Akademi Analis Kesehatan Delima Husada Gresik

Akademi Analis Kesehatan Delima Husada Gresik

  • Journal List
  • Trop Med Infect Dis
  • v.7(6); 2022 Jun
  • PMC9230370

Trop Med Infect Dis.
2022 Jun; 7(6): 83.

Comparison Epidemiology between Tuberculosis and COVID-19 in East Java Province, Indonesia: An Analysis of Regional Surveillance Data in 2022

Budi Utomo,1,
*
Chow Khuen Chan,2
Ni Made Mertaniasih,3,
4
Soedarsono Soedarsono,5
Shifa Fauziyah,6
Teguh Hari Sucipto,7
Febriana Aquaresta,8
Dwinka Syafira Eljatin,9
and I Made Dwi Mertha Adnyana9

Budi Utomo

1Department of Public Health and Preventive Medicine, Faculty of Medicine, Universitas Airlangga, Tambaksari, Surabaya 60132, East Java, Indonesia

Chow Khuen Chan

2Department of Biomedical Engineering, Faculty of Engineering, Universiti Malaya, Kuala Lumpur 50803, Malaysia; [email protected]

Ni Made Mertaniasih

3Department of Medical Microbiology, Faculty of Medicine, Universitas Airlangga, Tambaksari, Surabaya 60132, East Java, Indonesia; [email protected]

4Tuberculosis Laboratory, Institute of Tropical Disease, Universitas Airlangga, Mulyorejo, Surabaya 60115, East Java, Indonesia

Soedarsono Soedarsono

5Department of Pulmonology and Respiratory Medicine, Faculty of Medicine, Universitas Airlangga, Tambaksari, Surabaya 60132, East Java, Indonesia; [email protected]

Febriana Aquaresta

8Palembang Health Laboratory, Inspektur Yazid Street, Kemuning, Palembang 30126, South Sumatera, Indonesia; [email protected]

Dwinka Syafira Eljatin

9Master Program in Tropical Medicine, Faculty of Medicine, Universitas Airlangga, Tambaksari, Surabaya 60132, East Java, Indonesia; [email protected] (D.S.E.); [email protected] (I.M.D.M.A.)

I Made Dwi Mertha Adnyana

9Master Program in Tropical Medicine, Faculty of Medicine, Universitas Airlangga, Tambaksari, Surabaya 60132, East Java, Indonesia; [email protected] (D.S.E.); [email protected] (I.M.D.M.A.)

Roy Rillera Marzo,
Academic Editor

Received 2022 Apr 13; Accepted 2022 May 17.

Abstract

Tuberculosis and COVID-19 are among the infectious diseases that constitute a public health concern. Therefore, this study aims to examine the recent epidemiology of tuberculosis and COVID-19 in East Java Province, Indonesia, in 2022. Case-based surveillance data were acquired with a retrospective design between January and December 2022 by the East Java Health Officer. The data were analyzed using Quantum Geographic Information System (QGIS) for mapping, and Microsoft Excel for recording. Furthermore, the statistical analysis (Spearman correlation test) was carried out via Statistical Package for Social Science (SPSS) applications. A total number of 38,089 confirmed cases of tuberculosis was recorded, with an incidence rate of 95.49/100,000 population, a case fatality rate (CFR) of 3.6%, and an average treatment success rate of 87.78%. COVID-19 is a new viral disease, with a total of 84,133 confirmed COVID-19 cases in East Java, with an incidence rate of 232.9/100,000 population. The highest incidence rate was found in Mojokerto city, while the lowest was found in Sampang. Furthermore, the CFR values of tuberculosis and COVID-19 were 1.4% and 6.8%, respectively. The regional survey in East Java Province showed that the incidence of tuberculosis remains high. This indicated that the search for active cases and preventive promotion was not completed. Therefore, inter-sectoral collaboration can be adapted to provide suitable tuberculosis health care.

Keywords:

tuberculosis, COVID-19, infectious disease

1. Introduction

Coronavirus disease 2022 (COVID-19) was identified as an infectious illness caused by Coronavirus-2 Severe Acute Respiratory Syndrome (SARS-CoV-2). The daily increase in cases significantly affected the world, with 3.8 million fatalities reported in 2022; therefore, it was declared a pandemic by the World Health Organization [1].

During the pandemic threat, respiratory disorders were aggravated by COVID-19 infection. Due to the significant morbidity and mortality caused by COVID-19, several sectors in society attempted to avoid and conquer the pandemic. Pulmonary tuberculosis is caused by mycobacterium tuberculosis, which is transferred to people in close contact with patients, such as relatives, coworkers, colleagues, and friends, through coughing, talking, and sneezing [2]. This was particularly true for patients with pulmonary tuberculosis (TB), who are very susceptible to viral infection [3,4].

Studies on the existence of COVID-19 co-infection in pulmonary tuberculosis patients are important, due to the high risk and severity of COVID-19 disease. According to Coronel et al., tuberculosis patients have a very high risk of severe illness and mortality from COVID-19 [3]. Furthermore, incorrect treatment and hazardous conduct also increase the possibility of developing new diseases [4,5]. Therefore, this study aims to determine the epidemiology of the number of cases of pulmonary tuberculosis and COVID-19 in Indonesia, specifically in the province of East Java.

2. Materials and Methods

2.1. Study Design

The East Java Province is the eastern part of Java Island with a land area of 47,799.75 km2. It is located in 111°0′ to 114°4′ East Longitude (BT) and 7°12′ to 8°48′ South Latitude (LS) with four regional boundaries, namely, the north side (Java Sea), south, (Indian Ocean), west, (Central Java Province), and east (Bali Strait).

This was a retrospective cohort study using routinely regional surveillance data. The data were obtained from the Health Province Open Data Website, which offers free access to current epidemiological resources for infectious and non-communicable diseases (https://bit.ly/profil-kesehatan-2022 (accessed on 22 March 2022), including COVID-19 and TB [6]. The province consisted of 38 regencies, with a total population of 39,886,288, in accordance with the the East Java Health Profile. Therefore, the service was managed by East Java Health Officers from January to December 2022. Subsequently, the collected data were represented using graphs and geographical mapping for easier comprehension. COVID-19 cases were defined as all patients with or without symptoms of COVID-19 that were confirmed as positive using Reverse Transcriptase Polymerase Chain Reaction (RT-PCR) methods. Geographical mapping for the distribution of tuberculosis and COVID-19 cases was analyzed using Quantum Geographic Information System (QGIS) version 3.16.14-Hannover.

2.2. Statistical Analysis

All demographic data, together with tuberculosis and COVID-19 cases, were collected and analyzed using Statistical Package for Social Science software. The correlation between the incidence rate and the case fatality rate of tuberculosis and COVID-19 was calculated. An evaluation of the correlation between the case recovery rate and case fatality rate of tuberculosis, as well as the incidence rate and treatment success rate of tuberculosis, was also carried out. Furthermore, the correlation between treatment success rate and case fatality rate of tuberculosis, case recovery rate, and case fatality rate of COVID-19, was determined. We also calculated geographical factors, including the ratio of public health centres, number of doctors, nurses, midwifery, public health workers, environmental health workers, nutritionists, and pharmacists (Tables S1–S3). All the ratios were calculated per 100,000 of the population. These ratios were statistically tested by Pearson Correlation Test. For the sex distribution, the difference between both female and male patients with COVID-19 and tuberculosis was calculated. The data were analyzed using the Spearman correlation test, with a significance value of
p
< 0.05.

2.3. Ethical Clearance

This study used routine/annual surveillance data from regional open platforms, which were provided by the Health Officer of East Java Province. The data were already anonymized; therefore, no ethical clearance was needed.

3. Results

3.1. The Incidence Rate (IR) of Tuberculosis and COVID-19

In this study, the incidence rate of tuberculosis in East Java Province in 2022 was 95.49/100,000 population (Table 1), with a varying case recovery rate (Table 2). The number of cases was higher among males than females (Table 3
and
Table 4). The number for women in East Java in 2022 was 20,374,104, while the number for men was 20,291,592. Among all the residents in East Java, Probolinggo residents have a higher number of females (604) with tuberculosis than males (561). The highest infection rate was discovered in Madiun (296.51/100,000 population), while the lowest was proposed in Malang (0.07/100,000 population) (Table 1). When the data were analyzed according to sex, the incidence rate of tuberculosis in males (117.66/100,000 inhabitants) was higher than in females (93.49/100,000 inhabitants) (Table 3).


Table 1

Distribution of incidence rate (IR) and case fatality rate of TB and COVID-19 in 2022.

No. Regency TB Infection COVID-19 Infection
IR * CFR IR * CFR
1. Pacitan 51.8 1.9% 136.5 2.8%
2. Ponorogo 103.69 1.3% 142.2 4.0%
3. Trenggalek 57.63 0.9% 148.9 4.4%
4. Tulungagung 78.70 1.4% 129.8 2.1%
5. Blitar 55.08 1.7% 156.5 8.0%
6. Kediri 0.1 0.8% 152.8 7.8%
7. Malang 0.07 1.3% 56.5 5.7%
8. Lumajang 0.11 0.8% 230.9 6.6%
9. Jember 0.12 0.7% 180.4 4.7%
10. Banyuwangi 0.12 2.0% 253.4 9.3%
11. Bondowoso 114.54 1.0% 193.1 5.3%
12. Situbondo 142.47 0.7% 248.5 7.0%
13. Probolinggo 0.1 3.2% 188.4 5.1%
14. Pasuruan 0.11 0.8% 133.8 7.2%
15. Sidoarjo 0.11 1.2% 349.7 6.6%
16. Mojokerto 0.1 0.6% 132.0 3.0%
17. Jombang 0.1 1.4% 182.8 10.6%
18. Nganjuk 68.02 1.0% 103.8 9.9%
19. Madiun 86.28 1.8% 57.0 7.4%
20. Magetan 75.04 1.1% 150.1 5.0%
21. Ngawi 90.95 1.4% 71.1 5.9%
22. Bojonegoro 0.11 1.4% 102.8 7.2%
23. Tuban 0.11 1.7% 152.1 10.6%
24. Lamongan 0.13 1.0% 146.0 6.0%
25. Gresik 0.11 1.3% 313.9 6.6%
26. Bangkalan 100.48 0.7% 100.6 9.4%
27. Sampang 82.71 1.2% 52.5 5.2%
28. Pamekasan 82.07 1.2% 86.7 8.1%
29. Sumenep 0.15 2.1% 110.3 6.1%
30. Kediri City 199.92 1.2% 248.3 7.2%
31. Blitar City 166.67 1.1% 467.1 5.4%
32. Malang City 0.16 0.6% 422.8 9.9%
33. Probolinggo city 145.59 7.0% 611.7 7.3%
34. Pasuruan City 258.45 1.1% 497.1 11.0%
35. Mojokerto City 254.06 0.9% 789.9 5.7%
36. Madiun City 296.51 1.6% 227.7 7.7%
37. Surabaya City 0.14 0.4% 625.3 6.9%
38. Batu City 88.46 0.5% 498.7 8.3%
Average 68.44 0.013 232.93 0.067


Table 2

Case recovery rate (CRR) of TB and COVID-19 in East Java Province in 2022.

No. Regency Case Recovery Rate (CRR)
TB (%) COVID-19 (%)
1. Pacitan 81.5 79.71
2. Ponorogo 84.5 81.93
3. Trenggalek 91.2 83.92
4. Tulungagung 64.4 71.86
5. Blitar 75.9 85.61
6. Kediri 92.2 80.49
7. Malang 78.2 92.03
8. Lumajang 52.4 83.58
9. Jember 86 80.96
10. Banyuwangi 76.2 83.24
11. Bondowoso 68.7 90.82
12. Situbondo 85.4 87.61
13. Probolinggo 83.5 85.08
14. Pasuruan 57.8 83.84
15. Sidoarjo 74.3 92.62
16. Mojokerto 78 89.24
17. Jombang 81.1 85.25
18. Nganjuk 74.1 81.58
19. Madiun 73.4 65.89
20. Magetan 96.6 84.74
21. Ngawi 84.9 78.81
22. Bojonegoro 93.1 75.13
23. Tuban 75 64.8
24. Lamongan 82.9 86.52
25. Gresik 76.7 91.59
26. Bangkalan 92.2 74.9
27. Sampang 58.3 83.84
28. Pamekasan 84.5 68.44
29. Sumenep 77.4 74.19
30. Kediri City 74.8 79.53
31. Blitar City 84.3 86.2
32. Malang City 63.2 81.42
33. Probolinggo city 59.6 73.59
34. Pasuruan City 84.6 84.23
35. Mojokerto City 58.7 92.59
36. Madiun City 91.4 75.74
37. Surabaya City 72.5 92.32
38. Batu City 11.3 88.68
Average 75.81 82.17
Baca :   What is Your Name My Name is


Table 3

Distribution of TB and COVID-19 cases according to sex.

No. Regency TB (Number of People) * COVID-19 (Number of People) *
Male Female Male Female
1. Pacitan 170 118 386 373
2. Ponorogo 530 374 674 566
3. Trenggalek 237 165 491 548
4. Tulungagung 463 358 636 718
5. Blitar 366 275 913 908
6. Kediri 815 727 1066 1349
7. Malang 1026 802 761 720
8. Lumajang 630 499 1168 1244
9. Jember 1640 1407 2076 2369
10. Banyuwangi 1119 886 1902 2197
11. Bondowoso 477 415 503 1001
12. Situbondo 531 446 738 966
13. Probolinggo 561 604 926 1287
14. Pasuruan 910 860 1130 1061
15. Sidoarjo 1440 1080 4015 3965
16. Mojokerto 615 465 702 785
17. Jombang 706 582 1057 1262
18. Nganjuk 417 302 500 597
19. Madiun 345 245 198 192
20. Magetan 271 201 456 488
21. Ngawi 441 314 291 299
22. Bojonegoro 820 611 599 688
23. Tuban 714 572 844 946
24. Lamongan 858 637 834 903
25. Gresik 839 624 1878 2285
26. Bangkalan 534 465 507 493
27. Sampang 467 351 234 285
28. Pamekasan 409 320 350 420
29. Sumenep 952 660 480 725
30. Kediri City 319 259 290 428
31. Blitar City 134 104 367 300
32. Malang City 739 638 1817 1882
33. Probolinggo city 177 171 768 694
34. Pasuruan City 289 232 502 500
35. Mojokerto City 189 141 489 537
36. Madiun City 327 199 203 201
37. Surabaya City 2305 1846 8889 9275
38. Batu City 93 92 545 498
Total 23,875 19,047 40,185 43,955


Table 4

The incidence rate of TB and COVID-19 according to sex group.

No. Regency Incidence Rate of TB Incidence Rate of COVID-19
Male Female Male Female
1. Pacitan 57.88 40.36 131.42 127.57
2. Ponorogo 111.75 78.73 142.12 119.14
3. Trenggalek 64.51 45.36 133.65 150.65
4. Tulungagung 84.91 65.75 116.64 131.86
5. Blitar 59.37 45.29 148.09 149.53
6. Kediri 98.68 89.82 129.08 166.66
7. Malang 76.69 60.91 56.88 54.68
8. Lumajang 113.81 88.21 210.99 219.91
9. Jember 129.65 110.63 164.11 186.28
10. Banyuwangi 130.84 103.88 222.40 257.59
11. Bondowoso 124.80 105.35 131.60 254.11
12. Situbondo 157.68 127.72 219.15 276.62
13. Probolinggo 98.65 103.45 162.83 220.43
14. Pasuruan 113.22 107.20 140.59 132.25
15. Sidoarjo 137.33 104.43 382.90 383.38
16. Mojokerto 109.25 83.59 124.70 141.12
17. Jombang 106.23 89.06 159.04 193.13
18. Nganjuk 75.10 55.05 90.04 108.82
19. Madiun 93.52 65.26 53.67 51.14
20. Magetan 82.12 58.98 138.17 143.20
21. Ngawi 102.09 71.68 67.37 68.25
22. Bojonegoro 125.44 94.30 91.63 106.18
23. Tuban 119.33 95.39 141.06 157.75
24. Lamongan 127.55 94.87 123.98 134.48
25. Gresik 127.07 95.86 284.42 351.04
26. Bangkalan 102.15 86.50 96.98 91.70
27. Sampang 96.95 71.92 48.58 58.40
28. Pamekasan 98.09 73.89 83.94 96.98
29. Sumenep 175.41 113.46 88.44 124.63
30. Kediri City 222.12 180.89 201.93 298.92
31. Blitar City 180.55 138.79 494.50 400.36
32. Malang City 175.99 150.50 432.72 443.96
33. Probolinggo city 148.95 141.53 646.31 574.41
34. Pasuruan City 277.76 223.16 482.48 480.95
35. Mojokerto City 287.74 211.24 744.46 804.51
36. Madiun City 342.62 199.53 212.69 201.54
37. Surabaya City 161.74 127.39 623.72 640.03
38. Batu City 86.67 87.00 507.92 470.94
Average 131.16 102.29 221.87 236.13

The regency with the highest tuberculosis incidence rate in males was Madiun (342.62/100,000 population), while the lowest rate was found in Pacitan (57.88/100,000 population) (Table 3). For females, the regency with the highest incidence rate of tuberculosis was Pasuruan (223.16/100,000 inhabitants) and the lowest rate was discovered in Pacitan (93.49/100,000 inhabitants) (Table 3). The highest incidence rate of COVID-19 infection was discovered in Mojokerto (789.9/100,000 populations), while the lowest was found in Sampang (52.5/100,000 populations) (Table 1). An analysis based on sex showed that the incidence rate of COVID-19 in females (215.74/100,000 inhabitants) was higher than in males (198.04/100,000 inhabitants). Meanwhile, the regency with the highest rate of males was Mojokerto (744.46/100,000 inhabitants), while the lowest rate was found in Sampang (48.58/100,000 inhabitants) (Table 3). The regency with the highest incidence rate of COVID-19 in females was Mojokerto (804.51/100,000 inhabitants), while the lowest rate was found in Madiun (51.14/100,000 inhabitants) (Table 4).

3.2. The Case Fatality Rate (CFR) of Tuberculosis and COVID-19

The overall case fatality rate of tuberculosis in East Java Province in Indonesia was 3.6%. The highest CFR of TB infection was discovered in Probolinggo (7%), while the lowest was found in Surabaya (0.4%). Meanwhile, the highest CFR of COVID-19 infection was obtained in Pasuruan (11%), while the lowest was found in Tulungagung 2.1% (Table 1).

3.3. Case Recovery Rate (CRR) of Tuberculosis and COVID-19

The case recovery rate of tuberculosis was defined as patients with positive examination results upon treatment, bacteriological examination results at the end of treatment, and at one of the previous examinations.

The highest case recovery rate for tuberculosis was discovered in Magetan (96.6%), while the lowest was obtained in Batu City (11.3%). Meanwhile, the case recovery rate of COVID-19 was defined as COVID-19 patients with positive results at the beginning of RT-PCR, and negative results at the end of the examination. The highest case recovery rate of COVID-19 was found in Sidoarjo (92.6%), while the lowest was discovered in Tuban (64.5%) (Table 2).

3.4. The Treatment Success Rate (TSR) of Tuberculosis

The treatment success rate of tuberculosis is defined as the number of patients in all cured cases and complete treatment among treated and reported cases. In this study, the highest treatment success rate of tuberculosis was found in Magetan (95.97%), while the lowest was found in Bondowoso (65.89%) (Table 5).


Table 5

The treatment success rate of TB in 2022.

No. Regency Treatment Success Rate Tuberculosis (%)
1. Pacitan 82.96%
2. Ponorogo 85.49%
3. Trenggalek 94.03%
4. Tulungagung 89.20%
5. Blitar 88.85%
6. Kediri 79.65%
7. Malang 86.06%
8. Lumajang 92.27%
9. Jember 87.55%
10. Banyuwangi 90.17%
11. Bondowoso 65.89%
12. Situbondo 93.28%
13. Probolinggo 91.41%
14. Pasuruan 89.34%
15. Sidoarjo 91.08%
16. Mojokerto 89.40%
17. Jombang 88.02%
18. Nganjuk 79.17%
19. Madiun 89.82%
20. Magetan 95.97%
21. Ngawi 92.54%
22. Bojonegoro 93.57%
23. Tuban 92.33%
24. Lamongan 94.89%
25. Gresik 91.69%
26. Bangkalan 92.26%
27. Sampang 85.67%
28. Pamekasan 90.58%
29. Sumenep 89.44%
30. Kediri City 95.46%
31. Blitar City 81.07%
32. Malang City 85.14%
33. Probolinggo city 72.69%
34. Pasuruan City 91.51%
35. Mojokerto City 81.05%
36. Madiun City 93.66%
37. Surabaya City 90.61%
38. Batu City 71.78%
Average 87.78%

3.5. The Age Group of COVID-19 Cases

Based on age group, the highest number of COVID-19 cases was found in those between 46 to 59 years old (23,947 individuals), while the lowest was found in those between 3 and 6 years old (771 individuals) (Figure 1).


The distribution of COVID-19 cases based on age group.

3.6. The Correlation Test

The analysis of data with Spearman correlation showed no significant correlation between the incidence rate and case fatality rate of tuberculosis (p
= 0.912,
p
> 0.05) (Table 6). It was also discovered that there was no significant correlation between incidence rate and case fatality rate for COVID-19 (p
= 0.219,
p
> 0.05), the case recovery rate and case fatality rate for tuberculosis (p
= 0.698,
p
> 0.05), the incidence rate and treatment success rate for tuberculosis (p
= 0.795,
p
> 0.05), the treatment success rate and case fatality rate for tuberculosis (p
= 0.659,
p
> 0.05), and the case recovery rate and case fatality rate for COVID-19 (p
= 0.164,
p
> 0.05). The difference between the number of male and female patients with tuberculosis (p
= 0.202,
p
> 0.05) and COVID-19 (p
= 0.942,
p
> 0.05) was not significant (Table 6). In this study, we also calculated the geographical data consisting of the ratio number of public health centers, doctors, nurses, midwifery, public health workers, environmental health workers, nutritionists and pharmacists, and also the incidence rate of HIV in these areas (Tables S1–S3).
Table 7
shows that the total number of health workers per 100,000 populations was significantly correlated with the incidence rate of tuberculosis (p
< 0.05). These variables demonstrate a positive correlation with the tuberculosis incidence rate. Surprisingly, the incidence rate of HIV was also correlated with the incidence rate of TB (p
< 0.05) (Table 7). However, the case recovery rate between TB and case recovery rate of COVID-19 was also significantly different (Table 8). While in COVID-19 aspect, the incidence rate of COVID-19 was also significantly correlated with the incidence rate of HIV and the number of health workers (doctor, nurse, public health workers, environmental health workers, nutritionist, and pharmacist) (Table 9).


Table 6

The Results of Spearman Correlation and Mann–Whitney test.

Spearman Correlation Test (p-Value Was Calculated as Significant If
p
< 0.05)

p-Value
CFR_TB CFR_COVID-19 TSR_TB
IR_TB 0.912 0.795
IR_COVID-19 0.219
CRR_TB 0.698
CRR_COVID-19 0.164
IR_TB 0.795
CFR_TB 0.659
Mann–Whitney Test

p-Value
IR_TB_Female IR_COVID-19_Female
IR_TB_Male 0.202
IR_COVID-19 Male 0.942


Table 7

The results of Pearson correlation test of demographical factors related to the incidence rate of TB.

Bivariate Analysis of Geographical Factors with the Incidence Rate of Tuberculosis Correlation between Two Variables
Variables p-Value r-Correlation
Ratio of public health centre 0.001 * 0.53 Strong positive correlation
Ratio of doctor 0.000 * 0.65 Strong positive correlation
Ratio of nurse 0.000 * 0.70 Strong positive correlation
Ratio of midwifery 0.000 * 0.74 Strong positive correlation
Ratio of public health workers 0.002 * 0.49 Enough positive correlation
Ratio of environmental health workers 0.000 * 0.71 Strong positive correlation
Ratio of nutrinionist 0.000 * 0.72 Strong positive correlation
Ratio of pharmacist 0.000 * 0.67 Strong positive correlation
Incidence rate of HIV 0.002 * 0.48 Enough positive correlation


Table 8

The results of Mann–Whitney test for the comparison between case recovery rate of tuberculosis and case recovery rate of COVID-19.

p-Value of Mann–Whitney Test between Case Recovery Rate of TB and Case Recovery Rate of COVID-19
p-Value
CRR TB 0.051


Table 9

The results of Pearson Correlation test of demographical factors related to the incidence rate of COVID-19.

Bivariate Analysis of Geographical Factors with the Incidence Rate of COVID-19 Correlation between Two Variables
Variables p-Value r-Correlation
Ratio of public health centre 0.44 0.13 Very low positive correlation
Ratio of doctor 0.001 * 0.7 Strong positive correlation
Ratio of nurse 0.001 * 0.64 Strong positive correlation
Ratio of midwifery 0.27 0.18 Very low positive correlation
Ratio of public health workers 0.01 * 0.42 Enough positive correlation
Ratio of environmental health workers 0.01 * 0.41 Enough positive correlation
Ratio of nutrinionist 0.001 * 0.56 Strong positive correlation
Ratio of pharmacist 0.001 * 0.55 Strong positive correlation
Incidence rate of HIV 0.002 * 0.49 Enough positive correlation
Baca :   Tata Ruang Rapat Harus Disesuaikan Dengan

3.7. Interpretation by Quantum Geographic Information System (QGIS) Application

The geographical maps of the incidence of tuberculosis and COVID-19 are shown in
Figure 2
and
Figure 3.


An external file that holds a picture, illustration, etc.
Object name is tropicalmed-07-00083-g002.jpg

The geographical map of tuberculosis distribution in East Java Province in 2022.


An external file that holds a picture, illustration, etc.
Object name is tropicalmed-07-00083-g003.jpg

The geographical map of COVID-19 distribution in East Java Province in 2022.

4. Discussion

This study showed no significant correlation between the incidence rate and case fatality rate for tuberculosis (p
= 0.912;
p
< 0.05). The incidence rate of tuberculosis in East Java Province (586.24/100,000 inhabitants) in 2022 was higher than the national incidence rate (301/100,000 inhabitants). Furthermore, there was a decreasing incidence rate of tuberculosis in 2022 (95.49/100,000 inhabitants) compared to that in 2022 (95.925/100,000 inhabitants) [7]. The global incidence rate of tuberculosis in 2022 was 127/100,000 inhabitants [8]. This showed that the incidence rate in East Java needs to be properly managed. Meanwhile, one of the global milestones proposed by the World Health Organization (WHO) in 2022 is the reduction in incidence rate and tuberculosis deaths by 20% and 35%, respectively [8]. The overall case fatality rate of tuberculosis in East Java Province in 2022 was 3.6/100,000 inhabitants, while in 2022, it was 3.8/100,000 inhabitants [6].

The decrease in the incidence rate of tuberculosis was also in line with another report, where the global data showed a decline in three of the six WHO regions, namely Southeast Asia, the Eastern Mediterranean, and the Western Pacific. In 2022, Indonesia was one of the eight countries that reported a high TB rate, with an estimated incidence of, (1) India (26%), (2) China (8.5%), (3) Indonesia (8.4%), (4) the Philippines (6.0%), (5) Pakistan (5.8%), (6) Nigeria (4.6%), (7) Bangladesh (3.6%), and (8) South Africa (3.3%). The results showed that the incidence of tuberculosis was higher in men than in women. This is in line with the global data in 2022, which showed a tuberculosis rate of 56% in men, 33% in women, and 11% in children [8]. Moreover, these values were also obtained in the national tuberculosis survey in Vietnam [9].

The elimination of tuberculosis depends on the treatment success rate of infected people. In this study, some regencies in East Java with were discovered to have a TSR value below the target (<90%). A total of 20 regencies with a TSR of below 90% need to benefit from public health promotion and sensitize tuberculosis patients to complete their treatment. Indonesia can adopt one of the efforts used to increase the treatment success/completion rate in India through Private Provider Interface Agencies (PPIAs). In India, the effort was effective in increasing tuberculosis notification rates, testing, and treatment success rates [10,11]. PPIAs can provide interventions related to patient care, training physicians, tuberculosis diagnostics, treatment monitoring, and tuberculosis medicines [12].

Tuberculosis and COVID-19 are airborne diseases; the infection affects the lungs and has similar symptoms. Moreover, COVID-19 symptoms include fever or chills, cough, shortness of breath or difficulty breathing, fatigue and headache, muscle or body aches, loss of new taste or smell, sore throat, stuffy or runny nose, nausea, vomiting, and diarrhea. Meanwhile, tuberculosis symptoms are coughing up phlegm or blood, a cough that lasts more than 2 months, appetite and weight loss, chest pain, chills, fever or night sweats, and fatigue [13]. Previous studies have demonstrated an association between tuberculosis and COVID-19. Both active and a previous history of tuberculosis seem to be related to an increased risk for the development of COVID-19, and aggravate the prognosis of infection [11,14,15,16,17,18]. The damage caused by TB infection in the lungs exacerbates its impact on local immunity and increases the body’s susceptibility to airborne pathogens [19]. This increases the risk of COVID-19 developing in patients with a current or previous history of TB. Tuberculosis was found to be associated with a 2.10-fold increase in the risk of severe COVID-19 disease. In patients with previous respiratory disease, lung function can be impaired and a low resistance to viral infections can form, which can develop into acute respiratory distress syndrome (ARDS) [20,21].

In 2022, when all countries were affected by COVID-19, it was reported that there were 84,140 cases in East Java, Indonesia, where the number of infected females was higher than the number for males. This was not in line with the report from Peru, where the incidence rate in females was higher than in that males. COVID-19 can affect any age group due to its fast transmission rate; however, this study discovered that the highest incidence rate was in the age group between 46 and 59 years old. This was in line with the national survey in Peru, where the highest incidence was in people older than 50 years [22].

The elimination of tuberculosis has three pillars and components, namely: (1) integrated, patient-centered care, and prevention, (2) bold policies and supportive systems, (3) and intensified research and innovation. The first pillars can be translated into four activities: (a) early diagnosis of tuberculosis, including testing on universal drug susceptibility, screening of close contact groups, (b) treating and supporting people with tuberculosis to complete their treatment, (c) collaborative care that manages the comorbidities, (d) preventive treatment of people at high risk [8].

COVID-19 and tuberculosis data showed that there is a possibility of coinfection in a patient, where an individual can simultaneously be affected by both illnesses. However, the limitation of this study is its inability to capture co-infected patients or those who are only infected with one of the diseases. Therefore, clinicians should be concerned with chronic diseases in patients, such as coinfection with both COVID-19 and tuberculosis. This is because the coinfection with both diseases was already reported by studies in China [23,24], USA [25], and Italy [15,26], with various clinical characteristics.

Coinfection between tuberculosis and COVID-19 could have an important impact on the public health sector. In another case, public health also has an important role in combatting COVID-19 through various interventions, including physical distancing, self-quarantine, travel restrictions, a semi-lockdown, practicing good personal hygiene, eating nutritious food, increasing case-tracking, and vaccine development [27]. People with underlying respiratory diseases should be considered during the pandemic, to prevent its exacerbation [28].

Lung macrostructural changes caused by pulmonary tuberculosis affect the function and defence of the lower respiratory tract. This condition can be complicated due to the consequences of the inflammatory response exacerbated by SARS-CoV-2, such as oedema [18,29,30]. The reported complications of tuberculosis with COVID-19 coinfection that are hypoxemia, respiratory failure, acute respiratory distress syndrome (ARDS), the need for non-invasive ventilation, glucose abnormalities, and longer lengths of hospital stay, with a maximum of 130 days, and recurrent or concurrent bacterial infections [19,31,32,33,34]. The risk of recovery in COVID-19 patients with tuberculosis is 25% lower [16]. Meanwhile, the risk of mortality for COVID-19 patients with early treatment of pulmonary tuberculosis is 2.5 times higher, and a previous history of tuberculosis has a 50% higher mortality risk [17].

Previous studies showed that pulmonary tuberculosis patients had an increased susceptibility to COVID-19 infection and showed an increase in the severity of symptom development [14]. Cumulative research has reported 80 pulmonary tuberculosis patients with COVID-19 coinfection from China, India, Belgium, Brazil, France, Italy, Russia, Spain, Switzerland and Singapore. The highest case of tuberculosis sufferers presenting with COVID-19 coinfection occurred in Italy [35].

One of the principal efforts to suppress the transmission of tuberculosis in a community is the active case finding (ACF). Case finding could be deciphering this kind of activity, including house-to-house surveys, massive surveillance, increasing case-finding, and out-patient case detection, specifically in high-risk groups [36]. Historical results showed that mass radiography could screen 2000 cases in over 2 million individuals [37]. Sufficient case finding could lead to the successfully treatment of tuberculosis. In certain cases, case-finding could also find HIV-TB-coinfected patients, as mentioned in Nigeria, which could locate 109 HIV-TB infected patients. In Nigeria, successful treatment was proven to be associated with newly registered patients [38].

Health facilities were also a predictor of the treatment success rate for tuberculosis. According to this, intersectoral collaborations with the private sector should be increased. As in another report, private health facilities had a more successful treatment rate than public health facilities [39,40]. The other challenge in tuberculosis management was drug resistance; interestingly, if the treatment success rate reaches 85%, this could lead to a reduction in transmission, drug resistance, TB prevalence, and TB incidence. In East Java Province, the number of health facilities, specifically primary health centers, is 968 units. However, not all primary health centers have the same capacity to tackle tuberculosis, especially during the pandemic, when the all the health facilities were focused on COVID-19. In addition, Indonesia also had an endemic for another tropical disease, which was neglected [41].

Drug resistance in tuberculosis become a challenge in TB management, due to the increasing number of mechanisms that were involved. This phenomenon led to difficultes in the development of diagnostic procedures. However, whole-genome sequencing (WGS) may can help to identify polymorphisms related to drug resistance. In another case, the capacity of laboratories which can conduct WGS in developing countries is still limited [42]. During the pandemic, whole-genome sequencing (WGS) was introduced, specifically to understand the new variant of COVID-19, which continuously increased. According to the latest information, the COVID-19 variants can be classified into three groups, namely, variants of concern (VOC), variants of interest (VOI) and high-consequence variants (VOHC). This classification was formulated according to the capacity and the impact on global public health [41].

5. Conclusions

In conclusion, these respiratory diseases still need to be evaluated, specifically in a clinical setting. Although there have been major advances in infectious disease control in recent years, the number of infectious diseases, including TB and COVID-19 in East Java Province, is still a concern. Therefore, a retrospective study was carried out to evaluate the recent epidemiology of the infectious disease in East Java, which is the second largest province in Indonesia and consisted of 38 regencies with large populations. The results showed that the incidence rate of tuberculosis was higher in males than females, while the rate of COVID-19 was higher in females than in males. The highest cases of COVID-19 were discovered in the age group between 46 and 59 years old. The highest COVID-19 incidence rate was found in Mojokerto City, while the lowest was found in Sampang. Tuberculosis and COVID-19 are the pulmonary diseases which need to be considered. According to this study, the treatment success rate of tuberculosis needs to be improved to achieve a decline in case fatality rates and transmission in the community. During the pandemic, it is important to increase active tuberculosis case detection in order to minimize community transmission.

Acknowledgments

We would like thanks to the Universitas Airlangga that was provided research funding under Satu Joint Research Scheme with the number of funding grant no. 525/UN3/2022, and also Satu Joint Research Scheme Universiti Malaya (ST039-2022).

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/tropicalmed7060083/s1, Table S1. The demographical factor analysis (Ratio number of public health center, ratio number of doctor, and ratio number of nurse/100,000 populations); Table S2. The demographical factor analysis (Ratio number of midwifery, ratio number of public health workers, and ratio number of environmental health workers/100,000 populations); Table S3. The demographical factor analysis (Ratio number of nutritionist, ratio number of pharmacist, and incidence rate of HIV/100,000 populations).

Funding Statement

The present study was supported by a grant from the Satu Joint Research Scheme Universitas Airlangga (grant no. 525/UN3/2022) and Satu Joint Research Scheme Universiti Malaya (ST039-2022).

Author Contributions

Conceptualization: B.U., S.S. and N.M.M.; data curation: S.F. and I.M.D.M.A.; formal analysis: B.U.; funding acquisition: B.U. and C.K.C.; investigation: F.A. and D.S.E.; methodology: B.U.; project administration: T.H.S. and S.F.; resources: B.U. and C.K.C.; software: B.U. and S.F.; supervision: B.U. and C.K.C.; validation: B.U. and T.H.S.; visualization: T.H.S.; writing—original draft preparation: B.U., C.K.C., S.S., S.F., T.H.S., F.A., I.M.D.M.A. and D.S.E.; writing—review and editing: B.U., C.K.C., S.S., S.F., T.H.S., F.A., I.M.D.M.A. and D.S.E. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets used and/or analysed during the present study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Footnotes

Publisher’s Note:
MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

3.
Coronel Teixeira R., Aguirre S., Pérez Bejarano D. Thinking about Tuberculosis in Times of COVID-19.

J. Intern. Med.
2022;289:589–590. doi: 10.1111/joim.13192.

[PubMed] [CrossRef]
[Google Scholar]

4.
Wingfield T., Karmadwala F., MacPherson P., Millington K.A., Walker N.F., Cuevas L.E., Squire S.B. Challenges and Opportunities to End Tuberculosis in the COVID-19 Era.

Lancet Respir. Med.
2022;9:556–558. doi: 10.1016/S2213-2600(21)00161-2.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

5.
Wang G., Cai L., Chen D., Teng T., Li Q., Xie L. Influence of COVID-19 in Patients with Concurrent Tuberculosis Coinfections.

J. Med. Virol.
2022;93:1937–1939. doi: 10.1002/jmv.26801.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

8.
World Health Organization .
Global Tuberculosis Report 2022.
World Health Organization; Geneva, Switzerland: 2022.
[Google Scholar]

9.
Nguyen H.V., Tiemersma E.W., Nguyen H.B., Cobelens F.G.J., Finlay A., Glaziou P., Dao C.H., Mirtskhulava V., Nguyen H.V., Pham H.T.T., et al. The Second National Tuberculosis Prevalence Survey in Vietnam.

PLoS ONE.
2022;15:e0232142. doi: 10.1371/journal.pone.0236532.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

11.
Mistry N., Shah S., Shah S., Rangan S., Rai S., Lobo E., Kamble S., Dholakia Y. Effect of Public-Private Interface Agency in Patna and Mumbai, India: Does It Alter Durations and Delays in Care Seeking for Drug-Sensitive Pulmonary Tuberculosis?

Gates Open Res.
2022;4:32. doi: 10.12688/gatesopenres.13113.1.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

12.
Wells W.A., Uplekar M., Pai M. Achieving Systemic and Scalable Private Sector Engagement in Tuberculosis Care and Prevention in Asia.

PLoS Med.
2015;12:e1001842. doi: 10.1371/journal.pmed.1001842.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

13.
Visca D., Ong C.W.M., Tiberi S., Centis R., D’Ambrosio L., Chen B., Mueller J., Mueller P., Duarte R., Dalcolmo M., et al. Tuberculosis and COVID-19 Interaction: A Review of Biological, Clinical and Public Health Effects.

Pulmonology.
2022;27:151–165. doi: 10.1016/j.pulmoe.2022.12.012.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

14.
Chen Y., Wang Y., Fleming J., Yu Y., Gu Y., Liu C., Fan L., Wang X., Cheng M., Bi L., et al. Active or Latent Tuberculosis Increases Susceptibility to COVID-19 and Disease Severity.

MedRxiv.
2022;6:1–13. doi: 10.1101/2022.03.10.20033795.

[CrossRef]
[Google Scholar]

15.
Stochino C., Villa S., Zucchi P., Parravicini P., Gori A., Raviglione M.C. Clinical Characteristics of COVID-19 and Active Tuberculosis Co-Infection in an Italian Reference Hospital.

Eur. Respir. J.
2022;56
doi: 10.1183/13993003.01708-2022.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

16.
Sy K.T.L., Haw N.J.L., Uy J. Previous and Active Tuberculosis Increases Risk of Death and Prolongs Recovery in Patients with COVID-19.

Infect. Dis.
2022;52:902–907. doi: 10.1080/23744235.2022.1806353.

[PubMed] [CrossRef]
[Google Scholar]

17.
Davies M.-A. HIV and Risk of COVID-19 Death: A Population Cohort Study from the Western Cape Province, South Africa.

medRxiv Prepr. Serv. Health Sci.
2022:1–21. doi: 10.1101/2022.07.02.20145185.

[CrossRef]
[Google Scholar]

18.
Mousquer G.T., Peres A., Fiegenbaum M. Pathology of TB/COVID-19 Co-Infection: The Phantom Menace.

Tuberculosis.
2022;126:102022. doi: 10.1016/j.tube.2022.102022.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

19.
Tadolini M., Codecasa L.R., García-García J.M., Blanc F.X., Borisov S., Alffenaar J.W., Andréjak C., Bachez P., Bart P.A., Belilovski E., et al. Active Tuberculosis, Sequelae and COVID-19 Co-Infection: First Cohort of 49 Cases.

Eur. Respir. J.
2022;56
doi: 10.1183/13993003.01398-2022.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

20.
Gao Y., Liu M., Chen Y., Shi S., Geng J., Tian J. Association between Tuberculosis and COVID-19 Severity and Mortality: A Rapid Systematic Review and Meta-Analysis.

J. Med. Virol.
2022;93:194–196. doi: 10.1002/jmv.26311.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

21.
Zheng Z., Peng F., Xu B., Zhao J., Liu H., Peng J., Li Q., Jiang C., Zhou Y., Liu S., et al. Risk Factors of Critical & Mortal COVID-19 Cases: A Systematic Literature Review and Meta-Analysis.

J. Infect.
2022;81:e16–e25. doi: 10.1016/j.jinf.2022.04.021.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

22.
Ramírez-Soto M.C., Arroyo-Hernández H., Ortega-Cáceres G. Sex Differences in the Incidence, Mortality, and Fatality of COVID-19 in Peru.

PLoS ONE.
2022;16:10–19. doi: 10.1371/journal.pone.0253193.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

23.
Chen Z.Y.J., Wang Q., Liu W., Nan Q.Z.J., Huang H., Wu Y., Li L., Liang L., You L., Liu Y., et al. Three Patients with COVID-19 and Pulmonary Tuberculosis, Wuhan, China, January-February 2022.

Emerg. Infect. Dis.
2022;26:2754–2757. doi: 10.3201/EID2611.201536.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

24.
He G., Wu J., Shi J., Dai J., Gamber M., Jiang X., Sun W., Cai J. COVID-19 in Tuberculosis Patients: A Report of Three Cases.

J. Med. Virol.
2022;92:1802–1806. doi: 10.1002/jmv.25943.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

25.
Narita M., Hatt G., Gardner Toren K., Vuong K., Pecha M., Jereb J.A., Goswami N.D. Delayed Tuberculosis Diagnoses during the COVID-19 Pandemic in 2022—King County, Washington Masahiro.

Clin. Infect. Dis.
2022;15:S74–S76. doi: 10.1093/cid/ciab387.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

26.
Petrone L., Petruccioli E., Vanini V., Cuzzi G., Gualano G., Vittozzi P., Nicastri E., Maffongelli G., Grifoni A., Sette A., et al. Coinfection of Tuberculosis and COVID-19 Limits the Ability to in Vitro Respond to SARS-CoV-2.

Int. J. Infect. Dis.
2022;113:S82–S87. doi: 10.1016/j.ijid.2022.02.090.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

27.
Yamani L.N., Syahrul F. Public Health Perspective of the COVID-19 Pandemic: Host Characteristics and Prevention of COVID-19 in the Community (Review)

World Acad. Sci. J.
2022;2
doi: 10.3892/wasj.2022.62.

[CrossRef]
[Google Scholar]

28.
Bolaki M., Tsitoura E., Spandidos D., Symvoulakis E., Antoniou K. Respiratory Diseases in the Era of Covid-19: Pearls and Pitfalls.

Exp. Ther. Med.
2022;20:691–693. doi: 10.3892/etm.2022.8776.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

29.
Li G., Fan Y., Lai Y., Han T., Li Z., Zhou P., Pan P., Wang W., Hu D., Liu X., et al. Coronavirus Infections and Immune Responses.

J. Med. Virol.
2022;92:424–432. doi: 10.1002/jmv.25685.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

30.
Qin C., Zhou L., Hu Z., Zhang S., Yang S., Tao Y., Xie C., Ma K., Shang K., Wang W., et al. Dysregulation of Immune Response in Patients with Coronavirus 2022 (COVID-19) in Wuhan, China.

Clin. Infect. Dis.
2022;71:762–768. doi: 10.1093/cid/ciaa248.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

31.
Mishra A.K., Lal A., Sahu K.K., Sargent J. Cardiovascular Factors Predicting Poor Outcome in COVID-19 Patients.

Cardiovasc. Pathol.
2022;49:107246. doi: 10.1016/j.carpath.2022.107246.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

32.
Motta I., Centis R., D’Ambrosio L., García-García J.-M., Goletti D., Gualano G., Lipani F., Palmieri F., Sánchez-Montalvá A., Pontali E., et al. Tuberculosis, COVID-19 and Migrants: Preliminary Analysis of Deaths Occurring in 69 Patients from Two Cohorts.

Pulmonology.
2022;26:233–240. doi: 10.1016/j.pulmoe.2022.05.002.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

33.
Xiao F., Tang M., Zheng X., Liu Y., Li X., Shan H. Evidence for Gastrointestinal Infection of SARS-CoV-2.

Gastroenterology.
2022;158:1831–1833.e3. doi: 10.1053/j.gastro.2022.02.055.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

34.
Khurana A.K., Aggarwal D. The (in)Significance of TB and COVID-19 Co-Infection.

Eur. Respir. J.
2022;56
doi: 10.1183/13993003.02105-2022.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

35.
Mishra A., George A.A., Sahu K.K., Lal A., Abraham G. Tuberculosis and COVID-19 Co-Infection: An Updated Review.

Acta Biomed.
2022;92:e2022025. doi: 10.23750/abm.v92i1.10738.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

36.
Golub J.E., Mohan C.I., Comstock G.W., Chaisson R.E. Active Case Finding of Tuberculosis: Historical Perspective and Future Prospects.

Int. J. Tuberc. Lung. Dis.
2005;9:1183–1203.

[PMC free article]
[PubMed]
[Google Scholar]

37.
Horwitz O., Darrow M.M. Principles and Effects of Mass Screening: Danish Experience in Tuberculosis Screening.

Public Health Rep.
1976;91:146.

[PMC free article]
[PubMed]
[Google Scholar]

38.
Akanbi K., Ajayi I., Fayemiwo S., Gidado S., Oladimeji A., Nsubuga P. Predictors of Tuberculosis Treatment Success among HIV- TB Co-Infected Patients Attending Major Tuberculosis Treatment Sites in Abeokuta, Ogun State, Nigeria.

Pan. Afr. Med. J.
2022;32:7–10. doi: 10.11604/pamj.supp.2022.32.1.13272.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

39.
Gidado M., Ejembi C.L. Tuberculosis Case Management and Treatment Outcome: Assessment of the Effectiveness of Public—Private Mix of Tuberculosis Programme in Kaduna State, Nigeria.

Ann. Afr. Med.
2009;8:25–31. doi: 10.4103/1596-3519.55760.

[PubMed] [CrossRef]
[Google Scholar]

40.
Adejumo O., Daniel O., Otesanya A., Salisu-Olatunj S., Abdur-Razzaq H. Evaluation of Outcomes of Tuberculosis Management in Private for Profit and Private-Not-for Profit Directly Observed Treatment Short Course Facilities in Lagos State, Nigeria.

Niger. Med. J.
2017;58:44. doi: 10.4103/0300-1652.218417.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

41.
Fauziyah S., Miliyani S., Putri D.W.I., Salma Z., Wardhani H.R. How Should Indonesia Consider Its Neglected Tropical Diseases in the COVID-19 Era? Hopes and Challenges (Review)

Biomed. Rep.
2022;14:1–10. doi: 10.3892/br.2022.1429.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]

42.
Wibawa H., Hakim M.S., Trisnawati I., Khair R.E., Triasih R., Iskandar K., Anggorowati N., Daniwijaya E.W., Supriyati E., Nugrahaningsih D.A.A., et al. Molecular Epidemiology of SARS-CoV-2 Isolated from COVID-19 Family Clusters.

BMC Med. Genom.
2022;14:144. doi: 10.1186/s12920-021-00990-3.

[PMC free article]
[PubMed] [CrossRef]
[Google Scholar]


Articles from
Tropical Medicine and Infectious Disease
are provided here courtesy of
Multidisciplinary Digital Publishing Institute (MDPI)


Akademi Analis Kesehatan Delima Husada Gresik

Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230370/

Artikel Terkait

Leave a Comment