Hindawi Publishing Corporation

ISRN Pulmonology
Volume 2013, Article ID 486507, 5 pages
http://dx.doi.org/10.1155/2013/486507

Clinical Study
Factors Influencing Sputum Conversion among Smear-Positive
Pulmonary Tuberculosis Patients in Morocco

Khalid Bouti, Mohammed Aharmim, Karima Marc, Mouna Soualhi, Rachida Zahraoui,
Jouda Benamor, Jamal Eddine Bourkadi, and Ghali Iraqi
Respiratory Department, Moulay Youssef University Hospital, UM5S, 10000 Rabat, Morocco

Correspondence should be addressed to Khalid Bouti; khalid.bouti@um5s.net.ma

Received 12 May 2013; Accepted 13 June 2013

Academic Editors: S. L. Chan, Y. Dobashi, and T. J. Kelley

Copyright © 2013 Khalid Bouti et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Background. Sputum smear-positive pulmonary tuberculosis patients expel infectious viable bacilli for a period following the
commencement of treatment. Objective. To determine the time to sputum smear conversion and study the factors influencing
it. Design. A prospective study was undertaken at our hospital in Rabat over a six-month period on a cohort of 119 sputum smear
positive patients. Patients were followed up fortnightly. At each followup, specimens were collected and processed for microscopy
using standard protocol. Results. 96.6% of our patients completed the study (4 deaths). Sputum conversion rate was 42% after two
weeks, 73% after one month, and 95% after two months. Univariate and stepwise regression analysis showed that patients who had
high smear grading, miliary, and bilateral radiologic lesions were more likely to undergo delayed sputum conversion (𝑃 < 0.05).
Other factors were thought to influence sputum conversion but were not statistically proven in our study. Conclusion. Since viable
bacilli continue to be expelled for up to two months, infection control measures should be maintained for such a time. Patients with
high smear grading, miliary, and bilateral radiologic lesions need to be monitored more closely.

1. Introduction When SSP patients are initiated on multidrug antituber-

culosis treatment, there is a multifold reduction in bacillary
The World Health Organization (WHO) estimates that there load expelled in sputum [4]. Patients, who respond, are likely
are almost 13.7 milion people living with tuberculosis and that to become smear and culture negative during the course of
the disease kills more young people and adults than any other treatment. However, viable bacilli continue to be expelled for
infectious disease in the world. a period of time, during which they may continue to spread
In Morocco, the new cases of tuberculosis in 2008 were infection.
27000, and the incidence was 82/100000 people. Patients in It is expected that 80 to 90% of patients will undergo
our health system receive intermittent therapy with mul- smear conversion within two to three months of treatment
tidrug regimen based on directly observed treatment, short- [5]. Several factors have been identified that may delay the
course (DOTS). time to smear conversion. These include high initial sputum
Tuberculosis control aims to reduce the spread of the smear acid fast bacilli (AFB) grade, cavitatory lesion, uncon-
infection, and the most efficient method for preventing trolled hyperglycaemia/diabetes mellitus, old age, certain
transmission is the identification and cure of infectious ethnic initial treatment with less than four antitubercular
pulmonary tuberculosis patients [1]. drugs, and nonrifamycin-based treatment regimens [6].
Sputum smear-positive (SSP) pulmonary tuberculosis Infection control measures are recommended for all
patients are the most significant source of infection for sputum smear-positive patients to minimize the spread of
tuberculosis because, when they cough or sneeze, they infection.
expel droplet nuclei which carry infectious bacilli [2]. One Measures are to be maintained until noninfectiousness
untreated infectious tuberculosis patient is likely to infect 10 has been demonstrated. Demonstration of noninfectiousness
to 15 persons annually [3]. is best done by demonstration of culture conversion. The
2 ISRN Pulmonology

time required to report culture results and the availability Table 1: Sociodemographic characteristics and comorbidities of
of resources are limitations to the use of culture for the baseline population.
purpose of infection control. On the other hand, sputum
Number Percent 𝑃 value
smear microscopy, thought less sensitive than culture, can
be reported much earlier. Current recommendations include Sex
serial negative sputum smears for AFB before removal of Male 77 65% 0.02
infection control measures [7, 8]. Female 42 35%
In this background, it is essential to evaluate risk factors Age Group
such as age, smear grading, weight, and associated comorbid 10–20 10 8.4%
conditions like HIV infection and diabetes mellitus among 20–30 37 31.1%
TB patients that are likely to influence smear conversion. 30–40 24 20.2%
Although risk factors which influence smear conversion have 40–50 19 16% 0.14
been studied widely [9], there are no prospective studies on 50–60 16 13.4%
smear conversion in Moroccan patients.
60–70 9 7.6%
The present study was undertaken to determine the time
to smear conversion in Category I DOTS patients receiving >70 4 3.3%
uninterrupted therapy and to determine factors that prolong Smoking
smear conversion. Yes 43 36.1%
Smear conversion is defined as new smear-positive PTB No 61 51.3% 0.01
cases who became smear negative after a period of anti-TB Weaned 15 12.6%
treatment and are therefore no longer infectious (confirmed Comorbidities
by at least two consecutive negative sputum acid fast bacillus Diabetes 9 7.6%
(AFB)). Respiratory diseases 4 3.4%
HIV 1 0.8% 0.77
Others 10 8.4%
2. Study Population and Methods
This is a six-month prospective study. It was undertaken at
Moulay Youssef University Hospital, Rabat, Morocco. In this The goal and benefits of the study were explained to the
study, all new smear-positive pulmonary TB inpatients of our study participants, and oral informed consents were obtained
tertiary care hospital were enrolled from 1 January 2010 to 30 from the participants prior to enrollment.
June 2010. All the patients were consecutive ones.
For each patient enrolled, at least one culture was done 3. Results
to confirm the diagnosis and to exclude a drug resistant
tuberculosis. All patients received a four drug regimen From 1 January 2010 through 30 June 2010, 119 cases of smear-
(isoniazid, rifampicin, pyrazinamide, and ethambutol). positive tuberculosis were diagnosed, which included 77 men
When a patient was enrolled in the cohort, details of and 42 women. Patients were aged between 17 to 79 years. The
demographic, clinical and radiological findings, past history mean age for both men and women was 39 years. 96.6% of our
of tuberculosis, tobacco, alcohol, and drugs consumption, patients completed the study, four of our patients died during
BCG status, diabetes mellitus, renal diseases, and HIV coin- the study. They died of acute respiratory distress (2 cases),
fection were noted. septic shock (1 case), and hemoptysis lightning (1 case).
Patients were followed up fortnightly for up to 6 months The characteristics of the patients are given in Table 1.
or until they underwent smear conversion whichever was Of these patients, 88 (74%) had pulmonary disease alone,
earlier. At least two smear specimens were collected in each 8 (7%) had pulmonary and pleural disease, 15 (13%) had pul-
evaluation. monary and lymph node tuberculosis, and the 7 remaining
All expectorated and induced sputum specimens cases had pulmonary and another extrapulmonary location.
obtained by the microbiology laboratory for AFB smear were All cases were confirmed by culture, and no drug resistance
decontaminated with sodium hydroxide in combination with was detected.
N-acetyl-L-cysteine and processed in a standard manner. The rate of sputum conversion at the end of one month of
The Ziehl-Neelsen stain was used throughout the study. treatment was 73.1% (𝑃 < 0.01) while it was 95% (𝑃 < 0.05)
The smear grading was based on this classification: at the end of the second month.
negative (smear contains no AFB in 100 fields), 1+ (10–99 AFB Table 2 shows other characteristics of TB in the enrolled
in 100 fields), 2+ (1–9 AFB/field in at least 50 fields), and 3+ patients, while Table 3 shows patients undergoing smear
(>10 AFB/field in at least 20 fields). conversion.
Statistical analysis to determine factors that prolong time Smear grading (44.5% negativation in the 1st fortnight in
to conversion was done by univariate analysis and stepwise 1+/2+ group versus 12.1% in the 3+/4+ group; 𝑃 = 0.02),
regression analysis using SPSS 17.0 software. P value of <0.05 miliary (7.1% negativation in the 1st fortnight versus 57.1%
was considered as significant. Any patient unable to complete in the 4th fortnight or later; 𝑃 = 0.01), bilateral radiologic
the required followup was excluded from data analysis. lesions (26.9% negativation in the 1st fortnight versus 40.4%
ISRN Pulmonology 3

Table 2: TB features.
Characteristics All patients (𝑛 = 119) 𝑃 value
New cases, 𝑛 (%) yes/no 100 (84)/19 (16) 0.005
Radiological involvement, 𝑛 (%) unilateral/bilateral 50 (42)/68 (57.1) 0.56
Cavitation, 𝑛 (%) yes/no 42 (35.3)/76 (63.9) 0.06
Nodules and micronodules, 𝑛 (%) yes/no 101 (84.9)/17 (14.3) 0.01
Infiltrate, 𝑛 (%) yes/no 103 (86.5)/15 (12.6) 0.03
Smear grading, 𝑛 (%)
1–9 AFB/100 fields (1+) 8 (6.7)
1–9 AFB/10 fields (2+) 19 (16) 0.02
1–9 AFB/field (3+) 37 (31.1)
>9 AFB/field (4+) 55 (46.2)

Table 3: Cumulative patients undergoing smear conversion.

Smear conversion patients

Time 𝑃 value
Number % Cumulative %
1st fortnight 51 42,86 42,86 <0.001
2nd fortnight 36 30,25 73,11 <0.01
3rd fortnight 16 13,45 86,56 0.02
4th fortnight 10 8,4 94,96 0.03
8th fortnight 2 1,68 96,64 >0.05

in the 4th fortnight or later; 𝑃 < 0.01) were associated with patients continues. Studies have shown that nonconversion
longer smear conversion time. of positive smears at the end of the two months of treatment
There were no statistically significant differences in other is one of the strongest predictors for treatment failure [11–13],
evaluated variables, such as age, sex, weight, smoking, alco- although it is not a very reliable indicator because of its low
holism, addictions, respiratory diseases, diabetes mellitus, positive predictive value [14].
HIV infection, cavitations, TB contagion, previous TB dis- Indeed a positive sputum smear for AFB does not permit
ease, alternative anti-TB treatment, and related toxicity. one to know whether these are still viable bacteria or not
Multivariate logistic regression analysis indicated that after two months of antituberculosis treatment. To assess
all 3 significant variables from the univariate analysis were sputum sterilization, therefore, it is ideal to study cultures for
independently associated with delayed smear conversion mycobacteria at the end of the two months. However under
(smear grading 3+: OR 7.1, 95% CI 2.5–11.2; miliary: OR 8.8, programmed conditions, cultures for mycobacteria are not
95% CI 2.3–19.4; bilateral radiologic lesions: OR 13.4, 95% CI available under field conditions. Furthermore, conventional
1.8–55.6). results of culture on media would be available far too late
(after more than two months) to be useful [14].
Currently the duration of infectiousness after the initia-
4. Discussion tion of effective treatment is still a subject of discussion. From
our results it is shown that after two weeks of treatment about
The World Health Organization (WHO) recommends that 57.14% of the patients were still potentially infectious. This is
patients with previously untreated pulmonary TB receive a in contrary to the belief that patients become noninfectious
four-drug regimen during the two-month initial phase of after two weeks of standard treatment regimen. This finding
treatment that includes rifampicin. The overall rate of failure is in line with other results which have also shown that
or relapse (poor outcome) in patients receiving directly the conversion to a negative test and hence the loss of
observed treatment, short-course (DOTS) with a rifampicin- infectiousness of pulmonary tuberculosis patients during
containing regimen, is low [10]. therapy does not occur rapidly in all patients [15–17]. This
This study is a prospective assessment on TB cases reg- finding has implications to those countries which practise
istered and treated in a tertiary care Moroccan hospital. The patients’ isolation during the infectious period and are using
sample size (119) is relatively small for definitive biostatistical two weeks as a time which usually a patient is considered
conclusions but is close to some other studies. to become noninfectious. For example, in France and UK,
TB was suspected on the basis of symptoms, clinical guidelines indicate that the isolation of smear-positive tuber-
signs, and chest X-ray and confirmed by sputum smear culosis patients without risk factors for multidrugs resistant
examination. No case was confirmed by sputum culture. tuberculosis is generally only required for 2 weeks [18, 19].
The search for tools to estimate the duration of respira- Factors such as higher pretreatment smear grading, military,
tory isolation and to monitor the treatment of tuberculosis and bilateral radiographic involvement were associated with
4 ISRN Pulmonology

the delay of smear conversion. This applies to the univariate Supervised control of diabetes for two months in hospitalized
analysis and the multivariable analysis. Similar findings have patients might have reduced the difference between nondia-
been reported earlier [15, 20–22]. betics and well-controlled diabetic patients in our study.
In this study, the presence of numerous bacilli on initial No age groups had any significant association with a delay
pretreatment sputum smears was also an independent pre- in negativation. Kuaban et al. showed that age above or equal
dictor of a delay of conversion of positive sputum smears. to 40 years was an independent predictor of nonconversion
The direct influence of initial bacillary load on the absence of sputum smears [14]. Singla et al. observed in a similar
of sputum conversion at the two months of therapy has study that patients aged over 60 years had an almost six times
been reported by several authors [11, 13, 20, 23]. Rieder greater risk of remaining sputum positive after two months
et al. observed that sputum conversion at the end of the of treatment than patients aged 21–40 years, while patients
two months of directly observed therapy among patients aged 41–60 years were twice as likely to remain sputum
with initial weakly positive sputum was 90.9% while it positive [28]. Liu et al. also reported that the elderly were
was, respectively, 77.9% and 61.7% among patients with the least likely to have documented sputum conversion after
initial moderately positive and strongly positive sputum [11]. two months of treatment. The reason why old age should
Singla et al. reported that patients with numerous bacilli on predispose to delayed sputum smear conversion is not exactly
pretreatment sputum smear examination had an almost six known [29].
times greater risk of persistent sputum positivity than patients There is insufficient evidence to support an associa-
with few bacilli [20]. Meanwhile, Lienhardt et al. [13] reported tion of smoking and delayed smear conversion [30]. Three
sputum conversion at the end of two months in patients with researchers examined this association; one study showed
initial sputum smear 1+, 2+, and 3+ to be 96.2%, 85.8%, and significant effects, but two others did not [31–33]. New studies
81.8%, respectively [13]. should use cohort and case-control designs to examine the
Our results indicated also that bilateral radiological association of passive and active smoking with slower smear
involvement and miliary lesions were independent risk fac- conversion.
tors for delayed smear conversion, due to the high baseline Our study has several strengths, its prospectivity, sam-
bacillary burden of those patients. ple size, standard protocols of treatment and supervising
In contrast with previous studies [20, 24, 25], our results (DOTS), and studying environmental conditions.
indicated no relationship of cavitation with delayed smear It has also some limitations; the information was based on
conversion, although its presence has been significantly selected inpatients of our tertiary care hospital, at which only
associated with a longer time to smear conversion. This complicated cases are admitted. It may not reflect the patterns
discrepancy could be due to differences in methodologies and in the community in general.
populations.
In our cohort, it is difficult to speculate on the influence
of HIV status in smear conversion, as long as there is only one 5. Conclusion
patient. In conclusion, our analysis showed delayed smear conversion
The relationship between factors like age, sex, weight, in more than half of the patients. Smear grading, miliary, and
diabetes mellitus, smoking, alcoholism, addictions, respira- bilateral radiologic lesions were independently associated
tory diseases, previous TB contagion, previous TB disease, with delayed smear conversion. We suggest that intensified
alternative anti-TB treatment, and related toxicity and delays treatment and precautions against transmission should be
of conversion of positive sputum smears after two months especially considered for TB patients with these risk factors,
of treatment in our study had no statistically significant allowing the optimization of national TB control measures.
association. More prospective studies about sputum conversion and
There has been a concern that HIV-infected patients with also culture conversion are needed to consolidate our find-
tuberculosis are more infectious and are infectious for a ings.
longer period of time than patients with tuberculosis who are
not HIV-infected. In our study we had only one coinfection
HIV-TB which negated in the 2nd fortnight. Some studies, Conflict of Interests
by investigating contacts, have also concluded that HIV-
associated pulmonary tuberculosis is not more infectious The authors have no conflict of interests to declare.
than tuberculosis alone [26]. Otherwise, Telzak et al. and
Domı́nguez-Castellano et al. showed that it was more likely
that the sputum smears and cultures of HIV-infected patients
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