Reporting system for tuberculosis patients in

Khartoum State: assessment of completeness and estimation

of the number of unreported cases using the capture-recapture
method.
2010

Summary:
Introduction: Complete reporting of tuberculosis (TB) cases is critical for programme
planning and evaluation, and also for advocacy and is also necessary to accurately interpret
disease incidence or to make national and international comparisons.
Objective: To assess completeness of reporting of TB cases and to estimate the number of
unreported TB cases in East Nile Locality, Khartoum State.
Methodology: The reporting of new pulmonary tuberculosis cases is based on Tuberculosis
Management Units’ (TBMUs) registers. This study used the Tuberculosis Laboratory registers
as alternative sources to assess the completeness of the routine reporting using both the
inventory and the capture-recapture methods. New Positive smear pulmonary tuberculosis
cases from the tuberculosis laboratory registers were matched against new pulmonary
tuberculosis cases appearing in the TBMUs tuberculosis register. The cross matching was
done using an identifier composed of the patient name, age and address.
Results: According to the inventory method the completeness of reporting was 90.3%, while
according to the capture-recapture method the completeness of reporting was around
32.3%. Using the capture-recapture method, the number of missing pulmonary tuberculosis
cases and the number of missing smear positive pulmonary tuberculosis cases were found to
be 847 and 314 respectively .The study showed that around two thirds of the new
pulmonary tuberculosis cases had negative sputum smear tests. The study also showed that
out of a total of 240 suspected TB cases sent for sputum smear examination only 27.9% had
a positive result.
Conclusion: The current reporting of tuberculosis cases is still below the recommended level
and interventions, such as installing a tracing system for suspected cases with positive
sputum smear in addition to involving the private sector in the reporting process are
needed. It was also noticed that laboratory workers are over-burdened by workload, and
this necessitate the development of local clinical algorithms to assist health workers in
rightly recognizing suspected TB cases.

0
Introduction and Justification
Through the implementation of the DOTS strategy, the World Health Assembly planned to
combat tuberculosis by setting the goals of 70% case detection of infectious TB and
treatment of 85% of these by the end of 20051 (Xu et al 2007).
Since 2000, the United Nations millennium development goals (MDGs) also provide targets
for TB control. The indicators for TB have been formulated in ‘to halve TB prevalence and
death rates between 1990 and 20152.
Both the WHA and the MDGs require epidemiological information about the burden of TB to
be able to assess progress towards the targets2.
In Sudan, tuberculosis (TB) is considered as a public health priority. The country is
shouldering 15% of the TB burden in the Eastern Mediterranean Region, and is one of the
nine countries contributing 95% of TB burden in the region in 2010.3
The prevalence is 209 cases per 100,000 of the population, with 50,000 incident cases during
20094.
From 2000 to 2010, the case notification rate decreased from 41/100,000 to 25/100,000 3,
indicating a weak surveillance system.
The estimation of the notification rate depends on the number of reported TB cases to the
TB control programme which is usually derived from routine surveillance data. Accurate
routine surveillance would provide direct and continuous information, however, in resource
–limited countries with a considerable burden of TB, the surveillance records are often weak
and incomplete or even non-existent2,5. The under-reporting of TB cases will result in low
case notification even in the presence of effective case finding.
Complete reporting of TB cases is a critical for programme planning and evaluation, and also
for advocacy6,7 and is also necessary to accurately interpret disease incidence or to make
national and international comparisons7, therefore it is essential that patient data are
collected and reported regularly to be analyzed and used for decision making. 6
The completeness of TB reporting of TB in Sudan has not yet been assessed, and the aim of
this pilot study, the first of its kind was to assess completeness of reporting of TB cases and
to estimate the number of missing TB cases in East Nile Locality in Khartoum State.

Study design and setting:

This was a descriptive, retrospective facility based study of TB patient’s records during 2010.
Khartoum State, the capital, is composed of 7 localities, where a locality represents the most
peripheral administrative unit. East Nile locality was selected conveniently for this pilot
study. The population of the locality is homogeneous and stable. In East Nile locality,
Khartoum State Tuberculosis Control Programme (KSTBCP) services are provided through
seven Tuberculosis Management Units (TBMUs) situated at seven health centers.

Symptomatic patients reporting to (TBMUs), are screened for tuberculosis through sputum
microscopy for acid fast bacilli. Further investigations to confirm the disease in negative
sputum smear cases include sputum culture and chest X-ray. Confirmed TB cases are then
referred for treatment. Symptomatic cases reporting to Non - TBCP governmental health
facilities are to be referred to TBMUs for further management.

1
The process of registration of TB patients starts when they attend the TBMU as suspected
cases.
Suspected TB cases are registered in TB suspect register and then referred to the laboratory
for confirmatory investigations. The laboratory technician record all suspected TB patients in
the laboratory TB register along with their investigation results. Confirmed TB cases then
receive a TB treatment card that is filled with background information about the patient,
diagnosis, and treatment. Using this patient treatment card, a statistician fills the TBMU TB
register and submits it to the locality level. At the locality office a TB locality register is
compiled from all TBMUs in the locality and submitted to the Ministry of Health. The study
assessed the completeness of this locality TB register.
Case definition :

TB cases were defined as all new patients registered with the TCP between 1 January 2010 and 31 December
2010.

Data collection:
The completeness of reporting was done through two methods; the active case-finding in
additional data sources (inventory method) and the capture –recapture methods.

Data were obtained from tuberculosis registers at all seven TBMU at East Nile Locality that
are the base for the monthly reports submitted to the Ministry of Health during 2010.
Laboratory registers for TB patients submitting specimens for diagnosis were used for case
ascertainment. Only data about pulmonary TB patients diagnosed for the first time (new
cases) were used. Data about re-treatment cases including returning defaulters, and extra
pulmonary tuberculosis cases were excluded. From laboratory TB registers, TB patients
submitting a specimen for follow-up were excluded.

From the tuberculosis registers at the TBMUs, data about TB patients were transferred into
pre designed line-list (list A) . This comprised the reference list of TB patients. From the
laboratory tuberculosis registers, data were transferred into a line-list (list B).
The TB patient data recorded in the line-lists ( A and B) included the following: Patient
number, name, Gender, Age, Result of sputum microscopy, date of diagnosis and Patient
address. Assessment of list overlaps was performed through record linkage, using the fixed
combination of the full name in Arabic script, gender, age, date of diagnosis and address as
main identifiers. Arabic names were used to minimize undermatching due to inconsistent
recording , because they are reportedly less prone to pronunciation and spelling errors due
to the absence of homonyms in the Arabic language.
Patients who were found to be previously reported through routine surveillance and
unreported patients with positive sputum microscopy identified from laboratory registers
were assumed to represent true pulmonary TB cases

3.1. Data analysis:

The data were entered into Microsoft Excel spread sheet and frequencies were computed.
Completeness estimation through active case-finding in additional data sources (inventory
method):
The observed completeness of the locality TB reporting was defined as the number of locality TB registered
cases divided by the case ascertainment, i.e., the total number of patients observed in at least one register,
expressed as percentage
Completeness estimation using the "capture-recapture" technique :

2
The process followed the technique described in a WHO surveillance workshop. 8
The other source of data used with the reference line-list (TBMUs registers) was the
laboratory register. Cases from both sources were cross-checked and the matching cases
were identified. This resulted in a 2x2 table where information for 3 cells was known. The
missing cases, i.e. those that were on neither list (field shaded in gray; Tab.1), were
calculated as follows:

Table I: 2x2 table of data from two independent sources A and B, where TB cases are
documented. Field with grey cases: cases that are missed by both sources.

Alternative list from laboratory registry (list B)

Identified Not identified
Reference list-line Identified Common to A and B Only in A
from TBMUs registry Not identified Only in B On neither list
(list A) (missing TB cases)

The formula to calculate the total number of cases was conceptually derived as follows. The
probability P that a cases was identified in both systems was: P(A and B) = P(A) x P(B) (when
data sources are independent), so that:

and hence:

The more exact formula is:

The 95% confidence interval is:

The number of missing cases is then:

3
When A is the usual source of notifications the case detection rate was estimated as:

and the estimated multiplier for notification data in that context is:

Multiplier =

3.2. Ethical consideration:

The proposal was approved by the Research Advisory committee – Khartoum State Ministry
.of Health

4
Locality TB register Laboratory register
)n = 426( 405 21 )n = 67(
46

Figure 1: Distribution of observed number of new tuberculosis cases (N = 472) in East Nile
locality, Khartoum State, Sudan 2010.

A total of 472 TB cases were identified in in the registers of the 7 TBMUs in East Nile
locality. Figure (1) shows their distribution over the locality TB register and laboratory
register.
Four hundred and twenty six patients were registered in the locality TB register (observed
completeness 90.3%). The laboratory diagnosed 67 patients; 21 patients (4.4%) were known
to both locality TB and laboratory registers, but 68.7% of laboratory register patients were
missing from locality TB register (not notified)

5
 Laboratory register
150 21 46 )n = 67(
Locality TB register
)n 171(

Figure 2: Distribution of observed number of positive smear new tuberculosis cases (N =

227) in East Nile locality, Khartoum State, Sudan 2010.

A total of 227 positive smear new TB cases were identified in in the registers of the 7 TBMUs
in East Nile locality. Figure (2) shows their distribution over the locality TB register and
laboratory register.
One hundred and seventy one were registered in the locality TB register (observed
completeness 75.3%). The laboratory diagnosed 67 patients; 21 patients (9.3%) were known
to both locality TB and laboratory registers, but 68.7% of laboratory register patients were
missing from locality TB register (not notified)

Table (2): Estimation of the completeness of reporting of new pulmonary TB

cases - East Nile Locality Khartoum state 2010(capture-recapture method).

    List B = laboratory registry  

         
    Identified Not identified  
List A = 21 (common to
Identified
both lists)
405 426
Referenc
e list-line
from Not 46 (unreported 847 (missing 893
TBMUs identified TB cases) TB cases)
registry
67 1252
1319 (total
    TB cases)

Table (2) shows the process of estimating the completeness of reporting using the capture-
recapture method taking into account all new pulmonary TB cases regardless of result of
sputum smear. The 2X2 table shows data from two sources (list A the routinely reported
cases and list B composed of positive sputum smear cases from laboratory TB registers). The

6
table shows that cases common to both lists are 21, and cases from list B not appearing in
.list A (unreported cases) are 46
:The formula to calculate N, the total number of cases using the capture recapture method

Where:

N is the Total number of TB cases from all sources (A and B)

NA is the number of routinely reported cases (list A)

NB is number of positive sputum smear cases form laboratory TB registers (list B)

NAB number of cases common to list A and list B

Total = (426 +1)( 67+1)/ (21+1) -1 = (427)(68)/22 -1 = 1319 cases

The number of missing cases (by both sources) is then:

= 1319 – (426 + 67 -21) = 847 cases

The level of completeness of reporting (case detection rate) was estimated as:

= 426 /1319 = 32.3 %

7
 Table (3): Estimation of the completeness of reporting of new positive smear
pulmonary TB cases - East Nile Locality Khartoum state 2010(capture-recapture
method).
    B = laboratory register  
         
    Identified Not identified  
21 (common
A= Identified
cases)
150 171
Notification
Not 46(unreported 314 (missing
system
identified TB cases) TB cases)
360 (total TB
67 464
    cases)

Table (3) shows the process of estimating the completeness of reporting using the capture-
recapture method, taking into account only positive smear new TB cases. The 2X2 table
shows data from two sources (list A the Routinely Reported positive TB cases and list B
composed of positive sputum smear cases from laboratory TB registers). The table shows
that cases common to both lists are 21, and cases from list B not appearing in list A
.(unreported TB cases) are 46
:The formula to calculate N, the total number of cases using the capture-recapture method

Where:

N is the Total number of TB cases from all sources (A and B)

NA is the number of routinely reported positive smear cases (list A)

NB is number of positive sputum smear cases form laboratory TB registers (list B)

NAB number of cases common to list A and list B

Total = (171 +1)(67+1)/ (21+1) -1 = (172)(68)/22 -1 = 360 cases

The number of missing cases (by both sources) is then:

= 360 – (171 + 67 -21) = 314 cases

The level of completeness of reporting (case detection rate) was estimated as:

8
 = 171 /360 = 47.5%

Discussion
Ongoing evaluation of disease reporting completeness will continue to be a necessary part of
public health surveillance, enabling more accurate interpretation of surveillance data for
disease control and prevention.7,9
This study attempted to estimate the degree of completeness of reporting of pulmonary
tuberculosis cases from one of Khartoum State localities to the central level. Two methods,
both using the laboratory tuberculosis register as an alternative source of data, were
applied; the inventory method yielded a level of completeness of reporting of 90.3%, while
according to the capture-recapture method the level of completeness was only around
32.3% for all new cases, and 47.5% for new sputum smear positive cases. The discrepancy
between the two findings is due to the fact that the inventory method takes account only of
cases from the alternative source of data not reported through the routine surveillance
system. The capture recapture method on the other hand estimates the number of cases
missed by both sources of data and uses it for estimating the degree of completeness of
reporting. This level of completeness is low when compared with that of other countries.
Studies using the capture-recapture method found the level of completeness to be 97.9% in
Taiwan10, 73% in Pakistan11, 72% in Egypt5 and 71% in Yemen12.

This problem of underreporting is not limited to developing countries; a study in the United
States of America reported level of completeness of reporting as low as 40%, 7 while in the
United Kingdom the proportions of unreported tuberculosis cases ranged from 7% to 27 %. 13
In East Nile locality many reasons might have led to not reporting TB cases in the routine
surveillance registers. After being diagnosed by a positive sputum smear, some of the TB
cases might have sought care from sources that do not report TB cases, such as the private
sector. This highlights the importance of finding innovative methods to include the private
sector in the tuberculosis reporting system.
Also TB cases might have sought care from sources, public or private, outside the locality or
the state, and thus were missed from the locality registers. In addition to that some cases
might have not returned to receive the results of the sputum smear test, or even after
receiving the confirmation of the diagnosis, some TB cases did not seek further management
of the disease. The implication is that potentially infective cases are not treated and pose the
hazard of transmitting the infection in community. Recording full contact information of
suspected TB cases will facilitate tracing of those with positive smear tests if they do not
report to their respective TB treatment centers.
Another reason for underreporting might be that some TB cases do not present themselves
to the statistician at the TB treatment center for recording.
Health care providers may also be the reason behind underreporting. The systematic
collection of data and reporting are often regarded by programme staff as tedious and time-
consuming tasks, especially if the purpose of the activities is not clear. 6. Also insufficient
reward for reporting or penalty for not reporting, are some of the reasons for not reporting
TB cases.7
In all instances the consequences of no reporting are serious. Under-notification leads to an
underestimation of the disease burden and hinders implementation of appropriate
prevention and control strategies9,13. Cases not notified to the public health system have a

9
higher risk of morbidity and mortality and an increased risk of multi-drug resistant
tuberculosis as the result of sub-optimal treatment. Contacts of un-notified cases are also at
risk if they are not screened and treated appropriately for active or latent disease 13.
One striking finding of this study was that, around two thirds of the reported new pulmonary
TB cases were smear negative cases. This means that health care workers depended on tools
other than sputum smear on the diagnosis of TB cases. Although this does not impact
directly on the completeness of reporting it does impact on the sensitivity of the surveillance
system of detecting and hence reporting true TB cases, giving a false picture of the true
burden of the disease. There is little current evidence of effectiveness of the clinical
guidelines and algorithms in diagnosing TB. For clinical guidelines and algorithms to be valid
in detecting TB cases, local epidemiology, such as the prevalence of HIV, tuberculosis, and
other pulmonary disorders, and antibiotic-resistance patterns, need to considered before
implementation14,15.
Conclusion: The current reporting of tuberculosis cases is still below the recommended level
and interventions, such as installing a tracing system for suspected cases with positive
sputum smear in addition to involving the private sector in the reporting process are
needed.

3.1. Limitation of the study:

The study depended on secondary data from patients and laboratory registers which were
not complete and accurate and thus affected the process of matching of cases from different
.sources
The assumption that data sources used for the capture –recapture process are independent
is not fulfilled; this means that the total number of cases is underestimated. However, the
estimate will still be closer to the true number than when the unique cases of the two
.sources are simply added up

Conclusions:
The completeness of reporting of new pulmonary tuberculosis cases, using the inventory
method and taking the laboratory tuberculosis registry as an alternative source of data was
found to be 90.3%.

Using the capture-recapture method to estimate the number of missing new pulmonary
tuberculosis cases and the missing new smear positive pulmonary tuberculosis cases the
completeness of reporting was found to be 32.3% and 47.5% respectively. In both instances
the laboratory tuberculosis registry was taken as an alternative source of data.

Using the capture-recapture method, the number of missing new pulmonary tuberculosis
cases and the number missing new smear positive pulmonary tuberculosis cases were found
to be 847 and 314 respectively.

Using the capture-recapture method, the number of all new pulmonary tuberculosis cases
and the number of all new smear positive pulmonary tuberculosis cases were estimated to
be 1319 and 360 respectively.

The proportion of suspected tuberculosis cases submitting sputum samples for examination
who proved to have positive results was only 27.9%

10
Recommendations:

 Improving the reporting of tuberculosis cases to the central level needs

more investigation identify the reasons behind the underreporting,
however, the following interventions can nevertheless improve the current
situation:

o Involving the private sector in the reporting system for

tuberculosis patients through application of interventions such as
rewarding or linking issuance of private practice licenses with
compliance to reporting TB cases.

o Developing a tracing system for suspected TB cases who have

positive sputum smear tests to insure that they report for
treatment.

 Improving the capabilities of health workers in identifying suspected TB

cases who need further investigations to confirm the disease, through the
development of clinical guidelines and algorithms that respond to the local
situation.

11
References:

Bastian R CI,” A review of the diagnosis and treatment of smear-negative

pulmonary tuberculosis”, International Journal of Tuberculosis and lung
Diseases, 2000, vol 4(2), pp.97–107

Begum V, van der Werf M J, Becx-Bleumink M and Borgdorff M W,’Do we

have enough data to estimate the current burden of tuberculosis? The
example of Bangladesh, 2007,Tropical medicine and international health’ vol.
12 ( 3), pp. 317–322

Driver CR, Braden CR, Nieves RL, Navarro AM, Rullan J V, Valway SE, McCray
E,” Completeness of Tuberculosis Case Reporting, San Juan and Caguas
Regions, Puerto Rico,1992” Public Health Reports, 1996 , Vol.3

Doyle T J, Glynn M K, and Groseclose S L, Completeness of notifiable

Infectious Disease Reporting in the United States: An Analytical Literature
Review, 2002, American Journal of Epidemiology, Vol. 155, (. 9)

English R G, Bachmann MO, Bateman E D, Zwarenstein M F, Fairall L R,

Bheekie A, Majara B P, Lombard C, Scherpbier R and Ottomani SE,
”Diagnostic accuracy of an integrated respiratory guideline in identifying
patients with respiratory symptoms requiring screening for pulmonary
tuberculosis: a cross-sectional study”, BMC Pulmonary Medicine 2006, vol.
6:22

Kasse Y, Jasseh M, Corrah T, Donkor SA, Antonnio M, Jallow A, Adegbola RA

and Hill PC 2006, " Health seeking behaviour, health system experience and
tuberculosis case finding in Gambians with cough" , BMC Public Health, vol. 6
(143 ) the article is available from http://www.biomedcentral.com

Khartoum State Tuberculosis control Programme, annual Statistical Report,

2007

Laska E M ,’ The use of capture–recapture methods in public

health,2002,Bulletin of the World Health Organization , vol. 80 (11)

Morrison A,’ Capture-recapture: a useful methodological tool for counting

traffic related injuries?’ 2000, Injury Prevention vol.6, pp.299–304

Pillaye J and Clarke A,’ An evaluation of completeness of tuberculosis

notification in the United Kingdom’,2003,British Medical Journal Public Health,
vol., 3(31)

Siddiqi K, Lambert M L, and Walley J, ‘Clinical diagnosis of smear-negative

pulmonary tuberculosis in low-income countries: the current evidence”,

12
Lancet Infect Diseases, 2003; vol.3, pp. 288–96

Tilling K and Sterne J A C,’ Capture-Recapture Models Including Covariate

Effects, American Journal of Epidemiology, 1999, Vol. 149, ( 4)

WHO, 2008, Global tuberculosis control - surveillance, planning, financing,

published report, Geneva

WHO, tuberculosis Surveillance and monitoring,1991, report of a WHO

workshop, tuberculosis unit, division of communicable diseases, Geneva

Xu B, 2006 " Access to tuberculosis care in rural China – comparing the

impact of alternative control projects" Karolinska University Press, Stockholm,
Sweden.

Xu B, Diwan VK, and Bogg L 2007," Access to tuberculosis care: What did chronic
cough patients experience in the way of healthcare-seeking?", Scandinavian Journal
of Public Health, vol. 35, pp. 396 – 402

13
6. Financial Report:
S Item Unit Cost Budget /
No. SDG
Preparation of the 200 sheets * .5 SDG 100
questionnaire
Fieldwork 1 field supervisor *7 days * 100 700
SDG

Transportation 1 car * 6 days * 100 SDG 700

Data processing and
analysis:
Office editing 2 editors * 5 days * 100 SDG 1000
Data entry 1500
Data analysis 3000
Report writing 3000
Total 10000

Many studies have been conducted throughout the world to assess the degree of reporting
completeness of tuberculosis patients. Researchers usually measure reporting completeness by dividing
the number of cases reported to public health authorities by the total number of cases identified
through active case detection and the use of supplemental data sources such as hospital and laboratory
registers (Doyle et al 2002). Reporting Completeness levels ranged from 65% to 99% in some United
States of America, and from 23% to 93% in the United Kingdom(Doyle et al 2002; Pillaye and Clarke
2003)
After documenting the level of under-reporting, some authors went further to estimate the number of
unreported TB cases using the capture-recapture method. This method Capture-recapture has
traditionally been employed in biometrics, particularly in the estimation of animal populations. Recently,
the technique has increasingly been adopted in health studies of human populations to generate more
accurate rates of disease and disability. This involves estimating the number of cases in a defined
population using multiple sources of information, assuming that each source alone may under-count the
population (Tilling and Sterne 1999; Morrison 2000 ; Laska 2002)).
Several authors have described reasons for failure of health-care providers and laboratories to report
notifiable Diseases including TB. The systematic collection of data and reporting are often regarded by
programme staff as tedious and time-consuming tasks, especially if the purpose of the activities are not
clear (WHO 1991). Other reasons include a lack of understanding of how or to whom to report, an
assumption that someone else will report the case, intentional, and insufficient reward for reporting or
penalty for not reporting(Doyle et al 2002).

14
Annex 1

Line-list table form1

Patient S.No Pt identifier .availability at lab reg

1. Yes
2. No

15
 Annex 2

Line-list form2

To collect data from laboratory registers

.Patient S. no Patient identifier Sputum smear result
Positive .1
Negative .2

16
17