PTW
  • Users Online: 116
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 

 
ORIGINAL ARTICLE
Ahead of print publication  

COVID-19 and radiotherapy: The ordeal faced by patients and staff during the pandemic in the 1st year


1 Department of Radiation Oncology, Kanuni Training and Research Hospital, Trabzon; Department of Radiation Oncology, Recep Tayyip Erdogan University Faculty of Medicine, Rize, Turkey
2 Department of Radiation Oncology, Kanuni Training and Research Hospital, Trabzon, Turkey
3 Department of Radiation Oncology, Recep Tayyip Erdogan University Faculty of Medicine, Rize, Turkey

Date of Submission23-Feb-2022
Date of Acceptance26-Apr-2022
Date of Web Publication24-Aug-2022

Correspondence Address:
Sema Yilmaz Rakici,
Department of Radiation Oncology, Recep Tayyip Erdogan University Faculty of Medicine, Rize
Turkey
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jrcr.jrcr_14_22

  Abstract 

Background: The SARS-CoV-2 pandemic has also had a profound impact on cancer treatment delivery and organization. Oncology clinics have developed a number of procedures and used formulas related to radiotherapy doses to continue their activities. Aims and Objectives: We explored the impact of SARS-CoV-2 pandemy on the personnel and cancer patients undergoing radiotherapy in a radiotherapy department during the first year. Materials and Methods: 845 patients were treated over the course of a year, 195 of whom consented to participate in the study. The Elekta Mozoiq system and radiotherapy cards were evaluated, and the time intervals between the treatments during the radiotherapy were recorded. Biologically Effective Dose losses were calculated in the radiotherapy dose due to the interruption to treatment, and necessary calculations were made for the delivery of the initially planned dose. Results: The mean age of the patients was 59 years (range 19-78). There were 110 male (56.4%) and 85 female (43.5%) participants. The treatment of 4.6% (9 patients) of the patients was discontinued because of SARS-CoV-2 infection during radiotherapy. The greatest added fraction for a patient with prostate cancer was three while the lowest was one for a patient with lung cancer, based on the TDF calculation. During this period, 16% of the staff was infected with COVID-19. Conclusion: This study demonstrates the effect of the COVID-19 pandemy on patients and personnel in a radiotherapy clinic, and its management during one year.

Keywords: Cancer, COVID-19, pandemic, radiotherapy, biologically effective dose (BED), Withers formula, Orton-Ellis Model formula, Time-Dose-Factor (TDF)



How to cite this URL:
Uslu GH, Kucuktulu E, Rakici SY. COVID-19 and radiotherapy: The ordeal faced by patients and staff during the pandemic in the 1st year. J Radiat Cancer Res [Epub ahead of print] [cited 2022 Dec 4]. Available from: https://www.journalrcr.org/preprintarticle.asp?id=354444


  Introduction Top


The SARS-CoV-2 pandemic has had a profound impact on cancer treatment delivery and organization.[1],[2] Oncology and geriatric patients were undoubtedly the most affected in this process.[3] The set of measures taken in the initial months of the epidemic lacked special guidelines for oncology clinics. According to one of the recently published international recommendations, the ESTRO's telemedicine technology would result in a 60% reduction in patient volume.[4] Most national oncology associations have developed procedures to keep their clinics operational when limiting the spread of the virus. Hypofractionated schemes, adjustments in adjuvant patient treatment protocols, and extending the duration of hormone therapy are among the strategies taken to shorten patients' hospital stays and treatment times. Furthermore, because radiotherapy (RT) treatment necessitates teamwork, each new patient was in close contact with all employees of the unit. Therefore, oncology workers were not deployed to COVID-19 outpatient clinics. Despite these precautions, the TDF values for patients, whose treatments were interrupted for various reasons, were recalculated using the Orton-Ellis Model formula.[5] In cases where the duration of the treatment was unaltered but the fractionation dose changed, the EQD2 calculation was made using the Withers' formula.[6] This way, dose losses were prevented and the initial biologically effective dose (BED) planned at the onset of the study was provided.

RT is employed in at least two-thirds of cancer treatment regimens in Western countries, which varies in different studies.[7],[8] In addition to common mandatory protection measures against SARS-CoV-2, the protocols have been created to keep dosimetry formulas near to permitting interruption or shortening of treatment.


  Materials and Methods Top


Study design

The data of 845 patients treated in our clinic were retrospectively analyzed between March 2020 and March 2021, and 195 patients with written informed consent were included in the study. COVID-19 status was based on a positive real-time reverse transcriptase–polymerase chain reaction (rRT-PCR) test.[9] Each patient underwent an rRT-PCR test 24 h before the RT simulation and then every 10 days for the duration of the treatment.

The intervals during RT were collected using data from the Elekta MOSAIQ health information system that manages treatment of cancer patients, as well as RT files. Treatments were regulated using a variety of radiobiological formulas.

Interruption of treatment results in BED losses in the total treatment dose. For this, the TDF value calculated with the modified Orton-Ellis Model formula was obtained to calculate the dose that provides the maximum effect in the tumor without exceeding the normal tissue tolerance limit, which is defined as the normal standard dose (NSD), and thus the TDF value was obtained.[5] It was assured that the initially planned BED dose was delivered without being altered by the intervals. The formula is listed below, along with the abbreviations that go with it. TDF: d1.538 . X-0.169 .10-3; Orton–Ellis Model (d: Fraction number, X: Treatment time; Routine planning, the dose per fraction (d) is often the starting point, and D may be replaced by Nd, where X is a function of the number of treatment days per week).

Ethical approval

Ethical approvals were obtained from the Ministry of Health (T16-15-47, dated 02.05.2021) and the local ethics committee (2021/73, dated 20.04.2021). In addition to consent form was obtained from all patients.


  Results Top


The average age was 59 years. There were 110 (56.4%) males and 85 (43.5%) females. The patients were divided into ten groups: breast cancer in 52 (26.6%) patients, lung cancer in 28 (14.3%), prostate cancer in 32 (16.4%), gynecological cancer in 14 (7.1%), head and neck cancer in 18 (9.2%), brain tumor in 10 (5.1%), bone metastases in 4 (2%), gastrointestinal cancer in 20 (10.2%), bladder cancer in 7 (3.5%), and other cancers in 10 (3.5%).

Patients with real-time reverse transcriptase–polymerase chain reaction (+)

Nine patients had their treatment interrupted at some point due to rRT-PCR (+) for COVID-19 that was resumed after recovery. Patients characteristics who were rRT-PCR (+) for COVİD 19 are summarized in [Table 1].
Table 1: Patients characteristics who were real-time reverse transcriptase-polymerase chain reaction (+) for COVID-19

Click here to view


Patient 1

Patient 1 is a 62-year-old male patient with prostate cancer who was scheduled for definitive external RT (2 Gy/fraction per day, total 78 Gy). On the 7th day of his treatment, he was hospitalized and treated for COVID-19 infection. The RT dose was calculated with the BED calculation after a 25-day break from RT, with an additional three fractions to the treatment. Except for the symptoms of weakness and fatigue due to COVID-19 that he had during the treatment procedure, he did not develop any other complications.

Patient 2

Patient 2 is a 70-year-old male patient with operated laryngeal cancer. After simulation, initiation of treatment was delayed due to rRT-PCR (+) (2 Gy/fraction per day, total 66 Gy). The COVID-19 infection was successfully treated after 14 days. The chemoradiotherapy protocol was then used to finish the treatment.

Patient 3

Patient 3 is a 59-year-old male patient with lung cancer. Due to bone metastases, he was put on a 10-day palliative treatment program (3 Gy/fraction per day, total 30 Gy). The treatment was terminated 3 days later due to rRT-PCR (+). After that, he was not followed up and never returned to treatment.

Patient 4

Patient 4 is a 71-year-old female patient with rectal cancer. Neoadjuvant chemoradiotherapy was planned (1.8 Gy/fraction per day, total 50.4 Gy and oral capecitabine 825 mg/m2 twice daily). On the 1st day of treatment, her treatment was interrupted because she was in contact with a case of COVID-19. After a 10-day quarantine, she tested negative for rRT-PCR and started her treatment.

Patient 5

Patient 5 is a 78-year-old male patient. Urgent palliative RT was planned for superior vena cava syndrome (SVCS), related to lung cancer (3 Gy/fraction per day, total 30 Gy). The treatment of the patient, whose rRT-PCR was positive on the 3rd day of treatment due to cough and fatigue, was discontinued for 20 days because the patient was symptomatic. The patient who completed the COVID-19 infection treatment at home was admitted to our clinic when his rRT-PCR result was negative, and the remaining treatment was completed by adding 1 fraction.

Patient 6

Patient 6 is a 19-year-old male patient with anaplastic oligodendroglioma who received chemoradiotherapy (2 Gy/fraction per day, total 60 Gy, and oral temozolomide 75 mg/m2/day). rRT-PCR was positive on the 20 day of treatment and RT was interrupted for 30 days. The remaining dose was determined using the BED method, and three fractions were added. Due to the development of speech disorder complaints, the patient underwent cranial magnetic resonance imaging (MRI), and the results revealed that the mass had progressed. Based on the new MRI, RT was rescheduled.

Patient 7

Patient 7 is a 59-year-old female patient. With a diagnosis of breast cancer, she came to our clinic for adjuvant RT (2 Gy/fraction per day, total 50 Gy planned). Despite the fact that she was asymptomatic according to the in clinic pandemic procedure, treatment was delayed since the rRT-PCR result was positive before treatment. When two rRT-PCR (-) results were obtained 15 days after the COVID-19 follow-up and treatment, RT was started, and the treatment was completed.

Patient 8

Patient 8 is a 40-year-old female with operated cervical cancer and planned adjuvant RT (2 Gy/fraction per day, total 46 Gy + brachytherapy). On the 5th day of treatment, RT was interrupted for 10 days due to positive rRT-PCR. The patient finished the treatment by addition of 1 fraction.

Patient 9

Patient 9 is a 73-year-old female patient. RT was planned for atypical meningioma (2 Gy/fraction daily, total 54 Gy). Seven days after the initiation of RT, the rRT-PCR test was positive due to family contact history. The treatment was then put on hold. The patient died in the hospital on the 3rd day of COVID-19 treatment from COVID-19 infection.

Clinic personnel with real-time reverse transcriptase–polymerase chain reaction (+)

Of the total 25 employees, four (age range, 32–40 years) contracted COVID-19 within 1 year. Occupationally, one was medical physicist, one RT technician, one secretary, and one physician.

A medical physicist

The patient is a 34-year-old male. He was the first COVID-19-positive personnel in our clinic; the virus was transmitted outside the city where he was on leave in the 4th month of the pandemic, from a COVID-19 (+) relative who was not wearing a mask. On his return, after working routinely with personal protective equipment (PPE) in our clinic with mild fatigue, he found out that his contact relative was rRT-PCR (+). He was tested, and the result was positive. The personnel with whom he was in close contact in the clinic continued to work using PPE and symptom monitoring. One of our secretaries was quarantined once it was discovered that he had unmasked contact outside the hospital, but his rRT-PCR test came negative. After his COVID-19 infection was treated, our physicist employee returned to the work.

A radiotherapy technician

The patient is a 32-year-old male. In the 8th month of the pandemic, our employee whose spouse had rRT-PCR (+) was quarantined. Although he was asymptomatic, his rRT-PCR was found to be positive on the 5th day of quarantine. After completing his treatment, he returned to the clinic and started working.

A physician

The patient is a 40-year-old male. rRT-PCR was (+) performed due to flu infection symptoms that started in the 8th month of the pandemic. It was shocking that he became infected despite using PPE with extreme caution. Except for wearing the surgical mask for 8 h without changing it and one or two people in proximity, there was no risk of infection. The tests conducted on family members, patients, and clinic employees all came negative.

A secretary

The patient is a 35-year-old male. In the 9th month of the pandemic, his spouse's rRT-PCR resulted positive, and the test performed on the 4th day owing to his complaint was rRT-PCR (+) as well. Our employee who required medical care as a result of lung involvement returned to the clinic and resumed work after the treatment was finished.

A physician

The patient is a 46-year–old male. He was on leave for 3 months according to the Ministry of Health's circular on chronic patients' administrative leave due to the pandemic in our country, due to his current diagnosis of scleroderma.


  Discussion Top


Cancer patients are among the most vulnerable groups due to their clinical conditions, which include risk of local and distant metastases, as well as their ongoing treatment, which involves the risk of virus transmission. Treatments were disrupted due to the strict precautions implemented in the early days of the pandemic. Lockdowns, hospital bed shortages, the allocation of COVID-19 intensive care rooms, planning most procedures to prioritize the pandemic, and constraints such as deferring elective surgical treatments are all examples of these precautions. Furthermore, some patients delayed or cancelled their admittance to the hospital on their own initiative due to COVID-19 infection concerns. However, there has been a proportionate increase in the number of advanced cancer patients in oncology clinics in the last phases of this process.[10] In oncology treatment, RT alone is insufficient for the best local control (LC), just as it is in surgery. RT is not a stand-alone treatment for most cancer patients, but it is an essential treatment to prolong survival (SC) and establish LC. In several cancer diagnoses, it is utilized as an adjuvant therapy. For SC and LC, the timing of this treatment is just as crucial as the overall radiation dose. Delaying adjuvant RT for 8 weeks or more after surgery, for example, is known to double the chance of local recurrence in individuals with breast cancer.[11] Furthermore, RT lowered the chance of LC by 3.8% (from 25.2% to 21.4%) in the 15-year breast cancer mortality risk.[12] Treatment delays have also been reported to lower by 7.5% the overall survival outcomes of women with locally advanced cervical cancer in 4-year survival when delaying the start of RT more than 10 weeks.[13] Delaying RT for 48 days or longer after surgery reduced survival by almost 7 months in patients with newly diagnosed high-grade glioblastoma multiforme from brain tumors undergoing RT, according to research.[14]

Oncology and geriatric patients were definitely the most affected in the early days of the pandemic when the entire effort of the health struggle was focused on infection. The stress experienced by a geriatric oncology patient with breast cancer and Alzheimer's disease and her daughter has been published in a letter nearer the onset of the pandemic.[3] To shorten the duration of RT, the conventional approaches were modified. These measures, for example, hypofractionated schemes to shorten hospital stays and overall treatment time, were published by the National Radiation Oncology Association. Most RT clinics used a linear-quadratic model to provide various fraction doses, intervals, and dosages with the same BED value to solve clinical challenges. The TDF for BED losses owing to breaks was computed, and the effective treatment dose was administered. TDF is calculated using the Orton–Ellis Model.[5] In circumstances when the dose per fraction was altered without modifying the treatment duration, the Withers formula was used to determine the 2 Gray Fraction Equivalent Dose (EQD2), abbreviated as EQD2. The equation EQD2 = D × ([d + α/β])/2 Gy + α/β) was used to do the calculations. Here, D: Total dose, d: Dose per fraction, and α/β ratio was the dose where linear and quadratic components were equal.[6],[15] Furthermore, the LQ model, which was first developed in the 1980s, was derived using the formula BED = D (1 + d/α/β), which is most typically employed in bioefficiency evaluations, to change or shorten the overall treatment time, particularly with hypofractionated models.[16] To normalize the total dosage,[17] 2 Gy equivalent dose calculations are utilized in this formula, and it is used to provide the same equivalent dose in varied fraction doses.

One of the most serious syndromes encountered in oncological emergencies was our fifth patient who had VCSS that requires prompt RT. The COVID-19-induced acute respiratory syndrome can be mistaken as VCSS. Clinical and laboratory results should be investigated in these instances, which require a careful differential diagnosis. COVID-19 infection is indicated by clinical signs such as fever and cough in these patients. Although imaging is very useful in diagnosing and evaluating the condition, coronavirus rRT-PCR positivity is required for a conclusive diagnosis.[18] CT examination results were significantly faster than rRT-PCR during the 1st year, which normally took 5–6 h.[19] As a result, in such emergency cases, radiological diagnosis was taken into account. Infection with COVID-19 increases the chance of death in people with lung cancer,[20] especially in smokers.[21] The necessary functional results can be accomplished with the use of hypofractionated radiation therapies for palliation of oncological emergencies in the pandemic setting without postponing therapy.[22] For patients with oncological emergencies, many prospective studies and national guidelines support the use of shorter RT courses. Previous VCSS studies have shown that 8.5 Gy × 2 weeks or 4 Gy × 5 days fractions provide equal symptom alleviation to conventional fractionation.[23]

Infection with COVID-19 can be accompanied with a variety of neurological symptoms. A study claims that the virus reaches the brain via the olfactory nerve in anosmia patients, causing hyperdense MRI images,[24] which must be taken into account in patients with brain tumors. After COVID-19 infection, the MRI of our 6th patient with a brain tumor revealed that the current findings were tumor progression. As in this patient with a high-grade tumor, we think that it would be beneficial to perform new imaging if there is a break for more than 3 weeks.

Individuals with asymptomatic COVID-19 infection make up 86% of the whole case pool, as they did in our seventh and eighth cases.[25] These two asymptomatic patients were identified by rRT-PCR. As a result, the probability of intraclinical transmission was reduced to a minimum. During the 1st year with no vaccines, screening of asymptomatic patients with PCR test during the treatments provided the opportunity for early diagnosis.


  Conclusion Top


From an oncological standpoint, COVID-19 viral transmission can be increased due to long-term treatments. Difficulties in reaching treatment, tumor progression because of interrupted treatments, asymptomatic carrier patients, and symptom overlap that require careful differential diagnosis affect the management and RT of cancer patients. Hypofractionated regimens, which can shorten the treatment period, TDF calculations due to the intervals given, and the formulas we stated in our article, which will allow the initial dose of BED to be given, are all helpful in the management of RT during the pandemic.

As the duration of our study is not long enough to include LC and life time, these issues have been left out. In this study, attention has been drawn to the calculation of TDF for doctors facing the pandemic for the first time, decreasing the number of fractions and deferral of some patients. For sure, we are well aware that LC and life expectancy are the indicators of the clinical effectivity of the interventions. It may not be appropriate to mention the manipulations that are not reflected in this time frame. New studies will be conducted if/when the pandemic terminates, with a larger number of patients and longer follow-up periods, to see how patients have been affected throughout this time.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Mayor S. COVID-19: İmpact on cancer workforce and delivery of care. Lancet Oncol 2020;21:633.  Back to cited text no. 1
    
2.
Baumann M, Overgaard J, Bacchus C. Radiotherapy & oncology during the COVID-19 pandemic. Radiother Oncol 2020;146:221-2.  Back to cited text no. 2
    
3.
Rakici SY, Cankay TU. Do little things cast great shadows? Indian J Cancer 2020;57:358-9.  Back to cited text no. 3
[PUBMED]  [Full text]  
4.
Slotman BJ, Lievens Y, Poortmans P, Cremades V, Eichler T, Wakefield DV, et al. Effect of COVID-19 pandemic on practice in European radiation oncology centers. Radiother Oncol 2020;150:40-2.  Back to cited text no. 4
    
5.
Orton CG, Ellis F. A simplification in the use of the NSD concept in practical radiotherapy. Br J Radiol 1973;46:529-37.  Back to cited text no. 5
    
6.
Scalliet P, Cosset JM, Wambersie A. Application of the LQ model to the interpretation of absorbed dose distribution in the daily practice of radiotherapy. Radiother Oncol 1991;22:180-9.  Back to cited text no. 6
    
7.
Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: Estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer 2005;104:1129-37.  Back to cited text no. 7
    
8.
Chen HH, Kuo MT. Improving radiotherapy in cancer treatment: Promises and challenges. Oncotarget 2017;8:62742-58.  Back to cited text no. 8
    
9.
Corman VM, Landt O, Kaiser M, Molenkamp R, Meijer A, Chu DK, et al. Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR. Euro Surveill 2020;25:1-4.  Back to cited text no. 9
    
10.
Nagar H, Formenti SC. Cancer and COVID-19-potentially deleterious effects of delaying radiotherapy. Nat Rev Clin Oncol 2020;17:332-4.  Back to cited text no. 10
    
11.
Huang J, Barbera L, Brouwers M, Browman G, Mackillop WJ. Does delay in starting treatment affect the outcomes of radiotherapy? A systematic review. J Clin Oncol 2003;21:555-63.  Back to cited text no. 11
    
12.
Early Breast Cancer Trialists' Collaborative Group (EBCTCG), Darby S, McGale P, Correa C, Taylor C, Arriagada R, et al. Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: Meta-analysis of individual patient data for 10,801 women in 17 randomised trials. Lancet 2011;378:1707-16.  Back to cited text no. 12
    
13.
Lanciano RM, Pajak TF, Martz K, Hanks GE. The influence of treatment time on outcome for squamous cell cancer of the uterine cervix treated with radiation: A patterns-of-care study. Int J Radiat Oncol Biol Phys 1993;25:391-7.  Back to cited text no. 13
    
14.
Katsigiannis S, Krischek B, Barleanu S, Grau S, Galldiks N, Timmer M, et al. Impact of time to initiation of radiotherapy on survival after resection of newly diagnosed glioblastoma. Radiat Oncol 2019;14:73.  Back to cited text no. 14
    
15.
Lee YC, Rash DL, Stern RL, Mayadev JS. The equivalent dose contribution from high-dose-rate brachytherapy to positive pelvic lymph nodes in locally advanced cervical cancer. Brachytherapy 2013;12:555-9.  Back to cited text no. 15
    
16.
Jones B, Dale RG, Deehan C, Hopkins KI, Morgan DA. The role of biologically effective dose (BED) in clinical oncology. Clin Oncol (R Coll Radiol) 2001;13:71-81.  Back to cited text no. 16
    
17.
Kaya V, Aksu MG, Korcum AF, Tuncel N. Investigation of medulla spinalis doses in patients with head and neck cancer treated with radiotherapy. Turk J Oncol 2009;24:1-8.  Back to cited text no. 17
    
18.
Matucci-Cerinic M, Bruni C, Allanore Y, Clementi M, Dagna L, Damjanov NS, et al. Systemic sclerosis and the COVID-19 pandemic: World Scleroderma Foundation preliminary advice for patient management. Ann Rheum Dis 2020;79:724-6.  Back to cited text no. 18
    
19.
Long C, Xu H, Shen Q, Zhang X, Fan B, Wang C, et al. Diagnosis of the coronavirus disease (COVID-19): RRT-PCR or CT? Eur J Radiol 2020;126:108961.  Back to cited text no. 19
    
20.
Rogado J, Pangua C, Serrano-Montero G, Obispo B, Marino AM, Pérez-Pérez M, et al. COVİD-19 and lung cancer: A greater fatality rate? Lung Cancer 2020;146:19-22.  Back to cited text no. 20
    
21.
Luo J, Rizvi H, Preeshagul IR, Egger JV, Hoyos D, Bandlamudi C, et al. COVID-19 in patients with lung cancer. Ann Oncol 2020;31:1386-96.  Back to cited text no. 21
    
22.
Yerramilli D, Xu AJ, Gillespie EF, Shepherd AF, Beal K, Gomez D, et al. Palliative radiation therapy for oncologic emergencies in the setting of COVID-19: Approaches to balancing risks and benefits. Adv Radiat Oncol 2020;5:589-94.  Back to cited text no. 22
    
23.
Sundstrøm S, Bremnes R, Aasebø U, Aamdal S, Hatlevoll R, Brunsvig P, et al. Hypofractionated palliative radiotherapy (17 Gy per two fractions) in advanced non-small-cell lung carcinoma is comparable to standard fractionation for symptom control and survival: A national phase III trial. J Clin Oncol 2004;22:801-10.  Back to cited text no. 23
    
24.
DeKosky ST, Kochanek PM, Valadka AB, Clark RS, Chou SH, Au AK, et al. Blood biomarkers for detection of brain ınjury in COVID-19 patients. J Neurotrauma 2021;38:1-43.  Back to cited text no. 24
    
25.
Inkaya AC, Er AG, Demir AU, Ertenli AI, Alp A, Topeli Iskit A, et al. COVİD-19 Pandemic Report (20 March-20 November 2020); 2021.  Back to cited text no. 25
    



 
 
    Tables

  [Table 1]



 

 
Top
 
 
  Search
 
     Search Pubmed for
 
    -  Uslu GH
    -  Kucuktulu E
    -  Rakici SY
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusion
References
Article Tables

 Article Access Statistics
    Viewed245    
    PDF Downloaded12    

Recommend this journal