Childhood mortality and probable causes of death using verbal autopsy in Niakhar, Senegal, 1989–2000

Jean-François Etard1, Jean-Yves Le Hesran1, Aldiouma Diallo1, Jean-Pierre Diallo1, Jean-Louis Ndiaye1 and Valérie Delaunay2

1 Institut de Recherche pour le Développement (IRD) BP 1386 Dakar, Sénégal
2 Laboratoire Population-Environnement-Développement, UMR 151 IRD—Université, de Provence, Marseille, France

Correspondences: Jean-François Etard, IRD, BP 1386, CP 18524 Dakar, Senegal. E-mail: etard{at}mpl.ird.fr


    Abstract
 Top
 Abstract
 Population and Methods
 Results
 Discussion
 Conclusion
 References
 
Background In African rural settings, medically certified information on causes of death is largely lacking. The authors applied the verbal autopsy to identify causes of death before 15 years old in a rural area of Senegal where a demographic surveillance system is operating.

Methods Between 1989 and 2000, a postmortem interview was conducted using a standardized questionnaire which was independently reviewed by two physicians who assigned the probable underlying cause of death. Discordant diagnoses were discussed by a panel of physicians. Causes of death were grouped into a few categories; cause-specific mortality rates and fractions were generated.

Results Between 1989 and 1997, all-cause mortality fluctuated. Diarrhoeal diseases, malaria and acute respiratory infections explained between 30% and 70% of the mortality before 10 years of age. In children 1–9 years old, malaria death rate increased between 1989 and 1994 and thereafter did not change. The 1998–2000 years were marked by a peak in mortality, attributed to a meningitis outbreak in children more than one year old paralleled by an increase in death rate from fever of unknown origin, diarrhoeal diseases, and acute respiratory infections in children under 5 years.

Conclusions Verbal autopsy provided useful information on the mortality structure responsible for the 1998–2000 peak in mortality. It underlined that, outside outbreak situations, malaria was a leading cause of death for 1–9 year old children and that diarrhoea, acute respiratory infections, or fever from unknown origin accounted for up to 50% of the deaths among the children under 5 years.


Keywords Cause of death, infant, child, communicable diseases, preschool, rural population, Senegal

Accepted 14 May 2004

Medically certified information is not available for at least 70% of the worldwide deaths. In rural settings of developing African countries, vital registration infrastructure is poor, access to health centres with adequate diagnosis facilities limited and most childhood deaths occur at home. Reliable medical information on causes of death is therefore lacking and other sources of data must be used to estimate cause-specific mortality. Data from population monitoring laboratories conducting postmortem interviews with relatives of the deceased person to ascribe causes of death, so-called ‘verbal autopsies’, are one of the alternative sources.1–4 This method is most valid for diseases with well-defined symptoms recognizable by the local population, such as neonatal tetanus, measles, malnutrition and less so for diseases with shared symptoms, such as malaria and acute respiratory infections.5 Despite these limitations, its use within research settings and validation studies have been encouraged. In sub-Saharan Africa, verbal autopsy in childhood deaths has been applied in Kenya, Ethiopia, Congo, Tanzania, Liberia, The Gambia, and South Africa.6–12 In these settings only a few diseases account for most of the deaths and, for purpose of planning, it may be sufficient to identify major causes of death. In Senegal, it has been used in the two rural areas of Bandafassi (8000 inhabitants, 1984–1993) and Mlomp (6300 inhabitants, 1985–1989).13,14 The same approach has been used since 1983 in the rural study zone of Niakhar, but leading causes of death among under-5 children have only been briefly described for the period 1983–1986.15 We report here total and cause-specific death rates before 15 years of age for leading causes of death attributed by verbal autopsy and trends over a 12-year period, 1989–2000.


    Population and Methods
 Top
 Abstract
 Population and Methods
 Results
 Discussion
 Conclusion
 References
 
Study population and demographic surveillance system
Detailed descriptions of the study zone, the on-going demographic surveillance system (DSS), and long-term trends in child mortality over the period 1963–1999 have already been published (http://www.ird.sn/activites/niakhar/).16,17 Briefly, the study area located in the District of Fatick (Niakhar, N 14°30' W 16°30'), 135 km South-East of Dakar, includes 30 villages scattered over 230 km2. Population increased over the study period from about 25 000 residents in 1989 to 29 000 in 2000. Climate is typically sub-Sahelian (average temperature: 24°C–30°C; rainy season: July–October). Average annual precipitation decreased from more than 800 mm before 1960 to 418 mm for the period 1982–1989, and increased to 457 mm during the next decade, with large fluctuations between 323 mm and 646 mm, before reaching 562 mm in 2000–2001. Three health posts within the study area and two outside provide first-line health care services. Undernutrition is common: stunting and wasting reached 13.7% and 11.6% among those 9–10 months old.18 Vaccine coverage increased during the 1990s thanks to vaccine trials.19,20 DTP3 coverage exceeded 80% between 1991 and 1997 among those 6 months to one year old. Malaria transmission is mainly restricted to the months from August to October.21 After an initial survey in 1983, population census was updated on a yearly basis until 1987; from 1987 to 1997, weekly household visits and a bi-annual census were carried out; since March 1997, demographic data have been updated every quarter. Household visits were made in the local language by lay interviewers from the study zone and residents were interviewed for incident vital events and migrations since the preceding visit, limiting the recall period. A follow-up of the pregnancies improved registration of early deaths.

Assignment of probable cause of death by verbal autopsy procedure
A standardized questionnaire, initially developed at ICCDR-B in Bangladesh, was completed by a lay reporter in local language.22,23 The current version is a 15-page questionnaire available on the IRD website (http://www.ird.sn/activites/niakhar/). It comprised several parts: identification, use of health services preceding the fatal illness, open text and closed questions to record the actual history and the symptoms during the terminal illness, and summary sheets. Each questionnaire was reviewed independently by two clinicians who assigned the most likely cause of death based on their own medical judgement. Discordant diagnoses were discussed by the panel of clinicians involved in Niakhar and a consensus cause was searched. If a consensus was not reached, the death was categorized as ill-defined/unknown. Three-digit International Classification of Disease—Ninth Revision (ICD-9) codes were used. For general symptoms (code 780), the fourth digit was used. Based on the ICD-9 codes assigned, causes of deaths were aggregated into five broad categories, diarrhoeal diseases, acute respiratory infection (ARI), meningitis, malaria, fever of unknown origin (FUO), in addition to ill-defined/unknown causes and other causes (Table 1). During the 1980s and 1990s, measles and pertussis vaccine trials and adequate case management have led to a precise ascertainment of deaths due to these infections and a dramatic reduction in their incidence.19,20 The local epidemiological context (outbreaks, known seasonality in incidence) has been used as a piece of information. When an outbreak of cholera, meningitis, or shigellosis was notified after the bacteriological confirmation of the first cases, subsequent deaths matching the clinical case definition were attributed to the outbreak. In the case of an acute fever with convulsions or impaired consciousness, unphased seasonal incidences of malaria and epidemic meningococcal disease (humid season versus dry season) have been used to help in distinguishing between these two aetiologies. When the child had a history of fever and respiratory signs (cough, chest pain, expectoration, fast breathing) with no convulsions during the dry season, a death due to an acute respiratory infection (ARI) was accepted. When it was impossible to assign the underlying cause in front of a febrile illness with respiratory distress during the malaria season, the death was categorized as ‘fever from unknown origin’ (FUO). In developing countries, more than 50% of the deaths due to diarrhoea, ARI, malaria, and other infectious diseases are attributed to underweight.24 Rather than attempting to group deaths due to malnutrition into a ‘malnutrition’ category, we chose to classify these deaths into one of the five broad categories, depending on the terminal associated cause, or into the ‘other causes’ category when malnutrition was not followed by an infectious disease. The number of deaths due to measles was so low that measles death rates are not presented here but can be found elsewhere.19


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Table 1 Classification of causes of death used, Niakhar, rural Senegal, 1989–2000

 
Data analysis
Data on person-time exposed and risk of dying were provided by the DSS. All-causes and specific mortality rates were calculated for four age groups (<1 year, 1–4, 5–9, and 10–14 years) and four 3-year periods (1989–1991, 1992–1994, 1995–1997, 1998–2000). Neonatal mortality was expressed as the risk of dying before the 29th day per 1000 live births (lbirths). The trend in specific causes of death over time was expressed in proportion of total mortality rate (cause-specific mortality fraction, CSMF). CI around risk ratio (RR) and incidence rate ratios (IRR) used exact procedures.

The DSS design has been approved by Ministry of Health and Regional health authorities.


    Results
 Top
 Abstract
 Population and Methods
 Results
 Discussion
 Conclusion
 References
 
From 1989 to 2000, 159 016 person-years (p-y) and 3424 deaths were recorded before the age of 15. Only 31 deaths (0.9%) were not investigated due to refusal by the families. Until 1997, 75% of the verbal autopsy questionnaires were done within 2 weeks of death (median = 6 days, interquartile range = 10). Following the shift to a quarterly demographic surveillance in 1997, 75% of the interviews were conducted within two and a half months (median = 52 days, interquartile range = 57).

All-cause mortality
Neonatal mortality (0–28 days) declined over the study period from 40/1000 lbirths in 1989–1991 to 24/1000 lbirths in 1998–2000.

Infant mortality, 80/1000 lbirths on the average between 1989 and 1997, with a decreasing trend, increased abruptly in 1998 to 100/1000 lbirths (Figure 1).



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Figure 1 Trend in all-cause mortality per age, Niakhar, rural Senegal, 1989–2000

 
Between 1–4 years of age, the risk of dying fluctuated between 90 and 140/1000 before doubling in 1998.

In the older age groups (5–9, 10–14), mortality remained between 15 and 35/1000 before increasing abruptly in 1998.

The high level of mortality observed in 1998 started to decline in 1999.

Effect of gender on mortality
Over the study period, infant mortality among boys was larger than in girls (90 versus 75/1000 lbirths, RR = 1.19 [95% CI: 1.07, 1.33], P = 0.001). This effect was significant during the neonatal period (38 versus 28/1000 lbirths, RR = 1.36 [95% CI: 1.14, 1.63], P < 0.001) and the post-neonatal period (89 versus 75/1000 children alive at day-29, RR = 1.18 [95% CI: 1.06, 1.32], P < 0.01). No effect of gender in the other age groups/periods reached statistical significance.

Cause-specific mortality
Neonatal deaths (n =484)
More than 90% of these deaths were related to a cause different from the five broad categories with almost 60% linked to prematurity or perinatal infection.

Before one year old (n = 1200)
Since neonatal deaths accounted for 40.3% of these deaths, a large mortality fraction due to ‘other causes’ was observed. Over the whole study period, diarrhoeal diseases and ARI accounted for 30% of the infant mortality and malaria for 10%. In term of rates, compared with 1995–1997, an increase in mortality rate from FUO (IRR = 4.8; 95% CI: 2.4, 10.6), diarrhoeal disease (IRR = 1.9; 95% CI: 1.3, 2.9), and ARI (IRR = 1.5; 95% CI: 0.96, 2.4) was noticed in 1998–2000, while death rate from other causes tended to decline (IRR = 0.8; 95% CI: 0.6, 1.0) (Table 2).


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Table 2 Cause-specific death rates per 1000 person-years, rural Senegal, 1989–2000

 
Between 1–4 years old (n = 1742)
Malaria and diarrhoea largely predominated, each cause explaining 30% of the mortality over the whole study period. In term of rates, death rate attributed to malaria doubled between 1989–1991 and 1992–1994 (IRR = 2.1; 95% CI: 1.6, 2.9) and then reached a plateau. At the same time the proportion of deaths due to malaria almost doubled (19 to 36 percent). The last period, 1998–2000, was marked by a large increase in death rates attributed to meningitis (IRR = 6.6; 95% CI: 3.2, 15.2), FUO (IRR = 4.2; 95% CI: 2.6, 7.3), diarrhoea (IRR = 2.9; 95% CI: 2.2, 3.7), and ARI (IRR = 2.1; 95% CI: 1.3, 3.5), while death rate from other causes declined substantially between 1992–1994 and 1998–2000 (IRR = 0.4; 95% CI: 0.3, 0.6) (Table 2).

Between 5–9 years old (n = 340)
Until 1998, malaria and diarrhoea predominated, explaining respectively 46% and 13% of the mortality. As in the 1–4 year age group, the malaria death rate increased during 1989–1991 and 1992–1994 (RR = 2.6; 95% CI: 1.4, 5.0) and then did not change significantly until 1998. The proportion of deaths due to malaria paralleled this pattern. A major feature in this age group was the dramatic increase in the death rates attributed to meningitis and FUO during the period 1998–2000 compared with 1995–1997 (IRR = 56.5; 95% CI: 9.7, 2273.3 and IRR = 10.6; 95% CI: 2.6, 93.3, respectively) (Table 2).

Between 10–14 years old (n = 142)
Due to the low number of deaths in this age group, the mortality pattern should be interpreted cautiously, but diarrhoea remained a leading cause. As in the younger age groups, the period 1998–2000 was marked by a high mortality rate due to meningitis and FUO compared with the preceding period (IRR incalculable due to zero case in 1994–1997; rates changed from 0 to 2.33 deaths/1000 p-y and from 0 to 1.12 deaths/1000 p-y, respectively) (Table 2).

Seasonality of causes of death
Throughout the whole study period, two-thirds of deaths occurred during the second semester of the year with a maximum in September–October (16% and 18%, respectively). This distribution was observed for diarrhoea, ARI, FUO, ill-defined/unknown, and other causes. The months from February to April concentrated two-thirds of the meningitis deaths, and 92% of deaths attributed to malaria occurred during the second semester with a peak in September–October (26% and 31%, respectively). The peak in ARI deaths occurred later in October–November (Figure 2).



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Figure 2 Monthly distribution of the number of deaths according to the main causes of death, Niakhar, rural Senegal, 1989–2000

 
Deaths attributed to FUO did not differ by semester except for the period 1998–2000 when this proportion was significantly higher during the first semester than during the second one (17.5% versus 12.7%, P = 0.02). Compared with the three preceding periods, the first semester proportion increased two to three times in 1998–2000 (17.5% versus 8.4%, 5.8%, and 6.2%, respectively).


    Discussion
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 Abstract
 Population and Methods
 Results
 Discussion
 Conclusion
 References
 
Methodological issues
Throughout the whole study period, ill-defined and unknown causes accounted for only 3–7% of deaths depending upon age with a decreasing trend which could reflect a growing experience of verbal autopsy. Examination of basic assumptions and validation studies of verbal autopsy in childhood causes of death have not often been carried out.2 Large variability due to recall period has been reported.1 As a result of an experience in Niakhar, Garenne et al. recommended 2–4 months.1,23 In our study, the recall period was well under 4 months. In validation studies conducted in East Africa, verbal autopsy was judged to be appropriate to detect measles, neonatal tetanus, malnutrition, and traumas in children under one year old with high sensitivities and specificities, but it performed poorly for malaria, ARI, gastroenteritis, and meningitis with sensitivities below 50%.25,5 A study on maternal recall of symptoms confirmed that symptoms of Kwashiokor, measles, convulsions, and traumas were reported accurately. Conversely, fever, pallor, chest indrawing, severe diarrhoea, vomiting, all signs used to describe malaria, ARI and diarrhoea, were reported with high false positive rates.25 In other settings, however, verbal autopsy using diagnostic algorithms was judged able to diagnose major causes of deaths among children under 5 years old with some limitations for ARI.26–28 Indeed, it is widely recognized that diagnosis of malaria and ARI by verbal autopsy is particularly difficult due to the non-specific symptoms and clinical overlap with pneumonia.1,29–31 Consequently, the death rates due to malaria and ARI must be interpreted with caution since they are susceptible to misclassification bias. Outside meningitis outbreak periods, the differential diagnosis of severe malaria and meningitis is also problematic due to overlapping symptoms.32 However, meningitis outbreaks are recent in Niakhar and hit the study zone between January and May while malaria cases are concentrated between August and November.21,33 The seasonality mainly concerned meningitis and malaria. This seasonality is naturally generated by the local climatic conditions, but one can argue that the introduction of this characteristic in the diagnostic procedure could have artificially increased this pattern. However, this characteristic was primarily used by the clinicians to distinguish between the two diseases when faced with shared signs. The possible impact on the causes of death trends due to the change of clinicians involved over the years was lessened by sharing the same procedure and guidelines. In addition, the review of the discordant cases with a consensus approach reduced the difference between their clinical judgements. There was no health structure in the study zone with adequate medical facilities and staff to undertake a validation study, to obtain a ‘gold standard’ and estimates of sensitivities and specificities, and then adjust our results for misclassification bias. However, Chandramoham et al. showed that sensitivity and specificity estimates obtained in a given location, such as an hospital-based study, cannot be used for correction in another location showing a different pattern of underlying causes of deaths.34

Trends in causes of death before 1998
In spite of these limitations, verbal autopsy provided useful information on the major causes of death and trends. Among the children under 5 years old, diarrhoea and ARI accounted for up to a third of the mortality and FUO remained around 5%. For children between 1–9 years old, malaria was the leading cause of death, explaining a third of the mortality. A recent meta-analysis of verbal autopsy data on malaria mortality in children under 5 for the period 1982–1998 in West Africa using a modelling approach to correct misclassification yielded an average rate of 7.8 deaths/1000 child-years between 1982 and 1998.35 The estimate in Niakhar between 1989 and 1997 was 9.9/1000. This meta-analysis also showed an increase in the proportion of malaria deaths from 18% to 23% between 1982–1989 and 1990–1998. In our study in rural Senegal, the same trend, although more pronounced (19–36%), was observed between 1989–1991 and 1992–1998. Another modelling approach to ARI mortality provided estimates of the CSMF as a function of the under-5 mortality.36 Applied to the mortality level observed in Niakhar, one could expect between 20% and 25% of deaths due to ARI, while only 10% on the average were observed. When compared with data from rural Gambia, the underestimation seemed to affect primarily the first year of life.11 A number of ARI deaths are likely to have been classified in another category, such as FUO or ‘other causes’, due to overlapping symptoms.

1998–2000 mortality
Verbal autopsy was useful in revealing the structure by cause of the 1998–2000 mortality. The large meningitis mortality fraction (>40%) among 5–14 year old children in 1998–2000 is clearly linked to the major West African meningitis outbreak which struck Senegal in 1998–1999 with 2700 notified cases between October 1998 and February 1999.37 The first cases were observed in the study zone as soon as February 1998, and an immunization campaign was then launched by the regional health authorities. Verbal autopsy revealed a posteriori that meningitis was not the sole responsible cause of the 1998–2000 mortality peak, particularly among infants. An increase in death rates due to diarrhoea and ARI among the 0–5 year olds, and due to FUO in every age group paralleled the meningitis outbreak. The increase in the number of deaths due to diarrhoea could partly be explained by an outbreak of shigellosis which affected the study zone in 1999 with a case fatality rate of 7%.38 The increase in death rate due to FUO could be explained by the meningitis outbreak, the signs of the fatal illness being partially reported by the relatives and the death misclassified. Indeed, the proportion of deaths due to FUO was significantly higher during the meningitis outbreak period than the rest of the year, and then only for the period 1998–2000. In that case, the number of deaths due to meningitis has been underestimated.


    Conclusion
 Top
 Abstract
 Population and Methods
 Results
 Discussion
 Conclusion
 References
 
Despite its limitations, verbal autopsy provides useful information on the importance of causes of death, such as malaria or epidemic diseases, and allows the evaluation of the impact of public health intervention such as immunization on mortality from preventable diseases.20 But it also underlines the burden of less publicized causes of deaths, such as diarrhoea, ARI, or FUO. These latter causes accounted for up to 50% of the deaths among the children under 5 and 25% above. In the verbal autopsy approach, rather than a precise medical entity, they represent signs or symptoms reported by the relatives of the deceased. The low specificity of these signs implied a grouping of the diagnoses into large categories (Table 1). The standardization of the definition of these categories in verbal autopsy mortality studies should make it easier to compare them. Diarrhoea, ARI, and FUO causes provide an insight into the general status of the population. They reflect inadequacies in the health system at its most peripheral level in handling common diseases appropriately, and it shows the necessity of implementing more effective interventions.39,40


KEY MESSAGES

  • Verbal autopsy provided useful information on the mortality structure but methodological difficulties must not be overlooked
  • Malaria was a leading cause of death among the children 1–9 years old and malaria death rate increased twofold between 1989–1991 and 1992–1994.
  • Diarrhoea, acute respiratory infections, and fever from unknown origin accounted for up to 50% of the deaths among the children under 5 years.
  • The meningitis outbreak which affected the African meningitis belt in 1996 broadly explained the peak in mortality at the end of the 1990s.

 


    Acknowledgments
 
Funding: Institut de Recherche pour le Développement, France. We are grateful to the physicians who participated with us in the review of the verbal autopsies: Drs B Cissé, JY Gagnepain, P Guyon, P Imbert, S Ka, B Kodio, M Ndiaye, A EHM Ndiaye, MP Préziosi, B Samb, AG Simaga, JF Trape, and A Yam. We thank the field staff of Niakhar, E Faye (head of station), J Diatte, PN Diouf, B Fall (field supervisors), W Diafate, S Diatte, L Diome, A Diouf, D Diouf, S Diouf, S Diouf, R Dogue, A Faye, L Faye, O Faye, D Loum, M Sarr (field interviewers), and the staff in Dakar, Dr F Simondon (project coordinator 1989–95), A Diagne, P Lévi, A Marra, M Ndiaye, ET Ndiaye, E Ndiaye, O Ndiaye, A Ndour (data management). Over all, we wish to acknowledge the co-operation of the families who allowed the collection of these sensitive data.


    References
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 Abstract
 Population and Methods
 Results
 Discussion
 Conclusion
 References
 
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