Basic revised clinical, etiologic, anatomic, and pathophysiologic (CEAP) classification system.
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\r\n\tThe aims of this book are to present the updates and advances in the field of resuscitation including AHA guidelines, latest evidence for the airway protection equipment, the role of AED in cardiac arrest, latest advances and the evidence including ongoing updated research including return of spontaneous circulation and post resuscitation care and support including neurological and hemodynamic stability.
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\r\n\tThe content of this book will be focused on latest research in the field which will create a concise updated information for medical, nursing and paramedical personnel. Furthermore, the book will also touch upon controversial topics in resuscitation and will try to bring out latest evidence intending to solve the controversies in the field of resuscitation. This book will be an excellent extract of all available updates and ongoing research for a complete knowledge of resuscitation.
Venous ulcers are the most common form of leg ulcers and important medical problem, which causes significant morbidity and economic burden. Clinical findings and history are helpful in making the diagnosis, but additional diagnostic testing is helpful in confirming the diagnosis and excluding other causes of leg ulcerations. The main purpose of venous ulcer management includes healing of the ulcer and prevention of recurrence. This chapter highlights the epidemiology, pathophysiology, clinical presentation, diagnostic testing, differential diagnosis, and treatment of venous ulcers.
\nVenous leg ulcers (VLUs) are the most common lower extremity ulceration and responsible for 70% of all leg ulcers, with overall prevalence ranging from 0.06 to 2% [1–4]. It occurs frequently between the ages of 60 and 80 years; however, most people have their first ulcer before the age of 60 years [5, 6]. VLUs have slight female predominance, with a female‐to‐male ratio ranging from 1.5:1 to 10:1 [7, 8].
\nVenous ulcers have a significant socioeconomic impact with reduced work productivity and quality of life. Long‐term treatments are needed and recurrence is widely common, ranging from 54 to 78% of treated subjects [9]. The overall cost of VLU treatments was 1–2% of the healthcare budgets of European countries [10]. In the United States, approximately 2.5 billion dollars was expended for the treatment of VLUs per year [11].
\nAdvancing age, sex, race, phlebitis, family history, obesity, occupation involving prolonged standing, and number of pregnancies are risk factors that have been described with chronic venous insufficiency and, subsequently, with venous ulcers [12, 13].
\nThe venous system of the lower extremities includes the superficial veins, perforator veins, and the deep veins according to their relationship to the muscular fascia. The superficial veins comprises the reticular veins, the large (larger) and small (smaller) saphenous veins, and their tributaries. The great saphenous vein originates from where the dorsal vein of the first digit merges with the dorsal venous arch of the foot. After passing in front of the medial malleolus, it ascends the medial side of the leg. It joins the femoral vein just below the inguinal ligament. The small saphenous vein arises from the dorsal venous arch of the foot and ascends posterolaterally from behind the lateral malleolus. Usually, it drains into the popliteal vein near the popliteal fossa. The reticular veins, a network of veins parallel to the skin surface, communicate with either saphenous tributaries or the deep veins through perforators. The perforator veins connect the superficial and deep vein systems. The deep venous system is categorized as either intramuscular or intermuscular. Intermuscular veins are three paired tibial veins including, the posterior tibial vein, the anterior tibial vein, and the peroneal vein. These veins join to form the popliteal vein in the popliteal area. At the level of the adductor canal, the popliteal vein is renamed the superficial femoral vein. This vessel joins the deep femoral vein in the femoral triangle to form the common femoral vein. After passing beneath the inguinal ligament to enter the pelvis, the femoral vein is renamed the common iliac vein. The superficial veins are low‐pressure systems, whereas the deep veins are high‐pressure systems. All three venous systems have one‐way bicuspid valves, which only open toward the deep venous system and, under normal conditions, prevent reflux of blood. Normally, ambulation and the pumping action of the calf muscles propel venous blood upward toward the heart, and the valves close when pressure rises in the deep venous system, which prevents retrograde flow [4, 14, 15].
\nIn patients with venous disease or failure, venous pressure in deep system falls less than normal during ambulation and rises in orthostatic position, and this is termed venous hypertension. In conclusion, venous hypertension in the deep veins may be transmitted to the superficial veins [4, 16]. There is no general consensus about the transition from venous hypertension to venous ulceration. Several hypotheses have been proposed.
\nAccording to this theory of Browse and Burnand [17], venous hypertension leads to distention of capillary walls and leakage of macromolecules such as fibrinogen into the dermis and subcutaneous tissues of the calf. The leaked fibrinogen polymerizes to form precapillary fibrin cuffs in the extravascular space. These precapillary cuffs were assumed to act as a physical barrier, which impede the diffusion of oxygen and nutrients, resulting in ischemia, cell death, and ulceration [17–19]. In addition, local and systemic fibrinolytic/coagulation abnormalities such as prolonged euglobulin lysis time, elevated plasma fibrinogen levels, increased levels of protein C, fibrin‐related antigens, D‐dimer, D‐monomer, fibrin monomer, and reduction in factor XIII activity may present in patients with venous disease [20–22]. However, it is unclear whether these abnormalities are primary or secondary to venous disease.
\nAs a result of venous hypertension, there is a decreased pressure in capillary bed perfusion and capillary flux. This gives rise to erythrocyte aggregation and leukocyte plugging in the capillaries, leading to local ischemia. Moreover, these leukocytes release cytokines, tumor necrosis factor α (TNF‐α), proteolytic enzymes, and free radicals which can cause increased vascular permeability resulting in the leakage of fibrinogen into the pericapillary tissues and the decreased fibrinolytic activity [23–25].
\nFalanga and Eaglstein [26] recommended that macromolecules such as fibrinogen and α2macroglobulin, which leak into the dermis as a result of venous hypertension, bind to or trap growth factors, which then become unavailable for the maintenance of tissue integrity and repair process. The precapillary fibrin cuff of the venous ulcer contains growth factors such as transforming growth factor β (TGF‐β). Trapping of growth factors can impair activation of the cells that are needed for healing process [27].
\nIn general, the venous ulcer is an irregularly, well‐defined border and typically non‐painful [4, 8]. Nevertheless, deep ulcers or small venous ulcers surrounded by atrophie blanche are highly painful [28]. The size and site of ulcers are variable, but they usually located over the medial malleolus (Figure 1).
\nTypical venous ulcer over the medial malleolus.
There may be yellow fibrinous exudates on the ulcer bed. Varicose veins and ankle edema are common. The surrounding skin is erythematous or hyperpigmented with variable degrees of induration. Eczematous changes associated with venous dermatitis are commonly present. Long‐standing venous disease can lead to loss of the subcutaneous fat and fibrotic changes in the skin called lipodermatosclerosis, giving the characteristic “inverted champagne‐bottle” appearance of the leg [29]. The main complications of chronic venous ulcers are osteomyelitis and neoplastic transformation [4, 30]. Long‐term ulcers may require biopsy at regular intervals for malignant change. If osteomyelitis is suspected, radiography, bone scanning, and bone biopsy should be considered.
\nThe diagnosis of venous ulcers is mainly based on patient history and clinical examination; however, there are diagnostic tests to evaluate venous anatomy and aid the diagnosis.
\nDuplex ultrasound is the first‐line diagnostic test to evaluate the insufficiency in venous ulcers [31]. Continuous‐wave Doppler provides information about superficial venous incompetence or obstruction; nonetheless, it can be difficult to differentiate deep from superficial venous incompetence [32, 33].
\nPhotoplethysmography and air plethysmography measure the degree of venous reflux and the calf muscle pump efficiency [8, 34, 35].
\nIn case of suspected venous obstruction, additional contrast imaging with computed tomography venography or magnetic resonance venography should be done; whereupon diagnosis should be confirmed by contrast venography and intravascular ultrasound [31].
\nPatients who have a history of venous thrombosis and thrombophilia should undergo a workup for inherited hypercoagulable factors including protein C and S, factor V Leiden, antiphospholipid antibodies, prothrombin gene mutation, homocysteine, cryoglobulins, and cryoagglutinins [8, 31].
\nPatients with venous leg ulcers may have concomitant peripheral arterial disease component. Therefore, arterial pulse examination, Doppler ultrasound and ABI should be evaluated for the elimination of coexistent arterial disease. ABI is the ratio of the systolic blood pressure at the ankle compared with the systolic blood pressure in the arm. An ABI in the range of 0.9–1.1 is considered normal and 0.5–0.8 indicates moderate peripheral vascular disease and claudication, while less than 0.5 indicates more severe disease [4, 8, 36].
\nMost studies suggest wound biopsy for those that do not improve with standard wound and compression therapy after a period of 4–6 weeks of treatment. The biopsy specimen should be obtained from several sites, including the wound edge and central provisional matrix [31].
\nClassification of venous ulcers, known as CEAP [clinical findings (C), etiology (E), anatomical distribution (A), and pathophysiology (P)] based on clinical findings was introduced in 1994 and revised in 2004 [37, 38] (Table 1).
\nCEAP | \nDefinition | \n
---|---|
Clinical classification | \n\n |
C0 | \nNo visible or palpable signs of venous disease | \n
C1 | \nTelangiectasies or reticular veins | \n
C2 | \nVaricose veins | \n
C3 | \nEdema | \n
C4a | \nPigmentation and/or eczema | \n
C4b | \nLipodermatosclerosis and/or atrophie blanche | \n
C5 | \nHealed venous ulcer | \n
C6 | \nActive venous ulcer | \n
CS | \nSymptoms, including ache, pain, tightness, skin irritation, heaviness, muscle cramps, as well as other complaints attributable to venous dysfunction | \n
CA | \nAsymptomatic | \n
Etiologic classification | \n\n |
Ec | \nCongenital | \n
Ep | \nPrimary | \n
Es | \nSecondary (post‐thrombotic) | \n
En | \nNo venous etiology identified | \n
Anatomic classification | \n\n |
As | \nSuperficial veins | \n
Ap | \nPerforator veins | \n
Ad | \nDeep veins | \n
An | \nNo venous location identified | \n
Pathophysiologic classification (basic) | \n\n |
Pr | \nReflux | \n
Po | \nObstruction | \n
Pr,o | \nReflux and obstruction | \n
Pn | \nNo venous pathophysiology identifiable | \n
Basic revised clinical, etiologic, anatomic, and pathophysiologic (CEAP) classification system.
Modified from Eklöf et al. [38].
The clinical findings are divided into six categories, where C0indicates no visible or palpable signs of venous disease; C1, the presence of telangiectasies or reticular veins; C2, varicose veins; C3, edema; C4, changes in skin and subcutaneous tissue secondary to venous disease (C4a, pigmentation or eczema; C4b, lipodermatosclerosis or atrophie blanche); C5, skin changes with healed venous ulcer; C6, active venous ulcer. Each clinical class is further supplemented by (A) for asymptomatic and (S) for symptomatic presentation. Symptoms include aching, pain, skin irritation, tightness, heaviness, muscle cramps, and other complaints. The etiologic classification is separated into three categories; Ec, congenital; Ep, primary; Es, secondary (post‐traumatic or post‐thrombotic); and En, no venous cause identified. The anatomical classification is divided into four categories: As, superficial veins; Ap, perforator veins; Ad, deep veins; and An, no venous location identified. The pathophysiologic classification is divided into four categories; Pr, reflux; Po, obstruction; Pr,o, combination of reflux and obstruction; and Pn, no venous pathophysiology identifiable.
\nThe venous clinical severity score (VCSS) was developed because of subjective and inadequate definition of the categories in CEAP classification (Table 2).
\n\n | None: 0 | \nMild: 1 | \nModerate: 2 | \nSevere: 3 | \n
---|---|---|---|---|
Pain or other discomfort (i.e., aching, heaviness, fatigue, soreness, burning) | \n\n | Occasional pain or other discomfort (i.e., not restricting regular daily activities) | \nDaily pain or other discomfort (i.e., interfering with but not preventing regular daily activities) | \nDaily pain or discomfort (i.e., limits most regular daily activities) | \n
Presumes venous origin Varicose veins “Varicose” veins must be ≥3 mm in diameter to qualify in the standing position | \n\n | Few: scattered (i.e., isolated branch varicosities or clusters) Also induces corona phlebectatica (ankle flare) | \nConfined to calf or thigh | \nInvolves calf and thigh | \n
Venous edema Presumes venous origin | \n\n | Limited to foot and ankle area | \nExtends above ankle but below knee | \nExtends to knee and above | \n
Skin pigmentation Presumes venous origin | \nNone or focal | \nLimited to perimalleolar area | \nDiffuse over lower third of calf | \nWider distribution above lower third of calf | \n
Does not include focal pigmentation over varicose veins or pigmentation due to other chronic diseases | \n\n | \n | \n | \n |
Inflammation More than just recent pigmentation (i.e., erythema, cellulitis, venous eczema, dermatitis) | \n\n | Limited to perimalleolar area | \nDiffuse over lower third of calf | \nWider distribution above lower third of calf | \n
Induration Presumes venous origin of secondary skin and subcutaneous changes (i.e., chronic edema with fibrosis, hypodermitis) Includes white atrophy and lipodermatosclerosis | \n\n | Limited to perimalleolar area | \nDiffuse over lower third of calf | \nWider distribution above lower third of calf | \n
Active ulcer number | \n0 | \n1 | \n2 | \n≥3 | \n
Active ulcer duration (longest active) | \nN/A | \n<3 months | \n>3 months but <1 year | \nNot healed for <1 year | \n
Active ulcer size (largest active) | \nN/A | \nDiameter >2 cm | \nDiameter 2–6 cm | \nDiameter >6 cm | \n
Use of compression therapy | \n0 Not used | \n1 Intermittent use of stockings | \n2 Wears stockings most days | \n3 Full compliance: stockings | \n
Revised venous clinical severity score (VCSS) system.
Modified from Vasquez MA, Rabe E, McLafferty RB, Shortell CK, Marston WA, Gillespie D, et al. Revision of the venous clinical severity score: venous outcomes consensus statement: special communication of the American Venous Forum Ad Hoc Outcomes Working Group. J Vasc Surg 2010;52:1387–96.
A VCSS may range from 0 to 30 [31, 33, 39]. A score of more than eight indicates the progression of venous problem. In addition, the VCSS has been shown to be useful to evaluate the response to treatment.
\nArterial leg ulcers result from peripheral arterial occlusive disease. Arterial ulcers typically are round or punched out with a sharply demarcated border and extremely painful. A fibrous yellow base or necrotic eschar is commonly seen (Figure 2).
\nArterial ulcer.
The surrounding skin is cool to the touch. These ulcers frequently occur at the tips of the toes and over the bony prominences. Associated findings are weak or nonexistent arteria dorsalis pedis pulse, hair loss, atrophic skin, dystrophic nails, the presence of claudication, or rest pain. The ABI of 0.5 or less indicates severe arterial disease [4, 40, 41].
\nNeuropathic ulcers are more common in patients with diabetes mellitus (DM). Trauma and/or pressures can cause wounding and ulcer formation in patients with neuropathy [41–43]. These ulcers usually tend to be on the plantar surface of the foot. An abnormal, thickened callus develops at pressure areas, with ultimate disrupt of the tissue resulting in ulcer formation (Figure 3).
\nDiabetic neuropathic foot ulcer.
Pressure ulcers mostly occur in patients with limited mobility. These ulcers can start to develop when soft tissue is compressed for a prolonged period of time. The main risky sites are the heel of the foot, malleoli, and sacral and trochanter areas [4, 44].
\nHypertensive leg ulcers are extremely painful and commonly located on the distal portion of the lower leg above the lateral malleolus. These ulcers are seen in patients with prolonged, severe, or poorly controlled hypertension [41, 42]. The ulceration is secondary to tissue ischemia caused by increased vascular resistance.
\nPatients with mixed etiology ulcers have combined venous and arterial disease. Often further complicating factors such as DM, rheumatoid arthritis (RA), or lymphedema also exist [42].
\nPyoderma gangrenosum is a neutrophilic dermatosis. Clinically it starts with sterile pustules that rapidly progress and turn into painful ulcers with purplish‐blue, undermined borders [42, 45]. It may be associated with inflammatory bowel disease, rheumatic, or myeloproliferative disorders [8, 12] (Figure 4).
\nPyoderma gangrenosum.
Livedoid vasculopathy and tiny ulcerations.
Cutaneous vasculitis may present as palpable purpura, urticaria, nodule, bullae, livedo reticularis, necrotic areas, or skin ulceration. Vasculitic leg ulcers are often painful, multilocular and, surrounded by livid erythema and purpura (Figure 5). The different types of vasculitis that can cause cutaneous ulceration include small vessel vasculitis such as leukocytoclastic vasculitis, medium‐sized vessel vasculitis such as polyarteritis nodosa, microscopic polyangiitis, and Wegener granulomatosis [41, 46]. Routine blood work, sedimentation, antineutrophil cytoplasmic antibody (ANCA), urinalysis, chest X‐ray, and multiple skin biopsies should be done.
\nLivedoid vasculopathy (LV) is characterized by irregularly shaped, recurrent perimalleolar painful ulcers overlying areas of purpura. LV typically has three phases including livedo racemosa, ulcerations, and atrophie blanche [41, 42] (Figure 5).
\nApproximately 10% of individuals with RA develop leg ulcers [41] (Figure 6). The cause of leg ulcerations in RA is multifactorial, including vasculitis, venous insufficiency, paraproteinemias, medications, superficial ulcerating rheumatoid necrobiosis, pyoderma gangrenosum, and Felty\'s syndrome [45–48](Figure 6).
\nRheumatoid ulcer.
The prevalence of lower extremity ulcers in scleroderma is 3.6% and various parts of the leg can be affected [49]. These ulcers are painful and relatively refractory to standard treatment methods. Antiphospholipid antibody, fibrotic skin, vascular compromise, coagulation abnormalities, and tissue calcium deposition may have a role in their pathogenesis [45, 46, 48].
\nLeg ulcers of SLE are usually painful, sharply marginated, or punched out that located over the malleolar, supramalleolar, or pretibial areas [50]. Vasculitis, antiphospholipid antibody, thrombosis of vessels, venous insufficiency, lupus profundus, and drug‐induced lupus syndrome have been associated with leg ulcerations.
\nLeg ulcerations of Sjögren syndrome have been associated with cryoglobulinemia, anticardiolipin antibody, and vasculitis [46, 51].
\nLeg ulcers of dermatomyositis have been reported to involve calcinosis cutis and vasculitis [46].
\nMCTD is an overlap syndrome combining features of SLE, RA, systemic sclerosis, and dermatomyositis together with the presence of antibodies to U1‐RNP. Chronic leg ulcers are not rare in MCTD and they have been reported to be due to subcutaneous calcification, vasculitis, vasospasm (Raynoud\'s phenomenon), vascular thrombosis, and antiphospholipid antibodies [46, 52, 53].
\nNumerous infections can precipitate ulcerations on the lower legs. Ecthyma, atypical mycobacterial infections, late syphilis, cutaneous leishmaniasis, actinomycoses, nocardioses, human immunodeficiency virus (HIV) infection, herpes simplex, and cytomegalovirus infections must be considered [41, 43, 54]. In addition, all chronic wounds may be secondarily contaminated with bacteria. Tissue culture will help elucidate the cause [4].
\nVarious metabolic factors such as diabetes mellitus, amyloidosis, hyperhomocysteinemia, prolidase deficiency, oxalosis, calciphylaxis, and gout can play a role for the lower leg ulcerations.
\nNecrobiosis lipoidica is a rare, chronic granulomatous disease of the skin. Clinical presentation characterized by atrophic, indurated plaques with a yellowish center and telangiectasies [42]. The lower legs, especially the shins, are the most common sites of involvement. During the course, ulcerations may occur. Necrobiosis lipoidica frequently occurs in association with diabetes mellitus (Figure 7).
\nNecrobiosis lipoidica.
Calciphylaxis is an uncommon disorder, classically associated with renal disease and secondary parathyroidism [55]. Clinical presentation may begin as microlivedo that develop into painful ulcerations.
\nSeveral forms of anemia (thalassemia, sickle cell anemia, hereditary spherocytosis, glucose 6 phosphate dehydrogenase deficiency), and hypercoagulable disorders (antiphospholipid antibody syndrome, antithrombin III, protein C or S deficiency, essential thrombocythemia, thrombotic thrombocytopenic purpura, polycythemia, or abnormal clotting factors such as factor V Leiden, factor II mutant) have been associated with lower leg ulceration [54].
\nMany tumor types such as basal cell carcinoma, squamous cell carcinoma, and melanoma may present with skin ulceration. Basal cell carcinomas arising from venous ulcers appear as exuberant granulation tissue rolling onto the wound edges [4]. In addition, malignancy that presents as Marjolin\'s ulcers is most commonly associated with chronically inflamed, or scarred skin. Skin biopsy is necessary to identify ulcerated malignant tumors on the leg.
\nHydroxyurea is a cytostatic drug used in various myeloproliferative disorders. A rare complication is the development of painful ulcers, usually localized on the malleoli or in neighboring regions [42, 54]. The coumarin derivatives, nifedipine, diltiazem, barbiturates, and erythropoietin in very rare cases, may trigger ulcer development [42].
\nIt is essential to treat the patients with multidisciplinary approach. The complete assessment of the chronic venous insufficiency should be evaluated together with vascular surgeons. The decision of the surgical treatment in appropriate cases should be considered with plastic surgeons. Knowledge of pathogenesis of venous ulcers and avoiding from its risk factors will be provided to choose the optimal treatment for patients with venous leg ulcers, which cause both impairment of life quality and socioeconomic burden. A multidisciplinary team of specialists will be helpful in the evaluation of venous leg ulcers and providing the most appropriate treatment.
\nSeveral treatment options are available for the management of venous ulcers. Pain reduction, closure of the ulcers, and prevention of the recurrences are the main goals of the treatment [56]. Reversing the effects of venous hypertension is the primary purpose of the treatment of venous leg ulcers. The easiest method is leg elevation [57]. Although it seems to be impractical to most of the patients, elevation of the legs above the heart level for 30 minutes, 3–4 times a day, provides the dissolution of the swelling and improves the microcirculation [58]. Leg elevation can also be performed at night by raising the foot 15–20 cm high [59]. Moreover, good nutrition and assessment with each dressing change are necessary to support the therapy. Initially and at each dressing change, the depth, width, and height of the wound bed should be measured to evaluate the improvement. Appropriate therapy of the wound must be selected patient centered. Infection control, debridement, antibiotics, dressings, compression, and adjuvant therapies will be described in this section.
\nCleansers are the first and main step in preparing the wound bed. Wound cleansing with a neutral, nonirritating solution with a minimum chemical and mechanical trauma should be performed at each dressing change. Wound exudate and other debris around the wound area in venous leg ulcers must be cleansed with an appropriate solution. Although several cleansing solutions are in the market, the choice of the cleanser should have the purpose of avoiding toxicity to the viable tissue in the wound bed [31].
\nDebridement during the initial evaluation is recommended to remove the necrotic tissue, excessive bacterial burden, and nonviable cells [31]. Although debridement of the wound is commonly performed to allow the formation of good granulation tissue and proper epithelialization by creating an appropriate environment to keratinocyte migration, there is a lack of evidence that routine wound debridement accelerates wound healing [31]. There are several ways of wound debridement, including autolytic, chemical, and mechanical [60].
\nIn venous ulcers, it is possible that wound occlusion itself promotes re‐epithelialization, reduces associated pain, enhances autolytic debridement, and provides an additional barrier to bacteria [61, 62]. Hydrogels, alginates, hydrocolloids, foams, and films are the basic occlusive dressings. Wound features, exudate amount and cost of the material, and patient and physician preference affect the choice of dressing [63].
\nSeveral enzyme‐debriding agents have been developed to promote the removal of the necrotic tissue and the formation of proper granulation tissue [64, 65]. Specific proteolytic enzyme therapies to the venous ulcers may accelerate the removal of fibrin cuffs [66]. Various enzyme‐debriding agents are available, including collagenase, papain, trypsin, and tissue plasminogen activator [60, 67, 68]. Frequency of the application of the dressing may vary up to the manufacturer\'s recommendations. Enzymatic debridement, which does not require a trained clinician for application, has been found in several studies to remove nonviable tissue from the wound beds of venous leg ulcers, but there is no evidence that this method provides a benefit over surgical debridement [69, 70].
\nApplication of wet‐to‐dry dressings, hydrotherapy, irrigation, and dextranomers are some of the methods of mechanical debridement [71]. The removal of the viable tissue along with the necrotic material is the major disadvantage of mechanical debridement [72]. Hydrosurgical debridement was showed to have a shorter procedure time but requires additional cost and a trained clinician [73, 74]. Furthermore, it may be associated with a significant periprocedural pain [69]. Dextranomer\'s hydrophilic structure that provides a high absorptive capacity makes it useful for wounds with heavy exudate. The possibility of dehydration of the wound bed demands caution [4]. Surgical debridement, which may be performed with a curette, forceps, scalpel, or sharp scissors, is another way to remove necrotic tissue. As venous ulcers do not comprise frank necrosis or eschar tissue, this method is rarely used in venous ulcers [75]. During surgical debridement, local infiltrative, regional block, or general anesthesia may be required according to the extensity of the wound [31].
\nAntimicrobial therapy is suggested in venous ulcers with >1 × 106colony‐forming unit (CFU)/g of bacteria on quantitative culture and clinical evidence of infection. Systemic antibiotic therapy, guided by sensitivities performed on wound culture, is recommended. Oral antibiotics are preferred in the beginning of the therapy duration and should be limited to 2 weeks [31]. Combination of mechanical debridement and antibiotic therapy is thought to be successful in eradicating infection in venous leg ulcer. In case of cellulitis, beta‐lactam and non beta‐lactam antibiotics may be treatment options. Trimethoprim‐sulfamethoxazole and clindamycin are recommended as initial empiric therapy if methicillin‐resistant Staphylococcus aureus is the suspected reason of cellulitis [76]. The use of topical silver for infected venous ulcers is controversial [31]. Recently, cadexomer iodine is reported to shorten the healing time of venous ulcers [77].
\nIt is likely to be an increased risk of contact dermatitis in patients with chronic venous insufficiency, so in these patients any topical preparation must be used carefully [4]. There is a lack of evidence of the positive effects of topical antimicrobials in the healing of venous ulcers [31].
\nIt is important to keep the periulcer skin healthy to provide improvement in venous ulcers. Management of dermatitis and other abnormalities in periulcer skin accomplishes other therapy strategies in venous ulcers [31]. As mentioned above, contact dermatitis related to topical agents and dressings used in the treatment of venous ulcers are very common. In severe contact dermatitis, a short term of systemic steroids may be needed [4, 31]. Skin lubricants will be helpful in the terms of dermatitis in the calf and ankle due to venous hypertension [31]. Care of the periulcer skin will improve the venous wound healing; therefore, it is necessary to recognize the abnormalities in this area and start the appropriate treatment.
\nSeveral types of wound dressings including gauzes, films, gels, foams, hydrocolloids, alginates, hydrogels, and other polymers are being used beneath compression bandages. Some of the dressings show biological activity on its own, while some provide the release of bioactive constituents. Different types of wound dressings such as hydrogels, hydrocolloids, foams, films, and wafers may comprise of antimicrobials, anti‐inflammatory agents, analgesics, growth factors, and proteins, which would be useful in different problems of wound healing [78, 79]. During the choice of the wound dressing type, features of the ulcer should be considered and the mostly desired function of the dressing (such as cleaning, absorbing, regulating, creating a moist environment, and the possibility of adding medication, protecting the periulcer skin) should be decided [80]. Of course, the patient\'s needs and cost‐effectiveness are other factors affecting the dressing choice [81]. The optimal wound dressing should absorb the exudate and also maintain a moist, warm wound bed and protect the periulcer skin [31, 76]. Routine use of topical antimicrobial dressings is not recommended [31]. While using wound dressings, risk of allergy should be kept in mind in venous ulcers. In conclusion, topical wound dressings are recommended as a part of the standard therapy in venous ulcers [31].
\nCompression therapy remains the mainstay treatment of venous leg ulcers [76]. Compression is a kind of mechanical therapy, which is simply based on applying pressure to the limb [31]. There is a significant improvement in ulcer healing and reduction in recurrence rates with an appropriate compression therapy [4, 82]. Compression therapy corrects the venous hypertension by improving venous pumping function and lymphatic drainage [83]. And as a result of compression, local hydrostatic pressure increases and superficial venous pressure decreases; thus, the edema dissolves resulting in cutaneous blood flow increase [83]. Other effects of compression therapy are clinical improvement in lipodermatosclerotic skin through lymph propulsion along with the increase in lymph transport and fibrinolysis [4]. Besides the mechanical effect, compression reduces the release of macromolecules into the extravascular space, some of which play role in wound healing [84].
\nVarious types of devices have been used for compression therapy, such as different types of bandages, bandage systems, ready‐to‐use garments, and several pneumatic devices [31]. It is thought that an external pressure of 35–40 mm Hg at the ankle is necessary to overcome venous hypertension [85]. For acute disease, reducing edema and improving the healing process, inelastic or rigid bandages as well as elastic and multilayered bandages are suggested. The bandage system should have high pressures when the patient walks (working pressure) and low pressure when the patient is on rest (resting pressure). Traditional Unna boot, a moist zinc‐impregnated paste bandage, is a prototype of this system [83, 86]. Modified Unna boots (short‐stretch bandages) have the same properties. Their stable shape despite the volume changes in leg secondary to edema reduction, unpleasant odor due to wound exudate, and potential development of contact dermatitis are the limiting factors of Unna boots’ use [76, 77]. After edema reduces, long‐stretch bandages are beneficial as they provide appropriate working pressure and higher resting pressure. Its easy use and providing of frequent dressing changes make the elastic compression bandages practical. Covering the leg by overlapping the bandage between turns will produce a multilayer bandage. Different components of bandages may be applied at each layer. While this application increases the pressure and also makes the final multilayer bandage less elastic and more stiff due to the friction between the surfaces of each bandage [31], intermittent pneumatic compression (IPC) pumps are also used. These devices consist of plastic air chambers, encircling the lower leg. As the air chamber fills to a preset pressure then deflated. With this system, compression of the leg is provided periodically [87].
\nAlthough compression therapy is known to be effective in both healing of venous ulcers and prevention of recurrent ulcers, there is still no optimized compression method [31, 88].
\nSystemic pharmacotherapy may be useful as an adjuvant therapy in venous ulcers. Most of the systemic agents used as adjuvant therapy acts in mechanism of one or more points in the pathophysiology of venous leg ulceration.
\nPentoxifylline, an antifibrinolytic agent, is thought to promote wound healing as an adjunctive therapy. Pentoxifylline has been shown to play role in microcirculation by promoting leukocyte migration, reducing platelet aggregation and fibrinogen levels, decreasing plasma viscosity, stimulating collagenase production, and blocking the effects of tumor necrosis factor‐alpha on fibroblasts [89, 90]. Pentoxifylline may act in venous ulcer healing through the effects of cytokine production [91]. The conventional dose of pentoxifylline in venous leg ulcers is 400 mg three times a day. But recently, it has been proposed that the use of pentoxifylline 800 mg three times a day is more effective in venous ulcer healing. The main side effects reported were gastrointestinal disturbances such as nausea, indigestion, and diarrhea [89, 92, 93]. In studies, pentoxifylline has shown to be an effective adjuvant to compression therapy in venous leg ulcers. According to a Cochrane review, pentoxifylline plus bandaging is more effective than compression plus placebo and pentoxifylline may even be effective in the absence of compression [93].
\nThere is currently insufficient evidence for the effectiveness of aspirin in venous leg ulcers [94]. The use of acetylsalicylic acid as an adjunct for the treatment of venous ulcers has been evaluated in one pilot study and one randomized controlled trial to date. The effect of aspirin in venous ulcers is through its irreversible inhibition of cyclooxygenase, resulting in reduction in thromboxane A2 implicated in platelet aggregation [95].
\nThere are no specific indications for skin grafting of the ulcers of lower extremities [4]. Surgical treatment should only be considered in patients with venous ulcers that do not heal with conservative therapies [96]. Autografts, allografts, or human skin equivalents can be used, with a resulting healing rate of 73% [97]. In venous ulcers, skin grafting can also be followed by additional treatment to accelerate healing. The outcomes of the split‐thickness skin grafting in venous ulcers vary in different studies [31]. There is still lack of evidence in the routine use of split‐skin thickness skin grafting.
\nNegative pressure wound therapy (NPWT) is currently used widely in wound care and is promoted for use on wounds. In this system, a wound dressing is applied to the wound, to which a machine is attached. The negative pressure (or vacuum) that the machine applies sucks any wound and tissue fluid away from the treated area into a canister.
\nThe evidence is insufficient in clinical effectiveness of NPWT in the treatment of leg ulcers. It is thought to be effective in wound healing through providing excess drainage, promoting angiogenesis, and decreasing the bacterial load of the wound [98]. There is some positive evidence that the treatment may reduce time to healing as part of a treatment, tissue granulation, area and volume reduction have also been reported. NPWT is not suggested as a primary treatment for venous leg ulcers [31, 99].
\nIn recent years, cellular and/or tissue‐derived products (CTPs) such as extracellular matrix (ECM; OASIS®) [100], human skin equivalent (HSE; Apligraf®) [101–103], and living skin equivalent (LSE; Dermagraft®) [104–107] have been explored as alternative therapeutic options. Studies investigating the effects of CTPs are applied to the wounds that have been stuck in the inflammatory phase. CTPs provide the healing by supplying various biological factors, reducing levels of unnecessary cytokines or enzymes (such as matrix metalloproteinases), and/or forming a temporary ECM (which results in granulation) [108].
\nRecently, Apligraf, an allogeneic bilayer cellular therapy, has been approved by FDA for use in venous ulcers [31]. Before the application of cellular therapy, appropriate wound bed preparation, including the removal of debris and any necrotic tissue, should be done. The application of the graft is recommended to be done with a period of 1–3 weeks with observations of effectiveness before reapplication is considered. And reapplication is recommended as long as the venous ulcer continues to respond to the therapy [31]. In patients with venous leg ulcers who have failed with standard therapy for 4–6 weeks, cultured allogeneic bilayer skin replacements should be used [31].
\nEven though cellular treatments are initially more expensive, it may be more effective and less costly in the long term in chronic venous ulcers [109].
\nIn chronic wounds, human tissue (amniotic membrane, cryopreserved skin) or animal tissue (bladder, fetal bovine skin, others) constructs are being used. Growth factors or some other molecules, the tissues contain, may support healing process [110].
\nGranulocyte macrophage‐colony stimulating factor (GMCSF) is a growth factor that has stimulatory effects on keratinocyte proliferation and endothelial cell and fibroblast differentiation [111]. In some studies, both intradermal injections of GM‐CSF and topical application of GM‐CSF have been shown to be effective in healing rates of venous ulcers [98]. But, injection site and bone pain can limit the intradermal use of GM‐CSF [98].
\nSmall intestine submucosa (SIS, Oasis®) is a biomaterial derived from porcine SIS that acts as an extracellular matrix. It is composed of Type I, III, IV, and V collagen, glycosaminogylcans, proteoglycans, proteoglycans, fibronectin, and growth factors [98, 112]. Successful results have only been reported in studies of using porcine small intestinal submucosa in venous leg ulcers [100]. It has been approved by FDA for use in wounds including venous leg ulcers. Use of porcine small intestinal submucosa tissue construct in addition to compression therapy for the treatment of venous leg ulcers is only suggested in patients who did not respond to the standard therapy for 4–6 weeks [31]. It was shown to be well tolerated and nontoxic and did not induce an adverse immunological reaction even in patients given repeated applications.
\nUltrasound has been used as a therapeutic tool for nearly 50 years [113]. Recently, ultrasound therapy has been applied for the treatment of chronic wounds in some centers [114]. Although high‐frequency ultrasound (HFU) (1–3 MHz) has been shown to promote healing of some injuries [115, 116], it has some disadvantages such as, burns or endothelial injury. However, in some studies low‐dose application of ultrasound has been reported to be more successful than high‐dose ultrasound in the treatment of skin wounds [117]. Thus, noncontact ultrasound therapy is among the newer modalities. Use of lower frequency (40 kHz) ultrasound in wound management was approved by the FDA in 2004 [118]. Low‐frequency ultrasound therapy provides wound healing via the production, vibration, and movement of micron‐sized bubbles in the coupling medium and tissue. The healing process improves by the reduced bioburden, increased angiogenesis, stimulated cellular activity, and the removal of necrotic tissues [119]. Additional studies are necessary to determine standardized protocols of therapeutic ultrasound in venous ulcers treatment. Routine use of ultrasound therapy in venous ulcer management is not suggested [31].
\nSurgical procedures are often applied when dressings and compression therapies fail in the venous ulcer treatment [76]. There are two approaches in surgical treatment of venous ulcers: ameliorating the cause of the ulcer and treating the ulcer itself by surgical procedures [4].
\nSuperficial venous insufficiency is present in about forty to fifty percent of patients with venous ulcer [2]. Superficial vein surgery, simply comprised of ligation or sclerosis of the long and short saphenous systems, with or without communicating vein ligation or sclerosis, may be useful in patients with superficial venous insufficiency but only when deep veins are competent [120]. Although superficial vein surgery does not affect the success of improvement in venous ulcers, ulcer recurrence has shown to be reduced by the procedure [120]. Subfascial endoscopic perforating vein surgery, a new surgical technique, has proven to be effective in patients with perforator vein insufficiency [8]. In this technique, perforator veins are ligated by an endoscopic camera system through a small incision. This procedure has low complication rates and morbidity [121]. As mentioned above, it has been shown that venous surgery does not seem to improve the healing but delays or reduces the recurrences [76].
\nRadical excision of the diseased area including the whole ulcer bed, the fibrotic suprafascial tissues, and the abnormal superficial and perforating veins, and flapping this large soft tissue defect have been shown to be successful in a few cases. However, highly invasive character of this procedure limits its application [122].
\nSkin grafting has proven beneficial to heal large-size recalcitrant ulcers [120]. Contamination with microorganisms and risk of trauma are the main factors that should be kept in mind when grafting for ulcer [123]. Split‐thickness skin grafts, punch grafting, and meshed grafts are some of the grafting methods used in venous leg ulcers. While pinched grafts are suitable for small ulcers, meshed grafts are useful for large highly exudative ulcers [4].
\nIn the period that patient has no venous ulcers, it is important to keep in cooperation with and offer some simple lifestyle changes to the patient. Leg elevation is thought to provide venous return, reduce edema, and improve cutaneous circulation [98]. Elevation of the legs above heart level for 30 minutes three or four times a day is a simple and effective method in reducing edema and improving the cutaneous microcirculation in patients with chronic venous insufficiency [87]. Calf muscle pump dysfunction is usually present in venous insufficiency and venous ulcers. Appropriate calf exercise regimes have shown to be useful to improve muscular endurance and may even provide proper functioning of the muscle pump [124]. Even in the first stages of chronic venous disease, starting the effective treatment of symptoms will help for preventing progression to ulcer. The most important step is to persuade the patient, with risk factors or early signs of venous insufficiency, to apply the appropriate compression. It is important to make the patients understand that compression therapy will be a lifelong therapy. The elastic bandages with the appropriate length and strength of compression must be worn daily. Moreover, weight management of obesity, regular exercise programs (with the aim of improving the efficiency of calf muscle pump), and treatment of varicosities (endovenous laser ablation, radiofrequency ablation, and other approaches to repair veins and valves) should be planned. Thrombophilia is increasingly recognized as a major risk factor for DVT, which is the most common identifiable risk factor for the development of chronic venous ulcer. More than 40% of patients with CVU have at least one thrombophilia and chronic venous ulcer patients with post‐thrombotic disease are shown to have lower response rates to medical and surgical therapy. Thrombophilia screening is suggested to be performed in patients who have venous ulcer before the age of 50 to stratify the thrombotic risk and start the appropriate prophylactic and therapeutic management. Good nutrition is important in venous ulcer patients as protein deficiency is associated with impaired wound healing. Also smoking affects healing via decreasing the fibroblast proliferation [76]. All these factors together will help to prevent the progression of chronic venous disease to ulceration. Commitment to lifelong exercise programs, weight control, and protection against skin injury is necessary for the prevention of venous leg ulcers [31, 125].
\nExtremophile organisms capable of growing in extreme conditions draw considerable attention since they show that life is robust and adaptable and help us understand its limits. In addition, they show a high biotechnological potential [1, 2]. Most of the best-characterized extreme environments on Earth are geophysical constraints (temperature, pressure, ionic strength, radiation, etc.) in which opportunistic microorganisms have developed various adaptation strategies. Deep-sea environments, hot springs and geysers, extreme acid waters, hypersaline environments, deserts, and permafrost or ice are some or the most recurrent examples of extreme environments [3]. However, the atmosphere is rarely thought of as an extreme habitat. In the atmosphere, the dynamics of chemical and biological interactions are very complex, and the organisms that survive in this environment must tolerate high levels of UV radiation, desiccation (wind drying), temperature (extremely low and high temperatures), and atmospheric chemistry (humidity, oxygen radicals, etc.) [4]. These factors turn the atmosphere (especially its higher layers) into one of the most extreme environments described to date and the airborne microorganisms into extremophiles or, at least, multiresistant ones [5].
\nIt is known that airborne cells can maintain viability during their atmospheric residence and can exist in the air as spores or as vegetative cells thanks to diverse molecular mechanisms of resistance and adaptation [2, 6]. The big question is whether some of them can be metabolically active and divide. Bacterial residence times can be several days, which facilitate transport over long distances. This fact, together with the extreme conditions of the atmosphere, has led researchers to think for years that they do not remain active during their dispersion. However, recent studies strongly suggest that atmospheric microbes are metabolically active and were aerosolized organic matter and water in clouds would provide the right environment for metabolic activity to take place. Thus, the role played by microorganisms in the air would not only be passive but could also influence the chemistry of the atmosphere. In any case, only a certain fraction of bacteria in the atmosphere would be metabolically active [2, 7].
\nDespite recognizing its ecological importance, the diversity of airborne microorganisms remains largely unknown as well as the factors influencing diversity levels. Recent studies on airborne microbial biodiversity have reported a diverse assemblage of bacteria and fungi [4, 8, 9, 10, 11, 12], including taxa also commonly found on leaf surfaces [13, 14] and in soil habitats [15]. The abundance and composition of airborne microbial communities are variable across time and space [11, 16, 17, 18, 19]. However, the atmospheric conditions responsible for driving the observed changes in microbial abundances have not been thoroughly established. One reason for these limitations in the knowledge of aerobiology is that until recently, microbiological methods based on culture have been the standard, and it is known that such methods capture only a small portion of the total microbial diversity [20]. In addition, because pure cultures of microorganisms contain a unique type of microbes, culture-based approaches miss the opportunity to study the interactions between different microbes and their environment.
\nAnother limitation for the study of aerial microbial ecology at higher altitudes or in open ocean areas is the difficulty of repeated and dedicated use of airborne platforms (i.e., aircraft or balloons) to sample the air. Most studies to date on the atmospheric microbiome are restricted to samples collected near the Earth’s surface (e.g., top of mountains or buildings). Aircraft, unmanned aerial systems (UASs), balloons or even rockets, and satellites could represent the future in aerobiology knowledge [5, 21, 22]. These platforms could open the door to conducting microbial studies in the stratosphere and troposphere at high altitudes and in open-air masses, where long-range atmospheric transport is more efficient, something that is still poorly characterized today. The main challenge in conducting these kinds of studies stems from the fact that microbial collection systems are not sufficiently developed. There is a need for improvement and implementation of suitable sampling systems for platforms capable of sampling large volumes of air for subsequent analyses using multiple techniques, as this would provide a wide range of applications in the atmospheric, environmental, and health sciences.
\nIn aerobiology, dust storms deserve special mention. Most of them originate in the world’s deserts and semideserts and play an integral role in the Earth system [23, 24]. They are the result of turbulent winds, including convective haboobs [25]. This dust reaches concentrations in excess of 6000 μg m−3 in severe events [26]. Dust and dust-associated bacteria, fungal spores, and pollen can be transported thousands of kilometers in the presence of dust [9].
\nIn this chapter, we approach the atmosphere as an extreme environment and make use of some advanced data from an example of an in situ study of the atmosphere: the analysis of bacterial diversity of the low troposphere of the Iberian Peninsula during an intrusion of Saharan dust using a C-212 aircraft adequately improved for aerobiological sampling.
\nIt is well known that there is a biota in the atmospheric air. The first study dates back to the nineteenth century, which speak about the presence and dispersion of microorganisms and spores in the atmosphere [27, 28]. Although the atmosphere represents a large part of the biosphere, the density of airborne microorganisms is very low. Estimates suggest that from the ground surface up to about 18 km above sea level (troposphere), there is less than a billionth of the number of cells found in the oceans, soils, and subsurface. Between approximately 18 and 50 km above sea level (stratosphere), temperature, oxygen, and humidity decrease and with them the number of cells. Above the ozone layer (between 18 and 35 km into stratosphere), ultraviolet (UV) and cosmic radiation become lethal factors. Once in the mesosphere (above 50 km), life is difficult to imagine; however microorganisms of terrestrial origin could arrive to the stratosphere from lower layers via different phenomena (human activity, thunderstorms, dust storms, or volcanic activity), and bacteria have been found isolated up to 41 km or in dust samples from the International Space Station (\nFigure 1\n) [6, 29]. Therefore, airborne microbes are always present in the atmosphere [11, 30, 31], and their permanence is dynamic, resulting in an environment with enormous variability. Estimates calculate that over 1021 cells are lifted into the atmosphere every year, leading to considerable transport and dispersal around the atmosphere, with a large portion of these cells returning to the surface due to different atmospheric events as part of a feedback cycle. Undoubtedly, airborne microbes play an important role in meteorological processes. They have been linked to the nucleation phenomena that lead to the formation of clouds, rain, and snow and to the alteration of precipitation events [32, 33, 34]. Their presence is essential to understand long-range dispersal of plant and potential pathogens [7, 35, 36] and maintain diversity in ground systems and could interfere with the productivity of natural ecosystems [17, 18]. On the other hand, airborne bacteria can have important effects on human health, being responsible for different phenomena such as seasonal allergies and respiratory diseases. Based on data from terrestrial environments, the global abundance of airborne bacteria has been estimated to range between 104 and 106 m−3 [37]. However, more recent studies incorporating direct counting by microscopy or quantitative PCR have provided more accurate estimates of the number of airborne microbes, which apparently point to a higher number of cells present in the atmosphere [38, 39, 40, 41].
\nDiagram displaying atmosphere layers, temperature and airborne emission sources. Yellow line marks atmospheric temperature. Bottom of the figures shows the common sources of aerosolized bacteria, with special attention to dust storms.
There is a great variety of airborne microorganism sampling systems, allowing us to select the most suitable one depending on our objectives [42]. On the other hand, no standardized protocols exist, which is a major pitfall when developing our objectives. This fact has led some authors to propose the creation of consortiums of interested parties for establishing standardized protocol reproducibility [20], as well as the need to establish global networks of aerobiological studies [11]. Two approaches are proposed: particles or cells can be collected passively or directly from the atmosphere. Passive media usually involves decanting [43] and collecting particles over snow [44] or through the collection of atmospheric water [45]. On the other hand, active methodologies entail three major approaches: filtration, impaction, and liquid impingement. All three approaches are very efficient when developing culture-dependent techniques. In contrast, culture-independent approaches produce some serious problems that make the work difficult: the high variability of the system and the low biomass mean that sampling campaigns are, in many cases, extremely inefficient [20]. Lastly, the use of airborne platforms is not very extended, but they represent a good opportunity to conduct a more direct study of the atmosphere [5, 19, 31].
\nFiltration is a simple and cheap method that is often efficient. It involves pumping air through a filter where the mineral and biological particles are trapped. Filters of different materials and porosity are available made of cellulose, nylon, polycarbonate or fiberglass, or quartz. Sizes used range from 0.2 to 8 μm, depending on the size of the particles to be captured and the capacity of the pump. In many cases, a PM10 filter can give better results when collecting smaller bacteria, as it allows greater airflow. Airflow filtration rates generally range between 300 and 1000 L/minute [4, 46]. Microorganisms trapped in the filter can be cultured, or the filters can be directly used for DNA extraction. In addition, filters are a very suitable support for microscopy, and countless holders for filters are available (an example is shown in \nFigure 2A\n).
\nThree different samplers of airborne microorganisms. (A) Filter holder and a filter (PALL Corporation). (B) Impinger sampling of bioaerosols (BioSampler, SKC, Inc.). (C) Six-stages Andersen Cascade Impactor (Thermo Fisher Scientific).
In impingement, particles are collected in a liquid matrix [20]. Normally a buffer is used such as phosphate buffer saline (PBS) that helps maintain the viability of the cells. One of the more widely used liquid impingers is BioSampler SKC (\nFigure 2B\n). In this case, the tangential movement of the particles inside the flow impinger retains the particles in the collecting liquid. The suspension obtained could be used for culturing or for molecular ecology assays [20]. One of the advantages of impingement collection is that it facilitates quantitative techniques such as flow cytometry or in situ hybridization [47].
\nIn this system, the particles generally impact into a petri dish with an enrichment medium. It is, possibly, the most efficient and most used method to conduct studies based on culture. Airflow impacting onto the plates is controlled by slots that allow the homogeneous distribution of the air. The system can be single stage or several stages in cascade, causing the particles to be distributed by size in the different petri dishes [20]. Some variants replace petri dishes with agarose filters or Vaseline strips, in order to carry out independent culture methodologies, but efficiency is very low. The original and more popular impactor is the Andersen cascade impactor (\nFigure 2C\n) [48].
\nSeveral studies explain and compare sampling methodologies in aerobiology, but most of them focus on the surface of the Earth (e.g., on top of mountains or buildings) or indoors [42, 49, 50, 51, 52, 53, 54]. However, small studies have been conducted at higher altitudes or in open sea areas. The use of airborne platforms (balloons, aircraft, rockets, etc.) for aerobiology sampling would allow conducting a direct study of the microbial ecology of the atmosphere. Another advantage of airborne platforms is the possibility of studying the vertical distribution of airborne microbial communities. In addition, some aircraft allow us to develop studies in the upper troposphere or in the stratosphere. Unfortunately, atmospheric microbial collection instruments have not been developed enough for airborne platforms.
\nAmong the different airborne platforms, aircraft, due to their versatility and access, are particularly interesting. Some studies have been conducted, but not enough samples have been developed yet, and efficiency is still very low. As already mentioned, the efficiency of samplers in soil-level aerobiology faces a series of problems (low biomass, high variability of populations, lack of standardized protocols). In the case of airplanes, in addition to these intrinsic problems associated with atmospheric microbial ecology, other additional ones exist: (1) the high velocity of the aircraft in relation to the relative quiescent air mass. This makes it difficult to obtain an isokinetic sampler and, therefore, one that is sufficiently efficient that would allow us to obtain a correct quantification of the incoming air [55]; (2) the sampler must be in a location on the airplane that avoids chemical contamination from the operation of the device. Previous studies have used wing-mounted air samplers or the roof of the aircraft to reduce the possibility of in-flight contamination [21, 22, 56, 57, 58]. Similarly, it should allow the aseptic collection of samples, avoiding microbiological contamination during the process. This operation, which can be very simple in the laboratory or at ground level, becomes tremendously complicated on an airplane, since air intakes that are part of the fuselage of the aircraft are often difficult to sterilize. It is therefore necessary to develop robust sterilization protocols. The spectacular work of DeLeon-Rodríguez of 2013 has been criticized in this aspect [40, 59]; (3) sampling time. A possible solution to the low biomass of the atmosphere is to increase sampling time, but in the case of flights, we are limited to the flight autonomy of the aircraft. Although scarce, some studies from airplanes have been conducted. The first studies that were conducted in airplanes were carried out by impaction on a petri plate with enrichment means, which allowed isolating microorganisms from the upper troposphere and even from the stratosphere [21, 57, 60]. However, advances in molecular ecology have caused the most recent studies to favor filtration [40, 58].
\nThe European Facility for Airborne Research (EUFAR) program brings together infrastructure operators of both instrumented research aircraft and remote sensing instruments with the scientific user community. However, it lacked aircraft prepared for microbiological sampling. The National Institute for Aerospace Technology (INTA) belonging to the Spanish Ministry of Defence has two CASA C-212-200 aircraft that were suitably modified to be used as flying research platforms. Now, these two aircraft are a unique tool for the study of atmospheric microbial diversity and the different environments of the EUFAR program. Our research group has a CASA-212 aircraft with an air intake located on the roof of the aircraft. A metal tube fits the entrance and is fitted inside the aircraft to a filter holder, a flowmeter, and a pump (\nFigure 3\n). This simple system is easy to sterilize, and both the metal tube and the filter holder can be replaced in flight by other sterile ones if we want to take different samples. Using PM10 fiberglass filters, we can obtain isokinetic conditions and pass 1800 L of air per hour through the filter, as indicated by the flowmeter.
\nAirborne microorganisms sampler installed in INTA’s CASA C-212-200 aircraft.
In a series of recent experiments, we tried to install a multi-sampler system in our aircraft, where we had five systems in parallel and connected to the same intake of the plane: one filter holder, two impingement systems, and two impactors (\nFigure 4\n). The results clearly showed that in the case of our aircraft, filtration was more efficient (data not shown).
\nMulti-sampler system tested in INTA’s CASA C-212-200 aircraft. (A) Impinger sampler, design and manufacture own. (B) Impactor sampler (Impaktor FH6, Markus Klotz GmbH). (C) Coriolis μ (Bertin Technologies SAS) a impinger biological air sampler. (D) Filter holder (PALL Corporation). (E) Six-stages Andersen Cascade Impactor (Thermo Fisher Scientific).
Aerobiology studies have traditionally focused on the collection of bacterial cells and the analysis of samples by total counting and culture-based techniques. It is known that such methods capture only a small portion of the total microbial diversity [61]. The almost exclusive use, for years, of these methodologies is one of the reasons for these limitations in the knowledge of aerobiology. In addition, culture-dependent methods do not allow us to study the interactions between different species of microorganisms. Culture-independent methods have been used to assess microbial diversity, increasing the specificity of microbial identification and the sensitivity of environmental studies, especially in extreme environments. These methods have recently been applied to various areas of airborne microbiology [62, 63, 64, 65] revealing a greater diversity of airborne microorganisms when compared to culture-dependent methods. Some good studies approach the challenges and opportunities of using molecular methodologies to address airborne microbiology [20, 66]. Although molecular ecology methods allow the rapid characterization of the diversity of complex ecosystems, the isolation of the different components is essential for the study of their phenotypic properties in order to evaluate their role in the system and their biotechnological potential. A combination of culture-dependent and culture-independent methods is ideal to address the complete study of the system.
\nModern culture-independent approaches to community analysis, for example, metagenomics and individual cell genomics, have the potential to provide a much deeper understanding of the atmospheric microbiome. However, molecular ecology techniques face several particular challenges in the case of the atmospheric microbiome: (1) very low biomass [20]; (2) inefficient sampling methods [20]; (3) lack of standard protocols [9, 20]; (4) the composition of airborne microbes continuously changes due to meteorological, spatial, and temporal patterns [7, 62, 67, 68, 69, 70]; and (5) avoidance of the presence of foreign DNA in the system [59]. Because these issues are not yet resolved, most of the non-culturing approaches focus on microbial diversity, where they are highly efficient.
\nThe most recurrent techniques are those based on DNA extraction, gene amplification of 16S/18S rRNA, and next-generation sequencing (NGS) technologies. Often, this approach is more efficient due to the greater efficiency and sensitivity of this process, as opposed to gene cloning and Sanger sequencing; thus some authors are inclined toward metagenomics instead of amplification. This provides more information and avoids an intermediate step, but bioinformatic processing is tedious and often only provides data in relation to diversity, making the annotation of the rest of the information very complicated [20]. These approaches can be complemented with quantitative methods such as qPCR, flow cytometry, or fluorescence in situ hybridization (FISH) [41, 47, 66, 71]. FISH is surely the best and most specific cell quantification methodology that exists. However, in the case of aerobiology, it cannot always be used. A minimum number of cells must exist so that we can observe and count them under a fluorescence microscope. Due to the variability of microbial populations in the air, this is not always achieved. In our research group, we have obtained very good results in this regard, optimizing cell concentration. \nFigure 5\n shows epifluorescence micrographs of bacteria from an air sample. On this occasion, sampling was performed using a biological air sampler (Coriolis μ, Bertin Technologies SAS), where biological particles are collected and concentrated in a liquid (PBS). Sampling was conducted for 2 hours at ground level, pumping a total of 36,000 L of air. After this time, the sample was paraformaldehyde fixed and filtered through a 0.2 μm pore size, hydrophilic polycarbonate membrane, 13 mm diameter (GTTP, Millipore). A half sample was hybridized with the universal Bacteria domain probe, EUB338I-III [72], following a conventional protocol [73]. The second half was hybridized with the probe NON338 [74] as negative control. In this case, an average of 140 cells per liter of air was counted. Occasionally, FISH also allows to observe bacteria attached to mineral particles (\nFigure 5C\n–\nD\n).
\nEpifluorescence micrographs of bacteria from an air sample. (A and C) DAPI-stained cells; (B and D) same fields a A, and C, respectively, showing cells hybridized with probes EUB338I-III (Cy3 labeled), specific for Bacteria domain. All micrographs correspond to the same hybridization process, performed with a sample obtained after 4 hours sampling at ground. C and D show microorganisms attaches to a mineral particles (arrow sign). Bars, 5 μm.
DNA gives us much information about the diversity of the system, but if we wish to obtain information about the metabolic activity that is taking place in the ecosystem, metabolomic and metatranscriptomic approaches are needed [50, 66]. In the case of the atmosphere, this is crucial, since we are not fully certain if the cells present are active. Some studies indicate that a part of the microorganisms in the atmosphere are developing an activity [6], but until we conduct RNA-based and metabolite-based studies, we will not have the certainty that this is the case. The big problem is that it is very difficult to carry out these studies using the current microbial capture systems.
\nScanning electron microscopy (SEM) also provides much information of the aerobiology [7]. Specifically, it allows the characterization of eukaryotic cells (e.g., diatoms) and, above all, pollens and fungal spores, from which we can obtain great information with good images alone. \nFigure 6A\n shows pine tree pollen observed via SEM in a sample obtained after a 30 minutes flight of the C-212 aircraft.
\nSEM images of different airborne samples. (A) Pinus pollen. Ground sample after 2 hours sampling. (B) Air sample collected from C-212-200 aircraft during a Saharan dust intrusion (February 24, 2017). Filter appear completely cover of mineral particles. (B and C) Biological particles sampled using C-212-200 aircraft. (E) Diatomea sampled by C-212-200 aircraft in a fligth along the northern coast of Spain (9 March 2017). (F) Cell attached to mineral particles and organic matter.
As mentioned above, factors, such as the shortage of nutrients and substrates, high UV radiation, drying, changes in temperature and pH, or the presence of reactive oxygen species, make the atmosphere an extreme environment. However, it is possible that the high variability of its conditions is the one characteristic that makes this environment more extreme [1, 20]. Among the cells present in the atmosphere, a considerable portion appears in the resistance forms capable of withstanding low-temperature and high-radiation conditions. This is what probably happens with fungi and gram-positive bacteria. Bacillus strains recurrently isolated from the atmosphere have characteristics and a capacity to sporulate very similar to strains isolated from the soil. Undoubtedly, another part of the cells will be in the form of latency and may even suffer modifications of the cell wall and slow down or stop their metabolic activity [75, 76]. These transformations can improve resistance to physical stresses, such as UV radiation [58]. On the other hand, some of the bacteria present in the atmosphere, such as Geodermatophilus, show pigmentation that undoubtedly protects it from excessive radiation. The microorganisms that are usually detected in the atmosphere originate mainly from the soil, which means they will share similar mechanisms of resistance. In some strains, metabolic adaptations have been observed to lack nutrients such as cytochrome bd biosynthesis to survive iron deprivation [77]. Deinococcus is also a recurrent genus in the atmosphere, which, like those in soil, has multiresistance mechanisms based on high DNA-repair efficiency. Bacteria that do not form spores and certain archaea, in contrast, often have genomes rich in G + C, which may increase tolerance to UV rays and overall survival [78].
\nAnother strategy of resistance could be cell clustering and adhesion to particles. Several studies have confirmed the loss of viability and shielding or the reflective properties of the mineral particles as an important role for the protection of UV radiation [19, 31]. In that sense, it is very possible that many cells have mechanisms that promote aggregation. In our samples, we often find the cells adhered to each other or to minerals, which undoubtedly makes them more resistant (\nFigure 6\n).
\nGlobal and regional models have been used to explain bioaerosol emission, transport, and atmospheric impact [17, 18, 79, 80, 81, 82, 83, 84]. Even so, it is not an easy phenomenon to explain, since it depends on a large number of factors. On the one hand, there are numerous sources of tropospheric aerosols, which include sea salt, volcanic dust, cosmic dust, industrial pollutants, and desert and semidesert areas [6, 85]. We must also consider the factors that make the transfer of particles possible, for example, meteorological phenomena, solar radiation, temperature, tides, erosion, etc. [85]. On the other hand, anthropogenic activities can also affect dust emissions indirectly, by changing the climate and the hydrological cycle. In these aerosols, microorganisms will be included in a greater or lesser number. The degree of richness in cells of tropospheric aerosols will depend largely on the source of emission. Thus, the large wooded masses or fields of crops provide the atmosphere with a good number of microorganisms due to the effect of air or the aerosols produced by rain. Similarly, anthropogenic activity contributes large amounts of bacteria to the environment, treatment plants, and composting areas being sources of airborne microorganisms [85].
\nDesert dust storms play a major role in particle emissions and with them that of microorganisms. In this way, most of the material reaching the atmosphere from the surface comes from desert and semidesert areas, which is known as desert dust. The Sahara-Sahel desert, the Middle East, central and eastern Asia, and Australia are the major sources of desert dust, although all the arid zones of the world are emission sources [9, 86]. Dust storms are atmospheric events typically associated with dry lands due to the preponderance of dried and unconsolidated substrates with little vegetation cover. The strong and turbulent winds that blow on these surfaces raise fine-grained material, a large part of which consists of particles the size of silt (4–62.5 μm) and clay (<4 μm), reducing visibility to less than 1 km. The atmospheric concentrations of PM10 dust exceed 15,000 μg/m3 in severe events [87], although the concentrations naturally decrease with the distance from the areas of origin, extending hundreds of kilometers. The dust particles and cells associated with them are transported in this manner and will be deposited finally, by the effect of rain, snow, or other meteorological phenomena. Therefore, there is a continuous transfer of mineral and biological matter through the atmosphere that moves from the air to the terrestrial environment and changes its geographical area [7, 24].
\nThe Sahara-Sahel desert located in northwestern Africa is one of the major sources of windblown dust in the world [9]. This phenomenon has an impact on the Mediterranean coastline, but Saharan dust has been transported toward the north of Europe and has been found on numerous occasions in the Alps [88, 89] or blown toward the Atlantic and Caribbean [8, 90]. It has been estimated that 80–120 tons of dust are transported annually through the Mediterranean toward Europe [23, 91, 92]. In particular, dust transported by the winds can reach an elevation of up to 8 km in the atmosphere over the Mediterranean basin [93]. Because of its geographic position, the Iberian Peninsula is often affected by these dust events. Specifically, the Sahara-Bodele depression, located at the southern edge of the Sahara desert, has been described as the richest dust source reaching the Iberian Peninsula. Southern Spain is the main area affected, but dust can reach the Pyrenees and even France [43]. Different researchers have studied the mineralogical and chemical composition of Saharan dust, which has been observed to contain calcite, dolomite, quartz, different clay minerals, and feldspars as the main mineral components [94]. The intrusion of big amounts of these components is an important influence on nutrient dynamics and biogeochemical cycling in the atmosphere of the Iberian Peninsula.
\nDespite the large number of studies on dispersion, geochemistry, and mineralogy of African dust, few are focused on microbiology. All these studies conclude that there are microbes associated with dust because there are higher concentrations of aerosolized microorganisms during dust events [43, 90, 93, 94, 95, 96]. However, the magnitude of the concentrations and the specific microbes associated with dust events remain the subject of debate. On the other hand, the viability of these microorganisms is another big question. The United States Geological Survey (USGS) develops the Global Dust Program to investigate the viability of microorganisms transported in dust masses. USGS authors using DNA sequencing of the ribosomal gene were able to isolate and identify more than 200 viable bacteria and fungi in St. John’s samples in the USA [8, 36, 90]. Fungi and bacteria associated with atmospheric dust can be recovered and cultivated, but they must be gram-positive bacteria and many spore formers, which makes them resistant to the extreme conditions of the atmosphere.
\nTherefore, fungi and bacteria associated with dust may have been isolated from dust intrusions, but a percentage of the viable ones already remains an unanswered question. Another big question is the activity of these cells in the atmosphere. It is clear that they are resistant to extremophile conditions, but the question is whether they are developing their life cycle in this particular environment. This question could be answered by molecular ecology methodologies based on the isolation and sequencing of mRNA, but low atmospheric biomass and high variability are, once again, the great problem when developing this type of RNA-based methodologies. On the other hand, clinical records point to many of the viable microorganisms identified in the Saharan dust as the cause of respiratory diseases (asthma and lung infections or allergic reactions), cardiovascular diseases, and skin infections [7, 90, 97, 98]. It is known that other microbes associated with dust in the air are pathogenic to humans, including those that cause anthrax and tuberculosis, or to livestock (such as foot and mouth disease) or plants [7, 90, 97, 98]. Characterization, quantification, and feasibility studies are vital to address these problems.
\nIt is common to find fungal spores belonging to the genus Aspergillus, Nigrospora, Arthrinium, and Curvularia associated with Saharan dust. Bacterial taxa comprised a wide range of phyla, including Firmicutes, Proteobacteria, Actinobacteria, and Bacteroidetes. Generators of genus spores such as Clostridium and Bacillus are very common, along with other gram-positive ones such as Geodermatophilus or Streptococcus. Also, Alphaproteobacteria, a very common bacterium class in soils (e.g., the family Sphingomonadaceae), are associated with dust [4, 9]. As regards Archaea, there are few studies of the atmosphere, in general, and of dust, in particular, that focus on this domain. Surely, reduced cases of pathogenic archaea have been studied to a lesser extent. Aeropyrum is the most detected genus of airborne archaea, but it is related to marine aerosols [11]. On the other hand, studies of pollen associated with dust are widespread. An interesting study investigated pollen transported from North Africa to Spain through Saharan dust and found that pollen from five non-native plant species was detected exclusively during dust events [99]. Lastly, viruses and virus-like particles have a great interest in the emission of dust. One study mentions virus-like particles associated with a transoceanic dust event. This report is based on epifluorescent microscopy of filters stained with a specific nucleic acid stain. An increase in the order of magnitude of virus-like particles was observed, from 104 to 2105 m−3 between the baseline condition and dust conditions in the Caribbean [41]. It is speculated that free airborne viruses show worse resistance to high ultraviolet radiation and dry air associated with long-distance transport in dust events resist worse than others [9].
\nFour aerobiology sampling flights took place during February and March 2017 using the CASA C-212-200 aircraft from INTA. The study focused on microbial diversity in the atmosphere of the Iberian Peninsula during and after a Saharan dust intrusion. Flights took place under four different conditions: (1) during a strong Sahara dust storm that reached the north of the Iberian Peninsula, from February 22 to 24, 2017 (February 23, 2017) (\nFigure 7\n); (2) following precipitation (February 28, 2017); (3) following a dry period (March 8, 2017); and (4) along the northern coast of Spain (March 9, 2017). In each flight, samples were collected at different altitudes, and air samples were obtained simultaneously at ground level. A total of 20 samples were collected and are being analyzed. Cell presence was observed by scanning electron microscopy (SEM), and bacterial diversity is being studied by DNA extraction, 16S rRNA gene amplification, and Illumina MiSeq sequencing. Results are being analyzed via bioinformatics and biostatistical software (MOTHUR, SPSS, STAMP, CANOCO, and PAST) which will allow us to compare the results between the different flows and scenarios.
\nSaharan dust intrusion. Dust pours off the northweat Afrincan coast and blankets the Iberian Peninsula, 23 February, 2016. NASA satelital imagen via MODIS.
Although this study is not yet finished, some data can be advanced in this chapter. \nFigure 6\n shows SEM microphotographs obtained from samples in different scenarios. In general, the samples obtained during the days of dust intrusion (flight of February 23) appear completely covered with mineral particles. In these cases, more biological cells were detected than in the rest of the days. In the particular case of samples from the marine coast flight, more diatoms were observed (\nFigure 6E\n).
\nThe analysis of diversity using the Shannon index showed that, in all cases, diversity was greater on days of Saharan dust intrusion, both in the samples taken from the ground and those taken at higher altitudes with the aircraft. This indicates that Saharan dust contributes microorganisms that are not present in the atmosphere on a daily basis. Diversity analysis showed phylum characteristics of soils, being Alpha- and Betaproteobacteria the most abundant classes. All of the analyses performed showed that bacterial diversity detected at ground level and in-flight samples during the dust intrusion event were similar among one another. The genus taxonomic levels of Sphingomonas, Geodermatophilus, Methylobacter, Rhizobiales, Bacillus, or Clostridium were present in every sample, but their sequences were more abundant in the case of ground samples and dust intrusion samples collected during the day flight. However, sequences of the genus Flavobacterium, Streptococcus, or Cupriavidus were most abundant in the case of samples collected during flight.
\nPreliminary conclusions show that bacterial diversity of airborne bacteria during days of dust intrusion is higher and similar to bacterial diversity commonly detected in soil samples. Further analyses are being conducted with these samples to obtain a complete description of the evolution of bacterial diversity during those days.
\nIntense UV radiation, low pressure, lack of water and nutrients, and freezing temperatures turn the atmosphere into an extreme environment, especially its upper layers. However, it is widely known that airborne bacteria, fungal spores, pollen, and other bioparticles exist. Numerous bacteria and fungi have been isolated and can survive even at stratospheric altitudes. Microbial survival in the atmosphere requires extremophilic characteristics, and therefore airborne microbiota is potentially useful for biotechnological applications. The role of airborne microbial communities is vital in the Earth, including interactions among the atmosphere, biosphere, climate, and public health. Airborne microorganisms are involved in meteorological processes and can serve as nuclei for cloud drops and ice crystals that precede precipitation, which influences the hydrological cycle and climate. Furthermore, their knowledge is essential in understanding the reproduction and propagation of organisms through various ecosystems. Furthermore, they can cause or improve human, animal, and plant diseases.
\nAirborne platforms that allow conducting a direct study of microorganisms in the atmosphere and molecular methodologies (e.g., “omics”) could represent a major opportunity for approaching this question. Nevertheless, some challenges must yet be solved, such as low biomass, efficiency of sampling methods, the absence of standard protocols, or the high variability of the atmospheric environment.
\nDeserts and arid lands are one of the most important sources of aerosol emissions. Clouds of dust generated by storms mobilize tons of mineral particles, and it is known that microorganisms remain attached to the particles being transported over long distances. The large number of mineral particles and microorganisms thus placed into the atmosphere has global implications for climate, biochemical cycling, and health. North African soils, primarily the Sahara Desert, are one of the major sources of airborne dust on Earth. Saharan dust is often transported to southern Europe and could even reach high altitudes over the Atlantic Ocean and the European continent. Again, airborne platforms could be a perfect opportunity for conducting a direct study of the microbiology of this kind of events.
\nThis work has been supported by grants from the Spanish government (
IntechOpen implements a robust policy to minimize and deal with instances of fraud or misconduct. As part of our general commitment to transparency and openness, and in order to maintain high scientific standards, we have a well-defined editorial policy regarding Retractions and Corrections.
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\\n\\nA Retraction of a Chapter will be issued by the Academic Editor, either following an Author’s request to do so or when there is a 3rd party report of scientific misconduct. Upon receipt of a report by a 3rd party, the Academic Editor will investigate any allegations of scientific misconduct, working in cooperation with the Author(s) and their institution(s).
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\\n\\nA Statement of Concern detailing alleged misconduct will be issued by the Academic Editor or publisher following a 3rd party report of scientific misconduct when:
\\n\\nIntechOpen believes that the number of occasions on which a Statement of Concern is issued will be very few in number. In all cases when such a decision has been taken by the Academic Editor the decision will be reviewed by another editor to whom the author can make representations.
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\\n\\n3.1. ERRATUM
\\n\\nAn Erratum will be issued by the Academic Editor when it is determined that a mistake in a Chapter originates from the production process handled by the publisher.
\\n\\nA published Erratum will adhere to the Retraction Notice publishing guidelines outlined above.
\\n\\n3.2. CORRIGENDUM
\\n\\nA Corrigendum will be issued by the Academic Editor when it is determined that a mistake in a Chapter is a result of an Author’s miscalculation or oversight. A published Corrigendum will adhere to the Retraction Notice publishing guidelines outlined above.
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\\n\\nIntechOpen wishes to emphasize that the final decision on whether a Retraction, Statement of Concern, or a Correction will be issued rests with the Academic Editor. The publisher is obliged to act upon any reports of scientific misconduct in its publications and to make a reasonable effort to facilitate any subsequent investigation of such claims.
\\n\\nIn the case of Retraction or removal of the Work, the publisher will be under no obligation to refund the APC.
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\\n"}]'},components:[{type:"htmlEditorComponent",content:'IntechOpen’s Retraction and Correction Policy has been developed in accordance with the Committee on Publication Ethics (COPE) publication guidelines relating to scientific misconduct and research ethics:
\n\n1. RETRACTIONS
\n\nA Retraction of a Chapter will be issued by the Academic Editor, either following an Author’s request to do so or when there is a 3rd party report of scientific misconduct. Upon receipt of a report by a 3rd party, the Academic Editor will investigate any allegations of scientific misconduct, working in cooperation with the Author(s) and their institution(s).
\n\nA formal Retraction will be issued when there is clear and conclusive evidence of any of the following:
\n\nPublishing of a Retraction Notice will adhere to the following guidelines:
\n\n1.2. REMOVALS AND CANCELLATIONS
\n\n2. STATEMENTS OF CONCERN
\n\nA Statement of Concern detailing alleged misconduct will be issued by the Academic Editor or publisher following a 3rd party report of scientific misconduct when:
\n\nIntechOpen believes that the number of occasions on which a Statement of Concern is issued will be very few in number. In all cases when such a decision has been taken by the Academic Editor the decision will be reviewed by another editor to whom the author can make representations.
\n\n3. CORRECTIONS
\n\nA Correction will be issued by the Academic Editor when:
\n\n3.1. ERRATUM
\n\nAn Erratum will be issued by the Academic Editor when it is determined that a mistake in a Chapter originates from the production process handled by the publisher.
\n\nA published Erratum will adhere to the Retraction Notice publishing guidelines outlined above.
\n\n3.2. CORRIGENDUM
\n\nA Corrigendum will be issued by the Academic Editor when it is determined that a mistake in a Chapter is a result of an Author’s miscalculation or oversight. A published Corrigendum will adhere to the Retraction Notice publishing guidelines outlined above.
\n\n4. FINAL REMARKS
\n\nIntechOpen wishes to emphasize that the final decision on whether a Retraction, Statement of Concern, or a Correction will be issued rests with the Academic Editor. The publisher is obliged to act upon any reports of scientific misconduct in its publications and to make a reasonable effort to facilitate any subsequent investigation of such claims.
\n\nIn the case of Retraction or removal of the Work, the publisher will be under no obligation to refund the APC.
\n\nThe general principles set out above apply to Retractions and Corrections issued in all IntechOpen publications.
\n\nAny suggestions or comments on this Policy are welcome and may be sent to permissions@intechopen.com.
\n\nPolicy last updated: 2017-09-11
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