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Eur J Cardiothorac Surg 2007;32:156-162. doi:10.1016/j.ejcts.2007.03.024
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Preoperative small pulmonary artery did not affect the midterm results of Fontan operation

Iki Adachia, Toshikatsu Yagiharaa,*, Koji Kagisakia, Ikuo Haginoa, Toru Ishizakaa, Junjiro Kobayashia, Soichiro Kitamuraa, Hideki Uemurab

a Department of Cardiovascular Surgery, National Cardiovascular Center, Suita, Japan
b Department of Cardio-Thoracic Surgery, Royal Brompton Hospital, London, UK

Received 18 November 2006; received in revised form 14 March 2007; accepted 15 March 2007.

* Corresponding author. Address: Cardiovascular Surgery Department, National Cardiovascular Center, 5-7-1 Fujishirodai, Suita, Osaka 565-8565, Japan. Tel.: +81 6 6833 5012; fax: +81 6 6872 7486. (Email: yagihara{at}hsp.ncvc.go.jp).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
Objective: It was well discussed, in the primary Fontan era, that small pulmonary arterial size could affect the results immediately after the Fontan procedure. The objective of the present study is to determine whether this feature remains as a risk factor in the era of the staged Fontan completion and poses functional impediments in the longer terms. Methods: Between June 1991 and November 2004, the staged Fontan completion was carried out subsequent to the bidirectional Glenn procedure in consecutive 57 patients with a preoperative pulmonary artery index less than 250 mm2/m2 (Group-S; minimum index 104 mm2/m2). Clinical data were reviewed retrospectively. As background and reference information, similar data were collected in another consecutive 64 patients with larger pulmonary arteries who underwent the staged Fontan completion during the same period (Group-L; maximum index 697 mm2/m2). Results: No patients died after the Fontan procedure in Group-S, while six early deaths in Group-L. No takedown of the Fontan circulation was carried out in either group. The latest catheterizations, at 2.8 ± 2.7 years postoperatively, showed a pulmonary artery index significantly lower than the preoperative index (Group-S: 198 ± 37–176 ± 49 mm2/m2; P = 0.0082, Group-L: 360 ± 94–266 ± 89 mm2/m2; P < 0.0001). Hemodynamics in Group-S during the intermediate term were identical with those in Group-L in mean pulmonary arterial pressure (10 ± 2 in Group-S and 10 ± 3 mmHg in Group-L), mean atrial pressure for the systemic chambers (5 ± 2 and 6 ± 3 mmHg, respectively), mean transpulmonary gradient (5 ± 2 and 4 ± 2 mmHg, respectively), cardiac index (3.0 ± 0.7 and 3.0 ± 0.6 l/min/m2, respectively), and arterial oxygen saturation (93 ± 3% and 94 ± 2%, respectively). Similarly, brain natriuretic peptides concentration in the serum (19.4 ± 15.6 in Group-S and 28.3 ± 37.2 pg/ml in Group-L) and peak oxygen consumption on exercise testing (24.8 ± 4.5 and 24.0 ± 6.3 ml/kg/min, respectively) were not inferior in Group-S to those in Group-L. Conclusions: The outcome after the Fontan completion, including functional ones in the intermediate term, was acceptable in patients having a preoperative PA index smaller than 250 mm2/m2. Pulmonary artery index decreased still further postoperatively, but did not obviously militate against functional efficacy of the Fontan circulation.

Key Words: Fontan operation • Small pulmonary artery • Midterm results


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
Impact of the pulmonary arterial (PA) size has been discussed particularly focusing on the early postoperative outcome after the primary Fontan procedure [1–5] subsequent to the initial criteria proposed by Choussat et al. [6] in 1978. The objective of our present study is to clarify the influence of preoperatively smaller PA size on the midterm results after the Fontan completion in a staged fashion.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Statistical analysis
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
2.1 Patient population
The study population consisted of 57 consecutive patients who had a staged Fontan completion via the bidirectional Glenn procedure (BDG) between June 1991 and November 2004 and whose PA index (Nakata index) [1] was less than 250 mm2/m2 immediately before the final stage (Group-S, PA index 198 ± 37 mm2/m2, minimum PA index 104 mm2/m2). During the same period, another consecutive 64 patients underwent a staged Fontan operation with a larger preoperative PA index (250 mm2/m2 or greater) and a similar review was carried out in these patients to provide general information as a reference group (Group-L, PA index 360 ± 94 mm2/m2). Other than these 121 patients, between June 1991 and November 2004, we had 126 patients who underwent a primary Fontan establishment and another 16 who underwent (before 1993) the second stage Fontan following the conventional unidirectional Glenn procedure; all these 142 being excluded from this study. Our principal strategy for the Fontan completion changed from intra-cardiac total cavopulmonary connection (TCPC) to extra-cardiac TCPC without use of cardiopulmonary bypass in 1996 [7], and from the primary fashion to the routine staged approach in 2001. Accordingly, the BDG was employed, before 2000, not as a routine preparation but in selected patients who were considered to have risk factors for the primary Fontan establishment [8].

Baseline demographic and clinical data were available from the hospital records for all patients of the both groups (Table 1 ). Left isomerism of atrial appendages was seen in 11 patients (7 in Group-S and 4 in Group-L), and right isomerism in 31 (9 and 22, respectively). Ventricular morphology was of the dominant morphologically left type in 42 (27 and 15, respectively), of the dominant morphological right pattern in 69 (26 and 43, respectively), and of balanced two chambers in the remaining 9 (3 and 6, respectively). The initial palliative procedure was for systemic-to-pulmonary shunt in 47 (20 in Group-S and 27 in Group-L), for banding of the pulmonary trunk in 20 (12 and 8, respectively), for other closed palliations (reconstruction of the obstructed aortic arch or unifocalization of the pulmonary arteries) in 9 (3 and 6, respectively), and for any open heart palliations (including the Norwood procedure and repair of totally anomalous pulmonary venous connection) in 15 (9 and 6, respectively) except for 30 (13 and 17, respectively) undergoing the BDG as a first procedure. Number of previous operations prior to the Fontan completion was 2.3 ± 1.0 for the Group-S and 2.1 ± 1.0 for the Group-L. The features of the BDG were shown in Table 1. Augmentation of the central PA includes extensive preparation for the future off-pump Fontan procedure with the inferior caval vein (IVC) simply cross-clamped [9].


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  		Table 1 Preoperative demographics, morphologic features, and catheterization data
 
2.2 Fontan operation
Every patient underwent preoperative evaluations including cardiac catheterization at our institution to assess the indication of Fontan completion. Median intervals between the previous BDG and the Fontan completion were 10 months in both groups. While many variable data including PA pressure, ventricular function or the extent of collateral arteries were taken into account to decide the Fontan indication, the decision was mainly based on pulmonary vascular resistance calculated from catheterization study; the resistance less than 4 Wood unit times m2 was considered as indication. At least, none was excluded from consideration for the Fontan completion solely on the basis of small PA size.

The method for the Fontan procedure and concomitant procedures are summarized in Table 2 . According to our strategic policy, cardiopulmonary bypass was used, after 1996, in a selected group of patients where this was considered necessary for intra-cardiac maneuvers or other particular issues. Fenestration was equipped when preoperative pulmonary resistance was calculated as greater than 3.0 Wood unit times m2 or a trans-pulmonary gradient was greater than 15 mmHg immediately coming off bypass or 10 mmHg immediately after commencement of the Fontan circulation in the off-pump fashion. Use of fenestration was slightly more frequent in the groups of patients with a preoperatively smaller PA size (18 in Group-S and 9 in Group-L, and 32% and 14%, respectively).


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  		Table 2 Fontan completion
 
2.3 Anticoagulation and antiplatelet therapy
Warfarin sodium and dipyridamole were prescribed postoperatively, and the international normalized ratio was maintained at around 2.0. The duration of warfarin administration varied among patients according to a judgment by the patient's personal pediatrician; however in most cases, anticoagulation was discontinued when there are no particular issues identified in the Fontan pathway at the first catheterization 1 year postoperatively. Regarding dipyridamole, indefinite continuation was recommended when patient's compliance could be predicted and there were no obvious contraindications.

2.4 Catheterization
Data derived from preoperative catheterization in both groups were shown in Table 3 .


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  		Table 3 Preoperative and postoperative catheterization data
 
As an institutional policy, postoperative catheter studies were routinely carried out 1 year after surgery and then every 5 years to assess the Fontan circulation. Additional catheter investigations took place irregularly, on a case-by-case basis, when clinically indicated. All pulmonary angiograms were examined by one examiner (I.A.). Both left and right pulmonary arteries were measured just proximally to the first branch according to the technique described by Nakata et al. [1]; measurements were repeated three times for each angiogram with DCM View3 angiogram software (Climb Medical Systems Inc., Osaka, Japan) in order to minimize potential error caused by manual maneuvers, and a mean of the three values were used as the definitive values. The measured diameters of the pulmonary arteries were corrected for magnification, and the cross sectional areas were calculated from the corrected pulmonary artery diameter size, after which the areas were summed and divided by the patient's body surface area to yield the PA index.

2.5 Neurohormonal activity and exercise tolerance
The plasma level of brain natriuretic peptides (BNP) was assayed by radioimmunoassay [10]. Routine postoperative measurements of this neurohormonal factor were periodically carried out in the outpatient clinic. Peak oxygen consumption (VO2) was measured by means of symptom-limited treadmill exercise using a 30-s incremental protocol as previously described by Ohuchi et al. [11]. When multiple data for these variables were available in a patient, the latest values were used for analysis. These investigations were carried out according to the institutional regimen for evaluation with the Fontan circulation.


   3. Statistical analysis
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
All data sets were reviewed retrospectively. Data are expressed as frequencies, medians with ranges, and means with standard deviations as appropriate. In cases with missing data, the number of available values is given. The paired student t-test was used for comparison of two different PA index obtained pre and postoperatively in each group. The data were analyzed with StatView statistical software (Abacus Concepts Inc., Berkeley, CA). A P-value of 0.05 or less was considered statistically significant.


   4. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
5. Discussion
 6. Conclusion
 Appendix A
 References
 
4.1 Mortality and morbidity
There was no early death or Fontan takedown in Group-S. On the other hand, six patients died early in Group-L. Of these, three patients died of infection: mediastinitis in one and bacterial sepsis in two. Another patient died of massive airway bleeding which was associated with pulmonary venous obstruction. The remaining two patients died of low cardiac output associated with residual atrioventricular valve regurgitation.

For the early survivors, follow-up averaged 3.5 years for Group-S and 4.5 years for Group-L, although one patient (1/57, 2%) in Group-S and four patients (4/64, 6%) in Group-L were lost to follow-up. During the follow-up period, no patients required Fontan takedown and nor did late mortality occur in either group. No intractable protein-losing enteropathy has occurred thus far. The serous protein level below the normal range in routine blood tests was noted in three of the Group-S patients (2, 3 and 10 years after the operation), and in one of the Group-L patients (at 1 year postoperatively). All of these four patients were successfully treated by medication alone and without recurrence.

4.2 Serial changes in the pulmonary artery index
Fifty-three patients (93%) in Group-S and 60 patients (94%) in Group-L underwent postoperative catheter examination once at least. The latest catheter in each patient, at 2.8 ± 2.7 years postoperatively, demonstrated a decrease of the PA index within either of the groups (Group-S: preoperative 198 ± 37 to postoperative 176 ± 49 mm2/m2, P = 0.0082; Group-L: 360 ± 94–266 ± 89 mm2/m2, respectively, P < 0.0001). This change did not appear to be greater in the Group-S, in terms of either the absolute value ({delta} PA index, defined as latest –pre PA index) or ratio of change (% PA index, defined as latest/pre PA index x 100) (Table 3). Consecutive postoperative catheter in 37 patients also illustrated a tendency of progressive decrease in the PA index in both groups (Fig. 1 ).


Figure 1
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  		Fig. 1. Serial changes in the pulmonary arterial (PA) index for patients undergoing postoperative catheterizations at least twice postoperatively. This graph suggests that the postoperative PA index decreased in a milder fashion in patients with a smaller preoperative PA index during the first postoperative 5 years.

 
4.3 Other data from postoperative catheter
Mean PA pressure, atrial pressure for the systemic chambers, transpulmonary gradient, cardiac index, and arterial oxygen saturation in Group-S were ordinary for the Fontan circulation and identical with those in Group-L. This was also the case, when reviewing those data in selected patients without patent fenestration (Table 3).

4.4 Functional data in the midterm period
BNP level or exercise testing was not inferior in Group-S to those in Group-L (Table 3).


   5. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
6. Conclusion
 Appendix A
 References
 
Some studies supported the idea that pulmonary artery size connoted an impact on outcome after Fontan operation. In 1984, Nakata et al. [1] described a standardized method for quantification of pulmonary artery size. Their retrospective assessment of 15 patients undergoing Fontan operation led them to conclude that the Fontan operation was ideally indicated with a PA index greater than 250 mm2/m2. In the present study, a cut-off line was set with this particular value. In 1989, Fontan et al. [2] published their results of a multi-center study of 334 patients and concluded that dimensions of the right and left pulmonary arteries, expressed as the McGoon ratio, were one of the most powerful risk factors for death with or takedown from the Fontan circulation. They mentioned that the higher risk became especially evident at a McGoon ratio below some 1.8, and increased sharply with smaller pulmonary arteries still further. In 1993, Knott-Craig et al. [3] conducted a retrospective study of 139 patients undergoing the Fontan operation and reported that, among a low-risk subset of 30 patients with tricuspid atresia, those with poor outcome possessed significantly smaller pulmonary arteries than those with good results did.

In the same article, on the other hand, there was no significant difference in the PA size when their overall cohort was compared between patients with favorable and unfavorable outcomes with regard to early failure of the Fontan operation. Prior to this report, in 1985, Girod et al. [4] reported that there was no difference in operative mortality rates between patients with a PA index of less than 250 mm2/m2 and its counterpart, and warned that patients with a PA index below this cut-off line should not necessarily be excluded from consideration for the Fontan operation. They measured PA size intra-operatively; this was supported by an opinion that preoperative angiographic assessment could be subject to underestimation particularly when the pulmonary blood flow was reduced [12]. The minimal PA index in their series was not smaller than 188 mm2/m2. In 1989, Bridges et al. [5] also used the comparable PA index, preoperatively determined by echocardiography in their situation, for a comparative study and found no difference in operative mortality between 23 survivors and 6 non-survivors. In their series, the smallest PA index permitting survival was as low as 48 mm2/m2.

This controversial topic can be partially questioned from the viewpoint whether PA size at the hilum could be a good representative of the whole PA vascular bed. It is generally accepted that the major component of pulmonary vascular resistance is found not at the central PA level but at the arteriolar level unless the central PA is imbalancedly and restrictively small [13]. Some extreme cases could have born a discrepancy between the central PA size and the degree of development of the arteriolar vasculature. Assuming that the hilar PA sizes reasonably represent the intra-pulmonary vascular development, we are clearly able to address that a PA index 250 mm2/m2 is not a definite cut-off line for surgical indication of the Fontan procedure. Judging from our present data, the PA size does not grow in proportion, as maintaining the same PA index, after the Fontan procedure. In the healthy normal individual, in theory, the PA index should slightly increase with growth (Fig. 2 ). This plotting is based on the anticipated normal PA size and its cross-sectional area calculated from body surface area by Sievers et al. [14].


Figure 2
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  		Fig. 2. Theoretically anticipated pulmonary arterial (PA) index in a normal individual and its relation with patient's data. According to the anticipated normal values for right PA diameter and left PA cross-sectional area by Sievers et al. [13], an estimate trend in PA index (Nakata index) change was illustrated. The formulas used are shown below.
r-PA diameter (mm) = 14.6 x BSA0.586
r-PA area (mm2)* = {pi}(r-PA diameter/2)2 = 53.3{pi} x BSA1.172
l-PA area (mm2) = 0.86 x r-PA area + 4.5

*On the basis of the assumption that PA is round shape.

Figure 2

Both Group-S and Group-L were subdivided into three sub-groups according to preoperative BSA (Group-S, initial BSA < 0.5, n = 29: preoperative 204 ± 35 to postoperative 190 ± 61 mm2/m2; Group-S, 0.5 less double equals initial BSA < 1.0, n = 23: 203 ± 35–170 ± 46 mm2/m2, respectively; Group-S, initial BSA greater double equals 1.0, n = 4: 151 ± 45 to 147 ± 63 mm2/m2, respectively; Group-L, initial BSA<0.5, n = 35: 365 ± 100–257 ± 88 mm2/m2, respectively; Group-L, 0.5 less double equals initial BSA < 1.0, n = 16: 353 ± 67–244 ± 75 mm2/m2, respectively; Group-L, initial BSA greater double equals 1.0, n = 6: 370 ± 131–308 ± 66 mm2/m2, respectively). In each sub-group, changes in pre- and postoperative PA index (mean ± standard deviation) were indicated. r-PA, right pulmonary artery; BSA, body surface area; l-PA, left pulmonary artery; PA, pulmonary artery.

 
To the best of our knowledge, there has been no real report published describing the consecutive change in PA sizes long after the Fontan operation. In the setting of the BDG physiology, it has been described that the PA index may regress probably associated with a decreased amount of pulmonary blood flow [15–17]. On the same analogy, the regression in the PA index after the Fontan procedure is likely related to its peculiar low cardiac output status and non-pulsatile flow within the central PA because of the lack of a pumping chamber for the pulmonary circulation. In other words, this is a process of natural PA remodeling in which PA adjust its sizes in response to the amount of blood passing through it. As far as hemodynamics is maintained efficiently, a PA size is deemed above a required level for that particular Fontan circulation.

In this respect, one simple question came up to our mind with regard to which degree of the underdeveloped PA affected efficacy of the Fontan circulation in the longer term. Criteria for the successful Fontan procedure in the early phase is undoubtedly one important aspect, and a required PA size is another, since at the time of surgery invasive procedures and maneuvers, not only surgical but also for anesthetic and intensive care managements, should require a certain extra margin so as to recover securely from acute injury or reactions and to overcome artificial circumstances such as positive airway pressure on mechanical ventilation. Very few reports are available in the literature in the light of relation between the PA size and the functional efficacy of the Fontan circulation in the intermediate or long terms. From our results, there was a trend toward a higher incidence of hypoproteinemia in Group-S (5% in Group-S and 2% in Group-L). This could have been of clinical significance had the episodes been resistant to medical treatments. Severe protein-losing enteropathy could be regarded as failure of Fontan circulation. Nonetheless, this was not the case in our patients, at least at the current stage. Although we failed to determine a minimally required PA index for the Fontan circulation, even patients with PA index below 150 mm2/m2 turned out to be doing as actively as the other patients. In case the PA index is continuously coming down still further in the future and beyond a critical level for the efficient Fontan circulation at some stage, some or all patients might deteriorate because of circulatory restriction posed by the pulmonary arterial dimension. We hope this pessimistic story should not be the case. With an adequate amount of blood flow across the lungs to live on, the PA vascular bed ought to be maintained, at least, against excessive regression beyond a mortal level. Anyway, we unequivocally need far longer investigations whether the currently observed tendency of decrease in the PA index exceeds beyond a morbid level in the future or not.

Another question that came up to our mind was whether a PA size issue could be directly transferred into the era of the staged Fontan strategy. The above-mentioned studies on PA sizes for the Fontan criteria were conducted between the mid-80s and the early 90s, which was the era of the primary Fontan approach. It is well known that adaptation of the heart to the circulation in which the right heart is totally bypassed is better owing to the staged approach [18], and the procedure for the Fontan completion can be less invasive. Together with other modifications to make the Fontan procedure securer and less invasive [7–9,17–24], the Fontan indication has been expanded. The PA size issue is undoubtedly among the criteria to be reset. We strongly believe that establishment of the Fontan circulation in an off-pump fashion is one of the pertinent technical options. Inflammatory reaction was less intense and deleterious influence was calmer onto the pulmonary circulation after the off-pump Fontan [20]. We take this as an advantageous point particularly for patients who possess a smaller reservoir for the pulmonary circulatory capacity. Introduction of the off-pump Fontan in 1996 affected our PA size criteria; 96% of patients (55 out of 57) in Group-S underwent the Fontan completion after 1996, and in two thirds of these (36 of 55) cardiopulmonary bypass was not used. Because of the extended background indication, we needed to evaluate the hypothesis that a smaller PA index did not inevitably produce functional impediments in the longer terms.

Nowadays, some surgeons comment that PA sizes are no longer a limiting factor or cannot be used as a criterion because of the staged approach. In reality, a PA index would not represent the situation of the intra-pulmonary vasculature when an extensive PA reconstruction is to be carried out at the time of the hemi-Fontan procedure [24]. This is particularly true if such a PA augmentation extends beyond the hilar level. In our present series, all patients underwent bidirectional cavopulmonary anastomosis in an ordinary fashion rather than the hemi-Fontan maneuver, and no extensive PA augmentation was employed beyond the hilar PA. The measured PA index, accordingly, was regarded as a reasonably representative parameter for the condition of the lung vascular bed.

Obvious limitations of this study include its retrospective nature. There are major changes in our principal strategy for the Fontan operation due to the length of the period over which this study was completed, as described in Section 2. These changes should be considered as another limitation of this study due to possible impact on the patient's outcomes. Higher prevalence of fenestration use in patients with smaller PA might be another factor, because fenestration could affect not only early but also longer term results [25]. Such differences preclude us from the statistical analysis with patients having larger PA. Nonetheless, the results from the current review were rather encouraging, since we had expected more pessimistic situation even in the intermediate term.


   6. Conclusion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Conclusion
Appendix A
 References
 
The outcome after the Fontan completion, including functional ones in the intermediate term, was acceptable in patients having a preoperative PA index smaller than 250 mm2/m2. The PA index was still decreasing after establishment of the Fontan circulation over time, but this phenomenon did not appear to be associated with obvious functional impediments.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
References
 
Conference discussion

Dr G. Ziemer, (Tuebingen, Germany): Well, it is very interesting to hear this, but when I was taught to do this operation some 25 years ago, I was told that anatomy is one thing but functional parameters like pressures may be even more important. So, I never knew how to calculate these indices, and this is what I was taught by Dr Castaneda. So, you may have even huge pulmonary arteries with high pressure, for instance, after some big central shunt. As you have good surgical results, maybe you made a good selection, not only guided by your indices claimed.

My question would be, were there patients who were presented to you for possible Fontan operation who you turned down? And if there were these patients, were there patients with big pulmonary arteries and were there patients with small pulmonary arteries? Again, I don’t even know how to calculate these values and we have pretty good results also.

Dr B. Maruszewski (Warsaw, Poland): If you could explain if there were patients whom you excluded from your Fontan because of the size, of the too small size of the pulmonary arteries. What were exclusion criteria for Fontan as far as the size of PAs?

Dr Adachi: The important thing I can say is that there is no patient in our series who was excluded from consideration for Fontan operation solely on the basis of small PA size. There were no patients.

Dr Maruszewski: Nowadays, how would you define the contraindication to the Fontan operation, as far as the PA size is concerned?

Dr Adachi: Basically, we don’t consider the PA size. In my opinion, PA index around 100 is enough to achieve Fontan circulation.


   Acknowledgments
 
We wish to express our appreciation for the statistical advice from Akiko Kada (General Clinical Research Unit, National Cardiovascular Center, Japan).


   Footnotes
 
\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 

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