Contraindications to heart transplantation.
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More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
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Intraoperative management in heart transplant is quite complex and includes multiple steps from preoperative evaluation to ICU admission.
During this phase, we need to collect the consent from the patient after having explained to him all the possible complications coming from surgery, anesthesia, and ICU stay.
Above all, we need to know the background history of the patient, any previous issue with general anesthesia, allergies, difficult airway management, and any possible contraindication to the transplant itself [Table 1].
Absolute contraindications | Relative contraindications |
---|---|
Significant COPD (FEV1 < 1 L/min) | Age > 72 years |
Fixed pulmonary hypertension | Active infections |
PAPs >60 mmHg | BMI > 35 kg/m2 or <18 kg/m2 |
GTP > 15 mmHg | Creatinine clearance < 25 ml/min |
PVR > 6 wood units | Active mental illness or psychosocial instability |
Irreversible renal or hepatic dysfunction | Severe peripheral vascular disease |
AIDS/malignancy/lupus | Diabetes mellitus with end organ damage |
Contraindications to heart transplantation.
A multiorgan analysis must be taken into account:
Neurological history: syncopal episodes, carotid stenosis, ischemic or hemorrhagic stroke, transitory ischemic attack.
Respiratory history: smoke, COPD, spirometry, DLCO test.
Cardiovascular history:
origin of cardiomyopathy: dilated/hypertrophic/ischemic cardiomyopathy
noncompaction left ventricle (LV), sarcoidosis, amyloidosis, and others
arrhythmias: episodes of sudden cardiac death syndrome, implantation of an ICD
right side catheterization: pulmonary artery pressures (PAP), pulmonary capillary wedge pressure (PCWP), pulmonary vascular resistances (PVR), results of reversibility test with enoximone, origin of pulmonary hypertension (prepost capillary)
presence of prosthetic valves in situ
home medications: oral anticoagulants, ace inhibitors, b-blockers, diuretics
Renal history: chronic or acute renal failure, preoperative serum level of creatinine and urea, creatinine clearance, history of renal replacement therapy.
Hepatobiliary history: a systemic portal venous congestion can often derive from chronic congestive heart failure. In this case, high levels of transaminases and bilirubin may occur and this may influence the pharmacological and hemodynamic management during anesthesia.
Metabolic history: surgical stress and corticosteroid therapy may dramatically increase glycemia levels and hyperglycemia may dramatically increase the lactate levels during and after surgery; this is the reason why we need to know if the patient has diabetes and plan a proper blood glucose control with continuous infusion insulin (usually 50 UI/50 ml gelatin starting with a speed of 2–3 ml/h, depending on glucose plasma levels, with a target of 80–150 mg/dl). Among metabolic disorders, hypothyroidism can be further impaired during and after heart transplantation because plasma levels of triiodothyronine are often decreased during long periods of cardiopulmonary bypass, so that it’s important to plan an early replacement thyroid therapy.
Preoperative fasting: the patient should fast from food at least 8 hours and from fluids 4–6 hours before the operation.
Premedication: it’s important to avoid any preoperative oversedation since hypoxia may increase the pulmonary vascular resistances (PVR). We usually do not exceed a dose of 10—15 drops per os of diazepam in adult patients before going to theater, but, if the patient is really critical, we avoid any premedication.
Severe pulmonary hypertension in the recipient is one of the major contraindications to heart transplant [1, 2] due to high risk of right heart failure. When pulmonary hypertension persists up to 1 year from transplant, clinical outcomes and percentage of long-term survival are really poor [3]. For the above-mentioned reasons, a potential recipient must be evaluated with caution before being added to the waiting list. First of all, he needs to be sent for cath lab in order to evaluate his own pulmonary vascular resistances (PVR), mean pulmonary arterial pressure (m-PAP), pulmonary artery wedge pressure (PAWP), cardiac output (CO), cardiac index (CI), and the transpulmonary gradient (TPG).
This last equals the difference between mPAP and wedge pressure (TPG = mPAP − PAWP).
In case of high PVR (PVR > 3 wood units [WU]), it is important to perform the reversibility test with enoximone or dobutamine in order to quantify the reversibility degree of pulmonary hypertension. When postcapillary pulmonary hypertension (defined as mPAP ≥ 25 mmHg, PAWP > 15 mmHg and PVR > 3WU) is unresponsive to dobutamine reversibility test (i.e., PVR > 3 WU or mPAP > 35 mmHg with a TPG > 12 mmHg), a team made of cardiologists, anesthesiologists, and cardiac surgeons should seriously evaluate if the patient is suitable for receiving a new heart.
A preventive treatment with pulmonary vasodilators such as sildenafil should be considered since it has been shown to decrease the PVR in a period of few months [4].
A preventive treatment with sildenafil should also be considered when patients are scheduled for receiving an LVAD positioning as bridge to transplant, thanks to its effectiveness in long-term reduction of the PVR and major responsiveness to a further test with dobutamine [5].
Timing to get the patient ready to receive the new organ is crucial because the ischemia of the donor heart should be as short as possible to avoid the ischemia-reperfusion injury.
Everyone in the theater should wear sterile surgical gown, hat, mask, and sterile gloves for any procedure on the patient especially because he will go under immune deficiency. Once the patient is in the theater, he will be connected to multiparametric monitor, with the 12 lead ECG and oximetry probe. Two peripheral venous lines are placed (generally 18G for iv sedation and 14G for rapid fluid infusion), and an arterial catheter, generally 20G, is placed into the radial or humeral artery. When the patient is very unstable, an arterial catheter is placed in the left femoral artery, to estimate central to peripheral arterial pressure gradients. Placement of an arterial line can be very difficult in patients with previous implantation of LVADs as bridge to transplant, due to the absence of arterial pulse. In such situations, ultrasound guidance can be very helpful (see Table 2).
Device | Measure |
---|---|
PA radial | Invasive arterial pressure (peripheral) |
PA fem | Invasive arterial pressure (central) |
CVP | Central venous pressure |
ECG | 12 lead electrocardiography |
SpO2 | Oxygen saturation levels |
PAC | (pulmonary artery catheter) PAPs, PAPm, PAPd, sVO2 |
TEE | Biventricular function, shape of ventricular septum, filling, air etc. |
NIRS | ScvO2 correlation, adequate tissue perfusion, brain perfusion |
LAP | LV filling pressure |
Standard monitoring.
Induction of general anesthesia usually starts just with the final acceptance of the donor organ. Drugs used for general anesthesia should impact the less possible on hemodynamics. A rapid sequence induction is preferred since recipients are always very stressed and sometimes not present with an empty stomach [6].
Midazolam (10–15 mg) or etomidate (20 mg) are preferred to propofol for hypnosis, due to the less impact on hemodynamics. Opioids like fentanyl or sufentanil are preferred for the same reason (“stress-free anesthesia”), with an induction dose of 0.2–0.4 mcg/kg for sufentanil and 2–4 mcg/kg for fentanyl. Continuous infusion analgesia remifentanil is preferable for the less impact on renal function since it is metabolized by plasmatic esterase. This is particularly important in patients with low cardiac output and preexisting renal failure. Remifentanil will be turned off and replaced by morphine or tramadol (30 mg/die and 300 mg/die, respectively), before moving to the intensive care unit. Mean term muscle relaxant rocuronium (1 mg/kg) is usually the first choice for rapid sequence induction. Sometimes short-term cisatracurium besylate (0.15–0.2 mg/kg for induction and 1–2 mcg/kg/min for continuous iv infusion during surgery) is a good alternative since it is metabolized by ester hydrolysis and Hofmann reaction, so the duration of block is not affected by renal or hepatic function. During induction of general anesthesia, severe hypotension can occur, so that a fluid iv bolus ad availability of rapid onset vasoconstrictors as metaraminol, phenylephrine, noradrenaline should be ensured. Cardioplegia is not administered in the recipient during heart transplantation, so that the risk of related hemodilution is less than routine cardiac surgery. On pump, sevoflurane or iv 2% propofol infusion (4 mg/kg/h) are the options for maintenance of general anesthesia. Monitoring the depth of anesthesia with bispectral index (BIS) should be routinely adopted in order to decrease the risk of awareness. Once having put the patient asleep, central lines must be placed (queen central venous pressure [CVP] line and 8 Fr line for the pulmonary artery catheter [PAC]). The ideal site for puncture (blind or ultrasound-guided) is the left internal jugular vein (IJV), since the right one can be reserved for eventual postoperative biopsy (necessary to evaluate the level of graft rejection). When this is not possible (presence of ICD on the left side), we can adopt the right subclavian vein. Sometimes, when the preoperative renal function is really compromised, we can already place into the femoral or subclavian vein a catheter for continuous renal filtration afterwards. The PA catheter is flown through the 8 Fr line up to the right atrium, and then, once the new heart is placed, it will be advanced by the cardiac surgeon up to the superior right pulmonary artery. Vigilance calibration will be done immediately before weaning from the CPB.
If the graft is not carried out into the organ care system (OCS), the ischemic time is crucial and the risk of ischemic/reperfusion injury is proportionally high, with possible dramatic increase of blood lactate levels and decrease of the graft global function. This is the reason why we must ensure adequate glycemia control, urine output, and, in general, an optimal tissue perfusion during CPB. This means to guarantee an adequate oxygen delivery (DO2), which means to keep MAPs about 60–80 mmHg and Hb levels at least about 8–9 mg/dL. When the aorta is unclamped, VF can occur (50% of patients). A shock delivery (10–30 J) followed by lidocaine bolus (when VF is refractory to electrical therapy) will take to resolution of the arrhythmia and return to sinus rhythm. In case of sinus bradycardia, temporary epicardial pacing will ensure adequate heart rate (100–110 bpm). Due to limited muscular mass, the ability of the right ventricle (RV) to increase contractility is limited and a temporary pacing at about 110 bpm will increase RV output and will overpace possible arrhythmias. Surgeons will also place a left atrial catheter for continuous measurement of the left atrial pressure (LAP) as an indicator of the left ventricle performance and stiffness. This value, together with CVP, PAPs, MAPs, and SvO2, will influence the posttransplantation hemodynamic management. Throughout this period, it will be mandatory to ensure adequate MAPs and diastolic pressure to allow adequate coronary perfusion, while maintaining medium-low preload pressures (CVP < 12 mmHg, LAP/PCWP < 12 mmHg). The biventricular assessment with transesophageal echocardiography should be done simultaneously.
Pharmacological tools for CPB weaning will include the following [Tables 3 and 4]:
Isoprenaline at low-moderate dose (0.02–0.04 mcg/kg/min): it is the first choice in heart transplantation due to the positive chronotropic effect; it helps to guarantee a heart rate of 100–110 bpm. If it does not work, do not go beyond 0.04 mcg/kg/min, in order to avoid hypotensive effects. In this case, switching to atrial pacing is the best choice.
Adrenaline (0.02–0.2 mcg/kg/min): it provides inotropic support to the new heart, especially to the right ventricle, which is the one more at risk of failure.
Milrinone (0.2–0.5 mcg/kg/min) or other phosphodiesterase inhibitors (enoximone at 5–8 mcg/kg/min): they increase contractility especially of the right ventricle, while decreasing pulmonary vascular resistances. They both increase intracellular levels of cAMP, but they also decrease the systemic vascular resistances (SVR), so that the patient may benefit from low-moderate noradrenergic support in addition. If systemic peripheral resistances are really low, selective pulmonary vasodilators, aimed to decrease RV afterload without affecting peripheral resistances, are a better choice: inhaled nitric oxide (iNO) at 20–40 ppm [9, 17]) or aerosolized prostaglandins (iloprost 20 mcg/15 min, repeated after 4 hours).
Possible side effects of these selective inhalation drugs are inhibition of platelet activation and aggregation and inhibition of leucocyte adhesion.
Levosimendan (0.1–0.2 mcg/kg/min) has also been reported to reverse low cardiac output after heart transplantation [10], although its use has not been shown to reduce cardiac surgery mortality [11].
Sustain SVR and arterial pressure (if necessary) | Norepinephrine vasopressin |
Maintain DO2 level 272 ml/min/m2 | Raise in pump flow Raise Hb level Raise O2 sat Decrease body temp |
Support graft | Milrinone (0.2–0.5 mcg/kg/min) Dopamine (4–6 mcg/kg/min) Epinephrine (0.05–0.25 mcg/kg/min) |
Hb level | 11 g/dl |
Maintain regular rhythm and A-V synchrony 110 bpm | K+/Mg+ Pacing Isoprenaline (0.02–0.04 mcg/kg/min) |
Pacing with 110–120 bpm | Increase of HR increases CI, avoid overload |
Reduce PVR (if necessary) | iNO (20–40 ppm) Inhalatory iloprost (10–20 ng) Inhalatory milrinone (5 mg) for 15 min |
Slowly reduce CPB flow (careful monitoring CVP, TEE, LAP) | Check/change drug infusion rate Check chamber filling Check contractility |
Practice guide to wean from CPB.
Drug | Average dosage | Advantages | Side effects |
---|---|---|---|
Epinephrine | 0.05–0.25 mcg/kg/min | Support RV overload | Tachycardia, arrhythmias, raise O2 demand |
Norepinephrine | Up to 0.15 mcg/kg/min | Contrast vasodilatation | Increase PVR |
Levosimendan | 0.1–0.2 mcg/kg/min | Support RV overload | Vasodilation |
Milrinone | 0.2–0.5 mcg/kg/min | Support RV overload | Arrhythmias, raise O2 demand, vasodilation |
Vasopressin | 2.5–5 U/h | Contrast vasodilatation | Increase SVR impair forward flow of LVAD |
i-NO | 20–40 ppm | Reduce PVR (if not fixed) | |
i-Milrinone | 5 mg/15 min | Reduce PVR (if not fixed) | |
i-Iloprost | 20–30 mcg/15 min | Reduce PVR (if not fixed) | |
Methylene blue | 0.5–2 mg/kg | Contrast vasodilation |
Inotropes/vasoactive: average therapeutic dosage to support hemodynamics.
After having unclamped the aorta and before weaning from CPB, about 1 hour of assistance to the new heart is provided. During this period, an adequate temperature is achieved (36–36.5°C measured by nasopharyngeal temperature probe). Vigilance calibration is performed by providing Hb levels and SvO2 from gas analysis; it gives results about the indexed cardiac output, pulmonary vascular resistances, and systemic peripheral vascular resistances, indexed on the patient weight. PAPs are shown on the monitor together with CVP, LAP, MAPs, and ECG. The PAVR (pulmonary artery vascular resistance) equals: PAVR = [80 × (mean pulmonary artery pressure – pulmonary + capillary wedge pressure)/cardiac output] (normal value 100 dynes/cm−5).
The TPG (transpulmonary gradient) equals: TPG = mPAP − PCWP (normal value 6 mmHg).
A TPG > 15 mmHg is considered at high risk to develop early postoperative RV dysfunction [7]. The reason for RV dysfunction development may be found in the background of the donor heart. Especially when young and comparably small, it may not easily adapt to the already existing pulmonary hypertension in the recipient. Furthermore, as a result of a long ischemia and CPB time, with ischemia-reperfusion injury, RV dilates, becomes ischemic, and further reduces its own contractility. In this case, we need to adjust the amount of inotropes, chronotropes, and pulmonary vasodilators given, basing also on transesophageal echocardiography that can show the biventricular systolic-diastolic function and fluid responsiveness. Once the patient is stable and the heart rate is appropriate, we can start ventilation and slowly decrease the pump flow until 0.5–1 L/min. At that point, we come out from bypass. During CPB weaning, the heart should be loaded with caution because RV is very sensitive to distension. Echocardiographic parameters to asses the RV behavior will be RVFAC (fractional area change), leftward shift of IAS (interatrial septum) or “fluttering” of IVS (interventricular septum) during end-diastole, TAPSE(tricuspid annular plane systolic excursion), and MPI (myocardial performance index).
Basic ventilation strategies to reduce pulmonary artery resistances such as hyperoxia and moderate hyperventilation are mandatory. Ventilation should be set at 60–100% FiO2, 6–8 ml/kg TV (tidal volume), and low-moderate PEEP (5–6 cmH2O), after recruitment maneuver, with the intention to prevent lung atelectasis [12].
Chest closure can be very critical for hemodynamics. In some rare cases (i.e., 2.5%), primary graft failure can occur [13], and it is responsible for more than 30% of early deaths after cardiac transplantation. Clinical onset of primary graft failure is with hypotension, low cardiac output, high preload pressures (PVC, LAP, and wedge pressure), and biventricular failure. When necessary, a temporary IABP (intra-aortic balloon pump), as first step, and then peripheral (femoral vein-femoral artery) or central (left atrium, right atrium, aorta) VA-ECMO (venous-arteriosus extracorporeal membrane oxygenation) should be taken into account, whenever hemodynamics remain unsatisfactory despite high inotropic support (Table 5) [14].
Inotropic score | Dopamine (μg/kg/min) + dobutamine (μg/kg/min) + 100 × epinephrine (μg/kg/min) |
Vasoactive inotropic score (modified by Davidson et al. with inclusion of vasoactive medication | IS + 10 × milrinone (μg/kg/min) + 10 × vasopressin (U/kg/min) + 100 × norepinephrine (μg/kg/min |
Vasoactive inotropic score plus levosimendan | VIS + 10 × levosimendan (mcg/kg/min) |
Poor clinical outcome | VIS 20–24 (in the first 24 h) + VIS 15–19 (in the subsequent 24 h) |
Inotropic score.
Fluid management should be “goal directed,” that is, guided by the above-mentioned hemodynamic and echocardiographic parameters, and with the aim to avoid a fluid overload, which is very harmful for the lungs and the right ventricle, while providing adequate intravascular space filling. This should be done via balanced colloids and crystalloids in order to avoid electrolyte disorders and hyperchloremic hyperkalemic metabolic acidosis. Adequate oxygen delivery is ensured by maintaining the hemoglobin level around 10–11 g/dL and an adequate plasma oncotic power is ensured by giving the right amount of albumin.
To go on CPB, we need to provide an appropriate anticoagulation via unfractionated heparin (300–400 U/kg). A value of ACT at least of 480 s is enough to start the extracorporeal circulation. In case of low response to a full dose of heparin, we can achieve an adequate ACT by administering antithrombin III (AT3), especially when AT3 plasma levels are less than 70%. From 0.5 to 5% of patients with end-stage heart disease can develop HIT (heparin-induced thrombocytopenia), due to repeated heparin exposures related to the placement of IABP, LVADs, or frequent catheter procedures. Alternative anticoagulation, with direct thrombin inhibitors (bivalirudin and argatroban), [8] is recommended in such patients. At the end of organ implantation, once the aortic and right atrium cannulas are removed, we need to guarantee an appropriate heparin reversal with protamine (50 mg of protamine every 50 mg of heparin). We also give the patient 2 g of tranexamic acid at the induction of general anesthesia and 2 g (25–50 mg/kg) with protamine in association with 1 g of gluconate calcium, to avoid hyperfibrinolysis and replace calcium deficiency. Severe bleeding is not a rare condition especially in patients with previous heart surgery. Particularly, in patients with LVADs as bridge to transplant, severe bleeding can often occur due to the large wound area and pretreatment with multiple anticoagulants and platelet inhibitors. If hemostasis is insufficient and the patient is still bleeding, we need to check for coagulation disorders via ROTEM (i.e., hyperfibrinolysis, coagulation factor deficiency, and hypofibrinogenemia) or via TEG and correct the specific deficiency (prothrombin complex concentrate for clotting factor deficiency or fibrinogen concentrate for hypofibrinogenemia). We prefer this approach instead of large dose of fresh frozen plasma, in order to avoid TACO (transfusion-associated circulatory overload), TRALI (transfusion-related lung injury), immune modulation, and increased risk of infections.
Almost 90% of heart transplants are due to ischemic or dilatative cardiomyopathy and men over 40 years of age are the most involved. They all need a special care and a multimodal approach, even because not only cardiovascular balance but also respiratory care, fluid management, and immune system modulation impact on the overall survival.
Patients incoming from the operating room have to be placed in an isolated single bed room to avoid contamination, since they will undergo immunosuppressive therapy. Everyone in contact with them must wear mask, cup, and sterile gown and do routine sterile hand washing. Invasive hemodynamic monitoring, including systemic arterial pressure, right atrial pressure, pulmonary artery pressure through the PAC, and left atrial pressure, should be immediately reconnected in the room.
Twelve lead ECG at the arrival is mandatory to check heart rhythm disorders. Bradyarrhythmias and supraventricular arrhythmias are the most frequent and should be related to inotropic and chronotropic support, hypovolemia, and electrolyte disorders. If atrial fibrillation occurs, an acute rejection should be considered and a 500 mg bolus of methylprednisolone should be administered, eventually followed by amiodarone (300 mg iv bolus in 30 min) for pharmacological cardioversion and rate control. In case of failure of pharmacological cardioversion, we can try electrical cardioversion. Sinus bradycardia can be treated with low-dose isoprenaline (0.01–0.04 mcg/kg/min), adrenaline (0.01–0.04 mcg/kg/min), and/or temporary atrial pacing, in order to ensure a heart rate about 100–110 bpm. In case of severe AV block, a sequential pacing is required. Anyway, if the patient is still pacing dependent after 2 weeks from the operation, implantation of a permanent pace maker should be considered. Then, you can proceed to request chest X-ray to check the lungs, endotracheal and nasogastric tube position, chest drains, and intravascular devices (CVP line, PAC, and pacing wires) and send for laboratory tests including standard coagulation, renal and liver function, platelets, red blood cell and white blood cell counts, troponin I, CK, albumin, viral markers, thyroid markers, and glycaemia. Blood samples should be sent for good practice also for coagulation tests (ROTEM or TEG) in case of excessive bleeding. A plan for immunosuppressive therapy (methylprednisolone, thymoglobulins, etc.) must be provided in collaboration with specialist immunologist and cardiologist. Antibiotic therapy must be tailored on the background history of donor and/or recipient.
Hemodynamic stability, after heart transplant, may be impaired by several pathophysiological processes, including autonomic denervation, with subsequent chronotropic and inotropic failure, ischemia reperfusion injury, metabolic acidosis, and volume depletion. To support such effects, several endpoints must be taken into account:
A goal-directed therapy is the ideal way to ensure adequate fluid filling. It means using the above-mentioned hemodynamic parameters coming from invasive monitoring and from echocardiographic evaluation, to be guided in the fluid replacement. Once the need of fluids is clear, the physician should decide the most ideal fluid in order to avoid peripheral organ oncotic damage (i.e., hyperoncotic kidney failure from hydroxyethyl starches [15]); hyperchloremic hyperkalemic acidosis, which can impact itself on kidney function; and fluid overload into the interstitial space. Crystalloids have a less oncotic power than colloids; however, albumin can cross the pulmonary capillary membrane, if damaged, and anyway it can recirculate through the pulmonary barrier 24 hours from the administration: then balanced crystalloids and balanced colloids (albumin solution at 5 or 20%) should be given at the right per kilo amount and the fluid responsiveness should be tested while they are given.
During the recovery period (approximately 7–14 days), a narrow monitoring of hemodynamic and vital parameters is mandatory: IBP, CI, CO, ISVRI, IPVR, PAPs, HR, SvO2, LAP/PCWP, TPG, SpO2, ECG, body temperature, urine output, and lactate levels.
Target values are: CVP ≤ 12 mmHg, MAP > 65 mmHg, LAP 8–12 mmHg, SvO2 over 65%, HR about 100–110 bpm, urine output > 1.5 ml/kg, and lactate < 2 mmol/L.
The goal is to ensure adequate CO, avoiding excessive increase of cardiac preload and afterload, while maintaining adequate heart rate. Chronotropic support is achieved through low-moderate dose of isoprenaline or by atrial-sequential external pacing. Inotropic effect is achieved through moderate-high dose of adrenaline and, when necessary, with phosphodiesterase inhibitors as milrinone that also decreases peripheral vascular resistances. Other pharmacological tools that are aimed to control arterial ventricle coupling are nitroglycerin and sodium nitroprusside, very helpful to decrease the afterload of the left ventricle and increase cardiac output, when used together with an inotropic drug. In case of preexistent pulmonary hypertension, inhalation of nitric oxide and imbrication with sildenafil can help to reduce pulmonary vascular resistances [14]. In the further postoperative course, addition of an upstream therapy including ace inhibitors, b-blockers, or calcium antagonists may be helpful as cardiac protection.
The donor heart, particularly the right ventricle, in case of preexisting precapillary or postcapillary pulmonary hypertension, has to fight with high afterload [Table 6]. The preexisting conditions may be impaired in case of coexisting hypoxia or hypercapnia, prolonged extracorporeal circulation, and donor ischemia with consequent ischemia-reperfusion injury, blood transfusion, and protamine administration. Right ventricular failure may be challenging and really impacts on the overall survival of transplanted patients [18].
Monitor by PAC | CVP, MPAP, PCWP, CO, SvO2 |
---|---|
Mechanical ventilation | PaO2 100 mmHg, pCO2 30–35 mmHg, pH 7.5. Adequate peep level (5–10 cm H2O) to recruit lung and optimize PVR |
Restricted fluid therapy | Monitoring filling pressure CVP 10–12 mmHg, PCWP 12–15 mmHg Monitoring LVEDV, RVEDV by echocardiography |
Inotropes to support RV contractility | Epinephrine 0.02–0.25 mcg/kg/min |
Inodilator | Milrinone 0.2–0.5 mcg/kg/min Levosimendan 0.2 mcg/kg/min ± norepinephrine (up to 0.15 mcg/kg/min) to maintain right coronary perfusion pressure |
iNO | 5–40 ppm |
Phosphodiesterase V inhibitor | Revatio 3 × 20 mg p.o. |
Systemic vasodilators | Sodium nitroprusside, prostacyclin PGI2 analogon iloprost (2 ng/kg/min) |
Pulmonary artery hypertension monitoring and right ventricular dysfunction prevention.
Early PA pressure monitoring at the time of CPB weaning is fundamental and has to be continued in the early postoperative period. The first aim in hemodynamic management of the graft is to offload the right ventricle, decreasing PA pressures and pulmonary vascular resistances while ensuring an adequate RV contractility. Inhaled nitric oxide at 20–40 ppm is a rapid onset tool to decrease PA pressures. It seems to improve early clinical outcomes in heart transplanted patients, but literature is still lacking in terms of overall survival [9].
This is the reason why it is often used preventively during weaning from the CPB. Alternatively, the prostacyclin analog iloprost (6 × 5–10 mcg) can be given.
After the very early postoperative period, inhaled nitric oxide can be substituted by the phosphodiesterase-5 inhibitor sildenafil at the dosage of 20 mg × 3/die via NG tube with very small effects on the systemic pressures, avoiding also the rebound phenomena coming from the discontinuation of inhaled nitric oxide therapy. Sildenafil has also been shown to decrease PA pressures during inhalation of nitric oxide, since they seem to activate different regulatory mechanisms of the vascular tone [19, 20]. Inotropic support of the RV should be guaranteed by moderate-high dose of adrenaline (0.05–0.1 mcg/kg/min) or low-moderate doses of phosphodiesterase inhibitors as milrinone (0.2–0.3 mcg/kg/min).
Clearly, while supporting the right ventricle, we need to ensure adequate oxygenation, avoid hypercapnia, maintain adequate lung recruitment by PEEP (not over 6 cmH2O), and guarantee a negative fluid balance in order to reduce the preload and optimize the afterload [Table 6]. If all these maneuvers are not sufficient, we have to consider a temporary mechanical right ventricle support via peripheral VA-ECMO.
In case of concomitant LV insufficiency and signs of systemic hypoperfusion (with raising of LAP/PCWP and sudden reduction of CO, CI, and SvO2), we will need to increase the inotrope support and try to compensate the peripheral vasoconstriction with peripheral vasodilators as nitroprusside, when the MAPs allow to do that, in order to reduce left ventricle afterload and facilitate the ejection. The conditioning with inodilators as levosimendan [10] can be very helpful and, in case of massive peripheral vasodilatory response, it can be compensated with mean dosage of noradrenaline to ensure adequate MAPs. When this is not enough, an additional support with IABP should be considered, but, when insufficient, a central or peripheral VA-ECMO will be placed. The simultaneous presence of the IABP will help avoid pulmonary edema by reducing the afterload of LV.
A patient undergoing heart transplant comes from a long period of low cardiac output, so the kidney dysfunction is often preexisting.
In the immediate postoperative period, urinary output may decrease for several reasons including intravascular volume depletion and kidney damage coming from long lasting extracorporeal support or from the use of unbalanced solutions for fluid challenge. In addition, a high use of colloidal molecules may damage directly the renal tubules with a process called “osmotic-nephrosis.” If urine output is <0.5 ml/kg/h despite optimization of blood pressure, preload and CO, and use of standard diuretics (furosemide or torasemide), and the patient develops kidney failure with serum urea >200 mg/dL or hyperkalemia, kidney replacement therapy becomes mandatory.
We prefer early application of continuous venovenous hemofiltration (CVVH) for a complete hemodynamic and fluid rebalancing. In case kidney replacement therapy is necessary in a long-term postoperative period, the change is made to intermittent dialysis (three times weekly).
At first, we may exclude significant pericardial collection, assess left ventricle diastolic function of the new performing heart, related to its stiffness and hypertrophy, and think about which wedge pressure we are expected to find [21]. If the systolic function of the new heart is failing, we should exclude an acute graft rejection. Regarding the right ventricle, we must know the recipient preoperative pulmonary vascular resistances, if pre- or postcapillary pulmonary hypertension persists and if it is reversible with phosphodiesterase inhibitors.
RV dysfunction is identified early with a dilation of the right chambers, alteration of interventricular septum movement, and appearance of tricuspid valve insufficiency.
A patient undergoing heart transplant should remain under mechanical ventilation until hemodynamic stability is ensured, lactate levels are stable, and immunosuppressive therapy is started. To protect the lungs, we have to limit peak pressures and use low tidal volumes (6 ml/kg) with adequate PEEP level (at least 3–5 cmH2O).
However, disadvantages coming from permissive hypercapnia on the pulmonary vascular resistances and right ventricle afterload, myocardial function, and renal blood flow loads must be taken into account [16]. As a consequence, there are no universal evidences, but the choice must be tailored for the patient. The only certainty is we must avoid hypercapnia, hypoxia, and PEEP over 10 cmH2O and keep peak pressure under 35–40 cmH2O.
During mechanical ventilation, inhaled nitric oxide can be administered in order to reduce right PA pressures, pulmonary vascular resistances, and then right ventricle afterload, especially in the first 24 hours from CPB weaning at the maximum dosage of 20–40 ppm [17, 18]. Once mechanical ventilation is discontinued, inhaled nitric oxide can be substituted by iv or oral pulmonary vasodilators as sildenafil. The weaning criteria do not differ from those used in normal cardiosurgical patients, and the goal is the same: maintain adequate analgesia and sedation levels and wean the patient from the mechanical ventilation as soon as possible. If this is not possible, due to unstable hemodynamics, high inotropic score, respiratory failure, or neurological issues, a percutaneous dilatation tracheostomy will be packaged without further delay (within the first 5–7 days of mechanical ventilation).
Once the patient is awake and self-breathing and the LAP line is removed (generally 24–48 hours from surgery), the patient will need physiotherapy and mobilization.
Early feeding is important. It is initially given via NG tube (25–30 kcal/kg/day) and then self-feeding is achieved once there is no more gastrointestinal paresis.
Standard prophylaxis is due to cefuroxime 2 g iv every 6 hours in the first 24 hours from heart transplantation (the first two boluses are given in the operating room, at the induction of general anesthesia and once CPB is started). The amount of antibiotic given in the ICU should be tailored for the patient’s creatinine clearance, especially if the patient is not under renal filter. Further extension and change of antibiotic therapy should depend on microbiological results of the donor and on microbiological samples of the recipient once admitted in the ICU. Furthermore, in case of redo-operation with existing wound infection, the patient will receive vancomycin and meropenem as standard medication and vancomycin plasma levels should be tested daily. Obviously, due to the immunosuppressive therapy, transplanted patients are very prone to infections. Delivery of care should be done in sterile conditions and, besides standard iv antibiotic therapy, topical antifungal medications should be given in the early postoperative period.
A specific team is taking care of immunosuppressive therapy. It starts with 500 mg iv bolus of solumedrol at the CPB weaning. Once admitted in the ICU, the patient will receive 125 mg bolus of solumedrol every 8 hours, with a specific descending dose scheme.
Antithymocyte globulines (1.5 mg/kg iv) are usually given 4, 24, and 48 hours after the end of the transplantation. They will be adjusted based on eventual presence of high body temperature, bleeding, and thrombocytopenia. There are several possible immunosuppressive agents that will be tailored for the patient such as tacrolimus, cyclosporin A, everolimus, and mycophenolate.
An international consensus conference in 2014 has classified the graft dysfunction into primary graft dysfunction (PDG) and secondary graft dysfunction (SGD). The first one occurs 24 h from heart transplant and can involve the left, the right ventricle, or both, with different degrees of dysfunction. Typical signs are severe deficit of systolic function, low cardiac output, and high filling pressures without evidence of acute graft rejection or cardiac tamponade. The SGD has a specific reason such as acute rejection, pulmonary hypertension, or surgical complications. Risk factors to develop PGD may be related to the recipient, donor, or technical factors [22].
Donor-related risk factors may be:
Age (increased risk of 20% every decade)
Sex (nearly doubled risk with female)
Recipient-related risk factors may be:
High vasoactive or inotropic support (doubled risk)
Uncontrolled diabetes (doubled risk)
Technical risk factors are:
Warm ischemic time (= explant time + implant time); implant time was found to be a strong predictor of PGD.
Resternotomy (it has been identified as a risk factor for severe PGD due to adherences and tissue fibrosis that can extend the explant time and increase the risk of infections).
Prolonged CPB time, with subsequent systemic inflammatory response, vasoplegia, clotting and platelet dysfunction, leukocyte activation, free oxygen radical release, and larger amount of blood products given.
All these factors can increase the ischemic-reperfusion injury and the overall mortality [23].
The first step to treat a PDG is vasoactive and inotropic support. If it were not sufficient, an intra-aortic balloon pump (IABP) placement may help.
In case of very severe PGD, an extracorporeal membrane oxygenation (ECMO) becomes the only emergency treatment.
Pediatric heart transplant represents a small subgroup (14%) of total cardiac transplant where the differences in anatomy and physiology make the surgical procedure and the management more complex and creates a unique scenario [24].
The management of pediatric patients undergoing cardiac transplantation differs from the adult patients because it requires a specific knowledge of physiology and physiopathology at different stages of growth, from the newborns through childhood up to adulthood.
This heterogeneous population with a wide range of age, genetic disorders, anatomical anomalies, and symptoms can be classified in four different groups based on the different etiology: 1—CHD (congenital heart disease); 2—DCM (dilated cardiomyopathy); 3—RETX (retransplant); 4—OTHER (Table 7) [25]; each of these has specific features.
Category (abbreviation) | Diagnoses in category |
---|---|
Congenital heart disease (CHD) | Congenital heart defects: HLHS-unoperated, with surgery, without surgery, valvular heart disease |
Dilated cardiomyopathy (DCM) | Dilated myopathy due to alcohol, familiar, idiopathic, myocarditis, viral, postpartum, etc. |
Retransplant (RETX) | Due to acute rejection, coronary artery disease, etc. |
Other (OTHER) | Arrhythmogenic right ventricular dysplasia, cancer, coronary artery disease, myopathy-ischemia, hypertrophic cardiomyopathy, etc. |
Diagnosis for pediatric heart transplant.
The preoperative evaluation is an essential step in order to better analyze both the cardiac pathology and the possible related comorbidities.
Main preoperative features and examinations that must be considered are:
Type of heart disease (CHD, DCM, RETX, and OTHER)
Right heart catheterization (RHC): pulmonary artery pressure (PAP), pulmonary capillary wedge pressure (PCWP), pulmonary vascular resistances (PVR), and pulmonary hypertension etiology. Unfortunately, most patients with congenital heart defects have high PVR because of pulmonary vascular disease. However, the presence of systemic-to-pulmonary shunts, intrapulmonary shunting, and caval pulmonary circulation does not allow a correct assessment of PVR. For these patients, RHC should be performed at 3–6 month interval in adult patients but is not advocated as routine surveillance in children unless a clinical change is noted [26].
Numbers and types of previous operations (sternotomy and thoracotomy).
Cyanotic congenital heart disease (secondary erythrocytosis, hyperviscosity, and coagulation deficit).
Panel reactive antibody (PRA) identifies sensitized patients. It may be elevated in patients with allograft patch or with multiple redo-operations, due to the multiple transfusions. It may result in an increased risk of acute rejection [27].
Variable anatomic substrates (isomerism, issues of situs, MAPCAs, aberrant right or left subclavian artery, and persistence of left superior vena cava).
Previous venous or arterial thromboembolism (central venous catheter thrombosis).
Previous neurological history: syncope, previous stroke, and cerebral arteriovenous malformation.
Respiratory insufficiency: smoke, chronic obstructive pulmonary disease (COPD), anatomical anomalies of the pulmonary vessels, and presence of bronchial or pulmonary stents.
Arrhythmias and previous ICD implantation.
Liver disease: an evaluation of the patient’s liver profile is extremely important. Chronic heart failure and in particular the univentricular heart physiology can lead to a liver dysfunction.
Fontan-associated liver disease (FALD) is a liver dysfunction due to a chronic elevated central venous pressure, low cardiac output, persistent hypoxemia, and intrahepatic venous thrombosis. FALD can be expressed in different stages, from moderate hepatic congestion up to liver cirrhosis with portal hypertension. In several cases, liver function is preserved or is only slightly altered, with high international normalizer ratio (INR), low factor V levels, and elevated factor VIII levels [28].
Kidney disease: acute or acute-on-chronic renal dysfunction.
Coagulation anomalies may be present as result of chronic anticoagulation, liver disease, or as a result of cyanotic congenital heart disease (reduced levels of coagulation factors II, V, VII, IX, and X, accelerated fibrinolysis, and fibrinogen alterations).
Gastrointestinal disorders: necrotizing enterocolitis in newborns or protein losing enteropathy (PLE), which is an excessive protein loss through the gastrointestinal tract that can be present after Fontan operation (even if its origins are poorly understood) [29]
The anesthetic management should consider that these patients have a poor cardiac reserve and that the premedication, general anesthesia, and the surgical manipulation after the sternotomy can lead to a destabilization of the hemodynamics.
Antibiotic therapy differs according to age and weight and background of both the donor and recipient (Tables 8 and 9).
Newborn < 1200 g | 20 mg q 12 h |
Newborn ≥ 1200 g < 7 days of life | 20 mg q 12 h |
Newborn ≥ 1200 gr > 7 days of life | 20 mg q 8 h |
Infants and children | 100 mg/kg/24 h in 3 doses |
Antibiotic therapy (cefazolin).
Newborn < 1200 g | 5 mg q 12 h |
Newborn = 2000 g < 7 days of life | 5 mg q 12 h |
Newborn = 2000 g > 7 days of life | 5 mg q 8 h |
Newborn > 2000 g < 7 days of life | 5 mg q 8 h |
Newborn > 2000 g > 7 days of life | 5 mg q 6 h |
Infants and children | 15/40 mg/kg/24 h in 3–4 doses |
Antibiotic therapy (clindamycin).
In case of allergy to beta-lactams, clindamycin is administered.
Immunosuppression is started 1 hour before going to the operating room: thymoglobulin 1 mg/kg/12 h and methylprednisolone 7–10 mg/kg (max. 125 mg).
Premedication is performed, according to clinical condition, with low doses of benzodiazepines (midazolam 0.3–0.5 mg/kg orally or rectal in neonate) avoiding excessive sedation and consequently hypercapnia.
It is well known that in newborns and infants, placing an invasive monitoring before induction of anesthesia is not always possible; therefore, it is essential to have a noninvasive monitoring before starting the drug administration.
General anesthesia is induced by inhalation of sevoflurane/desflurane in newborns and infants and by intravenous injections of midazolam 0.3–0.5 mg/kg, fentanyl 2–4 mcg/kg, rocuronium 1 mg/kg, and propofol 2–4 mg/kg in adults and children. Moreover, for continuous infusion of the anesthesia, propofol 4–6 mg/kg/h in adults, while midazolam 0.2 mg/kg/h and fentanyl 2 mcg/kg/h in newborns and children are recommended. After induction, hydrocortisone 10–20 mg/kg is infused.
In all patients, regional cerebral monitoring is achieved with the use of near infrared spectroscopy (NIRS).
Different conditions may complicate the venous central catheter placing as: anatomical variables, possible occlusion due to previous repeated catheterizations, and previous positioning of central lines. In these cases, the echo-guided assistance is recommended. In smaller patients or in occluded jugular/subclavian veins, femoral veins can be also used. The sizing of the catheter and the numbers of lumens used depend on the weight and age of the patients. When possible, a pulmonary artery catheter (PAC) must be placed into the superior vena cava and then correctly repositioned by the cardiac surgeon before removing the aortic cross-clamp. In newborns and infants, placing PAC may be problematic or impossible due to the size of the patient. In these cases, it is possible to use the central venous oxygen saturation (SCvO2) as a surrogate of SVO2 even if the results are controversial [30].
As an alternative, the left atrial pressure (LAP) can be monitored with the insertion of a catheter through the right superior pulmonary vein.
Transesophageal echocardiography (TEE) is always recommended for a correct evaluation of biventricular function, after the CPB weaning, accordingly with the patient’s weight.
After induction of the anesthesia, the ventilation management requires extreme attention since the hypoxia and the hypercapnia can increase PVR leading to a low cardiac output syndrome. In case of hypotension, before infusing, a bolus of colloid is essential to secure the correct ventilation, avoiding respiratory acidosis.
The majority of patients with CHD undergoing cardiac transplantation are reoperation candidates, so it is important to put into account long operative times, due to dissection of the adhesions and complex reconstruction of the anatomy.
CPB management can be extremely complex and differs according to the patient’s weight and age. The main aim is to maintain a correct medium arterial pressure (MAP) and a correct DO2/VO2 ratio.
Sometimes, this is difficult to be achieved, due to the possible presence of anatomical extracardiac shunts. The dose of unfractionated heparin for the CPB is 200 U/kg in newborns and infants or 300 U/kg in the child and adult, in order to have an ACT > 400 s. In case of reduced response to heparin, administration of ATIII at a dose of 100 mg/kg is recommended. Furthermore, in case of HIT or low response to heparin, direct thrombin inhibitors are administered (bivalirudin and argatroban) as in adult patients. After the aortic cross-clamp is removed, methylprednisolone is administered with the dose of 7–10 mg/kg (max. 125 mg/kg).
Weaning from CPB always requires inotropic support and the right ventricular failure is a possible complication, characterized by restrictive pattern that can be managed by inhaled nitric oxide (5–40 ppm) and inotropic support (milrinone 0.3–0.75 mcg/kg/min, adrenaline 0.02–0.1 mcg/kg/min, and isoprenaline 0.1–1 mcg/kg/min) in order to vasodilate the pulmonary circulation improving biventricular contractility and providing a chronotropic effect if bradycardia occurs. It is extremely important to keep normal PVR by providing a proper ventilation, avoiding hypoxia and maintaining normocapnia.
Once the patient has been weaned form CBP, the vigilance or SCvO2 can monitor the hemodynamic profile and biventricular function can be evaluated with echocardiogram.
However, in case of poor CO, despite maximal inotropic support and correct ventilation, we should consider the support via an extracorporeal membrane oxygenation (ECMO).
At the end of CPB, heparin is antagonized with a ratio 2:1 or 1:1 with protamine based on the ACT values. Antifibrinolytic agents are administrated at the dosage of 50 mg/kg (25 mg/kg after general anesthesia induction and 25 mg/kg at the end of CPB). Severe bleeding is not uncommon in pediatric population. Main reasons of postoperative bleeding are previous heart surgery, cyanotic congenital heart disease, immature coagulation system, and excessive hemodilution due to the disproportionate ratio of CPB circuit volume to patient blood volume, especially in newborns and infants. Correct coagulation management is always achieved through ROTEM.
During the postoperative intensive care course, close monitoring of hemodynamic parameters, inotropes, ventilation, and acid base balance is required to predict pulmonary hypertension, biventricular failure, and LCOS. Normalization of the oxygenation and ventilation is the primary goal in these patients and ventilation support must be discontinued as soon as possible. The antibiotic therapy will be set according to microbiological surveillance. Immunotherapy during the postoperative course is managed by the cardiologist as follows: methylprednisolone, thymoglobulin, tacrolimus, and mycophenolate.
In the postoperative setting, the main problems for pediatric patients are comorbidities related to chronic decompensation and univentricular physiology.
Cyanotic congenital heart disease: patients with long standing hypoxemia often develop severe alteration of whole blood viscosity and alteration of coagulation profiles with high risk of postoperative bleeding [31].
Plastic bronchitis: it is a rare complication of univentricular physiology characterized by the formation of exudative airway casts that can occlude airways and cause respiratory failure. The etiology is still not well identified, but it seems to relate to an increased central venous pressure or lymphatic drainage alterations [32].
Protein losing enteropathy (PLE): it is defined as a possible complication of the univentricular circulation. It can arise after the Fontan operation (5–15% of the patients) [33]. It is characterized by the abnormal loss of proteins into the enteral lumen, which results in hypoproteinemia and hypoalbuminemia. This leads to an increase of lymphatic drainage and a dilation of intestinal lymphatic system with an impaired fat absorption resulting in steatorrhea. Moreover, the hypoproteinemia may result also in ascites, peripheral edema, and pleural/pericardial effusion. Therapy consists of diuretics, corticosteroids, and albumin supplementation.
BIS | bispectral index |
CI | cardiac index |
CO | cardiac output |
COPD | chronic obstructive pulmonary disease |
CPB | cardiopulmonary bypass |
CVC | central venous catheter |
CVP | central venous pressure |
CVVH | central venovenous hemofiltration |
DLCO | carbon monoxide lung diffusion |
ECMO | extracorporeal membranous oxygenation |
HIT | heparin-induced thrombocytopenia |
IABP | intra-aortic balloon pump |
ICD | implantable cardioverter defibrillator |
ISVR | indexed systemic vascular resistance |
LAP | left atrial pressure |
LV | left ventricle |
LVAD | left ventricular assist device |
NGT | nasogastric tube |
NO | nitrogen oxide |
OCS | organ care system |
PAC | pulmonary artery catheter |
PAP | pulmonary arterial pressure |
PCWP | pulmonary capillary wedge pressure |
PEEP | positive end expiratory pressure |
PPM | parts per millions |
PGD | primary graft dysfunction |
PVR | pulmonary vascular resistance |
RAP | right atrial pressure |
RV | right ventricle |
SIRS | systemic inflammatory response syndrome |
SVR | systemic vascular resistance |
TACO | transfusion-associated circulatory overload |
TPG | transpulmonary pressure gradient |
TRALI | transfusion-associated lung injury |
TV | tidal volume |
VAD | ventricular assist device |
WU | wood unit |
The history of the citrus industry in Brazil is intimately linked to its own history. Sweet orange seeds were introduced by the Portuguese jesuits 30 or 40 years after the discovery of Brazil (1500), in the States of Bahia and São Paulo. Due to favorable ecological conditions, the trees (as seedling) produced quite well. The activity remained unknown until the nineteenth century when, during the colonial period, the fruits of the ‘Bahia’ (‘Washington Navel’) orange, originated in the Bahia State, were recognized by the Portugal reign as being larger and juicier than those produced in that country. More important fact, however occurred after its introduction in California it was recognized as ‘more important as the gold extracted from the soils of the Golden State’ and considered as responsible for the development of the citriculture in the five continents. Nevertheless, only in the 1930s, the citriculture began to be implanted commercially in States of São Paulo, Rio de Janeiro and Bahia, with greater growth rate in the states of the Southeast. This chapter is a review on the Brazilian citriculture focusing the four main citrus poles (Figure 1) with their respective producing states and geographical locations, climate, harvested area, production and yield.
Map of Brazil with the physiographic regions and the main citrus poles. (1) South, represented by the State of Rio Grande de Sul (temperate climate), (2) São Paulo, Minas Gerais and Paraná States (central part of the country), (3) Amazon basin, represented by the States of Amazonas and Pará (equator region) and (4) Northeast, represented by the States of Bahia and Sergipe (typical tropical region).
There are no climatic limitations for citrus growing in Brazil. Irrigation is not necessary, except in the semiarid areas of the Northeast, where the rainfall is below 700 mm and in the south where frosts can occur. The altitude varies from 20 to 500 m. Rainfall varies from 1,000 to 1,800 mm, during the winter in the Northeast (March–August) and in the summer in the Southeast (September–March). In Rio Grande do Sul, the rainfall is almost monthly. The relative humidity is higher in the Northeast, where in the winter it almost reaches 100%, with the annual average being between 75 and 80%. The annual average temperature varies from 19°C in the South to 25°C in the Northeast. Independent of the area, flowering occurs in September, one or more times depending on the distance to equator. The farther from the equator, smaller are the fruits but they stay on the trees longer. The soils of the citrus-growing areas are sandy/loam, deep, well drained, but with poor fertility especially in phosphorous. Except the shallow soils of some areas, like the cocoa-growing area in Bahia, the humid Amazonian area or the loamy areas of the States of Paraná and São Paulo, where the coffee and the sugarcane are cultivated, there is an immense area which is available to the citrus industry in Brazil. In an analysis on the Brazilian territory (8.5 millions square meters), it would be possible to adopt a classification of the citriculture on four main citrus poles which are described as follows.
The citrus production in the South of the country is represented by the State of Rio Grande do Sul, which is achieved in 2016, 553,372 tonnes, being the largest concentrations of sweet orange (71.5%) and mandarin (25.4%) [8].
There are 35 microregions in the State of Rio Grande do Sul, 34 of them produce citrus (Figure 2). The regions that most stand out are: Montenegro, Frederico Westphalen and Erechim. The microregion of Montenegro has its production concentrated in orange (45.8%) and mandarin (47.0%) and only 7.2% in lemon. The most important counties are Montenegro, Harmonia, Pareci Novo, Tupandi and São José do Hortêncio. From these, Montenegro highlights the production of mandarin. The second most important microregion is Frederico Westphalen, whose participation in the production was 91.9% of orange, 7.1% of mandarin and 1.0% of lemon. From the 27 remaining countries that compound the microregion, only 3 deserve special mention: Liberato Salzano, Planalto and Alpestre. The microregion Erechim comes next and it is composed of 30 counties, the most important ones being Aratiba, Itatiba do Sul and Mariano Moro.
Concentration of the citrus production in Rio Grande do Sul in the principal microregions. Source: [8]. Obs.: Dark color means data not available.
In the State of Rio Grande do Sul, the latitudes varies from 27°14′56″ S in Alpestre to 30°53′27″ S in Santana do Livramento do Sul near to Uruguay. Longitudes varies from 53°02′06″ to 55°31′58″ W in the same municipalities. Annual media temperature varies from 19.8 to 18.4°C and the rainfall from 1,892 to 1,467 mm in the same municipalities. The climate of the State of Rio Grande do Sul is humid subtropical (or temperate). It is constituted by four reasonably well-defined seasons, with moderately cold winters and hot summers (mild in the higher parts), which are separated by intermediate seasons of approximately 3 months of duration and rains well distributed along the year. Due to its latitudinal situation (inserted in the context of the average latitude), Rio Grande do Sul presents peculiar features different from the climate of the rest of Brazil. The temperatures of the state, in diverse regions, are among the lowest ones of the Brazilian winters, reaching 6°C in cities like Bom Jesus, São José dos Ausentes and Vacaria, where frequent frosts and occasional snowfall happen, and where it is not recommended in the planting of citrus. There are still the altimetric differences, with special feature for Serra do Sudeste and Serra do Nordeste, which is not recommended for planting of citrus because of the high frequency of frosts. During autumn and winter, the state is also liable to the summer phenomenon, which consists of a succession of days with not normal high temperatures for the season. Different from the other states of Brazil, the occurrence of heavy frosts is relatively strong in the whole state demanding the usage of rootstock tolerant to cold.
The citriculture of the State of Rio Grande do Sul comprehends an almost complete chain, involving around 20,000 farmers, more than 100 nurserymen, producers of various inputs, beneficiators of fruit, industries of concentrated and ready to drink juices and of others byproducts of the fruit, wholesalers, marketers, retailers and around 11 millions of consumers. The annual production of orange is 396,000 tonnes (24,000 ha), of mandarin is 141,000 tonnes (11,000 ha) and of acid limes and true lemons is 17,000 tonnes (1,400 ha), being the state, respectively, the sixth, the fourth and the sixth greatest national producer of these fruits [8]. Even so, Rio Grande do Sul imports from others states, especially from Paraná and São Paulo, and from others countries, principally from Spain and Uruguay, almost 50% of the citrus which consume fruit and juice. The vast majority of the citrus growers is family-based, being the average planted area with citrus beneath two hectares per property. The business citriculture is conducted by less than a hundred producers located mainly in the regions of Vale do Caí and Campanha Gaúcha, with the cultivated area of 3–300 ha per property. The associativism is very practiced in Rio Grande do Sul, notably in Vale do Caí, wherewith the small citrus growers seek to overcome their limitations of production, mostly in the processing and in the marketing of the fruit. The principal poles of production are found in Vale do Caí, Campanha Gaúcha and in the northwest region of the state. The citriculture of the Vale do Caí exists for three generations, standing out, nowadays, for the production of mandarins. In the northwest region, the citriculture is much more recent and its expansion was supported by Emater – RS, it concerns small orchards where the orange tree Valência is primarily cultivated and good part of the fruits is destined to the industrial process. In the Campanha Gaúcha region, the production pole of seedless citrus is found. It was initiated in 1998 with the support of Embrapa Clima Temperado, where it is cultivated approximately 2500 hectares and the production is marketed in the principal supermarket network of the state and in others parts of the country. For cultivars, the region of the Vale do Caí detaches in the production of Montenegrina (principal), Caí and Pareci mandarins; the northwest region in orange tree Valência (principal) and Folha Murcha; and the Campanha Gaúcha in navel orange tree Navelina, Lane Late and Cara Cara (Figure 3), orange tree Salustiana, mandarin tree Okitsu and hybrids Ortanique and Nadorcott (Figure 4) and other varieties (Figure 5). The Trifoliata is the principal rootstock used, highlighting itself by the longevity of the plants, the tolerance to various diseases and to induce the high quality of the fruits. The system of conventional production is used in the great majority of citric properties. However, there are more than one hundred of organics products and practically the same number using the principles of integrated production. Among the main limitations of the culture, the phytosanitary nature ones are bounced. According to the producers, the black spot disease is outstandingly the biggest problem of the region of the Vale do Caí, followed by the citrus canker and by the brown spot of alternate. These two last diseases have been controlled especially by the usage of tolerant cultivars. The black pint and the brown spot of alternate do not exist up to the moment in the region of the Campanha Gaúcha, where the citric canker is the major limiting factor. These disease is endemic in the larger part of Rio Grande do Sul and it causes great losses notably in the rainy season. The handling of the disease has been conducted by means of spraying copper-based products and specific cultural practices to reduce source of inoculum. The Huanglongbing (HLB) has not been found in Rio Grande do Sul yet, according to the annual lifting accomplished by the Ministério da Agricultura, Pecuária e Abastecimento (MAPA) in partnership the Embrapa Clima Temperado. However, the vector insect exists in some regions. Although there are around 10 juice and citrus byproducts industries, the production is directed mainly to the market of fresh fruits, prioritizing the state demand.
‘Cara Cara’ (navel) sweet orange in Rio Grande do Sul, the first producing Brazilian state for fresh consumption. Source: Roberto Pedroso.
Harvesting of ‘Nadorcott’ mandarin in Rio Grande do Sul. Source: Roberto Pedroso.
‘Nova’ tangelo and ‘Meyer’ lemon in Rio Grande do Sul. Source: Roberto Pedroso.
The production of citrus in the principal citrus pole of the country encompasses the States of Minas Gerais, São Paulo and Paraná. The production from São Paulo, the most expressive one, is distributed in sweet orange, lemon and mandarin, with volumes of 12.8 million, 875,000 and 345,000 tonnes in 2016, respectively, in order of importance. In the State of Minas Gerais, the citrus production achieved 1,258,767 tonnes being 80% of orange and 13% of mandarin and 7% of lemon. The State of Paraná produced 922,422 tonnes of citrus—80% of orange and 20% of mandarin [8]. There are 63 microregions in the State of São Paulo, and from these, 25 microregions are the most important in the citrus production (Figure 6). Of these 25, the highest concentrations are in 7 microregions, in order of importance: Bauru, Avaré, São João da Boa Vista, Araraquara, São José do Rio Preto, Jaboticabal and Itapetininga. Lower concentrations occur in 18 microregions: Barretos, Botucatu, Mogi Mirim, Pirassununga, Itapeva, Novo Horizonte, Jales, Ourinhos, Catanduva, Limeira, Rio Claro, São Carlos, Franca, Lins, Fernandópolis, Jaú, Piracicaba and Sorocaba. Although Minas Gerais owns 66 microregions, just 2 of them stand out in the production of citrus: Frutal and Uberlândia. Both of them are part of the Triângulo Mineiro and in 2016 they produced about 414,000 and 259,000 tonnes, respectively. In the microregion of Frutal, the most important counties are Comendador Gomes and Frutal, while in the microregion of Uberlândia the counties that most highlight are Prata, Uberlândia and Monte Alegre de Minas. There are 39 microregions in Paraná, of which only 2 do not produce citrus. The two most important microregions in the citrus production are Paranavaí and Cerro Azul. Both microregions produce citrus, but Paranavaí presents the greatest volume in the orange production (99.4%) and Cerro Azul calls attention in the mandarin production (92.4%). The microregion of Paranavaí owns 29 counties, of which 9 do not produce any kind of citrus and the 3 that more stand out are Paranavaí, Guairaçá and Alto Paraná. In the microregion of Cerro Azul, two counties highlight, Cerro Azul and Doutor Ulysses, both of them concentrate their productions to the mandarin fruit.
Concentration of the citrus production in the states of Minas Gerais, São Paulo and Paraná, concerning the principal microregions. Source: [8]. Obs.: Dark color means data not available.
Citrus trees are cultivated in São Paulo State often under mountain subtropical climate, that is, Cwa according to Köppen’s classification. Considerable areas are in Cfa climate, and minor cultivation is carried under Aw and Cfb climates, respectively, on the coast and in the highlands. Considering Cwa as the prevalent condition, climate is characterized with hot, rainy summers, and dry, relatively cold winters. Two main climate types for citrus cultivation could be described: (i) mean annual air temperature higher than 17°C and annual water deficit of 0–60 mm and (ii) mean annual air temperature higher than 17°C and annual water deficit higher than 60 mm [16]. Minimal air temperatures are in the range of 8–10°C, and maximum can surpass 40°C. Annual rainfall ranges from 1,000 to 2,000 mm, often 1,400–1,800 mm, with distribution concentrated from November to March. Altitude ranges from 400 to 1000 m, but 550–750 m is prevalent. Citrus areas are free of severe frosts in São Paulo, even though it is regularly observed in the South of the State and in Paraná. Prolonged drought is frequent, especially on the North of São Paulo and in Minas Gerais State, as drought intensity decreases with the latitude. In recent years, heat stress associated to drought was reported in the main citrus areas in September–October, which is the period of the main blossom and fruit set.
The citrus belt comprises the Northwest of Paraná State (23°04’ S–52°27’ S); the Triângulo de Minas Gerais region (19°18’ S–48°55’ S) and São Paulo State (21°49’ S–49°12’ S), which is divided in the following areas (as percentage of the total citrus area in this state): North (22%), Northwest (11%), Center (29%), South (20%) and Southwest (18%) [16].
São Paulo, Minas Gerais and Paraná had about 430,000, 38,000 and 25,000 ha of sweet orange groves in 2016–2018, respectively [5, 6]. The main varieties are, in decreasing order, Pera (midseason), Valencia (late), Hamlin (early), Natal and Folha Murcha (both late) and the early season varieties of Valencia Americana, Westin and Rubi, although the former four comprise more than 80% of the total trees. Some other varieties including navels and acidless oranges are cultivated in smaller areas. Persian lime and lemons are also cultivated mainly in São Paulo (39,000 ha in 2018), and mandarins, largely Ponkan mandarin and Murcott tangor, are important for all states (12,000; 8,000 and 10,000 ha for São Paulo, Minas Gerais and Paraná, respectively). Sweet oranges are produced mainly for juice processing, and the citrus belt represents more than 85% of the Brazilian production. This is the most important orange production area in the world (34%) resulting in 56% of the juice produced and 76% of the marketed in the world [11]. Almost 97% of the juice is exported, while mandarins are for fresh fruit in the internal market, and limes and lemons are for fresh fruit and few processing, and exportation of fresh fruit too. Rangpur lime was the most used rootstock until the 2000s, as a result of its tolerance to both citrus tristeza virus (CTV) and drought, high and early yield, and great vigor and graft compatibility in the nursery. However, it is sensitive to citrus sudden death (CSD), blight, citrus nematode and gummosis of Phytophthora spp., and induces low juice quality, therefore after 2000, it has been increasingly replaced by the Swingle citrumelo. This rootstock is tolerant to all mentioned diseases. Despite being sensitive to drought, it induces high production of high quality juice [13]. Sunki mandarin is currently the third most used rootstock, especially for Pera since this scion in addition to Murcott and some selections of lemons are graft-incompatible with Swingle citrumelo. Cleopatra mandarin, trifoliate orange and Flying Dragon are used in a smaller amount. The Tropical selection of Sunki mandarin and a few citrandarins are been tested and used in increasing areas being considered promising rootstocks for the orchard diversification.
The citrus industry in São Paulo, Minas Gerais (Figure 7) and Paraná (Figure 8) employs more than 200,000 people and contributes with US$ 6.5 billion annually. Although about 6,000 farms cultivate oranges, 88% of the growers have less than 50,000 trees, while 12% of farms with more than 100,000 trees correspond to 77% of the total trees (194 millions) [6]. Therefore, the citrus cultivation in the citrus belt is nowadays a highly intensive, technological entrepreneurial activity. However, harvesting and fruit transportation reaches almost 50 of the production cost (Figure 9). Nursery stocks have been grown in insect-proof screen houses since 2003, and about 10 million grafted trees are produced annually in pots filled with potting media. Orchards use currently an average of 484 trees/ha, but new groves increased tree density to 656 trees/ha in average. About a third of the area is currently irrigated, and major cultivated area corresponds to trees from 5 to 15 years old. Citrus diseases and pests are major limiting factors to the citrus industry of the three states that substantially increase the production costs. Huanglongbing (HLB) is the most devastating one, and the average incidence in São Paulo and Triângulo de Minas Gerais was about 17% in 2017 [7]. The smaller the farm, the higher the incidence, because HLB management essentially depends on the eradication of symptomatic trees and on the control of the vector, the Asian citrus psyllid, in addition to control measures on inoculum sources outside the farm. As a result, management is more efficient if taken by all growers in an area wide approach. Other important phytossanitary problems include black spot, citrus canker, leprosis virus, citrus variegated chlorosis, citrus sudden death, post bloom fruit drop (Colletotrichum acutatum and C. gloeosporioides), Alternaria brown spot of mandarins, fruit flies, mites and scales.
Ponkan mandarin orchard in Minas Gerais. Source: Eduardo Girardi.
Planting of citrus in Paraná. Source: Eduardo Girardi.
Harvesting of sweet orange in São Paulo, the first citrus-producing state in Brazil. Source: Eduardo Girardi.
Considering the enormous area of Northern Brazil, citriculture is poorly exploited in this region, with the States of Pará and Amazonas showing the highest productions. From 270,370 tonnes of sweet orange, 53,806 tonnes of acid lime and 4,722 tonnes of mandarin, the State of Pará is responsible for 70.8% of sweet orange, 73.9% of acid lime and 20.9% of mandarin, while in the State of Amazonas these values are 14.9, 4.2 and 6.7%, respectively. Cultivated area comprises only 19,515 ha with the following distribution: 15,876 ha of sweet oranges, 3,054 ha of lemons/limes and 585 ha of mandarins. Average yield in these states is 14.1 t/ha indicating that the regional yield is about 54.6% of the national average (25.8 tonnes/ha).
All states in the North of Brazil produce citrus. However, Pará and Amazonas are highlighted once contribute with 70.6 and 13.0%, respectively, of the regional production, and these states rank in seventh and thirteenth position among Brazilian citrus-producing states. There are 22 microregions in the State of Pará, but citrus is cultivated in 17 of them. In this state, the two main citrus-producing areas are Guamá and Santarém. The former has the major concentration of citrus crops (sweet orange, lime/lemon and mandarin) (Figure 10). In the Guamá area, the greatest producer is the municipality of Capitão Poço, most notably with oranges, while in the Santarém area the production of lemon/lime is more important in the municipalities of Monte Alegre and Alenquer. The State of Amazonas has 13 microregions, and citrus production is mainly sweet orange cultivated in the Rio Preto da Eva microregion in the municipality with the same name.
Concentration of the citrus production in the States of Amazonas and Pará, concerning the principal microregion. Source: [8]. Obs.: Dark color means data not available.
The North region consists of the largest part of the Amazon Basin and it is characterized by low altitudes between 0 and 200 m. The climate is tropical equatorial with predominance of the type Af in the States of Amazonas and Acre, and of the type Am in the States of Pará, Amapá, Roraima and Rondônia. Only the State of Tocantins presents the climate type Aw. Atmospheric circulation systems, in the intertropical convergence zone, are responsible for the climate variability and for the rains in the state of the Amazon Basin. The average annual precipitation exceeds 2,000 mm, as until 3,000 mm in the estuary of the Amazonas River in Belém, and 2,400 mm in the innermost region of the Amazon Basin, in Manaus. In the direction of Roraima, East of Pará, there is less rainfall, with the annual total in the order from 1,500 to 1,700 mm. The rainy season in the greatest part of the region comprehends the period from December to May. During the rainiest months, March and April, precipitations of up to 400 mm monthly are reached. The ‘dry season’ from June to November still shows precipitations of 60–120 mm per month. Unlike, in the State of Roraima, due to the influence of the climatic conditions from the North hemisphere, the maximum rainfall indices occur in the period from April to September, with a longer dry season between October and March. Concerning the temperatures, the predominant climate is hot, with average annual temperatures varying from 22 to 28°C, average temperature of the coldest month of 18°C and maximum of 42°C in the hottest months. The temperatures are high in most of the region with low thermal amplitude except in some locals of higher altitude in Roraima and in Acre. In Rondônia, due to the entrance of cold air masses from the Atlantic Ocean, passing by the State of Mato Grosso, temperatures are reduced causing the phenomenon of ‘coldness’ for short periods of 5–6 days.
Considered as the largest citrus pole in the equatorial zone (Amazon basin), the citriculture of Pará is represented by the municipality of Capitão Poço in an area of 11,000 of hectares [4]. The fruit production, made by at least 1,000 growers, is destined for other states including for juice processing plants. It is reference as organic orange producer, being 70% of family farming, and the municipality restarted its certification process [9]. Different as compared to other producers in Brazil, the harvesting season occurs from September to December with a minor harvest in March and April. As in the Northeast region, the combination scion/rootstock cultivated is ‘Pera’ sweet orange × ‘Rangpur’ lime and the yield of orange and acid lime is very low, around 15 tonnes per hectare per year.
Oranges: in the orchards of the North region, there is a predominance of the ‘Pera’ sweet orange variety (Figure 11), even though some farmers produce the ‘Valencia’ in small scale. In spite of the good productivity and of the uniformity in fruit size of the ‘Valencia’, in the States of Amazonas and Roraima, there is a consensus among the producers in refusing this variety claiming that there is no market space for it. In smaller proportions, there are orchards with the ‘Folha Murcha’ variety. Mandarins: ‘Murcott’ and BRS Piemonte tangors and ‘Mexerica do Rio’ Mediterranean mandarin are the most commons in the North region. ‘Tahiti’ acid lime, especially the IAC-5 and ‘Quebra Galho’ clones, were initially used, and later substituted by the ‘CNPMF 2001’ clone. Although there are appropriate conditions, the productivity of mandarin is low. Rootstocks: since the period of the introduction of the citriculture in the North region, the rough lemon, the ‘Cleopatra’ mandarin and the ‘Rangpur’ lime were used as rootstocks, being the last one the predominant in the regional orchards nowadays. In smaller proportion, we still may find ‘Cleopatra’ mandarin orchards formed 15 years ago. ‘Rough’ lemon, in small scale, has been used by some growers as rootstock. ‘Swingle’ citrumelo has just been used grafted with the ‘Tahiti’ acid lime. As a characteristic of equatorial conditions, the ‘Pera’ sweet orange in the Amazon region presents greenish fruits even in the maturation period, although it presents the relation Brix/acidity and pulp coloration adequate to the consumption (Figure 12).
Big ‘Pera’ sweet orange tree in Amazonas. Source: Luciano Souza.
‘Pera’ sweet orange fruits in Amazonas. Source: Luciano Souza.
Sweet orange, lime and mandarin fruits are being produced in the states of the Northeast region, however the States of Alagoas, Pernambuco and Piauí do not produce mandarin. From the nine Northeastern States, Bahia and Sergipe stand out, with 66.2 and 26.1% of the regional production, and second place in the national production. From 1,744,673 tonnes of sweet orange, 169,123 tonnes of acid lime and 34,247 tonnes of mandarin, the State of Bahia is responsible for 64.8% of sweet orange, 88.1% of acid lime and 30.0% of mandarin, while in the State of Sergipe these values are 28.0, 4.9 and 30.3%, respectively. In these states, the citriculture occupies an area of 127,517 ha as follows: sweet orange 118,473 ha, acid lime 7,769 ha and just 1,275 ha with mandarin. The yield average is very low, just 14 tonnes/ha, representing almost half of the national average.
The Northeast region is located between 2 and 18° South latitude and 35° and 50° West longitude. The climate along the sea coast is hot and humid (tropical), with annual temperature average varying between 20 and 28°C and rainfall between 300 and 2,000 mm. The sunshine time varies from 2,300 per year in the humid areas up to 3,000 in the semiarid areas. The largest area in the Northeast is under semiarid conditions (‘Polígono das Secas’)—less than 750 mm of rain per year), The region comprises nine states: Maranhão, Piauí, Ceará, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Sergipe and Bahia, that occupies 18.2% of the national territory. Analyzing the regions and its ecological diversity, in relation to the citrus trees, it is possible divide them in three grand zones: (1) sea coast (Coastal Tablelands) represented by the municipality of Cruz das Almas (BA); (2) area of altitude, represented by the municipality of Morro do Chapéu—Chapada Diamantina (BA), over 1,000 m of altitude and (3) semiarid zone, represented by the municipality of Petrolina (PE).
The sea coast (Coastal Tablelands) is located along the sea, near the main capitals. The relative humidity is high and rainfalls around 1,000 mm per year but very concentrated during the summer time (December–March). Under these conditions, it predominates the sweet orange group represented almost exclusively by ‘Pera’ sweet orange (Figure 13), which fruit quality is typical in the tropical areas: larger fruits, juicier, less colored and less acid than those produced under subtropical conditions. More recently, the ‘monocitriculture’ of ‘Pera’ sweet orange × ‘Rangpur’ lime rootstock (almost 100% of the orchards) has been broken by the use of ‘Tahiti’ acid lime, unfortunately on the same rootstock. The fruit production destination is divided between the fresh fruit market and for processing (frozen concentrated juice). For a long time, Embrapa is stimulating the scion and rootstock diversification recommending as early varieties: ‘Rubi’, ‘Westin’ and ‘Salustiana’; midseason: ‘Pineapple’, ‘Pera’ and ‘Sincorá’; late: ‘Natal’, ‘Valencia’ and ‘Folha Murcha’ (Curled Leaf) [1], as well the following rootstocks: ‘Indio’, ‘Riverside’ and ‘San Diego’ citrandarins (from USDA), ‘Sunki Tropical’ mandarin and ‘Santa Cruz Rangpur’ lime. News rootstock hybrids are being released by the Embrapa Citrus Genetic Improvement Program [15] due to traditional areas that represent the Northeastern citriculture, the analyses on fruit productions will be concentrated in the States of Bahia and Sergipe. In Bahia, there are 32 microregions but only 4 can be considered as citrus producer: Alagoinhas, Santo Antonio de Jesus, Ribeira do Pombal and Entre Rios (Figure 14). From these, the first presents the largest citrus concentration represented by the municipalities of Rio Real, Inhambupe and Alagoinhas. In the Santo Antonio de Jesus microregion, sweet orange, acid and sweet lime and mandarin fruits are produced in the municipalities of Cruz das Almas, Sapeaçu, Muritiba, Governador Mangabeira and Cabaceiras do Paraguaçu as the most important. In Cruz das Almas, the largest participation comes from acid lime designated to the exporting market. Ribeira do Pombal microregion is concentrated just on sweet orange production and is located in a climatic transition zone which rainfall is less than 1,000 mm. The most important municipality is Itapicuru and its neighbors where exist the most appropriate conditions in the State for the citrus expansion, due to the existence of Tucano aquifer. In Entre Rios microregion, sweet orange production is concentrated in the municipalities of Esplanada and Jandaíra. In Sergipe State, there are 13 microregions being the most important, in a descending order, Boquim, Estância and Agreste de Lagarto. The Boquim microregion is most important in the production of sweet orange, mandarin and limes mainly in the municipalities of Itabaianinha, Cristinápolis, Salgado, Boquim, Arauá, Umbaúba and Tomar do Geru. In the microregion Estância, similarly, the citrus production is concentrated in the same groups. The main municipality producers are Santa Luzia do Itanhy, Estância and Indiaroba. Finally, Agreste de Lagarto microregion is predominated with the sweet orange and mandarin, mainly in the municipalities of Lagarto and Riachão do Dantas.
‘Pera CNPMF D-6’ sweet orange in Bahia—The most popular variety in Brazil. Source: Orlando Passos.
Concentration of the citrus production in the states of Bahia and Sergipe, considering their microregions. Source: [8]. Obs.: Dark color means data not available.
It is located in the States of Bahia, Pernambuco, Paraíba and Ceará with milder climate, low temperatures in the winter (July is the coldest month), and insufficient rainfall for the culture necessity, what requires complementary irrigation. Inside this ecosystem is the Chapada Diamantina tableland, whose altitude varies between 1,000 and 1,400 m. In this zone, the table fruits should be prioritized, preferably the mandarins without despising the seedless navel oranges (‘Bahia’ sweet orange). Among these fruits, some stand out: ‘Cara Cara’ (‘Bahia’ of red pulp), ‘Baianinha’ (litle Navel) and ‘Lima’ (no acidity). In the mandarins group, beyond the traditional ‘Ponkan’ and ‘Murcott’, special attention should be given to the tangelo mandarin tree ‘Page’ (seedless fruit, in isolated plantation), to the tangor mandarin tree ‘Piemonte’ (Figure 15) and to the BRS Salibe Murcott (fruits with few seeds).
‘Piemonte’ mandarin-tangor in Bahia—A new variety for fresh consumption. Source: Orlando Passos.
The Brazilian semiarid is an ecoregion defined from the isoieta of 800 mm. The climate can be classified, according to Köepen, as type Bswh, which corresponds to a very hot semiarid region. The annual rainfall index is 571.5 mm with concentration from December to March [2]. The average annual temperature is 26.4°C, with average minimum of 20.6°C, and with average maximums of 31.7°C. The daily thermal amplitude is around 10°C, monthly of 5–10°C and annually from 1 to 5°C; very strong insolation (annual average of 2,800 h/year); low relative humidity (annual average around 50% per year); and high evapotranspiration (average of 2,000 mm/year) [10, 14]. In areas of hot or tropical climate, like in the Northeast region, the amplitude is smaller, what implies in the fruit production of less coloring, not just inside but also outside. However, the contents of soluble solids (°Brix) are higher and present low acidity, resulting in sweeter fruits, but with the relation Brix/acidity unfavorable. It is worth pointing out that in hotter climates, like in the Northeastern semiarid, grapefruits and ‘Tahiti’ acid lime present a thin peel and a very colorful pulp, besides a great productivity, when compared to fruits produced in others regions of the country. It is important to accentuate that in citrus cultivation under high temperatures, the period between flowering and maturation is reduced, what enables anticipation of the harvesting in relation to the others producing areas. Although having a potential for grapefruit, lemons and acid limes, there are small areas producing citrus in the São Francisco Valley, specifically with ‘Tahiti’ acid lime (Figure 16) [12]. In 2016, the results were 204 ha of planted area with the yield of 26.2 t/ha, in the following counties: Juazeiro, Casa Nova, Sobradinho and Curaçá [8]. In this region, due to its production characteristics, it is recommended rootstocks that determine reduced size to the canopy, drought tolerance and fruits of good quality, like rootstocks hybrids obtained by Embrapa Citrus Breeding Program in crosses with ‘Trifoliate’ orange, ‘Swingle’ citrumelo and ‘Troyer’ and ‘Argentina’ citranges, among others. The citrandarins ‘Indio’, ‘Riverside’ and ‘San Diego’, obtained by USDA Citrus Breeding Program and recommended by Embrapa Mandioca e Fruticultura, are hybrids of ‘Sunki’ mandarin with trifoliate orange, and have been highlighting in the Northeastern citrus scenario, because of their citrus foot-rot tolerance and production of good quality fruits. In researches with citrus fulfilled by Embrapa Mandioca e Fruticultura in partnership with Embrapa Semiárido, in Petrolina-PE and in Juazeiro-BA, it was verified that the grapefruit and the ‘Tahiti’ acid lime behave well. The Flame grapefruit (Figure 17) present thin peel and deep flesh color and fair balance between Brix/acidity, what are considered outstanding characteristics [12]. Some sweet orange varieties have great potential under semiarid conditions, as the clones C-21, D-9, D-12 and D-25 of Pera, and Rubi, Westin, Salustiana, Natal CNPMF-112 and Valencia Tuxpan, besides ‘Page’ and ‘Piemonte’ mandarin hybrids [3]. Examining the different climatic situations, it is possible to point out as competitive advantages of the Northeast region: (1) multiplicity of climates and soils and area availability; (2) geographic privileged localization in relation to the main markets (Economic European Community and United States of America) in comparison to the others citrus fruit producers regions in the country; (3) non-occurrence of bacterial diseases, like the HLB (huanglongbing, ex-greening) and the citrus canker and others like leprosis (not in endemic form) and the black spot, which are causing serious losses to the Brazilian southwest citriculture, mainly in the States of São Paulo, Minas Gerais and Paraná.
‘Tahiti’ acid lime in Bahia—In Ascension in the northeastern region. Source: Nilton Sanches.
‘Flame’ grapefruit in the São Francisco Valley—An option for the regional citriculture. Source: Orlando Passos.
IntechOpen's Authorship Policy is based on ICMJE criteria for authorship. An Author, one must:
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