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The International Journal of Tuberculosis and Lung Disease logoLink to The International Journal of Tuberculosis and Lung Disease
. 2023 Sep 1;27(9):694–702. doi: 10.5588/ijtld.22.0668

Survival of people with untreated TB: effects of time, geography and setting

C A Rodriguez 1, S V Leavitt 2, T C Bouton 3,4, C R Horsburgh 1,2, P Abel zur Wiesch 5,6, B Nichols 7, H E Jenkins 2, L F White 2,
PMCID: PMC10443783  PMID: 37608480

Abstract

BACKGROUND:

An estimated 40% of people who developed TB in 2021 were not diagnosed or treated. Pre-chemotherapy era data are a rich resource on survival of people with untreated TB. We aimed to identify heterogeneities in these data to inform their more precise use.

METHODS:

We extracted survival data from pre-chemotherapy era papers reporting TB-specific mortality and/or natural recovery data. We used Bayesian parametric survival analysis to model the survival distribution, stratifying by geography (North America vs. Europe), time (pre-1930 vs. post-1930), and setting (sanitoria vs. non-sanitoria).

RESULTS:

We found 12 studies with TB-specific mortality data. Ten-year survival was 69% in North America (95% CI 54–81) and 36% in Europe (95% CI 10–71). Only 38% (95% CI 18–63) of non-sanitorium individuals survived to 10 years compared to 69% (95% CI 41–87) of sanitoria/hospitalized patients. There were no significant differences between people diagnosed pre-1930 and post-1930 (5-year survival pre-1930: 65%, 95% CI 44–88 vs. post-1930: 72%, 95% CI 41–94).

CONCLUSIONS:

Mortality and natural recovery risks vary substantially by location and setting. These heterogeneities need to be considered when using pre-chemotherapy data to make inferences about expected survival of people with undiagnosed TB.

Keywords: mortality, self-cure, natural recovery, Bayesian analysis, survival analysis


Low case detection and failure to cure those treated are major drivers of TB mortality and transmission.1 Clinical outcomes of individuals with untreated TB are important from a public health perspective and in modelling studies.

Several studies have mined the pre-chemotherapy era TB literature to understand outcomes for people with untreated TB;24 however, these studies are not homogeneous. They span decades during which tumultuous events occurred (e.g., World Wars, the Great Depression), sanatoria were used for treatment to varying degrees, studies were carried out in differing geographic regions (North America and Europe), and the quality and availability of medical care increased over time. TB outcomes among untreated individuals could vary significantly according to these factors.

Here, we use pre-chemotherapy era studies that recorded mortality and natural recovery outcomes to estimate TB mortality rates overall and by geographic and temporal context. We also aimed to explore outcome differences between sanitoria patients vs. those not in sanitoria.

METHODS

Search strategy

Since the development of anti-TB chemotherapy in the mid-twentieth century, studies reporting outcomes of untreated populations are unethical and pre-chemotherapy era studies are often not indexed in databases (e.g. PubMed, EMBASE). Therefore, we reviewed our personal libraries, which include publications of pre-chemotherapy era cohorts from a previous study,4 and publications used by Tiemersma, et al.2 in a similar review to this current study (Supplementary Table S1). We also reviewed the reference lists of these publications for further sources, and reference lists of those papers to capture additional data.

Review of studies

We included cohort studies comprised of TB patients who did not receive anti-TB chemotherapy, and that reported the proportion of the cohort within specified time interval(s) with the following four outcomes: died from TB, died from a non-TB cause, naturally recovered, and lost to follow-up (Supplementary Figure S1). Outcome definitions would depend on specific publications and are included in the results section and Supplementary Table S2. ‘Natural recovery’ in this literature was not clinically well-defined, and our definition had to be driven by publications that we identified. However, natural recovery likely included patients who no longer had detectable Mycobacterium tuberculosis in sputum smears, were able to work, or had symptom resolution.5

We excluded publications that were not about TB, did not contain data on natural recovery or TB-specific mortality, were restricted to patients with specific forms of TB (e.g., TB meningitis) or narrow age groups (e.g., children <2 years old), case reports, autopsy studies, or were primarily patients receiving anti-TB drugs. We excluded publications presenting population-level outcome rates, or that did not specify follow-up time or loss to follow-up. Additionally, we excluded reviews or editorials but we did search their reference lists for additional studies of interest.

Two reviewers (two of TCB, HEJ, CAR, LFW) independently read each publication to determine inclusion eligibility. Non-English publications were translated by authors fluent in the relevant language (PAzW, BN) and independently reviewed by HEJ and LFW, along with the relevant translator, to determine eligibility. Discrepancies were resolved by group discussion.

Data extraction

Two reviewers (two of TCB, HEJ, CAR, LFW, PAzW, BN) independently extracted data from each publication using a standardized electronic form. We extracted study type (e.g., population-based cohort, sanatorium-based cohort), cohort characteristics (geographic location, time period, forms of TB disease, age range), determination of death, outcome definitions, treatment (e.g., sanatorium, surgery, anti-TB drugs), and the start of follow-up time (i.e., notification/diagnosis, sanatorium entry or exit). For consistency among sanatorium studies, if the follow-up start time was the sanatorium exit and the average sanatorium stay was reported, the follow-up times were shifted ahead by this average length of stay so that the follow-up start was approximately entry into the sanatorium. If the average length of stay was not reported, then the follow-up times were shifted by 165 days, which was the average length of sanatoria stay in the United States between 1934 and 1938.6 We extracted data into life tables and stratified by disease severity when possible.

Publications often reported on multiple cohorts and occasionally, the same study reported data over multiple publications. Therefore, we enumerated findings using the following terminology: ‘publications’ are individual published reports in the literature; ‘studies’ are a population of patients recruited, diagnosed, and treated in a similar fashion during the same time period, which may be reported over multiple publications; and ‘cohorts’ are a patient population that may have been recruited, diagnosed, and/or treated differently over varying time periods but were in the same publication.

Discrepancies between reviewers were resolved by group discussion and reconciled extractions were entered into REDCap electronic data capture tools hosted at Boston University Medical Campus, Boston, MA, USA. Ethics approval was not required because all data were from published reports.

Mortality meta-analysis

We transformed the extracted life-table structured data and created individual-level data with the interval from entry/diagnosis to death or time of censoring for each individual in each cohort. We used parametric survival analysis with interval censoring to estimate the survival times for TB-specific mortality. TB deaths were considered events and deaths from other causes were considered censored observations.

We used a Bayesian framework to estimate the survival distribution, which included a frailty term for each study (see Supplementary Data). We analyzed all the studies together in one model and then we compared mortality outcomes by time (pre-1930 to post-1930), geography (North America vs. Europe), and setting (sanatorium/hospital studies and non-sanatorium studies) due to the difference in care pattern and start of follow-up time. We choose 1930 as a cut-off as the approximate mid-point of the total time period covered by our included studies. For all analyses, we plotted the study-level survival curves overlaid with the overall survival curves (the mean of the frailty distribution) with 95% credible intervals (CrI). We estimated study-specific 1, 5, and 10-year survival probabilities and median survival times with 95% CrIs.

We compared the baseline reported severity in individuals treated in sanitoria/hospitals to those not treated in sanitoria, where disease severity reporting was available. We provide summary statistics of these data and tested for associations using a χ2 test.

We used R v4.0.2 (R Computing, Vienna, Austria) with Bayesian models fit using JAGS with R2jags v0.6-1. Model diagnostic results are given in the Supplementary Data. All data and code are available on GitHub (https://github.com/sarahleavitt/TB_mortality).

RESULTS

Literature review

We identified 153 publications (93 from personal libraries, 60 from a manual reference search of personal library publications) and obtained 142 (93%) for full-text review (Figure 1). We excluded 122 publications, mostly due to not reporting an outcome of interest (n = 48), unclear follow-up time (n = 23), or reporting population-level rates (n = 17). Data from 20 publications were included; three publications included data from the same cohort but were stratified by disease severity across three publications. For two studies,7,8 data required modification to conform to a life table format (see Supplementary Data).

Figure 1.

Figure 1

Flow chart describing the review process and exclusions. LTFU = loss to follow-up.

Characteristics of cohorts

Of the 20 included publications, 10 (50%) were from North America and 10 (50%) from Western Europe (Table 1). Twelve studies (60%) were conducted primarily before 1930. Most publications enrolled patients between the 1910s and 1940s. Ten (50%) publications included patients treated at a sanatorium or an inpatient hospital. Six (30%) publications indicated a subset of patients received surgical treatment; anti-TB chemotherapy was provided to a minority in two publications (Table 1).

Table 1.

Descriptive characteristics of pre-treatment era cohorts with data on TB-specific mortality and/or natural recovery from TB (n = 20 publications, 18 studies)

Reference Enrollment period (years) Setting Population Diagnostic method Treatment Stratification
Heise21* 1917–1931 New York State, USA Sanatorium cohort of patients with PTB treated at Trudeau Sanatorium CXR Sanatoria (100%) By disease severity
Rutledge22* 1909–1914 Colorado, USA Sanatorium cohort treated at the Modern Woodmen of America Sanatorium Sputum smear and clinical findings Sanatoria (100%) By disease severity
Stephens8* 1919–1938 New York State, USA Employment-based sanatorium cohort of employees ages 17–64 of the Metropolitan Life Insurance Company Signs and symptoms (pre-1924) and CXR (1925+) Sanatoria (100%) By disease severity
Ferguson23* 1917–1924 Saskatchewan, Canada Sanatorium survivor cohort of patients ages 0–69 treated at Fort Qu’Appelle Sanatorium Not reported Sanatoria (100%), surgery (1%) None
Wherrett24 1917–1924 Saskatchewan, Canada Sanatorium survivor cohort of patients treated at Fort Qu’Appelle Sanatorium Not reported Sanatoria (100%) None
Zacks25* Approximately 1927–1932 Massachusetts, USA Cohort of children with PTB; unclear whether cohort were inpatient, outpatient, or population-representative Not reported Surgery and/or sanatoria (55%) None
Munchbach26 1920–1927 Black Forest, south-west Germany Sanatorium cohort of patients with PTB Not reported Sanatoria (100%) None
Baart de la Faille27 1922–1935 Bilthoven, The Netherlands Sanatorium-based cohort of adults with PTB at the Berg en Bosch sanatorium CXR Sanatoria (100% and collapse therapy (34%) None
Mitchell28* 1930–1939 New York State, USA Sanatorium cohort of patients aged >15 years with PTB treated at the Trudeau Sanatorium CXR and symptoms Sanatoria (100%) By disease severity
Alling, 1954,29 Alling, 1955,30 Lincoln31* 1938–1948 (Alling, 1954 and 1955); 1937–1947 (Lincoln) New York State, USA Outpatient clinical cohort of smear-positive patients aged >10 years with far advanced (Alling, 1954), moderately advanced (Alling, 1955), and minimal (Lincoln) TB treated at Hermann M Biggs Memorial Hospital Sputum smear and CXR Among far advanced patients: bed rest (27%), collapse therapy (27%)
Among moderately advanced patients: anti-TB drugs (‘a few’), collapse therapy (37%), bed rest (63%)
Among minimal patients: not reported
By disease severity
Braeuning32* 1920/1921, 1927/1928, 1930, 1933 Stettin, Germany (at the time of the study, currently Poland) Population-based cohort of PTB patients attending a public TB clinic CXR Surgery or sanatoria (% receiving each unclear) By disease severity
Stadler9 1893–1902 Marburg, Germany Population-based cohort of PTB patients attending public outpatient clinics Not reported Not reported None
Tattersall33* 1914–1940 Reading, UK Population-based cohort of smear-positive patients from the Tuberculosis Service of Reading County Borough Smear-positive Sanatoria (38%) By disease severity
Holst34 1891–1900 Norway People with TB as reported through forms filled out by doctors Clinical signs and symptoms Not reported None
Lissant Cox35* Approximately 1934–1935 Lancaster, UK Cohort of smear-positive patients while in residential treatment at sanatoria and pulmonary hospitals Sputum or other specimen smear, signs and symptoms Sanatoria (100%) By disease severity
Bentley36* 1942–1946 Brentwood, UK Hospital-based cohort of pediatric patients ages 0–16 years treated at High Wood Hospital CXR and clinical findings Sanatoria (100%) None
Lowe37* 1930–1951 Birmingham, UK Population-based cohort of all patients with PTB identified from registers Not reported Not reported None
Springett38 1947 Birmingham, UK Outpatient clinical cohort of sputum-positive, PTB patients ages >15 years seeking care at the Birmingham Chest Service Sputum smear Surgery (30%), anti-TB drugs (0.2%) None

*Data available on TB-specific mortality.

Data available on natural recovery.

Includes TB-specific mortality data that were not stratified by severity and for a subset of this cohort, TB-specific mortality and natural recovery data stratified by severity.

PTB = pulmonary TB; CXR = chest X-ray.

Outcome definitions were not standardized during the pre-chemotherapy era and definition reporting was minimal in some publications (Supplementary Table S2). Only five (25%) studies described determination of death. These included clinician-determined cause of death via questionnaires mailed to households, or through multiple sources such as family report or vital record review. Natural recovery definitions included patients with no longer detectable M. tuberculosis, able to work, and the more stringent, standardized definitions of the United States’ National Tuberculosis Association’s (USNTA) Diagnostic Standards, which required symptom resolution, negative culture, and improved chest X-ray for ≥2 years to establish recovery (Supplementary Table S2).5

The 20 publications represented 18 studies, following 84 cohorts with a total of 35,900 patients. Of the 18 studies, 12 (67%), representing 53 (63%) of the cohorts, reported TB-specific death. Of the 18 studies, 12 (67%) representing 63 (72%) of the cohorts classified alive patients as either having chronic TB or having naturally recovered by each time point.

Overall mortality results

Using all data, there were 12 studies, 53 cohorts and 17,166 patients with follow-up data on TB-specific mortality. Assuming a lognormal distribution, we estimated TB-specific mortality survival (meanlog = 2.51, sdlog = 1.72). Overall, 93% (95% CI 84–98) of individuals survived 1 year, while 55% (95% CI 36–73) of individuals survived 10 years, with a median survival time of 12.33 years (95% CI 5.47–28.93) (Table 2, Supplementary Figure S3). Model fit diagnostic plots for all models are shown in Supplementary Figures S11–S17.

Table 2.

Survival analysis results TB-specific mortality with the combined and stratified models

Setting Survival distribution 1-year survival
(95% CrI)
5-year survival (95% CrI) 10-year survival (95% CrI) Survival time median (95% CrI) Studies
n
Cohorts
n
Individuals
n
Combined Lognormal (2.51–1.72) 0.93 (0.84–0.98) 0.7 (0.52–0.85) 0.55 (0.36–0.73) 12.33 (5.47–28.93) 12 53 17,166
Time stratified
 Pre-1930 Lognormal (2.29–1.40) 0.95 (0.84–0.99) 0.69 (0.44–0.88) 0.50 (0.26–0.75) 9.90 (4.10–25.24) 7 30 10,732
 Post-1930 Lognormal (2.85–2.13) 0.91 (0.70–0.99) 0.72 (0.41–0.94) 0.60 (0.29–0.89) 17.23 (2.98–129.05) 5 23 6,434
Geography stratified
 North America Lognormal (3.06–1.56) 0.98 (0.94–0.99) 0.83 (0.71–0.90) 0.69 (0.54–0.81) 21.33 (11.54–37.95) 7 28 10,619
 Europe Lognormal (1.61–1.92) 0.8 (0.47–0.96) 0.5 (0.18, 0.82) 0.36 (0.10–0.71) 5.02 (0.86–28.73) 5 25 6,547
Setting stratified
 Sanatorium/hospital Lognormal (3.08–1.56) 0.98 (0.90–1.00) 0.83 (0.59–0.94) 0.69 (0.41–0.87) 21.77 (7.09–59.58) 7 41 12,330
 Non-sanatorium Lognormal (1.67–2.03) 0.80 (0.58–0.93) 0.51 (0.28–0.75) 0.38 (0.18–0.63) 5.29 (1.53–19.92) 5 12 4,836

CrI = credible interval.

Sanitoria results

Survival was higher in the sanatorium studies than in the non-sanatorium studies (Table 2, Figure 2, Supplementary Figure S4). Only 38% (95% CI 18–63) of non-sanitorium individuals survived to 10 years compared to 69% (95% CI 41–87) of sanitoria/hospitalized patients. There were more individuals with far advanced disease at baseline among those treated outside of sanitoria (43.0% vs. 22.0%), and overall, there was a significant difference in disease severity between those treated in sanitoria compared to those treated elsewhere (P < 0.001) (Supplementary Table S7).

Figure 2.

Figure 2

Survival curves for TB-specific mortality for the time period, study location, and treatment location stratified analyses. The thin, grey lines represent the specific survival curves for each study. The black dotted line represents the overall survival curve (the mean of the frailty distribution). The grey shaded area is the 95% credible interval for the overall survival curve.

Mortality by time

In studies primarily enrolling individuals prior to 1930, 10-year survival was 50% (95% CI 26–75), which was similar to survival estimated in studies primarily enrolling after 1930 (60%, 95% CI 29–89). The median TB survival time was nearly twice as long for studies conducted after 1930 (17.23 years, 95% CI 2.98–129.05 vs. 9.90 years, 95% CI 4.10–25.24) (Table 2, Figures 2 and 3, Supplementary Figure S5).

Figure 3.

Figure 3

Forest plot of 1, 5, and 10-year survival probabilities for TB-specific mortality for the combined model. The dots plot the estimated survival probabilities, while the bars depict their 95% credible intervals. Studies are classified by first year of enrollment (earliest to latest), with a horizontal line splitting the pre-1930 and post-1930 studies. The two panels stratify the studies by region and the dots and bars are colored according to setting. The overall estimate of the survival probabilities is located at the bottom of the plot and represented with a diamond.

Mortality by geography

Overall mortality outcomes in North American studies compared to European studies were much better. Ten-year survival was estimated to be 69% in North America (95% CI 54–81) compared to 36% in European studies (95% CI 10–71). The median survival times were fourfold higher in North American studies: 21.33 (95% CI 11.54–37.95) vs. 5.02 years (95% CI 0.86–28.73) (Table 2, Figure 2, Supplementary Figure S6).

Natural recovery data

The raw natural recovery data are summarized in Supplementary Figures S6–S9. Consistent with findings from mortality data, overall trends in reported recovery rates were higher among individuals treated in sanitoria, post-1930 and from North America.

DISCUSSION

Our study illustrates that researchers should be mindful of the context when using pre-chemotherapy era data. There are substantial differences in outcomes based on time, geography, and whether or not patients were in a sanatorium. Inferences from these data should account of these potential biases and not view pre-chemotherapy era data as homogeneous.

Geographically, people in North American studies experienced better outcomes than those in Europe. This may be because North America was more shielded from the worst effects of the two world wars in the early twentieth century than Europe. Also, an increased proportion of the North American studies used data from sanatoria (6/8 studies vs. 2/10 studies). Our results indicate that sanatoria outcomes were better than in studies using community data. However, for studies reporting data on severity at presentation, patients with less severe disease were more likely to spend time in a sanatorium, consistent with the hypothesis that sanatoria were less likely to admit moribund patients as they could not help them. Thus, providing an additional reason why data from North American studies could be biased towards improved outcomes, and illustrating a bias intrinsic to sanatoria data. Stadler et al. also suggested that sanatoria preferentially treated people of higher socioeconomic status;9 even if their stay was paid, some people declined a sanatorium stay because they had to work to support family; and some people were excluded as ‘unsuited’ for sanatoria. All these factors are still seen today regarding the inequities of who does and does not receive TB care. Most included studies were from the United States and the United Kingdom, and the gross domestic product per capita and life expectancies in these countries were notably similar during the study periods, although substantially lower in Germany and Norway when the included studies spanned an earlier time period (Supplementary Table S8). There were also no substantial differences in the mean ages or percentage male between North American and European studies, or sanatoria-based and community-based studies (Supplementary Table S9). We also did not observe significant differences in survival between studies enrolling individuals pre-1930 compared with those enrolling after 1930, although there were differences between these studies in terms of percentage male (58% and 48%, respectively) (Supplementary Table S9).

It is well documented that people with fewer resources, poor access to care, or those who live in political or social turmoil, such as war-torn areas, have poorer TB outcomes.1018 Our results are consistent with this in that people without access to sanatoria, or living through wartime experienced poorer TB outcomes. Aggregating the pre-chemotherapy era data obscures this important heterogeneity. When making inferences from these data for modern day TB management, it might be necessary to identify specific relevant studies for analysis, depending on the research question.

One strength is our focus on TB-specific mortality. Previous studies have looked at all-cause mortality, which would not only over-estimate TB-specific mortality, but might also suffer from other heterogeneities, thus obscuring differences in TB-specific mortality between groups.2,3 Furthermore, we have used parametric survival modeling to estimate parameters that can be used to generate survival probabilities and parameterize modeling studies.

Our study had some limitations. Sanatorium discharge start time was used for the sanatoria studies, with the average stay added (two of seven sanitoria studies) to this, whereas notification/diagnosis was used for the non-sanatoria studies. Therefore, only individuals who survived their sanatorium stay were included. Additionally, individuals who were moribund were not typically admitted to sanitoria.19 These factors may have contributed to improved survival in sanatorium studies. Asymptomatic patients were not included in our cohorts, as they would not have presented to medical services. Nonetheless, our analyses will have included nearly all symptomatic smear-positive patients. ‘A few’ patients were reported to receive anti-TB drugs and therefore our estimated survivals might be overestimates. However, as the availability of anti-TB drugs and types of regimens provided during our study period was limited and inferior to those used nowadays, it is unlikely that this affected our results substantially. Included studies were from Europe, United States, and Canada, which might limit generalizability to untreated populations today. However, many of the societal conditions that characterized the pre-treatment era cohorts—high-density households, malnutrition, little access to medical care, poor air quality, and high background TB incidence (Supplementary Data 9) —are similar to those in high TB burdens settings today.20 Additionally, there may be further studies that we did not find, due to the challenge of finding papers from this era – notably, we found no African or Asian studies. Finally, our data do not account for the impact of HIV co-infection on TB survival and recovery, as they were from the pre-HIV era.

Since around 40% of people estimated to develop TB disease in 2021 were not diagnosed,1 results from the pre-chemotherapy era provide important insights that are relevant nowadays. These data are also critical for modeling studies. However, the context must be considered when using these data to ensure that we make suitable inferences for twenty-first century TB management.

Supplementary Material

Acknowledgements

The authors thank M Zimmer for research assistance and A Mesman for translation support. The results reported herein correspond to specific aims of grants R01GM122876 and R35GM141821 to investigator LFW, HEJ and CRH, and R01GM122876-04S1 to CAR from the National Institute of General Medical Sciences of the National Institutes of Health (NIH; Bethesda, MD, USA). This work was also supported by grant K23 AI152930 from the NIH to TCB and a Burroughs Wellcome Fund/American Society for Tropical Medicine and Hygiene Postdoctoral Fellowship in Tropical Infectious Diseases to TCB. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

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