Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia: Systematic review and meta-analysis

Akine Eshete Abosetugn; Sisay Shewasinad Yehualashet

doi:10.1371/journal.pone.0258938

. 2021 Oct 28;16(10):e0258938. doi: 10.1371/journal.pone.0258938

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia: Systematic review and meta-analysis

Akine Eshete Abosetugn ^1,^*,^#, Sisay Shewasinad Yehualashet ^2,^#

Editor: Sina Azadnajafabad³

PMCID: PMC8553047 PMID: 34710155

Abstract

Background

Untreated sexual dysfunction is a serious sexual problem that adversely affects the quality of life. Body of evidence indicates non-communicable diseases are common comorbid conditions associated with sexual dysfunction. Therefore, this review was aimed to synthesize and estimate the burden of sexual dysfunction and its determinant factors among patients with non-communicable diseases in Ethiopia.

Methods

Cross-sectional studies were systematically searched using PubMed, Google Scholar, African Journals Online, Cochran Library, Scopus database, and gray literature. Data were extracted using a standardized Joanna Briggs Institute form. The I² statistic was used to check heterogeneity across the included studies. A funnel plot and Egger’s regression test were used to check the presence of publication bias. Sensitivity analysis was deployed to check the effect of a single study on the overall estimation. All statistical analyses were done using STATA version 11.0 software.

Result

A total of six studies with 2,434 study participants was included. The estimated pooled sexual dysfunction was 68.04% (95% CI: 56.41–79.67). Based on the subgroup analysis, the highest prevalence of sexual dysfunction was reported among patients with mental related illness, 73.02% (95% CI: 54.00–92.03).

Conclusion

In this review, nearly seven out of ten patients with chronic illness have sexual dysfunction, which implies sexual dysfunction was highly prevalent among non-communicable patients. Therefore, health care providers should screen and manage sexual dysfunction during follow-up for improving patient quality of life and sexual reproductive health satisfaction.

Introduction

The burden of non-communicable diseases (NCDs) is one of the major health threats in the world. According to the World Health Organization (WHO’s) report in 2018, NCDs killed 41 million people each year, accounting for 71% of all deaths in worldwide.

In developing countries, it is unacceptably high that contributed to 78% of deaths and 85% were premature deaths [1]. NCDs have been steadily increasing and contributing to 39.3% of deaths. Now a day NCDs have been becoming a major agenda in Ethiopia [2, 3].

Sexual dysfunction is a comorbidity of NCDs in both sexes [3, 4]. Evidence showed that sexual dysfunction was an organic complication associated with diabetes mellitus [5], cardiovascular diseases [6], hypertension [7], and stroke [8]. Unmet needs for sexual and reproductive health services in both sexes are compounded by the increased burden of noncommunicable diseases that negatively impact women’s [9] and men’s reproductive health [10]. Untreated sexual dysfunction can have major consequences for patients, as it decreases their quality of life and self-esteem, and is linked to a decrease in sexual satisfaction [11, 12].

Sexual dysfunction (SD) is a sexual behavior and sensation disorder that manifests as a lack of sexual psychology and physiological response [13]. It is any physical or psychological problem that prevents the person or couple from getting sexual satisfaction from sexual activity [14]. SD is a general term that includes erectile dysfunction, failure of sexual intercourse, and loss of desire [13].

In Ethiopia, SD is a common yet underappreciated complication of most NCDs. The global burden of SDs in both sexes has been reported in several studies, ranging from 43.8% to 85.5% [15–21]. Despite the fact that these studies differed, they all demonstrated that SD is considered a public health issue. However, these large variances throughout Ethiopia’s geographical areas may make it difficult for planners, policymakers, implementors, and service providers to create trustworthy evidence. As a result, this systematic review and meta-analysis was to synthesize and estimate the burden of SD and its determining factors among patients with noncommunicable diseases in Ethiopa. The goal of this systematic review is to find out "what is the estimated burden of SD among NCD patients in Ethiopia?". Finally, the findings of this systematic review and meta-analysis will be utilized to update planners and policymakers on how to improve patient and health-care provider communication in order to overcome SD. It was also used as a starting point for researchers looking for potential causes of SD in NCD patients.

Methods

Study settings

This systematic and meta-analysis study included studies done only in Ethiopia. Ethiopia is one of the east African countries in the Horn of Africa. It covers 1.104 million km² and is divided into nine regions specifically Tigray, Afar, Amhara, Oromia, Somali, Benishangul-Gumuz, Southern Nations, Nationalities, and People Region (SNNPR), Gambella, Harari, and two Administrative states (Addis Ababa town administration and Dire Dawa town administration).

Inclusion criteria

Type of studies

Cross-sectional studies and government reports on sexual dysfunction caused by non-communicable diseases were considered, both published and unpublished. Human subjects, full-text articles, gray and grey literature authored in English and published in peer-reviewed journals between 2000 and 2020 were included.

Study participants

Patients with any types of NCDs, including diabetes, hypertension, cancer, cardiovascular disease, and mental illness.

Types of outcome measures (sexual dysfunction)

A standardized tool was used to assess sexual dysfunction. The International Index of Erectile Function (IIEF-5) consists of five items, each of which was assessed on a five-point ordinal scale, with lower scores indicating poorer sexual function. As a result, a question response of 1 was deemed the least functional, while an answer of 5 was deemed the most functional. The IIEF-5 offers a range of possible scores from 1 to 25 (one question has a range of 1–5), with a score of 21 or higher indicating normal erectile function and a score of 21 or lower indicating Erectile Dysfunction (ED). On the basis of IIEF-5 scores, ED is divided into four categories: severe (1–7), moderate (8–11), mild to moderate (12–16), mild (17–21), and no ED (22–25) [22].

The total score for both the female and male based on the Changes in Sexual Functioning Questionnaire (CSFQ-14) was calculated by adding the values of items 1 to 14. Scores of 41 or less for females and 47 or less for men showed sexual dysfunction [23].

Exclusion criteria

Citations without abstracts and/or full text, commentaries, anonymous reports, letters, duplicate studies were excluded.

Search strategy

Initially, the Cochrane database of a systematic review, Joanna Briggs Institute (JBI) database of a systematic review and PROSPERO databases were checked for the presence of ongoing studies related to the current topic.

Electronic database searches were conducted using PubMed/PMC, Google Scholar, African Journals Online, Scopus database, and Cochrane Library from May 1-31/ 2020, and updated June 15/2021 to decrease time-lag bias. To check the availability of articles on institutional repositories, a manual search was undertaken from gray literature. To find relevant articles, we looked through the reference lists of all the articles we found. The search was organized using CoCoPop, with the following parameters: context (Ethiopia), condition (Sexual dysfunction related to NCDs), and population (patient with non-communicable diseases).

Using Boolean operators, the search strategies were developed. The following search strategy was applied.

	MeSH Terms	Article yield
First search	("sexual dysfunctions, psychological"[MeSH Terms] OR ("sexual"[All Fields] AND "dysfunctions"[All Fields] AND "psychological"[All Fields]) OR "psychological sexual dysfunctions"[All Fields] OR ("sexual"[All Fields] AND "dysfunction"[All Fields]) OR "sexual dysfunction"[All Fields] OR "sexual dysfunction, physiological"[MeSH Terms] OR ("sexual"[All Fields] AND "dysfunction"[All Fields] AND "physiological"[All Fields]) OR "physiological sexual dysfunction"[All Fields] OR ("sexual"[All Fields] AND "dysfunction"[All Fields])) AND ("ethiopia"[MeSH Terms] OR "ethiopia"[All Fields])	639
2^nd search	Burden[All Fields] AND ("noncommunicable diseases"[MeSH Terms] OR ("noncommunicable"[All Fields] AND "diseases"[All Fields]) OR "noncommunicable diseases"[All Fields] OR ("non"[All Fields] AND "communicable"[All Fields] AND "disease"[All Fields]) OR "non communicable disease"[All Fields]) AND ("sexual dysfunctions, psychological"[MeSH Terms] OR ("sexual"[All Fields] AND "dysfunctions"[All Fields] AND "psychological"[All Fields]) OR "psychological sexual dysfunctions"[All Fields] OR ("sexual"[All Fields] AND "dysfunction"[All Fields]) OR "sexual dysfunction"[All Fields] OR "sexual dysfunction, physiological"[MeSH Terms] OR ("sexual"[All Fields] AND "dysfunction"[All Fields] AND "physiological"[All Fields]) OR "physiological sexual dysfunction"[All Fields] OR ("sexual"[All Fields] AND "dysfunction"[All Fields])) AND ("ethiopia"[MeSH Terms] OR "ethiopia"[All Fields])	82

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Data extraction

The essential data were extracted using a standardized data extraction form developed by the Joanna Briggs Institute (JBI). The authors’ names, year of publication, study area, study design, sample size, a measurement for sexual dysfunction, prevalence of sexual dysfunction, and information about the domain of sexual dysfunction are all included in the data extraction format.

Two authors (AE, SS) were independently extracted all relevant data from each study. During the extraction process, data discrepancy among data extractors was resolved by discussion and consensus and also by referring back to the original study. The PRISMA flow chart was used to summarize the screening and selection procedure for the reviewed articles [24].

Risk of bias

To remove duplicate studies, the data was transferred to Endnote version 7. A search strategy was developed by the investigators (AE and SS). The reviewers were blinded to the journal, authors, and results. There were no conflicts between the two reviewers in the final decisions. The selections of identified studies were done in two stages. In the first stage, a selection of relevant studies is based on titles and abstracts. In the second stage, studies that met the inclusion criteria and the full paper were found for detailed assessment.

Using JBI criteria [25], two authors independently assessed articles eligibility and risk of bias for the included studies. JBI developed a critical appraisal checklist for cross-sectional studies to evaluate methodological quality and risk of bias (“S1 Table”).

Data synthesis and statistical analysis

The STATA software version 11.0 was used to analyze the data. A random-effects model is used to display the extracted data from each study in a meta-analysis. A forest plot was used to generate the pooled effect size of sexual dysfunction with a 95% confidence interval (CI).

Heterogeneity between studies were assessed using the Cochran’s Q and I² statistic [26] and I² statistical test with a value of ≥75% and p ≤ 0.05 indicating the presence of moderate to high levels of significant heterogeneity [27]. Subgroup analysis and meta-regression analysis were performed to investigate sources of heterogeneity. In a sensitivity analysis, potential individual outliers were treated by deleting each study one at a time. To determine the presence of publication bias, the funnel plot and Egger’s test were utilized [28]. The Egger test revealed a statistically significant publication bias with a p-value less than 0.05. To account for the impacts of publication bias, trim-and-fill analysis was performed.

Data presentation and reporting of results

PRISMA [29] form was used to report the findings. A PRISMA flow diagram was used to summarize the screening and selection procedure for the examined articles.

Results

Search results

The search strategy retrieved 823 studies from PubMed, Cochrane library, Google scholar, and gray literature. Of these, 13 articles were searched manually using grey literature. After removing duplicate publications, 205 articles remained. About 198 articles were excluded by reading the titles and abstracts of the studies based on the pre-defined eligibility criteria. Seven articles were included for systematic review and screened for further assessment. Finally, six studies were included for meta-analysis (Fig 1).

Characteristics of included studies

For a systematic review, the search approach provides a total of seven relevant papers with a total sample size of 3279. The samples of each article were varied significantly in size, ranges from 249 to 845. Two studies were conducted in the Amhara region [15, 16], two in the Tigray region [30, 31], two in Addis Ababa [19, 32], and one study in the Southern Nation Nationality People Region (SNNPR) [21]. Six studies were institution-based cross-sectional studies, whereas one study [31] was a community-based cross-sectional study. The quality of each study was scored based on the JBI quality assessment checklists. The main features including studies were presented in table (Table 1).

Table 1. Description of the included studies.

Authors, with a publication year	Study area/region	Sample	Prevalence of sexual dysfunction (SD), n (%), and other important findings	Type of NCDs	Type of measurement	JBI-Quality score
Ejigu AK et al., 2019 [32]	Addis Ababa	576	363(63.3%) had sexual dysfunction SD for male 67.4%, for female 55.6% Frequency of SD domains; sexual arousal problem, 97.8%, sexual pain problem, 11.3%, sexual desire problem, 94.8%, orgasmic dysfunction 89.9%, sexual pleasure problem 95.1%	Epilepsy	CSFQ-14-	8/9*100 = 89%
Asefa A. et al., 2019 [21]	SNNPR	398	212 (53.3%) had SD SD for male 52%, for female 56.6% Frequency of SD domains; sexual arousal problem, 40.2%, sexual desire problem, 48.2%, orgasmic dysfunction, 45.7%, sexual pleasure problem, 34.4%, desire frequency problem 55.8%	Diabetes mellitus	CSFQ-14	8/9*100 = 89%
Fanta T. et al., 2018 [19]	Addis Ababa	422	349 (82.7%) had SD SD for male 84.5, for female 78.6	Schizophrenia	CSFQ-14	8/9*100 = 89%
Walle B. et al. 2018 [16]	Amhara	422	361 (85.5%) had SD Category of ED: Mild ED, 66(18.3), Moderate ED, 234(34.18%) and severe ED, 61(16.9)	Diabetes mellitus	IIEF-5	8/9*100 = 89%
Seid A. et al. 2017 [30]	Tigray	249	174 (69.9%)) had SD Category of ED: Mild ED, 66(18.3%), Moderate ED, 234(34.18%) and severe ED, 61(16.9%)	Diabetes mellitus	IIEF-5	8/9*100 = 89%
Tesfaye et al. 2020 [15]	Amhara	367	195 (53.1) had SD	Diabetes mellitus	IIEF-5	8/9*100 = 89%

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Changes in Sexual Functioning Questionnaires (CSFQ-14-), International index of erectile function (IIEF-5), SNNPR; Southern Nations Nationalities and People Region, ED; Erectile dysfunction, SD; Sexual Dysfunction.

The burden of sexual dysfunction

The highest prevalence of sexual dysfunction was observed in Amhara (85.5%) [16] and Addis Ababa (82.7%) [19], whereas the lowest prevalence was in Tigray (43.8%) [31]. The highest burden of sexual dysfunction was associated with diabetes mellitus and schizophrenia patients [16, 19].

The sexual dysfunction among males was reported in both studies conducted in Addis Ababa (82.7%) [19], and (67.4%) [32], whereas in females, sexual dysfunction was observed in Addis Ababa (78.6%) [19]. In all included studies: sexual arousal dysfunction, sexual pain problem, pleasure dysfunction, sexual desire disorder, orgasmic dysfunction, desire dysfunction were the most prevalent sexual dysfunctions.

Erectile dysfunction was a problem for the patients. In a study conducted in Amhara, the prevalence of erectile dysfunction was high (85.5%) [16]. The majority of the patients [16, 30] had moderate erectile dysfunction. In one study, severe erectile dysfunction was found 16.9% [16].

Meta-analysis results

The estimate of sexual dysfunction

The estimated pooled sexual dysfunction among NCDs patients using the random effect model was 68.04 (95%CI: 56.41–79.67) with heterogeneity (I² = 97.8%; p < 0.001). The weights of studies using the random-effect model were ranging from 16.42 to 16.82 (Fig 2).

Subgroup analysis

The study area, publication year, and type of NCDs were used to create subgroups. There was variability among the included studies in all subgroup analyses (Table 2).

Table 2. Subgroup analysis by different category of the studies.

Categories	Sexual dysfunction with (95% CI)	Heterogeneity	No. studies
Study area / Regional status
• Addis Ababa	73.02 (54.00–92.03)	I2 = 98.0%, p = 0.000	2
• Amhara region	69.36 (37.61–101.11)	I2 = 99.1%, p = 0.000	2
• SNNPR and Tigray	61.53 (45.27–77.80)	I2 = 94.7%, p = 0.000	2
Year of publication
• >2019	56.71 (49.64–63.78)	I2 = 85.7%, p = 0.000	3
• <2017	79.71 (71.96, 87.47)	I2 = 90.8%, p = 0.000	3
Type of NCDs
• Mental health-related illness (Epilepsy and schizophrenia)	73.02 (54.00, 92.03)	I2 = 98.0%, p = 0.00	2
• Diabetes mellitus	65.50 (48.09, 82.91)	I2 = 98.2%, p = 0.000	4

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Meta-regression analysis

A meta-regression analysis of the study area, year of publication, type of NCDs, and sample size found that the number of covariates adjusted in the analysis was not associated with the estimated OR (P = 0.887, P = 0.149, P = 0.634, P = 0.972) respectively (Table 3).

Table 3. Meta-regression analysis for the included studies to identify the source(s) of heterogeneity.

Variable	Coef.	Std. Err.	P>\|t\|	95% CI
Study area/region	-0.02577	0.1701	0.887	(-0.497,0.4463)
Publication year	-0.1946	0.109	0.149	(-0.497, 0.108)
Type of NCDs	-0.14678	0.285	0.634	(-0.938, 0.645)
Sample size of study	0.001	0.00014	0.972	(-0.0039, 0.0041)

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Sensitivity analysis

Sensitivity analysis was performed, one study is excluded at a time and the impact of removing each of the studies is evaluated on the pooled estimate and heterogeneity. Sensitivity analyses using the random-effects model revealed that no single study influenced the estimates (Fig 3).

Publication bias

Regarding publication bias, the visual inspection of the funnel plot was asymmetrical at the bottom (Fig 4), but the Egger test showed that a p-value of 0.112 which indicated no evidence of publication bias. The trim-and-fill method imputed for missing studies and recalculated our pooled but no significant change in the finding (Fig 5).

Discussion

Sexuality is one of the facets of quality of life and wellbeing [33, 34]. However, sexual functioning and sexual satisfaction rarely consider aspects of the life of patients with NCD in clinical practice because NCD assessment and treatment typically focus on the reduction of symptoms. Little attention is dedicated to the strengths and positive outcomes of individuals with this condition.

This systematic review and meta-analysis was to synthesise and quantify the pooled level of sexual dysfunction among NCDs patients in Ethiopia. Sexual dysfunction was shown to be prevalent among non-communicable disease patients, ranging from 43.8% [31] to 85.5% [16]. Sexual arousal dysfunction, sexual pain problem, pleasure dysfunction, sexual desire disorder, orgasmic dysfunction, and desire dysfunction were the most common sexual dysfunctions in both sexes, according to the study. Understanding the barriers to sexual dysfunction associated with noncommunicable disease complications was therefore crucial in developing effective policies, programs, and interventions that were appropriate for the nature of the sexual disorder.

In this current meta-analysis, the estimated pooled sexual dysfunction was 68.04% with 95% CI: (56.41–79.67) among patients with non-communicable patients in Ethiopia. This pooled estimate of sexual dysfunction was nearly consistent with a systematic and meta-analysis study in the world 76% [35] and a systematic and meta-analysis study in Africa 71.45% [36]. As a result, this meta-analysis finding suggests that sexual dysfunction is a common but often neglected consequence among non-communicable disease patients. To manage sexual dysfunction as a result of NCDs, a multimodal therapeutic approach must be strengthened, with a focus on treatment adherence and psychological support.

Despite the fact that non-communicable disease patients have a high rate of sexual dysfunction, the majority of them do not seek medical help [37]. Researchers cited embarrassment, shame, stigmatization fear, and a threat to marriage as reasons for not reporting to doctors [37, 38]. On the other side, physicians are reluctant to engage with their patients on issues of sexual functioning due to socio-cultural barriers [39]. As a result, the unmet needs for sexual and reproductive health needs are coupled with the rising burden of non-communicable diseases that adversely affect the reproductive health of women [9] and men [10]. Indeed, untreated sexual dysfunction is strongly linked to a patient’s quality of life and self-esteem, both of which are directly linked to sexual satisfaction [11, 12].

Based on subgroup analysis, the pooled prevalence of sexual dysfunction among patient with mental related illness (particularly epilepsy and schizophrenia) was 73.02% (95% CI: 54.00–92.03). Several mental disorders and related treatments interfere with sexual function [40]. Several prospective cohort studies have explored the relation between sexual dysfunction and the risk of depression [41, 42]. The prevalence of sexual dysfunction may be explained by comorbid depression due to overlapping symptoms such as "loss of interest and pleasure feelings" and "loss of libido". As a result of this finding, clinicians can better design preventative strategies and therapies to increase patient quality of life and sexual satisfaction.

This systematic review and meta-analysis have different clinical and public health practice implications. Estimating the prevalence of sexual dysfunction among patients with noncommunicable diseases is critical for guiding healthcare professionals in minimizing NCD-related sexual satisfaction complications. Furthermore, it provides data on the burden and public health impact of sexual dysfunction caused by non-communicable diseases in a country, which can be used to improve health-care policy and clinical practice.

There are some limitations to this systematic review and meta-analysis study that should be considered in future research. First, because there are so few studies, it may be difficult to generalize the results to all NCD patients in the country. Second, in the included studies, different criteria for diagnosing sexual dysfunction were used, which could alter the assessment of the pooled prevalence of sexual dysfunction. Third, this study does not identify the barriers to sexual dysfunction among NCD patients or the factors that contribute to it.

Ethiopia, being one of Africa’s most populous countries, may suffer a burden of early deaths and disabilities due to NCDs by 2040. Even though, the national response to NCDs remains fragmented and insignificant, there are encouraging actions on NCDs in terms of political commitment, NCDs prevention, and treatment services at the primary health care level [43].

In order to improve a patient’s quality of life, screening and management of sexual dysfunction must be included as part of the assessment throughout their follow-up [44, 45]. These findings may have clinical implications, such as practical suggestions for the prevention and management of sexual dysfunction in NCD patients. A physician and health care provider should diagnose sexual dysfunction in NCD patients as soon as possible. Furthermore, the national health system must be reorganized to assure acknowledgement of the NCD burden, maintain political commitment, allot sufficient financing, and improve the organization and delivery of NCD services related to reproductive and sexual health at the primary health care level.

Despite the fact that pathophysiological variables are not yet identified in this investigation. This demonstrated that all-cause sexual dysfunction could reflect the existence of common pathogenic pathways among NCDs patients, therefore more research is needed to identify other risk variables such as disease duration or other pathological variables such as aging, inflammation, medication, and stress in the development of sexual dysfunction across a wide variety of illnesses. Furthermore, comprehending the barriers to sexual dysfunction associated with non-communicable disease complications was critical in developing context-based specific preventive strategies, as well as treatment focusing on adherence and psychological support for improving patient quality of life and sexual reproductive health satisfaction.

Unhealthy diets, physical inactivity, cigarette use, and alcohol abuse are the key risk factors for NCDs. As a result, the majority of these diseases are preventable, as they proceed early in life as a result of lifestyle factors [46]. In the public health sector, there is growing concern that inadequate eating has raised the risk of chronic diseases and nutrition difficulties [47]. As a result, the primary prevention of diseases focuses lifestyle modifications and interventions to reduce the risk of NCDs.

The NCD prevention plan is based on risk factor management, which includes resource allocation, multi-sectoral collaborations, knowledge and information management [48, 49]. Monitoring and assessing the progress of NCDs at the national, regional, and global levels is important.

NCDs are the primary health-care challenge in modern society. The management of risk factors is important in the treatment of NCDs. NCD required to deliver a variety of interventions from many perspectives and at various levels, including individual and national levels. Based on the assumptions developed throughout the scientific discussion above, it can be stated that modern strategies for the management of NCDs should be focused toward the individual level, where the individual is responsible because of their own health by simply living a healthy lifestyle.

To reduce NCD risk factors for disease burden and adverse outcomes, multi-sectoral activities are required. The findings will help policy and programming to reduce the burden of NCDs in the long run. Cultural norms may have an impact on how physicians manage patients with sexual problems in Ethiopia, where discussing sexual problems is taboo.

If we want to improve the treatment of sexual dysfunction caused by NCDs, we must first improve screening. Screening is not the only poor relation to the sexual health of patients suffering from NCDs. There are no specific scales allowing concrete evaluation of the perception of good health or good sexual health for these patients. Currently there are no well-structured protocols for treatment of sexual difficulties.

Conclusion

According to this systematic review and meta-analysis, sexual dysfunction was found to be 68.04% in Ethiopia, with a 95% confidence interval of (56.41–79.67). This means that roughly seven out of 10 non-communicable illness patients in Ethiopia experience sexual dysfunction, implying that sexual dysfunction is very common among non-communicable diseased patients. The combined prevalence of sexual dysfunction among individuals with mental illnesses (especially epilepsy and schizophrenia) was 73.02%t among all NCDs (95% CI: 54.00–92.03).

Supporting information

S1 Table. JBI critical appraisal checklist for studies reporting prevalence data.

(DOCX)

Click here for additional data file.^{(14.9KB, docx)}

Acknowledgments

We acknowledge the Authors of each article for reviewing their article. We would like to thank JBI for using their systemic review and meta-analysis guidance.

Abbreviations

ED: Erectile dysfunction
JBI: Joanna Briggs Institute
NCDs: Non-Communicable Diseases
PRISMA: Preferred Reporting Items for Systematic Review and Meta-Analysis
SD: Sexual Dysfunction
SNNPR: Southern Nations Nationalities and People Region

Data Availability

All relevant data are within the manuscript and its Supporting information files.

Funding Statement

The authors received no specific funding for this work.

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PLoS One. doi: 10.1371/journal.pone.0258938.r001

Decision Letter 0

Claudia Marotta

29 Sep 2020

PONE-D-20-18974

The Burden of Non-Communicable Disease on Sexual Dysfunction in Ethiopia: systematic review and meta-analysis

PLOS ONE

Dear Dr. Eshete,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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Claudia Marotta

Academic Editor

PLOS ONE

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Reviewer #1: Partly

Reviewer #2: No

Reviewer #3: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: I Don't Know

Reviewer #3: I Don't Know

**********

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

**********

5. 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: Question 1.

The paper by Eshete and Shewasinad reviewed sexual dysfunction (SD) among patients diagnosed with non-communicable diseases (NCD) in Ethiopia, synthesized and came up with an estimated burden of SD among patients with NCDs.

However, this differs from the objective of the study as stated by the authors which was to synthesize, and estimate the burden of non-communicable disease on SD and its determinant factors.

Based on the findings, the objective of the study ought to have been: to synthesize and estimate the burden of SD and its determinant factors among patients with non-communicable diseases in Ethiopia.

Secondly, the study did not find the ‘determinant factors’ stated in the objective. I suggest this aspect to be expunged.

Thirdly, based on the findings, the research question ought to have been: ‘What is the estimated burden of sexual dysfunction among patients with NCDs in Ethiopia’?

Fourthly, as stated by the authors under limitations, it will be difficult to generalize on the whole country based on just 6 papers! Furthermore, are the authors looking at NCD as a risk factor for sexual dysfunction, if so, there will be need for further studies to determine other risk factors for SD and compare them with those obtained elsewhere? Further studies should also aim at understanding the perspectives of the NCD patients found to have SD…. which of the two began first, did they happen at the same time or are they merely coincidental?. Qualitative studies will best answer these pertinent questions going forward.

Question 2: Yes

Question 3: Yes

Question 4.

I recommend language editing of the whole document as there are several typo graphical and grammar errors

Under the sub heading 'implications of the study findings', the first factual sentence 'Ethiopia will be the first among the most populous nations in Africa to experience the dramatic burden of premature deaths and disability from NCDs by 2040' should be backed by a reference.

For tables, the heading should be in italics and on top

For figures, the heading should be normal, non-italicized and below

Reviewer #2: The authors of this study made a precious effort to investigate the burden of non-communicable diseases (NCDs) on sexual dysfunction in Ethiopia, especially focusing on the quality of life of patients with NCDs. This systematic review and meta-analysis tried to investigate the mentioned notion through a comprehensive review and statistical analyses. However, some comments are necessary to be addressed and I provided them in the uploaded attachment file.

Reviewer #3: The manuscript reports on the prevalence of sexual dysfunction among patients with noncommunicable diseases in Ethiopia. While the manuscript provides important information, there is need for improvement of the manuscript. The authors may also consider revising the title of the manuscript.

The language needs significant improvement. Words are used inappropriately and sometimes incorrectly throughout the manuscript. There are several sentences which are unclear, with some sentences being very long. The wrong tense is used in several areas of the manuscript. Sentence construction needs to be improved in many areas; some of the phrases used are incomprehensible. There is some repetition; there is at least one instance in which the same sentence is used in different areas of the manuscript.

Acronyms are used without explanation, in the text JBI and in Tables (SD, ED). Some terms are being used interchangeably in the text – sexual dysfunction and erectile dysfunction, even though they do not have the same meaning.

There are areas where the text does not match what is presented in Table I. Numbers are sometimes quoted incorrectly and sometimes not listed

…the sexual dysfunction among males was reported in both studies conducted in Addis Ababa (82.7% [19] The SD listed for males for the said study is 84.5 in Table 1 and the SD for male in the second study [20} is not listed in the text

.….whereas the lowest prevalence was in Tigray (43.8%)[18]. That study is not listed in Table 1.

…………whereas in females, sexual dysfunction was observed in Addis Ababa( 78.6%) [19] There is another study done in Addis Ababa and listed in Table 1: Ejigu AK et al 2019 [20] also reported sexual dysfunction in females 55.6%, but this is not included in the text.

Although 7 studies are being cited in the text, only 6 studies are presented in Table 1. The Abstract also states 6 studies.

There is inconsistency in the way 96% CI are written in the text and Tables.

Sexual dysfunction and erectile dysfunction are being used interchangeably in the text.

Incorrect conclusions are made: The conclusion incorrectly states …..that sexual dysfunction in Ethiopia was 68.04%....without indicating that this was in patients with NCDS

The limitations section needs review. The authors seem unaware that the study limitations also need to be taken into consideration when conclusions are made in relation to this study.

Although the authors indicate that there was a small number of studies in the systematic review and meta-analysis, strong statements are made with no references provided: This indicates that seven out of ten patients with non-communicable disease have sexual dysfunction, which implies sexual dysfunction was highly prevalent among non -communicable (disease missing) patients in Ethiopia.

The Figures in the manuscript are not numbered sequentially.; 1,2, 3,5,6. There is an error in Figure 1: Records screened (n=7).

Implications of the Study Findings: This segment needs significant revision. A reference needed for the statement made in the 1st sentence. Very long unclear sentences are used in the final paragraph. Overall this section lacks clarity.

Please note that I am unable to comment on the statistical analyses used in this study. This is because I am not familiar with statistical analyses which are used for systematic reviews and meta-analyses.

**********

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Reviewer #1: Yes: Haruna Ismaila Adamu, MBBS; MPH; PhD

Reviewer #2: Yes: Sina Azadnajafabad

Reviewer #3: No

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Attachment

Submitted filename: Reviewer comments.docx

Click here for additional data file.^{(16.9KB, docx)}

PLoS One. 2021 Oct 28;16(10):e0258938. doi: 10.1371/journal.pone.0258938.r002

Author response to Decision Letter 0

17 Feb 2021

Dear Academic Editor!

PLOS ONE

Response to Reviewers

I am happy to resubmit for publication version of “Estimate the burden of sexual dysfunction due to non-communicable disease in Ethiopia: systematic review and meta-analysis” for a review as original research in PLOS ONE.

The comments of the editor and the reviewers were highly insightful and enabled us to greatly improve the quality of our manuscript. Therefore, based on the editor’s and the reviewers’ concerns we have made extensive edition in our manuscript. Particularly, we have extensively edited the manuscript by a professional language editor (English-language instructors of Debre Berhan University thoroughly edited the manuscript for language usage, spelling, and grammar) before submitting the revised version. The formatting of the text and document (text sizes and grammatical errors) was also edited. We have addressed yours’ concerns in a point by point format.

We look forward to hearing from you at your earliest convenience.

Thank you for your consideration of this manuscript!

Kind regards,

Akine Eshete

On behalf of authors

The authors of this study made a precious effort to investigate the burden of non-communicable diseases (NCDs) on sexual dysfunction in Ethiopia, especially focusing on the quality of life of patients with NCDs. This systematic review and meta-analysis tried to investigate the mentioned notion through a comprehensive review and statistical analyses. However, some comments are necessary to be addressed and I provide them below:

1. The title of the manuscript is not fully appropriate and consistent with the study aim. The last sentence of the background part of the abstract “estimate the burden of sexual dysfunction due to non-communicable disease in Ethiopia” is more appropriate for such investigation.

Response: We thank you very much for this important recommendation. We edited the title accordingly.

2. “Non-communicable disease” is better to be replaced by “Non-communicable diseases” in the last sentence of the background part of the abstract.

Response: thank you, for your important comment. Based on your recommendations, we have made revision of the manuscript accordingly

3. “Noncommunicable Diseases” is correct for keywords according to the MeSH database of PubMed.

Response: We would like to say thank you once again for your fruitful comments. This has been addressed as your recommendation.

4. The first two sentences of the introduction, exploring the statistics, need to be explained which year the belong to, provided in the reference.

Response: Based on your recommendations, we have addressed the issue.

In line 44-48.

5. A grammatical and linguistic edit is essential for this manuscript, as the numerous issues are apparent in it and make understanding the provided draft difficult.

Response: thank you very much for your important comment. We acknowledge that English is not our first language and we have edited the manuscript by an English language instructor. Based on your recommendations, we have made revision of the manuscript accordingly.

6. 2nd paragraph of introduction: are NCDs comorbidities of sexual dysfunction or sexual dysfunction is a comorbidity of NCDs?

Response: Based on your recommendations, we have addressed the issue.

In line 55-56.

7. 4th paragraph of introduction: references for the first sentence should be merged in a citation manager.

Response: Based on your recommendations, we have addressed the issue.

In line 67-69.

8. The knowledge gap is not well addressed in the introduction of the manuscript and needs to be explained more.

Response: Based on your recommendations, we have addressed the issue.

In line 49-54.

9. The “Objective” and “Research question” after the introduction, could be merged into the introduction part and is a repeat of the mentioned notions in the introduction.

Response: Based on your recommendations, we have addressed the issue.

In line 73-77.

10. In methods and materials: in inclusion criteria, types of included NCDs should be provided specifically.

Response: Based on your recommendations, we have addressed the issue.

11. In methods and materials: in inclusion criteria, what is the reference for the standardized tool for sexual dysfunction measurement? Is it validated before for the Ethiopian population?

Response: Based on your recommendations, we have addressed the issue.

In line 95-102.

12. In methods and materials: in exclusion criteria, are there any criteria of exclusion for any of NCDs, participants, or sexual dysfunction disorders? The exclusion criteria could be more detailed based on the aims of this study.

Response: Based on your recommendations, we have addressed the issue.

13. In methods and materials: why didn’t authors search the Scopus database?

Response: We thank you very much for this important recommendation and comment. It was writing problems, so it is corrected accordingly

14. In methods and materials: the search period is stated to be from inception to 2020 and also a period of 2000-2020? Please clarify which one is the searched period exactly.

Response: We thank you very much. Included study published from 2000-2020

Searching time was from May 1-31/ 2020 and updated June 5/2020

15. In methods and materials: there is not so much information about the screening process of the articles and about how did the screening was done by one or two authors.

Response: Based on your recommendations, we have addressed the issue.

In line 29-32.

16. The terms “gray literature” and “grey literature” are used both. Please, unify this term through the manuscript.

Response: Based on your recommendations, we have addressed the issue.

Gray literature is information produced by government agencies, academic institutions, and also the for-profit sector that is not typically made available by commercial publishers. Examples of gray literature include: Reports. Proceedings. Dissertations and theses.The term grey literature refers to research that is either unpublished or has been published in non-commercial form. Examples of grey literature include: government reports. policy statements and issues papers.

17. Results, Table 1, “type of measurement” column measures are not discussed in the Methods section and should be elaborated in detail and the issue of difference of measures among different studies should be addressed and discussed. How did the authors compare studies while the measure differed?

Response: Based on your recommendations, we have addressed the issue.

18. Subgroup analysis and sensitivity analysis explanations should be provided in the methods section instead of the results section.

Response: Based on your recommendations, we have addressed the issue.

19. “Fig” and “Figure” terms should be unified as “Figure” in the manuscript.

Response: we did based on the comments

20. Why there is no Figure 4 in or at the end of the manuscript?

Response: we did based on the comments

21. The terms “non-communicable patients” and “non-communicable clients” are not proper provided in many parts of the manuscript.

Response: Based on your recommendations, we have addressed the issue.

22. In discussion: did authors find any explanation for the higher prevalence of sexual dysfunction in patients with mental disorders? Please include some information about this important finding in the discussion section.

Response: Based on your recommendations, we have addressed the issue.

In line 219-223

23. In discussion: findings are not discussed well enough, and it seems authors could use literature to highlight the importance of the investigated notion and compare results with other similar studies.

Response: Based on your recommendations, we have addressed the issue.

In line 219-223

24. Also, authors could replace the paragraph “Implications of the study findings” into the discussion as a part for policymakers and public health authorities, besides the provided implications for the clinicians.

Response: Based on your recommendations, we have addressed the issue.

25. Figure 5 legend, “log” should be corrected in the legend and “LogitSD” on the figure.

Response: Based on your recommendations, we have addressed the issue.

26. The six articles included in the final analysis and report is inconsistent in Table 1 and Supplementary Table 1 in comparison to Figures 2 and 3. “Gerensea H. et al. (2018)” and “Zewlde KH. et.al. (2017)” are in tables, but “Walle et al. (2018)” and “Seid et al. (2017)” in figures.

Response: we did based on the comments

27. Included paper in analyses with reference numbers 15 “tesfaye t, bayisa m, mesfin N: Prevalence and associated factors of erectile dysfunction among men DM patients in Gondar university hospital, Gondar Ethiopia. In.: Research Square; 2020” and reference number 18 “Gebrezgabhier G, Desta H, Berhe T, Hailu E, Gebrehiwot F, Kifle Y: Prevalence and associated factors of Female Sexual Dysfunction among Female Population in Aksum Town, Tigray Region, Ethiopia, 2019. A Community Based Cross Sectional Study. In.: Research Square; 2019” included in reports are preprints in the Research Square database and not peer-reviewed articles. And this in contrast with your methods!

Response: We thank you very much for this important recommendation. We consider both published and unpublise research work. We modify the method parts

28. Included paper in analyses with reference numbers 16 “Gerensea H, Tarko S, Zenebe Y, Mezemir R, Walle B, Lebeta KR, Fita YD, Abdissa HG: Prevalence of erectile dysfunction and associated factors among diabetic men attending the diabetic clinic at Felege Hiwot Referral Hospital, Bahir Dar, North West Ethiopia, 2016. BMC endocrine disorders 2018, 11(1):130” is not traceable in online databases!

Response: We thank you very much for this important recommendation. We correct like Bizuayehu Walle, Kidist Reba Lebet , Yamrot Debela Fitaand Hordofa Gutema Abdissa. Prevalence of erectile dysfunction and associated factors among diabetic men attending the diabetic clinic at Felege Hiwot Referral Hospital, Bahir Dar, North West Ethiopia, 2016. BMC endocrine disorders 2018, 11(1):130”

29. Included paper in analyses with reference numbers 17 “Zewlde KH, Muluneh NY, Seraj ZR, GebreLibanos MW, Bezabih YH, Seid A: Prevalence and determinants of erectile dysfunction among diabetic patients attending in hospitals of central and northwestern zone of Tigray, northern Ethiopia: a cross-sectional study. BMC neurology 2017, 17(1):16” is not traceable in online databases!

Response: We thank you very much for this important recommendation. We correct like Awole Seid , Hadgu Gerensea, Shambel Tarko, Yosef Zenebe and Rahel Mezemir. Prevalence and determinants of erectile dysfunction among diabetic patients attending in hospitals of central and northwestern zone of Tigray, northern Ethiopia: a cross-sectional study. BMC neurology 2017.

30. Included paper in analyses with reference numbers 20 “Ejigu AK: Sexual dysfunction and associated factors among patients with epilepsy at Amanuel Mental Specialty Hospital, Addis Ababa - Ethiopia. Turkish journal of obstetrics and gynecology 2019, 19(1):255” is not published in the mentioned journal provided in the citation, instead of in the BMC Neurology journal!

Response: We thank you very much, we checked and published at BMC Neurology journal

Attachment

Submitted filename: response to reviewer SD.pdf

Click here for additional data file.^{(681.4KB, pdf)}

PLoS One. doi: 10.1371/journal.pone.0258938.r003

Decision Letter 1

Claudia Marotta

12 Mar 2021

PONE-D-20-18974R1

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia : systematic review and meta-analysis

PLOS ONE

Dear Dr. Eshete,

Please submit your revised manuscript by 25 March. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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'.

We look forward to receiving your revised manuscript.

Kind regards,

Claudia Marotta

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

dear authors follow Reviewers suggestions to improve your paper

[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: All comments have been addressed

Reviewer #2: (No Response)

Reviewer #3: (No Response)

**********

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

Reviewer #1: Yes

Reviewer #2: Partly

Reviewer #3: No

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: I Don't Know

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: No

**********

6. Review Comments to the Author

Reviewer #1: Question 1

My comments in the previous review have been adequately taken care of, the objective of the study now agrees with the findings

Reviewer #2: Authors of this study revised the manuscript based on the provided comments. The changes were noticeable. However, some major points still remain to be answered and considered in the manuscript. A response to the authors’ letter is provided below, by number of previous comments of mine:

1. Comment well addressed. Title is edited.

2. Comment not addressed.

3. Comment well addressed.

4. Comment well addressed.

5. Comment for language edit is addressed. However a final round of language edit is necessary prior to publication.

6. Comment well addressed.

7. Comment well addressed.

8. Comment not addressed. I meant the knowledge gap about the sexual dysfunction and NCDs in the literature. Authors added an irrelevant part about knowledge on diabetes to the introduction!

9. Comment well addressed.

10. Comment well addressed.

11. Comment partially addressed. Please add the full terms of IIEF and CSFQ. Also, please add whether the tool is standardized for the Ethiopian population or not.

12. Comment not addressed.

13. Comment well addressed.

14. Comment partially addressed. Please add the exact time period of search to the text.

15. Comment not addressed. The screening process is different from the data extraction. This comment is a major one and still needs to be answered.

16. Comment not addressed. Please provide reference for the difference you mean between gray and grey literature.

17. Comment partially addressed. Types of measurement are added to the methods. But still authors did not answer how they compare studies when the measurement tool is different. As the man concern, how did authors conduct the meta-analysis when the measurement tools were different among the included studies? It is recommended to do meta in each category separately.

18. Comment not addressed.

19. Comment well addressed.

20. Comment well addressed.

21. Comment well addressed.

22. Comment well addressed.

23. Comment well addressed.

24. Comment well addressed.

25. Comment not addressed.

26. Comment partially addressed. Reference to “Walle (2018)” is corrected. Reference to “Seid (2017)” is incorrect in the bibliography. Also, statistics of mild, moderate, and severe SD in Table 1 are not consistent with numbers in the original paper! Also, data for “Ejigu (2019)” has a problem as the total prevalence of SD was 63.9 and is stated to be 63.3.

27. Comment well addressed.

28. Comment well addressed.

29. Comment partially addressed. Citation number 34 is still incorrect in the bibliography of manuscript. Please correct it as you answered the comment.

30. Comment not addressed. Please correct the citation in the bibliography f manuscript.

Reviewer #3: The language used throughout the manuscript is sub-standard and needs significant improvement. Several of the paragraphs are constructed poorly, words are used incorrectly, poor grammar is used, some paragraphs include very long incomprehensible sentences. Acronyms are used in the manuscript sometimes without explanation, and at other times after an acronym is used, the full term is reused in the manuscript., instead of the acronym. The manuscript contains repetition.

The Discussion is not cohesive or logical. Many loose statements are made with no references. The Conclusion of the manuscript’s includes a repetition of the study results.

**********

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: Haruna Ismaila Adamu, MBBS; MPH; PhD

Reviewer #2: Yes: Sina Azadnajafabad MD MPH

Reviewer #3: No

PLoS One. 2021 Oct 28;16(10):e0258938. doi: 10.1371/journal.pone.0258938.r004

Author response to Decision Letter 1

16 Apr 2021

Dear Academic Editor!

PLOS ONE

Response to Reviewers

We look forward to hearing from you at your earliest convenience.

Thank you for your consideration of this manuscript!

Kind regards,

Akine Eshete

On behalf of authors

Reviewer #1: Question 1

My comments in the previous review have been adequately taken care of, the objective of the study now agrees with the findings

1. Comment well addressed. Title is edited.

2. Comment not addressed (“Non-communicable disease” is better to be replaced by “Non-communicable diseases” in the last sentence of the background part of the abstract.)

Response: We thank you very much for this important recommendation. We edited it accordingly.

3. Comment well addressed.

4. Comment well addressed.

5. Comment for language edit is addressed. However a final round of language edit is necessary prior to publication.

6. Comment well addressed.

7. Comment well addressed.

8. Comment not addressed. I meant the knowledge gap about the sexual dysfunction and NCDs in the literature. Authors added an irrelevant part about knowledge on diabetes to the introduction!

Response: thank you very much for your important comment, we deleted

9. Comment well addressed.

10. Comment well addressed.

11. Comment partially addressed. Please add the full terms of IIEF and CSFQ. Also, please add whether the tool is standardized for the Ethiopian population or not.

Response: thank you very much for your important comment; we adopted already standardized tools based on the context of Ethiopia

12. Comment well addressed.

13. Comment partially addressed. Please add the exact time period of search to the text (In methods and materials: the search period is stated to be from inception to 2020 and also a period of 2000-2020? Please clarify which one is the searched period exactly.)

Response: We thank you very much for this important recommendation. We edited on line 116 and 117

14. Comment not addressed. The screening process is different from the data extraction. This comment is a major one and still needs to be answered (In methods and materials: there is not so much information about the screening process of the articles and about how did the screening was done by one or two authors.)

Response: We thank you very much for this important recommendation. We edited on line 129 and 136

15. Comment not addressed. Please provide reference for the difference you mean between gray and grey literature.

Response: We thank you very much for this important recommendation. We edited on line 116

16. Comment partially addressed. Types of measurement are added to the methods. But still authors did not answer how they compare studies when the measurement tool is different. As the man concern, how did authors conduct the meta-analysis when the measurement tools were different among the included studies? It is recommended to do meta in each category separately.

Response: We thank you very much for this important recommendation; we understood that our outcome interest is sexual dysfunction. We summarized the prevalence of sexual dysfunction, which was assessed the same tool.

17. Comment not addressed (Subgroup analysis and sensitivity analysis explanations should be provided in the methods section instead of the results section).

Response: We thank you very much for this important recommendation. We edited on line from 207 to 209

18. Comment well addressed

19. Comment well addressed.

20. Comment well addressed.

21. Comment well addressed.

22. Comment well addressed

23. Comment well addressed

24. Comment not addressed (Figure 5 legend, “log” should be corrected in the legend and “LogitSD” on the figure.)

Response: We thank you very much for this important recommendation. We edited it accordingly.

25. Comment partially addressed. Reference to “Walle (2018)” is corrected. Reference to “Seid (2017)” is incorrect in the bibliography. Also, statistics of mild, moderate, and severe SD in Table 1 are not consistent with numbers in the original paper! Also, data for “Ejigu (2019)” has a problem as the total prevalence of SD was 63.9 and is stated to be 63.3.

Response: We thank you very much for this important recommendation. We edited it accordingly.

26. Comment well addressed.

27. Comment well addressed.

28. Comment partially addressed. Citation number 34 is still incorrect in the bibliography of manuscript. Please correct it as you answered the comment. It is corrected accordingly

Response: We thank you very much for this important recommendation. We edited it accordingly.

29. Comment not addressed. Please correct the citation in the bibliography f manuscript. . It is corrected accordingly

Response: We thank you very much for this important recommendation. We edited it accordingly.

Response: We thank you very much for these important comments. We corrected it accordingly the comments

Attachment

Submitted filename: Response to reviewre.docx

Click here for additional data file.^{(21.1KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0258938.r005

Decision Letter 2

Vanessa Carels

14 May 2021

PONE-D-20-18974R2

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia : systematic review and meta-analysis

PLOS ONE

Dear Dr. Eshete,

Please submit your revised manuscript by Jun 27 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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 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: http://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,

Vanessa Carels

Staff Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

Reviewer 3 has noted ongoing concerns with the language quality throughout the submission. PLOS ONE requires that the language in submitted articles must be clear, correct, and unambiguous in order to meet our fifth criterion for publication (http://journals.plos.org/plosone/s/criteria-for-publication#loc-5), and PLOS ONE does not copy edit accepted manuscripts. Please revise the manuscript for English grammar and usage as well as for scientific readability. Please note that further consideration of this work requires that this criterion is met, please ensure your revision is thorough.

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

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

Reviewer #3: (No Response)

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: No

**********

6. Review Comments to the Author

Reviewer #1: My observations in the previous reviews have been adequately addressed. I have no additional comments to make at this time.

Reviewer #2: Authors of this study revised the manuscript based on the provided comments. The changes were noticeable. The addressed comments and responses are acceptable. I hope a good production process for authors if other reviewers and dear editor approve the manuscript, too.

Reviewer #3: Review of PLOS Article Resubmission

The language used in the article is still sub-standard and needs to be improved. Some components of the manuscript are difficult to understand because of the poor sentence construction and grammar. Some sentences seem incomplete. An Acronym is introduced without explanation and then the full term is used in following text without use of the acronym. An Acronym is introduced and never used again in the text. The manuscript also contains long sentences which lack clarity.

Specifics are provided below:

Line 46 - The (WHO 2018) funding showed that 41 million cases and 57 million deaths - - Sentence unclear may be incomplete?

Line 47-49 - Sentences unclear - poor sentence construction and grammar

Lines 60-62 - long sentence and poor sentence construction

Lines 63-64 - incorrect grammar- “.....due to an “absent

The acronym SD is introduced in Line 63, but not used in the many other places following where sexual dysfunction is used (lines 68, 69, 70,73-74,78)

Lines 68-79 - unclear paragraph -

Lines 68-72 - is this about Ethiopia or worldwide (global)??

Lines 72-75 - incorrect grammar-...., this systematic review and meta-analysis were aimed to synthesize.....

Lines 76-79 - poor sentence construction and grammar

Lines 89-91 - incomplete sentence

Lines 94-100- Paragraph includes poor sentence construction and grammar

Lines 103-109 - unclear...Is that included as part of the Types of outcome measures?? Unclear what screening tool you are talking about..

Lines 118-120 - sentence incomplete

Line 124 - Acronym JBI used without explanation

Lines 124-127- Poor sentence construction

Line 129-135 - Poor grammar

Line 136- Unclear, poor sentence construction

Lines 141-150 - Poor paragraph/sentence construction, incomplete sentences, poor grammar

Lines 153-154 - incomplete sentence, incomprehensible

Lines 159 - 161 - poor sentence construction/grammar

Lines 171-172 - About 198 articles were excluded........ - Could the exact number of articles excluded be provided?..

Lines 175-176 - Poor grammar

Lines 195-197 - unclear paragraph

Lines 206-208 - To discover the potential reasons for the heterogeneity by subgroup meta-analyses were analyzed...awkward sentence/paragraph.

DISCUSSION

While improvements have been made to the Discussion by including references, the grammar and sentence construction still needs to be improved.

Lines 235-236 - poor grammar

Lines 239 - “sexual dysfunctions” - poor grammar

Line 240 - “complications was critical”- wrong tense

Lines 246-248 - poor sentence construction

Lines 251-252 - poor sentence construction

Lines 252-253 - poor sentence construction

Lines 257-259 - unclear sentence

Lines 262-266 - Very long unclear sentence

Lines 266-267 - unclear sentence

Lines 269 - 271 - poor sentence construction

Lines 274-279 - Poor construction of sentences and paragraph

Lines 280-281 - unclear sentence

Lines 285 -286 - It is “mandatory” to include screening and management ..... - Mandatory is a very strong word. - Please include reference.

Lines 294-302 - Poor grammar, very long sentence and tense confusion in the paragraph

Conclusion

The conclusion remains weak with results repeated. Requires revision.

**********

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: Haruna Ismaila Adamu, MBBS; MPH; PhD

Reviewer #2: Yes: Sina Azadnajafabad, MD, MPH.

Reviewer #3: Yes: Glennis Andall-Brereton

PLoS One. 2021 Oct 28;16(10):e0258938. doi: 10.1371/journal.pone.0258938.r006

Author response to Decision Letter 2

20 May 2021

Dear Academic Editor!

PLOS ONE

Response to Reviewers

The comments of the editor and the reviewers were highly insightful and enabled us to greatly improve the quality of our manuscript. We have addressed yours’ concerns in a point by point format.

Thank you for your consideration of this manuscript!

Kind regards,

Akine Eshet

Comments

Journal Requirements:

Response: thank you, for your important comment. We check and all references are complete and correct in line with the journal requirement.

Comments of reviewer

1. Line 46 - The (WHO 2018) funding showed that 41 million cases and 57 million deaths - - Sentence unclear may be incomplete?

2. Line 47-49 - Sentences unclear - poor sentence construction and grammar

3. Lines 60-62 - long sentence and poor sentence construction

4. Lines 63-64 - incorrect grammar- “.....due to an “absent

5. The acronym SD is introduced in Line 63, but not used in the many other places following where sexual dysfunction is used (lines 68, 69, 70,73-74,78)

6. Lines 68-79 - unclear paragraph –

Response: thank you, for your important comment. Based on your recommendations, we have made revision accordingly (Line 46-79)

7. Lines 68-72 - is this about Ethiopia or worldwide (global)??

Response: thank you, for your important comment. In the paragraph we mean that patients with non-communicable diseases in Ethiopia, we corrected

8. Lines 72-75 - incorrect grammar-...., this systematic review and meta-analysis were aimed to synthesize.....

9. Lines 76-79 - poor sentence construction and grammar

10. Lines 89-91 - incomplete sentence

11. Lines 94-100- Paragraph includes poor sentence construction and grammar

Response: thank you, for your important comment. Based on your recommendations, we have made revision accordingly (line 72-100)

12. Lines 103-109 - unclear...Is that included as part of the Types of outcome measures?? Unclear what screening tool you are talking about.

Response: thank you, for your important comment. Types of outcome measures/ domain of sexual dysfunction/, finally after computing these parameterise, researchers categorize having sexual dysfunction and not.

13. Lines 118-120 - sentence incomplete

14. Line 124 - Acronym JBI used without explanation

15. Lines 124-127- Poor sentence construction

16. Line 129-135 - Poor grammar

17. Line 136- Unclear, poor sentence construction

18. Lines 141-150 - Poor paragraph/sentence construction, incomplete sentences, poor grammar

19. Lines 153-154 - incomplete sentence, incomprehensible

20. Lines 159 - 161 - poor sentence construction/grammar

Response: thank you, for your important comment. Based on your recommendations, we have made revision accordingly (line 118-161)

21. Lines 171-172 - About 198 articles were excluded, Could the exact number of articles excluded be provided

Response: thank you, for your important comment. Using the developed Boolean operators any one checks and confirms the available studies, we excluded by considering the title and reading of abstracts

22. Lines 175-176 - Poor grammar

23. Lines 195-197 - unclear paragraph

24. Lines 206-208 - To discover the potential reasons for the heterogeneity by subgroup meta-analyses were analyzed...awkward sentence/paragraph.

Response: thank you, for your important comment. Based on your recommendations, we have made revision accordingly (line 118-161)

DISCUSSION

While improvements have been made to the Discussion by including references, the grammar and sentence construction still needs to be improved.

25. Lines 235-236 - poor grammar

26. Lines 239 - “sexual dysfunctions” - poor grammar

27. Line 240 - “complications was critical”- wrong tense

28. Lines 246-248 - poor sentence construction

29. Lines 251-252 - poor sentence construction

30. Lines 252-253 - poor sentence construction

31. Lines 257-259 - unclear sentence

32. Lines 262-266 - Very long unclear sentence

33. Lines 266-267 - unclear sentence

34. Lines 269 - 271 - poor sentence construction

35. Lines 274-279 - Poor construction of sentences and paragraph

36. Lines 280-281 - unclear sentence

Response; Thanks this important comments, we did accordingly (line 235-281)

37. Lines 285 -286 - It is “mandatory” to include screening and management ..... - Mandatory is a very strong word. - Please include reference.

Response; Thanks this important comments, we cited

38. Lines 294-302 - Poor grammar, very long sentence and tense confusion in the paragraph

Conclusion

39. The conclusion remains weak with results repeated. Requires revision.

Response; Thanks this important comments, we did accordingly

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(20.5KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0258938.r007

Decision Letter 3

Sina Azadnajafabad

30 Jun 2021

PONE-D-20-18974R3

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia : systematic review and meta-analysis

PLOS ONE

Dear Akine Abosetugn Eshete,

I am writing to notify you regarding the submitted manuscript "Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia : systematic review and meta-analysis". As an act of transparency, I am invited to handle your paper as a guest academic editor, after multiple rounds of commenting and reviewing your paper in the previous stages. After careful consideration and inspection based on the rounds of revision and the current status of your manuscript, I decided to invite one of the previous reviewers and two new expert reviewers to comment on your manuscript, as it still lacks some details and does not fully meet PLOS ONE’s publication criteria as it currently stands. However, the comments lead to a minor revision decision. Therefore, I invite you to submit a revised version of the manuscript that addresses the points raised during the recent review process.

Please submit your revised manuscript by July 12, 2021. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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'.

We look forward to receiving your revised manuscript.

Kind regards,

Sina Azadnajafabad

Academic Editor

PLOS ONE

Journal Requirements:

Additional Editor Comments (if provided):

Dear authors,

Please follow Reviewers suggestions to revise your paper.

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

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #3: All comments have been addressed

Reviewer #5: (No Response)

**********

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

Reviewer #3: Yes

Reviewer #4: Yes

Reviewer #5: Yes

**********

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

Reviewer #3: Yes

Reviewer #4: Yes

Reviewer #5: Yes

**********

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

Reviewer #3: Yes

Reviewer #4: Yes

Reviewer #5: Yes

**********

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

Reviewer #3: Yes

Reviewer #4: Yes

Reviewer #5: Yes

**********

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 #3: Yes: Glennis Andall-Brereton

Reviewer #4: Yes: Esmaeil Mohammadi, MD MPH

Reviewer #5: Yes: Mohammad Keykhaei

**********

6. Review Comments to the Author

Reviewer #4: I wanted to first thank the editorial board for the opportunity of reviewing this paper. It is a SRMA with title of ‘Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia: systematic review and meta-analysis'. It seems that the authors and prior reviewers have made a substantial effort to reach to this well-revised paper. The introduction has been designed accordingly to talk about the condition, gaps, and aims of project. Besides identification of abbreviations for their first appearance (e.g., IIEF-5), other parts of the methods was well organized based on the PICO. Based on the journal of preference, search string can be exported to the appendix. Table 1 needs abbreviations and explanations independent of main txt and all should be mentioned at footnote (e.g., SNNPR, ED...). I believe the first sentence of line 190 is not complete or it is just vague. Otherwise, the results sections are prepared well. The PRISMA chart is excrutiatingly messy and inconsistent. Please revise this part and unify numbers with the text. Authors have profoundly discussed their findings and have no comment on this part, though the conclusion can be further elaborate the need to understanding SD in NCD patients, so on so forth.

Reviewer #5: Dear Authors,

I read the manuscript entitled " Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia: systematic review and meta-analysis”. The paper is well written, and both the topic and data analysis are impressive, although attention to the following issues could improve the quality of the paper.

Minor comments

Introduction section:

1. Line 48, “of from” is not grammatically correct.

2. Line 49 “It” must be substituted with "NCDs".

3. Line 54, “Hypertension” should not be capitalized.

Methods:

1. The conducted search strategy is up to June 2020. This strategy should be updated.

2. In Figure 1, in the screening section, the authors have identified that 198 studies have been excluded. The exclusion might be due to some reasons including “review article”, “not relating to the subject” and etc. So, these reason with the numbers of articles in each exclusion section should be written in this fellow chart.

Discussion:

1. The authors should add additional paragraphs regarding the solutions for preventing or screening sexual dysfunction.

2. The authors have not discussed the reasons and potential solutions for sexual dysfunction in patients with diabetes. This part should be included.

PLoS One. 2021 Oct 28;16(10):e0258938. doi: 10.1371/journal.pone.0258938.r008

Author response to Decision Letter 3

22 Sep 2021

Dear Academic Editor!

PLOS ONE

Response to Reviewers

I am pleased to resubmit the revised version of "Estimate the burden of sexual dysfunction related to non-communicable disease in Ethiopia: systematic review and meta-analysis" to PLOS ONE for publication as original research.

The editor's and reviewers' comments were quite helpful, allowing us to significantly increase the quality of our article. As a result, we have made considerable revisions to our paper in accordance to the editor's and reviewers' comments.

Before submitting the revised version, the manuscript extensively edited by a professional language editor (English-language instructors of Debre Berhan University thoroughly edited the manuscript for language usage, spelling, and grammar). The text and document's formatting (text sizes and grammatical errors) were also edited. Your concerns have been addressed in a point-by-point approach.

We look forward to hearing from you at your earliest convenience.

Thank you for your consideration of this manuscript!

Kind regards,

Akine Eshete

On behalf of authors

Reviewer #4

Besides identification of abbreviations for their first appearance (e.g., IIEF-5)

Response: We thank you very much for this important recommendation. We edited it accordingly on line 91

Table 1 needs abbreviations and explanations independent of main txt and all should be mentioned at footnote (e.g., SNNPR, ED...).

Response: We thank you very much for this important recommendation. We edited it accordingly on line 170

I believe the first sentence of line 190 is not complete or it is just vague.

Response: We thank you very much for this important recommendation. We edited it accordingly on line 182.

The PRISMA chart is excruciatingly messy and inconsistent. Please revise this part and unify numbers with the text.

Response: We thank you very much for this important recommendation. We tried to modify based on the comments.

Reviewer #5

1. Line 48, “of from” is not grammatically correct.

Response: We thank you very much for this important recommendation. We edited it accordingly from line 47-48.

2. Line 49 “It” must be substituted with "NCDs".

Response: We thank you very much for this important recommendation. We edited it accordingly

3. Line 54, “Hypertension” should not be capitalized.

Response: We thank you very much for this important recommendation. We edited it accordingly on line 54

Methods:

1. The conducted search strategy is up to June 2020. This strategy should be updated.

Response: We thank you very much for this important recommendation. We edited it accordingly

Response: We thank you very much for this important recommendation. We edited it accordingly from line 157-158

Discussion:

1. The authors should add additional paragraphs regarding the solutions for preventing or screening sexual dysfunction.

Response: We thank you very much for this important recommendation. We edited it accordingly from line 285-310

2. The authors have not discussed the reasons and potential solutions for sexual dysfunction in patients with diabetes. This part should be included.

Response: We thank you very much for this important recommendation. We edited it accordingly from line 285-310

Attachment

Submitted filename: Response to reviewers.docx

Click here for additional data file.^{(17.1KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0258938.r009

Decision Letter 4

Sina Azadnajafabad

11 Oct 2021

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia : systematic review and meta-analysis

PONE-D-20-18974R4

Dear Dr. Akine Abosetugn Eshete,

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.

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,

Sina Azadnajafabad

Guest Editor

PLOS ONE

Additional Editor Comments (optional):

Dear Dr. Akine Abosetugn Eshete,

I am writing to you regarding the manuscript "Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia : systematic review and meta-analysis". As an act of transparency, I am invited to handle your paper as a guest academic editor for the second time, after multiple rounds of commenting and reviewing of your paper in the previous stages.

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Sina Azadnajafabad, MD MPH

PLoS One. doi: 10.1371/journal.pone.0258938.r010

Acceptance letter

Sina Azadnajafabad

19 Oct 2021

PONE-D-20-18974R4

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia: systematic review and meta-analysis

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Associated Data

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Supplementary Materials

S1 Table. JBI critical appraisal checklist for studies reporting prevalence data.

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Data Availability Statement

All relevant data are within the manuscript and its Supporting information files.

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PERMALINK

Estimate the burden of sexual dysfunction due to non-communicable diseases in Ethiopia: Systematic review and meta-analysis

Akine Eshete Abosetugn

Sisay Shewasinad Yehualashet

Roles

Abstract

Background

Methods

Result

Conclusion

Introduction

Methods

Study settings

Inclusion criteria

Type of studies

Study participants

Types of outcome measures (sexual dysfunction)

Exclusion criteria

Search strategy

Data extraction

Risk of bias

Data synthesis and statistical analysis

Data presentation and reporting of results

Results

Search results

Fig 1. The PRISMA flow diagram of identification and selection of studies for the systematic review and meta-analysis.

Characteristics of included studies

Table 1. Description of the included studies.

The burden of sexual dysfunction

Meta-analysis results

The estimate of sexual dysfunction

Fig 2. The pooled prevalence of sexual dysfunction in patients with non-communicable disease in Ethiopia.

Subgroup analysis

Table 2. Subgroup analysis by different category of the studies.

Meta-regression analysis

Table 3. Meta-regression analysis for the included studies to identify the source(s) of heterogeneity.

Sensitivity analysis

Fig 3. Plot of sensitivity analysis to assessing the influence of individual study.

Publication bias

Fig 4. Funnel plot of effect estimates against standard error of log estimate.

Fig 5. Result of trim and filled analysis for adjusting publication bias.

Discussion

Conclusion

Supporting information

Acknowledgments

Abbreviations

Data Availability

Funding Statement

References

Decision Letter 0

Claudia Marotta

Roles

Author response to Decision Letter 0

Decision Letter 1

Claudia Marotta

Roles

Author response to Decision Letter 1

Decision Letter 2

Vanessa Carels

Roles

Author response to Decision Letter 2

Decision Letter 3

Sina Azadnajafabad

Roles

Author response to Decision Letter 3

Decision Letter 4

Sina Azadnajafabad

Roles

Acceptance letter

Sina Azadnajafabad

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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