Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes.

OBJECTIVE: To study the fear of Covid 19 infection among Norwegian patients with type 1 diabetes. RESEARCH DESIGN AND METHODS: Fear of Covid 19 scale, a validated scale assessing the fear of Covid 19, was sent electronically to 16255 patients with type 1 diabetes in May 2021. The items are rated on a scale from 1 to 5 (total scores from 7 to 35). The higher the score, the greater the fear.
RESULTS: 10145 patients, 52% of the Norwegian adult type 1 diabetes population, completed the questionnaire. The mean total fear score was 13.8 (SD 5.8). Women experienced more fear than men (OR 1.96), and fear increased significantly with increasing age for both genders (p<0.05). Fear increased with increasing BMI, more pronounced for men than women. Fear was positively correlated to HbA1c (Spearman rho 0.067, p<0.05), and significantly increased in patients with micro- and macrovascular complications, compared with patients without complications (p<0.05). Smokers showed increased fear compared with non-smokers, (1.59 (1.39-1.81)), and non-European patients reported more fear than Europeans (OR of 2.02 (95% CI 1.55-2.63).
CONCLUSION: Assessment of fear of Covid 19 in the type 1 diabetes population in Norway revealed an overall low fear during the third wave of infection. Patients considered to be at high risk of serious disease, such as older individuals, smokers and obese individuals expressed more fear than low risk individuals. The degree of fear was also associated with sex, ethnicity, educational/working status, glycemic control and presence of complications.

Introduction

The coronavirus 2019 (Covid 19) is included in the family of β-coronavirus that affects pulmonary gas exchange and triggers a cytokines storm. Fever, dry cough, sneezing, shortness of breath and respiratory distress are the most common symptoms of Covid-19. Inflammation, hyper-coagulation, decreased lymphocytic count with increased neutrophilic count are often observed during the course of the disease. People with a weak immune system are more susceptible to an attack of coronavirus [1].

The Covid 19 pandemic has, to date, infected more than 245 million individuals and caused more than 5 million deaths worldwide [2]. The high infection rate and relatively high mortality rate, as well as limited effective treatment, has led to the Covid 19 pandemic potentially triggering fear and anxiety. Current evidence suggests that a psychiatric epidemic is co-occurring with the Covid 19 pandemic [3]. In line with this, some evidence suggests that infectious disease-related public health emergencies (like pandemics) may increase the suicide risk [4]. The disruption of normal life because of a government-imposed lockdown or quarantine rules has significantly contributed to mental health problems globally [5]. Fear of Covid 19 and an expected increase in psychological problems is an area that merits further investigation during and after the Covid 19 pandemic.

The risk of developing fear and anxiety is probably higher in elderly people, and in people with comorbidities, populations that are shown to have more frequent hospitalization, more severe disease, and higher mortality rates if infected with Covid 19 [6].

In 2016, the prevalence of diagnosed type 1 diabetes was 0.55% in the United States [7]. Diabetes mellitus and other chronic conditions such as severe kidney disease, ongoing cytostatic treatment, heart failure, severe immune deficiency and Downs syndrome carry increased risk of hospitalization for Covid 19 infections, and increased Covid 19 related mortality [6, 8]. A previous study demonstrated that hypertension and diabetes mellitus were the most common chronic illnesses in patients admitted to hospitals with Covid 19 [9].

Whether the increased risk is directly connected to diabetes or to associated factors such as age, obesity or other comorbidities is largely unknown. Regarding differences in severity of Covid 19 infection among subgroups of diabetes mellitus, three British studies indicate that type 1 and type 2 diabetes were both independently associated with significant increased odds of in-hospital death with Covid 19, but more pronounced in type 1 diabetes [10-12]. Furthermore, the French CORONADO study of 1317 diabetes patients hospitalized for Covid 19 infection (mostly type 2 diabetes) found that age, treatment for obstructive sleep apnea, microvascular and macrovascular complications were independently associated with the risk of death on day 7 [13].

In Norway patients with diabetes mellitus are advised to get an annual flu vaccine because of the increased risk of short-term diabetes complications and an increased risk of pneumonia. Despite this, people with diabetes mellitus were not given high priority during the rollout of the Covid 19 vaccination program in Norway. People with diabetes in older age groups have been prioritized, but diabetes as an underlying disease only qualified for the fifth of nine priority groups in the vaccine queue, and then only for patients above the age of 55 years. This may have contributed to more social isolation for diabetes patients than the background population.

In March 2020, Ahorsu et al published The Fear of Covid 19 Scale (FCV-19S), a seven-item scale, shown to have robust psychometric properties [14]. The scale has been found reliable and valid in assessing fear of Covid 19 among the general population, and has been translated into 35 languages, including Norwegian. We present the results of the fear of Covid 19 score collected electronically from 10145 Norwegian patients with type 1 diabetes who were registered in the Norwegian diabetes register for adults (NDR-A) during the third wave of the pandemic in Norway, in May 2021. The aim of this study is to assess the fear of Covid 19 among Norwegian patients with type 1 diabetes, and correlate the findings to demographic parameters, metabolic control and complications.

Methods and material

Participants/data collection

A total of 21484 individuals with type 1 diabetes were registered in the NDR-A in May 2021. Of these, 17828 people with type 1 diabetes aged ≥18 years had attended at least one consultation at a Norwegian diabetic outpatient clinic during the last 15 months. In May 2021, the NDR-A sent the fear of Covid 19 questionnaire electronically via Helsenorge and Digipost to the 16255 (91%) patients who were digitally active and reachable on at least one of the platforms. A reminder was sent after 14 days. In total, 10217 (64%) answered the questionnaires before the deadline at the end of May 2021. Patients who had not answered all seven questions (n = 72) were excluded, leaving 10145 patients to be included in the main calculations.

Measurements

Clinical and sociodemographic variables like ethnic origin, gender, age, diabetes duration, glycaemic control (HbA1c), insulin regimen, long-term diabetes complications and smoking habits were retrieved from the NDR-A. Self-reported data on education and employment status were obtained from supplementary questions included in the PROM questionnaire.

Fear of Covid 19 scale (FCV-19S)

The FCV-19S is a seven-item scale that assesses the fear of Covid 19. The seven items (e.g. “I am most afraid of corona”) are rated on a 5-point scale from 1 (strongly disagree) to 5 (strongly agree) with total scores ranging from 7 to 35. The higher the score, the greater the fear of Covid 19 [14]. The internal consistency reliability for the Norwegian version of the FCV-19S has been found to be very good when assessed by Cronbach’s alpha (0.88) [15].

Statistical analysis

Descriptive statistics were used to quantify patient characteristics. Continuous variables were reported as mean (SD), and median (range). Categorical variables were reported as number (n) and percent (percentage). Logistic regression analysis for binary categorical outcome variable was performed for establishing the association with the demographic indicators, where the outcome variable (Covid fear) was computed as a binary variable using count of any response as “agree” or “strongly agree” for fear questions.

Ethical considerations

All the participants have given written informed consent that their personal health data can be registered in the NDR-A and used for research. The NDR-A has ethical approval to collect PROMs in addition to demographic and clinical data from people with diabetes enrolled in the register. The present study has received approval from the Regional Committee for Medical and Health Research Ethics (REK Vest; ref. no. 171685) to extract data from the register for analyses.

Results

Study population

A total of 10217 patients were included in the study (see “Fig 1” for the selection of patients), where 10145 completed the FCV-19S, and 72 patients had only partly completed the FCV-19S. Furthermore, 7611 patients did not answer the questionnaire, or were not digitally active and could therefore not be contacted. Table 1 shows demographic characteristics for the patients that answered the form completely, compared with patients that did not answer, or only partially completed the FCV-19S.

Fig 1

Flowchart illustrating the inclusion of patients in the study.

Table 1

Demographic and clinical data for the study population that completed the fear of covid 19 questionnaire (responders, n = 10145), compared with patients that did not answer the form, or had incomplete answers (non-responders, n = 7683).

	Responders		Non responders
Variables
Gender (n (%))
Female	4653	(45.9)	3263	(42.5)
Male	5492	(54.1)	4420	57.5
Age categories, years (n (%))
18–29	1756	(17.3)	1863	(24.2)
30–39	1749	(17.2)	1397	(18.2)
40–49	2071	(20.4)	1219	(15.9)
50–59	2331	(23.0)	1333	(17.3)
60–69	1532	(15.1)	899	(11.7)
70–79	632	(6.2)	743	(9.7)
Education (n (%))
Primary and lower secondary school (10years)	707	(7.0)
Upper secondary school	3025	(29.8)
Vocational school	1655	(16.3)
University college (4 years or less)	2837	(28.0)
University (more than 4 years)	1863	(18.4)
Occupational status (n (%))
Unemployed (and not under education)	2700	(26.6)
Full-time work	5476	(54.0)
Part-time work	1081	(10.7)
Student	492	(4.8)
Part-time work and student	298	(2.9)
Ethnicity (n (%))
European	9223	(90.9)	6839	(89.0)
African	72	(0.7)	145	(1.9)
Asian	110	(1.1)	142	(1.8)
Other	46	(0.5)	37	(0.5)
Unknown	1	(0.0)	0	(0.0)
Smoking habits (n (%))
Never smoker	5847	(57.6)	4437	(57.8)
Daily smoker	1042	(10.3)	927	(12.1)
Ex-smoker	2839	(28.0)	1935	(25.2)
Unknown	66	(0.7)	79	(1.0)
Complications (n (%))
No complications	3036	(29.9)	2019	(26.3)
Microvascular complications	3184	(31.4)	2310	(30.1)
Macrovascular complications	1054	(10.4)	978	(12.7)
Insulin regime (n (%))
Insulin pen	6439	(63.5)	5228	(68.0)
Insulin pump	3563	(35.1)	2340	(30.5)
BMI kg/m2
BMI (mean (SD))	26.9	(4.9)	26.3	(5.0)
BMI < 25 (n (%))	3694	(36.4)	3143	(40.1)
BMI 25–30 (n (%))	3820	(37.7)	2640	(34.4)
BMI > 30 (n (%))	2131	(21.0)	1469	(19.1)
HbA1c mmol/mol
HbA1c (mean (SD))	59.2	(12.8)	63.0	(14.7)

Overall, more men (54.1%) than women answered the questionnaire and were included in the study. The majority of the study population were between 30 and 60 years of age (60.6%). A high proportion (46.4%) had a college or university degree, and 26.6% were either retired or unemployed.

Total fear score

The mean total fear score was 13.8 (SD 5.8), and the median score was 12 (range 7–35) (Table 2). “Fig 2” illustrates the mean fear score for each of the seven questions in the questionnaire. As shown, question 1 and question 2 contributed most to the fear of Covid 19, and question 6 and 7 contributed the least.

Table 2

Showing total fear score in the different patient categories.

	Total fear score
	Mean	SD
Age
Age < 50	13.4	5.7
Age ≥ 50	14.2	5.9
Age < 70	13.8	5.8
Age ≥ 70	13.7	5.7
HbA1c
HbA1c < 75	13.7	5.8
HbA1c ≥ 75	14.5	6.4
Complications
No complications	13.6	5.7
Microvascular complications	13.9	5.8
Macrovascular complications	14.6	6.1
Insulin device
Insulin pen	13.7	5.8
Insulin pump	14.0	5.8
Ethnicity
European	13.7	5.8
Non-european	16.7	7.3
African	15.5	7.2
Asian	17.8	7.7
Other	16.2	6.4
Occupational status
Unemployed (and not under education)	15.1	6.3
Full-time work	13.0	5.4
Part-time work	14.9	6.1
Student	12.8	5.5
Part-time work and student	13.0	5.1
Education
Primary and lower secondary school (10years)	15.9	6.9
Upper secondary school	14.2	6.1
Vocational school	14.1	5.9
University college (4 years or less)	13.2	5.4
University (more than 4 years)	12.7	5.2
Smoking habits
Never smoker	13.3	5.6
Daily smoker	15.1	6.5
Ex-smoker	14.2	5.9
Unknown	13.8	6.3

Footnote: For comparison, the mean total fear score across all categories was 13.8 with sd = 5.8.

Fig 2

Mean score of fear for the seven questions in the fear of Covid 19 scale in the whole study population.

A total of 11.9% of the patients strongly disagreed with all the questions and had the lowest possible total score on the FCV-19S. For three of the questions, all of which assessed somatic symptoms (q3, q6, and q7), very few patients “agreed” or “strongly agreed” with the question (4.9, 1.6, and 2.8% respectively).

Fear score assessed against various demographic and clinical variables

Age and gender

Women had significantly higher total fear scores than men at 15.1 vs. 12.6 (p<0.05) (Table 2). Women had twice the risk of fear compared with men, with an OR of 1.94 (95% CI 1.79–2.10) (Table 3). “Fig 3A” illustrates the correlation between the fear scores and age in both genders. As shown the total fear score was significantly higher in women than in men (p<0.05), and both genders showed significantly increased fear scores with increasing age (p<0.05). The highest fear score was found in women aged 60–69 years, with a mean total fear score of 15.8 (SD 5.9). There was a significantly higher mean fear score among patients more than 50 years old compared with patients less than 50 years old, 14.2 (5.9) vs. 13.4 (5.7) (p<0.05). We found no significant difference in fear score between those below and above 70 years of age 13.8 (5.8) vs. 13.7 (5.7) (p = 0.75).

Table 3

Table showing odds ratio (OR) of fear for different variables of interest.

Characteristics	Univariate analysis			Multivariate analysis
	OR	95% CI	P-value	OR	95% CI	P-value
Gender
Male	ref			ref
Female	1.94	1.79–2.10	<0.001	1.98	1.82–2.16	<0.001
European
Yes	ref			Ref
No	2.02	1.55–2.63	<0.001	1.98	1.50–2.61	<0.001
Smoking
Never smoker	ref			ref
Daily smoker	1.59	1.39–1.81	<0.001	1.44	1.24–1.66	<0.001
Ex-smoker	1.30	1.19–1.42	<0.001	1.31	1.18–1.44	<0.001
Unknown	1.25	0.77–2.05	0.365	1.13	0.67–1.91	0.650
Unemployed
No	ref
Yes	1.80	1.65–1.97	<0.001	1.7	1.54–1.87	<0.001

Fig 3

Correlation between fear score and increasing age (A), BMI (B) and HbA1c (C) for women and men. The difference and correlations are statistically significant with p<0.05.

BMI

“Fig 3B” illustrates a correlation between BMI and total fear score, more pronounced in men with a correlation coefficient of 0.096 compared with 0.062 for women. The differences and correlation were significant (p<0.05).

Glycemic control, complications, and treatment regimes

There was a significant correlation between HbA1c and total fear score (rho 0.067, p<0.05), more pronounced for women than men (“Fig 3C”). Patients with HbA1c below 75 mmol/mol had significantly lower fear scores (mean score 13.7, SD 5.76) compared with those with HbA1c above 75 mmol/mol (mean score 14.5, SD 6.36), p<0.05. The difference in mean total fear score between patients treated with multiple daily injection therapy compared with insulin pump was small, but significantly higher in pump users, with a mean score of 13.6 (SD 5.81) and 14.0 (5.83) respectively. There was also significantly higher total fear scores in patients with diabetic micro- and macrovascular complications, compared with patients without complications (Table 2).

Ethnicity, socioeconomic status and smoking habits

There was a significantly higher total fear score in non-European patients compared with European patients. Non-Europeans showed a twofold risk of fear compared with Europeans, with an OR of 2.02 (95% CI 1.55–2.63). The mean fear score was 16.7 (SD 7.37) compared with 13.7 (SD 5.77) respectively (p<0.05). The Asian patients showed the highest fear scores with a mean score of 17.8 (SD 7.7). Furthermore, there was a clear significant association between educational status and fear, with a lower fear score with increasing educational level (Table 2). In addition, for unemployed and retired patients the fear score was significantly higher than patients working part time or full time (p<0.05). Daily smokers had significantly higher fear scores than former smokers and non-smokers (p<0.05), and the OR for fear were 1.59 (1.39–1.81) for daily smokers compared with non-smokers.

Patients that did not answer the questionnaire or answered incompletely

The 7683 patients that did not answer (n = 7611), or answered the questionnaires incompletely (n = 72) had quite similar demographic and clinical data when compared to patients who answered all questions. See Table 1 for comparison.

Discussion

To the best of our knowledge, the present study comprises the largest cohort of patients assessed with a validated fear of Covid 19 scale reported to date. Approximately 52% (n = 10217) of the Norwegian adult type 1 diabetes population were included in the study [16]. The results showed an overall low level of fear of Covid 19. The fear score increased with increasing age and was more pronounced in women than men. Our data also showed a significant correlation between impaired glycemic control and fear, and an association between fear scores and the presence of diabetic complications.

The total fear score was generally low, with a total mean score of 13.8/35 for the whole diabetes population. This could be because the questionnaire was sent out in the end of the third wave of infection in Norway (May 2021), when patients had been exposed to the pandemic for 15 months. In addition, by May 2021, 32% of the adult population had received one vaccine dose, and 8.6% had received two doses [17]. Our findings are supported by a study from Denmark by Musche et al [18], which studied anxiety and fear of Covid 19 among diabetic patients earlier in the pandemic (April 2020). They found that generalized anxiety and depression were similar in patients with diabetes and healthy controls, but the diabetic patients reported higher Covid 19-related fear, increased risk perception, and behavioral changes.

As illustrated in “Fig 3A”, the fear score was higher in women than men. Our findings are in line with findings from Basit et al [19] who assessed the fear of Covid 19 among a subgroup of Pakistani patients with type 2 diabetes. However, this result is in contrast to the finding of Ahorsu et al, who has developed the fear of Covid 19 scale in the general Iranian population. They found that gender had no effect on the fear score [14].

“Fig 3A” shows a significant positive correlation between age and fear scores, stronger for men than for women. The finding is reasonable as older age was launched as a risk factor for serious disease and bad outcome early in the pandemic. The finding is however in conflict with findings from Basit et al, who found no association between fear scores and age [19], and findings from Lee et al, who assessed the coronavirus anxiety in healthy Turkish people. They found that younger people were more afraid of Covid 19 than older people [20].

Early in the pandemic obesity was highlighted as a risk factor for serious disease and increased mortality [21, 22]. We found higher BMI to be associated with increased fear scores (“Fig 3B”), and more pronounced for men than for women. In contrast, Kizilkaya et al [23] showed in their study of 568 obese Turkish patients that the population with the highest BMI (above 50 kg/m2) showed less fear of Covid 19, accessed by FCV-19S. However, these patients had a considerably higher BMI than the obese patients in our cohort and are probably not directly comparable.

Early in the pandemic, diabetes mellitus was flagged as an independent risk factor for poor prognosis and fatal outcome in Covid 19 infections. This was later adjusted to be true for type 2 diabetes and obesity, more than diabetes mellitus in general. We found fear scores to be correlated to HbA1c-level. There were also a significantly higher fear score in the group of patients with diabetic complications compared with patients without complications, with the highest fear score in patients with macrovascular complications. Serin et al found the same pattern for patients with diabetes type 2 in Turkey [24]. To the best of our knowledge, there are no other studies comparing the fear of Covid 19 scores to the glycemic control, treatment and complications in type 1 diabetic patients. Although a large Danish study has mapped Covid 19-specific worries and overall psychosocial health among people with diabetes in the initial phase of the Covid 19 pandemic in Denmark [25]. Their results showed that being female, having type 1 diabetes, diabetes complications and diabetes distress, feeling isolated and lonely, and having changed diabetes behaviors were associated with being more worried about Covid 19.

Non-European patients showed significantly higher fear scores compared with patients of European descent. Of the non-European patients, Asian patients had the highest fear scores. In addition, we found that patients with a higher level of education experienced less fear than patients with a lower level of education. The study of Lee et al revealed opposite findings, higher fear with higher educational level.

The World Health Organization released early in the pandemic a statement warning that smokers are more likely to experience a severe Covid 19 illness relative to non-smokers [26], a warning broadcasted in media outlets [27] and supported by scientific studies [28, 29]. Our findings revealed that smokers had significantly greater fear than former smokers and non-smokers. Basit et al showed similar findings with an odds ratio as high as four between non-smokers and daily smokers in the Pakistani type 2 diabetic population [19].

A large study performed in Bergen, Norway in June 2020 assessing fear of Covid 19 in the background population found similar finding to ours [15]. A higher FCV-19S score was positively associated with being female, older age groups, and lower socioeconomic status (lower education and income).

The high number of patients and the high response rate among type 1 diabetic patients are strengths of this study. The studied population is thought to be representative of type 1 diabetes patients in Norway. The results of the study should be interpreted in light of the prevalence of Covid 19 at the time of the data collection, and a possible limitation of our study is the relatively low level of viral transmission in the society when the questionnaire was distributed. In addition, the digital collection of data could have introduced bias into our results. The large number of participants could make the study “over powered”, finding statistically significant results that are rather weak and not clinically relevant. Nevertheless, our findings match quite well with what is expected based on patient groups flagged as high risk individuals by the health authorities and should help clinicians to identify subgroups of diabetes patients that may require addition psychological support to address fear of Covid 19 during diabetes follow-up.

Conclusion

In conclusion, we present a valid assessment of the fear of Covid 19 status in the population of patients with type 1 diabetes in Norway. Overall, we found that the fear of Covid 19 was low during the third wave of infection. Patients considered being at high risk of serious disease by the authorities, such as older individuals, smokers and obese individuals showed a higher level of fear than low risk individuals did. In addition, women, non-European individuals, patients with a lower level of education and not in regular employment showed a higher degree of fear. Finally, we revealed a higher degree of anxiety for Covid 19 in patients with poor glycemic control and diabetes patients with vascular complications. The need for additional psychological support among patient groups found to have increased fear of Covid 19 should be assessed during the diabetic consultation. Finally, the methodological principle with digital collection of data directly from the patient is a novel and exciting way to enrich clinical studies in the future.

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Reviewer #1: 1. Grammatical, formatting and spacing mistakes should be corrected in the manuscript. Font color should be black.

2. Introduction should include background of COVID-19 and type 1 diabetes especially prevalence, symptoms of COVID-19, its main variants and the role of immunity in prevention of this viral disease. Following articles can be used as references:

(Endocr Metab Immune Disord Drug Targets. 2022; https://doi.org/10.2174/1871530322666220110113028).

(J Med Virol. 2021; https://doi.org/10.1002/jmv.27256).

3. Reference format should be modified according to journal.

4. Most of the participants were male (54.1%) in your study but fear factor is more in female then man. justify this statement.

5. Result is too long, try to trim it by removing extra explanation.

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Reviewer #1: Yes: Sibgha Noureen

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

7 Apr 2022

Point-to-point rebuttal letter

Thank you for the constructive comments on our manuscript PONE-D-22-07616

“Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes”

We have now carefully revised the paper according to the comments by the reviewer as detailed below. Changes in the manuscript are made in red. We hope you will find the revised version acceptable for publication.

Editor Comments: The paper should be checked by a professional speaker of English before complete acceptance.

The paper has now been checked by last author of the manuscript, John Cooper, who is a native Englishman.

Journal Requirements:

When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

The manuscript is now formatted according to PLOS Ones style requirements.

2. Please provide additional details regarding participant consent. In the ethics statement in the Methods and online submission information, please ensure that you have specified (1) whether consent was informed and (2) what type you obtained (for instance, written or verbal, and if verbal, how it was documented and witnessed). If your study included minors, state whether you obtained consent from parents or guardians. If the need for consent was waived by the ethics committee, please include this information.

If you are reporting a retrospective study of medical records or archived samples, please ensure that you have discussed whether all data were fully anonymized before you accessed them and/or whether the IRB or ethics committee waived the requirement for informed consent. If patients provided informed written consent to have data from their medical records used in research, please include this information.

All the participants have given written informed consent. This information is now included in the method section, page 7 line 142.

3. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability.

"Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized.

Important: If there are ethical or legal restrictions to sharing your data publicly, please explain these restrictions in detail. Please see our guidelines for more information on what we consider unacceptable restrictions to publicly sharing data: http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. Note that it is not acceptable for the authors to be the sole named individuals responsible for ensuring data access.

We will update your Data Availability statement to reflect the information you provide in your cover letter.

Sharing of individual participant data with third parties was not specifically included in the informed consent of the study, and unrestricted distribution of such data may pose a potential threat of revealing participants’ identities. To minimise this risk, researchers who wish to inquire about access to individual participant data that underlie the results reported in this article can submit a request to the The Norwegian Adult Diabetes registry (noklus @noklus.no). To gain access, researchers will need to sign a data access agreement and obtain the approval of the local ethics committee.

4. Please include a copy of Table 2 which you refer to in your text on page 7.

We apologize for the mistake, as Table 2 was identical with Supplementary Table S1. We have now chosen to include Supplementary Table S2 in the main manuscript, as Table 3. We no longer need a supplementary file. The alterations in the numbering of tables are now marked in red throughout the manuscript.

5. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information

Supporting/supplementary file is no longer included in the manuscript.

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

________________________________________

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

________________________________________

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

________________________________________

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

________________________________________

5. Review Comments to the Author

Reviewer #1: 1. Grammatical, formatting and spacing mistakes should be corrected in the manuscript. Font color should be black.

We have reviewed the manuscript carefully, and hope that all grammatical, formatting and spacing mistakes are corrected. Font color is black.

2. Introduction should include background of COVID-19 and type 1 diabetes especially prevalence, symptoms of COVID-19, its main variants and the role of immunity in prevention of this viral disease. Following articles can be used as references:

(Endocr Metab Immune Disord Drug Targets. 2022; https://doi.org/10.2174/1871530322666220110113028).

(J Med Virol. 2021; https://doi.org/10.1002/jmv.27256).

Thank you for this valuable suggestion of improvement, we have now included this in the introduction page 3, line 47-53 and page 4 line 73-74.

3. Reference format should be modified according to journal.

We have now modified the reference to style Vancouver as required.

4. Most of the participants were male (54.1%) in your study but fear factor is more in female then man. justify this statement.

You are correct, there are more men than women with type 1 diabetes in Norway, and our study population is therefore representative for the actual patient population. In addition, we have a high number of study participants, and the statistical power is high- so the fact that more men than women are participating is not affecting the results.

5. Result is too long, try to trim it by removing extra explanation.

Thank you- we have now trimmed the results section from the original 854 words to 734 words.

6. Be specific with your topic and shorten your discussion up to 2 pages. References are also missing in most of the sentences in discussion.

We agree, the discussion was too long. We have shortened it from 1862 words to 1445 words, which corresponds to 4 pages instead of 6 (discussion without conclusion).

7. What are the limitations of your study?

We agree that the limitations of the study should have been presented more explicitly. We have addressed this problem with a revised section on page 14, line 315-322:

The results of the study should be interpreted in light of the prevalence of COVID 19 in the country at the time of the data collection. In Norway, the first cases of COVID 19 were confirmed in February 2020. The peak of the outbreak was during March and April 2020. The third wave of infection in Norway started in the middle of March 2021, and as of the 1st of May 2021 (when the fear questionnaire was sent out), the total number of confirmed Covid 19 cases was 113899 and there had been 766 deaths from Covid 19 (31). The relatively low level of viral transmission in the society when the questionnaire was distributed, and the digital collection of data could have biased our results, and is an important limitation of the study.

The large number of participants could make the study “over powered”, finding statistic significances that are rather weak and not clinically relevant.

8. What is the future perspective of your study?

Regarding future perspective of the study, we have presented the findings of this study at a national meeting for both doctors and nurses- to encourage vigilance in this area at diabetic outpatient clinics and, if necessary, to provide psychological help to those with a high level of fear of Covid 19.

Furthermore we have distributed a much larger questionnaire to all diabetes patients (both DM1 and DM2) in Norway registered in the national register for adults to assess how these patients have coped with the pandemic overall. The results are to be processed.

In addition, we think that the methodological principle with digital collection of data directly from the patient is a novel and exciting way to enrich clinical studies in the future. (Included in the conclusion of the manuscript)

Submitted filename: Point to point rebuttal letter Fear of covid 19 .docx

Click here for additional data file.

30 May 2022

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Muhammad Sajid Hamid Akash

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: No

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: 1. Summarize the whole manuscript comprehensively in the abstract (limit the words up to 250).

2. Figure 3 is not clear, re-draw this figure and add caption of graphs as well.

3. As you mentioned that you have cite the suggested paper on page 4 line 73-74, but in your manuscript suggested paper is cited on line 72 with reference # 8 rather than reference # 9. It means the sequence of references is incorrect.?

4. Font color should be black in introduction. Re-check your font setting and correct it.

5. Paragraph setting of whole manuscript is required as well. Paragraph setting should be justified.

6. Try to trim the discussion furthermore (maximum 3 pages).

7. Conclude your findings under a separate heading.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Sibgha Noureen

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

8 Jun 2022

Point-to-point rebuttal letter

Thank you for the constructive comments on our manuscript PONE-D-22-07616

“Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes”

We have addressed the comments of the reviewers in the revised paper. Changes in the manuscript are highlighted in red. The manuscript has been checked for grammar and syntax by native English speaker. We hope you will find the revised version acceptable for publication.

Reviewer #1:

1. Summarize the whole manuscript comprehensively in the abstract (limit the words up to 250).

We think the abstract comprehensively covers the whole manuscript, and it consists of 240 words.

2. Figure 3 is not clear, re-draw this figure and add caption of graphs as well.

Figure 3 is now re-drawn, and section 3A, 3B and 3C are submitted as individual figures to secure better resolution. All graphs have captions. The figure legend is also updated/improved.

3. As you mentioned that you have cite the suggested paper on page 4 line 73-74, but in your manuscript suggested paper is cited on line 72 with reference # 8 rather than reference # 9. It means the sequence of references is incorrect.?

The sequences of references are correct, however the page and line numbers were incorrect. We have rectified the error.

Suggested reference (Endocr Metab Immune Disord Drug Targets. 2022; https://doi.org/10.2174/1871530322666220110113028) is reference 1, page 3 line 52.

And suggested reference (J Med Virol. 2021; https://doi.org/10.1002/jmv.27256) is reference 8 at page 4 line 72.

4. Font color should be black in introduction. Re-check your font setting and correct it.

Font color is black in the introduction.

5. Paragraph setting of whole manuscript is required as well. Paragraph setting should be justified.

We have reassessed the paragraph setting of whole manuscript, and justified it.

6. Try to trim the discussion furthermore (maximum 3 pages).

We have shortened the discussion substantially, and it is now just over 3 pages.

7. Conclude your findings under a separate heading.

We have now established a separate heading for Conclusion (line 298).

Submitted filename: Ueland rebuttal rev 2 Fear of covid 19 08.06.2022 .docx

Click here for additional data file.

20 Jun 2022

PONE-D-22-07616R2

Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes

PLOS ONE

Dear Dr. Ueland,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we have decided that your manuscript does not meet our criteria for publication and must therefore be rejected.

The authors have not addressed all the comments raised by the reviewer. The responses are not sufficient to re-review this paper. My decision is to reject this paper at this stage.

I am sorry that we cannot be more positive on this occasion, but hope that you appreciate the reasons for this decision.

Kind regards,

Muhammad Sajid Hamid Akash

Academic Editor

PLOS ONE

- - - - -

For journal use only: PONEDEC3

1 Jul 2022

Point-to-point rebuttal letter

Thank you for the constructive comments on our manuscript PONE-D-22-07616

“Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes”

We have addressed the comments of the reviewers in the revised paper. Changes in the manuscript are highlighted in red. The manuscript has been checked for grammar and syntax by native English speaker. We hope you will find the revised version acceptable for publication.

Reviewer #1:

1. Summarize the whole manuscript comprehensively in the abstract (limit the words up to 250).

We think the abstract now comprehensively covers the whole manuscript, and it consists of 240 words.

2. Figure 3 is not clear, re-draw this figure and add caption of graphs as well.

Figure 3 is now re-drawn, and section 3A, 3B and 3C are submitted as individual figures to secure better resolution. All graphs have captions. The figure legend is also updated/improved.

If you want the figure to look different, please specify, and we will try to change it further.

3. As you mentioned that you have cite the suggested paper on page 4 line 73-74, but in your manuscript suggested paper is cited on line 72 with reference # 8 rather than reference # 9. It means the sequence of references is incorrect.?

The sequences of references are correct, however the page and line numbers were incorrect. We have rectified the error.

Suggested reference (Endocr Metab Immune Disord Drug Targets. 2022; (https://doi.org/10.2174/1871530322666220110113028) is referred in reference 1, page 3, line 52.

And suggested reference (J Med Virol. 2021; https://doi.org/10.1002/jmv.27256) is reference 8 at page 4 line 72.

4. Font color should be black in introduction. Re-check your font setting and correct it.

Font color is changed to black in the introduction, and the whole manuscript.

5. Paragraph setting of whole manuscript is required as well. Paragraph setting should be justified.

We have reassessed the paragraph setting of whole manuscript.

The introduction is divided into paragraphs without subheadings.

The method section is subdivided into paragraphs with the following subheadings: Participants/data collection, Measurements, Fear of Covid 19 scale, Statistical analysis and Ethical considerations.

The result section is divided into paragraphs with the following headings:

Study population, Fear score assessed against various demographic and clinical variables, patients that did not answer or answered incomplete.

The discussion part is divided into paragraphs without subheadings.

6. Try to trim the discussion furthermore (maximum 3 pages).

We have shortened the discussion substantially from 1632 words to 1047 words, and it is now 3 pages.

7. Conclude your findings under a separate heading.

We have now established a separate heading for Conclusion (line 299).

Submitted filename: Ueland rebuttal rev 3 Fear of covid 19 08.06.2022 .docx

Click here for additional data file.

13 Jul 2022

Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes

PONE-D-22-07616R3

Dear Dr. Ueland,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Your response to prior reviews has resulted in a large improvement in the manuscript.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Edward Jay Trapido, ScD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Thank you for being responsive to the reviews and for your multiple submissions. I believe your comments and changes have been useful.

Reviewers' comments:

18 Jul 2022

PONE-D-22-07616R3

Fear of Covid 19 during the third wave of infection in Norwegian patients with type 1 diabetes

Dear Dr. Ueland:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Edward Jay Trapido

Academic Editor

PLOS ONE