlier.a Then in the night the condition worsened. Before we could find the transport,a the baby died then in the morning. We went to the police." 97 
5. "The baby was very fine when we went to bed to sleep. Around early hours of today 22-06-18, the baby suddenly woke up crying terrified gazing here and there. The crying became worse such that we decided to take him to the clinic. We went to look for transport and as we came with transport, only to be told by the mother that the baby suddenly stopped breathing.a We rushed the baby to the clinic were the doctor, after examining the baby, informed us that the baby was dead. We took the body to UTH Police where we obtained a police report, then proceeded to the morgue where the doctor certified the baby dead at 05:00 h of 22-06-18. Cause of death: sudden death." 129 
NarrativeAge at Death, d
1. The father to the deceased stated that, “the baby fell ill on Saturday 14-04-18. The baby developed fever and dry cough, was taken to Chipata Clinic where was treated as an outpatient. The father does not know the medicines they were given at the clinic. The fever and dry cough persisted despite taking medication. Early hours of Tuesday 17-04-18, the baby started coughing a lot, such that became weak and developed fast difficult breathing. While we were arranging for transporta to take the baby to the clinic, the condition deteriorated and passed on.” 47 
2. "The baby fell ill on Monday 06-08-18, developed a dry cough and poor breastfeeding. The mother continued breastfeeding with difficulties. Vomited each time she coughed for 2 days. Tuesday 07-08-18 in the night, the baby developed severe cough, fast difficult breathing. Early hours of today [Wednesday], the baby became very weak with shallow respiration. The father went to look for transport to take the baby to the clinic,a by the time he came back home with transport, he was informed that the baby collapsed around 07:00 h. We took the baby to Kanyama Clinic where we were told the baby was already dead and went to obtain a police report at Los Angeles Police Post then proceeded here to the UTH morgue." 83 
3. "The uncle to the deceased stated that the baby fell sick 3 days ago. Developed fever and cough. Was taken to George Clinic was treated as an outpatient. Does not know the names of medicines given to them. Wednesday 30/05/18, late in the evening, the cough became severe such that [the baby] developed fast grunting breathing and very hot body. We gave the medicines we were given at the clinic but the breathing became difficulty. Early hours of 31/05/18, we decided to take the baby back to the clinic, however as we were arranging for transport,a the baby stopped breathing. We took the body to George Police who told us that the baby was already dead at 03:00 h of 31/05/18. We took the baby to UTH morgue." 92 
4. "The baby has been unwell for close to almost a month. We have been taking the baby to George Clinic. Baby has been having diarrhea on and off and coughing. The last time we took the baby to the clinic, we were given amoxicillin and Panadol [acetaminophen], so yesterday we observed the baby was having difficulties in breathing, it was grunting-like. We took the baby back to the clinic. We were told to go back home and complete the course of medicines we were given earlier.a Then in the night the condition worsened. Before we could find the transport,a the baby died then in the morning. We went to the police." 97 
5. "The baby was very fine when we went to bed to sleep. Around early hours of today 22-06-18, the baby suddenly woke up crying terrified gazing here and there. The crying became worse such that we decided to take him to the clinic. We went to look for transport and as we came with transport, only to be told by the mother that the baby suddenly stopped breathing.a We rushed the baby to the clinic were the doctor, after examining the baby, informed us that the baby was dead. We took the body to UTH Police where we obtained a police report, then proceeded to the morgue where the doctor certified the baby dead at 05:00 h of 22-06-18. Cause of death: sudden death." 129 

Narratives have been slightly edited to insert punctuation and correct spelling, with clarifying comments added in brackets as needed. UTH is Lusaka’s tertiary referral center.

a

Passages linked to the delay in question.

We found that 57 (24.7%) infants had delays in receiving adequate care. These include 16 (28%) infants who died while waiting in line, 20 (35%) who died in clinic while being attended to, and 14 (24.6%) who were seen in a peripheral clinic and referred to UTH but died en route. A representative summary of narratives with delay in receiving adequate care is shown in Table 5.

TABLE 5

Representative Narratives Documenting Delays in Adequate Care at Medical Facilities

NarrativeAge at Death, d
1. "The baby was just fine until the 18th of October when the baby developed some fever and later developed a distended abdomen; we rushed the baby to Kanyama Clinic. From there we were referred to UTH. The baby died on the way before reaching the hospital.a It was so sudden we don’t even know what killed the baby." 
2. Report given by the grandmother. "The baby was born prematurely and for this reason it was admitted in NICU for observations. After 5 days it was discharged. At home, it was active and feeding well by cup as per doctor’s instructions. Now just this morning, we observed that the baby was not breathing well; it would stop then start just like that, immediately we went to Chawama Clinic. As we were waiting to see the doctor, the condition got worse.a Then we were asked to go in.a The doctor just looked at the baby and told us it was already dead and that we should go to the police."a 10 
3. "The baby developed flulike symptoms on Tuesday and it was taken to Chawama level 1 hospital where it was given treatment (amoxicillin) and it was sent back home. Then Wednesday, the condition started getting worse (coughing, fever sneezing, and even failing to breath properly), so we decided to take the baby back to the hospital [Chawama]. At the hospital, we were still in the line when we noticed that the baby was not breathing.a Rushed to the nurses who actually confirmed our suspicion.a That is when we went to the police to report. We feel there was some negligence because the first-time we took the baby to the clinic they could have admitted the baby for treatment."a 25 
4. "The baby got sick on Friday. It started with flulike symptoms, sneezing, coughing and some fever. On Saturday, we took the baby to the clinic where we were given treatment and sent back home. But the Sunday the coughing got worse. The baby lost the voice and started laboring when breathing. Early hours of Monday we decided to take the baby back to the clinic. While on the line the nurse checked the temperature, she told us the temperature was just fine.a We should wait for the doctor in the line.a When we finally went in to see the doctor on examination, he told us the baby was already dead.a We got confused because it was not long from the time the nurse had looked at the baby. That’s how we went to the police." 35 
5. "The aunt stated that the baby was well all along. Yesterday [12/02/2018], was observed crying, but breastfeeding. The crying became worse after receiving vaccinations at Mtendere Clinic. This morning [13/02/2018], the baby developed severe hotness of the body. We took the baby to Mtendere Clinic, unfortunately passed on few minutes after being seen by the doctor around 08:00 h.a We then brought the body to UTH where was certified dead by the doctor at 12:00 h." 43 
6. The father said that, "the baby started crying on 24th October in the night. We were wondering why he was crying a lot because there were no signs of being sick. The body temperature was normal. On 25th October we took the baby to Matero level 1 hospital for medical attention. After the doctor saw the baby, he told us that the baby was very sick and referred us to UTH for complicated management.a But before the baby was seen at UTH, he died in the emergency department.a We were then asked to go to UTH Police for certification of death." 109 
7. The grandfather stated that, "the baby fell ill on 23/11/17 in the morning. The body became very hot and started vomiting. In the night of 23/11/17, developed diarrhea and vomited a lot. Had diarrhea ∼5 times and difficulty fast breathing with some neck stiffness.a This morning 24/11/17, took the baby to Chawama Clinic where he passed on while on the queuea to see the doctor." 109 
8. The aunt to the deceased stated that, "the baby fell ill a month ago; developed constipation and severe abdominal pains. We took the baby to a local village clinic where [it] received treatment. Despite having received treatment, the illness persisted such that [the baby] developed fever, difficulty breathing and sunken fontanel [grief counselor is paraphrasing]. The baby was taken to Kanyama Clinic where was treated as an outpatient.a On Monday 09-04-18, early hours of the morning, the baby was observed to have developed a dry cough, followed by fast difficult grunting respirations. We took the baby to Kanyama Clinic again, where we joined the queue to see the doctor.a We were on the que from 04 hours up until around 07:00 h, when the baby stopped breathing while in our hands.a The baby was taken to the emergency department where after being examined by the doctor, we were informed that the baby was dead. The baby maybe could have survived had the doctor attended to her early." 149 
9. "The baby was just fine until Sunday when he developed a high body temperature and started crying excessively and later developed blisters on both feet. Took the baby to the clinic and he was given some injections and Calpol syrup [acetaminophen] and sent back home. Despite all that, the temperature was not coming down. Yesterday in the night he started fitting [seizures or spasms]. So, this morning we took back the baby to the clinic; he was attended to and admitted. Now in the process of trying to find the vein, he started fitting again and he did not recover from that though the doctor really tried to resuscitate the baby.a That is how he died and we were told since we did not stay even 2 hours in hospital, we must go to the police and report the death." 163 
10. Informant: the uncle in the presence of the father to the child. "The baby started vomiting in the morning yesterday with no other symptoms, it vomited a lot until the mother decided to rush to the clinic where he was attended to and was given in injection to stop the vomiting.a And they were sent back home.a In the night, that was when it developed a fever, though the vomiting had reduced, the baby looked weak. So, in the morning we decided to go back to the clinic.a The mother was in the line for a long time and the baby’s condition was deteriorating. At the time they went in to see the doctor, the baby had collapsed and the doctor confirmeda [that the baby was dead] and said they can’t administer any medications, only asked us to go to the police." 173 
NarrativeAge at Death, d
1. "The baby was just fine until the 18th of October when the baby developed some fever and later developed a distended abdomen; we rushed the baby to Kanyama Clinic. From there we were referred to UTH. The baby died on the way before reaching the hospital.a It was so sudden we don’t even know what killed the baby." 
2. Report given by the grandmother. "The baby was born prematurely and for this reason it was admitted in NICU for observations. After 5 days it was discharged. At home, it was active and feeding well by cup as per doctor’s instructions. Now just this morning, we observed that the baby was not breathing well; it would stop then start just like that, immediately we went to Chawama Clinic. As we were waiting to see the doctor, the condition got worse.a Then we were asked to go in.a The doctor just looked at the baby and told us it was already dead and that we should go to the police."a 10 
3. "The baby developed flulike symptoms on Tuesday and it was taken to Chawama level 1 hospital where it was given treatment (amoxicillin) and it was sent back home. Then Wednesday, the condition started getting worse (coughing, fever sneezing, and even failing to breath properly), so we decided to take the baby back to the hospital [Chawama]. At the hospital, we were still in the line when we noticed that the baby was not breathing.a Rushed to the nurses who actually confirmed our suspicion.a That is when we went to the police to report. We feel there was some negligence because the first-time we took the baby to the clinic they could have admitted the baby for treatment."a 25 
4. "The baby got sick on Friday. It started with flulike symptoms, sneezing, coughing and some fever. On Saturday, we took the baby to the clinic where we were given treatment and sent back home. But the Sunday the coughing got worse. The baby lost the voice and started laboring when breathing. Early hours of Monday we decided to take the baby back to the clinic. While on the line the nurse checked the temperature, she told us the temperature was just fine.a We should wait for the doctor in the line.a When we finally went in to see the doctor on examination, he told us the baby was already dead.a We got confused because it was not long from the time the nurse had looked at the baby. That’s how we went to the police." 35 
5. "The aunt stated that the baby was well all along. Yesterday [12/02/2018], was observed crying, but breastfeeding. The crying became worse after receiving vaccinations at Mtendere Clinic. This morning [13/02/2018], the baby developed severe hotness of the body. We took the baby to Mtendere Clinic, unfortunately passed on few minutes after being seen by the doctor around 08:00 h.a We then brought the body to UTH where was certified dead by the doctor at 12:00 h." 43 
6. The father said that, "the baby started crying on 24th October in the night. We were wondering why he was crying a lot because there were no signs of being sick. The body temperature was normal. On 25th October we took the baby to Matero level 1 hospital for medical attention. After the doctor saw the baby, he told us that the baby was very sick and referred us to UTH for complicated management.a But before the baby was seen at UTH, he died in the emergency department.a We were then asked to go to UTH Police for certification of death." 109 
7. The grandfather stated that, "the baby fell ill on 23/11/17 in the morning. The body became very hot and started vomiting. In the night of 23/11/17, developed diarrhea and vomited a lot. Had diarrhea ∼5 times and difficulty fast breathing with some neck stiffness.a This morning 24/11/17, took the baby to Chawama Clinic where he passed on while on the queuea to see the doctor." 109 
8. The aunt to the deceased stated that, "the baby fell ill a month ago; developed constipation and severe abdominal pains. We took the baby to a local village clinic where [it] received treatment. Despite having received treatment, the illness persisted such that [the baby] developed fever, difficulty breathing and sunken fontanel [grief counselor is paraphrasing]. The baby was taken to Kanyama Clinic where was treated as an outpatient.a On Monday 09-04-18, early hours of the morning, the baby was observed to have developed a dry cough, followed by fast difficult grunting respirations. We took the baby to Kanyama Clinic again, where we joined the queue to see the doctor.a We were on the que from 04 hours up until around 07:00 h, when the baby stopped breathing while in our hands.a The baby was taken to the emergency department where after being examined by the doctor, we were informed that the baby was dead. The baby maybe could have survived had the doctor attended to her early." 149 
9. "The baby was just fine until Sunday when he developed a high body temperature and started crying excessively and later developed blisters on both feet. Took the baby to the clinic and he was given some injections and Calpol syrup [acetaminophen] and sent back home. Despite all that, the temperature was not coming down. Yesterday in the night he started fitting [seizures or spasms]. So, this morning we took back the baby to the clinic; he was attended to and admitted. Now in the process of trying to find the vein, he started fitting again and he did not recover from that though the doctor really tried to resuscitate the baby.a That is how he died and we were told since we did not stay even 2 hours in hospital, we must go to the police and report the death." 163 
10. Informant: the uncle in the presence of the father to the child. "The baby started vomiting in the morning yesterday with no other symptoms, it vomited a lot until the mother decided to rush to the clinic where he was attended to and was given in injection to stop the vomiting.a And they were sent back home.a In the night, that was when it developed a fever, though the vomiting had reduced, the baby looked weak. So, in the morning we decided to go back to the clinic.a The mother was in the line for a long time and the baby’s condition was deteriorating. At the time they went in to see the doctor, the baby had collapsed and the doctor confirmeda [that the baby was dead] and said they can’t administer any medications, only asked us to go to the police." 173 

Narratives have been slightly edited to insert punctuation and correct spelling, with clarifying comments added in [brackets] as needed. UTH is Lusaka’s tertiary referral center.

a

Passages linked to the delay in question.

Before their death, 85 infants (37%) were evaluated by a clinician and sent home. Of these, 34 infants (40%) had a delay in the family’s decision to reseek care subsequently, and 38 (44.7%) were determined to have a delay in receiving subsequent adequate care.

In 9% of infants, >1 delay was identified, most commonly a combination of delays in seeking care and delays in receiving adequate care, but no infant had all 3 delays.

The analysis of narratives told by families of BID infants in Lusaka, Zambia identified common delays in health-seeking behaviors and provision of care that contributed to these infants’ deaths. More than half of the families had delays in seeking care, with many of them having waited until morning when symptoms were noted at night. The most vulnerable were the neonates, with the highest death rate, and for whom delays in seeking care were most prevalent. We assume delays in reaching care were likely a significant factor considering the majority of infants died en route to a health care facility, although only a small number of families specifically mentioned this delay. Among infants who managed to arrive to a health care facility, some died while waiting in line, and others while being transported to a higher-level facility.

With our analysis, we suggest that delays in receiving acute care are a significant factor contributing to infant mortality. Significantly, >80% of all community infant deaths involved some form of delay. Although it is impossible to know what would have occurred in the absence of such delays, the majority of infant deaths in Lusaka are from causes for which effective treatments currently exist,1  including oral rehydration solutions for diarrhea and supplemental oxygen and/or antibiotics for pneumonia or sepsis.11,12  In other words, in many cases infants are dying because they do not receive existing treatments at all or receive them only after the illness has become unsalvageable. If our goal is to reduce child mortality, these findings have profound implications.

The traditional role of the VA is to ascribe an etiologic cause of death in situations in which a traditional autopsy cannot be conducted.13  The free-text narratives provided a glimpse into the sequence of events and decisions in the final days leading to each child’s death. Without discounting the evident value in knowing etiologies, the social factors that contributed to death may be as important and determinative in the outcome of a given illness.

We feel it important to emphasize that delays in seeking care are likely complex and multifactorial and do not necessarily imply negligence by the child’s caregivers. Logistic barriers may be insurmountable, particularly in deeply impoverished, underresourced communities, such as typified among the urban poor in Lusaka. The simplicity of the 3-delay model was helpful in framing the circumstances contributing to infant deaths, although many cases had multiple potential contributing forces, emphasizing the complexity of this issue.

The location of the infant’s death provides important clues to how we interpret deaths. For example, it is likely that infants that died at home had a high proportion of delays in seeking care. Notably, approximately a third of infants died en route. Such events may identify families who experienced difficulties securing safe, affordable, and timely transportation, even if the family did not specifically mention difficulty with transportation in the narrative. The informal public transportation in Lusaka is neither regular nor reliable and does not operate overnight. Fear of criminal activity and lack of street lighting make travel on foot undesirable.

A delay in the family’s decision to seek care was seen in the majority of infants with danger signs. It might be that the family failed to recognize urgency or severity of symptoms the infant displayed. This is even more challenging when it comes to neonates, who may display limited signs of distress and may deteriorate and succumb to their illness rapidly. That is why even when fever is the only symptom, neonates should be evaluated urgently. Neonates accounted for the largest age group in our cohort and had the highest rates of delays in seeking care. This is consistent with other reports in the literature and is probably why this population is by far the most studied in relation to delays in care.57,1418  Interventions targeting this age group could potentially have the highest impact.

More than a third of infants had been previously evaluated by a trained clinician, sent home, and then died shortly after. Without documentation of the visit, and relying merely on the families’ descriptions, we cannot know whether these infants died from errors in clinical management or if they were appropriately managed at the time but their condition later deteriorated. Nearly 40% of these infants had a subsequent delay in the family’s decision to seek care when the infant’s condition persisted or worsened. An encounter with a clinician is an important opportunity for educating the family regarding signs and symptoms that should prompt seeking care without delay and for the clinician to assess the ability of the family to reach care if things got worse.

Although the consequences of each delay might eventually lead to the same sad outcome, the implications of each, and remedies, differ markedly. Delay in seeking care is a proxy for patterns in health-seeking. As such, remedies would center on counseling parents what to do when infant falls ill, what kind of problems can wait until morning, and what constitutes an urgency or an emergency. By contrast, deaths due to delays at health care centers focus our attention on resource allocation within facilities and whether robust systems exist for triage or expedited referrals to higher levels of care.

Twenty-six infants (11.3%) were found dead in bed with no apparent preceding illness and were categorized as SUIDs. SUIDs include all causes of unexpected infant deaths, one of which is sudden infant death syndrome (SIDS).19  Such deaths are notable given how little SIDS deaths have been described in LMICs.20  In our view, this is an area that merits closer attention, particularly as low-cost, low-complexity strategies for preventing SIDS that were proven effective in high-income countries (ie, putting infants to sleep on their backs)21,22  could be feasible, effective and affordable in LMICs.

Analysis of these free-text narratives revealed how complex decision-making within families forced some subjectivity into how we interpreted specific events. For example, cases in which the family waited until morning to seek care suggested a delay in seeking care. But their decision could have reflected the distance to the nearest health care facility (delay in receiving adequate care) or the challenges finding safe transportation overnight (a delay in reaching care), and perhaps a combination of all 3. Simply identifying a “delay in seeking care” overlooks important contributing factors.

We hypothesize Lusaka is typical of other cities in Africa, and therefore the results of this analysis are likely relevant to other sites. However, more studies are needed to identify common delays in different populations.

Our study has several limitations. This was a retrospective analysis of narratives collected through an epidemiological study. Given the design of ZPRIME, we could not conduct a formal social autopsy, an in-depth analysis that takes weeks to implement.10,23  By comparison, our data were collected from the caregivers within a median of 15 hours of the infants’ deaths, while memories of events were still fresh. Second, the narratives were limited to information provided by caregivers, unprompted by specific questioning to identify delays. But, this is also the strength of our data, because the information reflects factors that the family perceived as salient and therefore decided to include in their story.

Finally, we acknowledge that in some cases the information provided in the narrative may have omitted important details; therefore, we were conservative and did not assume there was a delay if it was not clear from the narrative. Consequently, our conclusions are likely an underestimate of the real burden these delays play in the outcome of events.

The stories told by families of BID infants revealed tragic circumstances that contributed to a high rate of infant community deaths. From these stories arise a common narrative of possibly preventable deaths.

Interventions to reduce infant mortality rates in LMICs are, in many cases, high-tech and costly, take years to achieve and develop, and pose regulatory and logistic challenges. One example of such intervention is the development of a respiratory syncytial virus vaccine, in support of which the ZPRIME study was initiated. With our current analysis, we suggest that there are relatively simple interventions that are low-tech and could be achieved at low cost and in a timely manner. Effort and focus on high-tech interventions should not preclude development of simple low-tech interventions under local leadership.

We thank our colleagues at the Bill & Melinda Gates Foundation, and particularly our program officer Ms Prachi Vora, whose enthusiasm for this project gave us the strength to keep pursuing this difficult topic. We also thank Dr Lapidot’s extended mentorship team in the section of pediatric infectious diseases: Drs Stephen Pelton and Elizabeth Barnett. We offer deep gratitude to our data collection team members, whose work with the families collecting these narratives required a level of courage and stamina that is hard to imagine. Their work was emotionally wrenching, endlessly sad, and incredibly valuable. And most importantly, we thank the families of the deceased infants who were willing, under incredibly difficult circumstances, to share their stories. Despite the overwhelming grief at the loss of their children, their willingness to talk with us reflected their grace, patience, generosity, and humanity. Without them, this work would not have been possible.

Ms Lapidot led the development of the protocol and analysis plan, was one of the coders, and led the analysis of data and manuscript writing; Ms Larson Williams, Mr MecLeod, Ms Olowojesiku, and Mr Enslen participated in protocol and analysis plan, were coders, helped analyze the data, and participated in writing the manuscript; Ms Mwale led the data collecting team, helped with data collecting and analysis, and contributed to the final manuscript; Mr Mwananyanda led the field team, was the site principal investigator for Zambia Pertussis Respiratory Syncytial Virus Infant Mortality Estimation (ZPRIME), helped develop the protocol for ZPRIME (including the verbal autopsy data collection), helped analyze the data, and contributed to the final manuscript; Mr Munanjala, Mr Chimoga, and Mr Ngoma were members of the data collector team, helped with data analysis, and contributed to the final manuscript; Mr Thea was a coinvestigator on ZPRIME, helped with protocol and tool development and data analysis, and contributed to the final version of the manuscript; Mr Gill was the principal investigator for ZPRIME and was involved at all levels of this manuscript; and all authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

FUNDING: Funded by the Bill & Melinda Gates Foundation. The sponsors played no role in the development of this manuscript.

COMPANION PAPER: A companion to this article can be found online at www.pediatrics.org/cgi/doi/10.1542/peds.2020-044081.

     
  • BID

    brought in dead

  •  
  • LMIC

    low-middle-income country

  •  
  • SIDS

    sudden infant death syndrome

  •  
  • SUID

    sudden unexplained infant death

  •  
  • UTH

    University Teaching Hospital

  •  
  • VA

    verbal autopsy

  •  
  • ZPRIME

    Zambia Pertussis Respiratory Syncytial Virus Infant Mortality Estimation

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Competing Interests

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

Supplementary data