Neonatal tetanus: mortality rate and risk factors in Loralai District, Pakistan

Arshad Quddusa, Stephen Lubyb, Mohammad Rahbarc and Yousaf Pervaizd

a WHO EPI/Polio Eradication Program, Balochistan, Pakistan.
b Foodborne and Diarrheal Diseases, Centers for Disease Control, AtlantaGA, USA.
c Community Health Science Department, The Aga Khan University, Karachi, Pakistan.
d Department of Pediatrics, Sandemen Provincial Hospital, Quetta, Pakistan.


    Abstract
 Top
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 References
 
Background This study was conducted to estimate the neonatal tetanus (NNT) mortality rate and to identify the risk factors for NNT deaths in Loralai District, Pakistan.

Method We conducted a community-based cross-sectional survey during July–September 1997. We stratified the sample proportionate to population of union councils. The most populous village in a union council was selected first. We interviewed the women, selected randomly, who had a live birth in the 18 months preceding the survey. We conducted a matched case-control study to identify the risk factors for NNT deaths. We used the World Health Organization criteria to enrol cases, identified during the cross-sectional survey or registered at the district hospital. We enrolled three community-based controls per case, matched on the area of residence, immunization status and date of birth.

Results Of the 1547 live births, there were 36 neonatal deaths due to tetanus. The NNT mortality rate in the district was 23 per 1000 live births (95% CI: 16–30). For the case-control study, we enrolled 41 cases and 123 controls. Using conditional logistic regression, the risk of NNT death was increased with the use of soil as delivery surface (O.R = 3.2, 95% CI: 1.1–10.2), father's illiteracy (OR = 3.2, 95% CI: 1.3–8.1) and possession of sheep at home (OR = 2, 95% CI: 1.0–5.0). The population attributable risk per cent for soil as delivery surface was 64%.

Conclusion Transmission of infection while using soil as the delivery surface can occur through direct or indirect contamination of the fresh umbilical wound. Use of safer delivery practices in general and clean surfaces in particular should be encouraged to reduce the NNT mortality rate in the area.

Keywords Neonatal tetanus, mortality rate, District Loralai, elimination, delivery surface

Accepted 22 November 2001


    Introduction
 Top
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 References
 
Neonatal tetanus, caused by Clostridium tetani, is the second leading cause of death from vaccine-preventable diseases among children world-wide.1 Globally, an estimated 248 000 neonatal deaths were caused by neonatal tetanus (NNT) during 1997.1 Almost 11% (26 400) of these NNT deaths were in Pakistan with an NNT mortality rate of 5 per 1000 live births.1 Neonatal tetanus is one of the most underreported diseases2 and its estimated mortality rate varies widely from country to country and within countries.1,3,4,5 Therefore it is important to identify the high-risk areas by defining magnitude of the disease in different parts of a country.6

Achieving and maintenance of high levels of maternal immunization with tetanus toxoid through sustained effort is the cornerstone of control strategies for NNT.1,7,8 However, since Cl. tetani is ubiquitous in the environment, in regions where high levels of tetanus toxoid coverage are difficult to maintain, identification of other risk factors is critical in designing additional protective measures.9 An integrated approach with immunization and non-specific measures can help in efficient utilization of limited resources in eliminating NNT.10

In Pakistan, the magnitude of the disease and the risk factors vary across geographical regions within the country.11,12 Wrapping of the neonate in sheep's skin, use of straw as the delivery surface and application of Ghee (clarified butter) to the umbilical stump have been identified as risk factors in the northern areas of the country, while application of antimicrobials to the umbilical cord had a protective effect in a study from the province of Punjab.9,11,12 These findings suggest a diversity of birth practices enhance the risk of NNT in different regions of Pakistan and suggest different ways are needed to augment the effectiveness of the NNT elimination programme.

Balochistan is the least developed province of Pakistan and the infant mortality rate ranges between 96 per 1000 live births in Lasbella District and 143 per 1000 in Loralai District.13 Since the magnitude of NNT in the province was not evaluated in the past, we perceived a need to provide baseline information to help programme managers design an appropriate control policy. We conducted this study to estimate the NNT mortality rate and to identify the risk factors for NNT deaths in Loralai District, Balochistan.


    Methods and Materials
 Top
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 References
 
We conducted a community-based cross-sectional survey from July through September 1997 to estimate the NNT mortality rate in Loralai District, Balochistan Province, Pakistan. Eligibility criteria included women who had a live birth in the 18 months preceding the survey.

To calculate the necessary sample size to estimate NNT mortality, we assumed an NNT mortality rate of 20 per 1000 live births. This assumption was based on information from the 1990–1991 Maternal and Infant Mortality Survey, Balochistan,13 which showed a neonatal mortality rate of 66.4/1000 live births in Loralai. Since NNT is one of the leading causes of neonatal mortality in Pakistan,14 we assumed that at least 30% of the neonatal deaths in Loralai could be due to NNT, leading to an estimated NNT mortality rate of 20 per 1000 live births.

If the number of births required is ‘n’ and anticipated NNT mortality proportion is ‘p’, (assumed to be 20 per 1000 live births or 0.02) and the maximum acceptable difference from true value is 0.007, then for a significance level of 5%:



To account for non-response and incomplete questionnaires, the sample size was increased by 5% to 1600 live births.

The district is divided administratively into three subdivisions and the subdivisions into 16 union councils. The villages within a union council were the smallest administrative units. We distributed the total sample size of 1600 live births to the subdivisions, proportionate to their population size. In the second stage, we redistributed the sample size for each subdivision into its union councils according to the proportion of their population. In each of the union councils, we selected the most populous village. After arriving in the village, four teams of female interviewers departed in different directions towards their first household, selected randomly, to interview the eligible women. The subsequent households were the next closest ones. We obtained verbal consent from the eligible interviewee prior to the start of the interview and used a questionnaire to obtain detailed information about demographic and socioeconomic characteristics, birth practices and maternal immunization status with tetanus toxoid. To identify a neonatal death due to tetanus, we included a verbal autopsy form as part of the questionnaire. We interviewed the eligible women in the village until reaching the pre-assigned sample size. When the required sample size for that union council could not be achieved in the selected village we approached the next nearest village of the same union council, and continued to enrol study subjects until the sample size was reached.

To identify the risk factors for NNT death, we conducted a matched case-control study. A case was defined as a neonate with a history of normal cry and suck for the first 2 days, who developed symptoms beginning between the third and 28th days of life, including inability to suck, jaw locking, stiffness and convulsions, followed by death. All of the above symptoms were necessary for the case definition. The same criteria were used to identify NNT deaths during the cross-sectional survey. Infants who had symptoms of NNT but recovered were excluded as controls. Cases identified during the cross-sectional survey or diagnosed and registered at the District Headquarter Hospital during the 18 months preceding the survey, were eligible for inclusion in the case-control study.

We enrolled three community-based controls per case. The controls lived in the same union council as the case and were born within 1 month of the date of birth of the case. Both cases and controls had the same immunization status. Since untrained personnel conducted most of the deliveries in the area, for sample size calculation, we assumed that the proportion of unhygienic delivery practices in the area was 60%. We required 85 cases and 255 controls to detect a difference of at least 15% in the distribution of unhygienic delivery practices among the cases and controls with a significance level of 5% and power of at least 80%.

In the analysis, we computed the estimate for NNT mortality with its 95% CI. We obtained information on possession of household assets and ownership of agricultural land and animals as proxy indicators of wealth. We assigned the average current market price to each household item, unit of agricultural land (acre) and animal. On the basis of the monetary value of their overall assets, we classified people as having assets of <US$1100, US$1100–2200 and >US$2200.

In the matched analysis, we computed the maximum likelihood estimates and exact 95% CI for each variable of interest. In the comparison, we collapsed the variables with multiple categories in a biologically or socially meaningful way. We defined the category with the minimal level of NNT risk as the reference group for each risk factor.

In the multivariate analysis, we used cLogistic version 1.00E for conditional logistic regression.15 We based the criteria for the inclusion of risk factors in the multivariate analysis on both biological and statistical significance (P <= 0.05).

We assessed the interaction between the variables on the basis of the additive effect of these variables. An interaction term was considered positive, i.e. having synergism, if the joint effect of the two variables was greater than the sum of independent effect of the two. To judge the additive effect, we used a reference category where both the variables X1 and X2 were absent and then compared it with each of the three categories, where X1 was present only, where X2 was present only and where both X1 and X2 were present. Only those interaction terms biologically consistent with tetanus transmission were formed and investigated.

We used the Levin's formula16 to calculate the population attributable risk per cent: {lambda} = {nu} (R – 1)/{1 + {nu}(R – 1)}. In this formula, {lambda} indicates the population attributable risk, {nu} is the prevalence of risk factor in the population while R is the measure of risk associated with the risk factor of interest. Since the odds ratio is a good approximation of relative risk, R, for rare diseases,17 we used the adjusted odds ratio as a measure of risk for the variable of interest.


    Results
 Top
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 References
 
We approached 1553 eligible women and interviewed 1547 (99.6%) of them. Their mean age was 31 years. Only 4% of the mothers and 35% of the fathers in the area were literate (Table 1Go). A mother or father was considered illiterate when they had no formal schooling ever, otherwise they were labelled as literate irrespective of their level of education. The monetary value of overall assets of 44% of study population was <US$1100, while 38% and 17.5% had assets valued at US$1100–2200 and >US$2200, respectively. The home was the most common (96%) place of delivery and untrained personnel assisted most (60%) of the deliveries (Table 1Go). For 81% of the deliveries, soil was used as a surface for the delivery. Sixty-one per cent of the women had at least two pregnancies during the last 3 years (Table 1Go). Only 5% of the mothers either had documentation or gave a credible history of receiving two doses of tetanus toxoid at least 4 weeks apart during their last pregnancy (Table 1Go).


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Table 1 Basic characteristics of study population (n = 1547), Loralai District, Balochistan, Pakistan, 1997
 
Out of 1547 live births, 196 died during infancy (<1 year); 94 (48%) of the deaths were during the neonatal period (<1 month). The infant mortality rate and neonatal mortality rate of the district were 127 per 1000 live births (95% CI: 111– 143) and 61 per 1000 live births (95% CI: 50–72), respectively. Thirty-six neonatal deaths met the case definition for tetanus giving an NNT mortality rate of 23 per 1000 live births in Loralai District (95% CI: 23 ± 7). The NNT deaths accounted for 38% of all the neonatal deaths and 18% of the infant deaths.

Eight cases of NNT were registered in the district hospital during the 18 months preceding the survey. Three of the registered NNT cases recovered completely and were excluded from the study. Case fatality rate among the NNT cases admitted to the district hospital was almost 62%.

Univariate analysis
To identify the risk factors, we enrolled 41 cases and 123 matched controls (Table 2AGo). Of the 41 cases, 36 cases were identified during the cross-sectional survey while 5 cases were enrolled from the District Headquarter Hospital Loralai. Newborns who were delivered on soil were more likely to die of tetanus than the newborns delivered on plastic/bed sheet (Table 2Go). Possession of sheep at home, father's illiteracy and deliveries conducted by a relative increased the risk of NNT (Table 2Go). Mothers of neonates who died of tetanus were more likely to report multiple pregnancies during the last 3 years than mothers of neonates without tetanus. Parents who paid a fee for delivery services were less likely to have a neonate developing tetanus compared to the parents who did not pay (Table 2Go).


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Table 2 Univariate analysis of risk factors for neonatal tetanus mortality, Loralai District, Balochistan, Pakistan, 1997
 
Multivariate analysis
Based on the results of univariate analysis, we used a conceptual approach to identify the biologically important variables to be evaluated for confounding during multivariate analysis. We included distant factors (education, presence of sheep in the household compound), intermediate factors (birth attendant, fee for delivery services) and more proximal exposure (delivery surface).

On multivariate analysis, use of soil as delivery surface, illiteracy of fathers and possession of sheep at home were identified as the risk factors in the area (Table 3Go). Paying a fee for delivery services had a protective impact on the risk of developing NNT (Table 3Go). To ensure that the inclusion of cases enrolled outside of the community-based survey did not bias the result, we excluded the 5 cases enrolled from the District Headquarter Hospital and restricted our multivariate analysis to only 36 cases enrolled from the community. Exclusion of these cases did not appreciably change the point estimates.


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Table 3 Multivariate analysis of risk factors for neonatal tetanus, Loralai District, Balochistan, Pakistan, 1997
 
There was no interaction between the type of delivery surface and father's education or between the type of delivery surface and possession of sheep at home. The population attributable risk per cent for the use of soil as delivery surface was 64%.


    Discussion
 Top
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 References
 
The NNT mortality rate was 23 per 1000 live births in this community-based survey. Low immunization coverage with tetanus toxoid (5%) and high prevalence of the deliveries assisted by untrained personnel (86%) under unhygienic conditions (Table 1Go), contribute to the high mortality rate in the district. These results are consistent with estimates from studies conducted in the northern areas of Nigeria and the Kilfi district in Kenya where NNT mortality was 20.6 and 21.7 per 1000 live births, respectively.18,19 In comparison, in rural Punjab, Pakistan, the estimated NNT mortality is 11.6 per 1000.9 The higher maternal tetanus toxoid coverage rate of 23% in Punjab may be responsible for the lower NNT mortality rate in that province.20

Although NNT accounted for half of all neonatal deaths and one-fourth of all infant mortality in some countries during the 1980s,21 the situation has not changed much in this part of Pakistan, as NNT was responsible for 38% of neonatal and 18% of all the infant mortality. This implies that achieving NNT elimination will have a significant impact on reducing the neonatal and infant mortality, particularly in high-risk areas.

The case fatality rate among the NNT cases admitted to the district hospital was 62%. The case fatality rate can be affected by the interval between onset of symptoms and presentation for treatment in hospital, and certain other factors22 which were not measured in this study. However, our study shows that an optimal utilization of medical facilities can prevent a substantial proportion of deaths among NNT cases.

The unhygienic practice that contributed most to the high mortality rate in the area was the use of soil as delivery surface (OR = 3, 95% CI: 1.1–9.1). Most of the houses in the area were made of mud with the floor plastered by a thin layer of mud and hay. Prior to delivery, a layer of soil is typically spread on the floor and used as a soaking agent to avoid permanent contamination of floor by bleeding or other fluids discharged during the delivery. Typically agricultural farm soil from the vicinity is the source of soil. Agricultural soil is heavily contaminated with Cl. tetani but the presence of animals like sheep or goats (a risk factor in this study), also increases the probability of presence of Cl. tetani spores in the environment.23 Unhygienic delivery practices in such an environment can increase the risk of transmission of infection by contamination of the umbilical wound either directly or indirectly through the hands of birth attendant.9 The use of straw as delivery surface and living in close contact with animals were potential risk factors for NNT in studies conducted in Pakistan and India.4,14 The use of different kinds of delivery surfaces in various parts of the country has important policy implications and reflects the importance of delivery surface in reducing the risk of NNT within the country and in areas of developing countries where this habit is being practised.

Father's illiteracy was a potential risk factor in this study. Education acts by changing health-related behaviours like birth practices,23 hence it decreases the probability of being exposed to different risk factors. In our study, paying a fee for delivery services had a protective impact on the risk of developing NNT (Table 3Go). Paying a fee for delivery services is a surrogate for tendency among the parents to choose a birth attendant with more skills, hence reducing the possibility of being exposed to different risk factors. Paying a fee for delivery services is also proxy for some unmeasured variables that might lead to a safer delivery environment like clean hands and clean cord care practices. Delivery conducted by untrained personnel has been identified as a potential risk factor for NNT in different studies.14,24 The relative as delivery attendant was a potential risk factor during our univariate analysis (Table 2Go), but a small sample size and high correlation (P < 0.01) with the variable ‘paid a fee for delivery services’ might have limited our capacity to detect its impact during multivariate analysis (Table 3Go).

In our univariate analysis (Table 2Go), mothers of the tetanus cases were more likely to report multiple pregnancies during the last 3 years than the mothers of the controls. We did not include this variable in multivariate analysis, as it is not considered as a risk factor in our conceptual framework of causal pathway. A number of previous studies12,25,26 in Pakistan and other developing countries show that NNT tends to occur more commonly among children of mothers with previous history of NNT cases, due to repetition of unsafe practices in subsequent deliveries. In our study, multiple pregnancies among mothers of cases could be due to the desire to replace the child, i.e. if a mother loses a child she is more likely to strive to become pregnant and replace the child, thus resulting in repeated pregnancies.

Studies in Pakistan, Sudan and Egypt5,27 showed that unhygienic practices during circumcision were responsible for the higher proportion of neonatal deaths due to tetanus among males than females. We did not find any such disparity in the proportion of male and female NNT deaths. This is because, in our study area, people did not practise circumcision during the neonatal period, but after the child's first birthday.

One limitation of this study was the non-random selection of the villages. In each of the union councils, we selected the village with the highest proportion of population among all the villages of that union council. Smaller villages may have lower literacy rates and also higher prevalence of unhygienic birth practices due to lack of health facilities, which could bias the results toward underestimation. However, the proportion of women (4%) who sought care outside the home (Table 1Go) indicates a cultural uniformity in the area. Since the variation of birth practices from village to village within a union council was minimal, the magnitude of underestimation is likely not substantial. We did not achieve the desired sample size of 85 cases for the case-control study which might have limited our capacity to detect the effect of the factors that have lesser effect.

The identification of delivery surface (soil) as a risk factor and low immunization coverage with tetanus toxoid indicates deficiencies of the Maternal and Child Health Services and Expanded Program on Immunization in the area. The Expanded Program on Immunization should observe sub-national immunization days, particularly in high-risk districts, to raise the tetanus toxoid coverage level. Ongoing efforts are required through fixed vaccination centres, outreach workers and community involvement in order to sustain a high coverage level in the area. Additional strategies like school-based immunization services may also be considered to maintain the high coverage.

The population attributable risk per cent for the use of soil as delivery surface was 64%, which has important policy implications and shows that 64% of the NNT deaths in the general population of the area can be eliminated if we stop the use of soil as a delivery surface. Finally, with a 90% effective tetanus toxoid vaccine, even if the 80% coverage of maternal immunization with at least 2 doses of tetanus toxoid is achieved, millions of unprotected births will occur annually in developing countries and NNT deaths will continue among these unprotected neonates.9 Our study shows that a substantial proportion of these NNT deaths can be prevented through improved delivery practices, particularly the use of a clean delivery surface. The intent of this discussion is not to belittle the importance of immunization or to choose between immunization and non-specific measures. Rather it indicates that an integrated approach is required, combining specific and general measures to make the most effective and efficient use of limited resources in preventing deaths from NNT.

Since relatives conducted most of the deliveries (Table 1Go), only training traditional birth attendants will not deliver safe services to most of the mothers. This calls for community involvement and awareness in the area through health education at community level and counselling of pregnant mothers at individual level to encourage safe delivery practices in general and use of a clean delivery surface in particular. The possession of sheep at home as a risk factor also emphasizes the importance of safe delivery practices, particularly in areas of animal husbandry and agriculture.

In order to achieve the goal of NNT elimination in developing countries like Pakistan, it is important to alter the environmental conditions during the delivery by changing birth practices and improving immunization coverage with tetanus toxoid.


KEY MESSAGES

  • Neonatal tetanus (NNT) is still one of the major health problems in rural areas of Balochistan Province, Pakistan and is responsible for a substantial proportion of neonatal deaths in the area.
  • The unhygienic practice that contributed most to the high NNT mortality rate was the use of soil as a delivery surface.
  • In order to eliminate NNT in developing countries like Pakistan, it is important to alter the environmental conditions during delivery and improve tetanus toxoid immunization coverage.

 


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Table 2A Distribution of risk factors for neonatal tetanus mortality among cases and controls, District Loralai, Pakistan, 1997
 

    Acknowledgments
 
We are grateful to Mr Iqbal Azam and Mr Rasool Bux of The Aga Khan University, Karachi for their help in data management and analysis. We are also grateful to The British Council, sub-office Quetta, Pakistan, for the financial support.


    References
 Top
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 References
 
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27 World Health Organization. Prevention of neonatal tetanus: WHO meeting. World Health Forum 1982;3:432–33.





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