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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2017  |  Volume : 28  |  Issue : 4  |  Page : 806-817
Epidemiology and outcome of tuberculosis in immunocompromised patients

1 Department of Renal Medicine, The Royal Hospital, Muscat, Oman
2 Department of Infectious Disease, The Royal Hospital, Muscat, Oman
3 Department of Respiratory Medicine, The Royal Hospital, Muscat, Oman
4 The Saudi Center for Organ Transplantation, Riyadh, Saudi Arabia

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Date of Web Publication21-Jul-2017


The United States Renal Data System showed 1.2% and 1.6% incidences of tuberculosis (TB) in patients on peritoneal dialysis and hemodialysis (HD), respectively. Kidney transplant (KTX) patients have higher rates. We studied the epidemiology and outcome of TB in patients with kidney dysfunction in a tertiary care hospital in the past decade. We examined data of patients with TB with and without kidney dysfunction from 2006 to 2015 through an electronic system. Statistical analysis was completed using Stata software, Chicago, IL, USA. We found 581 patients with active TB of whom 37 had renal dysfunction including chronic kidney disease, HD, and KTX. No difference was found in the prevalence, age, or gender predilection. The age ranged from 1 to 95 with a mean (standard deviation) of 38.6 (21.1) years. The incidence of TB is 3 per 100,000. The number of patients per year with active TB ranges from 52 to 128 and 3 to 4 in the general population and kidney dysfunction group, respectively. Sixty-five percent of patients with kidney dysfunction had pulmonary TB, 5% had pleurisy, and 30% had extrapulmonary TB. Eighty-four percent of patients with kidney dysfunction completed the course of treatment with 16% treatment failure and 0.4% developed multidrug-resistant TB; 8% were lost to follow-up and 8% died during the treatment period. This study showed no gender predilection for TB in the general population and immunocompromised. Duration of symptoms before diagnosis of TB was shorter in kidney dysfunction patients in comparison to the general population. TB cultures were the most positive tests whereas bronchoalveolar lavage and skin test were the least positive for detecting TB in the kidney dysfunction group. Improvement in registries and screening is required to enhance the capturing rate and detection among this group, as well as providing accurate data to health authorities and the public about the magnitude, future trends, treatments, and outcomes regarding TB in kidney dysfunction.

How to cite this article:
Metry AM, Al Salmi I, Al-Abri S, Al Ismaili F, Al Mahrouqi Y, Hola A, Shaheen FA. Epidemiology and outcome of tuberculosis in immunocompromised patients. Saudi J Kidney Dis Transpl 2017;28:806-17

How to cite this URL:
Metry AM, Al Salmi I, Al-Abri S, Al Ismaili F, Al Mahrouqi Y, Hola A, Shaheen FA. Epidemiology and outcome of tuberculosis in immunocompromised patients. Saudi J Kidney Dis Transpl [serial online] 2017 [cited 2020 Aug 3];28:806-17. Available from: http://www.sjkdt.org/text.asp?2017/28/4/806/211340

   Introduction Top

Tuberculosis (TB) remains one of the main causes of infectious disease morbidity and mortality, especially in developing countries.[1] In 2014, 9.6 million people, globally, were diagnosed with TB, and of these, 1.5 million died from the disease.[2] Over 95% of TB deaths occur in low- and middle-income countries, and it is among the top 5 causes of death for women aged 15–44. Around one-third of the world’s population has latent TB.[1]

People who smoke and the immunocompromised, for example, those with HIV, diabetes, chronic kidney disease (CKD), and who have had organ transplants, are considered at a higher risk of activating TB infection.[3]

CKD, especially high urea levels, is an important known contributor to the immuno- suppression disturbing the body’s immune defense mechanisms, making such patients vulnerable to opportunistic infections including TB.[4]

A retrospective study reviewed the data of the United States Renal Data System between 1995 and 1999 found that there is a 1.2% and 1.6% cumulative incidence of TB in patients undergoing either peritoneal dialysis or hemodialysis (HD), respectively.[5],[6] Many similar studies have eluded that patients with kidney transplants (KTX) are at higher risk of TB reactivation.[4],[5],[7],[8]

Up to 15% of KTX patients in the Indian subcontinent developed TB compared with 1.7% in the United Kingdom.[5],[7],[9] In Turkey, TB was 8.5 times more common in KTX group than in the general population and 50% to 80% occurred within one year of transplantation.[10],[11],[12] This risk is augmented with the coexistence of chronic liver disease and other infections, particularly deep mycoses, Pneumocystis juvanni, nocardia, and cytomegalovirus (CMV).[9],[13],[14]

In Oman, the Royal Hospital is the only transplant center in the country that receives all cases of transplantation for the management of complications including infections such as polyomavirus (BKV), CMV, TB. No study has reported epidemiological data, clinical features, and outcomes for kidney dysfunction patients acquiring TB in Omani population. The aim of this study is to evaluate the outcome, management, drug resistance, morbidity, and mortality for people with kidney dysfunction.

   Methods Top

This is a retrospective descriptive study evaluating all cases of TB that have been seen at the Royal Hospital throughout the period from 2006 to 2015. The Royal Hospital has an internationally recognized electronic medical record system called Al Shifaa that uses International Classification of Diseases codes.

A list of all patients that have been diagnosed with TB by the different diagnostic methods was retrieved. This list was cross-checked with the pharmacy department and confirmed that anti-TB medications were dispensed to those patients and these were confirmed with laboratory records.

Initially, patients with a provisional diagnosis of TB were divided into four categories, the first two being latent TB (diagnosed by Mantoux test, confirmed by QuantiFERON Test, and treated with isoniazid (INH) prophylaxis for 6 months) and old TB (investigated for TB reactivation and found to have negative bacteriological and/or histological test results). The third category of patients is those with a high clinical suspicion of TB but who are found to have negative bacteriological or histological test results. Subsequently, other diagnoses were established in these patients such as other bacterial/fungal chest infection or malignancies.

The remaining group was those with newly diagnosed active TB of various organ involvements which was confirmed by either bacteriological or histological tests. This group was further divided into those with or without kidney dysfunction. Subsequently, those with kidney dysfunction were divided into three categories such as CKD, HD, and KTX groups.

Medical records of all patients were reviewed in detail for demographics, primary kidney disease, investigations [laboratory and radiological assessment including chest X-ray, computerized tomography (CT), and bronchos-copy], medications, and outcomes.

Clinical diagnosis of suspected TB was based on symptoms such as persisting cough (generally productive and lasting three weeks or longer), fever, night sweats, fatigue or weakness, unexplained weight loss, and/or loss of appetite or hemoptysis. Furthermore, TB was considered in case of recurrent pneumonia or unresolving pneumonia within two weeks after antibiotic therapy was initiated. The confirmed TB diagnosis was based on positive acid-fast bacilli smear in sputum, bronchoalveolar lavage (BAL) or histopathology, TB culture, or strong evidence from histopathology.

The study was approved by the Medical Ethics and Research Committee at Royal Hospital. The data entry was rechecked by two researchers. Quality control data were done as per our institute research guidelines. Statistical analysis was done using Stata software (Chicago, IL, USA).

   Results Top

During the period from 2006 to 2015, we found 840 patients with a provisional diagnosis of TB at the time of first evaluation, as shown in [Figure 1]. One hundred of them showed no evidence of TB based on various investigations done after their admission. Of the remaining 740, 102 had latent TB, 57 had nonactive old TB, and 581 had active TB, as shown in [Figure 1].
Figure 1: A total number of patients in Royal hospital with high suspicious diagnosis of tuberculosis and their classification including patients with kidney dysfunction.

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The age range of 581 patients included in the study was from one to 95 years with a mean [standard deviation (SD)] of 38.6 (21.1) years. Just over half (50.6%) of the patients were females with a mean (SD) age of 36.2 (21.3) years and 49.4% were males with a mean (SD) age of 41.1 (20.7) years. The majority (78.8%) of patients in this study were citizens of Oman and the remaining 21.2% were noncitizens.

The number of patients per year with active TB ranged from 52 to 128, as shown in [Table 1]. Of all the patients, approximately 90% of the cases were admitted to four main departments; infectious disease (38%), chest medicine (31%), pediatrics (13%), and renal medicine (4%), as shown in [Table 2]. Pulmonary TB and TB lymphadenopathy were the most common presentation types constituting 35.2% and 10.6%, respectively, while TB of the central nervous system accounted for 0.95% and was the least common presentation type of TB, as shown in [Table 3].
Table 1: A number of patients per year with tuberculosis in general in Royal Hospital and tuberculosis in kidney dysfunction patients.

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Table 2: A number of patient with newly diagnosed tuberculosis according to admitting department.

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Table 3: Diagnosis of TB in general according to organ affection and gender.

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Of the 581 patients with active TB, 37 had kidney dysfunction including 19 with CKD, five on HD, and 13 with KTX (on immunosuppression). Their ages ranged from 16 to 77 years with a mean (SD) of 47.0 (16.1) years. In the CKD group, the mean age (SD) was 50.2 (17.3), the HD group was 57.0 (7.8), and the KTX group was 38.3 (13.8) years, as shown in [Table 4].
Table 4: Diagnosis of TB in kidney dysfunction according to organ affection and gender.

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All 37 cases were diagnosed utilizing clinical, laboratory, and radiological modalities. The number of patients per year with TB ranged from three to six patients, as shown in [Table 1]. The mean (SD) for the total duration of symptoms before diagnosis of TB was 33.43 (69.6) days and was 18 (54.0), 18 (19.5), and nine (32.9) for CKD patients, HD patients and KTX patients, respectively.

Twenty-two of the patients resided in the capital area, Muscat (59.5%). Of these, 15 (68.2%) had CKD, three (13.6%) had HD, and had (18.2%) KTX. Thirty-four (91.9%) were citizens whereas three (8.1%) were non-citizens. While 15 (40.5%) were from outside of the capital area, [4 (16.7%) CKD, 2 (13.3%) HD, and 9 (60%) KTX]. The mean (SD) age of patients residing in the capital area was 51.2 (14.8) years whereas those residing in the outside of the capital area was 40.8 (16.5) years.

Clinical diabetic nephropathy as a primary kidney disease constituted 40.5% (15 cases), followed by chronic glomerulonephritis 35% (13 cases), clinical hypersensitive nephropathy 10.8% (4 cases), and other remaining causes contributed to about 13.5%. However, 21 (56.76%) patients had diabetes mellitus (DM), and their mean (SD) age was 50.4 (15.2) years.

On the other hand, hypertension (HTN) was found in 28 (76%) patients with mean (SD) age of 50.5 (14.9).

In the KTX group, four (30.8%) of the patient’s transplants were from living related donors (3 of the transplants were performed in Oman and one was done in the USA). The remaining nine (69.2%) patients had commercial living unrelated KTX; six were done in Pakistan and three were done one each in India, Iran, and China.

Induction therapy for the transplanted patients was used with an interleukin 2 R blocker (basiliximab or daclizumab) or anti-thymocyte globulin while the maintenance immunosuppressive therapy was prednisolone and mycophenolate mofetil in all 13 transplant patients, 11 patients received a calcineurin inhibitor, and two received a mammalian target of rapamycin inhibitor (one was on Sirolimus and other on Everolimus) at the time of diagnosis of TB.

Pulmonary TB and TB lymphadenopathy were the most common presentation constituting 64.9 % and 10.8%, respectively. Tuberculosis of bone and joint, pleurisy, and miliary TB were the least common TB presentation type and accounted for 5.4% in each [Table 4]. The total number of patients who had KTX during the period between 2006 and 2015 was 715, of which 13 had active TB infection with calculated incidence of 1.8%.

All patients with kidney dysfunction had complete blood count, C-reactive protein, erythrocyte sedimentation rate, urea and electrolytes, liver function test, bone profile, parathyroid function, and urinalysis except for two patients on whom HD urine analysis was not done, as there was no urine output for them, as shown in [Table 5] and [Table 6].
Table 5: Laboratory investigations of patients with CKD, HD, and KTX.

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Table 6: The incidence of proteinuria, hematuria, and leukocyturia in the kidney dysfunction group.

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All 37 patients were nonreactive for HIV. Three (8.1%) of the transplant patients were reactive for hepatitis B. Only one (2.7%) from the CKD group was reactive for hepatitis C. All transplant patients were negative for Epstein–Barr virus by polymerase chain reaction (PCR). Three (23.1%) of them were positive for CMV by PCR whereas only one (7.7 %) was positive BKV by PCR.

As shown in [Figure 2], radiological investigations were done in almost all patients, CXR (100%), CT (86.5%), and bronchoscopy (49%). Chest X-rays were performed for all 37 patients and 28 (64.9%) of them showed abnormal findings such as pneumonic patch, bronchiectasis, effusion, cavity, and hilar lymph node. CT scans were done in 32 cases, as shown in Figure 2, of which 24 showed signs of pulmonary TB, two showed signs suggestive of miliary deposition in both lungs, two showed bilateral pleural effusion, and four cases had generalized lymphadenopathy. In the remaining five patients, three were diagnosed with genitourinary TB by cystoscopy and two were diagnosed by culture of the joint aspiration.
Figure 2: Flowchart of radiological investigation in the kidney dysfunction group with suspected tuberculosis.

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The ultrasound investigations of the kidney graft was done for all transplant cases for size and echogenicity, and most of the patients had kidney size of 11–12 cm with abnormal echogenicity in 40% of cases. Echocardiography was done in 19 patients at time of TB diagnosis in the Kidney dysfunction group (11 CKD, 3 HD and 5 RTX). The Mean (SD) of EF was the highest [61.8 (7.33%)] in KTX group, and lowest in CKD group [48.5 (16.2)]. The Mean (SD) of left atrium (LA) measurement was highest in HD group [40.33, (3.06 mm)] and lowest was KTX [35 (2.4)], as shown in [Table 7].
Table 7: Echocardiography findings in kidney dysfunction group.

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A skin test was completed for all patients with kidney dysfunction and 18 (48.6%) of them were positive, 12 CKD, two HD, and four KTX and the remaining were negative. Two or more of sputum microscopy, BAL, culture for TB, or biopsy/histopathology tests were done for each one of the patients with kidney dysfunction, as shown in [Table 8]. Biopsies were done from four lymph nodes, two lungs, two pleural, two urinary bladders, and three bones for histopathological examination, as shown in [Table 8].
Table 8: Diagnostic tools of TB including skin test, sputum microscopy, BAL, and biopsy with histopathological examination.

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At the time of diagnosis, all 37 patients were started on antituberculous treatment. All 37 patients received induction therapy of anti-TB by four drugs; rifampicin, INH, ethambutol, and pyrazinamide for two months; however, two patients died (one with CKD and the other with HD) after completing a month of treatment. All 37 patients, including 24 with pulmonary TB, received pyridoxine and none showed toxic effects of antituberculous treatment; however, one case of pulmonary TB had resistance to INH and streptomycin based on routine microbiology culture and sensitivity test.

In the kidney dysfunction group, 31 (83.8%) patients completed the course of treatment, whereas six did not complete the treatment (16.2%), three of them died (one KTX died from CMV pneumonitis and TB was contributing factor, one CKD died from septic shock, and the last one on HD died from TB complications). In addition, three noncitizen patients returned to their home country and were lost to follow up. Mortality rate was three cases (8.1 %) among 37 patients.

   Discussion Top

Mycobacterium TB (MTB) infection leads to active disease in approximately 10% of people.[15] An effective immune response stops MTB multiplication, and the pathogen is completely eradicated in 10% while some bacilli escape termination and remain in a dormant state (latent TB) in old lesions.[15],[16] However, if the immune system is disturbed for whatever cause, latent TB can cause active disease.[17]

It has been reported that almost 33% of world population has latent TB and about 10% of infected people develop active disease during their lifetime.[18],[19],[20] The present study showed that during the period from 2006 to 2015, 840 patients had a provisional diagnosis of TB. Of these, 102 were latent TB and 57 were diagnosed as an old TB. The remaining 581 patients were newly diagnosed with active TB. A previous study by Al-Maniri et al analyzed trends of TB in Oman (1981–2005) in relation to the socioeconomic development of the country. It reported that the TB notification rate declined by around 15% per year, compared to only 3.6% per year in subsequent years during their study period.[21]

Our study had 581 cases of active TB that were fully documented and investigated over the past 10 years. With just over 50% of population being Omani citizens, our reported incidence is about 3% per 100,000. However, a study that analyzed countries with high TB prevalence rates revealed that the prevalence of TB in KTX patients was 43 times greater than in the general population (6.88% vs. 0.16%, respectively); in medium prevalence countries, the prevalence of TB in transplant patients was 83 times greater than in the general population (2.61% vs. 0.03%).[20],[22] A Turkish study reported that their prevalence of TB was 2.8% in KTX patients.[12] Furthermore, a Brazilian study reported that 3.9% of their transplants had TB diagnosed in various organs.[23] A systematic review and metaanalysis found that the pooled prevalence of TB-KTX was 2.51% (95% confidence interval = 2.17-2.85). They concluded that TB prevalence in KTX was 14 times greater than in the general population.[23]

Our study showed that 78.8% and 91.9% of general patients and those with kidney dysfunction were citizens, respectively. However, both citizens and noncitizens are treated in Ministry of Health Hospitals and no private clinics or hospitals manage such cases. Nonetheless, a previous study reported that non-citizens contributed 21% of all TB cases notified to the Ministry of Health.[21] Furthermore, they reported that males and those of 50 years and above had higher rates than females and younger age groups.[21] A study from Kuwait showed that of the 526 cases they studied, 16.5% were Kuwaiti citizens and 70.9% were male.[24] However, our study showed no gender predilection among our participants. In addition, our participants were young with an average age of 39 and 47 years for general participants and those with kidney dysfunction, respectively.

TB is a well-known infectious complication in patients with kidney dysfunction, as a result of immunosuppression from uremic toxins and drugs.[25],[26] Our study found 37 (6.4%) patients with various kidney dysfunctions out of 581 diagnosed with active TB. Furthermore, in patients with kidney dysfunction, TB presents important diagnostic difficulties because of the greater incidence of extrapulmonary involvement, negative sputum smear results, despite active disease and its atypical presentation, specifically reactivation of latent TB.[27],[28] Our results showed that 65% of all patients with kidney dysfunction had pulmonary TB and an additional 5% had pleurisy. However, only 30% had extrapulmonary TB. A retrospective study found no difference in the prevalence, age, or male/female ratio of TB among the kidney dysfunction group.[29],[30] This is exactly similar to the findings among participants in our study. However, another study found that TB of the lung was the more favored site of infection in patients on HD (77.3%) when compared with those with renal transplant (33.3%).[4] Our study showed that the majority of patients of whatever type of kidney dysfunction group have a predilection for pulmonary TB. However, generalized TB lymphadenopathy was not found in patients on HD but occurred in 23% of KTX (3 cases out of 4) and only a single case in a patient with CKD (5%).

The present study showed that the duration of symptoms before a TB diagnosis was 33.4 days on average, where CKD was 18, HD was 18, and KTX was nine days. KTX patients tend to have a low symptomatic period before diagnosis in view of frequent and regular follow-ups with easier access to health service and prompt response in view of graft concerns and thorough investigation.

A previous study reported that the mean patient delay before consulting a physician was 12.5 ± 10 days.[31] Another study found that 62% had a delay of longer than 60 days and delays were related to unemployment and general attitudes toward health. Although they reflect the way health services are organized, delays were not associated with access to care.[30] Health services in the Sultanate are provided freely and are easily accessible with no access payment required from any citizens or residents working in any government authority.[32]

Patients who had received KTX are at high risk of development of TB and more frequent among them than the general population, depending on its epidemicity in the geographic or regional area.[12] Commercial transplant, primarily from Pakistan, is the dominant form of KTX in our participants contributing to approapproximately 70%.

A study from Pakistan found that recipients of the vended kidneys are educated, wealthy, and self-selecting but often poor medical candidates.[8] Their outcome is poor, with possible return to dialysis if not death. In addition, our study found an association with other infections such as CMV.

Tuberculin skin test (TST) has several limitations regarding TB diagnosis in CKD patients.[18],[33],[34] A positive TST in a patient without overt signs of active disease suggests latent TB infection.[18],[33],[34] Our study showed that TST was positive in 18 (49%) out of 37 patients with kidney dysfunction and of which 12 (63%) had CKD, two (40%) had HD, and four (37%) had KTX, but 19 (51%) had negative TST. Most importantly, it showed that people with KTX and also those on HD respond poorly to tuberculin tests due to relative anergy to the antigen. Another cross-sectional study found that a TST test was positive in 33.6% of recipient candidates.[33] Our results showed a similar result for transplant cases and a higher positivity in the CKD group.

Profound alterations in immune responses associated with uremia and exacerbated by dialysis increases the risk of developing active TB.[25] Our study showed that, in addition to their kidney dysfunction, 56.8% of our participants had DM. The immune deficiencies of CKD and DM are predisposing factors to the development of TB and even worse, predispose to miliary TB.[35] It has been suggested that the risk of TB is higher among patients with DM and these patients also have poor TB treatment outcomes. [14],[23],[35] From a public health perspective, DM and TB represent a critical intersection between infectious and non-infectious diseases in these countries and the effect of DM on TB incidence and outcomes provide numerous opportunities for further studies and research.[14],[23],[35],[36] Furthermore, it has been shown that a history of TB, dialysis efficiency, the use of Vitamin D supplements, and serum albumin were not proven to significantly influence the risk for TB, in contrast to advanced age (>65 years), body mass index >30 kg/m2, DM, tuberculin reactivity, healed TB lesions on chest X-ray, and time spent on dialysis.[14]

Our study showed that 84% of our participants with kidney dysfunction completed the course of treatment. Treatment failure occurred in 16% of our participants, where 8% left the country and therefore were not followed up on, and there was 8% death during the treatment period. A cross-sectional study based on data from Brazil’s Notifiable Disease Surveillance System database found that 69.8% of TB cases were cured and 30.2% had treatment failure.[37],[38],[39]

The present study has certain limitations. It is a retrospective study that may not capture all cases. It is set in a single and only center, in the country with small population. Nevertheless, it does capture majority of kidney dysfunction patients with TB for managing complications of transplantations, especially infectious complications. However, still a percentage of the population may succumb to their death without reaching a health center for the management of their infection. Therefore, this may underestimate the incidence and prevalence as well as the magnitude of the problem.

The way forward is that we need to establish a national database for patients with CKD and those on renal replacement therapy with TB. The majority of transplant cases in our country are commercial; therefore, it is empirical to screen this population after their arrival from such TB-endemic areas.

   Conclusion Top

During the period of this study, we observed 581 patients with active TB, of whom 37 had kidney dysfunction.

This study showed no gender predilection for TB in the general population and the patients with kidney dysfunction. The majority were citizens with an average age of 39 years and 47 years for general participants and those with kidney dysfunction, respectively. The average total duration of symptoms before diagnosis of TB was shorter in kidney dysfunction patients in comparison to the general population (14 vs. 33.4 days). Skin tests were more positive in the CKD group than in HD and KTX cases. TB cultures were the most positive tests whereas BAL and skin test were the least positive for detecting TB in the kidney dysfunction group.

The majority (65%) of patients with kidney dysfunction had pulmonary TB, and in addition, 5% had pleurisy and only 30% had extra-pulmonary TB and 84% completed the course of treatment.

Conflict of interest: None declared.

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Correspondence Address:
Issa Al Salmi
Department of Renal Medicine, The Royal Hospital, P. O. Box 1331, Code 111, Muscat
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PMID: 28748883

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]


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