Factors Associated with Neonatal Sepsis among Neonates Admitted in Kibungo Referral Hospital, Ngoma District-Rwanda: A Retrospective Cross-Sectional Study

doi:10.21203/rs.3.rs-3939093/v1

About four million deaths occur every year worldwide due to neonatal sepsis, of which 99% take place in low-income countries. Nearly 71% of neonatal deaths are preventable and among these, 10% are due to neonatal sepsis. Nevertheless, limited information exists on neonatal sepsis and its associated factors in Rwanda. The objectives of the study were to find prevalence and factors associated with neonatal sepsis among neonates admitted in Kibungo Referral Hospital, Ngoma District, Rwanda. A retrospective cross-sectional study design was used to recruit all neonates admitted at Kibungo Hospital in 2017. Neonates related records were reviewed to collect data. Logistic regression and Odds ratios were calculated to identify the factors associated with neonatal sepsis at 95% CI, p < 0.05. A total of 422 neonates were enrolled in the study, 12.8% (n = 54) had neonatal sepsis, and 62% of blood culture revealed Klebsiella pneumoniae. Among neonates with neonatal sepsis, 38 (70%) recovered while 16 (30%) died. Strong association with neonatal sepsis was found with neonatal age less or equal to three days (AOR: 2.769, 95%; CI, 1.312–5.843; P = 0.008); and gestational weeks less than 37 weeks (aOR: 4.149; CI: 1.1878–9.167; p = < 0.001). Mothers and hospital environments should be monitored to prevent infection through the regular blood culturing and ward decontamination.

Health sciences/Diseases

Health sciences/Medical research

Neonatal Sepsis

Neonates

Factors

Rwanda

Neonatal sepsis remains a public health concern worldwide. More than one million deaths occur per year, with 99% occurring in low- and middle-income countries ^1–3. The global neonatal mortality rate has decreased over the past years, but to a lesser extent compared to other under-five child deaths ⁴. Globally, an estimate of 22%, 25% and 34% of under-five deaths resulted from neonatal infections, intrapartum related conditions and preterm birth complications respectively, with highest mortality rates being reported in Sub-Saharan Africa ⁵. Neonatal deaths account for 68% of under-five deaths in Rwanda ⁶. Rural hospitals mainly serve the poor community, and have limited resources for controlling infectious diseases which might increase the risks of developing sepsis. However, proper management of neonatal sepsis can improve patient outcomes ^7–12.

Neonatal sepsis is clinically having the same symptoms as for other infections and the onset is within 28 days after birth. Neonatal sepsis is subcategorized as early and late onset sepsis, which occur before and after 72 hours of life, respectively ^13–16. Early-onset sepsis is especially due to the germs acquired during gestation or childbirth. Otherwise, the germs responsible for the late onset are coming from the poor hygiene after birth either in the hospital settings or in the environment ^17–20. Neonatal sepsis is confirmed through blood culture, a white blood cells differential count, or an elevated C-Reactive Protein ²¹. The blood culture is the gold standard in sepsis confirmation even if not routinely available in low-income countries ^1,22. Poor hygiene and unenforced infection prevention and control procedures in hospital settings are the leading causes of neonatal sepsis ^23–27.

The incidence of neonatal mortality was higher in rural than in urban settings in Senegal and in Kenya ^28,29. The prevalence of early and late onset neonatal sepsis varies by region. Neonatal sepsis prevalence is between 1 and 10 per 1,000 of all live births in developed countries but increases threefold in low-income countries. Factors reported to be associated with sepsis vary by region and include maternal age, poor access to antenatal care, age of neonate, low birth weight, birth asphyxia ^30–35. The neonatal mortality rate is high in Rwanda with 19 out of 1,000 live births dying each year according to the 2019–2020 Rwanda Demographic Health Survey (RDHS) ³⁰. About 71% of neonatal deaths in Rwanda are preventable and neonatal sepsis account for 10% of total preventable causes. Asphyxia and sepsis are among the leading causes of neonatal deaths in Rwanda as well as prematurity ³⁶.

Only few studies on neonatal sepsis were conducted in Rwanda, and most of them focused to the urban settings ^37–39. To our knowledge no other study that has been conducted to assess factors associated with neonatal sepsis among neonates admitted in Ngoma District. This study aimed to determine the prevalence and factors associated with neonatal sepsis among neonates admitted in Kibungo Referral Hospital, Ngoma District of Rwanda.

Study design and setting

This retrospective, cross-sectional study reviewed the neonatal related records among neonates admitted at Kibungo Hospital, Ngoma District, Eastern Province, Rwanda from January-December 2017. Kibungo is a rural referral hospital located approximately 100 km from Kigali. It is the main referral facility for 12 health centers in its catchment area with only one neonatology unit serving about 85 neonates monthly.

Study population and sample size

The study included all neonates admitted in Kibungo Referral Hospital in 2017. The study reviewed 422 clinical records of neonates, mother’s files and their laboratory records. Neonates and their mothers that were having complete clinical files were included in the study. Neonates with missing data were excluded from the study.

Data collection and procedures

Data was collected in a structured tool developed in Microsoft Excel where all data on environment, mother and neonate’s characteristics were collected through the clinical patient’s files and laboratory result’s records. The data that were collected for neonates are: age, sex, birth weight, mode of delivery, place of birth, birth asphyxia (yes/no), gestational weeks, APGAR (Appearance, Pulse, Grimace, Activity and Respiration) score at birth, resuscitation after birth (yes/no), sepsis developed (yes/no), time of onset, bacteria isolate, antibiotic sensitivity, and sepsis outcome. The data that were collected for mothers are: age, fever (high fever deliberated at 37.5 ⁰C), number of pregnancies, place of delivery, educational level, occupation, marital status, health insurance, maternal infection, obstructed labor, premature rupture of membrane (PROM), foul smelling, meconium aspiration, ubudehe (socio-economic) category. Early and late onset sepsis appears before and after the 72 hours of life, respectively. The 72-hour cut-off point was selected for this study due to the wide range review of most recent articles ^40–42. All data

Data analysis

Statistical analysis for collected data was done using Stata Statistical Software: Release 13. College Station, TX: StataCorp LP. Descriptive statistics, including frequencies and percentages, were calculated to characterize the study population in terms of socio-demographic and other relevant variables. Analytical statistics were performed for bivariate and multivariable logistic regression. For the bivariate logistic regression, the association between independent and dependent variables was found at 95% confidence interval with p-value <0.05. Multivariable logistic regression was done for the variables that showed significant association at the bivariate analysis, and p-value ≤ 0.05 was considered statistically significant. The Stata software version 13. Also used to evaluate the appropriateness of the logistic regression models used in this study to detect multicollinearity using the Variance Inflation Factor (VIF) were we removed all variables with VIF>3 in the model. The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Ethical approval

The study obtained ethical clearance from the ethical committee of Kibungo referral hospital with a reference letter (Ref No:14/117/RJ/H1-1/2/2018). And all data were collected in accordance with all relevant guidelines and in declaration of Helsinki ⁴³. Moreover, no informed consent and assent were required as secondary data were used. Findings of the study were submitted to Kibungo Hospital and the University of Rwanda, College of Medicine and Health Sciences, School of Public Health.

Neonatal Characteristics

A total of 422 neonates admitted to the neonatology department in 2017 were recruited, and their records reviewed (Table 1). Among the neonates, 216 (51%) were males, 206 (49%) females; and 369 (87%) survived. Neonates born through normal delivery were 378 (77.7%) while those born through caesarean section were 94 (22.3%). Neonates delivered at the hospital level were, 251 (59.4%). Among 54 neonates with neonatal sepsis, 38 (70%) recovered, while 16 (30%) died. Almost 57% (31/54) and 43% (23/54) were early and late onset sepsis, respectively. (Table 1)

Table 1: Socio-demographic characteristics of neonates admitted at Kibungo

Hospital neonatology unit, January to December, 2017 (n=422)

Variables	Frequencies(n)	Percentages (%)
Sex
Male	216	51.18
Female	206	48.82
Age group in days
0-3	369	87.44
4-28	53	12.56
Birth weight
<2500	213	50.47
≥2500	209	49.53
Mode of delivery
caesarean	94	22.27
Normal	328	77.73
Place of birth
Hospital	251	59.48
health center	135	31.99
Home	36	8.53
Birth asphyxia
Yes	85	56.64
No	337	43.36
Gestational (Weeks)
<37	239	56.6
≥37	183	43.4
APGAR at birth n (357)
≤6	85	23.81
>6	272	76.19
Resuscitated
Yes	98	23.20
No	324	76.80
Sepsis developed
Yes	54	12.80
No	368	87.20

Neonates’ mothers’ characteristics

Seven percent (7%) of the mothers experienced more than five pregnancies; most of them were employed or self-employed; 396 (94%) had health insurance, while 26 (6%) had none. (Table 2)

Table 2: Socio-demographic characteristics of neonates’ mothers at Kibungo

Hospital neonatology unit, January to December, 2017 (N = 422)

Variables	Frequencies(n)	Percentages (%)
Age group in years
17-20	59	13.9
21-30 >30	254 109	60.2 25.9
Occupation
Employed	416	98.6
Unemployed	6	1.4
Obstructed labor
Yes	7	1.7
No	415	98.3
Education level
None	9	2.1
Primary	371	87.9
Secondary and high	42	10.0
Maternal fever
Yes	40	9.5
No	382	90.5
Health insurance
Yes	396	93.8
No	26	6.2

Neonatal sepsis characteristics, antibiotic susceptibility pattern and outcome

Fifty-four (12.8%) neonates had sepsis of whom 25 (46.3%) were confirmed using blood cultures. Almost 84% (21/25) of the blood cultures done were positive with 62% Klebsiella pneumoniae predominance, coagulase-negative staphylococci (9.5%), Escherichia coli (9.5%), Streptococcus pneumoniae with (9.5%), Acinetobacter baumanii (4.7%) and Staphylococcus aureus (4.7%). Bacteria sensitivity pattern revealed that Klebsiella pneumoniae (46.1%) was resistant to ciprofloxacin and 100% sensitive to meropenem and imipenem in carbapenems family of medications. The clinical outcome revealed that only 70.4 % of neonates with sepsis survived.

Environmental colonization monitoring

Information gathered from the laboratory for the study period showed the presence of various bacterial species in the neonatal and maternity wards: Enterobacter cloacae, Klebsiella pneumoniae, Serratia species, Providencia stuartii and Escherichia coli.

Bivariate analysis of neonatal characteristics

After bivariate analysis, neonates age group (P = 0.022) and gestational age (P = 0.031) were found to be significantly associated with neonatal sepsis (Table 3) and therefore, they were considered for the Multivariate logistic regression. Association of APGAR score at birth with neonatal sepsis was not statistically significant (P = 0.771).

Table 3: Bivariate and multivariate analysis of neonatal characteristics associated with sepsis at Kibungo Hospital

Variables		Sepsis developed				cOR (95% CI)	P -value
	N=422	Yes		No		cOR (95% CI)	P -value	aOR (95% CI)	P-value
	N=422	No	%	No.	%
Sex
Male	216	26	12.04	190	87.96	1	0.633
Female	206	28	13.59	178	86.41	0.869 (0.491 - 1.540)	0.633
Age group (days)
≤3	369	42	11.38	327	88.62	2.278 (1.110 - 4.677)	0.022	2.769(1312-5.8430	0.008*
≥4	53	12	22.64	41	77.36	1	0.022	1
Birth weight
<2500	213	32	15.02	181	84.98	1	0.167
≥2500	209	22	10.53	187	89.47	1.502 (0.841 - 2.684)	0.167
Mode of delivery
Caesarean	94	8	8.51	86	91.49	1	0.163
Normal	328	46	14.02	282	85.98	0.570 (0.259 - 1.254)	0.163
Birth asphyxia
Yes	85	11	12.94	74	87.06	1	0.964
No	337	43	12.76	294	87.24	1.016 (0.499 - 2.066)	0.964
Gestational age (weeks)
<37	239	38	15.90	201	84.10	2.573 (1.358 – 4.875)	0.004	4.149 (1.878 – 9.167)
≥37	183	16	8.74	167	91.26	1	0.004	1	<0.001**
APGAR at birth n (357)
≤6	85	11	12.94	74	87.06	1	0.771
≥7	272	32	11.76	240	88.24	1.114 (0.535 - 2.320)	0.771
Notes: : Statistical significance at p<0.05, *: statistical significant at p<0.01

Bivariate analysis of maternal characteristics

After the bivariate analysis of the maternal characteristics, it was seen that no maternal characteristic was statistically significant and eligible for the multivariable logistic regression. (Table 4)

Table 4: Bivariate analysis of maternal characteristics associated with sepsis at Kibungo Hospital

Variables		Sepsis developed
	N=422	Yes		No			cOR (95% CI)	P value
	N=422	Frequency	%		Frequency	%	cOR (95% CI)	P value
Age group
17-20	59	5	8.47		54	91.53	1.726 (0.645 - 4.613)	0.277
21-30	254	35	13.78		219	86.22	1
>30	109	14	12.84		95	87.16	1.084 (0.557 - 2.108)	0.811
Education level
No education	9	2	22.22		7	77.78	1
Primary	371	45	12.13		324	87.87	2.069 (0.417 - 10.273)	0.373
Secondary and higher	42	7	16.67		34	83.33	1.42 (0.243 - 8.375)	0.693
Occupation
Employed	416	54	12.98		362	87.02	1
Unemployed	6	0	0		6	100.00	1(Omitted)	0.345
Place of delivery
Hospital	251	28	11.16		223	88.84	1
Health center	135	20	14.81		115	85.19	0.721 (0.389 - 1.337)	0.300
Home	36	6	16.67		30	83.33	0.627 (0.240 - 1.640)	0.342
PROM
Yes	32	4	12.50		28	87.50	1
No	390	50	12.82		340	87.18	0.971 (0.326 - 2.886)	0.958
Foul smelling
Yes	8	2	25.00		6	75.00	1
No	414	52	12.56		362	87.44	2.320 (0.456 - 11.802)	0.310
Obstructed labor
Yes	7	1	14.29		6	85.71	1
No	415	53	12.77		362	87.23	1.138 (0.134 - 9.642)	0.905
Maternal fever
Yes	40	7	17.50		33	82.50	1
No	382	47	12.30		335	87.70	0.413 (0.457 - 1.284)	0.352
Health insurance
Yes	396	51	12.88		345	87.12	1
No	27	3	11.54		23	88.46	1.133 (0.328 - 3.910)	0.843

Multivariable analysis of characteristics associated with sepsis

Multivariable analysis was done only for the neonate characteristics that showed significant association with neonatal sepsis in bivariate analysis (neonate age and gestational weeks). Strong association with sepsis was found with neonatal age less or equal to three days (AOR: 2.769; 95% CI, 1.312- 5.843; P = 0.008), and gestational weeks less than 37 weeks

(aOR: 4.149; CI: 1.1878 – 9.167; p=<0.001). (Table 3)

The purpose of this study was to identify the factors associated with neonatal sepsis among neonates admitted in Kibungo Referral Hospital, Ngoma District, Rwanda. The study findings show that neonatal sepsis prevalence was 12.8%, 29.6% of neonates who experienced sepsis died. Decreasing deaths for newborns and mothers is a global priority to achieve Sustainable Development Goals, and to implement United Nations Global Strategy for Women, Children and Adolescent health.[5] Though Rwanda is among the few countries in Africa which achieved fourth Millennium Development Goal to reduce child mortality, mortality rate among neonates is still of great concern. Neonatal sepsis is still a leading cause of neonatal morbidity and mortality in Rwanda, including the study area.^44,45

The prevalence of 12.8% of neonatal sepsis found in this study is less than what was reported by studies from Sudan (37.8%), Tanzania (24%) and Nigeria (47.2%).[15,16,47] However, the prevalence in this study is comparable to the results reported in North Sinai, Cairo (12.8%), but higher than the results reported from South Sinai (8.6%) and Cairo (4.47%).³⁴ The difference in neonatal sepsis prevalence could be attributed to the difference in the study setting in terms of infection prevention and control, staffing, funding, and policy.

The study found that among the 54 with neonatal sepsis, early-onset neonatal sepsis was 57.4% and late-onset 42.6%, which was consistent with the study conducted in South Sinai that found the mothers and hospitals to be the main source of early-onset and late-onset of neonatal sepsis. ³⁴ Early onset neonatal sepsis was a little higher (57.4%) than late onset neonatal sepsis (42.6%) in this study and comparable to a study done in South Sinai where early-onset sepsis stood at 68.2% and late-onset sepsis (31.8%).³⁴ On the other hand, our study results contrasts with what was reported in a research conducted at Mansoura Hospital in Egypt, where early onset sepsis was lower at 44.2% and late onset sepsis was higher 55.8%.⁴⁶ This could be due to the differences in the different characteristics of mothers and the setting where the study was conducted.

The sepsis fatality rate was 29.6%, which is high and reflects inadequate management of sepsis, perhaps linked to delays in diagnosis and treatment. This sepsis fatality rate is almost similar to the findings of the study done in Tehran (27.4%) and South Sinai 25%. ^34,47 Blood cultures were not routinely performed to suspected cases, thus only 25 were collected among the 54 with sepsis, while the rest of neonatal sepsis cases were empirically confirmed. This could be due to the fact that microbiology results took much longer time, triggering the physicians to opt for empirical therapy. Among the 25 blood cultures done, 84% (21/25) were positive with predominance of Klebsiella pneumoniae (62%). The study finding agreed with research done in India, which found preponderance of Klebsiella pneumoniae among neonates.⁴⁸ Bacteria sensitivity pattern revealed that Klebsiella pneumoniae (46.1%) was resistant to ciprofloxacin and 100% sensitive to meropenem and imipenem in the carbapenem family of medications. The findings of current study are different from a study done in Sudan that reported susceptibility of Klebsiella pneumoniae of 87% to Ciprofloxacin, and 81% to meropenem, which was caused by a variation of antimicrobial susceptibility patterns in bacteria.⁴⁹

Multivariable analysis revealed that gestational weeks, and neonatal age (days) were statistically significantly associated with neonatal sepsis. Neonates aged 3 days or less were more likely to develop sepsis, (AOR=2.769, CI, 95%; P = 0.008) which is comparable with the study done in Ethiopia neonates with 3 days old or less (AOR = 2.802; CI, 95%, = 0.018) were more likely to develop sepsis.^50,51 Prolonged rupture of membrane, place of delivery, health center delivery, intrapartum fever, APGAR Score <7, low birth weight, abnormal amniotic fluid and assisted ventilation were not found as associated factors, in contrast to the studies done in Mexico and Ethiopia which were conducted in urban settings.^17,52

In this study information from the laboratory showed the presence of Enterobacter cloacae, Klebsiella pneumoniae, Serratia species, Providencia stuartii and Escherichia coli in the neonatal and maternity wards. The study done in Morocco, Brazil, Austria and India on neonatology environment reported the presence of different bacteria including Klebsiella pneumoniae, coagulase-negative staphylococci and other Enterobacteriaceae. ^31,53–55 The presence of those bacteria isolates in the neonatal and maternity settings highlights the need to regularly monitor their environment and execute infection control by improving hygiene and sanitation.

Limitation of the study

The current study did not assess adequately the environmental factors due to the fact that environmental monitoring was not regularly conducted. Inconsistent selection of antibiotics for antibiotic sensitivity did not allow a more robust assessment of blood sensitivity patterns.

The study highlighted that neonate age and age of gestation below 37 weeks were significantly associated with neonatal sepsis. Maternal and hospital characteristics were found to be the leading contributors to neonatal sepsis. The scarce information about the presence of bacteria in the maternity and neonatal environment could be the hidden cause of the sepsis in the study area thus routine environmental monitoring should be initiated. Improving the use of blood culture and consistent selection of antibiotics, when performing antibiotics susceptibility tests, could enhance the management of neonatal sepsis in the area. Lastly, improving record keeping could also facilitate efficient evidence-based decision-making.

Acknowledgments

Our appreciation goes to Kibungo Referral Hospital and University of Rwanda-School of Public Health for their support during this study.

Author’s contributions

JCN, JN, JO, and HN designed the study, collected, analyzed and interpreted the data, drafted and revised the manuscript. TD, PCB, ON, IC and HF participated in interpretation of data, drafted the manuscript and revised it critically. All authors approved the final version of the manuscript.

Funding

No funding or grant was allocated to this research from any sponsor or partner.

Conflicts of interest

All authors confirm that there is no conflict of interest from the conception of the proposal up to the finalization of the manuscript.

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No competing interests reported.

Factors Associated with Neonatal Sepsis among Neonates Admitted in Kibungo Referral Hospital, Ngoma District-Rwanda: A Retrospective Cross-Sectional Study

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Abstract

Introduction

Methods