Retrospective Study of the Pattern of Pulmonary and Extrapulmonary Tuberculosis Cases in Ain Shams University Hospitals during the Period of 2016– 2022

• This study evaluated the pattern of TB infection at Ain Shams University Hospitals (ASUH) among TB patients or suspects presenting to the hospital during the period from January 2016 through July 2022.
• TB is more prevalent among the male patients of productive age group, especially Pulmonary TB. There is an increasing trend among females. The positivity rate of TB cases showed a rising pattern from 2016 to 2018, where the highest rate (2.26%) was observed. Followed by an upwards and downwards pattern to reach its lowest rate (0.84%) in 2021, in concurrence with COVID-19. Afterwards, a sharp rise was noticed in 2022.
• We recommend adopting the control measures as those used for COVID-19, such as washing hands and wearing masks in crowded places. This would help to minimize the number of TB patients.

Table (1): Comparison between the positive and negative cases regarding age, sex and sample type.

BAL: Bronchoalveolar lavage, NA: Not applicable.

Table (2): Correlation of the studied patients according to age/distribution of cases in relation to age.

Table (3): Correlation between age and sex among studied patients.

X² Chi-squared test

Table (4): Distribution of HB and WBC levels among positive TB cases.

Table (5): Correlation between young and elderly individuals according to HB and WBC levels.

Table (6): The frequency of TB-positive cases and their relation to the total patient number from 2016 to 2022.

Table (7): Distribution of cases according to age group, sex and sample type during the study period.

DISCUSSION

Tuberculosis (TB) is responsible for most cases of illness and death worldwide, especially in Asia and Africa [8]. Although Egypt is not one of the 22 countries listed by the WHO for their high levels of tuberculosis (TB) infection, TB is a considerable public health problem in Egypt [9].

In the current study, we analyzed the records of 7704 patients registered for different diagnostic tests of TB from 1^st January 2016 to 31^st of July 2022. The lower respiratory samples represented most of the collected samples (92.16%), followed by blood (2.91%) and pleural fluid (2.17%). Urine was the least common sample type collected (0.09%). All ascitic fluid, synovial fluid, tissue, and urine samples were negative for TB. Regarding the type of TB, pulmonary TB cases outnumbered the extrapulmonary cases (EPTB). Pleural fluid represented the majority of EPTB cases (3/9, 33.33%). The age of the total positive TB cases was 41.84±16.06 years, with 58.87% in the productive age group (31–60 years) and 65.52% males. The comparison between the positive and negative cases revealed that there was a statistically significant difference between the two groups regarding age, age group, and sex. In the current study, males predominated, and most of the patients were under the age of 60 years. It is worth noting that starting in 2018, high positivity rates were observed among females.

These findings were in agreement with several Egyptian studies. They found that there was a male predominance among the TB patients, with much higher cases among reproductive age. They stated that pulmonary TB cases surpassed extrapulmonary cases [2, 7, 9-12]. Shafiek and colleagues (2022) stated that the majority of EPTB patients in their study had tuberculous pleural effusion (32%) [6].

Malik et al. (2021) also revealed that 3357 TB cases were identified in Giza Governorate from 2014 to 2018. They agreed with our results, as they reported a higher incidence of TB in the age group 18–65 years with lower values among extremes of age. This active age group is more exposed to infection with a high prevalence of smoking behavior. Moreover, they observed a higher frequency among male patients, and the highest number of cases was noted in 2017 [1]. Additionally, Mori and Leung (2010) stated that TB affects the most productive age groups and demands directing more attention to TB control programs targeting those age groups [18].

Malik and colleagues (2021) stated that the higher frequency of TB in males compared to females is due to several reasons. First, females tend to seek medical advice less than males because of their lack of education. Moreover, men are more exposed to outdoor activities. Another cause is the prevalence of the attitude of cigarette and shisha smoking among men [1]. On the other hand, Mohamed and his team (2010) [13] found that TB was more prevalent among female patients (70.87%) than males (29.13%) admitted to the Assiut Chest Hospital from 2005 to 2009. That variance can be attributed to the fact that in Upper Egypt, the female shares the male the responsibility of work both outside and inside the home, with a greater chance of exposure to infection.

In the present work, the increasing positivity rate among the female group can be attributable to the predominance of tobacco smoking among young females in Egypt and different parts of the Arab world [14]. Various studies have declared an increasing tendency towards consuming tobacco, either in the form of cigarettes or water pipes, among young ladies. Such a high consumption rate can be associated with the increasing numbers of employed women and admiration for Western culture. Some studies forewarned that if no active steps are taken to contain this problem, it might turn into a health disaster [15-17].

Malik and his colleagues (2021) reported a higher percentage of PTB from 2014 to 2018, except for 2017. The highest percentage of EPTB was noted in 2017 (51.6%) [1]. Similarly, Essawy et al. (2016) found that 72.8% were PTB and 27.2% were EPTB [19].

Unlike our findings, Hashem and colleagues (2022) reported that the number of EPTB cases was higher than that of PTB cases throughout the 4-year study period. This can be attributed to the higher number of TB patients included in their study (2256) compared to the low number (124) included in the present study. Moreover, different geographical areas might play a role in the distribution of TB cases, as their study took place in Assiut Chest Hospital in upper Egypt. Hashem et al. (2022) presented a number of explanations for the high EPTB cases in their work. They stated multiple risk factors, such as higher age, female gender, geographical distribution, birth in high TB-prevalent countries, exposure at residence or work, homelessness, and presence of other comorbid conditions [20-22].

Regarding the distribution of HB and WBC levels among positive TB cases, the mean HB level was 10.66, with 96 patients with HB level lower than 12 gm/dl. For WBCs, the mean was 9.4 x10⁹/L, and 35 cases exhibited leucocytosis. Our results regarding HB agreed well with Ghweil and colleagues (2018), who reported HB mean of 10.4 mg\dl. However, the mean WBC count in their study was higher (14.74 x10⁹/L) [11].

In the present study, the frequency of TB-positive cases in relation to the total number of patients from 2016 to 2022 revealed that there was a rising pattern from 2016 to 2018, where the highest percentage (2.26%) was observed in 2018. After that, the percentage of positive cases showed an upwards and downwards pattern to reach its lowest level (0.84%) in 2021. For the frequency of TB-positive cases, the lowest number was reported in 2016 (7/124, 5.65%), and the highest number was noticed in 2018 (22/124, 23.39%). No cases of EPTB were detected in 2016 and 2018, and the highest numbers were found in 2022.

In a similar fashion to our results, Hashem and colleagues (2022) reported that TB cases in their study from 2017 to 2020 showed a declining pattern until the first half of 2021, except for a rise noticed in 2018. Both their study and ours agreed that the magnitude of TB cases markedly declined in 2021. They linked this noticeable drop in tuberculosis case detection with the COVID-19 pandemic [20].

Similarly, countries known for their high burdens of TB, such as Indonesia, India, South Africa, and the Philippines, witnessed a significant reduction in TB incidence along with the COVID-19 pandemic, especially in the second quarter of 2020 and the first half of 2021, correlating with many TB management setting reports [23-26].

Some authors attribute this decline to the COVID-19 pandemic, where all healthcare systems directed their efforts toward the prevention, screening, and diagnosis of COVID-19. This led to the attrition of the healthcare system and the exhaustion of its resources, affecting tuberculosis screening programs and management facilities [20, 27].

They also assumed this phenomenon was because the lockdown and the reduction in public transportation hours made access to public health services more difficult. Another factor was the overwhelming fear of TB patients from contracting COVID-19 infection, resulting in missed or delayed diagnosis of TB cases. Additionally, reduced healthcare working power due to the closure of numerous tuberculosis outpatient clinics and a lack of personal protective equipment in some health facilities obliged them to halt conducting tuberculosis tests temporarily [23, 28]. Moreover, the similarities in symptoms between TB and COVID-19 masked some TB cases and thus were treated empirically as COVID-19 or refused to seek medical advice. Despite the release of the lockdown and restoration of most daily activities with the application of protective measures, TB cases continued to decline in 2021.

The rise in 2022 might be due to the cumulative cases seeking medical services after the lockdown period ended. Another hypothesized cause for that rise was the increased indoor/household infections during the lockdowns phase [28].

In May 2020, the WHO stated that TB and COVID-19 cases disseminate through close contact. Thus, similar measures can control both. However, it was concerned about the medical status of TB patients. The WHO stressed ensuring the availability of diagnostic techniques and therapeutics for TB patients when all efforts were directed at containing the COVID-19 pandemic. The WHO warned against the potential deterioration in progress achieved in lowering the death rate of TB patients in the last five years [29].

Alene and coworkers (2022) alerted that reallocating the available sources to control COVID-19 will threaten the lives of TB patients and might result in disastrous health problems. Hence, a balanced direction of expenses and services in case of an epidemic is mandatory to maintain supplying the requirements to TB patients [30].

On the other hand, Wu and colleagues (2022) from China offered an interestingly different opinion assuming that the decline in TB cases was true owing to the effect of the strict measures posed by the Chinese authorities for containing the COVID-19 crisis, such as social distancing, wearing masks, and frequently washing hands. Therefore, they studied the impact of these measures by introducing three models for the prediction of variation in the incidence of PTB cases in China after January 2020. One of them was noninterventional, and the other two were interventional with regular and strict interventions. They observed a marked overall reduction in PTB occurrence during 2020, which probably was the outcome of the intervening actions against COVID-19. They concluded that by applying the aforementioned strategy for the following two years, the incidence of PTB would decrease by approximately 1.03 per 100,000 people each month compared with the incidence predicted by the noninterventional model. They estimated that the annual incidence would be reduced from 59.15 to 50.65 per 100,000 in 2021 by performing strict instead of regular interventions. Based on their results, they suggested that the continuous application of regular interventions would play an important role in the future prevention and control of PTB [31].

They explained the difference between their study and the other studies in that they quantified the potential effect of preventive measures based on limiting close contact between infected people and uninfected people, which may exert positive effects in preventing PTB if continued to be implemented post-COVID-19 [31]. However, other studies stressed the compromising impact of these measures on TB diagnosis, thus resulting in an artificial decline in the number of TB cases [32, 33].

In summary, our findings have important implications for clinical and public health policies for tuberculosis prevention via the disruption of the chain of tuberculosis transmission. We recommend several strategies for the regular prevention of TB, including wearing masks in endemic regions, providing government-subsidized masks for crowded public places, maintaining good hand hygiene, avoiding large crowded indoor gatherings, and controlling the number of people in gatherings.

The limitations of the present work were the unavailability of data regarding clinical conditions, radiologic findings, smoking, residence rural/urban, socioeconomic status, history of previous treatment, and whether the infection was new or old. Additionally, different methods of diagnosis were used, and not all the samples were tested by Gene Xpert. Sputum analysis for acid fast bacilli was used as it is an affordable and quick test for diagnosis, but it might yield negative results with poor sample quality.

CONCLUSION

TB is more prevalent among the productive age group, especially PTB. Although TB is more common among men, we noted an increasing trend among females. Thus, it is suggested that the TB control approach should provide more care for those patients and propagate awareness to avoid unhealthy practices that participate in the dissemination of positive cases, such as tobacco smoking. The frequency of TB-positive cases was the highest (2.26%) in 2018. It reached its lowest level (0.84%) in 2021, in concurrence with COVID-19. We recommend encouraging hygienic practices similar to those used to control COVID-19, such as washing hands and wearing masks in crowded places. In our opinion, this would help us achieve our dream and minimize the number of TB patients, thus decreasing the financial burden. Additionally, we recommend conducting large-scale studies to propagate awareness and study the effect of implementing health practices on the number of TB cases.

Funding: None.

Conflict of interest: None.

Ethical Considerations: This research was approved by the Ethical Research Committee, Faculty of Medicine, Ain Shams University. (ethical approval number: FMASU R219/2023, FWA 000017585).