International Journal of Mycobacteriology xxx (2016) xxx– xxx

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Full Length Article The pattern of tuberculosis in Chest Hospital,

a, b c Eman Sobh *, Sayed Abd Elsabour Kinawy , Yasser Mohamad Ahmad Abdelkarim , Mahmoud Ahmed Arafa d a Chest Diseases Department, Faculty of Medicine for Girls, Al-Azhar University, , Egypt b Chest Diseases Department, Faculty of Medicine, Aswan University, Aswan, Egypt c Chest Diseases Department, Aswan Chest Hospital, Aswan, Egypt d Chest Diseases Department, Faculty of Medicine, Al-Azhar University, Cairo, Egypt

ARTICLE INFO ABSTRACT

Article history: Objective/background: Tuberculosis (TB) is a major health problem. The aim of this study Received 27 July 2016 was to examine the pattern of TB in Aswan Chest Hospital, Aswan, Egypt. Accepted 6 August 2016 Methods: This cross-sectional study was carried out using medical records from the TB Available online xxxx registry in Aswan Chest Hospital. The investigated variables included demographic charac- teristics, type of TB infection, and affected organs. All data were coded and statistically Keywords: analyzed. Extrapulmonary tuberculosis Results: The average age of the 557 patients infected with TB was 40.31 ± 18.87 years; 58.2% Pulmonary tuberculosis of the cases were men and 41.8% were women. In both sexes, the highest number of TB Tuberculosis patients was from the reproductive age groups. During the 5-year study period, the highest percentage of cases were new cases and the highest frequency of cases was during 2011 and the lowest frequency was during 2015. Pulmonary TB cases showed a sharp decline; however, there was a decrease in extrapulmonary TB cases during 2012 and 2013, with a slight rise in 2014 and 2015. Of the pulmonary TB cases, 82.5% were smear-positive TB. Conclusion: There was a decline in the total number of TB cases across the studied years and the most studied cases were pulmonary smear-positive and new cases. Younger people represented a large percentage of reported cases. Ó 2016 Asian-African Society for Mycobacteriology. Production and hosting by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).

Introduction an estimated 9.6 million new TB cases. More than 90% of new TB cases and deaths occur in developing countries [2]. Tuberculosis (TB) is a contagious bacterial disease [1] that is a Egypt has massively engaged in early case detection, major public health problem worldwide. In 2014, there were provision of adequate chemotherapy, and prevention of

* Corresponding author at: Chest Diseases Department, Al-Zahraa University Hospital, 11517 Al-Abbassia, Cairo, Egypt. E-mail address: [email protected] (E. Sobh). Peer review under responsibility of Asian African Society for Mycobacteriology. http://dx.doi.org/10.1016/j.ijmyco.2016.08.001 2212-5531/Ó 2016 Asian-African Society for Mycobacteriology. Production and hosting by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: E Sobh et al. The pattern of tuberculosis in Aswan Chest Hospital, Egypt. Int. J. Mycobacteriol. (2016), http:// dx.doi.org/10.1016/j.ijmyco.2016.08.001 2 International Journal of Mycobacteriology xxx (2016) xxx– xxx

transmission to new cases [3]. The prevalence rate of TB in registers, TB treatment cards, and files to record and report on Egypt was 26 per 100,000 people according to the World patient information. Health Organization estimate in 2014, while the incidence All patients registered with TB in Aswan Governorate rate was 15 per 100,000 people. Screening, diagnosis, notifica- between January 1, 2011 and December 30, 2015 (5 years) were tion, and registration of TB cases were implemented all over included in the study. Data were obtained from TB patient Egypt according to the National TB Strategy of the National registers and TB treatment cards in TB clinics. Tuberculosis Control Program (NTP) [4]. One of the registra- tion sites is Aswan Chest Hospital, Aswan, Egypt where the Statistical analysis current study was conducted. Aswan city lies in the Upper Egypt sector in the south of Egypt; it has 1425738 inhabitants Data were collected into a paper form by authors. Data were according to the 2015 report [5]. fed to the computer as an EXCEL sheet (Microsoft Corpora- The objectives of this study were to assess the TB pattern tion, Redmond, WA, USA), and were validated and analyzed and to provide an insight into the type of TB infection in by SPSS program version 15 (SPSS Inc., Chicago, IL, USA). Aswan Chest Hospital. Descriptive analysis was performed. Comparisons were made between variables using the chi-square test and 95% confi- Methods dence intervals where appropriate. A chi-square test was used to evaluate differences in proportions. The Student t test This was a hospital-based cross-sectional, retrospective study was used for mean comparisons. Comparisons at p < .05 were involving a record review of patients with TB notified, regis- considered significant. tered, and treated in Aswan Chest Hospital. We analyzed TB cases reported from January 1, 2011 to Ethical approval December 31, 2015. The diagnosis of TB in Aswan Chest Hospital is made in line with the National Egyptian TB Control Ethics approval to use, report, and publish the collected data Program Guidelines of the Ministry of Health (NTP). Cases was obtained from the Ministry of Health, Egypt. Patient infor- were categorized by major disease site, reported as either pul- mation was anonymized and deidentified prior to the monary TB (PTB) or extrapulmonary TB (EPTB). The PTB group analysis. comprised cases with PTB that were either sputum smear positive or sputum smear negative according to a sputum Results smear examination. If three successive samples of sputum smears were negative twice and chest radiography was com- Between January 1, 2011, and December 31, 2015, among patible with active PTB, the patient was diagnosed as smear- 551,440 cases attending Aswan Chest Hospital, the Epidemiol- negative PTB after discussion by expert committee including ogy Service of Aswan Chest Hospital was notified of 557 cases a clinician and a radiologist; or if acid fast bacilli were of TB (Table 1). detected by other means, for example, bronchoalveolar All cases received therapy through directly-observed ther- lavage. If the patient had a local extrapulmonary lesion with apy short course (DOTS) with either observed or packed doses symptoms compatible with TB, a positive purified protein to be received at home. derivative test was performed and other diseases excluded The highest frequency of cases was during Year 2011 and and if a biopsy from the lesion was positive for Mycobacterium the lowest frequency was during Year 2015 (Fig. 1). tuberculosis or had caseating granuloma, a diagnosis of EPTB There was a decline in the total number of cases across the was made. The EPTB group comprised any extrapulmonary studied period: PTB cases showed a sharp decline in 2015; disease site: pleural, lymphatic, bone and/or joint, genitouri- however, there was a decrease in EPTB cases during 2012 nary, meningeal, peritoneal, and few cases including eye, and 2013 with a slight rise in 2014 and 2015 (Fig. 1). breast, and pericardial TB reported as ‘‘other”. However, there There were 557 patients with TB. Men outnumbered were some unclassified EPTB disease sites listed as ‘‘un- women and 47.76% of patients were from urban areas and known” [6]. Anti-TB therapy was also recorded and patients 52.24% were from rural places. Higher numbers of affected are categorized as either new or previously treated cases according to the patient’s history. Anti-TB treatment is pro- vided for free and according to standardized regimens of NTP (Regimen I for new cases and Regimen II for retreatment Table 1 – Number of tuberculosis cases from 2011 to 2015. cases). Treatment for new PTB patients consists of an initial phase of rifampicin (R), isoniazid (H), pyrazinamide (Z), and Y Frequency % ethambutol (E) or streptomycin given daily for 2 months fol- 2011 125 22.4 lowed by a continuation phase of R and H daily for 4 months. 2012 118 21.2 Retreatment patients are given a standard retreatment Regi- 2013 108 19.4 men II (SHRZE for 2 months, HRZE for 1 month, then HRE 2014 113 20.3 for 5 months) [4]. Patients with EPTB are treated for varying 2015 93 16.7 lengths of time, depending on disease severity and treatment Total 557 100.0 response. Monitoring the response to therapy was done Note: Y = year. according to the National Guidelines of NTP, using TB patient

Please cite this article in press as: E Sobh et al. The pattern of tuberculosis in Aswan Chest Hospital, Egypt. Int. J. Mycobacteriol. (2016), http:// dx.doi.org/10.1016/j.ijmyco.2016.08.001 International Journal of Mycobacteriology xxx (2016) xxx– xxx 3

Fig. 1 – Number of tuberculosis (TB) cases in Aswan Chest Hospital, 2011–2015. Note: EPTB = extrapulmonary tuberculosis; PTB = pulmonary tuberculosis; Y = year.

patients were of reproductive age and lower numbers from There was a significant difference between males and extremes of age (Table 2). females with regards to age. Affected males were older than There was a male predominance among patients diag- females (Table 4). nosed with TB with a male/female ratio of 1.4:1 (Fig. 2). A small percentage of cases were below 15 years old (6.8%). Type of TB Of them, 57.9% were boys and 42.1% were girls; however, for adults (P15 years), 58.2% were men and 41.8% were women There were 557 patients with TB including either newly diag- (Table 3). nosed or previously treated cases. Of these, 62.7% (n = 349) had PTB and 37.3% (n = 208) had EPTB. Only one multidrug- resistant case was found (Table 5). About two-thirds of cases were PTB and only one-third Table 2 – Demographic characteristics of tuberculosis cases. were EPTB (Fig. 3). Frequency (n = 557) % EPTB cases were significantly younger and had a higher proportion of women. However, PTB cases were older and Sex had a higher number of men (Table 6).  Male 324 58.2  Female 233 41.8 The majority of cases were sputum smear positive (Table 7). Age group (y) The most common affected extrapulmonary site was  <15 38 6.8  15 – <30 142 25.5 lymph nodes followed by pleura, and then bone (Table 8).  30 – <45 128 23  45 – <60 139 25.0 Type of patient  P60 110 19.7 Residence The most common cases were new PTB cases (Tables 9 and 10  Urban 266 47.76 and Fig. 4).  Rural 291 52.24 Note: y = years. Discussion

TB ranks alongside the human immunodeficiency virus as a leading preventable cause of mortality from infectious dis- ease [2]. Delay in the diagnosis of pulmonary and laryngeal cases increases the chances of transmission [1]. This retro- spective study was done on the period from January 2011 to December 2015 to identify the pattern of TB infection among diagnosed patients with TB registered at Aswan Chest Hospital. In this study we reviewed the records of TB cases. All cases were diagnosed and treated at Aswan Chest Hospital and they received therapy through DOTS. We found 557cases registered for TB. Egypt follows the DOTS model for TB control and over the past number of years has had much success in reducing the Fig. 2 – Sex distribution of the studied population. disease burden caused by TB [4].

Please cite this article in press as: E Sobh et al. The pattern of tuberculosis in Aswan Chest Hospital, Egypt. Int. J. Mycobacteriol. (2016), http:// dx.doi.org/10.1016/j.ijmyco.2016.08.001 4 International Journal of Mycobacteriology xxx (2016) xxx– xxx

Table 3 – Distribution of cases in relation to age. Age (y) Range (y) No. of cases % Mean ± SD (y) p

<15 0.33–14 38 6.8 4.36 ± 3.64 <.001* P15 15–85 519 93.2 42.94 ± 16.72 Total 0.33–85 557 100 40.31 ± 18.87 Note: SD = standard deviation; y = years. * Significant.

Table 4 – Mean of age of cases in relation to sex. Sex No. of cases Mean age (y) SD Minimum age (mo) Maximum age (y) tp

f 233 38.3052 18.43234 3 80.00 2.13 .033* m 324 41.7494 19.07053 3 85.00 Total 557 40.3086 18.86626 3 85.00 Note: f = female; m = male; mo = months; SD = standard deviation; y = years. * Significant.

Table 5 – Distribution of cases according to type of tuberculosis (TB). Type No. tp

PTB 349 35.693 <0.01* EPTB 208 Total 557 Note: EOTB = extrapulmonary tuberculosis; PTB = pulmonary tuberculosis. * Significant.

The results of this study showed that the number of cases over the last few years according to the World Health Organi- diagnosed decreased over time with the lowest number being zation TB report in 2015 [2]. There was a decrease in TB preva- reported in 2015 (Table 1 and Fig. 1). This may be due to a lence rate in Egypt from 30/100,000 of the population in 2008 decreased overall incidence and prevalence of TB in Egypt to 26/100,000 population in 2014 [2,4]. This may be due to the fact that DOTSs are available at other centers within the city and its environment. The same results have been reported by other studies [6,7]—other studies have found decreased counts of TB cases over time. Analysis of the type of TB showed that there was a decrease in PTB cases over time with a sharp decrease during 2015. The pattern for EPTB was slightly different, although there was a decrease in the total number of EPTB cases, the pattern showed a slight rise during 2014 and 2015 (Fig. 1). Peto et al. [6] reported that almost one-fifth of US TB cases were EPTB. An unexplained annual case count decreases have occurred in EPTB compared with annual case count decreases in PTB cases. Wani et al. [8] reported that the number of cases showed a sawtooth pattern from year to year. In this study, the age of patients ranged from 3 months to 85 years; of them 93.2% of patients were >15 years and 6.8% were children. The mean age of cases was 40.31 ± 18.87 years. The age groups from 15 years to 30 years and from 30 years to 45 years compro- Fig. 3 – Distribution of cases according to type of mised 45.5%. This could be attributed to the increase in preva- tuberculosis (TB). Note. EPTB = extrapulmonary tuberculosis; lence of smoking behavior in this active age group in our PTB = pulmonary tuberculosis. society. Moreover, poverty, malnutrition, physical, mental,

Please cite this article in press as: E Sobh et al. The pattern of tuberculosis in Aswan Chest Hospital, Egypt. Int. J. Mycobacteriol. (2016), http:// dx.doi.org/10.1016/j.ijmyco.2016.08.001 International Journal of Mycobacteriology xxx (2016) xxx– xxx 5

Table 6 – Characteristics of patients with pulmonary tuberculosis (PTB) versus extrapulmonary TB (EPTB). Characteristics PTB EPTB tp

Age (y) Mean ± SD 42.69 ± 18.07 36.31 ± 19.53 3.9 <.001* Sex Male (%) 67.9 41.8 6.03 <.001* Female (%) 32.1 58.2 Note: SD = standard deviation; y = years. * Significant.

Table 7 – Distribution of the types of pulmonary tuberculosis (PTB) in the study population. Type of PTB Frequency %

 Smear positive 288 82.5  Smear negative 61 17.5 Total 349 100

Table 8 – Distribution of extrapulmonary tuberculosis (EPTB) cases according to organ affected. EPTB organ affected Frequency (n)%

Pleura 53 25 CNS 5 2.4 LN 57 27.4 Bone 31 14.9 GIT 20 9.6 Urinary tract 8 3.8 Reproductive system 5 2.4 Skin 5 2.4 Other (breast, pericardial, eye) 6 2.9 Unknown/not recorded 19 9.1 Total 208 100 Note: CNS = central nervous system; GIT = gastrointestinal tract; LN = lymph nodes.

Table 9 – Distribution of tuberculosis cases according to history of antituberculosis drugs. Frequency (n)%

New 493 88.5 Relapse 40 7.2 Treatment failure 9 1.6 Treatment after interruption 8 1.4 Other 7 1.3 Total 557 100.0

and occupational stress, and greater exposure to infection are et al. [8] reported most of the patients were young, with a other contributing factors [9]. Mori and Leung [10] stated that mean age of 34.44 ± 17.087 years. In the Ige and Akindele in Africa the age group of 15–44 years comprises about 74% of [12] study, 73.2% of the patients were between the ages of the population, whereas in the United States it is only 24%; 20 years and 49 years. therefore, in high-prevalence settings, TB affects the most The same results were reported by Zedan et al. [13] who productive age groups which necessitates more attention in found that 3.6% of cases were 615 years and the main age TB control programs targeting those age groups. In addition, in their study was 37.5 ± 16.0 years. Multiple studies [9,14– Kochi [11] reported that more than 75% of infected persons 17] conducted in Egypt revealed TB was common in the were below the age of 50 years in developing countries. Wani middle-aged group (from 15 years to 6 30 years). They

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Table 10 – Type of patient. PTB EPTB Frequency (n) % Frequency (n)%

New 303 86.8 190 91.3 Relapse 30 8.6 10 4.8 Treatment failure 6 1.7 3 1.4 Treatment after interruption 6 1.7 2 1.0 Other 4 1.1 3 1.4 Total 349 100.0 208 100.0 Note: EPTB = extrapulmonary tuberculosis; PTB = pulmonary tuberculosis.

Fig. 4 – Distribution of tuberculosis cases according to history of antituberculosis drugs. reported that the highest prevalence of TB was among indi- reported similar findings [17,21,22]. Increased TB cases in viduals between 15 years and 35 years of age and 35–45 years, rural areas could be explained by poverty, bad social condi- and the lowest prevalence was in the extremes of age (tho- tions, milk sanitation, and occupational exposure to infected se < 15 years and those > 60 years). In the study by Ige et al. animals. Moreover, it may be due to increased notification of [7], the highest number of cases of TB (27.8%) was in the 20– rural cases as a result of improved access to health care ser- 29 years age group followed by those younger than 40 years vices and the implementation of DOTS [23]. Other studies (26.0%). Less than 20% (18.3%) were P40 years old. [9,24] found that urban cases were significantly higher than In this study there were 58.2% men and 41.8% women with rural cases. They explained this result by demographic a male to female ratio of 1.6:1 (Table 1). Their mean age was changes like increasing life expectancy, population growth, 38.31 ± 18.43 years for women and 41.75 ± 19.07 years for and deterioration of living conditions in urban areas like over- men (Table 4). The same results have been obtained by previ- crowding. Also, it may be due to the shift of people from rural ous studies [7,9,18] as well as Floyd et al. [18]—they reported to urban areas. TB was more common among men than women. Higher TB In this study, regarding the type of TB infection, PTB out- notification rates among men may partly indicate differences numbered EPTB cases (62.66% were PTB and 37.34% were EPTB). in exposure due to more frequent social contacts, risk of Various studies [7,8,14,21] reported a higher number of PTB infection, and progression from infection to disease caused compared with the number of EPTB. However; some studies by sex differences in association with other risk factors for [13,25] reported a near equal proportion of EPTB to PTB cases. TB such as alcohol abuse and smoking which are associated In the current study, cases of EPTB were significantly with PTB. Also men are more active and vulnerable to stress younger (mean age 36.31 ± 19.53 years for EPTB vs. 42.69 which may modify their immune response [9]. However, Wani ± 18.07 years for PTB) and a significantly higher number of et al. [8] and Zedan et al. [13] reported a higher percentage of women (58.2% vs. 32.1%). However, for PTB there were a sig- women compared with men. nificant higher number of men (67.9% vs. 41.8%). Wani et al. In many countries, differences in TB incidence rates [8] found that most of the patients were young, with a mean between urban and rural areas have been described [4].TB age of 34.44 ± 17.087 years. Females of reproductive age out- in urban areas often results specifically among certain urban numbered the males in both PTB and EPTB. risk groups, such as slum dwellers who are exposed to poor In this study majority of PTB cases were sputum smear environmental conditions (overcrowding or poor living condi- positive (82.5%). Wani et al. [8] reported only 23% of the cases tions) [19]. TB is still believed to be a disease that dispropor- were smear positive. Shabana et al. [9] reported a high per- tionately affects the poor and marginalized [20]. In the centage of sputum negative cases (26.2%) and concluded this current study, 52.24% of patients were from rural areas and may be a false high percentage due to the decrease in the 47.76% were from urban areas (Table 2). Various studies have facilities of diagnosis in the governorate hospitals.

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