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Diagnosis and Management of Cystic Fibrosis

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A special issue of Diagnostics (ISSN 2075-4418). This special issue belongs to the section "Pathology and Molecular Diagnostics".

Deadline for manuscript submissions: closed (30 November 2020) | Viewed by 32695

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Prof. Dr. Giuseppe Castaldo

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Department of Molecular Medicine and Medical Biotechnology, Università degli Studi di Napoli Federico II, 80131 Naples, Italy
Interests: COVID-19; cystic fibrosis; metabolomics; haemophilia; inherited peripheral thrombosis; congenital diarrhea
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Cystic fibrosis (CF) is an autosomal recessive disease caused by mutations in the cystic fibrosis transmembrane regulator (CFTR) gene that encodes the CFTR membrane chloride channel. To date, about 2000 genetic variants have been reported, but the disease-liability of all these variants has been completed for 412 of the most common ones. The diagnosis of CF is supported by clinical symptoms, abnormal sweat chloride test, and by the identification of two CFTR disease-causing mutations. The use of next-generation sequencing (NGS) in molecular diagnostics has made incredible progress in identifying genetic variants with high accuracy and a significant cost reduction. However, the interpretation of genetic variations represents one of the limiting phases of NGS technologies, also because of the thousands of rare variants without pathogenic effects. Moreover, the advent of new drugs that can correct the basic defect of the CFTR protein is changing the fate of many patients, but not all. Indeed, new drugs, are currently available to patients with a specific subset of mutations. Although carrying the same mutation for which the drug was approved, not all patients respond to therapy. Therefore, despite the incredible advances, there is still much to do: from diagnosis to patient management, especially those with rare mutations not elected for current therapies.

In this Special Issue, we are looking for reviews and original articles to improve, disseminate, and homogenize the management of CF patients (and patients with CFTR-related disorders or CF-SPID) from diagnosis to therapeutic choice. Therefore, any contribution in the field of clinical and molecular diagnostics, in functional studies, and novel therapeutic approaches are welcome.

Prof. Dr. Giuseppe Castaldo
Guest Editor

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Keywords

Cystic fibrosis
CF-SPID
CFTR-related disorders
Newborn screening
Carrier screening
Personalized medicine
Molecular diagnosis
Prenatal diagnosis
Preimplantation diagnosis
Advanced sequencing technology
CF proteomics
CF metabolomics
CF microbiology (including microbiota)
Novel therapies (gene, cell, and molecular therapy)
Predictive markers of organ and tissue damage
CF inflammation
Genotype-phenotype correlation and modifier genes
Preclinical models (cell and tissue, organoids, animal models)

Published Papers (12 papers)

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Research

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12 pages, 273 KiB

Open AccessArticle

The Diagnosis of Cystic Fibrosis in Adult Age. Data from the Italian Registry

by Rita Padoan, Serena Quattrucci, Annalisa Amato, Vincenzo Carnovale, Donatello Salvatore, Marco Salvatore and Giuseppe Campagna

Diagnostics 2021, 11(2), 321; https://doi.org/10.3390/diagnostics11020321 - 16 Feb 2021

Cited by 6 | Viewed by 2887

Abstract

Cystic Fibrosis (CF) registries are an essential resource of epidemiological and clinical data. Although the median age at diagnosis is usually reported in the first months of life, a minority of individuals is diagnosed during adulthood. The aim of this study was to describe demographic, genetic, and clinical characteristics of this subgroup of the Italian CF population by using data from the Italian CF Registry (ICFR). Patients ≥18 years at diagnosis were selected and clinical data at diagnosis were analyzed from the 2012–2018 ICFR data (Cohort A). Subjects with diagnosis ≥18 years were selected from 2018 ICFR dataset (Cohort B) to describe their clinical status. In 2012–18 the incidence of late diagnosis was 18.2%, whereas, in 2018, the prevalence of patients diagnosed ≥18 years was 12.54%. The median age of late diagnosis was 36.2 years, ranging from 19.0 to 68.3. The male patients were diagnosed because of infertility in the 45.9% of cases. Median sweat chloride value (SCL) was 69 mmol/L (range 9–150). F508del mutation accounted for 28.3% of alleles. A wide variability in respiratory function was present with a median percent predicted Forced Expiratory Volume in the first second (ppFEV₁) of 90.8% (range 20–147%). Low prevalence of pancreatic insufficiency (25%) and of Pseudomonas aeruginosa (Pa) infection (17%) suggest a mild CF phenotype in the majority of patients. The assessment of the clinical status in the 2018 dataset and the comparison between genders showed a greater nutritional and respiratory impairment in females. Further studies are needed to clarify the importance of a true diagnostic delay or of late onset of CF symptoms. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

11 pages, 4840 KiB

Open AccessArticle

Quantitative Evaluation of CFTR Pre-mRNA Splicing Dependent on the (TG)mTn Poly-Variant Tract

by Manuela Sterrantino, Andrea Fuso, Silvia Pierandrei, Sabina Maria Bruno, Giancarlo Testino, Giuseppe Cimino, Antonio Angeloni and Marco Lucarelli

Diagnostics 2021, 11(2), 168; https://doi.org/10.3390/diagnostics11020168 - 25 Jan 2021

Cited by 5 | Viewed by 2182

Abstract

Genetic analysis in cystic fibrosis (CF) is a difficult task. Within the many causes of variability and uncertainty, a major determinant is poor knowledge of the functional effect of most DNA variants of the Cystic Fibrosis Transmembrane conductance Regulator (CFTR) gene. In turn, knowledge of the effect of a CFTR variant has dramatic diagnostic, prognostic and, in the era of CF precision medicine, also therapeutic consequences. One of the most challenging CFTR variants is the (TG)mTn haplotype, which has variable functional effect and controversial clinical consequences. The exact quantification of the anomalous splicing of CFTR exon 10 (in the HGVS name; exon 9 in the legacy name) and, consequently, of the residual wild-type functional CFTR mRNA, should be mandatory in clinical assessment of patients with potentially pathological haplotype of this tract. Here, we present a real time-based assay for the quantification of the proportion of exon 10+/exon 10− CFTR mRNA, starting from nasal brushing. Our assay proved rapid, economic and easy to perform. Specific primers used for this assay are either disclosed or commercially available, allowing any laboratory to easily perform it. A simplified analysis of the data is provided, facilitating the interpretation of the results. This method helps to enhance the comprehension of the genotype–phenotype relationship in CF and CFTR-related disorders (CFTR-RD), crucial for the diagnosis, prognosis and personalized therapy of CF. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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9 pages, 720 KiB

Open AccessArticle

CRMS/CFSPID Subjects Carrying D1152H CFTR Variant: Can the Second Variant Be a Predictor of Disease Development?

by Vito Terlizzi, Rita Padoan, Laura Claut, Carla Colombo, Benedetta Fabrizzi, Marco Lucarelli, Sabina Maria Bruno, Alice Castaldo, Paolo Bonomi, Giovanni Taccetti and Antonella Tosco

Diagnostics 2020, 10(12), 1080; https://doi.org/10.3390/diagnostics10121080 - 12 Dec 2020

Cited by 18 | Viewed by 1788

Abstract

Background: There are no predictive factors of evolution of cystic fibrosis (CF) screen positive inconclusive diagnosis subjects (CFSPIDs). Aim: to define the role of the second CFTR variant as a predictive factor of disease evolution in CFSPIDs carrying the D1152H variant. Methods: We retrospectively evaluated clinical characteristics and outcome of CFSPIDs carrying the D1152H variant followed at five Italian CF centers. CFSPIDs were divided in two groups: Group A: compound heterozygous for D1152H and a CF-causing variant; Group B: compound heterozygous for D1152H and a: (i) non CF-causing variant, (ii) variant with varying clinical consequences, or (iii) variant with unknown significance. The variants were classified according to CFTR2 mutation database. Results: We enrolled 43 CFSPIDs with at least one D1152H variant: 28 (65.1%) were classified in the group A, and 15 (34.9%) in the Group B. CFSPIDs of group A had the first IRT significantly higher compared to those of group B (p < 0.05) and had a more severe clinical outcome during the follow-up. At the end of the study period, after a mean follow-up of 40.6 months (range 6–91.6), 4 (9.3%) out of 43 CFSPIDs progressed to CFTR-RD or CF. All these subjects were in the group A. Conclusions: The genetic profile could help predict the risk of disease evolution in CFSPIDs carrying D1152H, revealing the subjects that need a more frequent follow-up. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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10 pages, 763 KiB

Open AccessArticle

Impaired Ratio of Unsaturated to Saturated Non-Esterified Fatty Acids in Saliva from Patients with Cystic Fibrosis

by Monica Gelzo, Paola Iacotucci, Vincenzo Carnovale, Alice Castaldo, Marika Comegna, Gustavo Cernera, Gaetano Corso and Giuseppe Castaldo

Diagnostics 2020, 10(11), 915; https://doi.org/10.3390/diagnostics10110915 - 08 Nov 2020

Cited by 3 | Viewed by 1619

Abstract

Impaired salivary non-esterified fatty acids (NEFA) levels have been previously observed in cystic fibrosis (CF). This study aimed to characterize the salivary NEFA profile in CF and to examine whether the alterations are related to the pancreatic status and/or lung disease severity. We analyzed salivary NEFA, cholesterol and interleukin-6 (IL-6) in CF patients (n = 66) and healthy subjects (n = 48). CF patients showed higher salivary levels of cholesterol, total NEFA (that was negatively correlated with serum triglycerides), unsaturated NEFA/saturated NEFA (U/S NEFA) ratio and IL-6 than controls. The U/S NEFA ratio was positively correlated with IL-6 in both patients and controls, suggesting an association between this parameter and local inflammation independently from the disease. No correlation between salivary lipids and pancreatic status was observed, while the U/S NEFA ratio was higher in patients with severe lung disease than mild/moderate severity and may represent a prognostic marker of lung disease in CF. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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11 pages, 612 KiB

Open AccessArticle

Cystic Fibrosis-Screening Positive Inconclusive Diagnosis: Newborn Screening and Long-Term Follow-Up Permits to Early Identify Patients with CFTR-Related Disorders

by Alice Castaldo, Chiara Cimbalo, Raimondo J. Castaldo, Marcella D’Antonio, Manuela Scorza, Laura Salvadori, Angela Sepe, Valeria Raia and Antonella Tosco

Diagnostics 2020, 10(8), 570; https://doi.org/10.3390/diagnostics10080570 - 08 Aug 2020

Cited by 18 | Viewed by 2623

Abstract

Background: Newborn screening (NBS) early-identifies cystic fibrosis (CF), but in CF-screening positive inconclusive diagnosis (CF-SPID) the results of immunoreactive trypsinogen (IRT), molecular analysis and sweat test (ST) are discordant. A percentage of CF-SPID evolves to CF, but data on long-term monitoring are lacking. We describe the follow-up of all CF and CF-SPID identified between 2008 and 2019. Methods: NBS was performed by IRT followed by molecular analysis and ST between 2008 and 2014; double IRT followed by molecular analysis and ST after 2014. Results: NBS revealed 47 CF and 99 CF-SPID newborn, a ratio 1:2.1—the highest reported so far. This depends on the identification by gene sequencing of the second variant with undefined effect in 40 CF-SPID that otherwise would have been defined as carriers. Clinical complications and pulmonary infections occurred more frequently among CF patients than among CF-SPID. Two CF-SPID cases evolved to CF (at two years), while eight evolved to CFTR-related disorders (CFTR-RD), between one and eight years, with bronchiectasis (two), recurrent pneumonia (four, two with sinonasal complications), recurrent pancreatitis (two). No clinical, biochemical or imaging data predicted the evolution. Conclusion: Gene sequencing within the NBS reveals a higher number of CF-SPID and we first describe an approach to early identify CFTR-RD, with relevant impact on their outcome. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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10 pages, 542 KiB

Open AccessArticle

Clinical and Genotypical Features of False-Negative Patients in 26 Years of Cystic Fibrosis Neonatal Screening in Tuscany, Italy

by Giovanni Taccetti, Matteo Botti, Vito Terlizzi, Maria Chiara Cavicchi, Anna Silvia Neri, Valeria Galici, Gianfranco Mergni, Claudia Centrone, Diego G. Peroni and Filippo Festini

Diagnostics 2020, 10(7), 446; https://doi.org/10.3390/diagnostics10070446 - 01 Jul 2020

Cited by 22 | Viewed by 2726

Abstract

Cystic fibrosis (CF) is a life-threatening and common genetic disorder. Cystic fibrosis newborn screening (CF NBS) has been implemented in many countries over the last 30 years, becoming a widely accepted public health strategy in economically developed countries. False-negative (FN) cases can occur after CF NBS, with the number depending on the method. We evaluated the delayed diagnosis of CF, identifying the patients who had false-negative CF NBS results over 26 years (1992–2018) in Tuscany, Italy. The introduction of DNA analysis to the newborn screening protocol improved the sensitivity of the test and reduced the FNs. Our experience showed that, overall, at least 8.7% of cases of CF received FNs (18 cases) and were diagnosed later, with an average age of 6.6 years (range: 4 months to 22 years). Respiratory symptoms and salt-loss syndrome (metabolic hypochloremic alkalosis) are suggestive symptoms of CF and were commons events in FN patients. In Tuscany, a region with a high CFTR allelic heterogeneity, the salt-loss syndrome was a common event in FNs. Therefore, we provided evidence to support the claim that the FN patients had CFTR mutations rarer compared with the true-positive cases. We underline the importance of vigilance toward clinical manifestations suggestive of CF on the part of the primary care providers and hospital physicians in a region with an efficient newborn screening program. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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9 pages, 414 KiB

Open AccessArticle

Salivary Cytokines and Airways Disease Severity in Patients with Cystic Fibrosis

by Alice Castaldo, Paola Iacotucci, Vincenzo Carnovale, Roberta Cimino, Renato Liguori, Marika Comegna, Valeria Raia, Gaetano Corso, Giuseppe Castaldo and Monica Gelzo

Diagnostics 2020, 10(4), 222; https://doi.org/10.3390/diagnostics10040222 - 15 Apr 2020

Cited by 12 | Viewed by 2451

Abstract

About 50% of patients with cystic fibrosis (CF) have sinonasal complications, which include inferior turbinate hypertrophy (NTH) and/or nasal polyposis (NP), and different degrees of lung disease, which represents the main cause of mortality. Monitoring of sinonasal disease requires complex instrumental procedures, while monitoring of lung inflammation requires invasive collection of bronchoalveolar lavage fluid. The aim of this study was to investigate the associations between salivary cytokines levels and CF-related airway diseases. Salivary biochemical parameters and cytokines, i.e., interleukin-6 (IL-6), IL-8, and tumor necrosis factor alpha (TNF-α), were analyzed in resting saliva from healthy subjects and patients with CF. Patients with CF showed significantly higher levels of salivary chloride, IL-6, IL-8, and TNF-α and lower calcium levels than healthy subjects. Among patients with CF, IL-6 and IL-8 were significantly higher in patients with NTH, while TNF-α was significantly lower in patients with NP. A decreasing trend of TNF-α in patients with severe lung disease was also observed. On the other hand, we did not find significant correlation between cytokine levels and Pseudomonas aeruginosa or Stenotrophomonas maltophilia colonization. These preliminary results suggest that salivary IL-6 and IL-8 levels increase during the acute phase of sinonasal disease (i.e., NTH), while the end stages of pulmonary disease and sinonasal disease (i.e., NP) show decreased TNF-α levels. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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Review

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16 pages, 757 KiB

Open AccessReview

Cystic Fibrosis-Related Diabetes (CFRD): Overview of Associated Genetic Factors

by Fernanda Iafusco, Giovanna Maione, Francesco Maria Rosanio, Enza Mozzillo, Adriana Franzese and Nadia Tinto

Diagnostics 2021, 11(3), 572; https://doi.org/10.3390/diagnostics11030572 - 22 Mar 2021

Cited by 15 | Viewed by 4492

Abstract

Cystic fibrosis (CF) is the most common autosomal recessive disease in the Caucasian population and is caused by mutations in the CF transmembrane conductance regulator (CFTR) gene that encodes for a chloride/bicarbonate channel expressed on the membrane of epithelial cells of the airways and of the intestine, as well as in cells with exocrine and endocrine functions. A common nonpulmonary complication of CF is cystic fibrosis-related diabetes (CFRD), a distinct form of diabetes due to insulin insufficiency or malfunction secondary to destruction/derangement of pancreatic betacells, as well as to other factors that affect their function. The prevalence of CFRD increases with age, and 40–50% of CF adults develop the disease. Several proposed hypotheses on how CFRD develops have emerged, including exocrine-driven fibrosis and destruction of the entire pancreas, as well as contrasting theories on the direct or indirect impact of CFTR mutation on islet function. Among contributors to the development of CFRD, in addition to CFTR genotype, there are other genetic factors related and not related to type 2 diabetes. This review presents an overview of the current understanding on genetic factors associated with glucose metabolism abnormalities in CF. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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19 pages, 959 KiB

Open AccessReview

The Multifaceted Roles of MicroRNAs in Cystic Fibrosis

by Fatima Domenica Elisa De Palma, Valeria Raia, Guido Kroemer and Maria Chiara Maiuri

Diagnostics 2020, 10(12), 1102; https://doi.org/10.3390/diagnostics10121102 - 17 Dec 2020

Cited by 12 | Viewed by 3667

Abstract

Cystic fibrosis (CF) is a lifelong disorder affecting 1 in 3500 live births worldwide. It is a monogenetic autosomal recessive disease caused by loss-of-function mutations in the gene encoding the chloride channel cystic fibrosis transmembrane conductance regulator (CFTR), the impairment of which leads to ionic disequilibria in exocrine organs. This translates into a chronic multisystemic disease characterized by airway obstruction, respiratory infections, and pancreatic insufficiency as well as hepatobiliary and gastrointestinal dysfunction. Molecular characterization of the mutational heterogeneity of CFTR (affected by more than 2000 variants) improved the understanding and management of CF. However, these CFTR variants are linked to different clinical manifestations and phenotypes, and they affect response to treatments. Expanding evidence suggests that multisystemic disease affects CF pathology via impairing either CFTR or proteins regulated by CFTR. Thus, altering the expression of miRNAs in vivo could constitute an appealing strategy for developing new CF therapies. In this review, we will first describe the pathophysiology and clinical management of CF. Then, we will summarize the current knowledge on altered miRNAs in CF patients, with a focus on the miRNAs involved in the deregulation of CFTR and in the modulation of inflammation. We will highlight recent findings on the potential utility of measuring circulating miRNAs in CF as diagnostic, prognostic, and predictive biomarkers. Finally, we will provide an overview on potential miRNA-based therapeutic approaches. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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13 pages, 602 KiB

Open AccessReview

Impact of Physical Activity on Cognitive Functions: A New Field for Research and Management of Cystic Fibrosis

by Valentina Elce, Alessandro Del Pizzo, Ersilia Nigro, Giulia Frisso, Lucia Martiniello, Aurora Daniele and Ausilia Elce

Diagnostics 2020, 10(7), 489; https://doi.org/10.3390/diagnostics10070489 - 18 Jul 2020

Cited by 9 | Viewed by 4222

Abstract

Cystic Fibrosis (CF) is a genetic disease inherited by an autosomal recessive mechanism and characterized by a progressive and severe multi-organ failure. Mutations in Cystic Fibrosis Conductance Regulator (CFTR) protein cause duct obstructions from dense mucus secretions and chronic inflammation related to organ damage. The progression of the disease is characterized by a decline of lung function associated with metabolic disorders and malnutrition, musculoskeletal disorders and thoracic deformities, leading to a progressive decrement of the individual’s quality of life. The World Health Organization (WHO) qualifies Physical Activity (PA) as a structured activity produced by skeletal muscles’ movements that requires energy consumption. In the last decade, the number of studies on PA increased considerably, including those investigating the effects of exercise on cognitive and brain health and mental performance. PA is recommended in CF management guidelines, since it improves clinic outcomes, such as peripheral neuropathy, oxygen uptake peak, bone health, glycemic control and respiratory functions. Several studies regarding the positive effects of exercise in patients with Cystic Fibrosis were carried out, but the link between the effects of exercise and cognitive and brain health in CF remains unclear. Animal models showed that exercise might improve learning and memory through structural changes of brain architecture, and such a causal relationship can also be described in humans. Indeed, both morphological and environmental factors seem to be involved in exercise-induced neural plasticity. An increase of gray matter volume in specific areas is detectable as a consequence of regular training in humans. Neurobiological processes associated with brain function improvements include biochemical modifications, such as neuromodulator or neurohormone release, brain-derived neurotrophic factor (BDNF) production and synaptic activity changes. From a functional point of view, PA also seems to be an environmental factor enhancing cognitive abilities, such as executive functions, memory and processing speed. This review describes the current state of research regarding the impacts of physical activity and exercise on cognitive functions, introducing a possible novel field of research for optimizing the management of Cystic Fibrosis. Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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Other

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1 pages, 164 KiB

Open AccessReply

Reply to Gambazza et al. Cystic Fibrosis, New Frontier: Exploring the Functional Connectivity of the Brain Default Mode Network. Comment on “Elce et al. Impact of Physical Activity on Cognitive Functions: A New Field for Research and Management of Cystic Fibrosis. Diagnostics 2020, 10, 489”

by Ausilia Elce, Valentina Elce and Alessandro Del Pizzo

Diagnostics 2021, 11(6), 1002; https://doi.org/10.3390/diagnostics11061002 - 31 May 2021

Viewed by 1119

Abstract

We appreciate the interest in our review and we are grateful for the comment by Gambazza S. [...] Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

4 pages, 707 KiB

Open AccessComment

Cystic Fibrosis, New Frontier: Exploring the Functional Connectivity of the Brain Default Mode Network. Comment on Elce et al. Impact of Physical Activity on Cognitive Functions: A New Field for Research and Management of Cystic Fibrosis. Diagnostics 2020, 10, 489

by Simone Gambazza, Rita Maria Nobili, Riccardo Biffi, Paul Eugene Summers, Carla Colombo and Antonella Costa

Diagnostics 2021, 11(6), 1001; https://doi.org/10.3390/diagnostics11061001 - 31 May 2021

Cited by 1 | Viewed by 1897

Abstract

We read with great interest the paper entitled “Impact of physical activity of cognitive functions: a new field for research and management of Cystic Fibrosis” by Elce et al. [...] Full article

(This article belongs to the Special Issue Diagnosis and Management of Cystic Fibrosis)

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