SUDANESE JOURNAL OF PAEDIATRICS

2021; Vol 21, Issue No. 2

ORIGINAL ARTICLE

Clinical spectrum of childhood tuberculosis and outcome at Mohammed Alamin Hamid Pediatric Hospital, Omdurman, Sudan

Walyeldin Elnour Mohamed Elfakey (1), Sara Altayeb Abd Algader Altayeb (2), Karimeldin Mohamed Ali Salih (1,3), Omaima Abdel Majeed Mohamed Salih (4)

(1) Department of Pediatrics and Child Health, College of Medicine, University of Bahri, Sudan

(2) Pediatrics Specialist, Ministry of Health, Sudan

(3) Department of Pediatrics, College of Medicine, University of Bisha, KSA

(4) Department of Pediatrics and Child Health, Omdurman Islamic University, Sudan

Correspondence to:

Walyeldin Elnour Mohamed Elfakey

Department of Pediatrics and Child Health, College of Medicine, University of Bahri, Sudan

Email: walyeldin [at] aol.co.uk

Received: 10 August 2020 | Accepted: 16 May 2021

How to cite this article:

Elfakey WEM, Altayeb SAAA, Salih KMA, Salih OAMM. Clinical spectrum of childhood tuberculosis and outcome at Mohammed Alamin Hamid Pediatric Hospital, Omdurman, Sudan. Sudan J Paediatr. 2021;21(2):144–151.

https://doi.org/10.24911/SJP.106-1597063699

ABSTRACT

The World Health Organization report in 2018 estimated 234,000 deaths due to tuberculosis (TB) in children less than 15 years; 40,000 of them occurring in human immunodeficiency virus (HIV) infected children. These deaths represent 15% of all TB deaths. This study aimed to determine the clinical spectrum and outcome of childhood TB at Mohamed Alamin Hamid Pediatric Hospital TB management unit. Retrospective observational hospital-based study was conducted during January 2017-December 2018, in children aged 0-18 years who were diagnosed with TB. A total of 174 patients were enrolled in this study. The majority of patients’ ages ranged from 5 to 17 years (111, 63.8%). Most of the patients were males (92, 52.9%) and (142, 81.6%) resided in Khartoum State. Lung opacity and hailer parenchymal shadows were the common presenting features (83, 47.7%) in chest X-ray. Sputum for acid fast bacilli was positive in only 20 (11.5%) patients. Testing for HIV was negative in 41 (23.6%) patients and was not done in 133 (76.4%). A total of 107 (61.5%) children were diagnosed as having pulmonary TB; extra pulmonary tuberculosis (EPTB) was 67 (38.5%). Tuberculous lymphadenitis was the commonest type of EPTB and was diagnosed in 38 (56.7%) patients. The majority 94 (87.9%) completed their treatment and 13 (12.1%) with smear positive results were cured. Defaulters were 20 (11.5%), and 6 patients (3.4%) were retreated after default, 11 (6.3%) were transferred out, and 14 (8%) are still on treatment. Thirteen patients (7.5%) died, and the outcome of three patients was not documented.

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KEYWORDS

Tuberculosis; tuberculosis management unit; pulmonary; extra-pulmonary tuberculosis; treatment outcome; children; Sudan.

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INTRODUCTION

Tuberculosis (TB) is one of the major hazards to communities in the developing countries [1]. The World Health Organization (WHO) estimated that 9 million persons are infected yearly in developing countries with an estimated mortality of 2 million [1-3] and 19%-43.5% of the population in the world are affected by Mycobacterium tuberculosis [4]. TB usually has non-specific symptoms and signs and hence diagnosis is challenging [5]; however, technology successfully addresses this issue [5,6]. The usual complaints are low or high grade fever, cough or running nose and majority of cases have pulmonary tuberculosis (PTB); however, a third of patients developed extra pulmonary tuberculosis (EPTB) [7]. There is great variation in clinical presentation across different age group. Whereas in pre-school age and adolescents symptoms and signs are usually exciting, no symptoms and signs may occur among school age children [7,8]. On the other hand, great number of children with positive radiological findings, have symptoms or signs, and are diagnosed only during tracing process [7]. In fact, radiology in children shows clear lymphadenopathy but less parenchymal infiltration [9]. Since the positivity of culture of gastric aspirate is insignificant, culture is not needed to make a diagnosis; and suggestive symptoms, signs, positive skin test and positive radiological changes with known contact are enough to start treatment in children [7,10]. We conducted this study to determine the clinical presentations and risk factors of childhood TB, identify the radiological findings and laboratories investigations, and explore the association of age with type of TB and the treatment outcome.

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MATERIALS AND METHODS

This is a retrospective cross-sectional hospital based study, which was conducted at Mohamed Alamin Hamid Pediatric Hospital TB management unit from January 2017 to December 2018. Mohamed Alamin Hamid Pediatric Hospital is a general paediatrics hospital in Omdurman, Khartoum State. It has 320 beds with neonatal intensive care unit, pediatric intensive care unit, infectious diseases word and renal dialysis unit; as well as referral clinics for TB, asthma, sickle cell disease, human immunodeficiency virus (HIV) infection and renal diseases. The hospital serves population from Omdurman city and from all other states and different parts of Sudan. We included any child from birth to18 years with TB, who agreed and their care giver agreed to be part of the study, after full explanation of the study purpose. Data about the main study variables (classification of pulmonary versus extra-pulmonary and treatment outcome) was extracted from the patients records using specially designed data collection sheet. The patients were classified and their treatment outcome was recorded as per WHO guidelines; patients with incomplete records were excluded. Secondary data was extracted from the patient’s records and then re-entered into a predesigned data collection form.

Statistical analysis

All collected data were cleaned, entered and analyzed using Statistical Package for the Social Sciences version 24 evolving into descriptive statistics in term of frequency tables with percentages and graphs. Means and standard deviations were presented with relevant graphical representation for quantitative data bi-variable analysis to determine the associations between the main outcome variable (disease outcome) and the other relevant factors; with Chi-square test (for categorical variables) and t- test (quantitative variables). p value of 0.05 or less is considered to be statistically significant.

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RESULTS

A total of 174 patients were enrolled in this study. The majority of patients’ ages ranged from 5-17 years (111, 63.8%). Most of the patients were males (92, 52.9%) and (142, 81.6%) resided in Khartoum State (Table 1).

Regarding the clinical presentation of the studied population (Table 2), prolonged fever was the most common presenting feature in 170 (97.7%), followed by weight loss in 139 (79.9%), cough in 125 (71.8%) and lymphadenopathy in 103 (59.2%).

The specific investigations done to the studied group was sputum for acid alcohol fast bacilli (AAFB) GeneXpert test. The GeneXpert test was done for 149 (85.6%) patients, and from this number only 20 were positive. The Mantoux skin test was done for the entire studied group, 25 (14.4%) were negative, 93 (53.4%) were borderline and 56 (32.2%) were positive. The erythrocyte sedimentation rate (ESR) was done for all patients; in 168 (96.6%) it was more than 40 mm/hour, 5 (2.9%) had their ESR between 20 and 40 mm/hour, and it was less than 20 mm/hour in only one.

Table 1. General characters of the studied group.

Variable	Frequency	Percentage
Age
5 and less	63	36.2
>5-17	111	63.8
Gender
Male	92	52.9
Female	82	47.1
Residence
Khartoum State	142	81.6
Outside Khartoum State	32	18.4
Risk factors
History of contact	105	60
Not vaccinated	33	19

Table 2. Clinical presentations.

Clinical presentation
Variable	Frequency	Percentage
Fever	170	97.7
Weight loss	139	79.9
Cough	125	71.8
Sweating	78	44.8
Fatigue	80	46.0
Convulsion	3	1.7
Liver enlargement	9	5.2
Splenomegaly	6	3.4
Ascites	8	4.6
Lymphadenopathy	103	59.2
Hemiplegia	1	0.6

Fine needle aspiration (FNA) cytology of lymph nodes was done for 90 patients, and was suggestive of TB in 41 (45.6%). Only 41 (23.6%) of the studied group were screened for HIV, and all of them had negative results.

The opacity and hailer parenchymal shadows were the most presenting radiological features in almost half of the patients (83, 47.7%). Other findings included hilar parenchymal shadow in 18 (10.3%), opacity in 18 (10.3%), lung collapse in 3 (1.7%), pleural effusion in 3 (1.7%), features of miliary TB in 2 (1.1%), cavity in 1 (0.6%) and in 1 (0.6%) of those selected for chest X-rays the scan was normal. In 45 (25.8%), chest X-ray was not done. The X-ray findings are shown in Figure 1.

Regarding the pattern of TB in the studied group (Figure 2), we found that the majority 107 (61.5%) had PTB. Tuberculous adenitis affected 38 (21.8%), gastrointestinal tuberculosis (GITB) was in 11 (6.3%), TB meningitis in 7 (4%), Pott’s disease of spine in 6 (3.4%), miliary TB in 2 (1.1%) and other types of TB were in 3 (1.7%).

Figure 1. Distribution of chest X-ray finding among 174 studied participants. NO, number; %, percentage.

Figure 2. Distribution of PTB and EPTB among the studied participants (n = 174). GITB, gastrointestinal tuberculosis; TB, tuberculosis; TB adenitis, tuberculous adenitis; TB meningitis, tuberculous meningitis.

The correlation between the age, treatment and the outcome (Table 3) revealed that the prognosis is better in the age group between 5 and 18 years compared to those who were less than 5 years, with significant statistical differences in retreatment after default and in those who completed treatment with cure.

Table 3. Correlation between the age, treatment and the outcome.

Outcome	Age		p value
	Less than 5 years	5-18 years
Death	8	5	0.405
Default	8	12	0.371
Not documented	1	2	0.564
On treatment	5	9	0.285
Retreatment after default	1	5	0.000
Transferred out	2	9	0.000
Treated (completed/cured)	38	69	0.003

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DISCUSSION

In our study, the majority (111, 63.8%) of patient’s age ranged between 5 and 17 years. This may reflect the uncertainty of symptoms in younger patients and difficulties of confirmatory investigations. The other factors contributing to this result is probably that the older children are more mobile in community than the younger, so they had a big chance to contact with diseased adult patients and their peers. These findings are in agreement with other local (Sudan) and regional studies [11-13].Most of the patients were males (92, 52.9%), which is comparable to other studies done in Sudan [11], South Africa [14] and Pakistan [15]. However, our study differs from that done in Iran where female patients were the majority [16]. It is difficult at this age to explain this gender differences.

The general signs of fever, weight loss and lymph-adenopathy were similar to the study done in Sudan [11], and other international studies in Nepal, Turkey and Iran [12,16,17]. Signs of EPTB such as paralysis, convulsions, ascites, hepatomegaly and splenomegaly were similar to the study done in Izmir, Turkey [17]. The chest X-ray findings is in agreement with the study done by Verma et al. [18] in India and the study done in developed countries by Tomà et al. [19].

In our study, the sputum for AAFB was positive in only 20 (11.5%) which is comparable to that reported in previous local studies [11,20]. The Manteux test showed induration in our cases less than that reported in Turkey [17], Nepal [12] and Philippine [21]. Whether these differences are related to coexisting infection in our context needs further work up.In our study, the ESR was significantly raised (more than 40 mm/hour) in 168 (96.5%). This was similar to studies done in Nepal [12] and Turkey [17]. We found that the FNA from the lymph nodes was suggestive of TB in 41 (45.6%) of patients. In the study done in Nepal [12], there were five children with lymph node TB and FNA was diagnostic in all of them. We can conclude from both studies that this procedure can be considered as a helping tool in diagnosis.

In almost two-thirds (61.5%) of our cases the diagnosis was PTB, which is similar to previous studies in Sudan [11,20]. Regionally in Nigeria [22], PTB was seen in 58 (76.3%) which is similar to our findings. In a study from sub-Saharan Africa Congo [22], 159 (56.1%) patients had EPTB which is higher than in our study.Again, the study done in Turkey [17] showed that 92 (78.6%) of the cases had PTB and 25 (21.4%) had EPTB, which is similar to our findings. In Delhi, Dhaked et al. [23] found that EPTB (70.2%) was almost three times more prevalent than pulmonary. The Nepal study [12] found the EPTB (59.38%) to be more common than PTB (40.62%), and these results are not similar to our result. These differences in occurrences of PTB and EPTB may be due to age distribution in studies, presences of other co-morbidities and efficacy and availability of diagnostic methods. TB cases are primarily pulmonary and are easier to diagnose than extra pulmonary, which requires high index of suspicion. The majority of studies show that PTB was more common than EPTB, and the non-specific symptoms of EPTB make its diagnosis more difficult and missed in younger patients.

The commonest type of EPTB was tuberculous lymphadenitis (38, 21.8%). In sub-Saharan Africa in Kinshasa [22], the EPTB cases included 118 (74.2%) of cases of peripheral lymphadenitis, 11 (6.9%) cases of pleural effusion, 8 (5.0%) cases of meningitis, 6 (3.8%) cases of vertebral TB, 5 (3.1%) cases of abdominal TB, 4 (2.5%) cases of military TB and pericardial TB and 3 (1.9%) cases of osteoarticular TB. Also in a study done in Delhi [23], the commonest site involved in approximately two-thirds of EPTB cases were lymph nodes (72.7%), which is similar to our study. Other types of TB we found were as follows: GITB 11 (6.3%), TB meningitis 7 (4.0%), Pott’s disease 6 (3.4%) and military which was the least one 2 (1.1%); in addition to others 3 (1.7%). All these results were similar to the above studies. In the study in Nepal [12], pleural effusion (39.47%) and abdominal TB (26.31%) were the most common types which were different from our study findings. Lotfian et al. [16] in Iran showed pleural TB to be more common, which is different from our study. The majority (94, 87.9%) completed their treatment and 13 (12.1%) with smear positive results were cured. This is considered as a favorable outcome and similar to a previous study done in Sudan by [11] where the cure rate was (76.5%). In study done in Nigeria [13], 51 (67.1%) completed treatment which is less than in our study, and 12 (15.8%) were cured which were more than in the present study.Defaulters were 20 (11.5%) which is similar to a previous study done in Sudan by Osman et al. [20] where they were 17.3%. Regionally in Nigeria [23], the defaulters constituted 1.3%, which is less than in our study. In Iran [17], the defaulters were more in adults where 54 (39%) adolescents were identified. This is more than in our study. Thirteen patients (7.5%) died which is similar to a previous study done in Sudan [11] and higher than the study done in Nigeria [23] where the deaths constituted 3.9%. The EPTB occurred in 52% of females which is similar to previous studies [19-21].

Limitations of the present study included its retrospectives nature leading to missed information and follow up data. Also, the study did not cover the social and psychological aspects, which are considered an effective factor in the outcome and clinical presentations. The determination of contacts and their distribution was difficult to assess in our methodology.

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CONCLUSION

The most affected children were male patients aged above 5 years. EPTB was the most common presenting type, especially tuberculous adenitis with favorable outcome among the study group, as patients who completed their treatment successfully were approaching 90%.

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RECOMMENDATIONS

Improving the notification system and increasing researches in alternatives investigative tools.

• The adolescents need more focusing in their adherence to follow up and treatment and transitional clinic with medicine department is needed.As adults are the main source of infection, a specialised center for psychological support to deal with stigma of the disease is needed.
• Improving the knowledge about TB transmissions and importance of screening.

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CONFLICT OF INTEREST

The authors declare that there is no conflict of interest regarding the publication of this article.

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FUNDING

None.

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ETHICAL APPROVAL

Ethics clearance and approval for conducting this research were obtained from the Ethics Committee of the SMSB and the Khartoum State Ministry Health Research Department. Informed consent for participation and publication was obtained from the guardians of the patients. Confidentiality was maintained at all levels.

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