ANNALS OF SURGERY
Vol. 223, No. 6, 765-776
© 1996 Lippincott-Raven Publishers
Repeat Hepatic Surgery for
Colorectal Cancer Metastasis to
C. Wright Pinson, M.D., M.B.A., J. Kelly Wright, M.D., William C. Chapman, M.D.,
C. Louis Garrard, M.D., Taylor K. Blair, and John L. Sawyers, M.D.
From the Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery,
Vanderbilt University Medical Center, and Veterans Affairs Medical Center, Nashville, Tennessee
The authors addressed whether a repeat hepatic operation is warranted in patients with recurrent
isolated hepatic metastases. Are the results as good after second operation as after first hepatic
Summary Background Data
Five-year survival after initial hepatic operation for colorectal metastases is approximately 33%.
Because available alternative methods of treatment provide inferior results, hepatic resection for
isolated colorectal metastasis currently is well accepted as the best treatment option. However,
the main cause of death after liver resection for colorectal metastasis is tumor recurrence.
Records of 95 patients undergoing initial hepatic operation and 10 patients undergoing repeat
operation for isolated hepatic metastases were reviewed for operative morbidity and mortality,
survival, disease-free survival, and pattern of failure. The literature on repeat hepatic resection for
colorectal metastases was reviewed.
The mean interval between the initial colon operation and first hepatic resection was 14 months.
The mean interval between the first and second hepatic operation was 17 months. Operative
mortality was 0%. At a mean follow-up of 33 ± 27 months, survival in these ten patients was 100%
at 1 year and 88% ± 12% at 2 years. Disease-free survival at 1 and 3 years was 60% ± 16% and
45% ± 17%, respectively. After second hepatic operation, recurrence has been identified in 60%
of patients at a mean of 24 ± 30 months (median 9 months). Two of these ten patients had a third
hepatic resection. Survival and disease-free survival for the 10 patients compared favorably with
the 95 patients who underwent initial hepatic resection.
Repeat hepatic operation for recurrent colorectal metastasis to the liver yields comparable results
to first hepatic operations in terms of operative mortality and morbidity, survival, disease-free
survival, and pattern of recurrence. This work helpsto establish that repeat hepatic operationis
the most successful form of treatment for isolated recurrent colorectal metastases.
Pinson and Others
The incidence ofhepatic surgery for colorectal metas-
tasis has increased in the last decade, 1-3 with reported 5-
year survival figures ofapproximately 33%, ranging from
16% to 45%.2 4'5 Improvements in anesthesia, postopera-
tive care, and better understanding of hepatic anatomy
have contributed to low operative mortality rates of0%
to 5%2,67 and a morbidity rate of25%, ranging from 10%
to 60%.2,8 Furthermore, the available alternative meth-
ods oftreatment provide inferior results, with most che-
motherapeutic regimens yielding less than a 30% re-
sponse over less than 6 months.9 Supportive care alone
in matched unresected patients yields significantly
poorer median survival of 3 to 24 months.5"10"' Thus,
hepatic resection for isolated colorectal metastasis cur-
rently is well accepted as the most successful treatment
and the only potentially curative form oftreatment. 12"13
However, the main cause ofdeath after liver resection
for colorectal metastasis is tumor recurrence. Between
rence,1,3,7,12,14-16 which involves the liver in 35% to 50%
of patients.'6,7,8,12 15-19 Isolated hepatic recurrence ini-
tially occurs in approximately 30% of patients, with au-
thorsreportingbetween 17% and 55%. 1,3,4,6,7,12,14-16,18-21
The question we addressed is whether a repeat hepatic
operation is warranted in this group of patients with re-
current isolated hepatic metastasis. It wou!d appear that
10% to 40% of such patients are candidates for further
experience and the literature to determine ifsurvival ver-
sus operative morbidity and mortality supports an ag-
gressive surgical approach.
4 16,19 21 We have reviewed our institutional
PATIENTS AND METHODS
From January 1984 to November 1995, a consecutive
sample of95 patients underwent hepatic surgery with cu-
rative intent for colorectal metastasis at Vanderbilt Uni-
versity Medical Center and the Nashville Veterans
Affairs Medical Center. Ofthese, six patients were iden-
tified who underwent a second hepatic operation. An-
other four patients underwent initial hepatic surgery
elsewhere, but repeat hepatic procedures were performed
at this institution. The ten repeat operations took place
between August 1987 and March 1995. These patients
underwent preoperative extensive tumor staging with
carcinoembryonic antigen level, computed tomography
Presented at the 107th Annual Session of the Southern Surgical Asso-
ciation, December 3-6, 1995, Hot Springs, Virginia.
Address reprint requests to C. W. Pinson, M.D., M.B.A., Division of
Hepatobiliary Surgery and Liver Transplantation, Oxford House,
Suite 801, Vanderbilt University Medical Center, Nashville, TN
Accepted for publication December 28, 1995.
(CT) of the abdomen, pelvis, and thorax, CT portogra-
phy of the liver, and/or whole-body positron emission
Patients underwent thorough exploratory laparotomy
and since 1990, intraoperative ultrasound evaluation.
The liver was fully mobilized23 and examined by biman-
ual palpation. Ultrasound was performed to assess the
extent and number ofhepatic tumors and their relation-
ship to intrahepatic vasculobiliary structures. Cholangi-
ogram usually was obtained as well.
In some hepatic operations, cryosurgery was used in
combination with standard surgical techniques to ablate
all lesions. Ultrasound was used to monitor cryosurgery
probe placement and extent ofthe freeze process. We at-
tempted to obtain a freeze zone larger than 1 cm around
tumors. Two freeze and spontaneous thaw cycles were
In patients in whom the tumor was adjacent to major
vascular structures, occlusion ofinflow by placing a vas-
cular clamp across the hepatoduodenal ligament or total
hepatic vascular isolation consisting of occlusion of the
portal inflow, occlusion ofthe inferior vena cava above
and below the liverand right adrenal vein was used. Oth-
erwise, standard techniques for hepatic resection were
Patients were followed at 3- to 6-month intervals with
carcinoembryonic antigen levels, abdominal CT scans,
and/or PET scans. Tumor recurrence was identified by
increasing carcinoembryonic antigen levels or increasing
findings on serial radiographic studies.
Data from the ten patients who underwent one or
more repeat hepatic operations were collected from
office and hospital charts and direct contact with pa-
tients. This included demographics, clinical course, pa-
thology (primary site and stage, number, size, and loca-
tion of lesions), surgical treatment, and outcome in
terms oftumor recurrence and survival. Patient survival
and recurrence data were compared with that ofpatients
who underwent initial hepatic operations. The literature
on repeat hepatic resections for colorectal metastasis was
reviewed. When individual patient data were available,
they were recorded and summarized with similar pri-
mary data from other reports and also used for compari-
Data are reported as mean ± standard deviation. Sur-
vival and disease-free survival were calculated by the
Kaplan-Meier product limit estimate of the survivor
function (NCSS, Kaysville, UT). Survival curves were
compared by Peto and Peto's log-rank testing, and
differences were accepted ifthe probability was < 0.05.
Ninety-five patients underwent initial hepatic surgery
for colorectal carcinoma metastasis. In 18 of these pa-
Vol. 223.No. 6
Hepatic Surgeryfor Metastasis
Figure 1. Survival curves for 95 pa-
tients who underwent an initial he-
patic operation and 10 patients who
underwent a second hepatic opera-
tion for colorectal carcinoma metas-
tasis to the liver. Standard error of the
cumulative proportion surviving
between 4% and 7% for initial he-
patic operations and is 12% for sec-
ond hepatic operations. The number
of patients with available follow-up at
each time point is shown in the pa-
.. .. ..
Years of Follow-v Up
tients, cryosurgical techniques were used in conjunction
with standard hepatic resection techniques. There were
four operative deaths (4%). Follow-up was available in
100% and current (within
month) in 99%. Follow-up
averaged 27 ± 28 months, with a median of 21 months
and a total of 212 years. Figure
shows the 1- to 5-year
4%,61% ± 6%,
actuarial survival estimates to be 80%
48% ± 6%, 43% ± 6%, and 38% ± 7%, respectively. Ac-
tual 5-year survival was 9 of 28 (32%) patients.
Figure 2 demonstrates the
1- to 5-year actuarial dis-
ease-free survival as 57% ± 5%, 35% ± 5%, 27% ± 5%,
5%,and 16% ± 5%, respectively. Recurrent colo-
rectal carcinoma metastasis has been found at a mean of
months and a median of 8 months in 67 of these
95 (71%) patients. This involved the liver in a total of 52
patients (55%) and was confined to the liver in 31 pa-
Ofthe 31 patients with recurrence confined initiallyto
the liver, 6 (19%) underwent a second hepatic operation.
This represents 6% of the 95 patients undergoing initial
surgery. Four other patients underwent initial resection
at another institution.
The ten patients (6 women, 4 men) who underwent re-
peat hepatic operations for colorectal carcinoma metastasis
were at the time of their initial colon resections 53 ± 10
yearsofage (median 56years).The location for the primary
resected colon lesion was in the rectum in three patients, in
the sigmoid colon in four patients, in the left colon in one
patient, in the transverse colon in one patient, and in the
right colon in one patient. The primary stagewas B in two
patients, C in three patients, and D in 5 patients. Eight of
these patients received adjuvant 5-fluorouracil-based che-
motherapy,and two also received radiationtherapy.All ten
patients had isolated hepatic metastasis treated by hepatic
surgeryeithersynchronously orupto 39 months later. This
interval averaged 14 ± 13 months, with a median of 15
months (Table 1).
The first hepatic operation in these ten patients in-
volved resection of one to three lesions by lobectomy in
one patient, left lateral segmentectomy in two patients,
and wedge resections in seven patients. Margins were
negative in all cases. Total hepatic isolation was used in
four patients. Transfusions were required in four ofthese
ten operations, totalling 21 units ofpacked erythrocytes.
There were no operative deaths, but two patients had
a pulmonary embolus, and one a
subphrenic abscess. Half of the patients (patients 2, 3,
6, 7, and 9) received postoperative 5-fluorouracil-based
The findings leading to the diagnosis of recurrent tu-
mor thereafter included an increase in the carcinoem-
bryonic antigen level in most patients (Table 2). The re-
maining patients had enlarging hypodense lesions on se-
concludingin the finding of isolated hepatic recurrence.
The interval between the first and second hepatic op-
Vol. 223-No. 6
Pinson and Others
Scond Hpatie -Operations
derwent an initial hepatic operation
and 10 patients who underwent a
second hepatic operation for colo-
rectal carcinoma metastasis to the
liver. Standard error of the cumulative
proportion surviving is 5% for initial
hepatic operations and 16% to 17%
for second hepatic operations for
each time point shown. The number
of patients with available follow-up at
each time point is shown in parenthe-
for 95 patients who
erations was 17 ± 11 months (median 14 months). At
this time, the mean age ofthe patients was 56 ± 10 years
of age (median 57 years). The second hepatic operation
addressed one to three lesions in eight patients but ad-
dressed five and eight lesions, respectively, in two pa-
tients. The operation consisted of a right lobectomy in
one patient, segmentectomy in one patient, and wedge
resections in seven patients, with cryosurgery used in
four patients. Margins were negative in all cases. One pa-
tient (patient 2) also underwent a simultaneous abdomi-
nal aortic aneurysm repair. Total vascular isolation was
used in two patients, and the Pringle maneuver was used
in one. Transfusions were used in six patients, totalling
32 units ofpacked erythrocytes, 12 units of fresh frozen
plasma, and 6 units ofplatelets. There were no operative
deaths, but six patients had complications consisting of
transient bile leaks in three, bile duct stenosis in one,
subphrenic abscess in one, and transient hepatic failure
in one. Intensive care unit stay was 2 ± 0.8 days, with
mean hospital stay of 1 1 ± 6 days. At the second hepatic
operation, hepatic artery catheters were placed in five pa-
tients (patients 2, 3, 4, 6, and 7) who received postopera-
tive fluorodeoxyuridine. One other patient (patient 9) re-
ceived fluorouracil systemically.
Follow-up in these ten patients was current in 100%.
The mean follow-up was 33 ± 27 months (median 25
months) and a total of 27 years. Survival in these ten
patients was 100% at
1 year and 88% ± 12% at 2 years
and thereafter (Fig. 1). Disease-free survival at
years was 60% ± 16% and 45% ± 17%, respectively (Fig.
2). With these limited data and follow-up, there was a
significant difference in the survival curves comparing
our 95 first-time hepatic operation patients with our 10
second hepatic operation patients (p < 0.05, Fig. 1).
However, there was no difference between the disease-
free survival curves for these two groups (Fig. 2).
After the second hepatic operation, recurrence has been
identified in six (60%) patients at a mean of24 ± 30 months
(median 9 months). This was isolated hepatic disease in one
patient, hepatic plus extrahepatic disease in four patients,
and pulmonary recurrence in one patient.
In the patient with isolated hepatic disease and one pa-
tient with hepatic and limited abdominal recurrence, a
third hepatic operation was performed. The interval
from the second to the third hepatic operation was 32
months and 90 months, respectively, in these two pa-
tients. One patient had three lesions and underwent
three wedge resections with negative margins. The sec-
ond patient had one hepatic lesion excised with the use
ofcryosurgical assistance, and an abdominal recurrence
also was excised with negative margins. Both patients
were discharged 6 days postoperatively. Follow-up in
these two patients identified tumor recurrence in both
after this third liver resection. The first patient recurred
at 15 months and the second at 6 months, both in the
liver, lung, and abdomen.
Repeat Hepatic Surgery for Metastasis
c'j01 CU CU) 10
ur ~ ~~~~
L gD D
Vol. 223-No. 6
Pinson and Others
Primary Colon Surgery
First Hepatic Surgery
Second Hepatic Surgery
Third Hepatic Surgery
Carcinoembryonic antigen (CEA) levels are in ng/mL.
*Primary colon surgery and first hepatic surgery were within 6 weeks in these 3 patientswith stageD disease.
Colorectal cancer is the second most common form
of cancer in the United States, with approximately
160,000 estimated new cases per year. Although many
patients are cured, with primary colon resection a large
number (range, 40%-80%) will develop recurrence of
the disease.24 For patients with recurrence involving
only the liver, approximately 15,000 per year, surgical
ablation offers the only chance for cure and is the ac-
cepted current therapeutic approach.'3 With experi-
ence, a high level of safety and efficacy of hepatic re-
sections routinely is seen. Operative mortality after
primary hepatic resection for tumor is less than 5%,
60%.2 82526 It generally is accepted that primary liver
resection can achieve long-term survival in 25% to
33% of patients with hepatic colorectal metastases.5'27
In our patients, the 5-year actual survival was 32% and
actuarial survival was 38% ± 7%. This is in contrast to
a less than 2% 5-year survival with the natural history
of the disease and less than 5% 5-year survival with
current nonoperative care.10'12'15 Disease-free survival
was 16% at 5 years for our 95 resected patients, in
agreement with disease-free survival rates of 15% to
25% at 5 years reported in the literature.'4"16'28
Unfortunately, a majority of patients develop recur-
rence after hepatic resection for colorectal metastasis,
most ofwhich are identified in the first 12 to 18 months
postoperatively.3" 6 The mechanisms of this failure may
include inadequate margin at the first operation, missed
lesion at the first operation, spread ofdisease at the time
of the first operation, or simply natural progression of
micrometastatic disease from the primary tumor.'5 The
incidence ofrecurrent disease after liver resection for co-
lorectal metastasis is reported at 55% to 80%.37 '2I4l6
tients, ,67,12,15,16,18,19 with isolatedhepaticinvolvement in
25% to 33% of patients. 6'7"12"16" 9 Ten to 40% of these
patients with isolated recurrence undergo second resec-
tions.12,14, 16,19,21In ourexperience, 71% ofpatientsre-
curred at a mean of 13 months, 55% involving the liver
and 33% involving the liver alone. Nineteen percent of
those with isolated recurrence underwent a second he-
Intense interest in repeat surgical resection for recur-
rent hepatic metastases can be seen in the numerous re-
ports in the surgical literature since 1984.1,3,6,12-21,28-48
Eight ofthese case series provided data on the number of
second hepatic operations in relationship to the number
of initial hepatic operations performed at each institu-
tion in a similar time period ranging from 6 to 21
In these 8 series, there were 248 sec-
ond hepatic procedures (8%) compared with 3182 initial
operations. Individual institutions reported from 5% to
16% incidence of repeat procedures compared with ini-
tial procedures. Six percent of our patients underwent
repeat procedures. There are 30 patients reported who
have undergone third hepatic procedures for colorectal
metastasis in five reports. 1"7"16"19'28The incidence ofthird
hepatic procedures in relationship to second hepatic pro-
cedures was 8% as well, 30 of 368 cases. In our own ex-
perience, there were two often patients who underwent
a third procedure.
The time interval from initial colon operation to first
Repeat Hepatic Surgery for Metastasis
hepatic operation was available for 53 individual pa-
tients from six case series, 1'6'7'12,'1720 with a mean of 13 +
16 months (median 11 months). This compares with our
experience of 14 ± 13 months (median 15 months). The
time interval between first and second hepatic proce-
dures was available for 80 individual patients in ten case
series,1'3,4'6,7"1215"17'20'31 with a mean of 17 ± 12 months
(median 12 months). In our experience, it was a mean of
17 ± 11 months (median 14 months). Others have re-
ported very similar interval periods.'6"19
Operative mortality for second hepatic procedures are
available for 425 cases from 24 reports,12'4'6'7'2"5
17,18-20,29-34,42-45with eight operative deaths (1.9%). In our
experience, the operative mortality rate was 0% for 10
second resections compared with an operative mortality
rate of4% for 95 primary resections.
Data on postoperative complications are available in
various forms in 15 reports. 14,3,6,7,12-21,31 Of457 patients
undergoing second operations, 113 patients (25%) had
reported complications. The most common complica-
tions reported were hemorrhage in 5%, significant pleu-
ral effusion in 5%, and infections in 10% ofpatients (in-
cluding abscess formation in 5% and pneumonia in
2.4%). Biliary leak was reported in 2.1% and biliary ste-
nosis in 1%. Transient hepatic failure developed in 1.7%.
These morbidity rates are similar to those seen in pri-
mary hepatic resections.5,7,814'19,21 In our ten patients, six
had complications that compared with two complica-
tions after their first hepatic operation. The mortality
and morbidity after third hepatic resections are also rel-
atively limited in our experience and that ofothers." 6'7"19
Operative blood loss increased with repeat hepatic re-
sections compared with primary resections in our expe-
rience. In the second hepatic operation, we used 32 units
ofpacked erythrocytes, 12 units of fresh frozen plasma,
and 6 units of platelets, compared with 21 units of
packed erythrocytes in the first hepatic operation for
these same ten patients. Similar experience with in-
creased blood loss has been reported by others.'1945 An
operative field that is distorted by adhesions making for
difficult exposure, intrahepatic anatomic variations in-
duced by prior resections dictating variable planes ofdis-
sections, and hepatic parenchymal hypertrophy and fri-
ability are among several factors that are implicated in
increasing the time required for repeat hepatic resection
and the need for increased blood replacement products.
It appears that carcinoembryonic antigen levels con-
tribute to optimal follow-up in patients who have un-
dergone hepatic resection (Table 2). In many patients,
especially those in whom carcinoembryonic antigen is
not useful, serial CT scan has been useful. We also have
found PET useful in following patients after hepatic re-
section.22 Based on the time to recurrence, we believe
this follow-up should occur at least every 6 months.
An improved prognosis for long-term survival with an
aggressive surgical approach is best demonstrated when
complete surgical resection with adequate tumor-free
margins and absence of extrahepatic disease after resec-
tion is achieved.'5 Therefore, in an effort to identify pa-
tients who can appropriately be rendered disease free by
surgical resection, preoperative staging of patients with
recurrent hepatic colorectal metastasis should be aggres-
sive to identify the number and distribution of lesions
present. Our own group employs a combination ofcon-
trasted chest and pelvic CT, CT portography, ultra-
sound, bone scan, and whole body PET imaging. We re-
cently reported that PET has been helpful in clarifying
the presence or absence of intra- and extrahepatic colo-
rectal metastases, differentiating surgical scar from re-
current tumor, and PET data have changed manage-
ment strategies in up to 25% ofour patients.22
The principles that apply to second-time resection are
the same as those that are used to select the first time
candidate: all known disease is resectable, adequate tis-
sue margins are obtainable, there is adequate liver re-
serve function to tolerate surgery, and there are no med-
ical diseases that would preclude surgery. In addition to
the two key factors for a good outcome, no extrahepatic
disease and ability to obtain 1-cm margins intrahe-
patically,14'28 some authors believe the number ofmetas-
tasis should be limited.6"2'34 Based on the early recur-
rence in our two patients with more than three lesions
who received second resection, we agree. Some authors
recommend delaying second hepatic operation in pa-
tients with more than a single lesion to observe for the
early development of widespread disease.7"2"3 This is a
reasonable approach. So far, there are no other prognos-
tic indications identified from the time of the original
colon operation or first hepatic resection. '4'28
In our patients, survival after repeat hepatic resection
for colorectal metastasis, admittedly with limited data,
compares favorably with our experience after primary
hepatic resections for isolated hepatic metastases (Fig. 1).
Other groups have reported equivalent survival results
when comparing primary and secondary resections of
the liver for isolated colorectal metastases, with long-
term survival as high as 32%.28 Fifteen published case
series on repeat hepatic surgery for colorectal metasta-
sis' 34,6,7,121517,20,21,30-34provided individual data on sur-
vival for a total of 124 patients undergoing a second he-
patic operation for colorectal metastasis. Our ten pa-
tients were added to this for a total of 134 patients. The
actuarial survival was 91% ± 3% at 1 year, 69% ± 5% at
2 years, 55% ± 5% at 3 years, 45% ± 6% at 4 years, and
40% ± 7% at 5 years (Fig. 3). Six patients were surviving
Vol. 223-No. 6
Pinson and Others
Ann. Surg.-June 1996
tients undergoing second hepatic
operations for colorectal metastasis.
This represents our 10 patients to-
gether with 124 more collected from
15 reports in the literature, with indi-
vidual follow-up available (seetext for
citation). The number of patientswith
available follow-up at each time point
is shown in parentheses.
3. Survival curve for 134 pa-
1.34 C"ollected -Second Il1epatfic.Operations
Yetars (Fof ikilo Up
at 5 years offollow-up, including one ofour own. These
figures are remarkably similar to our experience after
first-time resection and the experience of others.2 5 The
disease-free survival figures for our ten patients at 1, 2,
and 3 yearswas60% ± 16%, 60%+ 16%,and 45% ± 17%,
respectively. Others have reported figures of 70%, 50%,
and 21% to 36%, respectively.7"19
The pattern of failure after second liver resection for
colorectal metastasis is provided for a total of 217 pa-
tients from 10 reports. 367,12,15,16,20,21,34 Recurrence oc-
curred in 146 patients (67%). The liverwas involved with
recurrence in 104 patients (47%). Isolated hepatic in-
volvement occurred in 62 patients (28%). In our ten pa-
tients, 60% recurred at a mean of 24 months (median 9
months). A median of 6 to 9 months to recurrence is
reported by others. 122' The liver was among the sites in-
volved in 50%, and the liver only was involved in 10%.
These data would suggest that results of repeat resec-
tion are not very different from those with initial hepa-
tectomy. Review of the current literature and our own
experience at Vanderbilt support second-time hepatic
operation for recurrent colorectal metastasis. These re-
sections can be performed safely, without greater risk
than first-time resections, and offer a survival that is at
least as good as first-time resections (Fig. 3). This experi-
ence and discussion helps to establish that repeat hepatic
surgery is the best treatment option currently available
for selected patients with recurrent colorectal metastasis
to the liver.
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DR. RONALD K. TOMPKINS (Los Angeles, California):
Thank you, President Thompson, Secretary Copeland, Mem-
bers, and Guests. This is an excellent paper with extremely ac-
curate documentation of a very difficult procedure. I cannot
imagine going back in for a third hepatic resection, even ifI had
been there the first two times. I think it would be very difficult.
The authors have included some things in the manuscript
that they have not shown among the slides, and I would like to
ask them some questions about it.
First ofall, it seems that the median interval between the first
and second operation and then the second and third operations
grows successively shorter. And I wonder if they would com-
ment on what they are accomplishing in the natural history of
the disease by this aggressive approach. What is the role in their
experience, and their advice, on the proposal that we should
delay operation in patients in whom we have just discovered
hepatic metastases, to see if other extrahepatic metastases will
materialize in a few months?
This has been proposed by some; I think it is a highly contro-
versial proposal, but I would like to know how theyhave looked
at this and what their data might be.
Secondly, I think that the screening of these patients to rule
out extrahepatic malignancy is an extremely difficult thing.