Skip to main content
PLOS One logoLink to PLOS One
. 2020 Feb 24;15(2):e0229396. doi: 10.1371/journal.pone.0229396

Preoperative nutritional evaluation of patients with hepatic alveolar echinococcosis

Xie Liang 1,2, Wang Shu 3, Zhou Linyong 4, Li Jianshui 1,2, Gu Junqing 3, Dawa Enzhu 4, Xu Mingqing 5,*
Editor: Dong-Xin Wang6
PMCID: PMC7039506  PMID: 32092109

Abstract

Objective

This study is aimed at determining the preoperative nutritional status of patients with hepatic alveolar echinococcosis (HAE), and subsequently establish a concise and reasonable nutritional evaluation indicator. The established evaluation method could be used for clinical preoperative risk assessment and prediction of post-operation recovery.

Methods

The basic patient information on height, body weight, BMI and hepatic encephalopathy of 93 HAE patients were examined. Subsequently, abdominal ultrasonography, blood coagulation and liver function tests were done on the patients. Liver function was assessed using the Child-Pugh improved grading method while nutritional status was evaluated using the European Nutrition Risk Screening 2002 (NRS 2002) method. Additional parameters including hospitalization time, the hemoglobin (HGB) level on the 3rd day after the operation, and the number of postoperative complications of HAE patients were also recorded.

Results

The NRS 2002 score was negatively correlated with body weight, body mass index (BMI)and albumin (ALB) (P<0.01), and positively correlated with the transverse and longitudinal diameters of the lesions (P<0.01). A worse grading of liver function was associated with a low ALB and a high NRS 2002 score (P<0.01). Results of the NRS 2002 score indicate that the hospitalization time of the normal nutrition group was significantly shorter than that of the malnourished group (P < 0.05). The HGB level of the control group on the 3rd day after the operation was significantly higher than that of the malnourished group (P < 0.05), and the number of postoperative complications was lower than that of malnutrition group (P < 0.05).

Conclusion

Malnutrition is common in HAE patients. The nutritional status of HAE patients is related to many clinical factors, such as Child-Pugh classification of liver function, size of the lesion, and ALB among others. Although both BMI and ALB can be used as primary screening indicators for malnutrition in HAE patients, NRS 2002 is more reliable and prudent in judging malnutrition in HAE patients. Therefore, BMI and ALB are more suitable for preoperative risk assessment and prediction of postoperative recovery.

Introduction

Hepatic echinococcosis (HE) is an endemic helminthic disease categorized into hepatic cystic echinococcosis (HCE) and hepatic alveolar echinococcosis (HAE). Among the two forms of HE, HAE is the most life-threatening. Hepatic alveolar echinococcosis (HAE) is caused by infection with the Echinococcus multilocular helminth [1, 2], and accounts for 3% of the total number of human echinococcosis [3]. The disease is characterized by a slow but concealed onset, and invasive growth, similar to hepatocellular carcinoma. Notably, HAE is commonly known as "worm cancer" and "parasitic liver cancer" [4]. In China, HAE is more prevalent in the Tibet Autonomous Region, Qinghai Province, and the Ganzi Tibetan Autonomous Prefecture. The disease is a chronic consumptive disease. Damage to the liver impairs the synthesis and metabolism of nutrients such as albumin. A decrease in blood albumin levels results in a reduction in body weight, a poor general condition of patients and the inability to tolerate surgical treatment [5].

Nutrition refers to the process by which the human body ingests and metabolizes food through digestion, absorption, and metabolism to maintain life activities. Nutrition forms the basis of sustaining normal physiological functions of the human body. Proper nutrition is crucial to tissue repair, and the provision of active immunity and resistance to diseases. Malnutrition refers to the insufficient intake or absorption of nutrients by the body caused by hunger, illness, aging and other factors. These factors lead to a decrease in body composition (fat-free cell population), changes in the somatic cell population, and a reduction in physiological function, which cause adverse clinical outcomes of patients [6]. The incidence of malnutrition in surgical patients ranges from 20% to 60%. Malnutrition compromises the body’s immune resistance to stressful events such as surgery and infection. Malnutrition also damages the function of body organs and tissues, increases the incidence of complications and mortality after the operation, increases medical expenses, prolongs hospitalization time, and affects the clinical outcomes of patients [7, 8].

Hepatic alveolar echinococcosis (HAE) operation is characterized by long operation time, high operation difficulty, many postoperative complications and slow postoperative recovery. As a result, the nutritional status of HAE patients before operation significantly affects the success or failure, and rapid recovery post-operation. Therefore, effective screening and diagnosis of malnutrition in HAE patients before the operation and provision of active interventions are paramount to patient recovery and significantly improves prognosis [9]. These findings are also in line with the concept of treatment and rehabilitation of Enhanced Recovery After Surgery (ERAS), which emphasizes perioperative nutritional support [10]. At present, there is no convincing and compelling evaluation system of the preoperative dietary status of HAE patients. This study explored the preoperative nutritional status of HAE patients to establish concise and practical nutritional evaluation indicators for preoperative risk assessment. The study also evaluated the relationship between nutritional indicators, general conditions, clinical indicators, and postoperative recovery indicators of HAE patients.

Objects and methods

Objects

A total of 93 patients diagnosed with HAE during a hepatic echinococcosis screening project in Ganzi People's Hospital in April 2019 were included in this study. The study participants included 42 males and 51 females. The inclusion criteria included Tibetan patients diagnosed with HAE, of sound mind and could respond to questions appropriately, and who were available for the entire study period. The exclusion criteria included patients with malnutrition caused by other previous diseases and patients with HCE or other liver lesions such as hepatic hemangioma and hepatocellular carcinoma. Also excluded were patients with infectious diseases (respiratory tract infection, pulmonary infection, etc.) or other chronic consumptive diseases, and patients with other organ echinococcosis.

Methods

This study has been approved by the Medical Ethics Committee of the Affiliated Hospital of North Sichuan Medical College. All patients have been informed suitably, and we've asked for their verbal consent. We've obtained consent from parents or guardians when our study included minors under age 18.

Inspection indicators

The basic information of height, weight, occupation, nationality and information on the existence of hepatic encephalopathy were recorded in all patients. The location, number, transverse diameter, longitudinal diameter and the ascites status of hepatic alveolar echinococcosis (HAE) masses were assessed by abdominal ultrasonography. Blood routine, coagulation routine and liver function tests were performed to determine the patients’ hemoglobin (HGB), aspartate aminotransferase (AST), alanine aminotransferase (ALT), total bilirubin (TBIL), albumin (ALB) and prothrombin (PT). The hospitalization time, HGB value on the third day after the operation and the number of postoperative complications (including wound liquefaction and infection, lung infection, abdominal and liver wound infection, urinary tract infection, postoperative inflammatory intestinal obstruction, bile leakage and acute liver function injury) were recorded.

Classification of the standard of liver function

The Child-Pugh improved grading method was used for grading liver function [11]. The grading of liver function was calculated by measuring TBIL, ALB, PT, ascites and hepatic encephalopathy. The Child-Pugh grade A patients, 5–6 points, had a better liver function, grade B, 7-9points, had a moderate liver function, while grade C, 10–15 points, had severe damage on liver function.

Evaluation method of nutritional status

A body mass index (BMI) ≧ 24.0(Kg/m2) was defined as overweight, while BMI < 18.5 (Kg/m2) was defined as malnutrition. The nutritional status of patients was assessed by the European Nutrition Risk Screening 2002 (NRS 2002) [12]. Nutritional status parameters included recent weight changes, BMI, the severity of disease and feeding status. Patients with a total score ≧3 were assessed as having malnutrition risk (need to formulate reasonable clinical nutrition support plan) while an overall NRS score <3 was interpreted as no nutrition risk hence did not require clinical nutrition support, but concurrent screens were needed [13].

Statistical methods

All data were input and analyzed by statistical software SPSS17.0 (SPSS Inc., Chicago, IL, USA). Continuous data were presented as Mean±standard deviation. Correlations between nutritional indicators and patients' general condition, and ultrasonography results and hematological indicators were determined using Pearson correlation analysis. The LSD test was used for multiple comparisons of liver function classification and nutritional indicators. Student's T-test was used to compare the postoperative recovery indicators between groups.

Results

General conditions of study objects

A total of 93 patients aged 12–81, and of Tibetan origin were included in this study. The patients had an average age of 44.66±14.40 years; 42 males (45.16%) and 51 females (54.84%) height range of 140–183 cm, and an average height of 162.45±9.223cm. The weight of included patients ranged between 34 and 90 kg, with an average weight of 63.33±11.690kg. Data on the BMI, NRS 2002 score, liver function classification, serum ALB value, location, and the number of liver hydatid lesions are as shown in Table 1. The transverse and longitudinal diameters of liver hydatid lesions, serum ALT, AST, ALB, TBIL and blood HGB values are presented in Table 2.

Table 1. General conditions of patients.

Indicator Group N Percentage
sex male 42 45.16%
female 51 54.84%
BMI Overweight (BMI < 24) 41 44.09%
Normal (18.5 < BMI < 24) 46 49.46%
Malnutrition (BMI < 18.5) 6 6.45%
NRS 2002 score ≥3 34 36.56%
<3 59 63.44%
Classification of liver function Grade A group 58 62.37%
Grade B group 29 31.18%
Grade C group 6 6.45%
ALB Normal (ALB≥35g/L) 81 87.10%
Malnutrition ALB<35g/L) 12 12.90%
location of liver hydatid lesions Right lobe 65 69.90%
Left lobe 11 11.83%
Both left and right lobes 17 18.28%
number of liver hydatid lesions 1 73 78.50%
2 11 11.83%
≥3 9 9.68%

Table 2. Ultrasonography and hematological indicators of patients.

Indicator N min max Mean Std. Deviation
transverse diameters (cm) 93 1.2 16.4 5.957 3.2631
longitudinal diameters (cm) 93 1.1 17.2 4.894 2.8891
ALT (u/L) 93 3.0 144.0 39.989 30.0077
AST (u/L) 93 7.0 131.0 23.931 18.2513
ALB (g/L) 93 28.5 55.8 42.569 6.5359
TBIL (umol/L) 93 5.2 65.0 11.968 8.0408
HGB (g/L) 93 110 192 151.59 21.257

Analysis of the correlation between nutritional indicators and general conditions, ultrasonography and hematological indicators of patients

Results on the Pearson correlation analysis between nutritional indicators general conditions and morphological indicators of the lesion are shown in Table 3. It was found that the NRS2002 score was negatively correlated with body weight, BMI and ALB (P < 0.01), and positively correlated with the transverse and longitudinal diameter of the lesion (P < 0.01). The body mass index (BMI) was positively correlated with serum ALB, body weight and age (P < 0.01). Serum ALB was positively associated with body weight and BMI (P < 0.01), and negatively correlated with transverse and longitudinal diameters of lesions (P < 0.01).

Table 3. Pearson correlation analysis between nutritional indicators and general conditions and morphological indicators of lesions.

NRS2002 score BMI ALB body weight height age location of liver hydatid lesions number of liver hydatid lesions transverse diameters longitudinal diameters
NRS 2002 score Pearson correlation 1 -.338** -.481** -.352** -.123 .030 .161 .129 .348** .338**
Sig. (2-tailed) .001 < .001 .001 .241 .776 .124 .220 .001 .001
N 93 93 93 93 93 93 93 93 93 93
BMI Pearson correlation -.338** 1 .341** .789** .002 .359** .142 .117 -.088 -.100
Sig. (2-tailed) .001 .001 < .001 .985 < .001 .174 .265 .402 .342
N 93 93 93 93 93 93 93 93 93 93
ALB Pearson correlation -.481** .341** 1 .372** .136 .151 -.078 -.070 -.360** -.372**
Sig. (2-tailed) < .001 .001 < .001 .193 .149 .459 .504 < .001 < .001
N 93 93 93 93 93 93 93 93 93 93
body weight Pearson correlation -.352** .789** .372** 1 .602** .221* .047 .055 -.055 -.062
Sig. (2-tailed) .001 < .001 < .001 < .001 .034 .654 .597 .599 .558
N 93 93 93 93 93 93 93 93 93 93

**. Correlation is significant at the 0.01 level (2-tailed).

*. Correlation is significant at the 0.05 level (2-tailed).

The Pearson correlation analysis of nutritional indicators and hematological test indicators are shown in Table 4. It was found that there was no significant correlation between NRS 2002 score, BMI, serum ALB and AST, ALT, TBIL, HGB value in the blood (P > 0.05), and there was a significant positive correlation between body weight and blood ALT value (P < 0.01).

Table 4. Pearson correlation analysis between nutritional indicators and hematological indicators.

NRS 2002 score BMI ALB body weight ALT AST TBIL HGB
NRS 2002 score Pearson Correlation 1 -.338** -.481** -.352** .073 .196 .155 -.156
Sig. (2-tailed) .001 < .001 .001 .485 .059 .137 .136
N 93 93 93 93 93 93 93 93
BMI Pearson correlation -.338** 1 .341** .789** .188 -.024 -.121 -.120
Sig. (2-tailed) .001 .001 < .001 .071 .820 .250 .253
N 93 93 93 93 93 93 93 93
ALB Pearson correlation -.481** .341** 1 .372** .101 -.124 -.145 -.022
Sig. (2-tailed) < .001 .001 < .001 .333 .237 .166 .831
N 93 93 93 93 93 93 93 93
body weight Pearson correlation -.352** .789** .372** 1 .355** .051 -.042 -.013
Sig. (2-tailed) .001 < .001 < .001 < .001 .627 .691 .898
N 93 93 93 93 93 93 93 93

**. Correlation is significant at the 0.01 level (2-tailed).

*. Correlation is significant at the 0.05 level (2-tailed).

The results of LSD multiple comparisons between liver function classification and nutritional indicators are presented in Table 5. It was found that there were significant differences in NRS2002 score, body weight, BMI and serum ALB between Grades A and B patients (P < 0.01), and also between Grades A and C patients. The NRS2002 score and serum ALB of Grade B patients significantly differed from the scores of Grade C patients (P < 0.05).

Table 5. Multiple LSD comparisons of liver function classification and nutritional indicators.

dependent variable (I) liver function classification (J) liver function classification Mean Difference (I-J) Std. Error Sig. 95% Confidence Interval
Lower Bound Upper Bound
NRS 2002 score A B -1.828* .245 < .001 -2.31 -1.34
C -2.856* .463 < .001 -3.78 -1.94
B A 1.828* .245 < .001 1.34 2.31
C -1.029* .484 .036 -1.99 -.07
C A 2.856* .463 < .001 1.94 3.78
B 1.029* .484 .036 .07 1.99
BMI A B 2.7931* .7436 < .001 1.316 4.270
C 5.1161* 1.4022 < .001 2.330 7.902
B A -2.7931* .7436 < .001 -4.270 -1.316
C 2.3230 1.4665 .117 -.590 5.236
C A -5.1161* 1.4022 < .001 -7.902 -2.330
B -2.3230 1.4665 .117 -5.236 .590
body weight A B 9.621* 2.404 < .001 4.85 14.40
C 14.609* 4.532 .002 5.60 23.61
B A -9.621* 2.404 < .001 -14.40 -4.85
C 4.989 4.740 .295 -4.43 14.41
C A -14.609* 4.532 .002 -23.61 -5.60
B -4.989 4.740 .295 -14.41 4.43
ALB A B 8.9586* .9574 < .001 7.057 10.861
C 14.8006* 1.8053 < .001 11.214 18.387
B A -8.9586* .9574 < .001 -10.861 -7.057
C 5.8420* 1.8881 .003 2.091 9.593
C A -14.8006* 1.8053 < .001 -18.387 -11.214
B -5.8420* 1.8881 .003 -9.593 -2.091

*. The mean difference is significant at the 0.05 level.

Comparative analysis of postoperative recovery indicators between normal nutrition group and malnutrition group

A total of 74 patients (79.57%) completed the operation, while the other 19 patients (20.43%) were not admitted to the hospital because of various complexities surrounding the operation (7.45%, n = 7). The complexities included family factors (5.32%, n = 5), religious factors (4.26%, n = 4), economic factors (2.13%, n = 2), and remote medical treatment (1.06%, n = 1). Details on the grouping characteristics and the comparative analysis of postoperative recovery indicators between the normal nutrition group and the malnutrition group are presented in Tables 1 and 6, respectively. As shown in Table 6, the NRS 2002 nutrition scores indicate that there were no statistical differences in pre-operation HGB levels between the two groups (P>0.05). Compared to the normal nutrition group, hospitalization time and HGB levels on the third day after operation were significantly shorter (P < 0.05), and significantly higher (P < 0.05), respectively than in the malnutrition group. Also, the number of postoperative complications was lower than that of the malnutrition group (P < 0.05). However, no significant differences in BMI and ALB were noted between the two groups (P > 0.05).

Table 6. A comparative analysis of postoperative recovery indicators between normal nutrition group and malnutrition group.

postoperative recovery indicators NRS 2002 t P BMI t P ALB t P
Normal nutrition group (63.5%, n = 47) Malnutrition group (36.5%, n = 27) Normal nutrition group (93.2%, n = 69) Malnutrition group (6.8%, n = 5) Normal nutrition group (87.8%, n = 65) Malnutrition group (12.2%, n = 9)
hospitalization time (day) 10.4681 11.9259 4.030 < .001* 10.9855 11.2000 -.279 .781 10.9077 11.6667 -1.302 .197
HGB on the 3rd day after operation (g/L) 135.2340 120.9630 -3.127 .003* 130.8696 118.4000 1.354 .180 131.6308 118.4444 1.886 .063
Postoperative complications (person time) .2128 .4444 2.002 .049* .3043 .2000 .458 .648 .2923 .3333 -.234 .815

*. The mean difference is significant at the 0.05 level.

Discussion

Selection of nutritional indicators

Four nutritional indicators, including body weight, body mass index (BMI), albumin (ALB) and NRS2002 score values, were selected based on the ease of clinical access. Although body weight is one of the most intuitive nutritional indicators, it can only reflect one aspect of human characteristics. Assessment of the body mass index (BMI), which also considers the height factor, has become the most widely used nutritional evaluation method. According to the 2015 European Society for Parenteral and Enteral Nutrition (ESPEN) proposal, both weight and BMI should be used as diagnostic indicators of malnutrition [14]. However, long-term clinical practice has proved that the nutritional status of patients can conveniently be assessed by BMI alone, although significant differences in the reliability of BMI for different populations has been reported [15]. Individual differences and dietary habits affect the relationship between BMI and body function; hence, the composition of the human body is not constant. For example, the patients included in this study are Tibetans who dwell in pastoral areas. Their physical fitness, dietary habits, lifestyle, and exercise intensity are quite different from those of the Han nationality. Therefore, the BMI of Tibetans is generally higher than their actual nutrition. Among such individuals, some deviations exist in the status, and it is difficult to accurately reflect recent changes in body weight and preoperative nutritional status.

Subsequently, this study incorporated the NRS 2002 score, which is grounded on many evidence-based medical reports and is closely related to clinical prognosis. The score is suitable for adult or elderly community patients and inpatients and has high sensitivity, better specificity and a lower rate of false positives as compared to BMI. The NRS 2002 sore is a simple and highly operational screening method [1618]. In this study, the NRS 2002 survey of hepatic alveolar echinococcosis (HAE) of pre-operation patients was completed when the patients were admitted for history-taking and physical examination. The assessment for each patient only took 5–10 minutes. As such, we identified the malnourished patients for the first time, without incurring any additional costs and without incorporating any invasive operation.

The liver is the main body organ involved in the synthesis of albumin (ALB), and HAE can affect protein synthesis in the liver. As a result, serum ALB levels reflect the severity of HAE. An ALB < 35g/L indicates hypoproteinemia and induces malnutrition. Also, persistent hypoproteinemia is an essential objective indicator of malnutrition [19]. Since ALB has a half-life of about 20 days, ALB levels can be conveniently used as a measure of chronic malnutrition.

Relationship between nutritional status and postoperative recovery indicators of HAE patients

According to the results of the NRS 2002, BMI and ALB, HAE patients were divided into two groups: normal nutrition and malnutrition groups. Statistical differences in the postoperative recovery indicators between the groups were only observed in the NRS 2002 scores. The hospitalization time of the malnutrition group was longer, the hemoglobin level (HGB) was lower on the 3rd day after the operation, and the number of postoperative complications was higher. It can be seen that NRS 2002 is a reliable method to predict the postoperative recovery. According to the BMI or ALB results, the hospitalization time of the malnutrition group was slightly longer than that of normal nutrition group. Also, the HGB of the malnutrition group on the 3rd day after the operation was marginally lower than that of the normal nutrition group. However, the differences in both hospitalization time and hemoglobin levels between the two groups were not statistically significant. The lack of substantial differences in the two parameters could be caused by the small sample size used in our study, and the fact that BMI and ALB are less sensitive in the prediction of postoperative recovery.

Based on NRS 2002, malnourished HAE patients can be identified before operation by an NRS 2002 score ≥3. For such patients, substantial nutritional support and treatment should be provided before the surgery, and they suggested that the operation time should be postponed until the NRS 2002 scores of the patients improve. As such, the patient can better tolerate surgery and anesthesia, and the disease prognosis is improved. Also, the incidence of surgical complications and mortality are reduced, medical costs are reduced, and the hospitalization time is shortened [20].

Analysis of the nutritional status of HAE patients and their relationship with clinical indicators

When BMI and ALB were used as evaluation indicators, the malnutrition rate of patients was 6.45% and 12.90% respectively, which was increased when NRS 2002 was used (36.56%). The sensitivity of BMI and ALB in assessing malnutrition of HAE patients is lower than that of NRS 2002. The disparity in the outcome from the different parameters may be because Tibetans in pastoral areas prefer high-protein beef, mutton and dairy products. Also, their body is better adapted to high altitude hypoxic environments, and their exercise intensity is higher. Considering their BMI and ALB, HGB baseline values are slightly higher than those of Han nationality people of the same age [21, 22]. Therefore, the NRS 2002 method is more reliable and prudent in assessing malnutrition of HAE patients, but it may also have a lower sensitivity. However, BMI and ALB can be used as screening indicators for clinical reference.

In this study, 36.56% of HAE patients were malnourished, which may be due to the following reasons:

  1. The granulomatous reaction caused by Echinococcus multilocular can cause severe pathological damage to normal hepatocytes. Besides, HAE can cause various inflammatory cell infiltration and necrosis, while producing toxins that damage liver tissue, which causes extensive liver fibrosis [23]. Systematic infection and invasion of hepatocytes by Echinococcus multilocular cause disorders in nutrient synthesis and metabolism, resulting in malnutrition in HAE patients. The findings of this study revealed that a worse grading of liver function is associated with a lower ALB and a higher NRS2002 score. These findings indicate that the impairment of liver function caused by HAE is directly related to malnutrition in HAE patients.

  2. In HAE patients, the continuous proliferation of liver lesions forms fibrous connective tissue "mass" and inflammatory granulation tissue, that depress the bile ducts and blood vessels in regions adjacent to the liver. These tissues protrude from the surface of the liver and squeeze the adjacent digestive tract, resulting in a series of complications, such as pain around the organ, portal hypertension, obstructive jaundice, bloating, and nausea. Vomiting and other discomforts [24] affects the patient's ability to eat and absorb nutrients from the digestive tract, further aggravating the poor nutritional status of patients. In this study, we found that the larger the transverse and longitudinal diameters of liver lesions in HAE patients, the higher the NRS2002 score (P < 0.01) and the lower the ALB value (P < 0.01). However, the NRS2002 score, BMI and ALB were not significantly correlated to the number and location of liver lesions. These results show that the larger the size of the injury, the more the invasion and compression of the adjacent bile ducts, blood vessels and digestive tract, which cause the complications mentioned above, and subsequent malnutrition.

  3. Liver lesions in HAE patients stimulate the formation of adhesions within the nervous-rich liver capsule, which leads to chronic pain such as dull pain or swelling pain in the regions surrounding the liver. Subsequently, patients are more prone to depression, insomnia, anxiety and other negative emotions. Several other comprehensive psychological and physiological disorders, such as insomnia, oil-weariness, anorexia, long-term bed-rest, and reduced daily activities then arise. These disorders eventually lead to reduced diet regimes, slow gastrointestinal peristalsis, reduced nutrient absorption and utilization rates, and worsened the nutritional status of patients [25].

  4. The inhabitants of the Tibetan plateau are highly prone to developing HAE. The pastoral Tibetans have backward economic conditions, poor hygiene quality, low education level and strong religious beliefs. Due to this combination of factors, the individuals are not keen to identify diseases at an early stage, resulting in an increase in chronic liver function damage by the time patients seek medical attention. This study found that there was no significant correlation between NRS2002 score, BMI, serum ALB value and blood AST, ALT, TBIL value (P > 0.05). However, AST, ALT and TBIL are indicators of acute liver damage, which indicates that the nutritional status of HAE patients is less related to whether they have acute liver damage but closely associated with chronic liver damage.

Conclusions

Malnutrition is highly prevalent among hepatic alveolar echinococcosis (HAE) patients, and the nutritional status of HAE patients is related to many clinical factors, such as Child-Pugh classification of liver function, lesion size, and serum albumin. While the body mass index (BMI) and albumin (ALB) can be used as primary screening indicators for malnutrition in HAE patients, the NRS 2002 method may be more reliable and prudent in assessing nutrition in HAE patients. Also, the NRS 2002 method is more suitable for clinical preoperative risk assessment and prediction of postoperative. The proper evaluation of the preoperative nutritional status of HAE patients is recommended in the concept of perioperative dietary support of Enhanced recovery after surgery (ERAS). Besides, the assessment minimizes the risks associated with anesthesia and surgery, shortens the hospitalization time, reduces the incidence of postoperative complications, and improves the prognosis of patients.

Supporting information

S1 Table. List of basic information of HAE patients.

(XLS)

S1 File. CONSORT 2010 flow diagram.

(DOC)

S2 File. PLOSOne_Clinical_Studies_Checklist.

(DOCX)

S3 File. STROBE_checklist_v4_combined_PlosMedicine.

(DOCX)

S4 File. Trendstatement_TREND_Checklist.

(DOCX)

Data Availability

All relevant data are in the paper and Supporting Information files.

Funding Statement

This research is supported by the project of Sichuan Province health and Family Planning Commission (17PJ106)

References

  • 1.Nunnari G, Pinzone MR, Gruttadaurias et al. Hepatic echinococcosis: clinical and therapeuticaspects [J]. World J Gastroenterol, 2012, 18 (13): 1448–458. 10.3748/wjg.v18.i13.1448 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Guo YM, Zhu WJ, Zhao SY, et al. Surgical treatment strategy for complex hepatic echinococcosis: a review [J]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi, 2018, 30 (6):705–708. 10.16250/j.32.1374.2018169 [DOI] [PubMed] [Google Scholar]
  • 3.Bhutani N, Kajal P. Hepatic echinococcosis: A review [J].Ann Med Surg (Lond). 2018,36:99–105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Parsak CK, Demiryurek HH, Inal M, et al. Alveolar hydatid disease: imaging findings and surgical approach[J]. Acta Chir Belg, 2007, 107 (5): 572–577. 10.1080/00015458.2007.11680128 [DOI] [PubMed] [Google Scholar]
  • 5.Surgical treatment strategies for hepatic alveolar echinococcosis [J]. Salm L.A., Lachenmayer A., Perrodin S.F., Candinas D., Beldi G. Food and Waterborne Parasitology, 2019. 10.1016/j.fawpar.2019.e00050 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Cederholm T, Barazzoni R, Austin P, et al. ESPEN guidelines on definitions and terminology of clinical nutrition [J]. Clin Nutr, 2017, 36 (1): 49–64. 10.1016/j.clnu.2016.09.004 [DOI] [PubMed] [Google Scholar]
  • 7.van Stijn MF, Korkic-Halilovic I, Bakker MS, et al. Preoperative nutrition status and postoperative outcome in elderly general surgery patients: a systematic review [J]. J Parenter Enteral Nutr, 2013, 37 (1): 37–43. [DOI] [PubMed] [Google Scholar]
  • 8.Bresnahan KA, Tanumihardjo SA, Undernutrition, the acutephase response to infection, and its effects on micronutrient status indicators [J]. Adv Nutr, 2014, 5 (6):702–711. 10.3945/an.114.006361 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Brady M, Kinn S, Stuart P. Preoperative fasting for adults toprevent perioperative complications [J]. Cochrane DatabaseSyst Rev, 2003, (4):CD004423. [DOI] [PubMed] [Google Scholar]
  • 10.Chinese Expert Group on Enhanced Recovery After Surgery. Expert consensus on perioperative management of Enhanced Recovery After Surgery in China (2016)[J]. Chin J Surg, 2016, 54(6):335–337.27143201 [Google Scholar]
  • 11.Hackl C, Schlitt H J, Renner P. Liver surgery in cirrhosis and portal hypertension [J]. World J Gastroenterol. 2016;22(9):2725–35. 10.3748/wjg.v22.i9.2725 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Kondrup J, Rasmussen H H, Hamberg O, et al. Nutritional risk screening (NRS 2002): a new method based on an analysis of controlled clinical trials[J]. Clinical Nutrition, 2003, 22(3):321–336. 10.1016/s0261-5614(02)00214-5 [DOI] [PubMed] [Google Scholar]
  • 13.Puneeta T, Maitreyi R, Marina M, et al. A practical approach to nutritional screening and assessment in cirrhosis[J]. Hepatology,2017,65(3). [DOI] [PubMed] [Google Scholar]
  • 14.Cederholm T, Bosaeus I, Barazzoni R, et al. Diagnostic criteriafor malnutrition—An ESPEN consensus statement [J]. Clin Nutr, 2015, 34 (3):335–340. 10.1016/j.clnu.2015.03.001 [DOI] [PubMed] [Google Scholar]
  • 15.Deshmukh VR1, Kulkarni AA. Body Image and its Relation with Body Mass Index among Indian Adolescents. [J]. Indian Pediatr. 2017, 54(12):1025–1028. 10.1007/s13312-017-1205-0 [DOI] [PubMed] [Google Scholar]
  • 16.Liu N, Fang Y, Li ZY, et al. The application and clinical significance of PG-SGA and NRS 2002 in perioperative nutritional assessment of patients with gastrointestinal tumor[J]. Parenteral & Enteral Nutrition, 2016, 23(6):346–350. [Google Scholar]
  • 17.Li XY, Yu K, Yang Y, et al. Nutritional risk screening and clinical outcome assessment among patients with community- acquired infection: A multicenter study in Beijing teaching hospitals [J]. Nutrition, 2016, 32 (10):1057–1062. 10.1016/j.nut.2016.02.020 [DOI] [PubMed] [Google Scholar]
  • 18.Hertlein L, Kirschenhofer A, Fürst S, et al. Malnutrition and clinical outcome in gynecologic patients[J]. Eur J Obstet Gynecol Reprod Biol, 2014, 174(1):137–140. [DOI] [PubMed] [Google Scholar]
  • 19.Sibel T, Ahmet C, Osman D. spectroscopic investigations of the interactions of tramadol hydrochloride and 5-azacytidine drugs with human serum albumin and human hemoglobin proteins [J]. J Photochen Photobiol B, 2013,120(1):59–65. [DOI] [PubMed] [Google Scholar]
  • 20.Weimann A, Braga M, Carli Franco, et al. ESPEN guidelin:Clinical nutrition in surgery [J]. Clin Nutri, 2017(36):623–650. [DOI] [PubMed] [Google Scholar]
  • 21.Xu T, Han SM, Zhu GJ, et al. Comparison of Body Composition between Tibetan and Han Adolescents[J]. Medical Journal of Peking Union Medical College Hospital.2016. (02):110–114. [Google Scholar]
  • 22.Okumiya K, Sakamoto R, Ishimoto Y, et al. Glucose intolerance associated with hypoxia in people living at high altitudes in the Tibetan highland [J]. BMJ Open, 2016, 6: e009728 10.1136/bmjopen-2015-009728 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Zhang C, Wang J, Lü G, et al. Hepatocyte proliferation/growth arrest balance in the liver of mice during E. multilocularis infection: a coordinated 3-stage course.[J]. PLoS One. 2012;7(1):e30127 10.1371/journal.pone.0030127 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Lei JY, Hao JC, Wang WT, et al. Ex vivo liver resection followed by autotransplantation to a patient with advanced alveolar echinococcosis with a replacement of the retrohepatic inferior vena cava using autogenous vein grafting: a case report and literature review. Medicine (Baltimore), 2015, 94(7): e514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Hu J,Luo YL,Xiao FM,et al. Risk factors of malnutrition in patients with hepatic alveolar echinococcosis[J].J Prev Med Chin PLA, 2019(04):9–10. [Google Scholar]

Decision Letter 0

Dong-Xin Wang

23 Oct 2019

PONE-D-19-21935

Preoperative nutritional evaluation of patients with hepatic alveolar echinococcosis

PLOS ONE

Dear Mingqing,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. A major concern is that

your study did not compare the predictive effects of different nutritional assessment methods on surgical risk/clinical outcomes. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please be informed that the revision does not guarrantee the acception for publication.

We would appreciate receiving your revised manuscript by Dec 07 2019 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). This letter should be uploaded as separate file and labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.

We look forward to receiving your revised manuscript.

Kind regards,

Dong-Xin Wang

Academic Editor

PLOS ONE

Journal Requirements:

1. When submitting your revision, we need you to address these additional requirements.

Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

2. Please provide additional details regarding participant consent. In the ethics statement in the Methods and online submission information, please ensure that you have specified (1) whether consent was suitably informed and (2) what type you obtained (for instance, written or verbal). If your study included minors under age 18, state whether you obtained consent from parents or guardians. If the need for consent was waived by the ethics committee, please include this information.

3. We note that you have reported significance probabilities of 0 in places. Since p=0 is not strictly possible, please correct this to a more appropriate limit, eg 'p<0.0001'.

4. Thank you for sending us the data set underlying the results presented in your PLOS ONE submission. We notice that some of the information included in the data set may be potentially identifying. Please ensure that the data shared are in accordance with participant consent and provide only the data that are used in this specific study. To ensure patient confidentiality, we would recommend removing the columns with patient names. Additional guidance on preparing raw clinical data for publication can be found in our Data Policy FAQs (https://journals.plos.org/plosone/s/data-availability#loc-clinical-data).

5. Thank you for stating that “The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript” in your financial disclosure.

Please also provide the name of the funders of this study (as well as grant numbers if available) in your financial disclosure statement.

Please include your amended statements within your cover letter; we will change the online submission form on your behalf.

6. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information.

Comments to the Author

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

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: In the current manuscript, the authors evalued the nutritional status of 93 HAE patients retrospectively, to find a concise and reasonable nutritional evaluation indicator to serve the clinical preoperative risk assessment. And the results of the study showed that NRS 2002 may be more reliable and prudent than that of BMI or ALB level in judging malnutrition in HAE patients, and the nutritional status of HAE patients is related to many clinical factors, such as Child-Pugh classification of liver function, size of lesion, ALB and so on. The authors concluded that NRS 2002 is more suitable for preoperative risk assessment for HAE patients.

Overall, the current manuscript showed us some impressive information, e.g. "malnutrition is common in HAE patients", "compared to BMI and ALB, NRS 2002 can help diagnose more malnutrition in HAE patients".

However, there are still some issues that must be clarified to support the current conclusion drawn from the available results:

1. The purpose of the current study was to "find a concise and reasonable nutritional evaluation indicator" to find out the HAE patients with malnutrition, which could help serve the clinical preoperative risk assessment better, to guide preoperative nutritional support treatment and to reduce the risk of surgery for treatment of HAE. However, in the current study they did not compare the predictive effects of different nutritional assessment methods on surgical risk. It seems that they just considered NRS 2002 as the gold standard for diagnosis of malnutrition.

2. As mentioned before, no comparison was made to evaluate the predictive effects of different nutritional assessment methods (e.g. BMI, ALB, NRS 2002) on surgical risk of HAE, why the authors concluded that "NRS 2002 is more suitable for preoperative risk assessment for HAE patients"? Although NRS 2002 could diagnose more malnutrition patients than the other methods, this also means that with this indicator more HAE patients were not suitable for direct surgical treatment, unless a preoperative nutritional support was introduced. Is this consistent with the current status of HAE treatment (about 36.56% of the HAE patients should receive preoperative nutritional support before operation)? If so, the authors should state that point to emphasize the significance of this study, otherwise the results should be reinterpreted carefully, that maybe ALB or BMI, but not NRS 2002, is more suitable for preoperative risk assessment for HAE patients.

Reviewer #2: Xie et al. in their manuscript entitled "Preoperative nutritional evaluation of patients with hepatic alveolar echinococcosis" reported preoperative nutritional evaluation for patients with hepatic alveolar echinococcosis (HAE). This is a large sample-size research, as the HAE is rare disease and malnutrition did not get much attention for the investigators. The authors found malnutrition is common event, and several evaluation methods had subtle difference. While, several minor concerns may need to be addressed:

1. It is important to analysis the hemoglobin, wound complications and hospital stay for malnutrition patients.

2 As the present study enrolled 93 patients, it would be interesting if the author stratify those patients into the poor nutrition and good nutrition groups.

3. The conclusion should be more concise to show the goal of this study.

4. The abbreviations should be spelt out in full name the first time. This manuscript needs to be polished by an English-native speaker.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Yinmo Yang

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2020 Feb 24;15(2):e0229396. doi: 10.1371/journal.pone.0229396.r002

Author response to Decision Letter 0


14 Nov 2019

Response to Reviewers

Dear DongXin and reviewers,

We thank you and the reviewers for reviewing our manuscript entitled "Preoperative nutritional evaluation of patients with hepatic alveolar echinococcosis" (ID:PONE-D-19-21935). The reviewers comments have considerably helped to revise and improve our paper, in addition to providing important guidance to our research. We have studied the comments carefully and made corrections which we hope meet your approval. The main corrections are incorporated in the manuscript and responses to the reviewers’ comments are provided below.

Replies to the Journal Requirements

 1. When submitting your revision, we need you to address these additional requirements.

Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

Response:Several changes and adjustments have been made to comply with PLOS ONE's style requirements, including those for file naming. Thank you.

2.Please provide additional details regarding participant consent. In the ethics statement in the Methods and online submission information, please ensure that you have specified (1) whether consent was suitably informed and (2) what type you obtained (for instance, written or verbal). If your study included minors under age 18, state whether you obtained consent from parents or guardians. If the need for consent was waived by the ethics committee, please include this information.

Response:Thank you for pointing this out. Additional details concerning participants consent have been added in the ethics statement and the corresponding content has been added to the new 'cover letter'.

3. We note that you have reported significance probabilities of 0 in places. Since p=0 is not strictly possible, please correct this to a more appropriate limit, eg 'p<0.0001'.

Response:Thank you for the suggestion. This has been changed to 'p<0.001' in the manuscript.

4. Thank you for sending us the data set underlying the results presented in your PLOS ONE submission. We notice that some of the information included in the data set may be potentially identifying. Please ensure that the data shared are in accordance with participant consent and provide only the data that are used in this specific study. To ensure patient confidentiality, we would recommend removing the columns with patient names. Additional guidance on preparing raw clinical data for publication can be found in our Data Policy FAQs (https://journals.plos.org/plosone/s/data-availability#loc-clinical-data).

Response:I've deleted unnecessary columns in the data to ensure patient confidentiality, and named it 'S1 Table', and uploaded it again as Supporting information.

5. Thank you for stating that “The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript” in your financial disclosure.

Please also provide the name of the funders of this study (as well as grant numbers if available) in your financial disclosure statement.

Please include your amended statements within your cover letter; we will change the online submission form on your behalf.

Response:We have added a financial disclosure statement to the new 'cover letter'.

We also bring to your attention that, after careful discussion, we have revised the signature unit of the first author, because Xie Liang participated in this research at a time when support from the Affiliated Hospital of North Sichuan Medical College to Ganzi County People's Hospital(Tibet Aid Project) was provided, and the supporting unit of fund source is also the Affiliated Hospital of North Sichuan Medical college, so the Affiliated Hospital of North Sichuan Medical College should be the first completion unit of this paper. We apologize for the inconvenience.

6.Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information.

Response: Thank for this suggestion. We have added Supporting Information files at the end of my manuscript, renamed and uploaded the corresponding files.

Replies to the Reviewer #1:

1.The purpose of the current study was to "find a concise and reasonable nutritional evaluation indicator" to find out the HAE patients with malnutrition, which could help serve the clinical preoperative risk assessment better, to guide preoperative nutritional support treatment and to reduce the risk of surgery for treatment of HAE. However, in the current study they did not compare the predictive effects of different nutritional assessment methods on surgical risk. It seems that they just considered NRS 2002 as the gold standard for diagnosis of malnutrition.

Response: Thank you for the advice. We carried out a sub-comparison study to assess the predictive effects of different nutritional assessment methods on surgical risk. Please see the revised manuscript for details.

Specifically, we also noted that according to BMI or ALB group, the hospitalization time of malnutrition group was slightly longer than that of normal nutrition group, and the HGB on the 3rd day after operation was slightly lower than that of normal nutrition group, but both these differences were not statistical significant. For this regard, we think that, on one hand, the sample size may be insufficient, but at the same time, BMI and ALB are less sensitive to the prediction of postoperative recovery.

2. As mentioned before, no comparison was made to evaluate the predictive effects of different nutritional assessment methods (e.g. BMI, ALB, NRS 2002) on surgical risk of HAE, why the authors concluded that "NRS 2002 is more suitable for preoperative risk assessment for HAE patients"? Although NRS 2002 could diagnose more malnutrition patients than the other methods, this also means that with this indicator more HAE patients were not suitable for direct surgical treatment, unless a preoperative nutritional support was introduced. Is this consistent with the current status of HAE treatment (about 36.56% of the HAE patients should receive preoperative nutritional support before operation)? If so, the authors should state that point to emphasize the significance of this study, otherwise the results should be reinterpreted carefully, that maybe ALB or BMI, but not NRS 2002, is more suitable for preoperative risk assessment for HAE patients.

Response:Thank you for the advice. We have made new comparisons for postoperative recovery indicators between normal nutrition group and malnutrition group which has been sub-grouped by NRS2002. Please see the new manuscript for details.

According to NRS 2002 nutrition score, preoperation HGB was not different between the two groups (P>0.05). The hospitalization time of normal nutrition group was significantly shorter than that of malnutrition group (P < 0.05), HGB on the 3rd day after operation was significantly higher, and the number of postoperative complications was lower than in the malnutrition group (P < 0.05).

Replies to the Reviewer #2:

1. It is important to analysis the hemoglobin, wound complications and hospital stay for malnutrition patients.

Response:Thank you for the advice. The hospitalization time, HGB value on the 3rd day after operation and the number of postoperative complications (including wound liquefaction and infection, lung infection, abdominal and liver wound infection, urinary tract infection, postoperative inflammatory intestinal obstruction, bile leakage and acute liver function injury) were recorded and analyzed in the new manuscript. Please see the revised manuscript for details.

2. As the present study enrolled 93 patients, it would be interesting if the author stratify those patients into the poor nutrition and good nutrition groups.

Response:Thank you for the advice. All patients have been divided into the normal nutrition group and the malnutrition group according to NRS 2002, BMI and ALB. Please see Table 6 for the comparative analysis of postoperative recovery indicators between the normal nutrition group and the malnutrition group.

According to NRS 2002 nutrition score, preoperation HGB did not differ between the two groups (P>0.05). The hospitalization time of normal nutrition group was significantly shorter than that of malnutrition group (P < 0.05). HGB on the 3rd day after operation was significantly higher than in the malnutrition group (P < 0.05), and the number of postoperative complications was lower than in the malnutrition group (P < 0.05).

3. The conclusion should be more concise to show the goal of this study.

Response:Thank you for the suggestion. We have revised the conclusion of the manuscript to make it more concise.

4.The abbreviations should be spelt out in full name the first time. This manuscript needs to be polished by an English-native speaker.

Response:Thank you for pointing this out. The abbreviations have been spelt out in full name at the first use. We have sought the services of a professional editing company to improve the readability of the paper.

Once again, we appreciate your constructive comments and suggestions which have helped to improve the clarity and depth of the paper.

Yours sincerely,

Xie Liang

Email address: scuxl@foxmail.com

Corresponding author: Xu Mingqing

Email address: xumingqing@scu.edu.cn

Email address: scuxl@foxmail.com

Corresponding author : Xu Mingqing

Email address: xumingqing@scu.edu.cn

Attachment

Submitted filename: Response to Michelle Ellis.doc

Decision Letter 1

Dong-Xin Wang

6 Feb 2020

Preoperative nutritional evaluation of patients with hepatic alveolar echinococcosis

PONE-D-19-21935R1

Dear Dr. Xu Mingqing,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication.

Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

With kind regards,

Dong-Xin Wang

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

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

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: All my comments have been fully addressed, and the current manuscript looks to meet the publication requirements.

Reviewer #2: The authors have satisfactorily addressed the comments and the manuscript has been improved in the revised manuscript.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Acceptance letter

Dong-Xin Wang

10 Feb 2020

PONE-D-19-21935R1

Preoperative nutritional evaluation of patients with hepatic alveolar echinococcosis

Dear Dr. Mingqing:

I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

For any other questions or concerns, please email plosone@plos.org.

Thank you for submitting your work to PLOS ONE.

With kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Professor Dong-Xin Wang

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Table. List of basic information of HAE patients.

    (XLS)

    S1 File. CONSORT 2010 flow diagram.

    (DOC)

    S2 File. PLOSOne_Clinical_Studies_Checklist.

    (DOCX)

    S3 File. STROBE_checklist_v4_combined_PlosMedicine.

    (DOCX)

    S4 File. Trendstatement_TREND_Checklist.

    (DOCX)

    Attachment

    Submitted filename: Response to Michelle Ellis.doc

    Data Availability Statement

    All relevant data are in the paper and Supporting Information files.


    Articles from PLoS ONE are provided here courtesy of PLOS

    RESOURCES