Tuberculosis; Nutritional status; Treatment adherence; Anti-TB therapy; Malnutrition

Tuberculosis (TB) is a global health concern owing to its significant contribution to morbidity and mortality [1]. According to the World Health Organization (WHO), nearly one-third of the population is infected with Mycobacterium TB, with 8.8 million cases diagnosed every year, and it is the second-largest cause of death due to infections globally [2,3]. Approximately 45% of the cases are reported in Southeast Asian countries, including Indonesia, India, and China [4]. Early diagnosis and timely treatment of TB are crucial for decreasing the prevalence rate of the disease as well as for preventing complications and drug resistance [5].

In addition to common risk factors for TB, such as HIV infection, diabetes, tobacco use, and substance abuse, malnutrition is one of the major risk factors for this infection and is related to infection severity, poor prognosis, and mortality [6,7]. Malnutrition reduces the absorption capacity of anti-TB medicines in patients, worsening their condition and decreasing their chances of survival [8]. TB treatment modalities further increase the risk of hepatotoxicity. Therefore, nutrition and dietary adequacy are particularly important in preventing and fighting infections, particularly TB [7,9].

Malnutrition is associated with deficiencies in macronutrients; trace elements such as zinc and selenium; and essential vitamins such as vitamin A, vitamin C, and vitamin E [10]. Low intake of micronutrients and vitamins weakens the body’s immune system, ultimately leading to severe infections [11]. These essential vitamins are administered as part of the treatment regimen to improve the immunity of TB patients, which is beneficial for reducing the development of recurrent infection, especially in patients with primary TB infection [12]. Notably, including a single dose of 20 micrograms (mcg) of vitamin D for adults in daily supplementation could improve immunity against infection, especially among healthy individuals at risk of or exposed to TB infection [13,14]. Therefore, nutritional inventions for TB patients as a part of their primary course of therapy are effective for curing the infection [15,16].

Given the importance of infections, global health initiatives such as the Sustainable Development Goals (SDGs) have prioritized the reduction and elimination of infections such as TB worldwide [17]. Several programs have been launched to reduce and eliminate the number of TB cases, with a particular focus on Southeast Asia, where malnutrition is one of the key indicators resulting in the highest burden of infection [18]. These programs encompass various aspects of a region's prevention, diagnosis, and treatment of TB infection. However, assessing the nutritional status of infected patients to improve their immunity and support anti-TB treatment remains essential [19]. Although other countries in the same region have developed policies to address TB infection and malnutrition among patients, Pakistan requires baseline data on the nutritional status of TB patients to inform efforts required to address this critical gap [20]. Therefore, this study was conducted with the aim of assessing the nutritional status of TB patients visiting public healthcare facilities.

2.1. Study design and duration

This descriptive cross-sectional study was conducted over a period of one year, from June 2022 to May 2023.

2.2. Study settings

The study was conducted at the 360 bedded district headquarters (DHQ) hospital situated in Bhakkar, which has various operational clinical, administrative, diagnostic, and supporting departments, along with other services such as a blood bank, patient transfer services (1122), a hepatitis clinic, and a thalassemia center. Furthermore, the study also included tehsil headquarters (THQ) hospitals in Mankera and Kaloor Kot.

2.3. Participant selection

The study included all TB patients who were diagnosed via laboratory testing, had TB infection for more than three months and were above the age of 18 years. The three-month timeframe was chosen after the confirmed diagnosis of TB to ensure that only patients with visible infection were recruited, as it typically takes nine months for patients to fully recover. Moreover, this period also provides sufficient time for TB to start affecting the nutritional status of patients [21]. However, the study did not include pregnant women with TB or patients who had any other comorbidities, including diabetes mellitus (DM), thyroid gland functional issues, cancers, and chronic heart and kidney diseases. All patients provided written informed consent before inclusion in the study.

2.4. Sample size

The sample size of 323 TB patients was calculated via the online OpenEpi sample size calculator (version 3.01) while maintaining a 95% confidence level, a 5% margin of error, and a 70% incidence of TB in Pakistan, which was slightly increased to 329 to account for potential dropouts [22].

2.5. Sampling technique

A nonprobability purposive sampling method was employed for the selection of adult TB patients visiting the targeted outdoor departments of the DHQ and THQ hospitals.

2.6. Study tool development

A structured questionnaire with few open-ended questions was adopted to gather self-reported information about the TB patients [23]. The patients were asked to provide sociodemographic information such as age, education, sex, marital status, area of residence, employment status, average monthly income and family system and details regarding nutritional history, including declining food intake owing to the loss of appetite, weight loss, body mass index (BMI) (calculated using the standard formula, with height and weight measured during the interview) and medical history, by asking whether they took more than 3 prescription drugs per day [23]. Furthermore, the participants were asked about their daily intake of meals (1 meal, 2 meals, 3 meals), protein intake, fruit or vegetable intake, fluid intake, mode of feeding, perception of their own health status, health status compared with other TB patients, mid-arm circumference, and calf circumference (measured by the principal investigator using standard techniques for mid-arm and calf circumference). Finally, the Mini Nutritional Assessment (MNA^®) tool was used to determine the malnutrition status of the participants. Patients were asked to respond to the questions on the basis of their experiences from the past three months to reduce probable recall bias in patient responses.

2.7. Study measures

The study adopted the MNA^® tool, which has two parts, a screening section (with six questions and a maximum of 14 points) and an assessment section (with 12 questions and a maximum of 16 points) with an overall score of 30 [23]. Patients with points ranging from 24 to 30 were considered normal, whereas patients with scores ranging from 17 to 23.5 were considered at risk of malnutrition, and those scoring below 17 were classified as malnourished.

2.8. Data collection

Face‒to-face interviews were conducted with TB patients visiting the outpatient departments of the selected hospitals and who provided consent to participate in the study.

2.9. Ethical approval

The study was approved by the Institutional Review Board of Allama Iqbal Open University (No. AIOU-NSED-23-215). Prior permission was obtained from the concerned authorities of the hospitals before data collection.

2.10. Data analysis

The collected data were entered into SPSS 25.00 for analysis and interpretation in line with the study objectives. Descriptive statistics, e.g., frequency, percentage, mean, and standard deviation, were calculated for the quantitative and qualitative variables. The associations between sociodemographic indicators (i.e., sex and marital status) and BMI and the malnutrition status indicator were calculated via a chi-square test.

Table 1 shows the sociodemographic profile and nutritional history of the TB patients. The study participants had a mean age of 44.56 ± 17.30 years, with an average of 8.06 ± 5.09 years of education. Most of the patients were females (63.22%), married (79.94%), or urban residents (56.23%). Approximately two-thirds of the patients were employed (71.73%), followed by self-employed (22.19%) and unemployed (6.08%). The majority of the TB patients (41.46%) had average monthly incomes between Pakistani Rupees (PKRs) of 60,000 and 100,000.

Table 2 shows that 38.6% of the TB patients experienced a severe decrease in food intake, whereas 35.3% reported no change in food intake, and 26.1% reported a moderate decrease in food intake over the past three months. Moreover, 29.79% and 20.97% of the participants reported weight loss of more than 3 kg and between 1 and 3 kg, respectively. However, few TB patients reported a BMI <19 (5.47%). Furthermore, most of the TB patients (81.2%) took more than 3 prescription drugs per day.

Table 3 shows the nutritional, dietary, and anthropometric characteristics of the TB patients over the past 3 months. When patients were asked to describe their number of meals eaten per day, 65.3% of patients were eating two meals a day, followed by 18.8% and 15.8% patients who were eating one or three meals, respectively. The consumption markers for protein intake were relatively high, as 57.45% of patients had at least one serving of dairy products per day; 81.46% had two or more servings of legumes or eggs per week; and 53.8% had meat, fish or poultry every day. In addition, 83.9% of patients consumed two or more servings of fruit or vegetables per day. With respect to fluid, 51.37% of patients consumed 3 to 5 cups, followed by more than 5 cups (32.83%) and fewer than 3 cups (15.81%). Furthermore, almost two-thirds of the respondents reported having difficulty eating (69.3%), one-fifth reported having no difficulty eating, and 13.37% were unable to eat without assistance. In response to their self-reported nutritional status, 64.44% were unsure of their status, 18.84% considered themselves malnourished, and 16.72% considered that they were fit in terms of nutritional status. However, the malnutrition indicator score assessment revealed that 13.07% of the TB patients had a normal nutritional status, while half of the patients (50.46%) were at risk of malnourishment, and 36.47% were malnourished.

Table 4 shows the associations of patients' sociodemographic factors (i.e., sex and marital status) and BMI with malnutrition status indicators. There was no statistically significant association between sex and malnourishment in TB patients (p = 0.194). Similarly, the marital status of the patients was statistically insignificant, indicating that being married or unmarried was associated with the same likelihood of being malnourished (p = 0.339). However, the association between patients’ BMI and their nutritional status was significant (p = 0.001).

This study focused on the sociodemographic characteristics, nutritional history, and nutritional status of TB patients. Most study participants were females who were married and urban residents. The majority of the patients were employed and belonged to different socioeconomic groups by income. A reduction in food intake and weight loss is reported by patients, but many patients are uncertain whether they are malnourished or not malnourished. However, the malnutrition indicator score assessment revealed that more than half of the respondents were at risk of malnutrition. Some of them were already malnourished. Furthermore, malnutrition status indicators were not affected by sociodemographic indicators, but BMI was associated with the malnourished status of TB patients.

Our study results are consistent with those of the Burkinabé study, which revealed that 35.8% of TB patients were malnourished, with 7.7% being severely undernourished, 8.9% being moderately undernourished and 19.5% being minimally undernourished [24]. Similar results were reported in the Ethiopian study, with 40.4% of TB patients being underweight and 59.6% being normal or overweight according to their observed BMIs [25]. The findings from the Indian study were similar to ours, reporting high rates of malnourished TB patients. The study assessed the nutritional status of TB patients via anthropometric methods in rural settings and reported that 91.7% of the patients were malnourished [26]. Other studies conducted in different settings also reported high rates of malnutrition among TB patients, ranging from 44% to 48% [27,28].

In developing countries such as Pakistan, the high prevalence of malnutrition is attributed to poverty, food insecurity, and a shortage of food, which make it difficult for TB patients to access sufficient nutrition, ultimately worsening their health conditions [29,30]. In Pakistan’s rural areas where healthcare and diagnostic facilities are limited and where locals must travel long distances for early diagnosis and treatment endeavors, such outcomes are anticipated [31]. The high rate of malnutrition may also be due to the lack of public nutritional support programs, which could improve patients' nutritional status [32]. This issue is further supplemented by a scarcity of resources and a shortage of trained staff in healthcare facilities, which hinders the implementation of effective nutritional support programs [33].

A study conducted in the Somali Region of East Ethiopia reported findings in contrast with our study results that female sex was a predictor of malnutrition [28]. However, a study from Myanmar reported no relationship between sex and malnutrition among TB patients, which is consistent with our study results [34]. Moreover, a study highlighted a strong association between BMI and malnutrition in TB patients, as well as the risk of developing TB [35]. Furthermore, an Indian-based study revealed that BMI, TB and TB prognosis are related [36]. Similarly, another Indian study reported that patients with lower BMIs are at risk of developing multidrug-resistant TB [37]. A study conducted among individuals in South Korea further confirmed the findings of the current study, showing that BMI is closely related to malnourishment among tuberculosis patients [38].

The differences and similarities between our study findings and those of other studies may be due to various geographical, economic, and social determinants. The varying associations between gender and malnutrition show that poverty and food scarcity can affect both genders, whereas some studies highlight cultural factors and limited access to healthcare, which may contribute to gender differences [31]. Moreover, the correlation between BMI and malnutrition may be attributed to the limitations of healthcare infrastructure and the lack of nutritional support programs [32].

Our study highlighted the nutritional status of TB patients from the underprivileged areas of Punjab Province and provided baseline data. Malnutrition was assessed via nutritional indicator scores, and the malnutrition status of patients was compared on the basis of sex, marital status, and BMI. However, the study did not explore the primary causes of malnutrition or the qualitative factors influencing nutritional behaviors among TB patients, which is a notable limitation. Despite this, the study's strength lies in providing crucial data on malnutrition in disadvantaged areas, offering a ground for future research and the development of nutritional support programs.

The study concluded that malnutrition is prevalent among TB patients, with 36.7% malnourished and 50.46% at risk of malnourishment. The findings revealed no significant associations between malnutrition and sex or marital status, but a significant relationship was observed between malnutrition and BMI, indicating the importance of addressing malnutrition as a critical component of TB management.

Conceptualization, NAK, SK, SMASZ, AAR, and MJA; methodology, NAK, SK, SMASZ, AAR, FI and MJA; software, NAK, and FI; validation, SMASZ; formal analysis, NAK, and FI; investigation, NAK, and SMASZ; resources, NAK, SK, AAR, and MJA; data curation, FI; writing—original draft preparation, NAK, SMASZ, AAR, and FI; writing—review and editing, SK, and MJA; visualization, FI; supervision, SK; project administration, AAR, and MJA. All authors have read and agreed to the published version of the manuscript.

This research received no specific grant from the public, commercial, or not-for-profit funding agencies.

The study was approved by the Institutional Review Board of Allama Iqbal Open University (No. AIOU-NSED-23-215).

Not applicable.

The data supporting this study's findings are available from Niaz Ali Khan upon reasonable request.

None.

The authors declare no conflicts of interest.

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